Staphylococcus aureus in bovine intramammary infections: A global systematic review and meta-analysis of prevalence and antimicrobial resistance patterns

Md Jisan Ahmed; Md Arifur Rahman; Ritu Chalise; Prajwal Bhandari; Md Ismile Hossain Bhuiyan; Md Imran Hossain; Israt Jahan Kaderi; Md Afiqul Islam Rahi; Delower Hossain

doi:10.1016/j.nmni.2026.101860

. 2026 Sep 24;74:101860. doi: 10.1016/j.nmni.2026.101860

Staphylococcus aureus in bovine intramammary infections: A global systematic review and meta-analysis of prevalence and antimicrobial resistance patterns

Md Jisan Ahmed ^a,^b,^⁎, Md Arifur Rahman ^a,^c, Ritu Chalise ^a,^d, Prajwal Bhandari ^a,^d, Md Ismile Hossain Bhuiyan ^a,^e, Md Imran Hossain ^a,^b, Israt Jahan Kaderi ^a,^f, Md Afiqul Islam Rahi ^a, Delower Hossain ^a,^g

PMCID: PMC13635641 PMID: 42835315

Abstract

Background

Staphylococcus (S.) aureus is a globally pervasive and economically significant pathogen in bovine intramammary infections (IMIs) and is responsible for both clinical and subclinical mastitis.

Objectives

This study systematically investigated the global epidemiology of S. aureus from bovine IMIs, addressing antimicrobial resistance (AMR) among S. aureus isolates through a meta-analysis.

Methods

A total of 143 studies published between 2000 and 2025 were identified through comprehensive searches, which were based on predefined inclusion criteria. The data were systematically extracted, and the statistical analyses were performed in R (v4.5.2).

Results

The meta-analysis included 143 studies (145,457 samples), with a pooled S. aureus prevalence of 24.78% and high heterogeneity (I² = 99.51%). Subgroup analyses demonstrated significant heterogeneity in prevalence by study design, publication year, and region, with greater heterogeneity in cross-sectional studies (I² >95%, p < 0.001). Meta-regression identified sample size as a significant source of heterogeneity (β = −0.00002, p = 0.02; R² = 3.41%). The highest prevalence was reported in Cameroon (67%), Sri Lanka (64.3%), Indonesia (57%), and India (44%), with the lowest prevalence reported in Poland (0.7%), Taiwan (2.0%), Australia (5.5%), and New Zealand (5.3%). AMR was highest for doxycycline (70.7%), penicillin (65.2%), and ampicillin (62.8%); moderate to oxacillin (44.6%) and vancomycin (40.2%); and lowest for gentamicin (27.5%) and amikacin (18.3%).

Conclusion

S. aureus is highly prevalent in bovine IMIs worldwide, with marked regional heterogeneity and substantial resistance to commonly used antimicrobials, emphasizing the urgent need for targeted surveillance, prudent antimicrobial use, and improved mastitis control strategies at the global and regional levels.

Keywords: Staphylococcus aureus, Bovine intramammary infection, Mastitis, Antimicrobial resistance, Epidemiology

Highlights

•
Global pooled prevalence of S. aureus in bovine IMIs was 24.78%.
•
Considerable heterogeneity was observed across regions and study designs.
•
Highest prevalence occurred in Cameroon, Sri Lanka, Indonesia, and India.
•
Resistance was highest to doxycycline, penicillin, and ampicillin.
•
Findings support urgent surveillance and stronger mastitis control programs.

1. Introduction

Bovine intramammary infection (IMI) is often incorrectly equated with the mere presence of microorganisms in milk; however, infection, as defined by the Merriam-Webster Medical Dictionary, involves the invasion and multiplication of pathogenic microorganisms not normally present in the host, which may manifest as either subclinical or clinical disease [1]. IMI remains one of the most economically significant diseases affecting dairy cattle worldwide, with clinical cases occurring in approximately 1–2% of animals at any given time, while subclinical mastitis, particularly associated with coagulase-negative staphylococci, ranges from 6% to 55% at the udder quarter level [[2], [3], [4], [5]]. Among the etiological agents responsible for bovine IMI, Staphylococcus aureus is the most prevalent contagious udder pathogen globally and a main cause of chronic, predominantly subclinical IMI, typically associated with elevated somatic cell counts and reduced treatment success [[6], [7], [8]]. This Gram-positive, facultatively anaerobic coccus acts both as a commensal organism colonizing skin and mucosal surfaces and as an opportunistic pathogen capable of causing a wide spectrum of diseases in humans and animals [[9], [10], [11], [12]].

Globally, S. aureus is widely distributed and remains one of the most important contagious pathogens associated with bovine mastitis, with prevalence varying across regions, herd types, and management systems. It is a major cause of reduced milk quality and spoilage in dairy production worldwide [13,14]. The pathogen commonly establishes chronic intramammary infections that are difficult to eliminate due to poor response to antimicrobial therapy and efficient transmission within herds, leading to persistent production losses [15]. Its clinical importance is further strengthened by its virulence factors, including toxins and enzymes, which enhance its ability to cause disease in both animals and humans [[16], [17], [18], [19], [20]]. In veterinary systems, it is also responsible for intramammary and other infections in dairy cattle and goats, contributing to significant health and productivity issues [21]. Moreover, S. aureus asymptomatically colonizes around 30% of humans [[22], [23], [24]] and is capable of causing infections ranging from mild skin conditions to severe systemic diseases [[25], [26], [27], [28]], underscoring its broader public health relevance and involvement in foodborne outbreaks [[29], [30], [31]].

A critical challenge in controlling S. aureus IMI is its ability to acquire and disseminate resistance through mechanisms such as horizontal gene transfer involving mobile genetic elements, including plasmids, transposons, and staphylococcal cassette chromosomes [32,33]. The mecA gene, which encodes the altered penicillin-binding protein PBP2a, is the primary determinant of methicillin resistance, leading to the emergence of methicillin-resistant S. aureus (MRSA) and limiting the effectiveness of β-lactam antibiotics [[34], [35], [36]]. The growing prevalence of MRSA and other multidrug-resistant strains has further complicated treatment, increasing both economic burden and health risks in human and veterinary sectors [[37], [38], [39]]. This issue is particularly pronounced in developing countries such as Bangladesh, due to inappropriate antibiotic use and poor management practices [[40], [41], [42]].

The economic and zoonotic impacts of S. aureus, particularly in bovine mastitis, are substantial and globally significant. Mastitis caused by this pathogen leads to major financial losses estimated in billions of dollars annually due to reduced milk production, treatment costs, animal culling, and decreased milk quality [43]. These losses are further intensified by antimicrobial resistance (AMR), which reduces therapeutic effectiveness and contributes to increased morbidity, mortality, and broader economic and food production burdens across human, animal, and environmental health systems [39,[44], [45], [46], [47]]. In addition to economic damage, S. aureus represents a significant zoonotic and food safety hazard, as it can be transmitted from infected animals to humans through direct contact or consumption of contaminated milk and dairy products [48]. Contaminated food may harbor heat-stable enterotoxins responsible for staphylococcal food poisoning, a leading cause of acute gastroenteritis worldwide [[49], [50], [51]]. The emergence of livestock-associated methicillin-resistant S. aureus (LA-MRSA) further emphasizes the role of animal reservoirs in the transmission of resistant pathogens, reinforcing the need for a One Health approach [[52], [53], [54]].

Despite extensive research on S. aureus in bovine intramammary infections, significant gaps remain in understanding its global prevalence, distribution, and antimicrobial resistance patterns. Variability in study design, diagnostic methods, and regional factors has led to inconsistent findings, making it difficult to draw comprehensive conclusions. Therefore, there is a need for systematic approaches to synthesize existing data and identify trends. Meta-analysis serves as a powerful tool to integrate results from multiple studies, providing more robust estimates and insights into disease dynamics [55]. Understanding the prevalence and resistance patterns of S. aureus is essential for developing effective control strategies, guiding prudent antimicrobial use, and minimizing economic losses [56]. Accordingly, this study aims to estimate the global prevalence of S. aureus-associated bovine intramammary infections and evaluate the patterns of antimicrobial resistance reported across different regions, thereby contributing to improved disease management and public health protection.

2. Materials and methods

2.1. Guidelines and protocol

This study was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) framework for SRMA [57]. To maintain methodological rigor and ensure comprehensive inclusion of relevant information, the PRISMA 2020 checklist was strictly applied (Supplementary 1 Table 1).

Table 1.

Subgroup meta-analysis of S. aureus in bovine IMIs.

Subgroup	Name/Variables	% (95% CI)	τ²	I²	p value
Design	Cross sectional	25.08 [21.56, 28.76]	0.22	99.46	<0.001
Design	Longitudinal	1.07 [0.85, 1.30]	-	-	-
Year	2010	20.48 [16.30, 25.00]	-	-	-
	2011	23.63 [10.88, 39.36]	0.23	99.38	<0.001
	2012	30.27 [14.15, 49.38]	0.23	98.96	<0.001
	2013	17.29 [2.61,40.85]	0.43	99.63	<0.001
	2014	8.53 [1.29, 21.00]	0.10	97.11	<0.001
	2015	15.62 [4.23, 32.27]	0.16	98.17	<0.001
	2016	25.26 [18.18, 32.63]	0.08	96.64	<0.001
	2017	27.02 [16.99, 34.53]	0.10	97.15	<0.001
	2018	41.39 [29.31, 54.02]	0.13	97.04	<0.001
	2019	18.63 [8.63, 31.30]	0.20	99.48	<0.001
	2020	24.72 [5.41, 51.88]	0.58	99.67	<0.001
	2021	31.56 [15.98, 49.59]	0.48	99.18	<0.001
	2022	26.46 [19.75, 33.75]	0.09	97.22	<0.001
	2023	13.35 [7.14, 21.09]	0.10	99.30	<0.001
	2024	24.72 [14.92, 36.04]	0.17	98.46	<0.001
	2025	30.78 [18.16, 45.06]	0.20	98.04	<0.001
Country	Algeria	28.88 [24.75, 33.18]	0.00	0.00	0.40
	Argentina	20.95 [14.74, 27.90]	-	-	-
	Australia	5.49 [3.49, 7.89]	-	-	-
	Bangladesh	24.16 [8.47, 44.61]	0.29	98.61	<0.001
	Brazil	16.89 [4.58, 34.68]	0.30	99.70	<0.001
	Cameroon	67.00 [61.57, 72.22]	-	-	-
	China	20.90 [11.13, 32.75]	0.26	99.48	<0.001
	Czech Republic	22.79 [11.30, 36.84]	0.04	91.35	<0.001
	Egypt	32.90 [23.80, 42.69]	0.15	96.57	<0.001
	Ethiopia	23.94 [12.95, 37.01]	0.24	98.30	<0.001
	Germany	19.28 [0.00, 81.52]	0.92	99.21	<0.001
	India	44.02 [27.57, 61.17]	0.36	98.65	<0.001
	Indonesia	56.98 [46.34, 67.30]	-	-	-
	Iran	17.32 [13.17, 21.90]	0.03	90.50	<0.001
	Italy	20.28 [19.28, 21.30]	-	-	-
	Japan	47.44 [36.40, 58.59]	-	-	-
	Jordan	38.12 [11.40, 69.40]	0.19	93.95	<0.001
	Kazakhstan	17.66 [8.63, 29.03]	0.04	93.23	<0.001
	Kenya	30.05 [5.67, 63.13]	0.35	98.98	<0.001
	Lithuania	13.13 [11.38, 15.00]	-	-	-
	Malaysia	16.60 [12.09, 21.64]	-	-	-
	Mexico	48.00 [34.20, 61.95]	-	-	-
	New Zealand	5.32 [5.15, 5.50]	-	-	-
	North Africa	14.19 [10.47, 18.36]	-	-	-
	Norway	20.48 [16.30, 25.00]	-	-	-
	Pakistan	27.32 [18.75, 36.82]	0.06	95.86	<0.001
	Poland	0.70 [0.19, 1.47]	-	-	-
	Saudi Arabia	22.00 [14.37, 30.70]	-	-	-
	Slovakia	11.52 [7.34, 16.47]	-	-	-
	South Korea	7.98 [1.19, 19.90]	0.06	98.75	<0.001
	Sri Lanka	64.32 [59.37, 69.13]	-	-	-
	Sweden	10.36 [0.00, 48.32]	0.40	99.83	<0.001
	Thailand	23.15 [3.01, 54.21]	0.22	98.60	<0.001
	Turkey	12.41 [0.97, 33.50]	0.20	98.53	<0.001
	USA	22.99 [17.46, 29.02]	0.01	82.19	0.02
	Ukraine	12.98 [10.98, 15.12]	-	-	-
	Uruguay	47.07 [42.89, 51.27]	-	-	-
	Vietnam	12.00 [8.99, 15.38]	-	-	-
Continent	Africa	29.21 [22.66, 36.22]	0.19	97.81	<0.001
	Asia	25.88 [20.81, 31.30]	0.23	99.00	<0.001
	Europe	14.19 [6.98, 23.39]	0.17	99.74	<0.001
	Oceania	5.27 [5.10, 5.45]	0.00	0.01	0.81
	North America	28.15 [17.54, 40.13]	0.06	94.47	<0.001
	South America	20.22 [8.29, 35.66]	0.27	99.61	<0.001

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2.2. Systematic literature search strategy

A thorough literature search was conducted as part of this SRMA to identify peer-reviewed studies reporting epidemiological data on S. aureus associated with bovine IMI. The search strategy incorporated medical subject headings (MeSH) and other subject terms, along with appropriate search filters. The strategy was developed and executed by the authors (MJA, DH), with restrictions applied to publication type. Reviews, books, book chapters, and conference abstracts were excluded. Only studies published in English were considered eligible. In addition, the authors (MJA, MAR, MIH, IJK, MIHB) manually screened the reference lists of all included articles to identify any additional relevant studies. Supplementary searches were additionally performed by MAJ, DH, and MIH. Details of the databases searched, and the number of records retrieved from each, on the basis of the applied search strategies, are provided in Supplementary 1 Table 2.

Table 2.

Univariate meta-regression of covariates.

Covariates	β	95% CI	p value	R² (%)
Study Year	0.0056	−0.0138 to 0.0251	0.57	Nil
Positive Cases	−0.0001	−0.0004 to 0.0002	0.50	Nil
Country	−0.0067	−0.0066 to 0.0042	0.12	1.15
Continent	−0.0615	−0.1236 to 0.0006	0.05	2.38
Study design	−0.8445	−1.7601 to 0.0712	0.07	1.87
Sample Size	−0.00002	−0.00003 to −0.000003	0.02	3.41

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2.3. Inclusion and exclusion criteria

For this SRMA, stringent inclusion and exclusion criteria were predefined to ensure the selection of high-quality, scientifically relevant studies addressing S. aureus, AMR patterns, and AMR-associated genes in bovine IMIs worldwide. Eligible studies were peer-reviewed, English-language original research articles published between January 1, 2010, and December 31, 2025; indexed in PubMed, Scopus, and Web of Science; and reported primary data on the epidemiology, phenotypic AMR profiles, or genetic determinants of AMR in S. aureus isolated from bovine IMIs. Studies were excluded if they were non-primary publications (e.g., reviews, editorials, commentaries), published in languages other than English, conducted outside the specified time frame, or did not explicitly focus on S. aureus epidemiology, AMR patterns, or AMR genes. These criteria were applied to maximize methodological rigor and ensure the relevance and robustness of the synthesized evidence.

2.4. Data collection and extraction

Five authors (MIH, MIHB, MAR, IJK, and MJA) independently conducted all stages of the review process, including title and abstract screening, full-text assessment, data extraction, and quality assessment. Any discrepancies in study selection or data extraction were resolved through discussion among the authors, with a senior author (DH) consulted when consensus could not be reached. The screening process commenced with titles and abstracts, followed by full-text evaluation. The following data were extracted from each included study: country, author, publication year, total sample size, total S. aureus-positive samples, and study design. Data extraction specifically focused on resistance to commonly used antibiotics, including amikacin, amoxicillin, ampicillin, azithromycin, cefotaxime, cefoxitin, ceftazidime, ceftiofur, ceftriaxone, cefuroxime, cephalexin, cephalothin, chloramphenicol, clindamycin, ciprofloxacin, doxycycline, enrofloxacin, erythromycin, gentamicin, kanamycin, levofloxacin, methicillin, neomycin, norfloxacin, ofloxacin, oxacillin, oxytetracycline, penicillin, rifampicin, rifaximin, streptomycin, tetracycline, trimethoprim-sulfamethoxazole, tylosin, and vancomycin. These antibiotics were categorized into classes as follows: aminoglycosides (amikacin, gentamicin, kanamycin, neomycin, and streptomycin), β-lactams (amoxicillin, ampicillin, oxacillin, penicillin, and methicillin), macrolides (azithromycin, erythromycin, and tylosin), cephalosporins (cefotaxime, cefoxitin, ceftazidime, ceftiofur, ceftriaxone, cefuroxime, cephalexin, and cephalothin), phenicols (chloramphenicol), fluoroquinolones (ciprofloxacin, enrofloxacin, levofloxacin, norfloxacin, and ofloxacin), tetracyclines (doxycycline, tetracycline, and oxytetracycline), Lincosamides (clindamycin), sulfonamides (trimethoprim-sulfamethoxazole), glycopeptides (vancomycin), and rifaximin) (Supplementary 2).

2.5. Bias assessment and quality evaluation

The methodological quality and risk of bias of the included studies were evaluated via the Joanna Briggs Institute (JBI) critical appraisal tool, which is specifically designed for different study designs. These tools assess internal validity by systematically identifying potential sources of bias in the design, conduct, and analysis of each study, thereby ensuring a rigorous appraisal of study reliability and robustness [58]. The quality assessment addressed eight key domains: the suitability of the research design; clarity in describing the study setting; adequacy of population demographic information; quality of sample data; procedures for sample collection, transfer, and storage; appropriateness of microbiological media used; reporting of isolates; and transparency of data sources. Each domain was scored via a binary system, with a score of ‘1’ indicating adherence to the criterion (yes) and ‘0’ indicating nonadherence (no). The total score for each study, therefore, ranged from 0 to 8 (Supplementary 2). On the basis of the total quality score, studies were classified into three categories of bias risk: low risk of bias (>70%), moderate risk of bias (50-69%), and high risk of bias (<50%). To evaluate the robustness of the meta-analytic findings, sensitivity analyses were performed to assess the effect of excluding studies with a moderate or high risk of bias. This systematic approach to quality assessment strengthens the reliability of the review by explicitly identifying and accounting for potential sources of bias in the included studies.

2.6. Statistical analysis

The extracted data were subsequently compiled into a Microsoft Excel spreadsheet. All studies meeting the inclusion criteria were carefully examined and critically evaluated to ensure the accuracy, consistency, and reliability of the synthesized evidence. A random-effects meta-analysis model was applied to estimate the pooled prevalence of S. aureus, AMR patterns, and the epidemiology of AMR genes, with corresponding 95% CI [59,60]. Statistical heterogeneity was assessed using the I² statistic, with values of 25%, 50%, and 75% indicating low, moderate, and high heterogeneity, respectively, while an I² value of 0% denoted the absence of heterogeneity [61]. A random-effects meta-analysis model was used to generate summary estimates due to substantial between-study heterogeneity [62]. Subgroup analyses were performed according to country and year. For meta-regression analyses, categorical variables were dummy-coded by creating k-1 binary indicators for k categories, allowing their inclusion in the regression models [63]. In addition, univariate meta-regression analyses were performed to identify potential contributors to between-study heterogeneity. Funnel plots, together with sensitivity analyses, were used to visually assess the distribution of effect estimates and to evaluate study quality and potential bias. Small-study effects were formally examined using Egger’s regression test [64]. This test assesses the association between individual study effect estimates and their corresponding standard errors to identify the presence of potential small-study effects. When evidence of small-study effects was identified, the trim-and-fill method was applied to estimate the number of potentially missing studies and to generate bias-adjusted pooled estimates, thereby evaluating the robustness of the meta-analytic findings in the presence of possible publication bias [65]. A significant level of p < 0.05 was applied for all the statistical tests. The genotypic prevalence and AMR patterns of S. aureus were visualized via a heatmap, and the pooled prevalence of S. aureus is displayed on a map. Meta-analyses, including univariate meta-regression, subgroup analyses, forest plots, funnel plots, and sensitivity analyses, were performed using Stata v18.0 (StataCorp, College Station, TX, USA). Visualization of geographic distributions and heatmaps was conducted in R (v4.5.2) using different packages, such as ggplot2 and spdep, to generate figures and maps [66].

3. Results

3.1. Search results and eligible studies

A systematic literature search was performed to identify studies examining the epidemiology of S. aureus in accordance with the PRISMA 2020 guidelines (Fig. 1). The literature search initially identified 4693 records, including PubMed (n = 612), Scopus (n = 1699), and Web of Science (n = 2896), through database and registry searches (Supplementary 1 Table 2). After 2874 duplicate records were removed, 1819 unique articles were screened on the basis of titles and abstracts, resulting in the exclusion of 1079 studies that did not meet the inclusion criteria. The full texts of 740 articles were assessed for eligibility; 611 were excluded because they lacked prevalence data for S. aureus. Ultimately, 143 studies were included in the SRMA.

Fig. 1 — PRISMA flow diagram illustrates the literature search strategy and study selection process.

3.2. Descriptive characteristics of the included studies

This SRMA incorporated studies from 40 countries/regions globally. The included studies were distributed as follows: Algeria (n = 3) [[67], [68], [69]], Argentina (n = 1) [70], Australia (n = 1) [71], Bangladesh (n = 6) [[72], [73], [74], [75], [76], [77]], Brazil (n = 10) [[78], [79], [80], [81], [82], [83], [84], [85], [86], [87]], Colombia (n = 1) [88], Cameroon (n = 1) [89], China (n = 18) [[90], [91], [92], [93], [94], [95], [96], [97], [98], [99], [100], [101], [102], [103], [104], [105], [106], [107]], Czech Republic (n = 2) [108,109], Egypt (n = 15) [[110], [111], [112], [113], [114], [115], [116], [117], [118], [119], [120], [121], [122], [123], [124]], Ethiopia (n = 14) [[125], [126], [127], [128], [129], [130], [131], [132], [133], [134], [135], [136], [137], [138]], Germany (n = 2) [139,140], India (n = 12) [[141], [142], [143], [144], [145], [146], [147], [148], [149], [150], [151], [152]], Indonesia (n = 1) [153], Iran (n = 9) [[154], [155], [156], [157], [158], [159], [160], [161], [162]], Italy (n = 1) [163], Japan (n = 1) [164], Jordan (n = 2) [165,166], Kazakhstan (n = 2) [167,168], Kenya (n = 3) [[169], [170], [171]], Lithuania (n = 1) [172], Malaysia (n = 1) [173], Mexico (n = 1) [174], New Zealand (n = 2) [175,176], Rwanda (n = 1) [177], Norway (n = 1) [178], Pakistan (n = 6) [[179], [180], [181], [182], [183], [184]], Poland (n = 2) [185,186], Saudi Arabia (n = 1) [187], Slovakia (n = 1) [188], South Korea (n = 3) [[189], [190], [191]], Sri Lanka (n = 1) [192], Sweden (n = 2) [193,194], Taiwan (n = 1) [195], Thailand (n = 2) [196,197], Turkey (n = 5) [[198], [199], [200], [201], [202]], Ukraine (n = 1) [203], Uruguay (n = 1) [204], USA (n = 4) [[205], [206], [207], [208]], and Vietnam (n = 1) [209]. These studies collectively provide global coverage across Asia, Africa, Europe, North and South America, and Oceania and offer a comprehensive overview of the epidemiological landscape (Fig. 2).

Fig. 2 — Number of articles from different countries/regions.

The distribution of publications by research topic is presented in Fig. 3. A total of 143 articles were included in the analysis. Among these, studies focusing on the prevalence of S. aureus constituted the largest number (n = 126). In contrast, fewer studies have addressed AMR patterns (n = 66), while investigations targeting AMR-associated genes were the least represented (n = 32).

3.3. Meta-analysis of S. aureus

The SRMA included 126 published studies comprising 145,457 samples, of which 14,527 were positive for S. aureus (Fig. 4). The forest plot presents the prevalence estimates from individual studies, their corresponding 95% CIs, and the overall pooled prevalence. The pooled prevalence, calculated using a random-effects model, was 24.78% (95% CI: 21.27%-28.47%, with substantial heterogeneity among studies (I² = 99.51%, τ² = 0.22, χ² = 16333.70, p < 0.001). The estimated prevalence varied across studies from 0.70% (95% CI: 0.19%-1.47%) reported by Krukowski et al. [185] to 100.00% (95% CI: 94.53%-100.00%) reported by Ramasamy et al. [210].

3.4. Subgroup meta-analysis

The subgroup meta-analysis revealed substantial variability in the pooled prevalence of S. aureus associated with bovine IMIs across study designs, publication years, and geographical regions (Table 1). In terms of study design, cross-sectional studies reported a significantly greater pooled prevalence (25.08%, 95% CI: 21.56-28.76) than longitudinal studies (1.07%, 95% CI: 0.85-1.30), with marked heterogeneity observed among cross-sectional studies (I² = 99.45%, p < 0.001). Temporal stratification revealed significant fluctuations in prevalence estimates, ranging from 8.53% (95% CI: 1.29-21.00) in 2014 to a peak of 41.39% (95% CI: 29.31-54.02) in 2018. Most yearly subgroups exhibited high between-study heterogeneity (I²>95%, p < 0.001). The geographical subgroup analysis further highlighted pronounced regional differences. Higher pooled prevalence estimates were observed in countries/regions such as Cameroon (67.00%), Sri Lanka (64.32%), Indonesia (56.98%), India (44.02%), Mexico (48.00%), Japan (47.44%), and Uruguay (47.07%), whereas markedly lower prevalences were reported in Poland (0.70%), Australia (5.49%), and New Zealand (5.32%) (Fig. 5). Several country-specific estimates demonstrated substantial heterogeneity (I²>90%), underscoring the influence of regional management practices, diagnostic approaches, and study methodologies on reported prevalence. The continent-wise subgroup analysis demonstrated higher pooled prevalence estimates in Africa (29.21%, 95% CI: 22.66-36.22), North America (28.15%, 95% CI: 17.54-40.13), and Asia (25.88%, 95% CI: 20.81-31.30), with a comparatively lower prevalence in Europe (14.19%, 95% CI: 6.98-23.39) and Oceania (5.27%, 95% CI: 5.10-5.45) (Fig. 6). These findings indicate that both methodological and geographical factors significantly contribute to the observed heterogeneity in S. aureus prevalence among bovine IMIs.

Fig. 5 — Global prevalence of *S. aureus* in bovine IMIs.

Fig. 6 — Continent-wise prevalence of *S. aureus* in bovine IMIs.

3.5. Meta-regression

Univariate meta-regression was conducted to explore potential sources of heterogeneity in the pooled prevalence estimates among the study-level covariates (Table 2). Among these factors, study year (β = 0.0056, 95% CI: −0.0138 to 0.0251; p = 0.57) and the number of positive cases (β = −0.0001, 95% CI: −0.0004 to 0.0002; p = 0.50) were not significantly associated with prevalence. Similarly, country (β = −0.0067, 95% CI: −0.0067 to 0.0042; p = 0.12) and study design (β = −0.8445, 95% CI: −1.7601 to 0.0712; p = 0.07) had no statistically significant effects, accounting for only a small proportion of the between-study variance (R² = 1.15% and 1.87%, respectively). In contrast, sample size was significantly associated with prevalence estimates (β = −0.00002, 95% CI: −0.00003 to −0.000003; p = 0.02), explaining 3.41% of the between-study variance, indicating that studies with larger sample sizes tended to report lower prevalence estimates. These findings should be interpreted with caution, as the lack of statistical significance for most covariates may be attributable to substantial residual heterogeneity, limited statistical power, and unmeasured or inconsistently reported study-level characteristics.

3.6. Publication bias

The funnel plot showed visual asymmetry, which suggests potential publication bias among the included studies (Fig. 7). The uneven distribution of studies, particularly those with larger standard errors, suggests potential publication bias and/or small-study effects. This asymmetry indicates that studies reporting lower or null prevalence estimates may be underrepresented in the literature. Consequently, the pooled prevalence estimate should be interpreted with caution, as selective publication or methodological differences among smaller studies may have influenced the overall summary estimate. The presence of small-study effects was further evaluated using Egger’s regression test. The test demonstrated strong evidence of asymmetry (β = 7.60, p < 0.05), confirming statistically significant small-study effects. Collectively, these findings indicate that publication bias cannot be ruled out; therefore, the pooled prevalence estimates should be interpreted with caution.

3.7. Trim and fill analysis

Owing to evidence of small-study effects, a trim-and-fill analysis was performed to assess the potential influence of publication bias on the pooled prevalence estimate (Fig. 8). The procedure imputed 59 potentially missing studies, increasing the total number of included studies from 126 to 185. After trim-and-fill adjustment, the random-effects model estimated a pooled prevalence of 7.44% (95% CI: 4.53-10.97), while substantial heterogeneity persisted (τ² = 0.1730, I² = 99.4%; χ² = 29,663.43; p < 0.001).

Fig. 8 — Funnel plot with Trim and Fill. The gray circles indicate observed studies, while the white circles represent imputed studies added by the trim-and-fill method to account for possible publication bias.

3.8. Sensitivity analysis

To evaluate the robustness of the pooled prevalence estimate, a leave-one-out sensitivity analysis was performed in which each study was sequentially omitted (Fig. 9). The pooled prevalence estimates remained highly consistent across all studies, ranging from 0.24 (95% CI: 0.21-0.28) to 0.25 (95% CI: 0.22-0.29), indicating that no individual study exerted a disproportionate influence on the overall effect size. This stability across successive exclusions underscores the robustness of the meta-analytic findings and suggests that the observed heterogeneity is not driven by any single study.

Fig. 9 — Leave-one-out sensitivity analysis of the pooled prevalence of *S. aureus* in bovine IMIs estimated via a random effects model.

3.9. Meta-analysis of AMR carriage

The meta-analysis of AMR carriage revealed a high and variable prevalence of resistance across the antibiotics evaluated (Table 3). Resistance was most frequently reported for penicillin (65.19%, 95% CI: 56.13-74.25), ampicillin (62.80%, 95% CI: 53.14-72.46), oxytetracycline (62.42%, 95% CI: 41.17-83.68), doxycycline (70.73%, 95% CI: 40.06-100.00), and amoxicillin (52.07%, 95% CI: 39.64-64.50). Moderate levels of resistance were observed for erythromycin (37.56%), tetracycline (38.74%), trimethoprim-sulfamethoxazole (47.18%), oxacillin (40.23%), vancomycin (44.62%), and norfloxacin (40.40%). In contrast, comparatively lower resistance estimates were identified for amikacin (18.31%), gentamicin (27.51%), ciprofloxacin (30.81%), chloramphenicol (26.82%), and streptomycin (30.45%).

Table 3.

Meta-analysis of AMR carriage.

Antibiotics	N	% (95% CI)	τ²	χ²	I²	p value
Amikacin	6	18.31 [1.15, 35.48]	0.04	72.17	93.1	<0.001
Amoxicillin	21	52.07 [39.64, 64.50]	0.08	3215.33	99.4	<0.001
Ampicillin	34	62.80 [53.14, 72.46]	0.08	4278.31	99.2	<0.001
Azithromycin	3	36.49 [5.57, 67.40]	0.07	31.94	93.7	<0.001
Cefotaxime	6	24.73 [6.92, 42.54]	0.05	112.49	95.6	<0.001
Cefoxitin	27	31.95 [19.29, 44.62]	0.11	8646.75	99.7	<0.001
Ceftazidime	6	66.44 [37.33, 95.54]	0.13	634.24	99.2	<0.001
Ceftiofur	6	36.43 [0.00, 75.08]	0.23	4171.81	99.9	<0.001
Ceftriaxone	5	35.07 [1.28, 68.86]	0.15	865.77	99.5	<0.001
Cefuroxime	1	62.96 [42.37, 80.60]	-	-	-	-
Cephalexin	4	34.86 [0.00, 78.48]	0.20	857.36	99.7	<0.001
Cephalothin	3	33.21 [0.00, 95.36]	0.30	644.50	99.7	<0.001
Chloramphenicol	15	26.82 [12.18, 41.45]	0.08	4866.12	99.7	<0.001
Clindamycin	24	31.97 [19.45, 44.50]	0.10	1819.85	98.7	<0.001
Ciprofloxacin	19	30.81 [19.58, 42.04]	0.06	505.24	96.4	<0.001
Doxycycline	4	70.73 [40.06, 100.00]	0.09	90.74	96.7	<0.001
Enrofloxacin	3	35.95 [0.00, 90.28]	0.23	482.16	99.6	<0.001
Erythromycin	35	37.56 [27.28, 47.85]	0.09	6777.47	99.5	<0.001
Gentamicin	28	27.51 [16.78, 38.23]	0.08	4587.33	99.4	<0.001
Kanamycin	11	35.27 [15.77, 54.77]	0.11	1300.98	99.2	<0.001
Levofloxacin	5	32.16 [8.44, 55.87]	0.07	108.45	96.3	<0.001
Methicillin	1	12.77 [5.27, 24.48]	-	-	-	-
Neomycin	4	46.58 [7.50, 85.67]	0.16	520.47	99.4	<0.001
Norfloxacin	7	40.40 [15.64, 65.16]	0.11	197.46	97.0	<0.001
Ofloxacin	1	3.79 [1.24, 8.62]	-	-	-	-
Oxacillin	23	40.23 [25.75, 54.72]	0.12	3310.40	99.3	<0.001
Oxytetracycline	7	62.42 [41.17, 83.68]	0.08	310.88	98.1	<0.001
Penicillin	50	65.19 [56.13, 74.25]	0.10	19503.22	99.7	<0.001
Rifampicin	5	33.92 [7.23, 60.61]	0.09	70.90	94.4	<0.001
Rifaximin	1	5.26 [0.64, 17.75]	-	-	-	-
Streptomycin	17	30.45 [19.43, 41.46]	0.05	312.48	94.9	<0.001
Tetracycline	43	38.74 [29.10, 48.38]	0.10	7002.09	99.4	<0.001
Trimethoprim–sulfamethoxazole	18	47.18 [32.85, 61.51]	0.09	4248.83	99.6	<0.001
Tylosin	4	19.20 [6.80, 31.60]	0.01	24.40	87.7	<0.001
Vancomycin	9	44.62 [20.10, 69.13]	0.14	1503.35	99.5	<0.001

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3.10. Geographical AMR patterns of S. aureus and antibiotic classes

The AMR patterns of S. aureus varied at the continental level across major antibiotic classes (Fig. 10). Substantial heterogeneity in resistance patterns was observed among the continents and antibiotic groups. High resistance levels were most frequently observed for β-lactams, particularly in Europe and South America, where resistance was the highest across all antimicrobial classes. Europe also demonstrated elevated resistance to glycopeptides and macrolides. In contrast, North America generally exhibited comparatively lower resistance for several classes, including aminoglycosides, fluoroquinolones, and macrolides. Africa and Asia presented moderate to high resistance for multiple antimicrobial classes. Moreover, Asia has demonstrated significant resistance to tetracyclines, sulfonamides, and macrolides, whereas Africa has shown intermediate-to-high resistance to aminoglycosides and sulfonamides. Furthermore, resistance to cephalosporins was particularly pronounced in South America. Low resistance levels were mainly observed for fluoroquinolones and lincosamides in North America and parts of Europe, whereas intermediate resistance dominated most other continent-continent combinations.

The country-wide distribution of AMR patterns in S. aureus demonstrated pronounced inter-country heterogeneity across major antimicrobial classes (Fig. 11). Resistance levels vary substantially between countries/regions and antimicrobial classes within the same geographical region. High resistance to β-lactams has been consistently observed across a wide range of countries/regions, particularly in India, China, Egypt, Brazil, and Turkey. Moreover, resistance to tetracyclines and macrolides was also moderate to high in several countries/regions, including Bangladesh, India, Iran, and Indonesia. Aminoglycoside resistance showed marked heterogeneity, with elevated resistance in countries/regions such as India and South Africa, whereas lower levels were observed in Japan and South Korea. Fluoroquinolone resistance was generally moderate but reached relatively high levels in parts of South Asia and Southeast Asia. In contrast, resistance to glycopeptides has remained low to intermediate in most countries/regions.

Fig. 11 — Heatmap showing the prevalence of AMR patterns across antimicrobial classes in *S. aureus* across countries/regions. The colors indicate resistance levels: blue indicates low prevalence, red indicates high prevalence, and purple indicates intermediate values.

3.11. Genotypic resistance pattern

Although PCR has been widely used to detect resistance genes, assessing the overall prevalence of genotypic AMR remains challenging because primer sequences vary across studies. A heatmap shows the AMR gene distribution, with rows representing individual studies and columns corresponding to specific genes (Fig. 12). The color intensity indicates prevalence, with red indicating a higher prevalence and blue indicating a lower prevalence. Genes associated with β-lactam resistance, including blaZ and mecA, were highly prevalent, indicating widespread β-lactam resistance. Macrolide-lincosamide-and streptogramin (MLS) resistance genes, such as ermC, ermB, msrA, and mphC, were also commonly observed, reflecting broad resistance to these antibiotic classes. Tetracycline resistance genes, including tetK, tetM, and tetL, were present in a substantial proportion of the isolates, indicating significant resistance to tetracycline. Moreover, genes encoding aminoglycoside-modifying enzymes were identified, suggesting potential aminoglycoside resistance. Additional resistance determinants, including trimethoprim resistance, vancomycin resistance, and efflux pump-associated genes, were also detected, highlighting the presence of multidrug resistance (MDR) mechanisms in S. aureus.

Fig. 12 — Heatmap depicting the prevalence of AMR genes across published studies. Rows represent individual studies, columns correspond to specific AMR genes, and color intensity reflects prevalence, with red indicating higher and blue indicating lower prevalence.

4. Discussion

To the best of our knowledge, this is the first SRMA to explore the prevalence of S. aureus from bovine IMIs globally. Moreover, the AMR pattern to 35 antibiotics and the associated AMR genotype profile across 40 countries/regions around the world were determined. We collected data via a systematic review of peer-reviewed publications from 2010 to 2025. These findings demonstrate that S. aureus remains a major and persistent pathogen in bovine mastitis worldwide, with considerable heterogeneity observed among regions. This variability reflects differences in dairy production systems, herd management practices, diagnostic methodologies, AMU, and regulatory frameworks. Furthermore, the widespread occurrence of resistance to multiple antimicrobial classes, together with the frequent detection of resistance determinants, highlights the growing challenge of AMR S. aureus in the dairy sector and underscores its relevance within a One Health context, which emphasizes animal health, food safety, and public health.

This meta-analysis determined the pooled prevalence of S. aureus in bovine IMIs globally from 126 studies. The pooled prevalence was 24.78%, with significant heterogeneity (I² = 99.51%, p < 0.001). This outcome was compared with that of a previous SRMA reported by Ahmed et al. [60] (38.1%, 95% CI: 29.6-47) from meat and meat products, and by Wang et al. [211] (36.23%, 95% CI: 29.31-43.76) from bovine mastitis. However, substantially lower pooled prevalence estimates have been reported for methicillin-resistant S. aureus (MRSA). A meta-analysis of clinical and subclinical bovine mastitis cases reported an overall MRSA prevalence of 4.30% (95% CI: 3.24-5.50) [212], whereas a separate global analysis focusing on dairy farm settings estimated an even lower prevalence of 3.81% (95% CI: 2.61-5.20) [213]. The substantial differences in pooled prevalence estimates of S. aureus in bovine IMIs are likely driven by methodological and contextual heterogeneity among studies. Variations in sampling frames and diagnostic approaches, such as differences in culture methods and identification criteria, can significantly influence detection rates and contribute to inconsistency across estimates [214]. Additionally, regional and temporal factors, including geographic disparities in herd management, climate, and AMU practices, affect pathogen distribution and transmission dynamics, as evidenced by differing prevalence rates in Asia, Europe, and other regions [212,215]. Taken together, these factors underscore the need to interpret global prevalence estimates of S. aureus in the context of methodological and epidemiological diversity among underlying studies.

In the present meta-analysis, the pooled prevalence of S. aureus was greater in recent studies published between 2018 and 2025 than in those published between 2010 and 2017. This finding contrasts with earlier reports indicating a declining trend over time, which attributed the reduced prevalence to advances in technology and improved farm-level biosecurity measures [211]. The opposite pattern observed in our study may reflect enhanced surveillance and the wider adoption of sensitive diagnostic tools, including improved culture protocols and molecular methods, which increase the detection of S. aureus, which may have been underreported in earlier periods. Moreover, the intensification of dairy production systems, characterized by larger herd sizes, increased animal density, and higher milking frequency, may promote the persistence and transmission of S. aureus and other mastitis pathogens [135,216]. Persistent gaps in mastitis control programs and the emergence of AMR with the biofilm-forming capacity of S. aureus may further undermine the effectiveness of existing control strategies [217,218].

This SRMA identified significant geographic variation in the prevalence of S. aureus in bovine IMIs, with relatively low rates reported in Oceanian and some European countries/regions and higher rates reported in African, North American, and Asian regions. These disparities are consistent with the findings of global meta-analyses, which reported that Latin America often presented the highest pooled prevalence of mastitis pathogens (51%), whereas Oceania and Europe generally presented lower estimates (28%) for Staphylococcus spp., predominantly S. aureus, across large-scale surveys of dairy herds [215]. The possible explanation for these regional differences may reflect variations in herd management practices, diagnostic approaches, and the implementation of mastitis control programs, contributing to the observed heterogeneity in prevalence estimates.

Univariate regression identified sample size and continent as significant influencing factors for the prevalence of S. aureus. These findings are broadly consistent with those of previous studies, which reported that factors such as country can affect the prevalence of S. aureus and other mastitis pathogens, including E. coli and Salmonella spp. [60]. The observed differences in influencing factors across studies likely reflect heterogeneity in herd management, hygiene practices, environmental conditions, and diagnostic protocols among regions and sample sources [60,219]. This underscores the importance of considering study- and region-specific factors when interpreting prevalence estimates and designing targeted mastitis control strategies.

The overuse or irresponsible AMU promotes the emergence of AMR, which leads to MDR and reduces the effectiveness of treatment [220]. AMR is widely recognized as a silent pandemic and a critical public health concern that demands immediate and effective management rather than being viewed as a problem of the future [221]. Without effective preventive measures, AMR could become the leading cause of death globally by 2050, with AMR-related mortality increasing from over 1.2 million deaths in 2019 to an estimated 10 million deaths annually [222]. In this SRMA, beta-lactams, including penicillin, ampicillin, amoxicillin, and oxacillin; tetracyclines, including oxytetracycline, tetracycline, and doxycycline; and sulfonamide, had the highest resistance rate to S. aureus isolated from bovine IMI. This may be because MRSA strains are MDR and include human-specific clones (ST239 and ST8) isolated from bovine mastitis, which may indicate transmission between humans and animals and contribute to the prevalence of resistance [223]. Another possible cause is that uncontrolled and rational antibiotic use in dairy herds can select for and disseminate MDR clones, which is a key interpretation for the high resistance rates observed for common mastitis treatments, including preventive and therapeutic methods [223,224].

Moreover, resistance to these antimicrobials in S.aureus is further exacerbated by the predominantly biofilm-forming nature of these strains, which impedes antimicrobial penetration and is closely associated with reduced susceptibility and treatment failure [225]. Furthermore, the associations between average herd parity and resistance to ampicillin and tetracycline, as well as between herd size and tetracycline resistance, suggest that non-AMU factors, including herd demographics and management intensity, also play a significant role in shaping resistance patterns [226]. In contrast, amikacin, gentamicin, chloramphenicol, and ciprofloxacin had lower rates of AMR in this study, which is likely due to their less frequent use by clinicians [227].

Approximately 67% of AMU intensity hotspots are concentrated in Asia, primarily eastern China, southern and eastern India, Central Java (Indonesia), central Thailand, the eastern coastline of Vietnam, western South Korea, Bangladesh, Pakistan, and northwestern Iran [228]. In addition, Brazil, China, Australia, India, and the USA collectively account for 58% of the global AMU [228]. This study revealed that European countries/regions, including Turkey and Poland; Asian countries/regions, such as South Korea, China, and Iran; African countries/regions, including Cameroon, Ethiopia, and Egypt; and several Latin American countries/regions presented relatively high levels of AMR to β-lactams. Moreover, cephalosporin, aminoglycoside and macrolide resistance has also been shown in African and Asian nations. This widespread resistance may be attributed to the extensive and prolonged use of β-lactams in veterinary practice, particularly for growth promoters and prophylactic purposes [229].

Our results revealed that β-lactam resistance genes, especially blaZ and mecA, were highly prevalent in S. aureus. blaZ encodes a β-lactamase enzyme that hydrolyzes the β-lactam ring, conferring resistance to penicillin and related antibiotics [230], whereas mecA mediates resistance to methicillin and other β-lactams through the production of an altered penicillin-binding protein (PBP2a) with reduced antibiotic affinity [231]. The widespread presence of these genes suggests that β-lactam antibiotics may be largely ineffective against a significant proportion of bovine IMI isolates, posing challenges for empirical therapy and control of infections caused by β-lactam-resistant organisms.

In addition to β-lactam resistance determinants, a diverse array of MLS resistance genes are frequently detected. Genes such as ermC, ermB, msrA, and mphC were common, indicating broad resistance to MLS antibiotics. The erm genes encode methyltransferases that modify the ribosomal target site, leading to cross-resistance among macrolides, lincosamides, and streptogramin B drugs [232]. The msrA gene is associated with active efflux of macrolides [233], whereas mphC encodes a macrolide-phosphotransferase that inactivates the antibiotic [234]. The co-occurrence of these genes suggests that multiple resistance mechanisms may contribute to reduced susceptibility within the MLS group, potentially limiting the utility of these antibiotics in clinical practice.

Our results also revealed a substantial prevalence of tetracycline resistance genes, including tetK, tetM, and tetL. The tetK and tetL genes encode efflux pumps that actively expel tetracycline from bacterial cells [235], whereas tetM confers ribosomal protection that prevents tetracycline from inhibiting protein synthesis [236]. The high frequency of these determinants reflects significant selective pressure from tetracycline use, which may be driven by its widespread application in both the human and veterinary sectors. The presence of multiple tetracycline resistance genes within the same isolates highlights the potential for co-selection and horizontal gene transfer (HGT), which can facilitate the spread of resistance across different bacterial species. Moreover, a study reported that 22.28% of S. aureus isolates carried the mecA gene, indicating the occurrence of MRSA, while 6.28% harbored the pvl virulence gene, underscoring the coexistence of AMR and virulence determinants in bovine mastitis isolates [181].

HGT refers to the non-vertical transfer of genetic material between organisms and is a major mechanism by which bacteria acquire and spread AMR determinants, independent of reproduction from parent to offspring [237]. In bacteria, HGT is predominantly mediated by mobile genetic elements (MGEs), such as plasmids, transposons, integrative and conjugative elements (ICEs), and insertion sequences, which can carry resistance genes between cells through mechanisms including conjugation, transformation, and transduction [238]. MGEs facilitate rapid genomic plasticity, enabling resistance genes such as tetK, tetM, and tetL to be mobilized and incorporated into diverse bacterial genomes under antibiotic selection pressures [239]. Plasmids, in particular, can accumulate resistance determinants and be transferred across species barriers [240], whereas transposons can mobilize resistance genes between plasmid and chromosomal locations, increasing their potential for spread [241]. The linkage of resistance genes with MGEs thereby promotes coselection and dissemination of MDR strains within and between bacterial populations, contributing to the persistence and expansion of resistant phenotypes under clinical and environmental conditions [242].

4.1. Limitations

This study has a few limitations. First, the systematic review protocol was not prospectively registered in PROSPERO or any other registry. However, the review followed a predefined methodology based on PRISMA guidelines, including a systematic literature search, clearly defined inclusion and exclusion criteria, and a structured approach to data extraction and synthesis. We recognize that prospective registration could have further improved transparency and confidence in the study’s a priori design. Second, studies with incomplete reporting were excluded, which may have introduced bias into the findings. While the pooled prevalence estimates provide an overall summary, substantial heterogeneity across studies requires cautious interpretation. This heterogeneity may reflect differences in study design, sample sources, geographic regions, diagnostic methods, antimicrobial susceptibility testing protocols, and study periods among the included studies, despite the application of subgroup analyses, sensitivity analyses, and meta-regression. Third, data were collected from 40 countries/regions worldwide, but not all countries/regions within each continent were represented. Therefore, the findings should be interpreted cautiously, as they mainly reflect regions with available data. Finally, this study is subject to publication bias, which may have influenced the reported results. Furthermore, unpublished studies and selective reporting may have affected the pooled estimates, potentially limiting the overall generalizability of the findings. Consequently, the findings should be interpreted with caution.

4.2. Implications

AMR has emerged as a major threat to public health, undermining the prevention and treatment of infectious diseases. Its rise is driven by the misuse and overuse of antibiotics in healthcare and agriculture, as well as bacterial evolution and HGT. AMR continues to grow globally despite ongoing control efforts. This trend imposes severe economic burdens, including increased healthcare costs from increased hospitalizations and drug use. This study provides insights into the distribution and trends of S. aureus isolated from bovine IMI and AMR patterns with genotypes. The findings of this study highlight the urgent need for coordinated policies to control SA infections in dairy herds and mitigate the spread of AMR. Strategies should include the prudent use of antibiotics in veterinary and agricultural practices, routine surveillance of bacterial prevalence and resistance patterns, and the implementation of mastitis control programs. Moreover, strengthening regulations on antibiotic use, promoting farmer and veterinarian education, and encouraging the adoption of biosecurity and hygiene measures can help reduce the incidence of bovine IMI and limit the emergence of resistant strains. These actions are essential for safeguarding animal health, protecting public health, and reducing the economic burden associated with AMR.

5. Conclusion

S. aureus remains a pervasive and economically significant pathogen in bovine mastitis worldwide, driven by its diverse virulence factors, diagnostic complexity, and increasing AMR. From a One Health perspective, zoonotic risk, particularly associated with MRSA via occupational exposure and foodborne transmission, poses a notable public health concern. This SRMA demonstrated a considerable global burden of S. aureus in bovine IMI, with a relatively high prevalence in countries/regions such as Cameroon, Sri Lanka, Indonesia, India, Mexico, Japan, and Uruguay. Regionally, Asia has shown substantial resistance to tetracyclines, sulfonamides, and macrolides, while the highest resistance across all antimicrobial classes, especially β-lactams, has been observed in Europe and South America. The extensive use of antibiotics in food animal production for therapy, prophylaxis, and growth promotion has further intensified AMR, exposing even healthy animals to antimicrobial pressure. These findings highlight the urgent need for stricter regulations on antibiotic use across the food chain, alongside continuous surveillance of resistance patterns. Effective control of S. aureus in bovine mastitis requires coordinated efforts involving antimicrobial stewardship, farmer education, hygienic milking practices, selective dry cow therapy, and active engagement of veterinarians, healthcare professionals, farm workers, and consumers to reduce the disease burden and curb the spread of β-lactam resistance.

CRediT authorship contribution statement

Md Jisan Ahmed: Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Software, Resources, Project administration, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Md Arifur Rahman: Writing – review & editing, Writing – original draft, Validation, Data curation. Ritu Chalise: Writing – review & editing, Writing – original draft, Validation, Data curation. Prajwal Bhandari: Writing – review & editing, Writing – original draft. Md Ismile Hossain Bhuiyan: Writing – review & editing, Writing – original draft, Validation, Data curation. Md Imran Hossain: Validation, Data curation. Israt Jahan Kaderi: Validation, Data curation. Md Afiqul Islam Rahi: Writing – original draft, Validation, Data curation. Delower Hossain: Writing – review & editing, Writing – original draft, Validation, Supervision, Software, Resources, Methodology, Investigation, Data curation, Conceptualization.

Clinical trial

Not Applicable.

Availability of data and materials

The datasets used and/or analyzed during the current study are available in the supplementary materials.

Ethical approval and consent to participate

Not Applicable.

Consent for publication

Not applicable.

Funding

This study did not receive any grants from any funding agencies.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We acknowledge and appreciate the efforts of all members of the Association of Coding, Technology, and Genomics (ACTG) in facilitating this research. The authors appreciate the University of Milan, Italy for providing literature support.

Footnotes

^{Appendix A}

Supplementary data to this article can be found online at https://doi.org/10.1016/j.nmni.2026.101860.

Contributor Information

Md Jisan Ahmed, Email: jisan.path1506605@sau.edu.bd.

Md Arifur Rahman, Email: arif1707695@sau.edu.bd.

Ritu Chalise, Email: ritu-1910143@sau.edu.bd.

Prajwal Bhandari, Email: prajwal-1910152@sau.edu.bd.

Md Ismile Hossain Bhuiyan, Email: ismile.apma-1708046@sau.edu.bd.

Md Imran Hossain, Email: imran-1708049@sau.edu.bd.

Israt Jahan Kaderi, Email: isratjk1707663@sau.edu.bd.

Md Afiqul Islam Rahi, Email: afiqulislamrahi07@gmail.com.

Delower Hossain, Email: delowervet@sau.edu.bd.

Abbreviations

AMR: Antimicrobial resistance
AMU: Antimicrobial usage
CI: Confidence interval
HGT: Horizontal gene transfer
ICEs: Integrative and conjugative elements
IMI: Intramammary infection
MDR: Multidrug-resistant
MeSH: Medical subject headings
MGEs: Mobile genetic elements
MLS: Macrolide-lincosamide-streptogramin
MRSA: Methicillin-resistant Staphylococcus aureus
PBP2a: Penicillin-binding protein 2a
PRISMA: Preferred reporting items for systematic reviews and meta-analysis
PROSPERO: International prospective register of systematic reviews
SRMA: Systematic reviews and meta-analysis

Appendix A. Supplementary data

The following are the Supplementary data to this article:

Multimedia component 1

mmc1.docx^{(33.9KB, docx)}

Multimedia component 2

mmc2.xlsx^{(22KB, xlsx)}

References

1.M.W. Dictionary. 2020. Available from: www.Merriam-Webster.com.
2.Djabri B., Bareille N., Beaudeau F., Seegers H. Quarter milk somatic cell count in infected dairy cows: a meta-analysis. Vet Res. 2002;33(4):335–357. doi: 10.1051/vetres:2002021. [DOI] [PubMed] [Google Scholar]
3.Thorberg B.-M., Danielsson-Tham M.-L., Emanuelson U., Waller K.P. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J Dairy Sci. 2009;92(10):4962–4970. doi: 10.3168/jds.2009-2184. [DOI] [PubMed] [Google Scholar]
4.De Vliegher S., Fox L., Piepers S., McDougall S., Barkema H. Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J Dairy Sci. 2012;95(3):1025–1040. doi: 10.3168/jds.2010-4074. [DOI] [PubMed] [Google Scholar]
5.Muzammil I., Ijaz M., Saleem M.H., Ali M.M. Drug repurposing strategy: an emerging approach to identify potential therapeutics for treatment of bovine mastitis. Microb Pathog. 2022;171 doi: 10.1016/j.micpath.2022.105691. [DOI] [PubMed] [Google Scholar]
6.Boss R., Naskova J., Steiner A., Graber H. Mastitis diagnostics: quantitative pcr for Staphylococcus aureus genotype b in bulk tank milk. J Dairy Sci. 2011;94(1):128–137. doi: 10.3168/jds.2010-3251. [DOI] [PubMed] [Google Scholar]
7.Barkema H., Schukken Y., Zadoks R. Invited review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci. 2006;89(6):1877–1895. doi: 10.3168/jds.S0022-0302(06)72256-1. [DOI] [PubMed] [Google Scholar]
8.Botaro B.G., Cortinhas C.S., Dibbern A.G., Silva L.F.P.e., Benites N.R., dos Santos M.V. Staphylococcus aureus intramammary infection affects milk yield and scc of dairy cows. Trop Anim Health Prod. 2015;47(1):61–66. doi: 10.1007/s11250-014-0683-5. [DOI] [PubMed] [Google Scholar]
9.Sutra L., Poutrel B. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J Med Microbiol. 1994;40(2):79–89. doi: 10.1099/00222615-40-2-79. [DOI] [PubMed] [Google Scholar]
10.Tigabu A., Getaneh A. Staphylococcus aureus, eskape bacteria challenging current health care and community settings: a literature review. Clin Lab. 2021;67(7) doi: 10.7754/Clin.Lab.2020.200930. [DOI] [PubMed] [Google Scholar]
11.Haag A.F., Fitzgerald J.R., Penadés J.R. Staphylococcus aureus in animals. Microbiol Spectr. 2019;7(3) doi: 10.1128/microbiolspec.gpp1123-0060-2019. [DOI] [PMC free article] [PubMed] [Google Scholar]
12.Javed M.U., Ijaz M., Ahmed A., Rasheed H., Sabir M.J., Jabir A.A. Molecular dynamics and antimicrobial resistance pattern of β-lactam resistant coagulase positive Staphylococcus aureus isolated from goat mastitis. Pak Vet J. 2024;44(2) [Google Scholar]
13.Al-Majali A.M., Al-Qudah K.M., Al-Tarazi Y.H., Al-Rawashdeh O.F. Risk factors associated with camel brucellosis in Jordan. Trop Anim Health Prod. 2008;40(3):193–200. doi: 10.1007/s11250-007-9080-7. [DOI] [PubMed] [Google Scholar]
14.Sharifi A., Mahmoudi P., Sobhani K. The prevalence of adhesion and biofilm genes in Staphylococcus aureus isolates from bovine mastitis: a comprehensive meta‐analysis. Vet Med Sci. 2024;10(2) doi: 10.1002/vms3.1378. [DOI] [PMC free article] [PubMed] [Google Scholar]
15.Liu H., Xiao Y., Nie H., Huang Q., Chen W. Influence of (p) ppgpp on biofilm regulation in Pseudomonas putida kt2440. Microbiol Res. 2017;204:1–8. doi: 10.1016/j.micres.2017.07.003. [DOI] [PubMed] [Google Scholar]
16.Oranusi S., Galadima M., Umoh V. Toxicity test and bacteriophage typing of Staphylococcus aureus isolates from food contact surfaces and foods prepared by families in Zaria, Nigeria. Afr J Biotechnol. 2006;5(4):362–365. [Google Scholar]
17.Yamada H. Tea catechins and Staphylococcus aureus. Tea Health Dise Prevent. 2013:1207–1213. [Google Scholar]
18.Taiwo S., Onile B., Akanbi II A. Methicillin-resistant Staphylococcus aureus (mrsa) isolates in ilorin, Nigeria. Afr J Clin Exp Microbiol. 2004;5(2):189–197. [Google Scholar]
19.Odetokun I.A., Adetona M.A., Ade-Yusuf R.O., Adewoye A.O., Ahmed A.N., Ghali-Mohammed I., Al-Mustapha A.I., Fetsch A. S taphylococcus aureus contamination of animal-derived foods in Nigeria: a systematic review, 2002—2022. Food Safet Risk. 2023;10(1):6. [Google Scholar]
20.Sasirekha B., Usha M., Amruta A., Ankit S., Brinda N., Divya R. Evaluation and comparison of different phenotypic tests to detect methicillin resistant Staphylococcus aureus and their biofilm production. Int J PharmTech Res. 2012;4(2):532–541. [Google Scholar]
21.Smith T.C. Livestock-associated staphylococcus aureus: the United States experience. PLoS Pathog. 2015;11(2) doi: 10.1371/journal.ppat.1004564. [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Oliveira D., Borges A., Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins. 2018;10(6):252. doi: 10.3390/toxins10060252. [DOI] [PMC free article] [PubMed] [Google Scholar]
23.Ryu S., Song P.I., Seo C.H., Cheong H., Park Y. Colonization and infection of the skin by s. Aureus: immune system evasion and the response to cationic antimicrobial peptides. Int J Mol Sci. 2014;15(5):8753–8772. doi: 10.3390/ijms15058753. [DOI] [PMC free article] [PubMed] [Google Scholar]
24.Wertheim H.F., Melles D.C., Vos M.C., Van Leeuwen W., Van Belkum A., Verbrugh H.A., Nouwen J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751–762. doi: 10.1016/S1473-3099(05)70295-4. [DOI] [PubMed] [Google Scholar]
25.Aires de Sousa M., Lencastre de H. Bridges from hospitals to the laboratory: genetic portraits of methicillin-resistant Staphylococcus aureus clones. FEMS Immunol Med Microbiol. 2004;40(2):101–111. doi: 10.1016/S0928-8244(03)00370-5. [DOI] [PubMed] [Google Scholar]
26.Cheung G.Y., Bae J.S., Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12(1):547–569. doi: 10.1080/21505594.2021.1878688. [DOI] [PMC free article] [PubMed] [Google Scholar]
27.Touaitia R., Mairi A., Ibrahim N.A., Basher N.S., Idres T., Touati A. Staphylococcus aureus: a review of the pathogenesis and virulence mechanisms. Antibiotics. 2025;14(5):470. doi: 10.3390/antibiotics14050470. [DOI] [PMC free article] [PubMed] [Google Scholar]
28.Rojo P., Barrios M., Palacios A., Gomez C., Chaves F. Community-associated Staphylococcus aureus infections in children. Expert Rev Anti-infect Ther. 2010;8(5):541–554. doi: 10.1586/eri.10.34. [DOI] [PubMed] [Google Scholar]
29.Esposito S., Blasi F., Curtis N., Kaplan S., Lazzarotto T., Meschiari M., Mussini C., Peghin M., Rodrigo C., Vena A. New antibiotics for Staphylococcus aureus infection: an update from the world association of infectious diseases and immunological disorders (waidid) and the Italian society of anti-infective therapy (sita) Antibiotics. 2023;12(4):742. doi: 10.3390/antibiotics12040742. [DOI] [PMC free article] [PubMed] [Google Scholar]
30.Li X., Zhang J., Zhang H., Shi X., Wang J., Li K., Liang J., Xu X., Zhao W., Zhao C. Genomic analysis, antibiotic resistance, and virulence of Staphylococcus aureus from food and food outbreaks: a potential public concern. Int J Food Microbiol. 2022;377 doi: 10.1016/j.ijfoodmicro.2022.109825. [DOI] [PubMed] [Google Scholar]
31.Founou L.L., Founou R.C., Essack S.Y. Antibiotic resistance in the food chain: a developing country-perspective. Front Microbiol. 2016;7:1881. doi: 10.3389/fmicb.2016.01881. [DOI] [PMC free article] [PubMed] [Google Scholar]
32.Al-Saleh A., Shahid M., Farid E., Bindayna K. Trends in methicillin-resistant Staphylococcus aureus in the gulf cooperation council countries: antibiotic resistance, virulence factors and emerging strains. East Mediterr Health J. 2022;28(6) doi: 10.26719/emhj.22.042. [DOI] [PubMed] [Google Scholar]
33.Bitrus A., Peter O., Abbas M., Goni M.D. Staphylococcus aureus: a review of antimicrobial resistance mechanisms. Vet Sci: Res Rev. 2018;4(2):43–54. [Google Scholar]
34.Turner N.A., Sharma-Kuinkel B.K., Maskarinec S.A., Eichenberger E.M., Shah P.P., Carugati M., Holland T.L., Fowler V.G., Jr. Methicillin-resistant staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol. 2019;17(4):203–218. doi: 10.1038/s41579-018-0147-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
35.Kot B., Wierzchowska K., Piechota M., Grużewska A. Antimicrobial resistance patterns in methicillin-resistant Staphylococcus aureus from patients hospitalized during 2015–2017 in hospitals in Poland. Med Princ Pract. 2020;29(1):61–68. doi: 10.1159/000501788. [DOI] [PMC free article] [PubMed] [Google Scholar]
36.Rasheed H., Ijaz M., Ahmed A., Javed M.U., Shah S.F.A., Anwaar F. Discrepancies between phenotypic and genotypic identification methods of antibiotic resistant genes harboring Staphylococcus aureus. Microb Pathog. 2023;184 doi: 10.1016/j.micpath.2023.106342. [DOI] [PubMed] [Google Scholar]
37.Tobin E.H., Jogu P., Koirala J. Statpearls [internet] StatPearls Publishing; 2025. Methicillin-resistant Staphylococcus aureus. [PubMed] [Google Scholar]
38.Kong C., Neoh H.-m., Nathan S. Targeting Staphylococcus aureus toxins: a potential form of anti-virulence therapy. Toxins. 2016;8(3):72. doi: 10.3390/toxins8030072. [DOI] [PMC free article] [PubMed] [Google Scholar]
39.Murray C.J., Ikuta K.S., Sharara F., Swetschinski L., Aguilar G.R., Gray A., Han C., Bisignano C., Rao P., Wool E. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–655. doi: 10.1016/S0140-6736(21)02724-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
40.Khan S.A., Imtiaz M.A., Sayeed M.A., Shaikat A.H., Hassan M.M. Antimicrobial resistance pattern in domestic animal-wildlife-environmental niche via the food chain to humans with a Bangladesh perspective; a systematic review. BMC Vet Res. 2020;16(1):302. doi: 10.1186/s12917-020-02519-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
41.Argudín M.A., Deplano A., Meghraoui A., Dodémont M., Heinrichs A., Denis O., Nonhoff C., Roisin S. Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics. 2017;6(2):12. doi: 10.3390/antibiotics6020012. [DOI] [PMC free article] [PubMed] [Google Scholar]
42.Byarugaba D. Antimicrobial resistance in developing countries and responsible risk factors. Int J Antimicrob Agents. 2004;24(2):105–110. doi: 10.1016/j.ijantimicag.2004.02.015. [DOI] [PubMed] [Google Scholar]
43.Hogeveen H., Huijps K., Lam T. Economic aspects of mastitis: new developments. N Z Vet J. 2011;59(1):16–23. doi: 10.1080/00480169.2011.547165. [DOI] [PubMed] [Google Scholar]
44.Islam M.S., Paul A., Talukder M., Roy K., Sobur M.A., Ievy S., Nayeem M.M.H., Rahman S., Nazir K.N.H., Hossain M.T. Migratory birds travelling to Bangladesh are potential carriers of multi-drug resistant enterococcus spp., salmonella spp., and vibrio spp. Saudi J Biol Sci. 2021;28(10):5963–5970. doi: 10.1016/j.sjbs.2021.06.053. [DOI] [PMC free article] [PubMed] [Google Scholar]
45.Roy K., Islam M.S., Paul A., Ievy S., Talukder M., Sobur M.A., Ballah F.M., Khan M.S.R., Rahman M.T. Molecular detection and antibiotyping of multi‐drug resistant Enterococcus faecium from healthy broiler chickens in Bangladesh. Vet Med Sci. 2022;8(1):200–210. doi: 10.1002/vms3.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
46.Tawyabur M., Islam M.S., Sobur M.A., Hossain M.J., Mahmud M.M., Paul S., Hossain M.T., Ashour H.M., Rahman M.T. Isolation and characterization of multidrug-resistant Escherichia coli and salmonella spp. from healthy and diseased turkeys. Antibiotics. 2020;9(11):770. doi: 10.3390/antibiotics9110770. [DOI] [PMC free article] [PubMed] [Google Scholar]
47.Talukder M., Islam M.S., Ievy S., Sobur M.A., Ballah F.M., Najibullah M., Rahman M.B., Rahman M.T., Khan M.F.R. Detection of multidrug resistant salmonella spp. from healthy and diseased broilers having potential public health significance. J Adv Biotechnol Exp Ther. 2021;4(2):248–255. [Google Scholar]
48.Nitz J., Wente N., Zhang Y., Klocke D., Tho Seeth M., Krömker V. Dry period or early lactation—time of onset and associated risk factors for intramammary infections in dairy cows. Pathogens. 2021;10(2):224. doi: 10.3390/pathogens10020224. [DOI] [PMC free article] [PubMed] [Google Scholar]
49.Rajkovic A., Jovanovic J., Monteiro S., Decleer M., Andjelkovic M., Foubert A., Beloglazova N., Tsilla V., Sas B., Madder A. Detection of toxins involved in foodborne diseases caused by gram‐positive bacteria. Compr Rev Food Sci Food Saf. 2020;19(4):1605–1657. doi: 10.1111/1541-4337.12571. [DOI] [PubMed] [Google Scholar]
50.Kerro Dego O., Tareke F. Bovine mastitis in selected areas of southern Ethiopia. Trop Anim Health Prod. 2003;35(3):197–205. doi: 10.1023/a:1023352811751. [DOI] [PubMed] [Google Scholar]
51.Kadariya J., Smith T.C., Thapaliya D. Staphylococcus aureus and staphylococcal food‐borne disease: an ongoing challenge in public health. BioMed Res Int. 2014;2014(1) doi: 10.1155/2014/827965. [DOI] [PMC free article] [PubMed] [Google Scholar]
52.Abunna F., Abriham T., Gizaw F., Beyene T., Feyisa A., Ayana D., Mamo B., Duguma R. Staphylococcus: isolation, identification and antimicrobial resistance in dairy cattle farms, municipal abattoir and personnel in and around asella, Ethiopia. J Vet Sci Technol. 2016;7(383):2. [Google Scholar]
53.Badawy B., Elafify M., Farag A.M., Moustafa S.M., Sayed-Ahmed M.Z., Moawad A.A., Algammal A.M., Ramadan H., Eltholth M. Ecological distribution of virulent multidrug-resistant Staphylococcus aureus in livestock, environment, and dairy products. Antibiotics. 2022;11(11):1651. doi: 10.3390/antibiotics11111651. [DOI] [PMC free article] [PubMed] [Google Scholar]
54.Suleiman A.S., Abbass M., Hossain M., Choudhary P., Bhattacharya P., Islam M.A. Impact of antibiotic-coated sutures on surgical site infections: a second-order meta-analysis. Int J Surg. 2024;110(1):507–519. doi: 10.1097/JS9.0000000000000822. [DOI] [PMC free article] [PubMed] [Google Scholar]
55.Fenta M.D., Tafere F.A., Mebratu A.S., Malede B.A. Quarter-wise proportion and beta-lactam resistance rate of bovine mastitis associated-staphylococcus aureus among infectious episodes in Ethiopia: systematic review and meta-analysis. Heliyon. 2023;9(7) doi: 10.1016/j.heliyon.2023.e18180. [DOI] [PMC free article] [PubMed] [Google Scholar]
56.Nikolic P., Mudgil P. The cell wall, cell membrane and virulence factors of Staphylococcus aureus and their role in antibiotic resistance. Microorganisms. 2023;11(2):259. doi: 10.3390/microorganisms11020259. [DOI] [PMC free article] [PubMed] [Google Scholar]
57.Page M.J., McKenzie J.E., Bossuyt P.M., Boutron I., Hoffmann T.C., Mulrow C.D., Shamseer L., Tetzlaff J.M., Akl E.A., Brennan S.E., Chou R., Glanville J., Grimshaw J.M., Hróbjartsson A., Lalu M.M., Li T., Loder E.W., Mayo-Wilson E., McDonald S., McGuinness L.A., Stewart L.A., Thomas J., Tricco A.C., Welch V.A., Whiting P., Moher D. The prisma 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71. [DOI] [PMC free article] [PubMed] [Google Scholar]
58.Grammatopoulos T., Hunter J.W., Munn Z., Stone J.C., Barker T.H. Reporting quality and risk of bias in jbi systematic reviews evaluating the effectiveness of interventions: a methodological review protocol. JBI Evid Synth. 2023;21(3):584–591. doi: 10.11124/JBIES-22-00317. [DOI] [PubMed] [Google Scholar]
59.DerSimonian R., Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188. doi: 10.1016/0197-2456(86)90046-2. [DOI] [PubMed] [Google Scholar]
60.Ahmed M.J., Hossain M.I., Bhuiyan M.I.H., Rahman M.A., Kaderi I.J., Nirob A.I., Rahi M.A.I., Mamun M., Alam K.E., Chowdhury M.J., Bhandari P., Chalise R., Alam M.J., Chowdhury M.T.I., Ali M., Hossain D. Antimicrobial resistance in meat and meat products from Asia: an urgent one health challenge- a systematic review and meta-analysis. Poult Sci. 2025;104(11) doi: 10.1016/j.psj.2025.105811. [DOI] [PMC free article] [PubMed] [Google Scholar]
61.Higgins J.P., Thompson S.G. Quantifying heterogeneity in a meta‐analysis. Stat Med. 2002;21(11):1539–1558. doi: 10.1002/sim.1186. [DOI] [PubMed] [Google Scholar]
62.Ahmed M.J., Hossain M.I., Hossain D. Emerging pathogen alert: global epidemiology of the zoonotic potential of escherichia albertii: a systematic review and meta-analysis. Int J Food Microbiol. 2026;447 doi: 10.1016/j.ijfoodmicro.2025.111564. [DOI] [PubMed] [Google Scholar]
63.Alkharusi H. Categorical variables in regression analysis: a comparison of dummy and effect coding. Int J Educ. 2012;4(2):202. [Google Scholar]
64.Egger M., Smith G.D. Meta-analysis bias in location and selection of studies. BMJ. 1998;316(7124):61–66. doi: 10.1136/bmj.316.7124.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
65.Duval S., Tweedie R. Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–463. doi: 10.1111/j.0006-341x.2000.00455.x. [DOI] [PubMed] [Google Scholar]
66.Wickham H. Ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3(2):180–185. [Google Scholar]
67.Akkou M., Antri K., Bachtarzi M.-A., Bes M., Tristan A., Dauwalder O., Kaidi R., Meugnier H., Tazir M., Etienne J. Phenotypic and genotypic characterization of Staphylococcus aureus strains associated with bovine mastitis and nasal carriage of workers in contact to animals in Algeria. Pak Vet J. 2016;36(2):184–188. [Google Scholar]
68.Akkou M., Titouche Y., Bentayeb L., Bes M., Laurent F., Ramdani-Bouguessa N. Risk factors for dairy cows mastitis in Algeria, antibiotic resistance and molecular typing of the causative Staphylococcus aureus. Vet Res Commun. 2024;48(5):3007–3018. doi: 10.1007/s11259-024-10457-2. [DOI] [PubMed] [Google Scholar]
69.Benhamed N., Moulay M., Aggad H., Henni J., Kihal M. Prevalence of mastitis infection and identification of causing bacteria in cattle in the Oran region west Algeria. J Anim Vet Adv. 2011;10(22):3002–3005. [Google Scholar]
70.Crespi E., Pereyra A.M., Puigdevall T., Rumi M.V., Testorelli M.F., Caggiano N., Gulone L., Mollerach M., Gentilini E.R., Srednik M.E. Antimicrobial resistance studies in staphylococci and streptococci isolated from cows with mastitis in Argentina. J Vet Sci. 2021;23(6):e12. doi: 10.4142/jvs.21062. [DOI] [PMC free article] [PubMed] [Google Scholar]
71.Al-Harbi H., Ranjbar S., Moore R.J., Alawneh J.I. Bacteria isolated from milk of dairy cows with and without clinical mastitis in different regions of Australia and their amr profiles. Front Vet Sci. 2021;8 doi: 10.3389/fvets.2021.743725. [DOI] [PMC free article] [PubMed] [Google Scholar]
72.Al Emon A., Hossain H., Chowdhury M.S.R., Rahman M.A., Tanni F.Y., Asha M.N., Akter H., Hossain M.M., Islam M.R., Rahman M.M. Prevalence, antimicrobial susceptibility profiles and resistant gene identification of bovine subclinical mastitis pathogens in Bangladesh. Heliyon. 2024;10(14) doi: 10.1016/j.heliyon.2024.e34567. [DOI] [PMC free article] [PubMed] [Google Scholar]
73.Fazal M.A., Rana E.A., Akter S., Alim M.A., Barua H., Ahad A. Molecular identification, antimicrobial resistance and virulence gene profiling of staphylococcus spp. associated with bovine sub-clinical mastitis in Bangladesh. Vet Anim Sci. 2023;21 doi: 10.1016/j.vas.2023.100297. [DOI] [PMC free article] [PubMed] [Google Scholar]
74.Hoque M., Das Z., Rahman A., Haider M., Islam M. Molecular characterization of Staphylococcus aureus strains in bovine mastitis milk in Bangladesh. Int J Vet Sci Med. 2018;6(1):53–60. doi: 10.1016/j.ijvsm.2018.03.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
75.Islam M.M., Hossain M.I., Islam M.S., Azam M.G., Sultana S. Prevalence, antibiotic resistance patterns, and virulence factors of Staphylococcus aureus isolates associated with bovine mastitis in northern Bangladesh. Heliyon. 2025;11(3) doi: 10.1016/j.heliyon.2025.e42107. [DOI] [PMC free article] [PubMed] [Google Scholar]
76.Rana E.A., Fazal M.A., Alim M.A. Frequently used therapeutic antimicrobials and their resistance patterns on Staphylococcus aureus and Escherichia coli in mastitis affected lactating cows. Int J Vet Sci Med. 2022;10(1):1–10. doi: 10.1080/23144599.2022.2038494. [DOI] [PMC free article] [PubMed] [Google Scholar]
77.Singha S., Koop G., Persson Y., Hossain D., Scanlon L., Derks M., Hoque M.A., Rahman M.M. Incidence, etiology, and risk factors of clinical mastitis in dairy cows under semi-tropical circumstances in Chattogram, Bangladesh. Animals. 2021;11(8):2255. doi: 10.3390/ani11082255. [DOI] [PMC free article] [PubMed] [Google Scholar]
78.Castelani L., Santos A.F.S., Miranda M.d.S., Zafalon L.F., Pozzi C.R., Arcaro J.R.P. Molecular typing of mastitis-causing Staphylococcus aureus isolated from heifers and cows. Int J Mol Sci. 2013;14(2):4326–4333. doi: 10.3390/ijms14024326. [DOI] [PMC free article] [PubMed] [Google Scholar]
79.Costa F., Belo N., Costa E., Andrade G., Pereira L., Carvalho I., Santos R. Frequency of enterotoxins, toxic shock syndrome toxin-1, and biofilm formation genes in Staphylococcus aureus isolates from cows with mastitis in the northeast of Brazil. Trop Anim Health Prod. 2018;50(5):1089–1097. doi: 10.1007/s11250-018-1534-6. [DOI] [PubMed] [Google Scholar]
80.Dorneles E.M., Fonseca M.D., Abreu J.A., Lage A.P., Brito M.A., Pereira C.R., Brandão H.M., Guimarães A.S., Heinemann M.B. Genetic diversity and antimicrobial resistance in Staphylococcus aureus and coagulase‐negative staphylococcus isolates from bovine mastitis in minas gerais, Brazil. Microbiologyopen. 2019;8(5) doi: 10.1002/mbo3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
81.Gonçalves M.S., Dorneles E.M.S., Heinemann M.B., Brito M.A.V.P.e., Guimarães A.d.S. Genetic diversity and antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in minas gerais, Brazil. Ciência Rural. 2022;53(3) [Google Scholar]
82.Guimarães F., Manzi M., Joaquim S., Richini-Pereira V., Langoni H. Outbreak of methicillin-resistant Staphylococcus aureus (mrsa)-associated mastitis in a closed dairy herd. J Dairy Sci. 2017;100(1):726–730. doi: 10.3168/jds.2016-11700. [DOI] [PubMed] [Google Scholar]
83.Kroning I.S., Iglesias M.A., Mendonça K.S., Lopes G.V., Silva W.P. Presence of classical enterotoxin genes, agr typing, antimicrobial resistance, and genetic diversity of Staphylococcus aureus from milk of cows with mastitis in southern Brazil. J Food Protect. 2018;81(5):738–742. doi: 10.4315/0362-028X.JFP-17-436. [DOI] [PubMed] [Google Scholar]
84.Marques V.F., da Motta C.C., da Silva Soares B., de Melo D.A., de Oliveira Coelho S.d.M., da Silva Coelho I., Barbosa H.S., de Souza M.M.S. Biofilm production and beta-lactamic resistance in Brazilian Staphylococcus aureus isolates from bovine mastitis. Braz J Microbiol. 2017;48(1):118–124. doi: 10.1016/j.bjm.2016.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
85.Rall V., Miranda E., Castilho I., Camargo C., Langoni H., Guimarães F., Júnior J.A., Júnior A.F. Diversity of staphylococcus species and prevalence of enterotoxin genes isolated from milk of healthy cows and cows with subclinical mastitis. J Dairy Sci. 2014;97(2):829–837. doi: 10.3168/jds.2013-7226. [DOI] [PubMed] [Google Scholar]
86.Rossi B., Bonsaglia E., Castilho I., Dantas S., Salina A., Langoni H., Pantoja J., Budri P., Fitzgerald-Hughes D., Júnior A.F. Genotyping of long term persistent Staphylococcus aureus in bovine subclinical mastitis. Microb Pathog. 2019;132:45–50. doi: 10.1016/j.micpath.2019.04.031. [DOI] [PubMed] [Google Scholar]
87.Silva A.T.F., Gonçalves J.L., Dantas S.T.A., Rall V.L.M., de Oliveira P.R.F., Dos Santos M.V., Peixoto R.d.M., Mota R.A. Genetic and phenotypic characterization of subclinical mastitis-causing multidrug-resistant Staphylococcus aureus. Antibiotics. 2023;12(9):1353. doi: 10.3390/antibiotics12091353. [DOI] [PMC free article] [PubMed] [Google Scholar]
88.Rodríguez M.F., Gomez A.P., Ceballos-Garzon A. Antimicrobial resistance profiles of staphylococcus isolated from cows with subclinical mastitis: do strains from the environment and from humans contribute to the dissemination of resistance among bacteria on dairy farms in Colombia? Antibiotics. 2023;12(11):1574. doi: 10.3390/antibiotics12111574. [DOI] [PMC free article] [PubMed] [Google Scholar]
89.Esemu S.N., Nya’Nying S.F., Ndip L.M., Bessong P.O., Tanih N.F., Smith S.I., Ndip R.N. Isolation and characterization of methicillin-resistant Staphylococcus aureus from bovine mastitis in north west Cameroon: public health implications. BMC Res Notes. 2024;17(1):389. doi: 10.1186/s13104-024-07073-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
90.Bao H., Zhang H., Zhou Y., Zhang L., Wang R. Prevalence, enterotoxin gene and antimicrobial resistance of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from clinical healthy dairy cows. SEa. 2004;55(310) [Google Scholar]
91.Chen C., Sun C., Li J., Ji X., Wang Y., Song C., Wang G. Characterisation of Staphylococcus aureus isolates from bovine mastitis in Ningxia, Western China. J Glob Antimicrob Resist. 2021;25:232–237. doi: 10.1016/j.jgar.2021.03.021. [DOI] [PubMed] [Google Scholar]
92.Gao J., Barkema H.W., Zhang L., Liu G., Deng Z., Cai L., Shan R., Zhang S., Zou J., Kastelic J.P. Incidence of clinical mastitis and distribution of pathogens on large Chinese dairy farms. J Dairy Sci. 2017;100(6):4797–4806. doi: 10.3168/jds.2016-12334. [DOI] [PubMed] [Google Scholar]
93.Li L., Feng W., Zhang Z., Xue H., Zhao X. Macrolide-lincosamide-streptogramin resistance phenotypes and genotypes of coagulase-positive Staphylococcus aureus and coagulase-negative staphylococcal isolates from bovine mastitis. BMC Vet Res. 2015;11(1):168. doi: 10.1186/s12917-015-0492-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
94.Li L., Zhao X. Characterization of the resistance class 1 integrons in Staphylococcus aureus isolates from milk of lactating dairy cattle in northwestern China. BMC Vet Res. 2018;14(1):59. doi: 10.1186/s12917-018-1376-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
95.Liu J., Wang X., Bi C., Mehmood K., Ali F., Qin J., Han Z. Molecular characterization of multi-drug-resistant Staphylococcus aureus in mastitis bovine milk from a dairy farm in Anhui, China. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.966533. [DOI] [PMC free article] [PubMed] [Google Scholar]
96.Liu K., Tao L., Li J., Fang L., Cui L., Li J., Meng X., Zhu G., Bi C., Wang H. Characterization of Staphylococcus aureus isolates from cases of clinical bovine mastitis on large-scale Chinese dairy farms. Front Vet Sci. 2020;7 doi: 10.3389/fvets.2020.580129. [DOI] [PMC free article] [PubMed] [Google Scholar]
97.Qu Y., Zhao H., Nobrega D.B., Cobo E.R., Han B., Zhao Z., Li S., Li M., Barkema H.W., Gao J. Molecular epidemiology and distribution of antimicrobial resistance genes of staphylococcus species isolated from Chinese dairy cows with clinical mastitis. J Dairy Sci. 2019;102(2):1571–1583. doi: 10.3168/jds.2018-15136. [DOI] [PubMed] [Google Scholar]
98.Ren Q., Liao G., Wu Z., Lv J., Chen W. Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang, China. J Dairy Sci. 2020;103(4):3368–3380. doi: 10.3168/jds.2019-17420. [DOI] [PubMed] [Google Scholar]
99.Shi D., Hao Y., Zhang A., Wulan B., Fan X. Antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis in China. Transbound Emerg Dis. 2010;57(4):221–224. doi: 10.1111/j.1865-1682.2010.01139.x. [DOI] [PubMed] [Google Scholar]
100.Wang D., Zhang L., Zhou X., He Y., Yong C., Shen M., Szenci O., Han B. Antimicrobial susceptibility, virulence genes, and randomly amplified polymorphic DNA analysis of Staphylococcus aureus recovered from bovine mastitis in Ningxia, China. J Dairy Sci. 2016;99(12):9560–9569. doi: 10.3168/jds.2016-11625. [DOI] [PubMed] [Google Scholar]
101.Wang W., Lin X., Jiang T., Peng Z., Xu J., Yi L., Li F., Fanning S., Baloch Z. Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in beijing, China. Front Microbiol. 2018;9:1123. doi: 10.3389/fmicb.2018.01123. [DOI] [PMC free article] [PubMed] [Google Scholar]
102.Wang X., Wang X., Wang Y., Guo G., Usman T., Hao D., Tang X., Zhang Y., Yu Y. Antimicrobial resistance and toxin gene profiles of Staphylococcus aureus strains from holstein milk. Lett Appl Microbiol. 2014;58(6):527–534. doi: 10.1111/lam.12221. [DOI] [PubMed] [Google Scholar]
103.Yang F., Shi W., Meng N., Zhao Y., Ding X., Li Q. Antimicrobial resistance and virulence profiles of staphylococci isolated from clinical bovine mastitis. Front Microbiol. 2023;14 doi: 10.3389/fmicb.2023.1190790. [DOI] [PMC free article] [PubMed] [Google Scholar]
104.Zhang D.-X., Li Y., Yang X.-Q., Su H.-Y., Wang Q., Zhang Z.-H., Liu Y.-C., Tian C.-L., Cui C.-C., Liu M.-C. In vitro antibiotic susceptibility, virulence genes distribution and biofilm production of Staphylococcus aureus isolates from bovine mastitis in the Liaoning Province of China. Infect Drug Resist. 2020:1365–1375. doi: 10.2147/IDR.S247765. [DOI] [PMC free article] [PubMed] [Google Scholar]
105.Zhang L., Gao J., Barkema H.W., Ali T., Liu G., Deng Y., Naushad S., Kastelic J.P., Han B. Virulence gene profiles: alpha-hemolysin and clonal diversity in Staphylococcus aureus isolates from bovine clinical mastitis in China. BMC Vet Res. 2018;14(1):63. doi: 10.1186/s12917-018-1374-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
106.Zhang T., Luo Q., Chen Y., Li T., Wen G., Zhang R., Luo L., Lu Q., Ai D., Wang H. Molecular epidemiology, virulence determinants and antimicrobial resistance of campylobacter spreading in retail chicken meat in central China. Gut Pathog. 2016;8:1–9. doi: 10.1186/s13099-016-0132-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
107.Zhang Z., Chen Y., Li X., Wang X., Li H. Detection of antibiotic resistance, virulence gene, and drug resistance gene of Staphylococcus aureus isolates from bovine mastitis. Microbiol Spectr. 2022;10(4) doi: 10.1128/spectrum.00471-22. e00471-00422. [DOI] [PMC free article] [PubMed] [Google Scholar]
108.Vikova H., Babak V., Vrtkova I., Cervinkova D., Marosevic D., Moravkova M., Jaglic Z. Epidemiology of intramammary infections with Staphylococcus aureus and mastitis streptococci in a dairy cattle herd with a history of recurrent clinical mastitis. Pol J Vet Sci. 2017;20(1) doi: 10.1515/pjvs-2017-0017. [DOI] [PubMed] [Google Scholar]
109.Zigo F., Farkašová Z., Výrostková J., Regecova I., Ondrašovičová S., Vargová M., Sasáková N., Pecka-Kielb E., Bursová Š., Kiss D.S. Dairy cows’ udder pathogens and occurrence of virulence factors in staphylococci. Animals. 2022;12(4):470. doi: 10.3390/ani12040470. [DOI] [PMC free article] [PubMed] [Google Scholar]
110.Abd El-Razik K.A., Arafa A.A., Fouad E.A., Soror A.H., Abdalhamed A.M., Elgioushy M. Phenotypic and genotypic characterization of erythromycin-resistant Staphylococcus aureus isolated from bovine subclinical mastitis in Egypt. Vet World. 2023;16(7):1562. doi: 10.14202/vetworld.2023.1562-1571. [DOI] [PMC free article] [PubMed] [Google Scholar]
111.Abd El-Razik K.A., Soliman Y.A., Fouad E.A., Arafa A.A., Syame S.M., Soror A.H. Macrolides-resistant Staphylococcus aureus associated with clinical mastitis in cattle and buffalo in Egypt. J Adv Vet Res. 2023;13(3):461–468. [Google Scholar]
112.Algammal A.M., Enany M.E., El-Tarabili R.M., Ghobashy M.O., Helmy Y.A. Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of mrsa isolated from subclinical bovine mastitis in Egypt. Pathogens. 2020;9(5):362. doi: 10.3390/pathogens9050362. [DOI] [PMC free article] [PubMed] [Google Scholar]
113.Ameen F., Reda S.A., El-Shatoury S.A., Riad E.M., Enany M.E., Alarfaj A.A. Prevalence of antibiotic resistant mastitis pathogens in dairy cows in Egypt and potential biological control agents produced from plant endophytic actinobacteria. Saudi J Biol Sci. 2019;26(7):1492–1498. doi: 10.1016/j.sjbs.2019.09.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
114.Asfour H.A., Darwish S.F. 2011. Phenotypic and genotypic detection of both meca-and blaz-genes mediated β-lactam resistance in staphylococcus strains isolated from bovine mastitis. [Google Scholar]
115.Eidaroos N.H., Algammal A.M., Mohamaden W.I., Alenzi A.M., Alghamdi S., Kabrah A., El-Mahallawy H.S., Eid H.M., Algwad A.A., Asfor S.A. Virulence traits, agr typing, multidrug resistance patterns, and biofilm ability of mdr Staphylococcus aureus recovered from clinical and subclinical mastitis in dairy cows. BMC Microbiol. 2025;25(1):155. doi: 10.1186/s12866-025-03870-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
116.El-shenawy F., Ahmed H.A., El-Shemy M.M., Talayea A. Genotyping of methicillin-resistant Staphylococcus aureus (mrsa) isolated from bovine mastitis. Egypt J Vet Sci. 2025;56(8):1919–1930. [Google Scholar]
117.Elhaig M.M., Selim A. Molecular and bacteriological investigation of subclinical mastitis caused by Staphylococcus aureus and Streptococcus agalactiae in domestic bovids from Ismailia, Egypt. Trop Anim Health Prod. 2015;47(2):271–276. doi: 10.1007/s11250-014-0715-1. [DOI] [PubMed] [Google Scholar]
118.Ewida R.M., Al-Hosary A.A. Prevalence of enterotoxins and other virulence genes of Staphylococcus aureus caused subclinical mastitis in dairy cows. Vet World. 2020;13(6):1193. doi: 10.14202/vetworld.2020.1193-1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
119.Gad W.A., Osman S.A., Abd El K.A.E.-H., Soror A.H., Soliman Y.A., Fouad E.A. In prevalence and molecular characterization of resistant Staphylococcus aureus strains in bulk milk tanks of dairy cattle in northern Egypt. Vet Res Forum. 2025:317. doi: 10.30466/vrf.2024.2038109.4398. [DOI] [PMC free article] [PubMed] [Google Scholar]
120.Ibrahim E.S., Arafa A.A., Dorgam S.M., Eid R.H., Atta N.S., El-Dabae W.H., Sadek E.G. Molecular characterization of genes responsible for biofilm formation in Staphylococcus aureus isolated from mastitic cows. Vet World. 2022;15(1):205. doi: 10.14202/vetworld.2022.205-212. [DOI] [PMC free article] [PubMed] [Google Scholar]
121.Mostafa Abdalhamed A., Zeedan G.S.G., Ahmed Arafa A., Shafeek Ibrahim E., Sedky D., Abdel nabey Hafez A. Detection of methicillin‐resistant Staphylococcus aureus in clinical and subclinical mastitis in ruminants and studying the effect of novel green synthetized nanoparticles as one of the alternative treatments. Vet Med Int. 2022;2022(1) doi: 10.1155/2022/6309984. [DOI] [PMC free article] [PubMed] [Google Scholar]
122.Selim A., Kelis K., AlKahtani M.D., Albohairy F.M., Attia K.A. Prevalence, antimicrobial susceptibilities and risk factors of methicillin resistant Staphylococcus aureus (mrsa) in dairy bovines. BMC Vet Res. 2022;18(1):293. doi: 10.1186/s12917-022-03389-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
123.Tartor Y.H., Enany M.E., Ismail N.I., El-Demerdash A.S., Eidaroos N.H., Algendy R.M., Mahmmod Y., Elsohaby I. Vancomycin-resistant Staphylococcus aureus endangers Egyptian dairy herds. Sci Rep. 2024;14(1) doi: 10.1038/s41598-024-81516-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
124.Younis G., Sadat A., Maghawry M. Characterization of coa gene and antimicrobial profiles of Staphylococcus aureus isolated from bovine clinical and subclinical mastitis. Adv Anim Vet Sci. 2018;6(4):161–168. [Google Scholar]
125.Abebe R., Hatiya H., Abera M., Megersa B., Asmare K. Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at hawassa milk shed, south Ethiopia. BMC Vet Res. 2016;12(1):270. doi: 10.1186/s12917-016-0905-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
126.Abunna F., Fufa G., Megersa B., Regassa A. Bovine mastitis: prevalence, risk factors and bacterial isolation in small-holder dairy farms in addis ababa city, Ethiopia. Glob Vet. 2013;10(6):647–652. [Google Scholar]
127.Bihon A., Syoum A., Assefa A. Assessment of risk factors and isolation of Staphylococcus aureus and Escherichia coli from bovine subclinical mastitic milk in and around gondar, northwest Ethiopia. Trop Anim Health Prod. 2019;51(4):939–948. doi: 10.1007/s11250-018-1777-2. [DOI] [PubMed] [Google Scholar]
128.Chawicha T.G., Yunus H.A., Soma M. Antimicrobial susceptibility of major bacterial pathogens isolated from bovine mastitis in bench maji zone, southwest Ethiopia. Multidiscip Sci J. 2021;3(2) 2021010-2021010. [Google Scholar]
129.Dabele D.T., Borena B.M., Admasu P., Gebremedhin E.Z., Marami L.M. Prevalence and risk factors of mastitis and isolation, identification and antibiogram of staphylococcus species from mastitis positive zebu cows in toke kutaye, cheliya, and dendi districts, west shewa zone, Oromia, Ethiopia. Infect Drug Resist. 2021:987–998. doi: 10.2147/IDR.S295257. [DOI] [PMC free article] [PubMed] [Google Scholar]
130.Demil E., Teshome L., Kerie Y., Habtamu A., Kumilachew W., Andualem T., Mekonnen S.A. Prevalence of subclinical mastitis, associated risk factors and antimicrobial susceptibility of the pathogens isolated from milk samples of dairy cows in northwest Ethiopia. Prev Vet Med. 2022;205 doi: 10.1016/j.prevetmed.2022.105680. [DOI] [PubMed] [Google Scholar]
131.Getahun D.D., Tarekegn H.T., Azene B.T., Abebe L.T., Belete M.A., Tessema T.S. Virulence genes and antibiotic resistance profiling of staphylococcus species isolated from mastitic dairy cows in and around bahir dar, Ethiopia. BMC Microbiol. 2025;25(1):210. doi: 10.1186/s12866-025-03886-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
132.Grima L.Y.W., Leliso S.A., Bulto A.O., Ashenafi D. Isolation, identification, and antimicrobial susceptibility profiles of Staphylococcus aureus from clinical mastitis in sebeta town dairy farms. Vet Med Int. 2021;2021(1) doi: 10.1155/2021/1772658. [DOI] [PMC free article] [PubMed] [Google Scholar]
133.Haftu R., Taddele H., Gugsa G., Kalayou S. Prevalence, bacterial causes, and antimicrobial susceptibility profile of mastitis isolates from cows in large-scale dairy farms of northern Ethiopia. Trop Anim Health Prod. 2012;44(7):1765–1771. doi: 10.1007/s11250-012-0135-z. [DOI] [PubMed] [Google Scholar]
134.Seyoum B., Kefyalew H., Abera B., Abdela N. Prevalence, risk factors and antimicrobial susceptibility test of Staphylococcus aureus in bovine cross breed mastitic milk in and around asella town, Oromia regional state, southern Ethiopia. Acta Trop. 2018;177:32–36. doi: 10.1016/j.actatropica.2017.09.012. [DOI] [PubMed] [Google Scholar]
135.Shille M., Dulo F., Abera S., Ayechew S. Isolation, identification, and antibiogram characteristics of Staphylococcus aureus from dairy cows kept under extensive management system, in the uba debretsehay district of southern Ethiopia. Vet Med Sci. 2025;11(4) doi: 10.1002/vms3.70503. [DOI] [PMC free article] [PubMed] [Google Scholar]
136.Tariku Sori T.S., Jemal Hussien J.H., Molalegne Bitew M.B. 2011. Prevalence and susceptibility assay of Staphylococcus aureus isolated from bovine mastitis in dairy farms of jimma town, south west Ethiopia. [Google Scholar]
137.Wodaje A., Belete M.A., Menkir A.S., Zegeye Z.B., Yihunie F.B. Detection of virulence genes and antimicrobial susceptibility profiles of Staphylococcus aureus isolates from bovine mastitis in chagni, northwestern Ethiopia. Vet Med Int. 2025;2025(1) doi: 10.1155/vmi/6473601. [DOI] [PMC free article] [PubMed] [Google Scholar]
138.Yimana M., Tesfaye J. Isolation, identification and antimicrobial profile of methicillin‐resistant Staphylococcus aureus from bovine mastitis in and around adama, central Ethiopia. Vet Med Sci. 2022;8(6):2576–2584. doi: 10.1002/vms3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]
139.Kadlec K., Entorf M., Peters T. Occurrence and characteristics of livestock-associated methicillin-resistant Staphylococcus aureus in quarter milk samples from dairy cows in Germany. Front Microbiol. 2019;10:1295. doi: 10.3389/fmicb.2019.01295. [DOI] [PMC free article] [PubMed] [Google Scholar]
140.Ruban W., Raveendra Hegde R.H., Kumar G. Methicillin resistance pattern of Staphylococcus aureus from mastitis milk in correlation to its possession of methicillin resistance gene k. Nithin prabhu. 2012 [Google Scholar]
141.Harini H., Sumathi B. Screening of bovine milk samples for sub-clinical mastitis and antibiogram of bacterial isolates. Vet World. 2011;4(8):358. [Google Scholar]
142.Mistry H., Sharma P., Mahato S., Saravanan R., Kumar P.A., Bhandari V. Prevalence and characterization of oxacillin susceptible meca-positive clinical isolates of Staphylococcus aureus causing bovine mastitis in India. PLoS One. 2016;11(9) doi: 10.1371/journal.pone.0162256. [DOI] [PMC free article] [PubMed] [Google Scholar]
143.Mitra S., Velu D., Bhuvana M., Krithiga N., Banerjee A., Shome R., Rahman H., Ghosh S., Shome B. Staphylococcus aureus spa type t267, clonal ancestor of bovine subclinical mastitis in India. J Appl Microbiol. 2013;114(6):1604–1615. doi: 10.1111/jam.12186. [DOI] [PubMed] [Google Scholar]
144.Mubarack H.M., Doss A., Vijayasanthi M., Venkataswamy R. Antimicrobial drug susceptibility of Staphylococcus aureus from subclinical bovine mastitis in coimbatore, Tamilnadu, South India. Vet World. 2012;5(6):352. [Google Scholar]
145.Mushtaq M., Agrawal R., Bhat M.A., Singh R., Pande N. Antibiotic resistance gene typing in Staphylococcus aureus isolated from bovine mastitis. Indian J Anim Sci. 2019;89:1188–1191. [Google Scholar]
146.Neelam, Jain V., Singh M., Joshi V.G., Chhabra R., Singh K., Rana Y. Virulence and antimicrobial resistance gene profiles of Staphylococcus aureus associated with clinical mastitis in cattle. PLoS One. 2022;17(5) doi: 10.1371/journal.pone.0264762. [DOI] [PMC free article] [PubMed] [Google Scholar]
147.Ramasamy T., Keerthana S., Srinivasan M., Chandrasekar D., Porteen K., Borthakur A., Elamaran A., Sriram P. Molecular characterization of antibiotic resistance gene pattern of Staphylococcus aureus and Escherichia coli in mastitis affected dairy cows. Indian J Anim Res. 2021;55(4):463–468. [Google Scholar]
148.Roshan M., Arora D., Behera M., Vats A., Gautam D., Deb R., Parkunan T., De S. Virulence and enterotoxin gene profile of methicillin-resistant staphylococcus aureus isolates from bovine mastitis. Comp Immunol Microbiol Infect Dis. 2022;80 doi: 10.1016/j.cimid.2021.101724. [DOI] [PubMed] [Google Scholar]
149.Sentitula B. Yadav, Kumar R. Incidence of staphylococci and streptococci during winter in mastitic milk of sahiwal cow and murrah buffaloes. Indian J Microbiol. 2012;52(2):153–159. doi: 10.1007/s12088-011-0207-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
150.Shah M.S., Qureshi S., Kashoo Z., Farooq S., Wani S.A., Hussain M.I., Banday M., Khan A.A., Gull B., Habib A. Methicillin resistance genes and in vitro biofilm formation among staphylococcus aureus isolates from bovine mastitis in India. Comp Immunol Microbiol Infect Dis. 2019;64:117–124. doi: 10.1016/j.cimid.2019.02.009. [DOI] [PubMed] [Google Scholar]
151.Singh A., Batabyal S., Bandyopadhyay S., Maity A., Polley S., Banerjee D., Chattopadhyay S. Molecular chara cterization of methicillin-resistant staphylococcus aureus (mrsa) isolated from bovine mastitis in and around kolkata, India. Explor Anim Med Res. 2019;9(1) [Google Scholar]
152.Singh R., Kumar R., Yadav B. Distribution of pathogenic factors in staphylococcus aureus strains isolated from intra-mammary infections in cattle and buffaloes. Indian J Biotechnol. 2011;10(4):410–416. [Google Scholar]
153.Qolbaini E.N., Khoeri M.M., Salsabila K., Paramaiswari W.T., Tafroji W., Artika I.M., Safari D. Identification and antimicrobial susceptibility of methicillin-resistant staphylococcus aureus-associated subclinical mastitis isolated from dairy cows in bogor, Indonesia. Vet World. 2021;14(5):1180. doi: 10.14202/vetworld.2021.1180-1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
154.Bahraminia F., Emadi S.R., Emaneini M., Farzaneh N., Rad M., Khoramian B. In A high prevalence of tylosin resistance among staphylococcus aureus strains isolated from bovine mastitis. Vet Res Forum. 2017:121. [PMC free article] [PubMed] [Google Scholar]
155.Dastmalchi Saei H., Panahi M. Genotyping and antimicrobial resistance of staphylococcus aureus isolates from dairy ruminants: differences in the distribution of clonal types between cattle and small ruminants. Arch Microbiol. 2020;202(1):115–125. doi: 10.1007/s00203-019-01722-z. [DOI] [PubMed] [Google Scholar]
156.Havaei S.A., Assadbeigi B., Esfahani B.N., Hoseini N.S., Rezaei N., Havaei S.R. Detection of meca and enterotoxin genes in Staphylococcus aureus isolates associated with bovine mastitis and characterization of staphylococcal cassette chromosome mec (sccmec) in mrsa strains. Iran J Microbiol. 2015;7(3):161. [PMC free article] [PubMed] [Google Scholar]
157.Jamali H., Radmehr B., Ismail S. Prevalence and antibiotic resistance of Staphylococcus aureus isolated from bovine clinical mastitis. J Dairy Sci. 2014;97(4):2226–2230. doi: 10.3168/jds.2013-7509. [DOI] [PubMed] [Google Scholar]
158.Khazaie F., Ahmadi E. Bovine subclinical mastitis-associated methicillin-resistant Staphylococcus aureus, selective genotyping and antimicrobial susceptibility profile of the isolates in Kurdistan province of Iran. Iran J Microbiol. 2021;13(1):65. doi: 10.18502/ijm.v13i1.5494. [DOI] [PMC free article] [PubMed] [Google Scholar]
159.Khoramrooz S.S., Mansouri F., Marashifard M., Hosseini S.A.A.M., Chenarestane-Olia F.A., Ganavehei B., Gharibpour F., Shahbazi A., Mirzaii M., Darban-Sarokhalil D. Detection of biofilm related genes, classical enterotoxin genes and agr typing among Staphylococcus aureus isolated from bovine with subclinical mastitis in southwest of Iran. Microb Pathog. 2016;97:45–51. doi: 10.1016/j.micpath.2016.05.022. [DOI] [PubMed] [Google Scholar]
160.Mohsenzadeh M., Ghazvini K., Azimian A. In frequency of specific agr groups and antibiotic resistance in Staphylococcus aureus isolated from bovine mastitis in the northeast of Iran. Vet Res Forum. 2015:295. [PMC free article] [PubMed] [Google Scholar]
161.Pourtaghi H., Azizi A.G., Sodagari H. Antimicrobial resistance patterns of Staphylococcus aureus isolated from bovine subclinical mastitis in Alborz province, Iran. Bulg J Vet Med. 2016;19(2):169–174. [Google Scholar]
162.Saei H.D. Coa types and antimicrobial resistance profile of Staphylococcus aureus isolates from cases of bovine mastitis. Comp Clin Pathol. 2012;21(3):301–307. [Google Scholar]
163.Maisano A., Luini M., Gazzola A., Sala L., Vezzoli F., Bertocchi L., Lorenzi V., Cremonesi P., Castiglioni B., Bergagna S. Staphylococcus aureus adlb gene is associated with high prevalence of intramammary infection in dairy herds of northern Italy: a cross-sectional study. J Dairy Sci. 2023;106(5):3421–3435. doi: 10.3168/jds.2022-22496. [DOI] [PubMed] [Google Scholar]
164.Hata E. Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus new York/Japan clone. J Vet Diagn Invest. 2016;28(3):291–298. doi: 10.1177/1040638716643126. [DOI] [PubMed] [Google Scholar]
165.Alekish M., Al-Qudah K., Al-Saleh A. Prevalence of antimicrobial resistance among bacterial pathogens isolated from bovine mastitis in northern Jordan. Rev Med Vet. 2013;164(6):319–326. [Google Scholar]
166.Ismail Z.B. Molecular characteristics, antibiogram and prevalence of multi-drug resistant Staphylococcus aureus (mdrsa) isolated from milk obtained from culled dairy cows and from cows with acute clinical mastitis. Asian Pac J Trop Biomed. 2017;7(8):694–697. [Google Scholar]
167.Baymenov B.M., Bulashev A.K., Chuzhebayeva G.D., Aliyeva G.K., Beishova I.S., Kokanov S.K., Raketsky V.A. Phenotypic and genotypic resistance to antibiotics in Staphylococcus aureus strains isolated from cattle milk in northern Kazakhstan. Vet World. 2023;16(9):1815. doi: 10.14202/vetworld.2023.1815-1820. [DOI] [PMC free article] [PubMed] [Google Scholar]
168.Rychshanova R., Mendybayeva A., Miciński B., Mamiyev N., Shevchenko P., Bermukhametov Z., Orzechowski B., Miciński J. Antibiotic resistance and biofilm formation in Staphylococcus aureus isolated from dairy cows at the stage of subclinical mastitis in northern Kazakhstan. Arch Anim Breed. 2022;65(4):439–448. doi: 10.5194/aab-65-439-2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
169.Mbindyo C.M., Gitao G.C., Mulei C.M. Prevalence, etiology, and risk factors of mastitis in dairy cattle in Embu and Kajiado counties, Kenya. Vet Med Int. 2020;2020(1) doi: 10.1155/2020/8831172. [DOI] [PMC free article] [PubMed] [Google Scholar]
170.Mbindyo C.M., Gitao G.C., Plummer P.J., Kulohoma B.W., Mulei C.M., Bett R. Antimicrobial resistance profiles and genes of staphylococci isolated from mastitic cow’s milk in Kenya. Antibiotics. 2021;10(7):772. doi: 10.3390/antibiotics10070772. [DOI] [PMC free article] [PubMed] [Google Scholar]
171.Michira L., Kagira J., Maina N., Waititu K., Kiboi D., Ongera E., Ngotho M. Prevalence of subclinical mastitis, associated risk factors and antimicrobial susceptibility pattern of bacteria isolated from milk of dairy cattle in Kajiado central sub‐county, Kenya. Vet Med Sci. 2023;9(6):2885–2892. doi: 10.1002/vms3.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
172.Klimiene I., Ruzauskas M., Spakauskas V., Matusevicius A., Mockeliunas R., Pereckiene A., Butrimaite-Ambrozeviciene C., Virgailis M. Antimicrobial resistance patterns to beta-lactams of gram-positive cocci isolated from bovine mastitis in Lithuania. Pol J Vet Sci. 2011;14(3) doi: 10.2478/v10181-011-0069-9. [DOI] [PubMed] [Google Scholar]
173.Saeed S.I., Mat Yazid K.A., Hashimy H.A., Dzulkifli S.K., Nordin F., Nik Him N.A., Omar M.F.F.b., Aklilu E., Mohamad M., Zalati C.W.S. Prevalence, antimicrobial resistance, and characterization of Staphylococcus aureus isolated from subclinical bovine mastitis in east Coast Malaysia. Animals. 2022;12(13):1680. doi: 10.3390/ani12131680. [DOI] [PMC free article] [PubMed] [Google Scholar]
174.Aguirre-Sánchez J.R., Castro-del Campo N., Medrano-Félix J.A., Martínez-Torres A.O., Chaidez C., Querol-Audi J., Castro-del Campo N. Genomic insights of S. Aureus associated with bovine mastitis in a high livestock activity region of Mexico. J Vet Sci. 2024;25(4):e42. doi: 10.4142/jvs.23286. [DOI] [PMC free article] [PubMed] [Google Scholar]
175.Greening S.S., Zhang J., Midwinter A.C., Wilkinson D.A., McDougall S., Gates M.C., French N.P. The genetic relatedness and antimicrobial resistance patterns of mastitis-causing Staphylococcus aureus strains isolated from New Zealand dairy cattle. Vet Sci. 2021;8(11):287. doi: 10.3390/vetsci8110287. [DOI] [PMC free article] [PubMed] [Google Scholar]
176.Petrovski K., Laven R., Lopez-Villalobos N. A descriptive analysis of the antimicrobial susceptibility of mastitis-causing bacteria isolated from samples submitted to commercial diagnostic laboratories in New Zealand (2003–2006) N Z Vet J. 2011;59(2):59–66. doi: 10.1080/00480169.2011.552853. [DOI] [PubMed] [Google Scholar]
177.Antók F.I., Mayrhofer R., Marbach H., Masengesho J.C., Keinprecht H., Nyirimbuga V., Fischer O., Lepuschitz S., Ruppitsch W., Ehling-Schulz M. Characterization of antibiotic and biocide resistance genes and virulence factors of staphylococcus species associated with bovine mastitis in Rwanda. Antibiotics. 2019;9(1):1. doi: 10.3390/antibiotics9010001. [DOI] [PMC free article] [PubMed] [Google Scholar]
178.Garmo R.T., Waage S., Sviland S., Henriksen B.I., Østerås O., Reksen O. Reproductive performance, udder health, and antibiotic resistance in mastitis bacteria isolated from Norwegian red cows in conventional and organic farming. Acta Vet Scand. 2010;52(1):11. doi: 10.1186/1751-0147-52-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
179.Ahmed A., Ijaz M., Khan J.A., Anjum A.A. Molecular characterization and therapeutic insights into biofilm positive Staphylococcus aureus isolated from bovine subclinical mastitis. Pak Vet J. 2022;42(4) [Google Scholar]
180.Haq I.U., Kamal M., Swelum A.A., Khan S., Ríos-Escalante P.R.D.l., Usman T. Alarming multidrug resistance in Staphylococcus aureus isolated from raw milk of cows with subclinical mastitis: antibiotic resistance patterns and occurrence of selected resistance genes. PLoS One. 2024;19(5) doi: 10.1371/journal.pone.0301200. [DOI] [PMC free article] [PubMed] [Google Scholar]
181.Ijaz M., Ghumman N.Z., Javed M.U., Ahmed A., Rasheed H., Anwaar F., Sabir M.J., Muzammil I. Genotypic insights to panton–valentine leukocidin positive methicillin-resistant Staphylococcus aureus isolated from cattle mastitis. J Dairy Res. 2024;91(2):211–213. doi: 10.1017/S0022029924000244. [DOI] [PubMed] [Google Scholar]
182.Shah A.U., Ali Khan J., Avais M., Zaman S.H., Munir Z., Abbas S., Tariq M., Rahman M.u., Tariq F., Nawaz S. Prevalence and chemotherapy of Staphylococcus aureus mastitis in dairy cattle. PLoS One. 2025;20(2) doi: 10.1371/journal.pone.0315480. [DOI] [PMC free article] [PubMed] [Google Scholar]
183.Shahid M., Hussain R., Nawaz Z., Aslam B., Ahmad M.Z., Siddique A.B., Ahsan H., Fatima A., Khan I., Mustafa B. Occurrence of virulence genes among methicillin-resistant Staphylococcus aureus isolated from subclinical bovine mastitis. ACS Omega. 2023;8(41):38111–38117. doi: 10.1021/acsomega.3c04206. [DOI] [PMC free article] [PubMed] [Google Scholar]
184.Shahzad M.A., Yousaf A., Ahsan A., Irshad H., Riaz A., Khan A., Ullah I., Sattar S., Bostan N., Javed S. Virulence and resistance profiling of Staphylococcus aureus isolated from subclinical bovine mastitis in the Pakistani pothohar region. Sci Rep. 2024;14(1) doi: 10.1038/s41598-024-65448-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
185.Krukowski H., Bakuła Z., Iskra M., Olender A., Bis-Wencel H., Jagielski T. The first outbreak of methicillin-resistant Staphylococcus aureus in dairy cattle in Poland with evidence of on-farm and intrahousehold transmission. J Dairy Sci. 2020;103(11):10577–10584. doi: 10.3168/jds.2020-18291. [DOI] [PubMed] [Google Scholar]
186.Szweda P., Schielmann M., Frankowska A., Kot B., Zalewska M. Antibiotic resistance in Staphylococcus aureus strains isolated from cows with mastitis in eastern Poland and analysis of susceptibility of resistant strains to alternative nonantibiotic agents: lysostaphin, nisin and polymyxin b. J Vet Med Sci. 2014;76(3):355–362. doi: 10.1292/jvms.13-0177. [DOI] [PMC free article] [PubMed] [Google Scholar]
187.Alharbi A., Al-Dubaib M., Saeed E.M., Elbehiry A. 2021. Comparison of maldi-tof mass spectrometry with phenotypic methods for identification and characterization of Staphylococcus aureus causing mastitis. [DOI] [PubMed] [Google Scholar]
188.Bujňáková D., Karahutová L. Molecular characteristics and antibiotic resistance of Staphylococcus aureus and Staphylococcus haemolyticus isolated from bovine mastitis. Res Vet Sci. 2024;177 doi: 10.1016/j.rvsc.2024.105365. [DOI] [PubMed] [Google Scholar]
189.Kang H.J., You J.-Y., Hong S., Moon J.-S., Kim H.-Y., Choi J.-H., Kim J.-M., Lee Y.J., Kang H.-M. Prevalence of pathogens and antimicrobial resistance of isolated staphylococcus spp. in bovine mastitis milk in South Korea, 2018–2022. J Vet Med Sci. 2024;86(12):1219–1226. doi: 10.1292/jvms.24-0239. [DOI] [PMC free article] [PubMed] [Google Scholar]
190.Nam H.-M., Lee A.-L., Jung S.-C., Kim M.-N., Jang G.-C., Wee S.-H., Lim S.-K. Antimicrobial susceptibility of Staphylococcus aureus and characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitis in Korea. Foodborne Pathog Dise. 2011;8(2):231–238. doi: 10.1089/fpd.2010.0661. [DOI] [PubMed] [Google Scholar]
191.Song J.W., Yang S.J., Shin S., Seo K.S., Park Y.H., Park K.T. Genotypic and phenotypic characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitic milk in Korea. J Food Protect. 2016;79(10):1725–1732. doi: 10.4315/0362-028X.JFP-16-067. [DOI] [PubMed] [Google Scholar]
192.Ranasinghe R., Deshapriya R., Abeygunawardana D., Rahularaj R., Dematawewa C. Subclinical mastitis in dairy cows in major milk-producing areas of Sri Lanka: prevalence, associated risk factors, and effects on reproduction. J Dairy Sci. 2021;104(12):12900–12911. doi: 10.3168/jds.2021-20223. [DOI] [PubMed] [Google Scholar]
193.Duse A., Persson-Waller K., Pedersen K. Microbial aetiology, antibiotic susceptibility and pathogen-specific risk factors for udder pathogens from clinical mastitis in dairy cows. Animals. 2021;11(7):2113. doi: 10.3390/ani11072113. [DOI] [PMC free article] [PubMed] [Google Scholar]
194.Woudstra S., Wente N., Zhang Y., Leimbach S., Gussmann M., Kirkeby C., Krömker V. Strain diversity and infection durations of staphylococcus spp. and streptococcus spp. causing intramammary infections in dairy cows. J Dairy Sci. 2023;106(6):4214–4231. doi: 10.3168/jds.2022-22942. [DOI] [PubMed] [Google Scholar]
195.Chu C., Wei Y., Chuang S.-T., Yu C., Changchien C.-H., Su Y. Differences in virulence genes and genome patterns of mastitis-associated Staphylococcus aureus among goat, cow, and human isolates in Taiwan. Foodborne Pathog Dise. 2013;10(3):256–262. doi: 10.1089/fpd.2012.1278. [DOI] [PubMed] [Google Scholar]
196.Intrakamhaeng M., Komutarin T. Antibiotics resistance and rapd-pcr typing of multidrug resistant mrsa isolated from bovine mastitis cases in Thailand. Sci Asia. 2012;38:30–35. [Google Scholar]
197.Pumipuntu N., Tunyong W., Chantratita N., Diraphat P., Pumirat P., Sookrung N., Chaicumpa W., Indrawattana N. Staphylococcus spp. associated with subclinical bovine mastitis in central and northeast provinces of Thailand. PeerJ. 2019;7 doi: 10.7717/peerj.6587. [DOI] [PMC free article] [PubMed] [Google Scholar]
198.Aslantaş Ö., Demir C. Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. J Dairy Sci. 2016;99(11):8607–8613. doi: 10.3168/jds.2016-11310. [DOI] [PubMed] [Google Scholar]
199.Aslantas Ö., Öztürk F., Ceylan A. Prevalence and molecular mechanism of macrolide and lincosamide resistance in staphylococci isolated from subclinical bovine mastitis in Turkey. J Vet Med Sci. 2011;73(12):1645–1648. doi: 10.1292/jvms.11-0003. [DOI] [PubMed] [Google Scholar]
200.Cengiz S., Dinc G., Cengiz M. Evaluation of antimicrobial resistance in staphylococcus spp. isolated from subclinical mastitis in cows. Pak Vet J. 2015;35(3) [Google Scholar]
201.Hande G., Arzu F., Nilgün G., Serhat A.S., Alper Ç., Ece K., Serhat A., Murat F. Investigation on the etiology of subclinical mastitis in Jersey and hybrid Jersey dairy cows. Acta Vet. 2015;65(3) [Google Scholar]
202.Ikiz S., Başaran B., Bingol E.B., Cetin O., Kasikci G., Ozgur N.Y., Ucmak M., Yilmaz O., Gunduz M.C., Sabuncu A. Presence and antibiotic susceptibility patterns of contagious mastitis agents (Staphylococcus aureus and Streptococcus agalactiae) isolated from milks of dairy cows with subclinical mastitis. Turk J Vet Anim Sci. 2013;37(5):569–574. [Google Scholar]
203.Elias L., Balasubramanyam A.S., Ayshpur O.Y., Mushtuk I.U., Sheremet N.O., Gumeniuk V.V., Musser J.M., Rogovskyy A.S. Antimicrobial susceptibility of staphylococcus aureus, Streptococcus agalactiae, and Escherichia coli isolated from mastitic dairy cattle in Ukraine. Antibiotics. 2020;9(8):469. doi: 10.3390/antibiotics9080469. [DOI] [PMC free article] [PubMed] [Google Scholar]
204.De los Santos R., González-Revello Á., Majul L., Umpiérrez A., Aldrovandi A., Gil A., Hirigoyen D., Zunino P. Subclinical bovine mastitis associated with staphylococcus spp. in eleven Uruguayan dairy farms. J Infect Dev Ctries. 2022;16(4):630–637. doi: 10.3855/jidc.12960. [DOI] [PubMed] [Google Scholar]
205.Abdi R.D., Gillespie B.E., Ivey S., Pighetti G.M., Almeida R.A., Kerro Dego O. Antimicrobial resistance of major bacterial pathogens from dairy cows with high somatic cell count and clinical mastitis. Animals. 2021;11(1):131. doi: 10.3390/ani11010131. [DOI] [PMC free article] [PubMed] [Google Scholar]
206.Anderson K., Lyman R., Moury K., Ray D., Watson D., Correa M. Molecular epidemiology of Staphylococcus aureus mastitis in dairy heifers. J Dairy Sci. 2012;95(9):4921–4930. doi: 10.3168/jds.2011-4913. [DOI] [PubMed] [Google Scholar]
207.Sun W., Liu J., Li S., Zhu X., Wu X., Dou B., Pang X., Tian K., Wang P., Hao H. Antimicrobial resistance and molecular characteristics of bovine mastitis-associated methicillin-resistant staphylococcus aureus: potential for cross-species transmission of st59-mrsa. Microbiol Spectr. 2025 doi: 10.1128/spectrum.02800-24. e02800-02824. [DOI] [PMC free article] [PubMed] [Google Scholar]
208.Thomas A., Chothe S., Byukusenge M., Mathews T., Pierre T., Kariyawasam S., Luley E., Kuchipudi S., Jayarao B. Prevalence and distribution of multilocus sequence types of Staphylococcus aureus isolated from bulk tank milk and cows with mastitis in Pennsylvania. PLoS One. 2021;16(3) doi: 10.1371/journal.pone.0248528. [DOI] [PMC free article] [PubMed] [Google Scholar]
209.Son H.M., Duc H.M. Prevalence and phage-based biocontrol of methicillin-resistant Staphylococcus aureus isolated from raw milk of cows with subclinical mastitis in Vietnam. Antibiotics. 2024;13(7):638. doi: 10.3390/antibiotics13070638. [DOI] [PMC free article] [PubMed] [Google Scholar]
210.Ramasamy T., Keerthana S., Srinivasan M., Chandrasekar D., Porteen K., Borthakur A., Elamaran A., Sriram P. 2021. Molecular characterization of antibiotic resistance gene pattern of Staphylococcus aureus and Escherichia coli in mastitis affected dairy cows. [Google Scholar]
211.Wang K., Cha J., Liu K., Deng J., Yang B., Xu H., Wang J., Zhang L., Gu X., Huang C., Qu W. The prevalence of bovine mastitis-associated Staphylococcus aureus in China and its antimicrobial resistance rate: a meta-analysis. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.1006676. [DOI] [PMC free article] [PubMed] [Google Scholar]
212.Zaatout N., Hezil D. A meta-analysis of the global prevalence of methicillin-resistant Staphylococcus aureus (mrsa) isolated from clinical and subclinical bovine mastitis. J Appl Microbiol. 2022;132(1):140–154. doi: 10.1111/jam.15192. [DOI] [PubMed] [Google Scholar]
213.Khanal S., Boonyayatra S., Awaiwanont N. Prevalence of methicillin-resistant Staphylococcus aureus in dairy farms: a systematic review and meta-analysis. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.947154. [DOI] [PMC free article] [PubMed] [Google Scholar]
214.Dobrut A., Siemińska I., Sroka-Oleksiak A., Drożdż K., Sobońska J., Mroczkowska U., Brzychczy-Włoch M. Molecular and phenotypic identification of bacterial species isolated from cows with mastitis from three regions of Poland. BMC Vet Res. 2024;20(1):193. doi: 10.1186/s12917-023-03869-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
215.Krishnamoorthy P., Suresh K.P., Jayamma K.S., Shome B.R., Patil S.S., Amachawadi R.G. An understanding of the global status of major bacterial pathogens of milk concerning bovine mastitis: a systematic review and meta-analysis (scientometrics) Pathogens. 2021;10(5):545. doi: 10.3390/pathogens10050545. [DOI] [PMC free article] [PubMed] [Google Scholar]
216.Abebe R., Hatiya H., Abera M., Megersa B., Asmare K. Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at hawassa milk shed, south Ethiopia. BMC Vet Res. 2016;12(1):270. doi: 10.1186/s12917-016-0905-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
217.Rychshanova R., Mendybayeva A., Miciński B., Mamiyev N., Shevchenko P., Bermukhametov Z., Orzechowski B., Miciński J. Antibiotic resistance and biofilm formation in Staphylococcus aureus isolated from dairy cows at the stage of subclinical mastitis in northern Kazakhstan. Arch Anim Breed. 2022;65(4):439–448. doi: 10.5194/aab-65-439-2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
218.Fidelis C.E., Orsi A.M., Freu G., Gonçalves J.L., Santos M.V.D. Biofilm formation and antimicrobial resistance of Staphylococcus aureus and Streptococcus uberis isolates from bovine mastitis. Vet Sci. 2024;11(4) doi: 10.3390/vetsci11040170. [DOI] [PMC free article] [PubMed] [Google Scholar]
219.Essack S. Water, sanitation and hygiene in national action plans for antimicrobial resistance. Bull World Health Organ. 2021;99(8):606. doi: 10.2471/BLT.20.284232. [DOI] [PMC free article] [PubMed] [Google Scholar]
220.Muinde P., Maina J., Momanyi K., Yamo V., Mwaniki J., Kiiru J. Antimicrobial resistant pathogens detected in raw pork and poultry meat in retailing outlets in Kenya. Antibiotics. 2023;12(3):613. doi: 10.3390/antibiotics12030613. [DOI] [PMC free article] [PubMed] [Google Scholar]
221.Founou R.C., Blocker A.J., Noubom M., Tsayem C., Choukem S.P., Dongen M.V., Founou L.L. The covid-19 pandemic: a threat to antimicrobial resistance containment. Future Sci OA. 2021;7(8) doi: 10.2144/fsoa-2021-0012. [DOI] [PMC free article] [PubMed] [Google Scholar]
222.Tang K.W.K., Millar B.C., Moore J.E. Antimicrobial resistance (amr) Br J Biomed Sci. 2023;80 doi: 10.3389/bjbs.2023.11387. 11387. [DOI] [PMC free article] [PubMed] [Google Scholar]
223.Türkyılmaz S., Tekbıyık S., Oryasin E., Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin‐resistant Staphylococcus aureus isolated from bovine milk. Zoonos Publ Health. 2010;57(3):197–203. doi: 10.1111/j.1863-2378.2009.01257.x. [DOI] [PubMed] [Google Scholar]
224.Dagnaw M., Bazezew M., Mengistu B., Anagaw B., Mebratu A.S. Rate of beta-lactam resistance and epidemiological features of S. Aureus-associated bovine mastitis in cross-bred Ethiopian cows: systematic review. Vet Med Res Rep. 2024;15(null):39–55. doi: 10.2147/VMRR.S415339. [DOI] [PMC free article] [PubMed] [Google Scholar]
225.Pérez V.K.C., Custódio D.A.C., Silva E.M.M., de Oliveira J., Guimarães A.S., Brito M.A.V.P., Souza-Filho A.F., Heinemann M.B., Lage A.P., Dorneles E.M.S. Virulence factors and antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis in Brazil. Braz J Microbiol. 2020;51(4):2111–2122. doi: 10.1007/s42770-020-00363-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
226.Saini V., McClure J.T., Scholl D.T., DeVries T.J., Barkema H.W. Herd-level association between antimicrobial use and antimicrobial resistance in bovine mastitis Staphylococcus aureus isolates on Canadian dairy farms. J Dairy Sci. 2012;95(4):1921–1929. doi: 10.3168/jds.2011-5065. [DOI] [PubMed] [Google Scholar]
227.Sharifi A., Sobhani K., Mahmoudi P. A systematic review and meta-analysis revealed a high-level antibiotic resistance of bovine mastitis Staphylococcus aureus in Iran. Res Vet Sci. 2023;161:23–30. doi: 10.1016/j.rvsc.2023.05.016. [DOI] [PubMed] [Google Scholar]
228.Mulchandani R., Wang Y., Gilbert M., Van Boeckel T.P. Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Publ Health. 2023;3(2) doi: 10.1371/journal.pgph.0001305. [DOI] [PMC free article] [PubMed] [Google Scholar]
229.Peng M., Salaheen S., Biswas D. Animal health: global antibiotic issues. Encyclop Agri Food Syst. 2014:346–357. doi: 10.1016/B978-0-444-52512-3.00187-X. Epub 2014 Aug 21. [DOI] [Google Scholar]
230.Kernodle D.S. Gram‐positive pathogens. 2006. Mechanisms of resistance to β-lactam antibiotics; pp. 769–781. [Google Scholar]
231.Fergestad M.E., Stamsås G.A., Morales Angeles D., Salehian Z., Wasteson Y., Kjos M. Penicillin-binding protein pbp2a provides variable levels of protection toward different β-lactams in Staphylococcus aureus rn4220. Microbiologyopen. 2020;9(8) doi: 10.1002/mbo3.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
232.Cattoir V., Leclercq R. In: Antimicrobial drug resistance: mechanisms of drug resistance, volume 1. Mayers D.L., Sobel J.D., Ouellette M., Kaye K.S., Marchaim D., editors. Springer International Publishing; Cham: 2017. Resistance to macrolides, lincosamides, and streptogramins; pp. 269–280. [Google Scholar]
233.Guo Y., Huang C., Su H., Zhang Z., Chen M., Wang R., Zhang D., Zhang L., Liu M. Luteolin increases susceptibility to macrolides by inhibiting msra efflux pump in Trueperella pyogenes. Vet Res. 2022;53(1):3. doi: 10.1186/s13567-021-01021-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
234.Noguchi N., Takada K., Katayama J., Emura A., Sasatsu M. Regulation of transcription of the mph (a) gene for macrolide 2′-phosphotransferase i in escherichia coli: characterization of the regulatory gene mphr (a) J Bacteriol. 2000;182(18):5052–5058. doi: 10.1128/jb.182.18.5052-5058.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
235.Huang L., Wu C., Gao H., Xu C., Dai M., Huang L., Hao H., Wang X., Cheng G. Bacterial multidrug efflux pumps at the frontline of antimicrobial resistance: an overview. Antibiotics. 2022;11(4):520. doi: 10.3390/antibiotics11040520. [DOI] [PMC free article] [PubMed] [Google Scholar]
236.Connell Sean R., Tracz Dobryan M., Nierhaus Knud H., Taylor Diane E. Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob Agents Chemother. 2003;47(12):3675–3681. doi: 10.1128/aac.47.12.3675-3681.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
237.Saccone S., Brancato D., Bruno F., Coniglio E., Sturiale V., Federico C. Origin and evolution of genes in eukaryotes: mechanisms, dynamics, and functional implications. Genes. 2025;16(6):702. doi: 10.3390/genes16060702. [DOI] [PMC free article] [PubMed] [Google Scholar]
238.Tokuda M., Shintani M. Microbial evolution through horizontal gene transfer by Mobile genetic elements. Microb Biotechnol. 2024;17(1) doi: 10.1111/1751-7915.14408. [DOI] [PMC free article] [PubMed] [Google Scholar]
239.Khedkar S., Smyshlyaev G., Letunic I., Maistrenko Oleksandr M., Coelho Luis P., Orakov A., Forslund S.K., Hildebrand F., Luetge M., Schmidt T.S.B., Barabas O., Bork P. Landscape of Mobile genetic elements and their antibiotic resistance cargo in prokaryotic genomes. Nucleic Acids Res. 2022;50(6):3155–3168. doi: 10.1093/nar/gkac163. [DOI] [PMC free article] [PubMed] [Google Scholar]
240.Vrancianu C.O., Popa L.I., Bleotu C., Chifiriuc M.C. Targeting plasmids to limit acquisition and transmission of antimicrobial resistance. Front Microbiol. 2020;11 doi: 10.3389/fmicb.2020.00761. 761. [DOI] [PMC free article] [PubMed] [Google Scholar]
241.Partridge Sally R., Kwong Stephen M., Firth N., Jensen Slade O. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev. 2018;31(4) doi: 10.1128/cmr.00088-17. [DOI] [PMC free article] [PubMed] [Google Scholar]
242.Gillieatt B.F., Coleman N.V. Unravelling the mechanisms of antibiotic and heavy metal resistance co-selection in environmental bacteria. FEMS (Fed Eur Microbiol Soc) Microbiol Rev. 2024;48(4) doi: 10.1093/femsre/fuae017. [DOI] [PMC free article] [PubMed] [Google Scholar]

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Supplementary Materials

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Data Availability Statement

The datasets used and/or analyzed during the current study are available in the supplementary materials.

[bib1] 1.M.W. Dictionary. 2020. Available from: www.Merriam-Webster.com.

[bib2] 2.Djabri B., Bareille N., Beaudeau F., Seegers H. Quarter milk somatic cell count in infected dairy cows: a meta-analysis. Vet Res. 2002;33(4):335–357. doi: 10.1051/vetres:2002021. [DOI] [PubMed] [Google Scholar]

[bib3] 3.Thorberg B.-M., Danielsson-Tham M.-L., Emanuelson U., Waller K.P. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J Dairy Sci. 2009;92(10):4962–4970. doi: 10.3168/jds.2009-2184. [DOI] [PubMed] [Google Scholar]

[bib4] 4.De Vliegher S., Fox L., Piepers S., McDougall S., Barkema H. Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J Dairy Sci. 2012;95(3):1025–1040. doi: 10.3168/jds.2010-4074. [DOI] [PubMed] [Google Scholar]

[bib5] 5.Muzammil I., Ijaz M., Saleem M.H., Ali M.M. Drug repurposing strategy: an emerging approach to identify potential therapeutics for treatment of bovine mastitis. Microb Pathog. 2022;171 doi: 10.1016/j.micpath.2022.105691. [DOI] [PubMed] [Google Scholar]

[bib6] 6.Boss R., Naskova J., Steiner A., Graber H. Mastitis diagnostics: quantitative pcr for Staphylococcus aureus genotype b in bulk tank milk. J Dairy Sci. 2011;94(1):128–137. doi: 10.3168/jds.2010-3251. [DOI] [PubMed] [Google Scholar]

[bib7] 7.Barkema H., Schukken Y., Zadoks R. Invited review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci. 2006;89(6):1877–1895. doi: 10.3168/jds.S0022-0302(06)72256-1. [DOI] [PubMed] [Google Scholar]

[bib8] 8.Botaro B.G., Cortinhas C.S., Dibbern A.G., Silva L.F.P.e., Benites N.R., dos Santos M.V. Staphylococcus aureus intramammary infection affects milk yield and scc of dairy cows. Trop Anim Health Prod. 2015;47(1):61–66. doi: 10.1007/s11250-014-0683-5. [DOI] [PubMed] [Google Scholar]

[bib9] 9.Sutra L., Poutrel B. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J Med Microbiol. 1994;40(2):79–89. doi: 10.1099/00222615-40-2-79. [DOI] [PubMed] [Google Scholar]

[bib10] 10.Tigabu A., Getaneh A. Staphylococcus aureus, eskape bacteria challenging current health care and community settings: a literature review. Clin Lab. 2021;67(7) doi: 10.7754/Clin.Lab.2020.200930. [DOI] [PubMed] [Google Scholar]

[bib11] 11.Haag A.F., Fitzgerald J.R., Penadés J.R. Staphylococcus aureus in animals. Microbiol Spectr. 2019;7(3) doi: 10.1128/microbiolspec.gpp1123-0060-2019. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib12] 12.Javed M.U., Ijaz M., Ahmed A., Rasheed H., Sabir M.J., Jabir A.A. Molecular dynamics and antimicrobial resistance pattern of β-lactam resistant coagulase positive Staphylococcus aureus isolated from goat mastitis. Pak Vet J. 2024;44(2) [Google Scholar]

[bib13] 13.Al-Majali A.M., Al-Qudah K.M., Al-Tarazi Y.H., Al-Rawashdeh O.F. Risk factors associated with camel brucellosis in Jordan. Trop Anim Health Prod. 2008;40(3):193–200. doi: 10.1007/s11250-007-9080-7. [DOI] [PubMed] [Google Scholar]

[bib14] 14.Sharifi A., Mahmoudi P., Sobhani K. The prevalence of adhesion and biofilm genes in Staphylococcus aureus isolates from bovine mastitis: a comprehensive meta‐analysis. Vet Med Sci. 2024;10(2) doi: 10.1002/vms3.1378. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib15] 15.Liu H., Xiao Y., Nie H., Huang Q., Chen W. Influence of (p) ppgpp on biofilm regulation in Pseudomonas putida kt2440. Microbiol Res. 2017;204:1–8. doi: 10.1016/j.micres.2017.07.003. [DOI] [PubMed] [Google Scholar]

[bib16] 16.Oranusi S., Galadima M., Umoh V. Toxicity test and bacteriophage typing of Staphylococcus aureus isolates from food contact surfaces and foods prepared by families in Zaria, Nigeria. Afr J Biotechnol. 2006;5(4):362–365. [Google Scholar]

[bib17] 17.Yamada H. Tea catechins and Staphylococcus aureus. Tea Health Dise Prevent. 2013:1207–1213. [Google Scholar]

[bib18] 18.Taiwo S., Onile B., Akanbi II A. Methicillin-resistant Staphylococcus aureus (mrsa) isolates in ilorin, Nigeria. Afr J Clin Exp Microbiol. 2004;5(2):189–197. [Google Scholar]

[bib19] 19.Odetokun I.A., Adetona M.A., Ade-Yusuf R.O., Adewoye A.O., Ahmed A.N., Ghali-Mohammed I., Al-Mustapha A.I., Fetsch A. S taphylococcus aureus contamination of animal-derived foods in Nigeria: a systematic review, 2002—2022. Food Safet Risk. 2023;10(1):6. [Google Scholar]

[bib20] 20.Sasirekha B., Usha M., Amruta A., Ankit S., Brinda N., Divya R. Evaluation and comparison of different phenotypic tests to detect methicillin resistant Staphylococcus aureus and their biofilm production. Int J PharmTech Res. 2012;4(2):532–541. [Google Scholar]

[bib21] 21.Smith T.C. Livestock-associated staphylococcus aureus: the United States experience. PLoS Pathog. 2015;11(2) doi: 10.1371/journal.ppat.1004564. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib22] 22.Oliveira D., Borges A., Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins. 2018;10(6):252. doi: 10.3390/toxins10060252. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib23] 23.Ryu S., Song P.I., Seo C.H., Cheong H., Park Y. Colonization and infection of the skin by s. Aureus: immune system evasion and the response to cationic antimicrobial peptides. Int J Mol Sci. 2014;15(5):8753–8772. doi: 10.3390/ijms15058753. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib24] 24.Wertheim H.F., Melles D.C., Vos M.C., Van Leeuwen W., Van Belkum A., Verbrugh H.A., Nouwen J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751–762. doi: 10.1016/S1473-3099(05)70295-4. [DOI] [PubMed] [Google Scholar]

[bib25] 25.Aires de Sousa M., Lencastre de H. Bridges from hospitals to the laboratory: genetic portraits of methicillin-resistant Staphylococcus aureus clones. FEMS Immunol Med Microbiol. 2004;40(2):101–111. doi: 10.1016/S0928-8244(03)00370-5. [DOI] [PubMed] [Google Scholar]

[bib26] 26.Cheung G.Y., Bae J.S., Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12(1):547–569. doi: 10.1080/21505594.2021.1878688. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib27] 27.Touaitia R., Mairi A., Ibrahim N.A., Basher N.S., Idres T., Touati A. Staphylococcus aureus: a review of the pathogenesis and virulence mechanisms. Antibiotics. 2025;14(5):470. doi: 10.3390/antibiotics14050470. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib28] 28.Rojo P., Barrios M., Palacios A., Gomez C., Chaves F. Community-associated Staphylococcus aureus infections in children. Expert Rev Anti-infect Ther. 2010;8(5):541–554. doi: 10.1586/eri.10.34. [DOI] [PubMed] [Google Scholar]

[bib29] 29.Esposito S., Blasi F., Curtis N., Kaplan S., Lazzarotto T., Meschiari M., Mussini C., Peghin M., Rodrigo C., Vena A. New antibiotics for Staphylococcus aureus infection: an update from the world association of infectious diseases and immunological disorders (waidid) and the Italian society of anti-infective therapy (sita) Antibiotics. 2023;12(4):742. doi: 10.3390/antibiotics12040742. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib30] 30.Li X., Zhang J., Zhang H., Shi X., Wang J., Li K., Liang J., Xu X., Zhao W., Zhao C. Genomic analysis, antibiotic resistance, and virulence of Staphylococcus aureus from food and food outbreaks: a potential public concern. Int J Food Microbiol. 2022;377 doi: 10.1016/j.ijfoodmicro.2022.109825. [DOI] [PubMed] [Google Scholar]

[bib31] 31.Founou L.L., Founou R.C., Essack S.Y. Antibiotic resistance in the food chain: a developing country-perspective. Front Microbiol. 2016;7:1881. doi: 10.3389/fmicb.2016.01881. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib32] 32.Al-Saleh A., Shahid M., Farid E., Bindayna K. Trends in methicillin-resistant Staphylococcus aureus in the gulf cooperation council countries: antibiotic resistance, virulence factors and emerging strains. East Mediterr Health J. 2022;28(6) doi: 10.26719/emhj.22.042. [DOI] [PubMed] [Google Scholar]

[bib33] 33.Bitrus A., Peter O., Abbas M., Goni M.D. Staphylococcus aureus: a review of antimicrobial resistance mechanisms. Vet Sci: Res Rev. 2018;4(2):43–54. [Google Scholar]

[bib34] 34.Turner N.A., Sharma-Kuinkel B.K., Maskarinec S.A., Eichenberger E.M., Shah P.P., Carugati M., Holland T.L., Fowler V.G., Jr. Methicillin-resistant staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol. 2019;17(4):203–218. doi: 10.1038/s41579-018-0147-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib35] 35.Kot B., Wierzchowska K., Piechota M., Grużewska A. Antimicrobial resistance patterns in methicillin-resistant Staphylococcus aureus from patients hospitalized during 2015–2017 in hospitals in Poland. Med Princ Pract. 2020;29(1):61–68. doi: 10.1159/000501788. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib36] 36.Rasheed H., Ijaz M., Ahmed A., Javed M.U., Shah S.F.A., Anwaar F. Discrepancies between phenotypic and genotypic identification methods of antibiotic resistant genes harboring Staphylococcus aureus. Microb Pathog. 2023;184 doi: 10.1016/j.micpath.2023.106342. [DOI] [PubMed] [Google Scholar]

[bib37] 37.Tobin E.H., Jogu P., Koirala J. Statpearls [internet] StatPearls Publishing; 2025. Methicillin-resistant Staphylococcus aureus. [PubMed] [Google Scholar]

[bib38] 38.Kong C., Neoh H.-m., Nathan S. Targeting Staphylococcus aureus toxins: a potential form of anti-virulence therapy. Toxins. 2016;8(3):72. doi: 10.3390/toxins8030072. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib39] 39.Murray C.J., Ikuta K.S., Sharara F., Swetschinski L., Aguilar G.R., Gray A., Han C., Bisignano C., Rao P., Wool E. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–655. doi: 10.1016/S0140-6736(21)02724-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib40] 40.Khan S.A., Imtiaz M.A., Sayeed M.A., Shaikat A.H., Hassan M.M. Antimicrobial resistance pattern in domestic animal-wildlife-environmental niche via the food chain to humans with a Bangladesh perspective; a systematic review. BMC Vet Res. 2020;16(1):302. doi: 10.1186/s12917-020-02519-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib41] 41.Argudín M.A., Deplano A., Meghraoui A., Dodémont M., Heinrichs A., Denis O., Nonhoff C., Roisin S. Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics. 2017;6(2):12. doi: 10.3390/antibiotics6020012. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib42] 42.Byarugaba D. Antimicrobial resistance in developing countries and responsible risk factors. Int J Antimicrob Agents. 2004;24(2):105–110. doi: 10.1016/j.ijantimicag.2004.02.015. [DOI] [PubMed] [Google Scholar]

[bib43] 43.Hogeveen H., Huijps K., Lam T. Economic aspects of mastitis: new developments. N Z Vet J. 2011;59(1):16–23. doi: 10.1080/00480169.2011.547165. [DOI] [PubMed] [Google Scholar]

[bib44] 44.Islam M.S., Paul A., Talukder M., Roy K., Sobur M.A., Ievy S., Nayeem M.M.H., Rahman S., Nazir K.N.H., Hossain M.T. Migratory birds travelling to Bangladesh are potential carriers of multi-drug resistant enterococcus spp., salmonella spp., and vibrio spp. Saudi J Biol Sci. 2021;28(10):5963–5970. doi: 10.1016/j.sjbs.2021.06.053. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib45] 45.Roy K., Islam M.S., Paul A., Ievy S., Talukder M., Sobur M.A., Ballah F.M., Khan M.S.R., Rahman M.T. Molecular detection and antibiotyping of multi‐drug resistant Enterococcus faecium from healthy broiler chickens in Bangladesh. Vet Med Sci. 2022;8(1):200–210. doi: 10.1002/vms3.669. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib46] 46.Tawyabur M., Islam M.S., Sobur M.A., Hossain M.J., Mahmud M.M., Paul S., Hossain M.T., Ashour H.M., Rahman M.T. Isolation and characterization of multidrug-resistant Escherichia coli and salmonella spp. from healthy and diseased turkeys. Antibiotics. 2020;9(11):770. doi: 10.3390/antibiotics9110770. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib47] 47.Talukder M., Islam M.S., Ievy S., Sobur M.A., Ballah F.M., Najibullah M., Rahman M.B., Rahman M.T., Khan M.F.R. Detection of multidrug resistant salmonella spp. from healthy and diseased broilers having potential public health significance. J Adv Biotechnol Exp Ther. 2021;4(2):248–255. [Google Scholar]

[bib48] 48.Nitz J., Wente N., Zhang Y., Klocke D., Tho Seeth M., Krömker V. Dry period or early lactation—time of onset and associated risk factors for intramammary infections in dairy cows. Pathogens. 2021;10(2):224. doi: 10.3390/pathogens10020224. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib49] 49.Rajkovic A., Jovanovic J., Monteiro S., Decleer M., Andjelkovic M., Foubert A., Beloglazova N., Tsilla V., Sas B., Madder A. Detection of toxins involved in foodborne diseases caused by gram‐positive bacteria. Compr Rev Food Sci Food Saf. 2020;19(4):1605–1657. doi: 10.1111/1541-4337.12571. [DOI] [PubMed] [Google Scholar]

[bib50] 50.Kerro Dego O., Tareke F. Bovine mastitis in selected areas of southern Ethiopia. Trop Anim Health Prod. 2003;35(3):197–205. doi: 10.1023/a:1023352811751. [DOI] [PubMed] [Google Scholar]

[bib51] 51.Kadariya J., Smith T.C., Thapaliya D. Staphylococcus aureus and staphylococcal food‐borne disease: an ongoing challenge in public health. BioMed Res Int. 2014;2014(1) doi: 10.1155/2014/827965. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib52] 52.Abunna F., Abriham T., Gizaw F., Beyene T., Feyisa A., Ayana D., Mamo B., Duguma R. Staphylococcus: isolation, identification and antimicrobial resistance in dairy cattle farms, municipal abattoir and personnel in and around asella, Ethiopia. J Vet Sci Technol. 2016;7(383):2. [Google Scholar]

[bib53] 53.Badawy B., Elafify M., Farag A.M., Moustafa S.M., Sayed-Ahmed M.Z., Moawad A.A., Algammal A.M., Ramadan H., Eltholth M. Ecological distribution of virulent multidrug-resistant Staphylococcus aureus in livestock, environment, and dairy products. Antibiotics. 2022;11(11):1651. doi: 10.3390/antibiotics11111651. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib54] 54.Suleiman A.S., Abbass M., Hossain M., Choudhary P., Bhattacharya P., Islam M.A. Impact of antibiotic-coated sutures on surgical site infections: a second-order meta-analysis. Int J Surg. 2024;110(1):507–519. doi: 10.1097/JS9.0000000000000822. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib55] 55.Fenta M.D., Tafere F.A., Mebratu A.S., Malede B.A. Quarter-wise proportion and beta-lactam resistance rate of bovine mastitis associated-staphylococcus aureus among infectious episodes in Ethiopia: systematic review and meta-analysis. Heliyon. 2023;9(7) doi: 10.1016/j.heliyon.2023.e18180. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib56] 56.Nikolic P., Mudgil P. The cell wall, cell membrane and virulence factors of Staphylococcus aureus and their role in antibiotic resistance. Microorganisms. 2023;11(2):259. doi: 10.3390/microorganisms11020259. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib57] 57.Page M.J., McKenzie J.E., Bossuyt P.M., Boutron I., Hoffmann T.C., Mulrow C.D., Shamseer L., Tetzlaff J.M., Akl E.A., Brennan S.E., Chou R., Glanville J., Grimshaw J.M., Hróbjartsson A., Lalu M.M., Li T., Loder E.W., Mayo-Wilson E., McDonald S., McGuinness L.A., Stewart L.A., Thomas J., Tricco A.C., Welch V.A., Whiting P., Moher D. The prisma 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib58] 58.Grammatopoulos T., Hunter J.W., Munn Z., Stone J.C., Barker T.H. Reporting quality and risk of bias in jbi systematic reviews evaluating the effectiveness of interventions: a methodological review protocol. JBI Evid Synth. 2023;21(3):584–591. doi: 10.11124/JBIES-22-00317. [DOI] [PubMed] [Google Scholar]

[bib59] 59.DerSimonian R., Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188. doi: 10.1016/0197-2456(86)90046-2. [DOI] [PubMed] [Google Scholar]

[bib60] 60.Ahmed M.J., Hossain M.I., Bhuiyan M.I.H., Rahman M.A., Kaderi I.J., Nirob A.I., Rahi M.A.I., Mamun M., Alam K.E., Chowdhury M.J., Bhandari P., Chalise R., Alam M.J., Chowdhury M.T.I., Ali M., Hossain D. Antimicrobial resistance in meat and meat products from Asia: an urgent one health challenge- a systematic review and meta-analysis. Poult Sci. 2025;104(11) doi: 10.1016/j.psj.2025.105811. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib61] 61.Higgins J.P., Thompson S.G. Quantifying heterogeneity in a meta‐analysis. Stat Med. 2002;21(11):1539–1558. doi: 10.1002/sim.1186. [DOI] [PubMed] [Google Scholar]

[bib62] 62.Ahmed M.J., Hossain M.I., Hossain D. Emerging pathogen alert: global epidemiology of the zoonotic potential of escherichia albertii: a systematic review and meta-analysis. Int J Food Microbiol. 2026;447 doi: 10.1016/j.ijfoodmicro.2025.111564. [DOI] [PubMed] [Google Scholar]

[bib63] 63.Alkharusi H. Categorical variables in regression analysis: a comparison of dummy and effect coding. Int J Educ. 2012;4(2):202. [Google Scholar]

[bib64] 64.Egger M., Smith G.D. Meta-analysis bias in location and selection of studies. BMJ. 1998;316(7124):61–66. doi: 10.1136/bmj.316.7124.61. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib65] 65.Duval S., Tweedie R. Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–463. doi: 10.1111/j.0006-341x.2000.00455.x. [DOI] [PubMed] [Google Scholar]

[bib66] 66.Wickham H. Ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3(2):180–185. [Google Scholar]

[bib67] 67.Akkou M., Antri K., Bachtarzi M.-A., Bes M., Tristan A., Dauwalder O., Kaidi R., Meugnier H., Tazir M., Etienne J. Phenotypic and genotypic characterization of Staphylococcus aureus strains associated with bovine mastitis and nasal carriage of workers in contact to animals in Algeria. Pak Vet J. 2016;36(2):184–188. [Google Scholar]

[bib68] 68.Akkou M., Titouche Y., Bentayeb L., Bes M., Laurent F., Ramdani-Bouguessa N. Risk factors for dairy cows mastitis in Algeria, antibiotic resistance and molecular typing of the causative Staphylococcus aureus. Vet Res Commun. 2024;48(5):3007–3018. doi: 10.1007/s11259-024-10457-2. [DOI] [PubMed] [Google Scholar]

[bib69] 69.Benhamed N., Moulay M., Aggad H., Henni J., Kihal M. Prevalence of mastitis infection and identification of causing bacteria in cattle in the Oran region west Algeria. J Anim Vet Adv. 2011;10(22):3002–3005. [Google Scholar]

[bib70] 70.Crespi E., Pereyra A.M., Puigdevall T., Rumi M.V., Testorelli M.F., Caggiano N., Gulone L., Mollerach M., Gentilini E.R., Srednik M.E. Antimicrobial resistance studies in staphylococci and streptococci isolated from cows with mastitis in Argentina. J Vet Sci. 2021;23(6):e12. doi: 10.4142/jvs.21062. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib71] 71.Al-Harbi H., Ranjbar S., Moore R.J., Alawneh J.I. Bacteria isolated from milk of dairy cows with and without clinical mastitis in different regions of Australia and their amr profiles. Front Vet Sci. 2021;8 doi: 10.3389/fvets.2021.743725. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib72] 72.Al Emon A., Hossain H., Chowdhury M.S.R., Rahman M.A., Tanni F.Y., Asha M.N., Akter H., Hossain M.M., Islam M.R., Rahman M.M. Prevalence, antimicrobial susceptibility profiles and resistant gene identification of bovine subclinical mastitis pathogens in Bangladesh. Heliyon. 2024;10(14) doi: 10.1016/j.heliyon.2024.e34567. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib73] 73.Fazal M.A., Rana E.A., Akter S., Alim M.A., Barua H., Ahad A. Molecular identification, antimicrobial resistance and virulence gene profiling of staphylococcus spp. associated with bovine sub-clinical mastitis in Bangladesh. Vet Anim Sci. 2023;21 doi: 10.1016/j.vas.2023.100297. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib74] 74.Hoque M., Das Z., Rahman A., Haider M., Islam M. Molecular characterization of Staphylococcus aureus strains in bovine mastitis milk in Bangladesh. Int J Vet Sci Med. 2018;6(1):53–60. doi: 10.1016/j.ijvsm.2018.03.008. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib75] 75.Islam M.M., Hossain M.I., Islam M.S., Azam M.G., Sultana S. Prevalence, antibiotic resistance patterns, and virulence factors of Staphylococcus aureus isolates associated with bovine mastitis in northern Bangladesh. Heliyon. 2025;11(3) doi: 10.1016/j.heliyon.2025.e42107. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib76] 76.Rana E.A., Fazal M.A., Alim M.A. Frequently used therapeutic antimicrobials and their resistance patterns on Staphylococcus aureus and Escherichia coli in mastitis affected lactating cows. Int J Vet Sci Med. 2022;10(1):1–10. doi: 10.1080/23144599.2022.2038494. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib77] 77.Singha S., Koop G., Persson Y., Hossain D., Scanlon L., Derks M., Hoque M.A., Rahman M.M. Incidence, etiology, and risk factors of clinical mastitis in dairy cows under semi-tropical circumstances in Chattogram, Bangladesh. Animals. 2021;11(8):2255. doi: 10.3390/ani11082255. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib78] 78.Castelani L., Santos A.F.S., Miranda M.d.S., Zafalon L.F., Pozzi C.R., Arcaro J.R.P. Molecular typing of mastitis-causing Staphylococcus aureus isolated from heifers and cows. Int J Mol Sci. 2013;14(2):4326–4333. doi: 10.3390/ijms14024326. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib79] 79.Costa F., Belo N., Costa E., Andrade G., Pereira L., Carvalho I., Santos R. Frequency of enterotoxins, toxic shock syndrome toxin-1, and biofilm formation genes in Staphylococcus aureus isolates from cows with mastitis in the northeast of Brazil. Trop Anim Health Prod. 2018;50(5):1089–1097. doi: 10.1007/s11250-018-1534-6. [DOI] [PubMed] [Google Scholar]

[bib80] 80.Dorneles E.M., Fonseca M.D., Abreu J.A., Lage A.P., Brito M.A., Pereira C.R., Brandão H.M., Guimarães A.S., Heinemann M.B. Genetic diversity and antimicrobial resistance in Staphylococcus aureus and coagulase‐negative staphylococcus isolates from bovine mastitis in minas gerais, Brazil. Microbiologyopen. 2019;8(5) doi: 10.1002/mbo3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib81] 81.Gonçalves M.S., Dorneles E.M.S., Heinemann M.B., Brito M.A.V.P.e., Guimarães A.d.S. Genetic diversity and antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in minas gerais, Brazil. Ciência Rural. 2022;53(3) [Google Scholar]

[bib82] 82.Guimarães F., Manzi M., Joaquim S., Richini-Pereira V., Langoni H. Outbreak of methicillin-resistant Staphylococcus aureus (mrsa)-associated mastitis in a closed dairy herd. J Dairy Sci. 2017;100(1):726–730. doi: 10.3168/jds.2016-11700. [DOI] [PubMed] [Google Scholar]

[bib83] 83.Kroning I.S., Iglesias M.A., Mendonça K.S., Lopes G.V., Silva W.P. Presence of classical enterotoxin genes, agr typing, antimicrobial resistance, and genetic diversity of Staphylococcus aureus from milk of cows with mastitis in southern Brazil. J Food Protect. 2018;81(5):738–742. doi: 10.4315/0362-028X.JFP-17-436. [DOI] [PubMed] [Google Scholar]

[bib84] 84.Marques V.F., da Motta C.C., da Silva Soares B., de Melo D.A., de Oliveira Coelho S.d.M., da Silva Coelho I., Barbosa H.S., de Souza M.M.S. Biofilm production and beta-lactamic resistance in Brazilian Staphylococcus aureus isolates from bovine mastitis. Braz J Microbiol. 2017;48(1):118–124. doi: 10.1016/j.bjm.2016.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib85] 85.Rall V., Miranda E., Castilho I., Camargo C., Langoni H., Guimarães F., Júnior J.A., Júnior A.F. Diversity of staphylococcus species and prevalence of enterotoxin genes isolated from milk of healthy cows and cows with subclinical mastitis. J Dairy Sci. 2014;97(2):829–837. doi: 10.3168/jds.2013-7226. [DOI] [PubMed] [Google Scholar]

[bib86] 86.Rossi B., Bonsaglia E., Castilho I., Dantas S., Salina A., Langoni H., Pantoja J., Budri P., Fitzgerald-Hughes D., Júnior A.F. Genotyping of long term persistent Staphylococcus aureus in bovine subclinical mastitis. Microb Pathog. 2019;132:45–50. doi: 10.1016/j.micpath.2019.04.031. [DOI] [PubMed] [Google Scholar]

[bib87] 87.Silva A.T.F., Gonçalves J.L., Dantas S.T.A., Rall V.L.M., de Oliveira P.R.F., Dos Santos M.V., Peixoto R.d.M., Mota R.A. Genetic and phenotypic characterization of subclinical mastitis-causing multidrug-resistant Staphylococcus aureus. Antibiotics. 2023;12(9):1353. doi: 10.3390/antibiotics12091353. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib88] 88.Rodríguez M.F., Gomez A.P., Ceballos-Garzon A. Antimicrobial resistance profiles of staphylococcus isolated from cows with subclinical mastitis: do strains from the environment and from humans contribute to the dissemination of resistance among bacteria on dairy farms in Colombia? Antibiotics. 2023;12(11):1574. doi: 10.3390/antibiotics12111574. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib89] 89.Esemu S.N., Nya’Nying S.F., Ndip L.M., Bessong P.O., Tanih N.F., Smith S.I., Ndip R.N. Isolation and characterization of methicillin-resistant Staphylococcus aureus from bovine mastitis in north west Cameroon: public health implications. BMC Res Notes. 2024;17(1):389. doi: 10.1186/s13104-024-07073-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib90] 90.Bao H., Zhang H., Zhou Y., Zhang L., Wang R. Prevalence, enterotoxin gene and antimicrobial resistance of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from clinical healthy dairy cows. SEa. 2004;55(310) [Google Scholar]

[bib91] 91.Chen C., Sun C., Li J., Ji X., Wang Y., Song C., Wang G. Characterisation of Staphylococcus aureus isolates from bovine mastitis in Ningxia, Western China. J Glob Antimicrob Resist. 2021;25:232–237. doi: 10.1016/j.jgar.2021.03.021. [DOI] [PubMed] [Google Scholar]

[bib92] 92.Gao J., Barkema H.W., Zhang L., Liu G., Deng Z., Cai L., Shan R., Zhang S., Zou J., Kastelic J.P. Incidence of clinical mastitis and distribution of pathogens on large Chinese dairy farms. J Dairy Sci. 2017;100(6):4797–4806. doi: 10.3168/jds.2016-12334. [DOI] [PubMed] [Google Scholar]

[bib93] 93.Li L., Feng W., Zhang Z., Xue H., Zhao X. Macrolide-lincosamide-streptogramin resistance phenotypes and genotypes of coagulase-positive Staphylococcus aureus and coagulase-negative staphylococcal isolates from bovine mastitis. BMC Vet Res. 2015;11(1):168. doi: 10.1186/s12917-015-0492-8. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib94] 94.Li L., Zhao X. Characterization of the resistance class 1 integrons in Staphylococcus aureus isolates from milk of lactating dairy cattle in northwestern China. BMC Vet Res. 2018;14(1):59. doi: 10.1186/s12917-018-1376-5. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib95] 95.Liu J., Wang X., Bi C., Mehmood K., Ali F., Qin J., Han Z. Molecular characterization of multi-drug-resistant Staphylococcus aureus in mastitis bovine milk from a dairy farm in Anhui, China. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.966533. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib96] 96.Liu K., Tao L., Li J., Fang L., Cui L., Li J., Meng X., Zhu G., Bi C., Wang H. Characterization of Staphylococcus aureus isolates from cases of clinical bovine mastitis on large-scale Chinese dairy farms. Front Vet Sci. 2020;7 doi: 10.3389/fvets.2020.580129. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib97] 97.Qu Y., Zhao H., Nobrega D.B., Cobo E.R., Han B., Zhao Z., Li S., Li M., Barkema H.W., Gao J. Molecular epidemiology and distribution of antimicrobial resistance genes of staphylococcus species isolated from Chinese dairy cows with clinical mastitis. J Dairy Sci. 2019;102(2):1571–1583. doi: 10.3168/jds.2018-15136. [DOI] [PubMed] [Google Scholar]

[bib98] 98.Ren Q., Liao G., Wu Z., Lv J., Chen W. Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang, China. J Dairy Sci. 2020;103(4):3368–3380. doi: 10.3168/jds.2019-17420. [DOI] [PubMed] [Google Scholar]

[bib99] 99.Shi D., Hao Y., Zhang A., Wulan B., Fan X. Antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis in China. Transbound Emerg Dis. 2010;57(4):221–224. doi: 10.1111/j.1865-1682.2010.01139.x. [DOI] [PubMed] [Google Scholar]

[bib100] 100.Wang D., Zhang L., Zhou X., He Y., Yong C., Shen M., Szenci O., Han B. Antimicrobial susceptibility, virulence genes, and randomly amplified polymorphic DNA analysis of Staphylococcus aureus recovered from bovine mastitis in Ningxia, China. J Dairy Sci. 2016;99(12):9560–9569. doi: 10.3168/jds.2016-11625. [DOI] [PubMed] [Google Scholar]

[bib101] 101.Wang W., Lin X., Jiang T., Peng Z., Xu J., Yi L., Li F., Fanning S., Baloch Z. Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in beijing, China. Front Microbiol. 2018;9:1123. doi: 10.3389/fmicb.2018.01123. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib102] 102.Wang X., Wang X., Wang Y., Guo G., Usman T., Hao D., Tang X., Zhang Y., Yu Y. Antimicrobial resistance and toxin gene profiles of Staphylococcus aureus strains from holstein milk. Lett Appl Microbiol. 2014;58(6):527–534. doi: 10.1111/lam.12221. [DOI] [PubMed] [Google Scholar]

[bib103] 103.Yang F., Shi W., Meng N., Zhao Y., Ding X., Li Q. Antimicrobial resistance and virulence profiles of staphylococci isolated from clinical bovine mastitis. Front Microbiol. 2023;14 doi: 10.3389/fmicb.2023.1190790. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib104] 104.Zhang D.-X., Li Y., Yang X.-Q., Su H.-Y., Wang Q., Zhang Z.-H., Liu Y.-C., Tian C.-L., Cui C.-C., Liu M.-C. In vitro antibiotic susceptibility, virulence genes distribution and biofilm production of Staphylococcus aureus isolates from bovine mastitis in the Liaoning Province of China. Infect Drug Resist. 2020:1365–1375. doi: 10.2147/IDR.S247765. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib105] 105.Zhang L., Gao J., Barkema H.W., Ali T., Liu G., Deng Y., Naushad S., Kastelic J.P., Han B. Virulence gene profiles: alpha-hemolysin and clonal diversity in Staphylococcus aureus isolates from bovine clinical mastitis in China. BMC Vet Res. 2018;14(1):63. doi: 10.1186/s12917-018-1374-7. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib106] 106.Zhang T., Luo Q., Chen Y., Li T., Wen G., Zhang R., Luo L., Lu Q., Ai D., Wang H. Molecular epidemiology, virulence determinants and antimicrobial resistance of campylobacter spreading in retail chicken meat in central China. Gut Pathog. 2016;8:1–9. doi: 10.1186/s13099-016-0132-2. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib107] 107.Zhang Z., Chen Y., Li X., Wang X., Li H. Detection of antibiotic resistance, virulence gene, and drug resistance gene of Staphylococcus aureus isolates from bovine mastitis. Microbiol Spectr. 2022;10(4) doi: 10.1128/spectrum.00471-22. e00471-00422. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib108] 108.Vikova H., Babak V., Vrtkova I., Cervinkova D., Marosevic D., Moravkova M., Jaglic Z. Epidemiology of intramammary infections with Staphylococcus aureus and mastitis streptococci in a dairy cattle herd with a history of recurrent clinical mastitis. Pol J Vet Sci. 2017;20(1) doi: 10.1515/pjvs-2017-0017. [DOI] [PubMed] [Google Scholar]

[bib109] 109.Zigo F., Farkašová Z., Výrostková J., Regecova I., Ondrašovičová S., Vargová M., Sasáková N., Pecka-Kielb E., Bursová Š., Kiss D.S. Dairy cows’ udder pathogens and occurrence of virulence factors in staphylococci. Animals. 2022;12(4):470. doi: 10.3390/ani12040470. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib110] 110.Abd El-Razik K.A., Arafa A.A., Fouad E.A., Soror A.H., Abdalhamed A.M., Elgioushy M. Phenotypic and genotypic characterization of erythromycin-resistant Staphylococcus aureus isolated from bovine subclinical mastitis in Egypt. Vet World. 2023;16(7):1562. doi: 10.14202/vetworld.2023.1562-1571. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib111] 111.Abd El-Razik K.A., Soliman Y.A., Fouad E.A., Arafa A.A., Syame S.M., Soror A.H. Macrolides-resistant Staphylococcus aureus associated with clinical mastitis in cattle and buffalo in Egypt. J Adv Vet Res. 2023;13(3):461–468. [Google Scholar]

[bib112] 112.Algammal A.M., Enany M.E., El-Tarabili R.M., Ghobashy M.O., Helmy Y.A. Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of mrsa isolated from subclinical bovine mastitis in Egypt. Pathogens. 2020;9(5):362. doi: 10.3390/pathogens9050362. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib113] 113.Ameen F., Reda S.A., El-Shatoury S.A., Riad E.M., Enany M.E., Alarfaj A.A. Prevalence of antibiotic resistant mastitis pathogens in dairy cows in Egypt and potential biological control agents produced from plant endophytic actinobacteria. Saudi J Biol Sci. 2019;26(7):1492–1498. doi: 10.1016/j.sjbs.2019.09.008. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib114] 114.Asfour H.A., Darwish S.F. 2011. Phenotypic and genotypic detection of both meca-and blaz-genes mediated β-lactam resistance in staphylococcus strains isolated from bovine mastitis. [Google Scholar]

[bib115] 115.Eidaroos N.H., Algammal A.M., Mohamaden W.I., Alenzi A.M., Alghamdi S., Kabrah A., El-Mahallawy H.S., Eid H.M., Algwad A.A., Asfor S.A. Virulence traits, agr typing, multidrug resistance patterns, and biofilm ability of mdr Staphylococcus aureus recovered from clinical and subclinical mastitis in dairy cows. BMC Microbiol. 2025;25(1):155. doi: 10.1186/s12866-025-03870-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib116] 116.El-shenawy F., Ahmed H.A., El-Shemy M.M., Talayea A. Genotyping of methicillin-resistant Staphylococcus aureus (mrsa) isolated from bovine mastitis. Egypt J Vet Sci. 2025;56(8):1919–1930. [Google Scholar]

[bib117] 117.Elhaig M.M., Selim A. Molecular and bacteriological investigation of subclinical mastitis caused by Staphylococcus aureus and Streptococcus agalactiae in domestic bovids from Ismailia, Egypt. Trop Anim Health Prod. 2015;47(2):271–276. doi: 10.1007/s11250-014-0715-1. [DOI] [PubMed] [Google Scholar]

[bib118] 118.Ewida R.M., Al-Hosary A.A. Prevalence of enterotoxins and other virulence genes of Staphylococcus aureus caused subclinical mastitis in dairy cows. Vet World. 2020;13(6):1193. doi: 10.14202/vetworld.2020.1193-1198. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib119] 119.Gad W.A., Osman S.A., Abd El K.A.E.-H., Soror A.H., Soliman Y.A., Fouad E.A. In prevalence and molecular characterization of resistant Staphylococcus aureus strains in bulk milk tanks of dairy cattle in northern Egypt. Vet Res Forum. 2025:317. doi: 10.30466/vrf.2024.2038109.4398. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib120] 120.Ibrahim E.S., Arafa A.A., Dorgam S.M., Eid R.H., Atta N.S., El-Dabae W.H., Sadek E.G. Molecular characterization of genes responsible for biofilm formation in Staphylococcus aureus isolated from mastitic cows. Vet World. 2022;15(1):205. doi: 10.14202/vetworld.2022.205-212. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib121] 121.Mostafa Abdalhamed A., Zeedan G.S.G., Ahmed Arafa A., Shafeek Ibrahim E., Sedky D., Abdel nabey Hafez A. Detection of methicillin‐resistant Staphylococcus aureus in clinical and subclinical mastitis in ruminants and studying the effect of novel green synthetized nanoparticles as one of the alternative treatments. Vet Med Int. 2022;2022(1) doi: 10.1155/2022/6309984. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib122] 122.Selim A., Kelis K., AlKahtani M.D., Albohairy F.M., Attia K.A. Prevalence, antimicrobial susceptibilities and risk factors of methicillin resistant Staphylococcus aureus (mrsa) in dairy bovines. BMC Vet Res. 2022;18(1):293. doi: 10.1186/s12917-022-03389-z. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib123] 123.Tartor Y.H., Enany M.E., Ismail N.I., El-Demerdash A.S., Eidaroos N.H., Algendy R.M., Mahmmod Y., Elsohaby I. Vancomycin-resistant Staphylococcus aureus endangers Egyptian dairy herds. Sci Rep. 2024;14(1) doi: 10.1038/s41598-024-81516-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib124] 124.Younis G., Sadat A., Maghawry M. Characterization of coa gene and antimicrobial profiles of Staphylococcus aureus isolated from bovine clinical and subclinical mastitis. Adv Anim Vet Sci. 2018;6(4):161–168. [Google Scholar]

[bib125] 125.Abebe R., Hatiya H., Abera M., Megersa B., Asmare K. Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at hawassa milk shed, south Ethiopia. BMC Vet Res. 2016;12(1):270. doi: 10.1186/s12917-016-0905-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib126] 126.Abunna F., Fufa G., Megersa B., Regassa A. Bovine mastitis: prevalence, risk factors and bacterial isolation in small-holder dairy farms in addis ababa city, Ethiopia. Glob Vet. 2013;10(6):647–652. [Google Scholar]

[bib127] 127.Bihon A., Syoum A., Assefa A. Assessment of risk factors and isolation of Staphylococcus aureus and Escherichia coli from bovine subclinical mastitic milk in and around gondar, northwest Ethiopia. Trop Anim Health Prod. 2019;51(4):939–948. doi: 10.1007/s11250-018-1777-2. [DOI] [PubMed] [Google Scholar]

[bib128] 128.Chawicha T.G., Yunus H.A., Soma M. Antimicrobial susceptibility of major bacterial pathogens isolated from bovine mastitis in bench maji zone, southwest Ethiopia. Multidiscip Sci J. 2021;3(2) 2021010-2021010. [Google Scholar]

[bib129] 129.Dabele D.T., Borena B.M., Admasu P., Gebremedhin E.Z., Marami L.M. Prevalence and risk factors of mastitis and isolation, identification and antibiogram of staphylococcus species from mastitis positive zebu cows in toke kutaye, cheliya, and dendi districts, west shewa zone, Oromia, Ethiopia. Infect Drug Resist. 2021:987–998. doi: 10.2147/IDR.S295257. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib130] 130.Demil E., Teshome L., Kerie Y., Habtamu A., Kumilachew W., Andualem T., Mekonnen S.A. Prevalence of subclinical mastitis, associated risk factors and antimicrobial susceptibility of the pathogens isolated from milk samples of dairy cows in northwest Ethiopia. Prev Vet Med. 2022;205 doi: 10.1016/j.prevetmed.2022.105680. [DOI] [PubMed] [Google Scholar]

[bib131] 131.Getahun D.D., Tarekegn H.T., Azene B.T., Abebe L.T., Belete M.A., Tessema T.S. Virulence genes and antibiotic resistance profiling of staphylococcus species isolated from mastitic dairy cows in and around bahir dar, Ethiopia. BMC Microbiol. 2025;25(1):210. doi: 10.1186/s12866-025-03886-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib132] 132.Grima L.Y.W., Leliso S.A., Bulto A.O., Ashenafi D. Isolation, identification, and antimicrobial susceptibility profiles of Staphylococcus aureus from clinical mastitis in sebeta town dairy farms. Vet Med Int. 2021;2021(1) doi: 10.1155/2021/1772658. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib133] 133.Haftu R., Taddele H., Gugsa G., Kalayou S. Prevalence, bacterial causes, and antimicrobial susceptibility profile of mastitis isolates from cows in large-scale dairy farms of northern Ethiopia. Trop Anim Health Prod. 2012;44(7):1765–1771. doi: 10.1007/s11250-012-0135-z. [DOI] [PubMed] [Google Scholar]

[bib134] 134.Seyoum B., Kefyalew H., Abera B., Abdela N. Prevalence, risk factors and antimicrobial susceptibility test of Staphylococcus aureus in bovine cross breed mastitic milk in and around asella town, Oromia regional state, southern Ethiopia. Acta Trop. 2018;177:32–36. doi: 10.1016/j.actatropica.2017.09.012. [DOI] [PubMed] [Google Scholar]

[bib135] 135.Shille M., Dulo F., Abera S., Ayechew S. Isolation, identification, and antibiogram characteristics of Staphylococcus aureus from dairy cows kept under extensive management system, in the uba debretsehay district of southern Ethiopia. Vet Med Sci. 2025;11(4) doi: 10.1002/vms3.70503. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib136] 136.Tariku Sori T.S., Jemal Hussien J.H., Molalegne Bitew M.B. 2011. Prevalence and susceptibility assay of Staphylococcus aureus isolated from bovine mastitis in dairy farms of jimma town, south west Ethiopia. [Google Scholar]

[bib137] 137.Wodaje A., Belete M.A., Menkir A.S., Zegeye Z.B., Yihunie F.B. Detection of virulence genes and antimicrobial susceptibility profiles of Staphylococcus aureus isolates from bovine mastitis in chagni, northwestern Ethiopia. Vet Med Int. 2025;2025(1) doi: 10.1155/vmi/6473601. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib138] 138.Yimana M., Tesfaye J. Isolation, identification and antimicrobial profile of methicillin‐resistant Staphylococcus aureus from bovine mastitis in and around adama, central Ethiopia. Vet Med Sci. 2022;8(6):2576–2584. doi: 10.1002/vms3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib139] 139.Kadlec K., Entorf M., Peters T. Occurrence and characteristics of livestock-associated methicillin-resistant Staphylococcus aureus in quarter milk samples from dairy cows in Germany. Front Microbiol. 2019;10:1295. doi: 10.3389/fmicb.2019.01295. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib140] 140.Ruban W., Raveendra Hegde R.H., Kumar G. Methicillin resistance pattern of Staphylococcus aureus from mastitis milk in correlation to its possession of methicillin resistance gene k. Nithin prabhu. 2012 [Google Scholar]

[bib141] 141.Harini H., Sumathi B. Screening of bovine milk samples for sub-clinical mastitis and antibiogram of bacterial isolates. Vet World. 2011;4(8):358. [Google Scholar]

[bib142] 142.Mistry H., Sharma P., Mahato S., Saravanan R., Kumar P.A., Bhandari V. Prevalence and characterization of oxacillin susceptible meca-positive clinical isolates of Staphylococcus aureus causing bovine mastitis in India. PLoS One. 2016;11(9) doi: 10.1371/journal.pone.0162256. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib143] 143.Mitra S., Velu D., Bhuvana M., Krithiga N., Banerjee A., Shome R., Rahman H., Ghosh S., Shome B. Staphylococcus aureus spa type t267, clonal ancestor of bovine subclinical mastitis in India. J Appl Microbiol. 2013;114(6):1604–1615. doi: 10.1111/jam.12186. [DOI] [PubMed] [Google Scholar]

[bib144] 144.Mubarack H.M., Doss A., Vijayasanthi M., Venkataswamy R. Antimicrobial drug susceptibility of Staphylococcus aureus from subclinical bovine mastitis in coimbatore, Tamilnadu, South India. Vet World. 2012;5(6):352. [Google Scholar]

[bib145] 145.Mushtaq M., Agrawal R., Bhat M.A., Singh R., Pande N. Antibiotic resistance gene typing in Staphylococcus aureus isolated from bovine mastitis. Indian J Anim Sci. 2019;89:1188–1191. [Google Scholar]

[bib146] 146.Neelam, Jain V., Singh M., Joshi V.G., Chhabra R., Singh K., Rana Y. Virulence and antimicrobial resistance gene profiles of Staphylococcus aureus associated with clinical mastitis in cattle. PLoS One. 2022;17(5) doi: 10.1371/journal.pone.0264762. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib147] 147.Ramasamy T., Keerthana S., Srinivasan M., Chandrasekar D., Porteen K., Borthakur A., Elamaran A., Sriram P. Molecular characterization of antibiotic resistance gene pattern of Staphylococcus aureus and Escherichia coli in mastitis affected dairy cows. Indian J Anim Res. 2021;55(4):463–468. [Google Scholar]

[bib148] 148.Roshan M., Arora D., Behera M., Vats A., Gautam D., Deb R., Parkunan T., De S. Virulence and enterotoxin gene profile of methicillin-resistant staphylococcus aureus isolates from bovine mastitis. Comp Immunol Microbiol Infect Dis. 2022;80 doi: 10.1016/j.cimid.2021.101724. [DOI] [PubMed] [Google Scholar]

[bib149] 149.Sentitula B. Yadav, Kumar R. Incidence of staphylococci and streptococci during winter in mastitic milk of sahiwal cow and murrah buffaloes. Indian J Microbiol. 2012;52(2):153–159. doi: 10.1007/s12088-011-0207-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib150] 150.Shah M.S., Qureshi S., Kashoo Z., Farooq S., Wani S.A., Hussain M.I., Banday M., Khan A.A., Gull B., Habib A. Methicillin resistance genes and in vitro biofilm formation among staphylococcus aureus isolates from bovine mastitis in India. Comp Immunol Microbiol Infect Dis. 2019;64:117–124. doi: 10.1016/j.cimid.2019.02.009. [DOI] [PubMed] [Google Scholar]

[bib151] 151.Singh A., Batabyal S., Bandyopadhyay S., Maity A., Polley S., Banerjee D., Chattopadhyay S. Molecular chara cterization of methicillin-resistant staphylococcus aureus (mrsa) isolated from bovine mastitis in and around kolkata, India. Explor Anim Med Res. 2019;9(1) [Google Scholar]

[bib152] 152.Singh R., Kumar R., Yadav B. Distribution of pathogenic factors in staphylococcus aureus strains isolated from intra-mammary infections in cattle and buffaloes. Indian J Biotechnol. 2011;10(4):410–416. [Google Scholar]

[bib153] 153.Qolbaini E.N., Khoeri M.M., Salsabila K., Paramaiswari W.T., Tafroji W., Artika I.M., Safari D. Identification and antimicrobial susceptibility of methicillin-resistant staphylococcus aureus-associated subclinical mastitis isolated from dairy cows in bogor, Indonesia. Vet World. 2021;14(5):1180. doi: 10.14202/vetworld.2021.1180-1184. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib154] 154.Bahraminia F., Emadi S.R., Emaneini M., Farzaneh N., Rad M., Khoramian B. In A high prevalence of tylosin resistance among staphylococcus aureus strains isolated from bovine mastitis. Vet Res Forum. 2017:121. [PMC free article] [PubMed] [Google Scholar]

[bib155] 155.Dastmalchi Saei H., Panahi M. Genotyping and antimicrobial resistance of staphylococcus aureus isolates from dairy ruminants: differences in the distribution of clonal types between cattle and small ruminants. Arch Microbiol. 2020;202(1):115–125. doi: 10.1007/s00203-019-01722-z. [DOI] [PubMed] [Google Scholar]

[bib156] 156.Havaei S.A., Assadbeigi B., Esfahani B.N., Hoseini N.S., Rezaei N., Havaei S.R. Detection of meca and enterotoxin genes in Staphylococcus aureus isolates associated with bovine mastitis and characterization of staphylococcal cassette chromosome mec (sccmec) in mrsa strains. Iran J Microbiol. 2015;7(3):161. [PMC free article] [PubMed] [Google Scholar]

[bib157] 157.Jamali H., Radmehr B., Ismail S. Prevalence and antibiotic resistance of Staphylococcus aureus isolated from bovine clinical mastitis. J Dairy Sci. 2014;97(4):2226–2230. doi: 10.3168/jds.2013-7509. [DOI] [PubMed] [Google Scholar]

[bib158] 158.Khazaie F., Ahmadi E. Bovine subclinical mastitis-associated methicillin-resistant Staphylococcus aureus, selective genotyping and antimicrobial susceptibility profile of the isolates in Kurdistan province of Iran. Iran J Microbiol. 2021;13(1):65. doi: 10.18502/ijm.v13i1.5494. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib159] 159.Khoramrooz S.S., Mansouri F., Marashifard M., Hosseini S.A.A.M., Chenarestane-Olia F.A., Ganavehei B., Gharibpour F., Shahbazi A., Mirzaii M., Darban-Sarokhalil D. Detection of biofilm related genes, classical enterotoxin genes and agr typing among Staphylococcus aureus isolated from bovine with subclinical mastitis in southwest of Iran. Microb Pathog. 2016;97:45–51. doi: 10.1016/j.micpath.2016.05.022. [DOI] [PubMed] [Google Scholar]

[bib160] 160.Mohsenzadeh M., Ghazvini K., Azimian A. In frequency of specific agr groups and antibiotic resistance in Staphylococcus aureus isolated from bovine mastitis in the northeast of Iran. Vet Res Forum. 2015:295. [PMC free article] [PubMed] [Google Scholar]

[bib161] 161.Pourtaghi H., Azizi A.G., Sodagari H. Antimicrobial resistance patterns of Staphylococcus aureus isolated from bovine subclinical mastitis in Alborz province, Iran. Bulg J Vet Med. 2016;19(2):169–174. [Google Scholar]

[bib162] 162.Saei H.D. Coa types and antimicrobial resistance profile of Staphylococcus aureus isolates from cases of bovine mastitis. Comp Clin Pathol. 2012;21(3):301–307. [Google Scholar]

[bib163] 163.Maisano A., Luini M., Gazzola A., Sala L., Vezzoli F., Bertocchi L., Lorenzi V., Cremonesi P., Castiglioni B., Bergagna S. Staphylococcus aureus adlb gene is associated with high prevalence of intramammary infection in dairy herds of northern Italy: a cross-sectional study. J Dairy Sci. 2023;106(5):3421–3435. doi: 10.3168/jds.2022-22496. [DOI] [PubMed] [Google Scholar]

[bib164] 164.Hata E. Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus new York/Japan clone. J Vet Diagn Invest. 2016;28(3):291–298. doi: 10.1177/1040638716643126. [DOI] [PubMed] [Google Scholar]

[bib165] 165.Alekish M., Al-Qudah K., Al-Saleh A. Prevalence of antimicrobial resistance among bacterial pathogens isolated from bovine mastitis in northern Jordan. Rev Med Vet. 2013;164(6):319–326. [Google Scholar]

[bib166] 166.Ismail Z.B. Molecular characteristics, antibiogram and prevalence of multi-drug resistant Staphylococcus aureus (mdrsa) isolated from milk obtained from culled dairy cows and from cows with acute clinical mastitis. Asian Pac J Trop Biomed. 2017;7(8):694–697. [Google Scholar]

[bib167] 167.Baymenov B.M., Bulashev A.K., Chuzhebayeva G.D., Aliyeva G.K., Beishova I.S., Kokanov S.K., Raketsky V.A. Phenotypic and genotypic resistance to antibiotics in Staphylococcus aureus strains isolated from cattle milk in northern Kazakhstan. Vet World. 2023;16(9):1815. doi: 10.14202/vetworld.2023.1815-1820. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib168] 168.Rychshanova R., Mendybayeva A., Miciński B., Mamiyev N., Shevchenko P., Bermukhametov Z., Orzechowski B., Miciński J. Antibiotic resistance and biofilm formation in Staphylococcus aureus isolated from dairy cows at the stage of subclinical mastitis in northern Kazakhstan. Arch Anim Breed. 2022;65(4):439–448. doi: 10.5194/aab-65-439-2022. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib169] 169.Mbindyo C.M., Gitao G.C., Mulei C.M. Prevalence, etiology, and risk factors of mastitis in dairy cattle in Embu and Kajiado counties, Kenya. Vet Med Int. 2020;2020(1) doi: 10.1155/2020/8831172. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib170] 170.Mbindyo C.M., Gitao G.C., Plummer P.J., Kulohoma B.W., Mulei C.M., Bett R. Antimicrobial resistance profiles and genes of staphylococci isolated from mastitic cow’s milk in Kenya. Antibiotics. 2021;10(7):772. doi: 10.3390/antibiotics10070772. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib171] 171.Michira L., Kagira J., Maina N., Waititu K., Kiboi D., Ongera E., Ngotho M. Prevalence of subclinical mastitis, associated risk factors and antimicrobial susceptibility pattern of bacteria isolated from milk of dairy cattle in Kajiado central sub‐county, Kenya. Vet Med Sci. 2023;9(6):2885–2892. doi: 10.1002/vms3.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib172] 172.Klimiene I., Ruzauskas M., Spakauskas V., Matusevicius A., Mockeliunas R., Pereckiene A., Butrimaite-Ambrozeviciene C., Virgailis M. Antimicrobial resistance patterns to beta-lactams of gram-positive cocci isolated from bovine mastitis in Lithuania. Pol J Vet Sci. 2011;14(3) doi: 10.2478/v10181-011-0069-9. [DOI] [PubMed] [Google Scholar]

[bib173] 173.Saeed S.I., Mat Yazid K.A., Hashimy H.A., Dzulkifli S.K., Nordin F., Nik Him N.A., Omar M.F.F.b., Aklilu E., Mohamad M., Zalati C.W.S. Prevalence, antimicrobial resistance, and characterization of Staphylococcus aureus isolated from subclinical bovine mastitis in east Coast Malaysia. Animals. 2022;12(13):1680. doi: 10.3390/ani12131680. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib174] 174.Aguirre-Sánchez J.R., Castro-del Campo N., Medrano-Félix J.A., Martínez-Torres A.O., Chaidez C., Querol-Audi J., Castro-del Campo N. Genomic insights of S. Aureus associated with bovine mastitis in a high livestock activity region of Mexico. J Vet Sci. 2024;25(4):e42. doi: 10.4142/jvs.23286. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib175] 175.Greening S.S., Zhang J., Midwinter A.C., Wilkinson D.A., McDougall S., Gates M.C., French N.P. The genetic relatedness and antimicrobial resistance patterns of mastitis-causing Staphylococcus aureus strains isolated from New Zealand dairy cattle. Vet Sci. 2021;8(11):287. doi: 10.3390/vetsci8110287. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib176] 176.Petrovski K., Laven R., Lopez-Villalobos N. A descriptive analysis of the antimicrobial susceptibility of mastitis-causing bacteria isolated from samples submitted to commercial diagnostic laboratories in New Zealand (2003–2006) N Z Vet J. 2011;59(2):59–66. doi: 10.1080/00480169.2011.552853. [DOI] [PubMed] [Google Scholar]

[bib177] 177.Antók F.I., Mayrhofer R., Marbach H., Masengesho J.C., Keinprecht H., Nyirimbuga V., Fischer O., Lepuschitz S., Ruppitsch W., Ehling-Schulz M. Characterization of antibiotic and biocide resistance genes and virulence factors of staphylococcus species associated with bovine mastitis in Rwanda. Antibiotics. 2019;9(1):1. doi: 10.3390/antibiotics9010001. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib178] 178.Garmo R.T., Waage S., Sviland S., Henriksen B.I., Østerås O., Reksen O. Reproductive performance, udder health, and antibiotic resistance in mastitis bacteria isolated from Norwegian red cows in conventional and organic farming. Acta Vet Scand. 2010;52(1):11. doi: 10.1186/1751-0147-52-11. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib179] 179.Ahmed A., Ijaz M., Khan J.A., Anjum A.A. Molecular characterization and therapeutic insights into biofilm positive Staphylococcus aureus isolated from bovine subclinical mastitis. Pak Vet J. 2022;42(4) [Google Scholar]

[bib180] 180.Haq I.U., Kamal M., Swelum A.A., Khan S., Ríos-Escalante P.R.D.l., Usman T. Alarming multidrug resistance in Staphylococcus aureus isolated from raw milk of cows with subclinical mastitis: antibiotic resistance patterns and occurrence of selected resistance genes. PLoS One. 2024;19(5) doi: 10.1371/journal.pone.0301200. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib181] 181.Ijaz M., Ghumman N.Z., Javed M.U., Ahmed A., Rasheed H., Anwaar F., Sabir M.J., Muzammil I. Genotypic insights to panton–valentine leukocidin positive methicillin-resistant Staphylococcus aureus isolated from cattle mastitis. J Dairy Res. 2024;91(2):211–213. doi: 10.1017/S0022029924000244. [DOI] [PubMed] [Google Scholar]

[bib182] 182.Shah A.U., Ali Khan J., Avais M., Zaman S.H., Munir Z., Abbas S., Tariq M., Rahman M.u., Tariq F., Nawaz S. Prevalence and chemotherapy of Staphylococcus aureus mastitis in dairy cattle. PLoS One. 2025;20(2) doi: 10.1371/journal.pone.0315480. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib183] 183.Shahid M., Hussain R., Nawaz Z., Aslam B., Ahmad M.Z., Siddique A.B., Ahsan H., Fatima A., Khan I., Mustafa B. Occurrence of virulence genes among methicillin-resistant Staphylococcus aureus isolated from subclinical bovine mastitis. ACS Omega. 2023;8(41):38111–38117. doi: 10.1021/acsomega.3c04206. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib184] 184.Shahzad M.A., Yousaf A., Ahsan A., Irshad H., Riaz A., Khan A., Ullah I., Sattar S., Bostan N., Javed S. Virulence and resistance profiling of Staphylococcus aureus isolated from subclinical bovine mastitis in the Pakistani pothohar region. Sci Rep. 2024;14(1) doi: 10.1038/s41598-024-65448-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib185] 185.Krukowski H., Bakuła Z., Iskra M., Olender A., Bis-Wencel H., Jagielski T. The first outbreak of methicillin-resistant Staphylococcus aureus in dairy cattle in Poland with evidence of on-farm and intrahousehold transmission. J Dairy Sci. 2020;103(11):10577–10584. doi: 10.3168/jds.2020-18291. [DOI] [PubMed] [Google Scholar]

[bib186] 186.Szweda P., Schielmann M., Frankowska A., Kot B., Zalewska M. Antibiotic resistance in Staphylococcus aureus strains isolated from cows with mastitis in eastern Poland and analysis of susceptibility of resistant strains to alternative nonantibiotic agents: lysostaphin, nisin and polymyxin b. J Vet Med Sci. 2014;76(3):355–362. doi: 10.1292/jvms.13-0177. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib187] 187.Alharbi A., Al-Dubaib M., Saeed E.M., Elbehiry A. 2021. Comparison of maldi-tof mass spectrometry with phenotypic methods for identification and characterization of Staphylococcus aureus causing mastitis. [DOI] [PubMed] [Google Scholar]

[bib188] 188.Bujňáková D., Karahutová L. Molecular characteristics and antibiotic resistance of Staphylococcus aureus and Staphylococcus haemolyticus isolated from bovine mastitis. Res Vet Sci. 2024;177 doi: 10.1016/j.rvsc.2024.105365. [DOI] [PubMed] [Google Scholar]

[bib189] 189.Kang H.J., You J.-Y., Hong S., Moon J.-S., Kim H.-Y., Choi J.-H., Kim J.-M., Lee Y.J., Kang H.-M. Prevalence of pathogens and antimicrobial resistance of isolated staphylococcus spp. in bovine mastitis milk in South Korea, 2018–2022. J Vet Med Sci. 2024;86(12):1219–1226. doi: 10.1292/jvms.24-0239. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib190] 190.Nam H.-M., Lee A.-L., Jung S.-C., Kim M.-N., Jang G.-C., Wee S.-H., Lim S.-K. Antimicrobial susceptibility of Staphylococcus aureus and characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitis in Korea. Foodborne Pathog Dise. 2011;8(2):231–238. doi: 10.1089/fpd.2010.0661. [DOI] [PubMed] [Google Scholar]

[bib191] 191.Song J.W., Yang S.J., Shin S., Seo K.S., Park Y.H., Park K.T. Genotypic and phenotypic characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitic milk in Korea. J Food Protect. 2016;79(10):1725–1732. doi: 10.4315/0362-028X.JFP-16-067. [DOI] [PubMed] [Google Scholar]

[bib192] 192.Ranasinghe R., Deshapriya R., Abeygunawardana D., Rahularaj R., Dematawewa C. Subclinical mastitis in dairy cows in major milk-producing areas of Sri Lanka: prevalence, associated risk factors, and effects on reproduction. J Dairy Sci. 2021;104(12):12900–12911. doi: 10.3168/jds.2021-20223. [DOI] [PubMed] [Google Scholar]

[bib193] 193.Duse A., Persson-Waller K., Pedersen K. Microbial aetiology, antibiotic susceptibility and pathogen-specific risk factors for udder pathogens from clinical mastitis in dairy cows. Animals. 2021;11(7):2113. doi: 10.3390/ani11072113. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib194] 194.Woudstra S., Wente N., Zhang Y., Leimbach S., Gussmann M., Kirkeby C., Krömker V. Strain diversity and infection durations of staphylococcus spp. and streptococcus spp. causing intramammary infections in dairy cows. J Dairy Sci. 2023;106(6):4214–4231. doi: 10.3168/jds.2022-22942. [DOI] [PubMed] [Google Scholar]

[bib195] 195.Chu C., Wei Y., Chuang S.-T., Yu C., Changchien C.-H., Su Y. Differences in virulence genes and genome patterns of mastitis-associated Staphylococcus aureus among goat, cow, and human isolates in Taiwan. Foodborne Pathog Dise. 2013;10(3):256–262. doi: 10.1089/fpd.2012.1278. [DOI] [PubMed] [Google Scholar]

[bib196] 196.Intrakamhaeng M., Komutarin T. Antibiotics resistance and rapd-pcr typing of multidrug resistant mrsa isolated from bovine mastitis cases in Thailand. Sci Asia. 2012;38:30–35. [Google Scholar]

[bib197] 197.Pumipuntu N., Tunyong W., Chantratita N., Diraphat P., Pumirat P., Sookrung N., Chaicumpa W., Indrawattana N. Staphylococcus spp. associated with subclinical bovine mastitis in central and northeast provinces of Thailand. PeerJ. 2019;7 doi: 10.7717/peerj.6587. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib198] 198.Aslantaş Ö., Demir C. Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. J Dairy Sci. 2016;99(11):8607–8613. doi: 10.3168/jds.2016-11310. [DOI] [PubMed] [Google Scholar]

[bib199] 199.Aslantas Ö., Öztürk F., Ceylan A. Prevalence and molecular mechanism of macrolide and lincosamide resistance in staphylococci isolated from subclinical bovine mastitis in Turkey. J Vet Med Sci. 2011;73(12):1645–1648. doi: 10.1292/jvms.11-0003. [DOI] [PubMed] [Google Scholar]

[bib200] 200.Cengiz S., Dinc G., Cengiz M. Evaluation of antimicrobial resistance in staphylococcus spp. isolated from subclinical mastitis in cows. Pak Vet J. 2015;35(3) [Google Scholar]

[bib201] 201.Hande G., Arzu F., Nilgün G., Serhat A.S., Alper Ç., Ece K., Serhat A., Murat F. Investigation on the etiology of subclinical mastitis in Jersey and hybrid Jersey dairy cows. Acta Vet. 2015;65(3) [Google Scholar]

[bib202] 202.Ikiz S., Başaran B., Bingol E.B., Cetin O., Kasikci G., Ozgur N.Y., Ucmak M., Yilmaz O., Gunduz M.C., Sabuncu A. Presence and antibiotic susceptibility patterns of contagious mastitis agents (Staphylococcus aureus and Streptococcus agalactiae) isolated from milks of dairy cows with subclinical mastitis. Turk J Vet Anim Sci. 2013;37(5):569–574. [Google Scholar]

[bib203] 203.Elias L., Balasubramanyam A.S., Ayshpur O.Y., Mushtuk I.U., Sheremet N.O., Gumeniuk V.V., Musser J.M., Rogovskyy A.S. Antimicrobial susceptibility of staphylococcus aureus, Streptococcus agalactiae, and Escherichia coli isolated from mastitic dairy cattle in Ukraine. Antibiotics. 2020;9(8):469. doi: 10.3390/antibiotics9080469. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib204] 204.De los Santos R., González-Revello Á., Majul L., Umpiérrez A., Aldrovandi A., Gil A., Hirigoyen D., Zunino P. Subclinical bovine mastitis associated with staphylococcus spp. in eleven Uruguayan dairy farms. J Infect Dev Ctries. 2022;16(4):630–637. doi: 10.3855/jidc.12960. [DOI] [PubMed] [Google Scholar]

[bib205] 205.Abdi R.D., Gillespie B.E., Ivey S., Pighetti G.M., Almeida R.A., Kerro Dego O. Antimicrobial resistance of major bacterial pathogens from dairy cows with high somatic cell count and clinical mastitis. Animals. 2021;11(1):131. doi: 10.3390/ani11010131. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib206] 206.Anderson K., Lyman R., Moury K., Ray D., Watson D., Correa M. Molecular epidemiology of Staphylococcus aureus mastitis in dairy heifers. J Dairy Sci. 2012;95(9):4921–4930. doi: 10.3168/jds.2011-4913. [DOI] [PubMed] [Google Scholar]

[bib207] 207.Sun W., Liu J., Li S., Zhu X., Wu X., Dou B., Pang X., Tian K., Wang P., Hao H. Antimicrobial resistance and molecular characteristics of bovine mastitis-associated methicillin-resistant staphylococcus aureus: potential for cross-species transmission of st59-mrsa. Microbiol Spectr. 2025 doi: 10.1128/spectrum.02800-24. e02800-02824. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib208] 208.Thomas A., Chothe S., Byukusenge M., Mathews T., Pierre T., Kariyawasam S., Luley E., Kuchipudi S., Jayarao B. Prevalence and distribution of multilocus sequence types of Staphylococcus aureus isolated from bulk tank milk and cows with mastitis in Pennsylvania. PLoS One. 2021;16(3) doi: 10.1371/journal.pone.0248528. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib209] 209.Son H.M., Duc H.M. Prevalence and phage-based biocontrol of methicillin-resistant Staphylococcus aureus isolated from raw milk of cows with subclinical mastitis in Vietnam. Antibiotics. 2024;13(7):638. doi: 10.3390/antibiotics13070638. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib210] 210.Ramasamy T., Keerthana S., Srinivasan M., Chandrasekar D., Porteen K., Borthakur A., Elamaran A., Sriram P. 2021. Molecular characterization of antibiotic resistance gene pattern of Staphylococcus aureus and Escherichia coli in mastitis affected dairy cows. [Google Scholar]

[bib211] 211.Wang K., Cha J., Liu K., Deng J., Yang B., Xu H., Wang J., Zhang L., Gu X., Huang C., Qu W. The prevalence of bovine mastitis-associated Staphylococcus aureus in China and its antimicrobial resistance rate: a meta-analysis. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.1006676. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib212] 212.Zaatout N., Hezil D. A meta-analysis of the global prevalence of methicillin-resistant Staphylococcus aureus (mrsa) isolated from clinical and subclinical bovine mastitis. J Appl Microbiol. 2022;132(1):140–154. doi: 10.1111/jam.15192. [DOI] [PubMed] [Google Scholar]

[bib213] 213.Khanal S., Boonyayatra S., Awaiwanont N. Prevalence of methicillin-resistant Staphylococcus aureus in dairy farms: a systematic review and meta-analysis. Front Vet Sci. 2022;9 doi: 10.3389/fvets.2022.947154. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib214] 214.Dobrut A., Siemińska I., Sroka-Oleksiak A., Drożdż K., Sobońska J., Mroczkowska U., Brzychczy-Włoch M. Molecular and phenotypic identification of bacterial species isolated from cows with mastitis from three regions of Poland. BMC Vet Res. 2024;20(1):193. doi: 10.1186/s12917-023-03869-w. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib215] 215.Krishnamoorthy P., Suresh K.P., Jayamma K.S., Shome B.R., Patil S.S., Amachawadi R.G. An understanding of the global status of major bacterial pathogens of milk concerning bovine mastitis: a systematic review and meta-analysis (scientometrics) Pathogens. 2021;10(5):545. doi: 10.3390/pathogens10050545. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib216] 216.Abebe R., Hatiya H., Abera M., Megersa B., Asmare K. Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at hawassa milk shed, south Ethiopia. BMC Vet Res. 2016;12(1):270. doi: 10.1186/s12917-016-0905-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib217] 217.Rychshanova R., Mendybayeva A., Miciński B., Mamiyev N., Shevchenko P., Bermukhametov Z., Orzechowski B., Miciński J. Antibiotic resistance and biofilm formation in Staphylococcus aureus isolated from dairy cows at the stage of subclinical mastitis in northern Kazakhstan. Arch Anim Breed. 2022;65(4):439–448. doi: 10.5194/aab-65-439-2022. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib218] 218.Fidelis C.E., Orsi A.M., Freu G., Gonçalves J.L., Santos M.V.D. Biofilm formation and antimicrobial resistance of Staphylococcus aureus and Streptococcus uberis isolates from bovine mastitis. Vet Sci. 2024;11(4) doi: 10.3390/vetsci11040170. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib219] 219.Essack S. Water, sanitation and hygiene in national action plans for antimicrobial resistance. Bull World Health Organ. 2021;99(8):606. doi: 10.2471/BLT.20.284232. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib220] 220.Muinde P., Maina J., Momanyi K., Yamo V., Mwaniki J., Kiiru J. Antimicrobial resistant pathogens detected in raw pork and poultry meat in retailing outlets in Kenya. Antibiotics. 2023;12(3):613. doi: 10.3390/antibiotics12030613. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib221] 221.Founou R.C., Blocker A.J., Noubom M., Tsayem C., Choukem S.P., Dongen M.V., Founou L.L. The covid-19 pandemic: a threat to antimicrobial resistance containment. Future Sci OA. 2021;7(8) doi: 10.2144/fsoa-2021-0012. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib222] 222.Tang K.W.K., Millar B.C., Moore J.E. Antimicrobial resistance (amr) Br J Biomed Sci. 2023;80 doi: 10.3389/bjbs.2023.11387. 11387. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib223] 223.Türkyılmaz S., Tekbıyık S., Oryasin E., Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin‐resistant Staphylococcus aureus isolated from bovine milk. Zoonos Publ Health. 2010;57(3):197–203. doi: 10.1111/j.1863-2378.2009.01257.x. [DOI] [PubMed] [Google Scholar]

[bib224] 224.Dagnaw M., Bazezew M., Mengistu B., Anagaw B., Mebratu A.S. Rate of beta-lactam resistance and epidemiological features of S. Aureus-associated bovine mastitis in cross-bred Ethiopian cows: systematic review. Vet Med Res Rep. 2024;15(null):39–55. doi: 10.2147/VMRR.S415339. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib225] 225.Pérez V.K.C., Custódio D.A.C., Silva E.M.M., de Oliveira J., Guimarães A.S., Brito M.A.V.P., Souza-Filho A.F., Heinemann M.B., Lage A.P., Dorneles E.M.S. Virulence factors and antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis in Brazil. Braz J Microbiol. 2020;51(4):2111–2122. doi: 10.1007/s42770-020-00363-5. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib226] 226.Saini V., McClure J.T., Scholl D.T., DeVries T.J., Barkema H.W. Herd-level association between antimicrobial use and antimicrobial resistance in bovine mastitis Staphylococcus aureus isolates on Canadian dairy farms. J Dairy Sci. 2012;95(4):1921–1929. doi: 10.3168/jds.2011-5065. [DOI] [PubMed] [Google Scholar]

[bib227] 227.Sharifi A., Sobhani K., Mahmoudi P. A systematic review and meta-analysis revealed a high-level antibiotic resistance of bovine mastitis Staphylococcus aureus in Iran. Res Vet Sci. 2023;161:23–30. doi: 10.1016/j.rvsc.2023.05.016. [DOI] [PubMed] [Google Scholar]

[bib228] 228.Mulchandani R., Wang Y., Gilbert M., Van Boeckel T.P. Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Publ Health. 2023;3(2) doi: 10.1371/journal.pgph.0001305. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib229] 229.Peng M., Salaheen S., Biswas D. Animal health: global antibiotic issues. Encyclop Agri Food Syst. 2014:346–357. doi: 10.1016/B978-0-444-52512-3.00187-X. Epub 2014 Aug 21. [DOI] [Google Scholar]

[bib230] 230.Kernodle D.S. Gram‐positive pathogens. 2006. Mechanisms of resistance to β-lactam antibiotics; pp. 769–781. [Google Scholar]

[bib231] 231.Fergestad M.E., Stamsås G.A., Morales Angeles D., Salehian Z., Wasteson Y., Kjos M. Penicillin-binding protein pbp2a provides variable levels of protection toward different β-lactams in Staphylococcus aureus rn4220. Microbiologyopen. 2020;9(8) doi: 10.1002/mbo3.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib232] 232.Cattoir V., Leclercq R. In: Antimicrobial drug resistance: mechanisms of drug resistance, volume 1. Mayers D.L., Sobel J.D., Ouellette M., Kaye K.S., Marchaim D., editors. Springer International Publishing; Cham: 2017. Resistance to macrolides, lincosamides, and streptogramins; pp. 269–280. [Google Scholar]

[bib233] 233.Guo Y., Huang C., Su H., Zhang Z., Chen M., Wang R., Zhang D., Zhang L., Liu M. Luteolin increases susceptibility to macrolides by inhibiting msra efflux pump in Trueperella pyogenes. Vet Res. 2022;53(1):3. doi: 10.1186/s13567-021-01021-w. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib234] 234.Noguchi N., Takada K., Katayama J., Emura A., Sasatsu M. Regulation of transcription of the mph (a) gene for macrolide 2′-phosphotransferase i in escherichia coli: characterization of the regulatory gene mphr (a) J Bacteriol. 2000;182(18):5052–5058. doi: 10.1128/jb.182.18.5052-5058.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib235] 235.Huang L., Wu C., Gao H., Xu C., Dai M., Huang L., Hao H., Wang X., Cheng G. Bacterial multidrug efflux pumps at the frontline of antimicrobial resistance: an overview. Antibiotics. 2022;11(4):520. doi: 10.3390/antibiotics11040520. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib236] 236.Connell Sean R., Tracz Dobryan M., Nierhaus Knud H., Taylor Diane E. Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob Agents Chemother. 2003;47(12):3675–3681. doi: 10.1128/aac.47.12.3675-3681.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib237] 237.Saccone S., Brancato D., Bruno F., Coniglio E., Sturiale V., Federico C. Origin and evolution of genes in eukaryotes: mechanisms, dynamics, and functional implications. Genes. 2025;16(6):702. doi: 10.3390/genes16060702. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib238] 238.Tokuda M., Shintani M. Microbial evolution through horizontal gene transfer by Mobile genetic elements. Microb Biotechnol. 2024;17(1) doi: 10.1111/1751-7915.14408. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib239] 239.Khedkar S., Smyshlyaev G., Letunic I., Maistrenko Oleksandr M., Coelho Luis P., Orakov A., Forslund S.K., Hildebrand F., Luetge M., Schmidt T.S.B., Barabas O., Bork P. Landscape of Mobile genetic elements and their antibiotic resistance cargo in prokaryotic genomes. Nucleic Acids Res. 2022;50(6):3155–3168. doi: 10.1093/nar/gkac163. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib240] 240.Vrancianu C.O., Popa L.I., Bleotu C., Chifiriuc M.C. Targeting plasmids to limit acquisition and transmission of antimicrobial resistance. Front Microbiol. 2020;11 doi: 10.3389/fmicb.2020.00761. 761. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib241] 241.Partridge Sally R., Kwong Stephen M., Firth N., Jensen Slade O. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev. 2018;31(4) doi: 10.1128/cmr.00088-17. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib242] 242.Gillieatt B.F., Coleman N.V. Unravelling the mechanisms of antibiotic and heavy metal resistance co-selection in environmental bacteria. FEMS (Fed Eur Microbiol Soc) Microbiol Rev. 2024;48(4) doi: 10.1093/femsre/fuae017. [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Staphylococcus aureus in bovine intramammary infections: A global systematic review and meta-analysis of prevalence and antimicrobial resistance patterns

Md Jisan Ahmed

Md Arifur Rahman

Ritu Chalise

Prajwal Bhandari

Md Ismile Hossain Bhuiyan

Md Imran Hossain

Israt Jahan Kaderi

Md Afiqul Islam Rahi

Delower Hossain

Abstract

Background

Objectives

Methods

Results

Conclusion

Highlights

1. Introduction

2. Materials and methods

2.1. Guidelines and protocol

Table 1.

2.2. Systematic literature search strategy

Table 2.

2.3. Inclusion and exclusion criteria

2.4. Data collection and extraction

2.5. Bias assessment and quality evaluation

2.6. Statistical analysis

3. Results

3.1. Search results and eligible studies

Fig. 1.

3.2. Descriptive characteristics of the included studies

Fig. 2.

Fig. 3.

3.3. Meta-analysis of S. aureus

Fig. 4.

3.4. Subgroup meta-analysis

Fig. 5.

Fig. 6.

3.5. Meta-regression

3.6. Publication bias

Fig. 7.

3.7. Trim and fill analysis

Fig. 8.

3.8. Sensitivity analysis

Fig. 9.

3.9. Meta-analysis of AMR carriage

Table 3.

3.10. Geographical AMR patterns of S. aureus and antibiotic classes

Fig. 10.

Fig. 11.

3.11. Genotypic resistance pattern

Fig. 12.

4. Discussion

4.1. Limitations

4.2. Implications

5. Conclusion

CRediT authorship contribution statement

Clinical trial

Availability of data and materials

Ethical approval and consent to participate

Consent for publication

Funding

Declaration of competing interest

Acknowledgments

Footnotes

Contributor Information

Abbreviations

Appendix A. Supplementary data

References

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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