Skip to main content
Download PDF
Download ePub

A survey of prevalence and phenotypic and genotypic assessment of antibiotic resistance in Staphylococcus aureus bacteria isolated from ready-to-eat food samples collected from Tehran Province, Iran

Tropical Medicine and Health volume 49, Article number: 81 (2021) Cite this article

Abstract

Background

Resistant Staphylococcus aureus (S. aureus) bacteria are considered among the major causes of foodborne diseases. This survey aims to assess genotypic and phenotypic profiles of antibiotic resistance in S. aureus bacteria isolated from ready-to-eat food samples.

Methods

According to the previously reported prevalence of S. aureus in ready-to-eat food samples, a total of 415 ready-to-eat food samples were collected from Tehran province, Iran. S. aureus bacteria were identified using culture and biochemical tests. Besides, the phenotypic antibiotic resistance profile was determined by disk diffusion. In addition, the genotypic pattern of antibiotic resistance was determined using the PCR.

Results

A total of 64 out of 415 (15.42%) ready-to-eat food samples were contaminated with S. aureus. Grilled mushrooms and salad olivieh harbored the highest contamination rate of (30%), while salami samples harbored the lowest contamination rate of 3.33%. In addition, S. aureus bacteria harbored the highest prevalence of resistance to penicillin (85.93%), tetracycline (85.93%), gentamicin (73.43%), erythromycin (53.12%), trimethoprim-sulfamethoxazole (51.56%), and ciprofloxacin (50%). However, all isolates were resistant to at least four antibiotic agents. Accordingly, the prevalence of tetK (70.31%), blaZ (64.06%), aacA-D (57.81%), gyrA (50%), and ermA (39.06%) was higher than that of other detected antibiotic resistance genes. Besides, AacA-D + blaZ (48.43%), tetK + blaZ (46.87%), aacA-D + tetK (39.06%), aacA-D + gyrA (20.31%), and ermA + blaZ (20.31%) were the most frequently identified combined genotypic patterns of antibiotic resistance.

Conclusion

Ready-to-eat food samples may be sources of resistant S. aureus, which pose a hygienic threat in case of their consumption. However, further investigations are required to identify additional epidemiological features of S. aureus in ready-to-eat foods.

Background

Ready-to-eat food samples are among the most popular foodstuffs among Iranian people. Diverse kinds of ready-to-eat food samples, particularly hamburgers, chicken nuggets, salad olivieh (chicken meat-based salad with eggs and potatoes), salami, falafel (pea-based food with high amounts of different spices), grilled mushrooms, and Mexican corn are presented as street foods in Iran. Use of low-quality raw materials and poor hygienic conditions in preparation of these foodstuffs cause microbial contamination [1, 2].

Staphylococcus aureus (S. aureus), i.e. a Gram-positive and catalase-positive bacterium, is a major cause of food-borne diseases with a short incubation period as well as symptoms, such as weakness, vomiting, nausea, and abdominal cramps in people [3, 4]. Contaminated foodstuffs, particularly ready-to-eat food samples, are considered reservoirs of S. aureus [5, 6].

This bacterium develops resistance to diverse kinds of antibiotic agents [7]. Resistant S. aureus bacteria are responsible for about 100,000 infectious disease cases, with about an annual mortality rate of 20–30% in the United States [8]. Resistant S. aureus bacteria cause complicated diseases for a long period [9]. Research reports that S. aureus bacteria harbor high resistance to diverse kinds of antibiotic drugs, particularly penicillins, cephalosporins, tetracyclines, aminoglycosides, macrolides, and fluoroquinolones [7, 10].

Some antibiotic resistance genes are responsible for development of antibiotic resistance in S. aureus strains [11]. TetK and tetM (tetracycline resistance genes), ermA and msrA (macrolide resistance genes), gyrA and grlA (fluoroquinolone resistance genes), blaZ (penicillin resistance gene), dfrA (folate inhibitor resistance gene), rpoB (ansamycin resistance gene), aacA-D (aminoglycoside resistance gene), linA (lincosamide resistance gene), and cat1 (phenicol resistance gene) are the major resistance genes among S. aureus bacteria [11].

Given the high consumption rate of ready-to-eat foodstuffs in Iran and the high importance of S. aureus as a food-borne pathogen, the present survey was performed to assess the prevalence as well as phenotypic and genotypic patterns of antibiotic resistance in S. aureus bacteria isolated from diverse kinds of ready-to-eat food samples.

Results

Table 1 shows the prevalence of S. aureus in diverse kinds of ready-to-eat food samples. A total of 64 out of 415 (15.42%) ready-to-eat food samples were contaminated with S. aureus. Accordingly, grilled mushrooms (30%) and salad olivieh (30%) were the most commonly contaminated samples. In contrast, the lowest prevalence of S. aureus was found in salami samples (3.33%). A statistically significant difference was observed between different types of ready-to-eat food samples and S. aureus prevalence (P < 0.05).

Table 1 Prevalence of S. aureus in diverse kinds of ready-to-eat food samples
Full size table

Table 2 shows the phenotypic profile of antibiotic resistance in S. aureus strains isolated from diverse kinds of ready-to-eat food samples. Accordingly, S. aureus isolates harbored the highest prevalence of resistance to the antibiotics of penicillin (85.93%), tetracycline (85.93%), gentamicin (73.43%), erythromycin (53.12%), trimethoprim-sulfamethoxazole (51.56%), and ciprofloxacin (50%). However, the lowest prevalence of resistance was found to the antibiotic agents of rifampin (26.56%), doxycycline (26.56%), and chloramphenicol (28.12%). The prevalence of resistance to the antibiotic agents of amikacin, azithromycin, levofloxacin, and clindamycin was 35.93%, 42.18%, 37.50%, and 37.50%, respectively. Accordingly, a statistically significant difference was observed between various types of ready-to-eat food samples and prevalence of antibiotic resistance (P < 0.05). Moreover, significant differences were observed in the prevalence of resistance between antibiotic agents of gentamicin and amikacin (P < 0.05), azithromycin and erythromycin (P < 0.05), tetracycline and doxycycline (P < 0.05), as well as ciprofloxacin and levofloxacin (P < 0.05).

Table 2 Phenotypic profile of antibiotic resistance in S. aureus isolates recovered from diverse kinds of ready-to-eat food samples
Full size table

Figure 1 shows the prevalence of multi-drug resistant S. aureus strains isolated from ready-to-eat food samples. Accordingly, the prevalence of resistance to at least four antibiotic agents was 100%, while it amounted to 37.50% in more than eight antibiotic agents.

Fig. 1
figure 1

Prevalence of multi-drug resistant S. aureus bacteria isolated from ready-to-eat food samples; the results were interpreted from a total of 64 S. aureus isolates

Full size image

Table 3 shows the genotypic profile of antibiotic resistance in S. aureus strains isolated from diverse kinds of ready-to-eat food samples. According to the table, TetK (70.31%), blaZ (64.06%), aacA-D (57.81%), gyrA (50%), and ermA (39.06%) were the most frequently identified antibiotic resistance genes. Prevalence of tetM (10.93%), grlA (10.93%), linA (18.75%), and rpoB (18.75%) was lower than that of other antibiotic resistance genes. Besides, there was a statistically significant difference between various types of samples and prevalence of antibiotic resistance genes (P < 0.05). Furthermore, statistically significant differences were observed in the distribution of the antibiotic resistance genes of tetK and tetM (P < 0.05), msrA and ermA (P < 0.05), as well as gyrA and grlA (P < 0.05).

Table 3 Genotypic profile of antibiotic resistance in S. aureus isolates recovered from diverse kinds of ready-to-eat food samples
Full size table

Table 4 shows the combined genotypic profile of antibiotic resistance in S. aureus strains isolated from diverse kinds of ready-to-eat food samples. Accordingly, a total of 19 diverse combined genotypic patterns of antibiotic resistance were identified in the S. aureus isolates. Besides, AacA-D + blaZ (48.43%), tetK + blaZ (46.87%), aacA-D + tetK (39.06%), aacA-D + ermA (20.31%), aacA-D + gyrA (20.31%), and ermA + blaZ (20.31%) were the most frequently identified combined genotypic patterns of antibiotic resistance. In addition, prevalence of msrA + gyrA (3.12%), ermA + rpoB (3.12%), tetK + rpoB (4.68%), aacA-D + rpoB (6.25%), blaZ + rpoB (7.81%), tetK + msrA (10.93%), and ermA + gyrA (10.93%) was lower than that of other identified combined antibiotic resistance profiles. However, none of the S. aureus isolates harbored the combined msrA + rpoB genotypic pattern.

Table 4 Combined genotypic profile of antibiotic resistance in S. aureus isolates recovered from diverse kinds of ready-to-eat food samples
Full size table

Discussion

Contaminated ready-to-eat food samples, especially those of an animal origin, are considered probable causes of S. aureus transmission to the human population [12].

The present survey was performed to evaluate the prevalence as well as phenotypic and genotypic profiles of antibiotic resistance in S. aureus bacteria isolated from the samples of hamburgers, salami, grilled mushrooms, falafel, salad olivieh, chicken nuggets, and Mexican corn. The prevalence of S. aureus was 15.42% in the examined samples. Besides, a higher prevalence was observed in grilled mushrooms (30%) and salad olivieh (30%), while a lower prevalence was found in salami samples (3.33%). This finding could have been due to the different levels of water activity (aw) and pH values in diverse food samples. Furthermore, the use of low-quality and contaminated raw ingredients might be the reason for the high prevalence of bacteria in ready-to-eat food samples. However, the transmission of S. aureus from infected staff to food samples should be recognized as well. Foodstuff contamination with S. aureus may be directly caused by infected food animals, or their products, such as meat, or by poor hygiene throughout their processing. The low prevalence of S. aureus in salami samples could have been due to the high temperature used in their processing. A similar survey was conducted by Safarpoor Dehkordi et al. [13], in which they showed the prevalence of S. aureus in raw meat, raw chicken, grilled meat, grilled chicken, soup, salad, and rice samples collected from hospital kitchens was 26.31%, 27.02%, 16.12%, 8.53%, 6.38%, 7.14%, and 4.20%, respectively. Besides, they showed that food sample manipulation by the infected staff of hospital kitchens was the main causative factor for development of S. aureus. Hasanpour Dehkordi et al. [7] reported that the prevalence of S. aureus bacteria in diverse kinds of food samples was within the range of 10.00 and 24.00%. A high prevalence of S. aureus bacteria was also reported in diverse kinds of foodstuffs from the continents of Asia [12, 14], Europe [15,16,17,18,19,20], Africa [21], America [22, 23], and Australia [24]. In the same vein, Wu et al. [25] reported that the prevalence of S. aureus in raw meat, pork, beef, poultry and mutton, sausages, frozen meat, pork, beef, poultry, mutton, and dumpling, and ready-to-eat meat, pork, beef, poultry, and mutton samples were 51.00%, 47.70%, 50.40%, 67.90%, 54.50%, 18.60%, 43.30%, 50.00%, 31.40%, 60.90%, 30.90%, 29.40%, 12.20%, 12.70%, 25.00%, 11.80% and 0%, respectively. In addition, they reported that the prevalence of S. aureus in ready-to-eat food samples was relatively lower than that in raw products, which could have been due to processing operations, such as heating as well as the adding of additives to ready-to-eat food samples. Achi and Madubuike (2007) reported that the prevalence of S. aureus in ready-to-eat fish sausage, meat sausage, fried fish, fried meat, suya, moin moin, wash water, and rinse water samples was 23.60%, 29.70%, 8.30%, 6.60%, 17.20%, 13.40%, 27.60%, and 18.10%, respectively [26]. Similarly, they introduced water and ready-to-eat food samples as the sources of S. aureus.

Findings of the present survey showed a high prevalence of resistance to diverse classes of antibiotic agents, particularly penicillins, tetracyclines, aminoglycosides, macrolides, fluoroquinolones, phenicols, and ansamycins. Additionally, some strains harbored antibiotic resistance genes. Chloramphenicol is a forbidden antibiotic agent, which is sometimes used to treat infections in poultry. Emergence of resistance to this antibiotic may imply its unauthorized prescription. Besides, development of antibiotic resistance to chloramphenicol could indirectly imply the poultry-based origin of the isolated S. aureus bacteria. Most of the examined samples, particularly salad olivieh, chicken nuggets, and hamburgers were made from poultry meat and its products. Additionally, S. aureus bacteria isolated from salad olivieh, chicken nugget, and hamburger samples had a moderate prevalence of chloramphenicol resistance (16.66%, 80%, and 14.28%, respectively). Moreover, the prevalence of the cat1 chloramphenicol encoding gene among the S. aureus bacteria isolated from salad olivieh, chicken nugget, and hamburger samples was high, having been 27.77%, 40%, and 28.57%, respectively. Thus, the findings could indirectly verify the origin of the S. aureus isolates.

A high prevalence of multi-drug resistant S. aureus harboring resistance to tetracyclines [13, 27,28,29], phenicols [13, 27, 28], penicillins [13, 27,28,29,30] macrolides [13, 27,28,29,30], aminoglycosides [13, 27,28,29,30,31], folate inhibitors [12, 25,26,27,28,29], lincosamides [13, 27,28,29,30], fluoroquinolones [13, 27,28,29,30,31], ansamycins [13, 27,28,29], and cephems [13, 27,28,29,30] was also established by diverse studies. Besides, the high prevalence of linA, aacA-D, ermA and msrA, gyrA and grlA, blaZ, cat1, tetK and tetM, rpoB, and dfrA1 antibiotic resistance genes was reported in the current survey. Safarpoor Dehkordi et al. [13] reported that the prevalence of resistance of S. aureus bacteria isolated from processed food samples to penicillin, ceftaroline, gentamicin, amikacin, kanamycin, azithromycin, erythromycin, tetracycline, doxycycline, ciprofloxacin, levofloxacin, clindamycin, trimethoprim-sulfamethoxazole, chloramphenicol, and rifampin antibiotic agents was 100%, 10%, 81.08%, 70.27%, 43.24%, 59.45%, 86.48%, 100%, 81.08%, 48.64%, 43.24%, 48.64%, 83.78%, 29.72%, and 35.13%, respectively. Besides, they reported that the prevalence of aacA-D, tetK, tetM, msrA, ermA, ermC, and linA antibiotic resistance genes was 62.16%, 72.97%, 27.02%, 64.86%, 72.97%, 27.02%, and 43.24%, respectively. In contrast to our findings, they found that vatA (45.94%), vatB (18.91%), and vatC (5.40%) antibiotic resistance genes were among methicillin-resistant Staphylococcus aureus (MRSA) isolates. Besides, a higher prevalence of resistance to antibiotic agents was reported in their study because they assessed MRSA isolates, which according to them, harbored a higher prevalence of resistance. Fowoyo and Ogunbanwo [32] reported that the S. aureus bacteria isolated from ready-to-eat foodstuffs harbored a high prevalence of resistance to trimethoprim-sulfamethoxazole (74.90%), ampicillin (86.70%), cefotaxime (3.50%), amoxicillin-clavulanic acid (52.50%), ciprofloxacin (23.90%), oxacillin (35.70%), gentamicin (11.40%), erythromycin (15.70%), and ofloxacin (7.10%). Compared to the present research, they reported a higher prevalence of resistance to trimethoprim-sulfamethoxazole (74.90%), while a lower prevalence of resistance to erythromycin (15.70%), gentamicin (11.40%), and ciprofloxacin (23.90%) was reported by them. This finding could be due to the fact that they only assessed the antibiotic resistance pattern of the coagulase-negative staphylococcal genus. The relatively low prevalence of resistance to chloramphenicol (8.33%) may be due to its illegal and unselective prescription, especially in veterinary medicine [33, 34]. A high prevalence of tetK, blaZ, aacA-D, gyrA, and ermA antibiotic resistance genes was reported in Algeria [35], South Africa [36], China [37], and Taiwan [38]. Akanbi et al. [39] reported that blaZ, mecA, rpoB, ermB, and tetM were the most commonly identified antibiotic resistance genes among the S. aureus bacteria isolated from food samples in South Africa. A high distribution of mecA, gyrA, grlA, and cfr was reported in the S. aureus bacteria recovered from chicken meat in Egypt [40]. Consistent with the present survey, an Iranian survey [41] showed that oxacillin, gentamicin, penicillin, tetracycline, and erythromycin-resistant S. aureus bacteria, isolated from milk and dairy products, carried a high prevalence of blaZ, aacA-aphD, mecA, tetK and tetM, ermB, ermA, ermT, ermC, msrB, and msrA antibiotic resistance genes. In the same vein, a similar phenotypic profile of antibiotic resistance was reported in Iran [42] and China [43].

Findings of the present research revealed that the prevalence of resistance to more than one antibiotic agent was high among the S. aureus isolates. On the other hand, all isolated bacteria harbored resistance to at least four types of antibiotic agents. Furthermore, the prevalence of resistance to more than eight antibiotic agents was 28.12%. Moreover, the isolates harbored the concurrent presence of two antibiotic resistance genes, particularly aacA-D + blaZ, tetK + blaZ, aacA-D + tetK, aacA-D + gyrA, and ermA + blaZ together. A high prevalence of multi-drug resistant S. aureus was reported in previous investigations as well [44,45,46]. However, the literature review showed no report on the prevalence of gyrA, vatC, blaZ, vatA, cat1, rpoB, dfrA, linA, vatB, msrA, aacA-D, ermA, grlA, tetK, and tetM genes among the S. aureus bacteria recovered from ready-to-eat food samples. The methylase enzyme modulates the most important mechanism involving resistance to clindamycin, often encoded by the ermA gene [47]. The majority of our isolates carried two tetracyclines, two erythromycins, one macrolide, and several streptogramin resistance genes. According to research, the presence of the tetK gene on small multicopy plasmids and tetM on conjugative transposons makes them spread [48]. Some of the S. aureus bacteria harbored the ermA gene that is often located on small multicopy plasmids present in many different staphylococcal species. The ermA gene is usually carried by transposons, which explains its high prevalence among the S. aureus bacteria. The blaZ gene encoding beta-lactamase production mainly causes resistance to benzylpenicillin. Our results suggest that blaZ may play a major role in the occurrence of resistance to penicillins, but it cannot be used alone as an indicator for penicillin resistance.

Conclusion

In conclusion, the high prevalence of S. aureus in the examined samples, particularly in grilled mushrooms and olivieh salad and a high prevalence of resistance to diverse classes of antibiotic agents and different antibiotic resistance genes were reported in this study. A high prevalence of resistance to penicillin, tetracycline, gentamicin, erythromycin, trimethoprim-sulfamethoxazole, and ciprofloxacin antibiotic agents as well as the presence of tetK, blaZ, aacA-D, gyrA, and ermA antibiotic resistance genes were reported in the present survey. Furthermore, the high prevalence of multi-drug resistant bacteria and the presence of aacA-D + blaZ, tetK + blaZ, aacA-D + tetK, aacA-D + gyrA, and ermA + blaZ genes together may indicate the leading role of ready-to-eat food samples in the transmission of antibiotic-resistant S. aureus to human populations. Accordingly, the use of high-quality raw materials, proper hygienic food-processing conditions, the adequate cooking of food samples, cross-contamination prevention, and antibiotic prescription rendering the outcomes of disk diffusion could diminish the risk of antibiotic-resistant S. aureus in the examined samples. Further surveys are recommended to be conducted to illuminate other epidemiological aspects of antibiotic-resistant S. aureus in ready-to-eat food samples.

Methods

Samples

From April to November 2018, a total of 415 different kinds of ready-to-eat food samples, such as hamburgers (n = 75), chicken nuggets (n = 70), salad olivieh (n = 60), salami (n = 60), falafel (n = 50), grilled mushrooms (n = 50), and Mexican corn (n = 50) were randomly collected from the fast-food restaurants of the Tehran province, Iran. Sampling was performed in highly consumed ready-to-eat food samples. According to the low diversity of ready-to-eat food-producing restaurants in Iran, sampling was done in all of them. To this end, simple stratified sampling was performed according to the production volume of each fast food unit. Besides, the samples (100 g) were directly delivered to the Food Hygiene Research Center. In addition, the food samples were transported in cool boxes with ice packs.

S. aureus isolation and identification

As many as 20 g of each collected ready-to-eat food sample was blended with 225 mL of buffered peptone water (Merck, Germany). Next, the solutions were homogenized using a stomacher (Interscience, Saint-Nom, France). Consequently, 5 mL of the produced solution was transferred to 50 mL of Trypticase Soy Broth (TSB, Merck, Germany) supplemented with 10% NaCl and 1% sodium pyruvate, which was then incubated for 18 h at 35 °C. Next, a loopful culture was transferred to the Baird-Parker agar supplemented with an egg yolk tellurite emulsion (Merck, Germany) and incubated at 37 °C for about 24 h. Black shiny colonies surrounded with 2- to 5-mm clear zones were identified based on gram staining, hemolytic activity on the sheep blood agar (Merck, Germany), catalase test, coagulase test (rabbit plasma), oxidase test, OF glucose test, bacitracin sensitivity test (0.04 U), mannitol fermentation on the Mannitol salt agar (Merck, Germany), urease activity, nitrate reduction, phosphatase, deoxyribonuclease (DNase, Merck, Germany) test, Voges-Proskauer (VP) (Merck, Germany) test, and carbohydrate (xylose, sucrose, trehalose and maltose, fructose, lactose, and mannose) fermentation test [13].

Phenotypic assessment of antibiotic resistance

The phenotypic pattern of antibiotic resistance in S. aureus bacteria was investigated using the disk diffusion method on the Mueller–Hinton agar (Merck, Germany). For this purpose, the principles of the Clinical Laboratory Standard Institute (CLSI) were used [49]. Accordingly, various kinds of antibiotic agents, including aminoglycosides (amikacin (30 µg/disk) and gentamicin (10 µg/disk)), fluoroquinolones (levofloxacin (5 µg/disk) and ciprofloxacin (5 µg/disk)), lincosamides (clindamycin (2 µg/disk)), macrolides (erythromycin (15 µg/disk) and azithromycin (15 µg/disk)), penicillins (penicillin (10 µg/disk)), tetracyclines (doxycycline (30 µg/disk) and tetracycline (30 µg/disk)), phenicols (chloramphenicol (30 µg/disk)), folate pathway inhibitors (trimethoprim-sulfamethoxazole (25 µg/disk)) and ansamycins (rifampin (5 µg/disk)) were used (Oxoid, UK). The test was performed using the protocol already explained [49,50,51,52]. Besides, S. aureus (ATCC 43,300) was used as a quality control organism to determine antimicrobial susceptibility.

Genotypic assessment of antibiotic resistance

S. aureus isolates were sub-cultured on TSB media (Merck, Germany) and incubated for 48 h at 37 °C. Besides, genomic DNA was extracted from bacterial colonies using the DNA extraction kit (Thermo Fisher Scientific, St. Leon-Rot, Germany) according to the manufacturer's instructions. Next, the purity (A260/A280) and concentration of the extracted DNA were checked (NanoDrop, Thermo Scientific, Waltham, MA, USA). In addition, the DNA's quality was assessed on a 2% agarose gel stained with ethidium bromide (0.5 μg/mL) (Thermo Fisher Scientific, St. Leon-Rot, Germany) [53, 54].

Table 5 shows the PCR conditions met for genotypic assessment of antibiotic resistance [48, 55,56,57,58,59,60,61]. A programmable DNA thermocycler (Eppendorf Mastercycler 5330, Eppendorf-Nethel-Hinz GmbH, Hamburg, Germany) was used in all PCR reactions. In addition, amplified samples were analyzed by electrophoresis (120 V/208 mA) in a 2.5% agarose gel that was stained with 0.1% ethidium bromide (0.4 µg/ml). Besides, UVI doc gel documentation systems (Grade GB004, Jencons PLC, London, UK) were used to analyze images.

Table 5 PCR circumstances used for genotypic assessment of antibiotic resistance [48, 55,56,57,58,59,60,61]
Full size table

Statistical analysis

Statistical analysis was performed by SPSS Statistics 21.0 (SPSS Inc., Chicago, IL, USA). Chi-square and Fisher's exact two-tailed tests were performed to assess any significant relationship between the prevalence of S. aureus bacteria and their phenotypic and genotypic properties of antibiotic resistance. Besides, p-value < 0.05 was considered statistically significant [62].

Availability of data and materials

All data generated or analyzed throughout this research are included in this published article.

Abbreviations

S. aureus :

Staphylococcus aureus

PCR:

Polymerase chain reaction

SPSS:

Statistical package for the social sciences

References

  1. Eslami A, Gholami Z, Nargesi S, Rostami B, Avazpour M. Evaluation of microbial contamination of ready-to-eat foods (pizza, frankfurters, sausages) in the city of Ilam. Environ Health Eng Manag J. 2017;4:117–22.

    Article  CAS  Google Scholar 

  2. Oje O, Ajibade V, Fajilade O, Ajenifuja O. Microbiological analysis of ready-to-eat (rte) foods vended in mobile outlet catering units from Nigeria. J Adv Food Sci Technol. 2018;5:15–9.

    Google Scholar 

  3. Wang L, Ruan S. Modeling nosocomial infections of methicillin-resistant Staphylococcus aureus with environment contamination. Sci Rep. 2017;7:580.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Fijałkowski K, Peitler D, Karakulska J. Staphylococci isolated from ready-to-eat meat–identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol. 2016;238:113–20.

    Article  PubMed  CAS  Google Scholar 

  5. Yang X, Zhang J, Yu S, Wu Q, Guo W, Huang J, Cai S. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail ready-to-eat foods in China. Front Microbiol. 2016;7:816.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Islam MA, Parveen S, Rahman M, Huq M, Nabi A, Khan ZUM, Ahmed N, Wagenaar JA. Occurrence and characterization of methicillin resistant Staphylococcus aureus in processed raw foods and ready-to-eat foods in an urban setting of a developing country. Front Microbiol. 2019;10:503.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hasanpour Dehkordi A, Khaji L, Sakhaei Shahreza M, Mashak Z, Safarpoor Dehkordi F, Safaee Y, Hosseinzadeh A, Alavi I, Ghasemi E, Rabiei-Faradonbeh M. One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat. Trop Biomed. 2017;34:396–404.

    CAS  PubMed  Google Scholar 

  8. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA. 2007;298:1763–71.

    Article  CAS  PubMed  Google Scholar 

  9. Li B, Webster TJ. Bacteria antibiotic resistance: new challenges and opportunities for implant-associated orthopedic infections. J Orthop Res. 2018;36:22–32.

    PubMed  Google Scholar 

  10. Madahi H, Rostami F, Rahimi E, Dehkordi FS. Prevalence of enterotoxigenic Staphylococcus aureus isolated from chicken nugget in Iran. Jundishapur J Microbiol. 2014. https://doi.org/10.5812/jjm.10237.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Abdolmaleki Z, Mashak Z, Dehkordi FS. Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrob Resist Infect Control. 2019;8:54.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kwon NH, Park KT, Jung WK, Youn HY, Lee Y, Kim SH, Bae W, Lim JY, Kim JY, Kim JM. Characteristics of methicillin resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet Microbiol. 2006;117:304–12.

    Article  CAS  PubMed  Google Scholar 

  13. Safarpoor Dehkordi F, Gandomi H, Akhondzadeh Basti A, Misaghi A, Rahimi E. Phenotypic and genotypic characterization of antibiotic resistance of methicillin-resistant Staphylococcus aureus isolated from hospital food. Antimicrob Resist Infect Control. 2017;6:104.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Uji T, Kitagawa H. Characterization of methicillin-resistant Staphylococcus aureus isolated from retail raw chicken meat in Japan. J Vet Med Sci. 2005;67:107–10.

    Article  CAS  PubMed  Google Scholar 

  15. Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia N, Parisi A, Greco G, Bellacicco A, Virgilio S, Celano G. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int J Food Microbiol. 2007;117:219–22.

    Article  CAS  PubMed  Google Scholar 

  16. De Boer E, Zwartkruis-Nahuis J, Wit B, Huijsdens X, De Neeling A, Bosch T, Van Oosterom R, Vila A, Heuvelink A. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol. 2009;134:52–6.

    Article  PubMed  CAS  Google Scholar 

  17. Gundogan N, Citak S, Yucel N, Devren A. A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci. 2005;69:807–10.

    Article  CAS  PubMed  Google Scholar 

  18. Richter A, Sting R, Popp C, Rau J, Tenhagen B-A, Guerra B, Hafez H, Fetsch A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol Infect. 2012;140:2223–32.

    Article  CAS  PubMed  Google Scholar 

  19. Tang Y, Larsen J, Kjeldgaard J, Andersen PS, Skov R, Ingmer H. Methicillin-resistant and-susceptible Staphylococcus aureus from retail meat in Denmark. Int J Food Microbiol. 2017;249:72–6.

    Article  CAS  PubMed  Google Scholar 

  20. Fox A, Pichon B, Wilkinson H, Doumith M, Hill R, McLauchlin J, Kearns A. Detection and molecular characterization of livestock-associated MRSA in raw meat on retail sale in North West England. Lett Appl Microbiol. 2017;64:239–45.

    Article  CAS  PubMed  Google Scholar 

  21. Karmi M. Prevalence of methicillin-resistant Staphylococcus aureus in poultry meat in Qena, Egypt. Vet World. 2013;6:711–5.

    Article  Google Scholar 

  22. Costa WLR, Ferreira JDS, Carvalho JS, Cerqueira ES, Oliveira LC, Almeida RCDC. Methicillin-resistant Staphylococcus aureus in raw meats and prepared foods in public hospitals in Salvador, Bahia, Brazil. J Food Sci. 2015;80:M147–50.

    Article  CAS  PubMed  Google Scholar 

  23. Ge B, Mukherjee S, Hsu C-H, Davis JA, Tran TTT, Yang Q, Abbott JW, Ayers SL, Young SR, Crarey ET. MRSA and multidrug-resistant Staphylococcus aureus in US retail meats, 2010–2011. Food Microbiol. 2017;62:289–97.

    Article  PubMed  Google Scholar 

  24. Ou Q, Peng Y, Lin D, Bai C, Zhang T, Lin J, Ye X, Yao Z. A meta-analysis of the global prevalence rates of Staphylococcus aureus and methicillin-resistant S. aureus contamination of different raw meat products. J Food Prot. 2017;80:763–74.

    Article  Google Scholar 

  25. Wu S, Huang J, Wu Q, Zhang J, Zhang F, Yang X, Wu H, Zeng H, Chen M, Ding Y. Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity. Front Microbiol. 2018. https://doi.org/10.3389/fmicb.2018.02767.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Achi O, Madubuike C. Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from retail ready-to-eat foods in Nigeria. Res J Microbiol. 2007;2:516–23.

    Article  Google Scholar 

  27. Momtaz H, Dehkordi FS, Rahimi E, Asgarifar A, Momeni M. Virulence genes and antimicrobial resistance profiles of Staphylococcus aureus isolated from chicken meat in Isfahan province, Iran. J Appl Poultry Res. 2013;22:913–21.

    Article  CAS  Google Scholar 

  28. Paludi D, Vergara A, Festino AR, Di Ciccio P, Costanzo C, Conter M, Zanardi E, Ghidini S, Ianieri A. Antimicrobial resistance pattern of methicillin-resistant Staphylococcus aureus in the food industry. J Biol Regul Homeost Agents. 2011;25:671.

    CAS  PubMed  Google Scholar 

  29. Sallam KI, Abd-Elghany SM, Elhadidy M, Tamura T. Molecular characterization and antimicrobial resistance profile of methicillin-resistant Staphylococcus aureus in retail chicken. J Food Prot. 2015;78:1879–84.

    Article  CAS  PubMed  Google Scholar 

  30. Jackson CR, Davis JA, Barrett JB. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol. 2013;51:1199–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Daka D, Yihdego D. Antibiotic-resistance Staphylococcus aureus isolated from cow’s milk in the Hawassa area, South Ethiopia. Ann Clin Microbiol Antimicrob. 2012;11:26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fowoyo P, Ogunbanwo S. Antimicrobial resistance in coagulase-negative staphylococci from Nigerian traditional fermented foods. Ann Clin Microbiol Antimicrob. 2017;16:4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Aalipour F, Mirlohi M, Jalali M. Determination of antibiotic consumption index for animal originated foods produced in animal husbandry in Iran, 2010. J Environ Health Sci Eng. 2014;12:1–7.

    Article  CAS  Google Scholar 

  34. Rahi A, Kazemeini H, Jafariaskari S, Seif A, Hosseini S, Dehkordi FS. Genotypic and phenotypic-based assessment of antibiotic resistance and profile of staphylococcal cassette chromosome mec in the methicillin-resistant Staphylococcus aureus recovered from raw milk. Infect Drug Resist. 2020;13:273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Achek R, Hotzel H, Cantekin Z, Nabi I, Hamdi TM, Neubauer H, El-Adawy H. Emerging of antimicrobial resistance in staphylococci isolated from clinical and food samples in Algeria. BMC Res Notes. 2018;11:663.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Pekana A, Green E. Antimicrobial resistance profiles of Staphylococcus aureus isolated from meat carcasses and bovine milk in abattoirs and dairy farms of the Eastern Cape, South Africa. Int J Environ Res Public Health. 2018;15:2223.

    Article  CAS  PubMed Central  Google Scholar 

  37. Li S-M, Zhou Y-F, Li L, Fang L-X, Duan J-H, Liu F-R, Liang H-Q, Wu Y-T, Gu W-Q, Liao X-P. Characterization of the multi-drug resistance gene cfr in methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from animals and humans in China. Front Microbiol. 2018;9:2925.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Wang YT, Lin YT, Wan TW, Wang DY, Lin HY, Lin CY, Chen YC, Teng LJ. Distribution of antibiotic resistance genes among Staphylococcus species isolated from ready-to-eat foods. J Food Drug Anal. 2019;27:841–48.

  39. Akanbi OE, Njom HA, Fri J, Otigbu AC, Clarke AM. Antimicrobial susceptibility of Staphylococcus aureus isolated from recreational waters and beach sand in Eastern Cape Province of South Africa. Int J Environ Res Public Health. 2017;14:1001.

    Article  PubMed Central  CAS  Google Scholar 

  40. Osman K, Badr J, Al-Maary KS, Moussa IM, Hessain AM, Girah Z, Amin M, Abo-shama UH, Orabi A, Saad A. Prevalence of the antibiotic resistance genes in coagulase-positive-and negative-staphylococcus in chicken meat retailed to consumers. Front Microbiol. 2016;7:1846.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Jamali H, Paydar M, Radmehr B, Ismail S, Dadrasnia A. Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control. 2015;54:383–8.

    Article  CAS  Google Scholar 

  42. Shahraz F, Dadkhah H, Khaksar R, Mahmoudzadeh M, Hosseini H, Kamran M, Bourke P. Analysis of antibiotic resistance patterns and detection of mecA gene in Staphylococcus aureus isolated from packaged hamburger. Meat Sci. 2012;90:759–63.

    Article  CAS  PubMed  Google Scholar 

  43. Rong D, Wu Q, Xu M, Zhang J, Yu S. Prevalence, virulence genes, antimicrobial susceptibility, and genetic diversity of Staphylococcus aureus from retail aquatic products in China. Front Microbiol. 2017;8:714.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Chaję̨cka-Wierzchowska W, Zadernowska A, Nalepa B, Sierpinska M, Łaniewska-Trokenheim Ł. Retail ready-to-eat food as a potential vehicle for Staphylococcus spp. harboring antibiotic resistance genes. J Food Prot. 2014;77:993–8.

  45. Aung KT, Hsu LY, Koh TH, Hapuarachchi HC, Chau ML, Gutiérrez RA, Ng LC. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in retail food in Singapore. Antimicrob Resist Infect Control. 2017;6:94.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Contreras CPÁ, da Silva LNN, Ferreira DCG, dos Santos FJ, de Castro Almeida RC. Prevalence of methicillin-resistant Staphylococcus aureus in raw hamburgers and ready-to-eat sandwiches commercialized in supermarkets and fast food outlets in Brazil. Food Nutr Sci. 2015;6:1324.

    CAS  Google Scholar 

  47. Zelazny AM, Ferraro MJ, Glennen A, Hindler JF, Mann LM, Munro S, Murray PR, Reller LB, Tenover FC, Jorgensen JH. Selection of strains for quality assessment of the disk induction method for detection of inducible clindamycin resistance in staphylococci: a CLSI collaborative study. J Clin Microbiol. 2005;43:2613–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Johler S, Layer F, Stephan R. Comparison of virulence and antibiotic resistance genes of food poisoning outbreak isolates of Staphylococcus aureus with isolates obtained from bovine mastitis milk and pig carcasses. J Food Prot. 2011;74:1852–9.

    Article  CAS  PubMed  Google Scholar 

  49. CLSI. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement. CLSI document M100-S25. 2015.

  50. Ranjbar R, Farsani FY, Dehkordi FS. Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk. Antimicrob Resist Infect Control. 2018;7:1–4.

    Article  Google Scholar 

  51. Ranjbar R, Seif A, Safarpoor DF. Prevalence of antibiotic resistance and distribution of virulence factors in the shiga toxigenic Escherichia coli recovered from hospital food. Jundishapur J Microbiol. 2019;12: e82659.

    CAS  Google Scholar 

  52. Ranjbar R, Yadollahi Farsani F, Safarpoor DF. Antimicrobial resistance and genotyping of vacA, cagA, and iceA alleles of the Helicobacter pylori strains isolated from traditional dairy products. J Food Saf. 2019;39: e12594.

    Article  CAS  Google Scholar 

  53. Dehkordi FS, Haghighi N, Momtaz H, Rafsanjani MS, Momeni M. Conventional vs real-time PCR for detection of bovine herpes virus type 1 in aborted bovine, buffalo and camel foetuses, Bulgarian. J Vet Med. 2013;16(2):102–11.

    Google Scholar 

  54. Dehkordi FS, Valizadeh Y, Birgani TA, Dehkordi KG. Prevalence study of Brucella melitensis and Brucella abortus in cow’s milk using dot enzyme linked immuno sorbent assay and duplex polymerase chain reaction. J Pure Appl Microbiol. 2014;8(2):1065–9.

    CAS  Google Scholar 

  55. Lina G, Quaglia A, Reverdy M-E, Leclercq R, Vandenesch F, Etienne J. Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother. 1999;43:1062–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Strommenger B, Kettlitz C, Werner G, Witte W. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol. 2003;41:4089–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Baddour M, AbuElKheir M, Fatani A. Comparison of mecA polymerase chain reaction with phenotypic methods for the detection of methicillin-resistant Staphylococcus aureus. Curr Microbiol. 2007;55:473.

    Article  CAS  PubMed  Google Scholar 

  58. Van TTH, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol. 2008;124:217–23.

    Article  CAS  PubMed  Google Scholar 

  59. Schmitz FJ, Köhrer K, Schering S, Verhoef J, Fluit A, Heinz HP, Jones ME. The stability of grlA, grlB, gyrA, gyrB and norA mutations and MIC values of five fluoroquinolones in three different clonal populations of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect. 1999;5:287–90.

    Article  CAS  PubMed  Google Scholar 

  60. Shittu AO, Okon K, Adesida S, Oyedara O, Witte W, Strommenger B, Layer F, Nübel U. Antibiotic resistance and molecular epidemiology of Staphylococcus aureus in Nigeria. BMC Microbiol. 2011;11:92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Aboshkiwa M, Rowland G, Coleman G. Nucleotide sequence of the Staphylococcus aureus RNA polymerase rpoB gene and comparison of its predicted amino acid sequence with those of other bacteria. Biochim Biophys Acta (BBA) Gene Struct Expr. 1995;1262:73–8.

    Article  Google Scholar 

  62. Dehkordi FS. Prevalence study of Bovine viral diarrhea virus by evaluation of antigen capture ELISA and RT-PCR assay in Bovine, Ovine, Caprine, Buffalo and Camel aborted fetuses in Iran. AMB Express. 2011;1:1–6.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to extend their gratitude to prof. Eslampour and prof. Kohdar for their valuable guide. In addition, the present survey was monetarily supported by the Islamic Azad University, Karaj Branch, Karaj, Iran. The authors would like to thank the Research Deputy of the Islamic Azad University, Science and Research Branch, Tehran, Iran, for supporting the current research.

Funding

The authors of this study supported it financially.

Author information

Authors and Affiliations

  1. Faculty of Veterinary Medicine, Karaj Branch, Islamic Azad University, Karaj, Iran

    Arash Mesbah

  2. Department of Food Hygiene, Karaj Branch, Islamic Azad University, Karaj, Iran

    Zohreh Mashak

  3. Department of Pharmacology, Karaj Branch, Islamic Azad University, Karaj, Iran

    Zohreh Abdolmaleki

Authors
  1. Arash Mesbah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zohreh Mashak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zohreh Abdolmaleki
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZM designed the study and performed the culture-based identification and PCR genetic alignment tasks. AM and ZA supported the study and performed sample collection, disk diffusion, and statistical analysis. In addition, AM wrote and drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Zohreh Mashak.

Ethics declarations

Ethics approval and consent to participate

The present study was approved by the Ethics Committee of the Faculty of Veterinary Medicine, Karaj Branch, Islamic Azad University, Karaj, Iran. This research and licenses related to the sampling process were approved by Dr. Zohreh Abdolmaleki and Dr. Zohreh Mashak (Approval ref. no. 25277).

Consent for publication

There was no consent to publish the work.

Competing interests

The authors declare that there is no conflict of interests regarding the publication of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mesbah, A., Mashak, Z. & Abdolmaleki, Z. A survey of prevalence and phenotypic and genotypic assessment of antibiotic resistance in Staphylococcus aureus bacteria isolated from ready-to-eat food samples collected from Tehran Province, Iran. Trop Med Health 49, 81 (2021). https://doi.org/10.1186/s41182-021-00366-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s41182-021-00366-4

Keywords

  • Staphylococcus aureus
  • Prevalence
  • Phenotype of antibiotic resistance
  • Genotype of antibiotic resistance
  • Ready-to-eat food

Tropical Medicine and Health

ISSN: 1349-4147

Contact us