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Iranian Journal of Veterinary Research logoLink to Iranian Journal of Veterinary Research
. 2023;24(2):110–115. doi: 10.22099/IJVR.2023.43730.6410

The examination of some virulence factors in S. aureus isolates obtained from the healthy human population, sheep mastitis, and cheese

L Rahbarnia 1, R Khosravi Rad 2, AR Dehnad 3,*, B Naghili 1
PMCID: PMC10542877  PMID: 37790118

Abstract

Background:

Staphylococcus aureus is responsible for many infections in humans and animals from skin and soft tissue infections to life-threatening diseases. In this study to explore the origin of S. aureus infections in humans, the antibiotic resistance profile and the variety of virulence factors in S. aureus isolates were examined in three groups: a healthy human population, cheese, and the milk of sheep with mastitis.

Aims:

The examination of some virulence factors in S. aureus isolates obtained from the healthy human population, sheep mastitis, and cheese.

Methods:

A total of 400 nasal swab samples from healthy students, 30 cheese samples, and 122 sheep milk samples were collected for the detection of S. aureus isolates from January 1, 2018, to March 1, 2018. The frequency of hla, hlb, Acme/arcA, pvl, and tsst-1 virulence genes and mecA gene was determined in each group by PCR assay.

Results:

There was a direct relationship between the antibiotic susceptibility profile of the isolates from a healthy population and those from mastitis milk samples. Of 400 nasal samples, 15% (60/400) were positive for S. aureus, of which 60% (36/60) were positive for mecA. While 50% (15/30) of cheese samples were positive for S. aureus. of which 7 cases (46.66%, 7/15) were positive for mecA. The prevalence of S. aureus among students was dependent on gender (P=0.025). Also, 47.5% (58/122) of milk samples from sheep mastitis were positive for S. aureus, and 41.37% (24/58) were positive for the mecA gene. Based on PCR results, the highest rate of hla (68.33%, 41/60), hlb (53.33%, 32/60), and Acme/arcA (46.66%, 28/60) genes were related to a healthy population, and the highest frequency of pvl (41.38%, 24/58), and tsst-1 (27.59%, 16/58) was related to milk samples (P<0.05). A significant correlation was observed between the presence of the arginine catabolic mobile element (ACME)-arcA gene and resistance to methicillin (P<0.05).

Conclusion:

The high rate of virulence factors in the S. aureus isolates obtained from mastitis and dairy products is an alert point, because they could be source of the spreading of S. aureus to humans. There is an essential need for continuous monitoring to control staphylococcal food poisoning.

Key Words: Dairy products, Healthy population, Mastitis, S. aureus, Virulence factors

Introduction

Staphylococcus aureus is a leading cause of different infections from the skin and soft tissue infections to life-threatening diseases (Lindsay and Holden, 2004). The escalating prevalence of multi-drug resistant (MDR) strains is now serious challenges in clinical settings.

In animals, S. aureus is a predominant cause of intramammary infections (IMIs), or mastitis (Kwiatkowski et al., 2022). Mastitis is responsible for notable economic losses on dairy farms due to decreased milk yield, the production of unsuitable milk for consumption, and treatment costs (Peton and Le Loir, 2014; Aghamohammadi et al., 2018). Particularly, milk and milk products such as cheese, are considered as a reservoir of S. aureus strains (Szczuka et al., 2022). On the other hand, S. aureus colonization in healthy individuals is a risk factor for further infections. For this reason, we evaluated and characterized S. aureus isolates in milk, cheese, and healthy individuals.

S. aureus can be directly transferred to milk through an animal infected with mastitis and indirectly by an unhygienic environment. S. aureus colonization may occur in milk consumers often through the consumption of infected milk and dairy products (Anderson et al., 2011). Based on reports, S. aureus colonization occurs in 30 to 50% of the healthy carriers (Zeinalpour Ahrabi et al., 2019). The ability of contagiousness of the mastitis infection might be associated with the presence and the variation of S. aureus virulence factors (Magro et al., 2017). Based on reports, some of the virulence factors produced by S. aureus play a key role in the escape of infection from the host immune system (Magro et al., 2017; Monistero et al., 2018). Alpha-hemolysin (hla) gene is usually the cause of clinical symptoms such as brain abscess, pneumonia, and sepsis (Xiao et al., 2016). Haemolysin beta (hlb) rises cytotoxicity and the adherence of S. aureus to bovine mammary epithelial cells (Ito et al., 2003), it is mostly the main cause of eye and lung infections (Dehnad et al., 2020). Exotoxins (such as leukocidins, enterotoxins, and toxic shock syndrome toxin-1) can support the bacteria versus host immune response. The combination of these factors seems to be essential to the incidence of infection in humans and animals (Fluit, 2012; Koymans et al., 2015).

Arginine catabolic mobile element (ACME) is known as an enhancing factor of S. aureus colonization in the skin and mucous membranes, which act through the neutralization of acidic pH and enhancement of the acid tolerance of pathogen (Thurlow et al., 2013). Panton-Valentine leukocidin LukSF-PV (PVL), as a pore-forming toxin, has a key role in the incidence of skin and soft tissue infections (Niemann et al., 2018). Because of the importance of S. aureus infections in humans and animals, there is an essential need for awareness regarding S. aureus prevalence and the relationship between the occurrence of virulence factors in healthy populations and dairy products. The present study examined the antibiotic resistance profile, and diversity of virulence factors in S. aureus isolates obtained from dairy products, sheep mastitis, and a healthy population of humans.

Materials and Methods

Ethics committee approval

Tabriz University of Clinical Research Ethics Committee (reference No.: IR. TBZMED. REC.1398. 989). The swab samples were obtained after written consent with a brief description of the importance of the study to the participants.

Bacterial identification

A cross-sectional study was conducted from January 1, 2018 to March 1, 2018 in several high schools from Tabriz city. A total of 400 students aged 16 to 17 years were participated in this study. The healthy students without previous antibiotic consumption (during the last three months) were included in this study. The nasal swab samples were collected from 400 students, transferred into tryptic soy broth media, and incubated overnight at 37°C. A total of 122 milk samples related to 53 dairy herds in East Azerbaijan province of Iran were obtained from ewes infected with mastitis. The cheese samples were also obtained from 150 factories producing traditional cheese. The samples were cultured for the identification of S. aurous isolates. The S. aureus isolates were diagnosed through conventional microbiological and biochemical methods (Ghavghani et al., 2019).

Antibiotic susceptibility testing

The antibiotic resistance profile of S. aureus isolates was evaluated using the disk diffusion method based on the Clinical Laboratory Standards Institute (CLSI) guidelines (Weinstein and Lewis II, 2020). Antibiotic disks (Biomaxima, Poland) were included cefazolin (30 μg), amoxicillin/clavulanic acid (20/10 μg), chloramphenicol (30 μg), penicillin (6 μg), erythromycin (15 μg), oxacillin (1 μg), clindamycin (2 μg), ciprofloxacin (5 μg), and cefoxitin (30 μg). To perform antibiotic susceptibility tests, the bacterial concentrations of 0.5 McFarland were used to inoculate onto Muller-Hinton agar plates. The inoculated plates containing the antibiotic disks were incubated overnight at 37°C. S. aureus ATCC 33591 (oxacillin-resistant) and S. aureus ATCC 29213 (oxacillin-susceptible) were utilized as positive and negative controls, respectively.

The detection of virulence factors by PCR reaction

DNA was extracted from S. aureus isolates by the boiling method using TE buffer (10 mM Tris, 1 mM EDTA). The quality and quantity of DNA were evaluated by the ratio of absorbance at 260 nm and 280 nm wavelength using Nanodrop (Thermo Scientific NanoDropTM). PCR reaction was performed for detection of nucA, mecA, ACME-arcA, Tsst-1, hla, hlb, and PVL genes using designed primers (Table 1) in a 25 μL reaction for 30 cycles (94°C for 1 min, 49°C/53°C for 1 min, 72°C for 1 min) after an initial denaturation at 94°C for 4 min. The final extension was performed at 72°C for 5 min. PCR products were visualized by 1% agarose gel electrophoresis. For further confirmation, PCR products were sequenced.

Table 1.

The sequence of primers used for the detection of virulence factors by PCR reaction

Primer Primer sequence (5´→3´) Annealing Tm (°C) Size (bp) Reference
nucA F: 5´-GCGATTGATGGTGATACGGTT-3´ 53 276 Dehnad et al. (2020)
R: 5´-CAAGCCTTGACGAACTAAAGC-3´
mecA F: 5´-AGAAATGACTGAACGTCC-3´ 49 305 Dehnad et al. (2020)
R: 5´-ATTCCACATTGTTTCGGTC-3´
Tsst-1 F: 5´-ACAAGCGCTATTTTTATTTCAG-3´ 49 271 Zeinalpour Ahrabi et al. (2019)
R: 5´-CCCATCCCCAACCACTTTT-3´
Hla F: 5´-GTACAGTTGCAACTACCT-3´ 49 253 Dehnad et al. (2020)
R: 5´-CTTTCCAGCCTACTTTTTTATCAGT-3´
Hlb F: 5´-GTGCACTTACTGACAATAGTGC-3´ 49 313 Dehnad et al. (2020)
R: 5´-GTTGATGAGTAGCTACCTTCAGT-3´
Acme-arcA F: 5´-CTAGGTGCATAAATGTACGTG-3´ 49 577 Sabat et al. (2015)
R: 5´-CCAGAAGTACGCGAGAAC-3´
PVL F: 5´-AGGTAAAATGTCTGGACATG-3´ 49 427 Hoppe et al. (2018)
R: 5´-GCATCAACTGTATTGGATAGC-3´
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Statistical analysis

Statistical analysis was performed by SPSS version 16. Demographic and clinical variables were compared by Chi-square test. P<0.05 was assumed as the statistical significance.

Results

Frequency of S. aureus isolates

In total, 15% (60/400) of nasal samples were positive for S. aureus, of which 5.5% (22/400) of the isolates were from female students, and 9.5% (38/400) of them were obtained from male students. Based on the results, the frequency of S. aureus was dependent on gender (P=0.025). Based on disk diffusion results, 98.33% of the isolates were resistant to a penicillin antibiotic, and 18.33% (11/60) of the isolates were methicillin-resistant Staphylococcus aureus (MRSA) based on resistance to cefoxitin (Fig. 1). Among 122 milk samples obtained from mastitis ewes, 58 (47.5%) S. aureus isolates were identified, of which 45% (26/58) of them were resistant to cefoxitin and MRSA. Of 15 S. aurous in cheese products, 7 cases (46.66%) were MRSA (Fig. 1).

Fig. 1.

Fig. 1

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The comparison of antibiotic susceptibility profile of the S. aureus isolates in three groups including health community, ewe’s mastitis, and cheese products performed using disc diffusion method

Detection of mecA resistance gene and virulence factors by PCR

After the confirmation of S. aureus isolates by nucA amplification, the presence of hla, hlb, ACME/arcA, pvl, and tsst-1 virulence genes and mecA gene was examined by PCR assay (Figs. 2A-F). Based on the results, 54.54% (36/60) of the student isolates were positive for mecA, and 46.66% (28/60) were positive for ACME-arcA gene. The highest rate of PVL was related to the isolates obtained from mastitis samples 41.38% (24/58). Based on the results, 11.66% (7/60) of the student isolates were positive for both PVL and ACME-arcA genes. A direct relationship was found between resistance to methicillin, and the presence of the ACME-arcA gene (P<0.05), whereas 90% (9/10) of the PVL positive isolates were sensitive to methicillin (P<0.05). The incidence rate of PVL and ACME-arcA genes in student isolates was independent of gender (P=0.337, P=0.142, respectively). In mastitis isolates, (27.58%, 16/58) cases were positive for three virulence factors, and (8.62%, 5/58) isolates were positive for both PVL and ACME-arcA genes. The highest frequency of PVL (41.38%, 24/58) and Tsst-1 (27.59%, 16/58) was related to mastitis samples. Regarding cheese samples, frequency of virulence factors was including ACME-arcA (13.33%, 2/15), Tsst-1 (20%, 3/15), hla (26.66%, 4/15), and hlb (1/15, 6.66%) (Fig. 3).

Fig. 2.

Fig. 2

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PCR amplification of pvl, ACME-arcA, mecA, Tsst-1, hla, and hlb gene fragments by specific primers. (A) PCR reaction to detect pvl gene as a band of 427 bp, (B) Amplification of ACME-arcA gene fragment as a sharp band of 577 bp, (C) A single band of 305 bp related to mecA gene fragment, (D) A single band of 271 bp related to Tsst-1 gene, (E) A single band of 253 bp related to hla gene, and (F) A single band of 313 bp related to hlb gene displayed in electrophoresis gel. M: Marker 100 bp, P: Positive control, and N: Negative control

Fig. 3.

Fig. 3

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The comparison of frequency of virulence genes in three groups including health community, ewes mastitis, and cheese products performed by PCR assay

Discussion

The variability in virulence factors plays a key role in S. aureus pathogenicity and intramammary infections in dairy animals. A 2.75% prevalence of MRSA was found in healthy students in our region (North-West of Iran), which were less than the reported rate from students in the central part of Iran (4.5%) (Japoni-Nejad et al., 2013) and the results obtained from farm workers (8.7%) in Turkey (den Heijer et al., 2013); (Garipcin and Seker, 2015). Based on the results, the frequency of MRSA colonization in this study was dependent on gender, consistent with similar studies carried out regarding a higher prevalence of MRSA carriage in men (Humphreys et al., 2015); (Garoy et al., 2019). Based on our results, 16.66% of the student isolates were positive for the PVL gene and 46.66% of the cases were positive for the ACME-arcA gene. These findings were not consistent with a study completed in the center of Iran, with a prevalence of 17% and 20% for ACME-arcA and PVL genes, respectively (Fard-Mousavi et al., 2015). Also, 11.66% of the PVL-positive isolates were positive for the ACME-arcA gene. Consistent with previous research (Motamedi et al., 2015), in this study, there is a direct association between the frequency of mecA positive strains and the presence of the ACME-arcA gene in the student population. In contrast, 85.71% PVL positive isolates were MSSA indicating a lack of association between the occurrence of PVL and the rate of MRSA.

Regarding the presence of S. aureus in dairy products, 50% of cheese samples (15/30) were positive for S. aureus, while 46.66% of them were positive for mecA. Also, 47.54% of mastitis samples were positive for S. aureus, and 41.37% were positive for the mecA gene. The prevalence of S. aureus in mastitis samples was less than the previous report (60%) from Shahrekord, Iran (Ebrahimi et al., 2014) but more than the prevalence of S. aureus (13.82%) in the North-West of Iran (Dastmalchi Saei and Panahi, 2020).

The highest rate of hla (68.33%, 41/60) and hlb (53.33%, 32/60), and ACME/arcA genes were related to the students, and the highest frequency of pvl (41.38%, 24/58), and tsst-1 (16/58, 27.59%) was related to the mastitis samples. The prevalence of ACME-positive MRSA strains in a healthy population can be one of the leading causes of skin infections. The rate of tsst-1 in mastitis isolates was less than in a previous study (44.19%) in the North-West of Iran (Dastmalchi et al., 2013). Also, the PVL rate was more than in the previous studies (Ünal et al., 2012; Mistry et al., 2016; Wang et al., 2018). The frequency of tsst-1 in cheese samples was almost similar to a report from Brazil (Castro et al., 2020). Our findings revealed a high diversity of virulence factors and antibiotic resistance profiles in dairy products and mastitis compared to the healthy population. One of the limitations of this study was related to the small sample sizes.

The presence of S. aureus virulence factors in the mastitis and dairy products is an alert point. Because contaminated dairy products are sources of S. aureus infection in humans. These results highlight an essential need for continuous monitoring to control staphylococcal food poisoning.

Conflict of interest

The authors have no conflict of interest.

Acknowledgements

This study was supported by the Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran. This research received no specific grants from the funding agency.

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