Skip to main content
NCBI home page
Health Science Reports logoLink to Health Science Reports
. 2025 Sep 9;8(9):e71158. doi: 10.1002/hsr2.71158

Prevalence of Salmonella Typhimurium in Foods, Animals, and Human Origin in Iran: A Systematic Review and Meta‐Analysis

Negar Narimisa 1,2, Shabnam Razavi 1,2, Faramarz Masjedian Jazi 1,2,✉
PMCID: PMC12420347  PMID: 40937013

ABSTRACT

Background and Aims

Salmonella enterica is a globally significant foodborne pathogen, with Typhimurium being one of the most prevalent serotypes linked to foodborne illnesses. Despite its importance, there is a notable absence of meta‐analytical studies examining the prevalence of this bacterium in Iran. This meta‐analysis aims to assess the prevalence of S. Typhimurium in food, animals, and human populations in Iran.

Methods

Studies on the prevalence of S. Typhimurium published from 1936 to December 2023 were gathered from databases including PubMed, Scopus, Web of Science, and SID. The data collected were analyzed using Stata software.

Results

A total of 52 studies met the inclusion criteria for the analysis of S. Typhimurium prevalence in clinical and environmental isolates in Iran. The overall prevalence of S. Typhimurium in total isolates from food, animals, and human sources was determined to be 4% (95% CI: 3%–6%). Additionally, the analysis revealed a nearly stable trend in the prevalence of S. Typhimurium over the years.

Conclusion

The relatively high prevalence of S. Typhimurium in animal isolates underscores the necessity for implementing stricter infection control measures. Furthermore, it is essential to establish appropriate diagnostic criteria and management guidelines for screening this pathogen across various sample types to mitigate its spread.

Keywords: databases, Iran, meta‐analysis, prevalence, Salmonella Typhimurium

1. Introduction

Salmonella is a Gram‐negative facultative anaerobic bacterium that belongs to the Enterobacteriaceae family. While Salmonella species are widespread in the environment, their main habitat is the intestinal tract of animals [1, 2]. Salmonella is an important foodborne pathogen that is estimated to cause 115 million human infections and 370,000 deaths globally each year [3, 4]. Infections can occur through the consumption of contaminated food (such as eggs, milk, and poultry) or water, contact with infected animals, or international food trade. The burden of infectious diseases extends beyond morbidity and mortality in humans and animals, also affecting trade and causing socioeconomic problems [5, 6]. Infected animals may exhibit a range of symptoms, from mild gastroenteritis to severe cases that could ultimately result in death [7].

The genus Salmonella consists of two species: S. enterica (with six subspecies) and S. bongori (non‐subspecies). Salmonella enterica is composed of six subspecies: S. enterica subsp. enterica, S. enterica subsp. salamae, S. enterica subsp. arizonae, S. enterica subsp. diarizonae, S. enterica subsp. houtenae, and S. enterica subsp. indica [8]. The most clinically significant subspecies is S. enterica subspecies Enterica, which can cause infection in humans and warm‐blooded animals. It includes approximately 1500 serovars, all of which have the potential to be pathogenic to humans. Among these serovars, approximately 80 serovars are responsible for around 99% of Salmonella infections in humans and animals [9, 10].

Non‐typhoidal Salmonella such as Salmonella enterica serotype Typhimurium is a significant enteric infection in humans, especially among neonates and young children [11]. The morbidity and mortality associated with Salmonella infections pose a considerable burden in both developing and developed nations [12]. The rise of antibiotic‐resistant foodborne pathogens has heightened public concern, as these strains exhibit increased virulence, leading to higher mortality rates among affected individuals [13].

Salmonella enterica serovar Enteritidis and serovar Typhimurium are the predominant agents responsible for non‐typhoidal salmonellosis in humans. Serovar Typhimurium is now recognized as one of the most prevalent Salmonella serotypes linked to human infections [14, 15]. In Europe, it ranks as the most frequently identified serovar among isolates from humans, pigs, and pork. Conversely, in the United States, it is among the top five serovars associated with human cases of salmonellosis [16, 17, 18].

Despite improvements in food hygiene and safety standards, infections caused by this bacterium remain a common public health problem worldwide [19]. Therefore, this study aims to analyze the prevalence of S. Typhimurium isolated from animals, food, and humans in Iran using a meta‐analysis approach. The results of this study can help to understand the prevalence and origin of S. Typhimurium in Iran, which in turn can be useful for eradicating and preventing diseases caused by S. Typhimurium.

2. Material and Method

2.1. Search Strategies

A systematic literature search was performed across Web of Science, PubMed, Scopus, and SID, covering the period from 1936 to December 2023. The search strategy employed the terms (“Salmonella Typhimurium” OR “S. Typhimurium”) AND (Iran). This review was carried out and reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta‐Analyzes (PRISMA) guidelines [20]. All identified articles were compiled using EndNote X20 Citation Manager Software, and duplicates were eliminated before the review process. The remaining citations were subsequently uploaded to Rayyan, a citation classification application [21].

2.2. Eligibility Criteria

Two reviewers independently evaluated titles, abstracts, and full texts to identify studies that met the inclusion criteria. Any discrepancies were resolved through consensus.

The studies included in this review were selected based on the following criteria: (1) Original articles reporting the prevalence of S. Typhimurium isolates in food, animal, and human samples, either relative to the total isolates or the total Salmonella serotypes identified; (2) studies conducted in Iran; and (3) studies published in either Persian or English.

Studies were excluded based on the following criteria: (1) studies that did not provide the exact number of S. Typhimurium isolates; (2) duplicate reports; (3) review; (4) case reports; (5) clinical trial studies; (6) short communications; (7) conference papers; (8) letters; (9) book chapters; and (10) studies published in languages other than English or Persian.

2.3. Quality Assessment

The quality of eligible studies was assessed independently by two authors using the prevalence Joanna Briggs Institute (JBI) Critical Appraisal Checklist [15]. This checklist comprises nine questions that evaluate research quality, focusing on appropriate sampling techniques, research objectives, and data analysis methods. Each item is rated as “yes,” “no,” or “unclear.” A “yes” response receives a score of 1 point, while “no” or “unclear” responses receive 0 points. The average score for each paper was assessed independently by two reviewers, with any disagreements resolved through consensus or discussion with a third author. Studies scoring 7 or higher were classified as high quality, those scoring between 5 and 7 as medium quality, and studies scoring 4 or lower as low quality.

2.4. Data Extraction

For each included study, the following details were extracted: the first author's name, publication year, sample size, source of isolation, method of S. Typhimurium detection, and the province and regions from which the isolates were collected (Table 1). To estimate the overall prevalence through meta‐analysis, we utilized the “metaprop” package in STATA version 17.0 (STATA, College Station, TX, USA) [7]. The pooled prevalence of S. Typhimurium across various samples, alongside a 95% confidence interval, was calculated using the Freeman‐Tukey double arcsine transformation within a random‐effects model.

Table 1.

Characteristics of included studies.

First author Quality Publication year Province Region Source Origin Method Total Salmonella Salmonella Typhimurium
Moosavy [22] 8 2015 East Azarbayjan Northwest Food Egg Multiplex PCR 150 2 1
Nosrati [23] 8 2012 Tehran Center Meat Food (cow meat) PCR 170 3 2
Basti [24] 7 2004 Animal Fish Serologically 120 5 1
Jamshidi [25] 8 2008 Khorasan Northeast Animal Poultry carcasses Multiplex PCR 60 5 1
Ranjbari [26] 8 2015 Fars Center Food Duck eggs and turkey PCR 300 7 7
Tajbakhsh [27] 7 2015 Chaharmahal va Bakhtiari Southwest Food Food (Processed food) PCR 50 9 1
Askari [28] 9 2020 Tehran Center Animal Dog PCR 200 11 7
Karimi [29] 8 2013 Kurdistan Northwest Meat Meat (cow) Multiplex PCR 60 12 4
Asma Afshari [30] 6 2017 Khorasan Northeast Animal Broiler Multiplex PCR 100 14 5
Monadim [31] 6 2014 Kohgiluyeh and Boyer‐Ahmad Southwest Food Egg Multiplex PCR 210 14 12
Zare [32] 5 2015 East Azarbayjan Northwest Animal Domestic Serologically 250 15 5
STAJI [33] 8 2017 Semnan Center Animal Duck Multiplex PCR 247 18 10
Rahimi [34] 7 2011 Animal Seafood Serologically 384 19 4
Tajbakhsh [35] 8 2013 Chaharmahal va Bakhtiari Southwest Animal Cow, Sheep and Goat's Milk PCR 1100 20 7
Khakrizi [36] 8 2022 Tehran Center Animal Pet dogs Serologically 256 21 4
Nazari [37] 7 2017 Meat Camel meat PCR 150 22 3
Bokaeian [38] 5 2006 Sistan and Baluchestan Southeast Animal Chicken (skin, meat,.) Serologically 250 28 4
Momtaz [39] 7 2014 Chaharmahal va Bakhtiari Southwest Meat poultry meat PCR 620 28 12
Manafi [40] 9 2020 West Azerbaijan Northwest Meat Meat Multiplex PCR 120 29 3
Moghadam [41] 7 2022 Alborz Center Animal livestock Serologically 30 4
Salehi [42] 8 2006 Animal Bovine Serologically 400 33 22
Moghadam [43] 9 2023 Chaharmahal va Bakhtiari Southwest Meat Poultry meat Multiplex PCR 400 36 36
Namroodi [44] 5 2016 Animal Dog Serologically 210 40 14
Shimi [45] 6 1997 Animal Cat Serologically 301 42 16
Firouzabadi [46] 8 2019 Kerman Southeast Animal Broiler chickens PCR 110 53 26
Akbarmehr [47] 7 2010 East Azarbayjan Northwest Animal Poultry Multiplex PCR 634 58 13
Firoozeh [48] 8 2011 Tehran Center Human Human Multiplex PCR 58 5
Fardsanei [49] 8 2021 Human Human Multiplex PCR 2116 59 11
Siasi [50] 8 2020 Tehran Center Human Human Serologically 676 60 30
Ranjbar [51] 7 2017 Tehran Center Human Human Serologically 68 21
Ezatpanah [52] 7 2013 Markazi Center Animal Chicken Serologically 245 75 4
Mehrabian [53] 7 2007 Tehran Center Meat Meat Serologically 400 80 12
Bonyadian [54] 6 2006 Yazd Center Animal Chicken carcasses Serologically 435 90 47
Abdollahi [55] 7 2011 Human Human Serologically 96 35
Alzwghaibi [56] 8 2018 Tehran Center Multiplex PCR 100 32
Moghadam [57] 7 2017 Kerman Southeast Human Human PCR 1125 130 29
Ranjbar [58] 6 2011 Tehran Center Human Human Serologically 5900 139 20
Doosti [59] 9 2016 Chaharmahal va Bakhtiari Southwest Animal Poultry Multiplex PCR 300 245 138
Doosti [60] 9 2016 Animal Poultry PCR 600 287 49
Mashouf [61] 5 2007 Hamadan Center Human Human 296 57
MOGHADDAM [62] 6 1990 Tehran Center Human Human Serologically 508 232
Khaltabadi [63] 7 2019 PCR 884 150
Azizpour [64] 8 2021 Ardebil Northwest Meat Chicken Meat PCR 100 1
Dilmaghani [65] 7 2011 Animal Avians Multiplex PCR 1,870 52
Halimi [66] 8 2014 Khorasan Northeast Animal Cow PCR 332 13
JAMSHIDI [67] 7 2010 Khorasan Northeast Food Egg Multiplex PCR 250 4
Keshmiri [68] 9 2022 Serologically 31 11
NAZER [69] 6 1994 Fars Center Food Egg Serologically 100 10
Rahimi [70] 8 2021 Qazvin Center Food Egg Real‐Time PCR 20 4
Ranjbar [71] 6 2013 Tehran Center Human Human Serologically 650 21
Estabergi [72] 7 2020 Food Food Biochemical 138 12
Moghadam [73] 6 2017 Kerman Southeast Human Human PCR 891 48
Open in a new tab

The heterogeneity among the studies included in the meta‐analysis was assessed using the I² statistic. An I² value of ≤ 25% indicates low heterogeneity, values between 25% and 75% indicate moderate heterogeneity, and values exceeding 75% suggest high heterogeneity.

Subgroup analyzes were conducted based on publication year, city of study, source of isolation, type of animal from which the isolate was obtained, and the method used for detecting S. Typhimurium.

To assess publication bias, we utilized funnel plots. This method generates a scatterplot with effect sizes on the horizontal axis and a measure of each study's size on the vertical axis [74]. We also applied Begg's rank correlation test, which evaluates potential publication bias by examining the correlation between the ranks of effect estimates and their variances [75]. Additionally, we employed Egger's regression test, which performs a linear regression of the intervention effect estimates based on their standard errors, weighted by inverse variance. A p‐value of less than 0.05 was deemed indicative of publication bias [76, 77].

Furthermore, we conducted a sensitivity analysis to determine the robustness of the model, checking whether specific studies influenced the results or if other potential sources of bias were present [78].

3. Results

3.1. Search Results

A total of 1105 studies were initially retrieved. After removing duplicates using EndNote software, 655 studies were screened, resulting in a full‐text examination of 83 studies that reported the prevalence of S. Typhimurium. Ultimately, 52 studies met the eligibility criteria and were included in the meta‐analysis.

Figure 1 illustrates the studies selection process in accordance with the Preferred Reporting Items for Systematic Reviews and Meta‐Analyzes (PRISMA) guidelines. Table 1 presents the characteristics of the included studies along with their quality assessment scores. Of the total studies reviewed, 39 were classified as high quality, while 13 were deemed medium quality (Table 1).

Figure 1.

Figure 1

Open in a new tab

The study prisma flow diagram.

3.2. Meta‐Analysis

3.2.1. Prevalence of S. Typhimurium in Total Isolates

This study included 44 studies from 52 included studies reported the prevalence of S. Typhimurium in total isolates. The prevalence of S. Typhimurium in these isolates was 4% (95% CI: 3%–6%; I2 = 95.98%; p < 0.001) (Figure 2).

Figure 2.

Figure 2

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in total isolates.

Funnel plots (Figure 3) showed publication bias for the prevalence result of S. Typhimurium in the total human, food, and animal isolates. Additionally, Begg's and Egger's tests were performed to quantitatively evaluate the publication biases. According to the results of Begg's test (p = 0.0640) and Egger's test (p = 0.0798), a significant publication bias was not observed. The sensitivity analysis indicated that excluding individual literature sources did not significantly alter the pooled effect estimate.

Figure 3.

Figure 3

Open in a new tab

Funnel plot for identification of publication bias about the prevalence of S. Typhimurium in total isolates.

Our meta‐analysis revealed significant heterogeneity in the prevalence of S. Typhimurium among all isolates and Salmonella isolates. Various factors may contribute to this heterogeneity, including sample type, as differences in the types of samples analyzed (human, animal, and food) can influence prevalence due to varying exposure risks and transmission dynamics [79]. Geography also plays a role, with geographic differences in climate, agricultural practices, and public health policies potentially impacting the prevalence of S. Typhimurium. Additionally, population characteristics related to demographic factors can affect prevalence rates through differences in exposure and susceptibility [80, 81]. To further explore these influences, we conducted subgroup analyzes to assess how these variables affect the observed heterogeneity.

3.2.2. Subgroup Meta‐Analysis of Prevalence of S. Typhimurium in Total Isolates

The analysis of S. Typhimurium prevalence over time indicated a nearly constant prevalence of this serovar across various time periods (p = 0.043) (Figure 4).

Figure 4.

Figure 4

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in total isolates across different time intervals.

We categorized the origin of the isolates into samples isolated from humans, animals, meat, and food (including processed foods and eggs).

Twenty‐one studies investigated the spread of S. Typhimurium in animal samples, eight studies focused on food, six studies on humans, and eight studies on meat samples. The highest prevalence was observed in S. Typhimurium isolates from animals at 5% (95% CI 3%–8%), and the lowest in isolates from humans at 2% (95% CI 1%–5%), (p = 0.296) (Figure 5).

Figure 5.

Figure 5

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different sources.

Additionally, the prevalence of S. Typhimurium was analyzed based on the type of animal from which the samples were isolated. Twelve studies investigated the spread of S. Typhimurium in avian samples, two studies focused on bovine samples, three examined dogs, and two explored the presence of the bacteria in sea animals. The results showing that samples isolated from avians had the highest prevalence of S. Typhimurium at 7% (95% CI 3%–12%), (p < 0.001) (Figure 6).

Figure 6.

Figure 6

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different animals.

Thirteen studies have examined the prevalence of S. Typhimurium in central cities of Iran. Additionally, four studies were conducted in the northeastern regions, six in the northwestern regions, four in the southeastern regions, and six in the southwestern regions. The southwestern region of Iran exhibited the highest prevalence of S. Typhimurium, recorded at 8% (95% CI 1%–21%), (p = 0.142) (Figure 7).

Figure 7.

Figure 7

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different regions of Iran.

We also examined the hypothesis that different detection methods could influence the prevalence of S. Typhimurium through subgroup analyzes. Thirteen studies used the multiplex PCR method, while another thirteen employed standard PCR, and sixteen studies utilized serological methods. The multiplex PCR method reported a prevalence of 5% (95% CI 2%–9%), higher than the other methods, although this difference was not statistically significant (p = 0.793) (Figure 8).

Figure 8.

Figure 8

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different detection methods.

3.2.3. Prevalence of S. Typhimurium in Isolated Salmonella Species

Forty‐two studies provided information on the number of S. Typhimurium isolates among the Salmonella species that were isolated. The prevalence of S. Typhimurium was found to be 33% (95% CI: 27%–40%; I2 = 93.09%; p < 0.001) as illustrated in Figure 9. Funnel plots (Figure 10) displayed publication bias for the prevalence result of S. Typhimurium in the Salmonella species.

Figure 9.

Figure 9

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different Salmonella isolates.

Figure 10.

Figure 10

Open in a new tab

Funnel plot for identification of publication bias about the prevalence of S. Typhimurium in different Salmonella isolates.

Furthermore, Begg's and Egger's tests were performed to quantitatively assess publication bias. The results indicated no significant publication bias, with Begg's test yielding a p‐value of 0.0994 and Egger's test a p‐value of 0.1768.

In our articles, funnel plots depict publication bias, while Begg's and Egger's tests show no significant bias. This difference may occur because small studies with large effect sizes can create visual asymmetries that may not be statistically significant [82]. The sensitivity analysis confirmed that the exclusion of individual literature sources did not materially affect the pooled effect estimate.

3.2.4. Subgroup Meta‐Analysis of Prevalence of S. Typhimurium in Isolated Salmonella Species

The analysis of S. Typhimurium prevalence over time indicated a nearly constant prevalence of this serovar across various time periods (p = 0.052) (Figure 11).

Figure 11.

Figure 11

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different Salmonella species isolates across different time intervals.

Twenty‐one studies investigated the prevalence of S. Typhimurium in animal samples, four studies in food, ten studies in humans, and seven studies in meat samples. The highest prevalence was observed in S. Typhimurium isolated from food at 68% (95% CI 16%–100%), and the lowest in isolates isolated from humans at 28% (95% CI 19%–38%) (p = 0.415) as shown in Figure 12.

Figure 12.

Figure 12

Open in a new tab

Forest plot showing the prevalence of S. Typhimurium in different Salmonella isolates in different sources.

4. Discussion

To the best of our knowledge, there are limited systematic reviews investigating the prevalence of S. Typhimurium in Iran. Therefore, we systematically reviewed the published literature and conducted a meta‐analysis to determine the overall prevalence of S. Typhimurium in foods, animals, and humans in Iran.

Recent reports indicate a rising prevalence of Salmonella strains resistant to antimicrobial agents, which is a significant public health concern [83]. The application of antimicrobial agents in various environments creates conditions that favor the survival of antibiotic‐resistant pathogens [84]. The common practice of administering antimicrobial agents to domestic livestock for disease prevention, treatment, and growth promotion significantly contributes to the development of antibiotic‐resistant bacteria, which can then be transmitted to humans through the food chain [85, 86]. Most infections caused by antimicrobial‐resistant S. Typhimurium are linked to the consumption of contaminated animal‐derived foods [87].

Our study revealed that the overall prevalence of S. Typhimurium was 4% in all human and food samples. Furthermore, our analysis indicated that the level of infection with S. Typhimurium in animals was higher than in other samples, highlighting the importance of monitoring animals to prevent infections caused by this bacterium. The prevalence of S. Typhimurium among Salmonella species isolated from different sources was 33%, demonstrating the relatively high prevalence of this serovar among Salmonella species and emphasizing its importance.

A study conducted by Sinwat examined clinical samples from individuals working in the meat‐handling industry in Thailand and the Lao People's Democratic Republic. The findings revealed a concerning prevalence of Salmonella, with 34.6% of samples testing positive in Thailand and 47.4% in the Lao PDR. Further molecular analysis of these isolates identified S. Typhimurium as the predominant serotype, accounting for 34% of isolates in Thailand and 20.6% in the Lao PDR [88]. This highlights a potential risk for Invasive non‐typhoidal Salmonella (iNTS) disease in these regions [88]. In a 6‐year study in Colombia conducted by Rodríguez, 32.5% of S. enterica isolates sourced from blood and fecal samples were identified as S. Typhimurium [89]. Furthermore, literature indicates that S. enterica serovar Typhimurium is frequently linked to iNTS cases in sub‐Saharan Africa, underscoring the global significance of this serotype in public health concerns [90, 91].

Our analysis reveals that S. Typhimurium is the most prevalent serovar among Salmonella species in food samples. Alarmingly, 68% of the contaminated foods tested positive for this serovar. Additionally, 28% of human salmonellosis infections were caused by S. Typhimurium, underscoring the need for proper food screening and hygiene to prevent human infections. A meta‐analysis conducted by Ferrari et al. indicated that serovar Typhimurium is the most common worldwide [16]. Studies also showed that serovar Typhimurium ranks second in prevalence in Europe and third in the United States [92].

According to the predictions by the Organization for Economic Co‐operation and Development and the Food and Agricultural Organization (OECD‐FAO), factors such as low production costs, short production cycles, high feed conversion ratios, and low product prices are the main reasons for choosing poultry meat for producers and consumers [93]. A meta‐analysis by Ferrari et al. showed that serovars Typhimurium and Sofia are the most common serovars in poultry in North America and Oceania [16]. The meta‐analysis conducted by Sun et al. showed that serovar Typhimurium was the third most common serovar isolated from poultry in China, with a prevalence of 9.1% [94]. Paião et al. reported that in Brazil, S. Enteritidis and S. Typhimurium were found in 12% and 3% of broiler chicken samples, respectively [95]. In a study conducted in Turkey, Mutluer et al. found that 27.5% of broiler carcasses were contaminated with Salmonella spp. Among their isolates, serotyping results indicated that 25.5% were identified as S. Typhimurium [96]. Aury et al. investigated Salmonella in turkeys in France, identifying the five most prevalent serotypes: S. Derby (29.2%), S. Enteritidis (11.7%), S. Typhimurium (10.1%), S. Hadar (8.4%), and S. Mbandaka (6.8%) [97]. In a study by Kanaan, 150 raw and frozen poultry meat samples were collected from various retail markets in Iraq. Of these, 19 samples tested positive for Salmonella, with S. Enteritidis accounting for 63.2% and S. Typhimurium for 36.8% [98]. Our study also revealed that among the tested animals, avian had the highest prevalence of Typhimurium serovar at 7%, indicating the need for more effective intervention strategies during processing to control the quality and safety of poultry products in Iran.

In terms of geographical distribution, the prevalence of S. Typhimurium was highest in southwestern region. Farming practices and the presence of infected animals can significantly influence Salmonella prevalence [99]. Additionally, the elevated levels of S. Typhimurium in these areas may be attributed to inadequate sanitation conditions, including the use of contaminated equipment, poor water quality, high humidity in operational areas, personnel hygiene during manual processing, and airborne contamination during slaughter [100, 101]. Therefore, consistent monitoring of S. Typhimurium prevalence and food markets is essential for effective control of salmonellosis in these regions.

This study provides valuable insights into the prevalence of S. Typhimurium; however, it has limitations. These include the geographical dispersion of the included studies, a limited number of studies conducted in specific provinces, and a notable absence of research on the prevalence of this serotype in several provinces of Iran. To address these gaps, we conducted an investigation into the prevalence of S. Typhimurium, aiming to encompass a larger number of studies across five distinct regions of Iran.

In conclusion, our data confirm that S. Typhimurium has a high prevalence in animal and food isolates, and 28% of the Salmonella isolated from humans is Typhimurium. These results highlight the importance of further research to understand the prevalence of this microorganism in different regions, as well as increased monitoring in regions with high prevalence to prevent diseases caused by this bacterium.

Author Contributions

Negar Narimisa: conceptualization, investigation, writing – original draft, writing – review and editing, software. Shabnam Razavi: methodology, validation, visualization, writing – review and editing. Faramarz Masjedian Jazi: data curation, supervision, resources, writing – review and editing.

Ethics Statement

The authors have nothing to report.

Consent

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Transparency Statement

The lead author Faramarz Masjedian Jazi affirms that this article is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.

Acknowledgments

This article was funded by Microbial Biotechnology Research Center (Iran University of Medical Sciences) by a research grant (No. 28076).

Data Availability Statement

The data that supports the findings of this study are available in the supporting material of this article. All the data in this review are included in the article.

References

  • 1. Abulreesh H. H., Salmonellae in the Environment (InTech, 2012). [Google Scholar]
  • 2. Narimisa N., Razavi S., Khoshbayan A., Gharaghani S., and Jazi F. M., “Targeting Lon Protease to Inhibit Persister Cell Formation in Salmonella Typhimurium: A Drug Repositioning Approach,” Frontiers in Cellular and Infection Microbiology 14 (2024): 1427312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Yan S., Zhang W., Li C., et al., “Serotyping, MLST, and Core Genome MLST Analysis of Salmonella Enterica From Different Sources in China During 2004–2019,” Frontiers in Microbiology 12 (2021): 688614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4. Narimisa N., Amraei F., Kalani B. S., and Jazi F. M., “Evaluation of Gene Expression and Protein Structural Modeling Involved in Persister Cell Formation in Salmonella Typhimurium,” Brazilian Journal of Microbiology 52 (2021): 207–217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Gómez‐Aldapa C. A., Torres‐Vitela M. R., Villarruel‐López A., and Castro‐Rosas J., “The Role of Foods in Salmonella Infections,” in Salmonella‐A Dangerous Foodborne Pathogen (2012), 21–46. [Google Scholar]
  • 6. Popa G. L. and Popa M. I., “Salmonella spp. Infection‐A Continuous Threat Worldwide,” Germs 11, no. 1 (2021): 88–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7. Gast R. K. and R. E. Porter, Jr. , “Salmonella Infections,” in Diseases of Poultry (2020), 717–753. [Google Scholar]
  • 8. Pearce M. E., Langridge G. C., Lauer A. C., Grant K., Maiden M. C. J., and Chattaway M. A., “An Evaluation of the Species and Subspecies of the Genus Salmonella With Whole Genome Sequence Data: Proposal of Type Strains and Epithets for Novel S. Enterica Subspecies VII, VIII, IX, X, and XI,” Genomics 113, no. 5 (2021): 3152–3162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Branchu P., Bawn M., and Kingsley R. A., “Genome Variation and Molecular Epidemiology of Salmonella Enterica Serovar Typhimurium Pathovariants,” Infection and Immunity 86, no. 8 (2018): e00079‐18, 10.1128/iai.00079-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10. Sangal V.. Multilocus Sequence Typing Analyses of Salmonella Enterica Subspecies Enterica. 2009.
  • 11. Gal‐Mor O., Boyle E. C., and Grassl G. A., “Same Species, Different Diseases: How and Why Typhoidal and Non‐Typhoidal Salmonella Enterica Serovars Differ,” Frontiers in Microbiology 5 (2014): 391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12. Balasubramanian R., Im J., Lee J.‐S., et al., “The Global Burden and Epidemiology of Invasive Non‐Typhoidal Salmonella Infections,” Human Vaccines and Immunotherapeutics 15, no. 6 (2019): 1421–1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13. Narimisa N., Razavi S., and Masjedian Jazi F., “Prevalence of Antibiotic Resistance in Salmonella Typhimurium Isolates Originating From Iran: A Systematic Review and Meta‐Analysis,” Frontiers in Veterinary Science 11 (2024): 1388790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14. Wagenaar J. A., Hendriksen R. S., and Carrique‐Mas J. J., “Practical Considerations of Surveillance of Salmonella Serovars Other Than Enteridis and Typhimurium: ‐En‐ ‐Fr‐ Considérations Pratiques Sur La Surveillance Des Sérovars De Salmonella Hors Enteritidis Et Typhimurium ‐Es‐ Consideraciones Prácticas En Torno Ala Vigilancia De Serovares De Salmonella Distintos De Enteritidis Y Typhimurium,” Revue Scientifique et Technique de l'OIE 32, no. 2 (2013): 509–519. [DOI] [PubMed] [Google Scholar]
  • 15. Arya G., Holtslander R., Robertson J., et al., “Epidemiology, Pathogenesis, Genoserotyping, Antimicrobial Resistance, and Prevention and Control of Non‐Typhoidal Salmonella Serovars,” Current Clinical Microbiology Reports 4 (2017): 43–53. [Google Scholar]
  • 16. Ferrari R. G., Rosario D. K. A., Cunha‐Neto A., Mano S. B., Figueiredo E. E. S., and Conte‐Junior C. A., “Worldwide Epidemiology of Salmonella Serovars in Animal‐Based Foods: A Meta‐Analysis,” Applied and Environmental Microbiology 85, no. 14 (2019): e00591–19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Naser J. A., Hossain H., Chowdhury M. S. R., et al., “Exploring of Spectrum Beta Lactamase Producing Multidrug‐Resistant Salmonella Enterica Serovars in Goat Meat Markets of Bangladesh,” Veterinary and Animal Science 25 (2024): 100367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18. Rahman M. M., Hossain H., Chowdhury M. S. R., et al., “Molecular Characterization of Multidrug‐Resistant and Extended‐Spectrum β‐lactamases‐producing Salmonella Enterica Serovars Enteritidis and Typhimurium Isolated From Raw Meat In Retail Markets,” Antibiotics (USSR) 13, no. 7 (2024): 586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Popa G. L. and Popa M. I., “Salmonella Spp. Infection ‐ a Continuous Threat Worldwide,” Germs 11, no. 1 (2021): 88–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Page M. J., McKenzie J. E., Bossuyt P. M., et al., “The Prisma 2020 Statement: An Updated Guideline for Reporting Systematic Reviews,” International Journal of Surgery 88 (2021): 105906. [DOI] [PubMed] [Google Scholar]
  • 21. Ouzzani M., Hammady H., Fedorowicz Z., and Elmagarmid A., “Rayyan‐a Web and Mobile App for Systematic Reviews,” Systematic Reviews 5, no. 1 (2016): 210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22. Moosavy M.‐H., Esmaeili S., Bagheri Amiri F., Mostafavi E., and Zahraei Salehi T., “Detection of Salmonella Spp in Commercial Eggs in Iran,” Iranian Journal of Microbiology 7, no. 1 (2015): 50–54. [PMC free article] [PubMed] [Google Scholar]
  • 23. Nosrat A., Azar S., Mehrooz D., Bahman T., and Fatemeh F., “Prevalence of Salmonella Enteritidis, Typhi and Typhimurium From Food Products in Mofid Hospital,” Journal of Research in Medical Sciences 36, no. 1 (2012): 43–48. [Google Scholar]
  • 24. Basti A. A., Salehi T. Z., and Bokaie S., “Some Bacterial Pathogens in the Intestine of Cultivated Silver Carp and Common Carp,” Developments in Food Science 42: Elsevier (2004): 447–451. [Google Scholar]
  • 25. Jamshidi A. E., Basami M., and Afshari N. S. Identification of Salmonella spp. and Salmonella Typhimurium by a Multiplex PCR‐Based Assay From Poultry Carcasses in Mashhad‐Iran. 2009.
  • 26. Ali Ghorbani R., Shahriar N., Abdollah Z., and Nazanin Ghorbani R., “A Study of Salmonella Spp. Contamination in Egg of Ducks and Turkeys, Consumed in Fars Province,” Yafteh 17, no. 1 (2015): 104–109. [Google Scholar]
  • 27. Elaheh T. and Manouchehr M., “Detection of Staphylococcus Areus and Salmonella Typimurium in Traditional and Industrial Olivie Salads in Shahrekord City,” Journal of Food Microbiology 2, no. 1 (2015): 39–48. [Google Scholar]
  • 28. Nader Askari S. M. R. and Amini K., “Identification, Serotyping and Determination of Antibiotic Resistance of Salmonella Isolates Obtained From Stray Dogs in Tehran,” Journal of Veterinary Microbiology 16, no. 1 (2020): 43–52. [Google Scholar]
  • 29. Karimi Darehabi H., Esmailneshad F., and Ebrahimi Mohammadi K., “Contamination of Fresh Beef to Salmonella Typhimurium and Salmonella Enteritidis in Sanandaj During 2012,” Quarterly Scientific–Research Journal Food Hygiene 2, no. 3 (2012): 41. [Google Scholar]
  • 30. Afshari A., Baratpour A., Khanzade S., and Jamshidi A., “Salmonella Enteritidis and Salmonella Typhimorium Identification in Poultry Carcasses,” Iranian Journal of Microbiology 10, no. 1 (2018): 45–50. [PMC free article] [PubMed] [Google Scholar]
  • 31. Monadim K., Naghihaa M., and Najafia M., “Molecular Detection of Salmonella Serovar Isolated From Eggs,” Medical Laboratory Journal 9, no. 1 (2015): 17. [Google Scholar]
  • 32. Zare P., Ghorbani‐Choboghlo H., Tolouei M., and Hadavi J., “Evaluation of the Occurrence of Salmonella Serovars and Its Antibiotic Susceptibility in Apparently Healthy Domestic Animals in Rural Areas of East Azerbaijan Province,” Iranian Journal of Microbiology 10 (2016): 88–92. [Google Scholar]
  • 33. Staji H., Rezaei S., Rassouli M., and Namroodi S., “Prevalence and Genetic Characteristics of Salmonella Strains in Wild Mallard Ducks (Anas platyrhynchos) in Semnan Suburb, Iran,” Bulgarian Journal of Veterinary Medicine 20, no. 4 (2017): 348–356. [Google Scholar]
  • 34. Rahimi E., Shakerian A., and Falavarjani A. G., “Prevalence and Antimicrobial Resistance of Salmonella Isolated From Fish, Shrimp, Lobster, and Crab in Iran,” Comparative Clinical Pathology 22 (2013): 59–62. [Google Scholar]
  • 35. Tajbakhsh F., Tajbakhsh E., Rahimi E., and Momenii M., “Determination of Antibiotic Resistance in Salmonella Spp Isolated From Raw Cow, Sheep and Goat's Milk in Chaharmahal va Bakhtiyari Provience, Iran,” Global Veterinaria 10 (2013): 681–685. [Google Scholar]
  • 36. Akbari Khakrizi A., Yahyaraeyat R., Ashrafi Tamai I., Beikzadeh B., and Zahraei Salehi T., “Prevalence Assessment of Salmonella Serovars in Apparently Healthy Pet Dogs in Tehran,” Iran. Iranian Journal of Veterinary Science and Technology 14, no. 2 (2022): 11–18. [Google Scholar]
  • 37. Marziyeh Nazari M., Ebrahim R., and Amir S., “Salmonella Contamination of Camel Meat in Various Stages of Destruction in Isfahan and Chaharmahal va Bakhtiari,” Journal of Food Microbiology 4, no. 2 (2017): 29–36. [Google Scholar]
  • 38. Mohammad B., Amir H. M., and Roqiah G., “An Investigation on Contamination of Poultries by Salmonella Species in Zahedan (South‐East Iran) During 2004,” Research Journal of Microbiology 5, no. 11 (2010): 1185–1188. [Google Scholar]
  • 39. Hasan M., Mohsen G., and Manouchehr M., “Detection of Virulence Factors in Salmonella Typhimurium and Salmonella Enteritidis Serotypes Isolated From Chicken Meat in Chaharmahal va Bakhtiari Province of Iran,” Journal of Food Microbiology 1, no. 1 (2014): 17–22. [Google Scholar]
  • 40. Manafi L., Aliakbarlu J., and Dastmalchi Saei H., “Antibiotic Resistance and Biofilm Formation Ability of Salmonella Serotypes Isolated From Beef, Mutton, and Meat Contact Surfaces at Retail,” Journal of Food Science 85, no. 8 (2020): 2516–2522. [DOI] [PubMed] [Google Scholar]
  • 41. Moghadam S., Moradi Bidhendi S., and Khaki P., “Molecular Identification of Salmonella Strains Isolated From Livestock in Alborz Province and Their Serotyping,” Iranian Journal of Medical Microbiology 16, no. 4 (2022): 305–311. [Google Scholar]
  • 42. Zahraei Salehi T., Tadjbakhsh H., Atashparvar N., Nadalian M. G., and Mahzounieh M. R., “Detection and Identification of Salmonella Typhimurium in Bovine Diarrhoeic Fecal Samples by Immunomagnetic Separation and Multiplex PCR Assay,” Zoonoses and Public Health 54, no. 6–7 (2007): 231–236. [DOI] [PubMed] [Google Scholar]
  • 43. Nazari Moghadam M., Rahimi E., Shakerian A., and Momtaz H., “Prevalence of Salmonella Typhimurium and Salmonella Enteritidis Isolated From Poultry Meat: Virulence and Antimicrobial‐Resistant Genes,” BMC Microbiology 23, no. 1 (2023): 168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Namroodi S., Estaji H., and Dehmordeh M., “Frequency and Antimicrobial Resistance Pattern of Salmonella Spp in Asymptomatic Rural Dogs,” Journal of Mazandaran University of Medical Sciences 1, no. 1 (2018): 44–50. [Google Scholar]
  • 45. Shimi A. and Barin A., “Salmonella in Cats,” Journal of Comparative Pathology 87, no. 2 (1977): 315–318. [DOI] [PubMed] [Google Scholar]
  • 46. Firouzabadi A., Saadati D., Najimi M., and Jajarmi M., “Prevalence and Related Factors of Salmonella spp. and Salmonella Typhimurium Contamination Among Broiler Farms in Kerman Province, Iran,” Preventive Veterinary Medicine 175 (2020): 104838. [DOI] [PubMed] [Google Scholar]
  • 47. Akbarmehr J., Salehi T. Z., and Brujeni G., “Identification of Salmonella Isolated From Poultry by MPCR Technique and Evaluation of Their Hsp groEL Gene Diversity Based on the PCR‐RFLP Analysis,” African Journal of Microbiology Research 4, no. 15 (2010): 1594–1598. [Google Scholar]
  • 48. Firoozeh F., Shahcheraghi F., Zahraei Salehi T., Karimi V., and Aslani M. M., “Antimicrobial Resistance Profile and Presence of Class I Integrongs Among Salmonella Enterica Serovars Isolated From Human Clinical Specimens in Tehran, Iran,” Iranian Journal of Microbiology 3, no. 3 (2011): 112–117. [PMC free article] [PubMed] [Google Scholar]
  • 49. Fardsanei F., Soltan Dallal M. M., Zahraei Salehi T., Douraghi M., Memariani M., and Memariani H., “Antimicrobial Resistance Patterns, Virulence Gene Profiles, and Genetic Diversity of Salmonella Enterica Serotype Enteritidis Isolated From Patients With Gastroenteritis in Various Iranian Cities,” Iranian Journal of Basic Medical Sciences 24, no. 7 (2021): 914–921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50. Elham S., Bahareh A., and Sedigheh M., “Comparison of Virulence Genes (int, inv, spv (vir)) in Salmonella Typhimurium and Infantis From Clinical Cases by Multiplex PCR,” Iranian Journal of Infectious Diseases 25, no. 90 (2021): 27–36. [Google Scholar]
  • 51. Ranjbar R., Elhaghi P., and Shokoohizadeh L., “Multilocus Sequence Typing of the Clinical Isolates of Salmonella Enterica Serovar Typhimurium in Tehran Hospitals,” Iranian Journal of Medical Sciences 42, no. 5 (2017): 443–448. [PMC free article] [PubMed] [Google Scholar]
  • 52. Ezatpanah E., Bidhendi S. M., Khaki P., Ghaderi R., Jasbi E. S., and Far S. M., “Isolation, Serotyping and Antibiotic‐Resistance Pattern of Isolated Salmonella From Chicken of Arak,” Iranian Veterinary Journal 9, no. 39 (2013): 88–96. [Google Scholar]
  • 53. Mehrabian S. and Jaberi E., “Isolasion, Identification and Antimicrobial Resistance Patterns of Salmonella From Meat Products in Tehran,” Pakistan Journal of Biological Sciences 10, no. 1 (2006): 122–126. [DOI] [PubMed] [Google Scholar]
  • 54. Bonyadian M., Ale A. S., and Motahari F. A. Isolation and identification of Salmonellae From Chicken Carcasses in Processing Plants in Yazd Province, Central Iran. 2007.
  • 55. Abbas A., Sohrab N., Seyyed Amin K., Mohammad Hassan M., and Majid Naghdi Other A., “Salmonella Enterica: Serotyping, Drug Resistance and Extended Spectrum of β‐Lactamase (ESBLs),” Journal of Advanced Biomedical Sciences 1, no. 1 (2011): 38. [Google Scholar]
  • 56. Alzwghaibi A. B., Yahyaraeyat R., Fasaei B. N., Langeroudi A. G., and Salehi T. Z., “Rapid Molecular Identification and Differentiation of Common Salmonella Serovars Isolated From Poultry, Domestic Animals and Foodstuff Using Multiplex PCR Assay,” Archives of Microbiology 200 (2018): 1009–1016. [DOI] [PubMed] [Google Scholar]
  • 57. Abolfazl M. and Shahram Nazarian D., “Evaluation of Class 1, 2 and 3 Integrons in Clinical Salmonella Enteritidis Strains by Pcr Method. Jorjani Biomedicine,” Journal 5, no. 2 (2018): 1–10. [Google Scholar]
  • 58. Ranjbar R., Giammanco G. M., Farshad S., Owlia P., Aleo A., and Mammina C., “Serotypes, Antibiotic Resistance, and Class 1 Integrons in Salmonella Isolates From Pediatric Cases of Enteritis in Tehran, Iran,” Foodborne Pathogens and Disease 8, no. 4 (2011): 547–553. [DOI] [PubMed] [Google Scholar]
  • 59. Doosti A., Mahmoudi E., Jami M.‐S., and Mokhtari‐Farsani A., “Prevalence of aadA1, aadA2, aadb, strA and strB Genes and Their Associations With Multidrug Resistance Phenotype in Salmonella Typhimurium Isolated From Poultry Carcasses,” Thai Journal of Veterinary Medicine 46, no. 4 (2016): 691–697. [Google Scholar]
  • 60. Doosti A., Zohoor A., Chehelgerdi M., and Mokhtari‐Farsani A., “Distribution of TEM‐1 Gene in Salmonella Enterica Isolated From Poultry Carcasses in Iran,” Thai Journal of Veterinary Medicine 46, no. 1 (2016): 9–15. [Google Scholar]
  • 61. Yousefi‐Mashouf R. and Moshtaghi A., “Frequency of Typhoidal and Non‐Typhoidal Salmonella Species and Detection of Their Drugs Resistance Patterns,” Journal of Research in Health Sciences 7, no. 1 (2023): 49–56. [PubMed] [Google Scholar]
  • 62. Farhoudi‐Moghaddam A. A., Katouli M., Jafari A., Bahavar M. A., Parsi M., and Malekzadeh F., “Antimicrobial Drug Resistance and Resistance Factor Transfer Among Clinical Isolates of Salmonellae in Iran,” Scandinavian Journal of Infectious Diseases 22, no. 2 (1990): 197–203. [DOI] [PubMed] [Google Scholar]
  • 63. Khaltabadi R. F., Shahrokhi N., Ebrahimi‐Rad M., and Ehsani P., “Salmonella Typhimurium in Iran: Contribution of Molecular and IS 200 PCR Methods in Variants Detection,” PLoS One 14, no. 3 (2019): e0213726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64. Azizpour A., “Prevalence and Antibiotic Resistance of Salmonella Serotypes in Chicken Meat of Ardabil, Northwestern Iran,” Iranian Journal of Medical Microbiology 15, no. 2 (2021): 232–246. [Google Scholar]
  • 65. Dilmaghani M., Ahmadi M., Zahraei Salehi T., and Talebi A., “The Analysis of groEL Gene in Salmonella Enterica Subspecies Enterica Serovar Typhimurium Isolated From Avians by PCR‐Restriction Fragment Length Polymorphism Method,” Veterinary Research Communications 35 (2011): 133–143. [DOI] [PubMed] [Google Scholar]
  • 66. Halimi H. A., Seifi H. A., and Rad M., “Bovine Salmonellosis in Northeast of Iran: Frequency, Genetic Fingerprinting and Antimicrobial Resistance Patterns of Salmonella Spp,” Asian Pacific Journal of Tropical Biomedicine 4, no. 1 (2014): 1–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67. Jamshidi A., Kalidari G. A., and Hedayati M., “Isolation and Identification of Salmonella Enteritidis and Salmonella Typhimurium From the Eggs of Retail Stores in Mashhad, Iran Using Conventional Culture Method and Multiplex PCR Assay,” Journal of Food Safety 30, no. 3 (2010): 558–568. [Google Scholar]
  • 68. Keshmiri M. A., Nemati A., Askari Badouei M., Ashrafi Tamai I., and Zahraei Salehi T., “Clonal Relatedness and Antimicrobial Susceptibility of Salmonella Serovars Isolated From Humans and Domestic Animals in Iran: A One Health Perspective,” Iranian Journal of Veterinary Research 23, no. 2 (2022): 104–110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69. Nazer A. and Safari G., “Bacterial Flora From Dead‐in‐Shell Chicken Embryos and Their Drug Resistance in Fars Province of Iran,” Indian Journal of Animal Sciences 64, no. 10 (1994): 1006–1009. [Google Scholar]
  • 70. Rahimi Z., Ghajarbeygi P., Mahmoudi R., Mosavi S., and Mehrabi A., “The Prevalence of Salmonella Enteritidis in Packaged and Tray Eggs Samples, Qazvin, Iran,” Journal of Chemical Health Risks 13, no. 3 (2023): 1–13. [Google Scholar]
  • 71. Ranjbar R. and Mirzaee A., “Determining of the Variety of Genotypes in Salmonella Typhimurium by ERIC‐PCR,” Journal of Babol University of Medical Sciences 15, no. 1 (2012): 51. [Google Scholar]
  • 72. Estabergi E., Amini K., Shojaee Saadi B., and Eghdamian S., “Molecular Study of Salmonella Typhimurium Integrons Gene Isolated From Food Sources and the Effect of Probiotic Bifidobacterium Bifidum on its Expression by Real Time PCR. Razi,” Journal of Medical Sciences 27, no. 7 (2020): 65–77. [Google Scholar]
  • 73. Moghadam A. and Nazarian S. Genotyping of Clinical Isolates of Salmonella Enterica Serovar Typhimurium From Medical Centers of Kerman Province Using ERICPCR Method. 2018.
  • 74. Sterne J. A. C., Sutton A. J., Ioannidis J. P. A., et al., “Recommendations for Examining and Interpreting Funnel Plot Asymmetry in Meta‐Analyses of Randomised Controlled Trials,” BMJ 343 (2011): d4002. [DOI] [PubMed] [Google Scholar]
  • 75. Begg C. B. and Mazumdar M., “Operating Characteristics of a Rank Correlation Test for Publication Bias,” Biometrics 50, no. 4 (1994): 1088–1101. [PubMed] [Google Scholar]
  • 76. Becker L. M.. The Effects of Exercise Versus Methylphenidate on Attention and Behavior in Children With Attention Deficit Hyperactivity Disorder, Predominantly Inattentive Type: The University of Alabama at Birmingham; 1997.
  • 77. Freeman S. and Sutton A., Identifying Publication Bias in Meta‐analyses of Continuous Outcomes (Cochrane Training, 2020). [Google Scholar]
  • 78. Patsopoulos N. A., Evangelou E., and Ioannidis J. P., “Sensitivity of Between‐Study Heterogeneity in Meta‐Analysis: Proposed Metrics and Empirical Evaluation,” International Journal of Epidemiology 37, no. 5 (2008): 1148–1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79. Belina D., Hailu Y., Gobena T., Hald T., and Njage P. M. K., “Prevalence and Epidemiological Distribution of Selected Foodborne Pathogens in Human and Different Environmental Samples in Ethiopia: A Systematic Review and Meta‐Analysis,” One Health Outlook 3, no. 1 (2021): 19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80. Feczko E. and Fair D. A., “Methods and Challenges for Assessing Heterogeneity,” Biological Psychiatry 88, no. 1 (2020): 9–17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81. Ruppar T., “Meta‐Analysis: How to Quantify and Explain Heterogeneity?,” European Journal of Cardiovascular Nursing 19, no. 7 (2020): 646–652. [DOI] [PubMed] [Google Scholar]
  • 82. Sterne J. A. C. and Harbord R. M., “Funnel Plots in Meta‐Analysis,” Stata Journal: Promoting Communications on Statistics and Stata 4 (2004): 127–141. [Google Scholar]
  • 83. Medalla F., Gu W., Friedman C. R., et al., “Increased Incidence of Antimicrobial‐Resistant Nontyphoidal Salmonella Infections, United States, 2004–2016,” Emerging Infectious Diseases 27, no. 6 (2021): 1662–1672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84. Serwecińska L., “Antimicrobials and Antibiotic‐Resistant Bacteria: A Risk to the Environment and to Public Health,” Water 12, no. 12 (2020): 3313. [Google Scholar]
  • 85. Aarestrup F. M.. “The Livestock Reservoir for Antimicrobial Resistance: A Personal View on Changing Patterns of Risks, Effects of Interventions and the Way Forward,” Philosophical Transactions of the Royal Society, B: Biological Sciences 370, no. 1670 (2015): 20140085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86. Bengtsson‐Palme J., Kristiansson E., and Larsson D. G. J., “Environmental Factors Influencing the Development and Spread of Antibiotic Resistance,” FEMS Microbiology Reviews 42, no. 1 (2018): fux053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87. Hald T., Lo Fo Wong D. M. A., and Aarestrup F. M., “The Attribution of Human Infections With Antimicrobial Resistant Salmonella Bacteria in Denmark to Sources of Animal Origin,” Foodborne Pathogens and Disease 4, no. 3 (2007): 313–326. [DOI] [PubMed] [Google Scholar]
  • 88. Sinwat N., Angkittitrakul S., Coulson K. F., Pilapil F. M. I. R., Meunsene D., and Chuanchuen R., “High Prevalence and Molecular Characteristics of Multidrug‐Resistant Salmonella in Pigs, Pork and Humans in Thailand and Laos Provinces,” Journal of Medical Microbiology 65, no. 10 (2016): 1182–1193. [DOI] [PubMed] [Google Scholar]
  • 89. Rodríguez E. C., Díaz‐Guevara P., Moreno J., et al., “Vigilancia Por Laboratorio De Salmonella Enterica En Casos Clínicos Humanos En Colombia 2005 a 2011,” Enfermedades Infecciosas y Microbiología Clínica 35, no. 7 (2017): 417–425. [DOI] [PubMed] [Google Scholar]
  • 90. Reddy E. A., Shaw A. V., and Crump J. A., “Community‐Acquired Bloodstream Infections in Africa: A Systematic Review and Meta‐Analysis,” Lancet Infectious Diseases 10, no. 6 (2010): 417–432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91. Graham S. M., “Nontyphoidal Salmonellosis in Africa,” Current Opinion in Infectious Diseases 23, no. 5 (2010): 409–414. [DOI] [PubMed] [Google Scholar]
  • 92. The European Union Summary Report on Antimicrobial Resistance in Zoonotic and Indicator Bacteria From Humans, Animals and Food in 2015,” EFSA Journal 15, no. 2 (2017): e04694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93. OECD/FAO . OECD‐FAO Agricultural Outlook 2020–2029. OECD. 2020.
  • 94. Sun T., Liu Y., Qin X., et al., “The Prevalence and Epidemiology of Salmonella in Retail Raw Poultry Meat in China: A Systematic Review and Meta‐Analysis,” Foods 10, no. 11 (2021): 2757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95. Paião F. G., Arisitides L. G. A., Murate L. S., Vilas‐Bôas G. T., Vilas‐Boas L. A., and Shimokomaki M., “Detection of Salmonella spp, Salmonella Enteritidis and Typhimurium in Naturally Infected Broiler Chickens by a Multiplex PCR‐Based Assay,” Brazilian Journal of Microbiology 44 (2013): 37–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96. Mutluer B., Yargülü B., Hartung M., and Erol I. Incidence and Serovar Distribution of Salmonella in Market Broilers in Turkey. 1992.
  • 97. Aury K., Chemaly M., Petetin I., et al., “Prevalence and Risk Factors for Salmonella Enterica Subsp. Enterica Contamination in French Breeding and Fattening Turkey Flocks at the End of the Rearing Period,” Preventive Veterinary Medicine 94, no. 1–2 (2010): 84–93. [DOI] [PubMed] [Google Scholar]
  • 98. Kanaan M. H. G., “Prevalence and Antimicrobial Resistance of Salmonella Enterica Serovars Enteritidis and Typhimurium Isolated From Retail Chicken Meat in Wasit Markets, Iraq,” Veterinary World 16, no. 3 (2023): 455–463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99. Telli A. E., Biçer Y., Telli N., Güngör C., Türkal G., and Ertaş O. N., “Pathogenic Escherichia coli and Salmonella spp. in Chicken Carcass Rinses: Isolation and Genotyping by ERIC‐PCR,” Pakistan Veterinary Journal 42, no. 4 (2022): 493–498. [Google Scholar]
  • 100. Shah A. and Korejo N., “Antimicrobial Resistance Profile of Salmonella Serovars Isolated From Chicken Meat,” Journal of Veterinary and Animal Sciences 2 (2012): 40–46. [Google Scholar]
  • 101. Balakrishnan S., Sangeetha A., and Dhanalakshmi M., “Prevalence of Salmonella in Chicken Meat and its Slaughtering Place From Local Markets in Orathanadu, Thanjavur District, Tamil Nadu,” Journal of Entomology and Zoology Studies 6, no. 2 (2018): 2468–2471. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that supports the findings of this study are available in the supporting material of this article. All the data in this review are included in the article.

Articles from Health Science Reports are provided here courtesy of Wiley

RESOURCES