S. aureus is considered as one of the most common causes of nosocomial infections, as well as the cause of most cases of food poisoning in hospitals [4, 20]. Hospital meals are an indispensable portion of patient care. Safe and complete meals can encourage patients to eat well and giving them the nutrients they need to recover from surgery or illness.
Foodstuff contamination with S. aureus may occur directly from infected food-producing animals or may result from poor hygiene during production processes, or the retail and storage of food, since humans may also harbor microorganisms. The current research is the first report of the biotyping and molecular characterization of antibiotic resistance in the MRSA strains isolated from various types of raw and cooked hospital food samples. Findings obtained from this research revealed that the prevalence of S. aureus in different types of hospital food samples was 9.69%. The prevalence rate of the S. aureus in hospital food samples of our research was higher than that of Spain (6.10%) [21] and Iran (6.42%) [22], Portugal (11.10%) [23] and Brazil (50%) [24].
Investigations conducted in the U.S. as well as numerous other countries, including Canada, Taiwan, China, Denmark, South Korea, Austria, France, Belgium, Italy, and The Netherlands, have isolated MRSA mainly from different types of foods [4, 20]. Costa et al. (2015) [25] revealed that 28.10% of hospital food samples harbored MRSA strains. They showed that the prevalence of MRSA strains in beef, chicken, pork and fish samples were 23.30, 23.30, 37.50 and 30%, respectively which was higher than that found in our study.
Biotyping is a simple method used to trace the origin of S. aureus strains isolated from food samples. The results of our study showed that all of the MRSA strains isolated from rice, salad and soup samples were derived from humans. Furthermore, 48.64% of MRSA isolates of hospital food samples had human origin. Generally, the results revealed the role of infected humans in the dissemination and also transmission of MRSA strains to hospital food samples. The role of food handlers in transmission of MRSA strains into the food samples has also been reported by Castro et al. (2016) [23], Ferreira et al. (2014) [24], Costa et al. (2015) [25] and Ayçiçek et al. (2004) [26]. A study which was conducted by Kitai et al. (2005) [27] supported the high prevalence of poultry-based biotypes found in our investigation (71.42%). They reported that about 80% of all S. aureus isolates of foodstuffs belonged to the poultry-based biotypes, while prevalence of human-based biotypes was 22.10%. Normanno et al. (2007) [28] revealed that the prevalence of human, ovine, not-host-specific, bovine and poultry-based biotypes of the S. aureus isolates of Italian food samples were 50.40, 23.20, 17.60, 7.20 and 1.60%, respectively.
S. aureus causes food intoxication and doesn’t lead to food infection [2, 3]. Therefore, the risk of MRSA contaminated hospital food might be due to the cross-contamination. High prevalence of MRSA strains in cooked food samples may be due to the cross-contamination of cooked foods through food handlers and kitchen equipment.
Our results showed that the antibiotic resistance pattern and prevalence of the antibiotic resistance genes were highly dependent to the biotypes of the MRSA strains. The human-based biotypes of the MRSA strains harbored higher prevalence of resistance against human-based antibiotics including ceftaroline, amikacin, kanamycin, azithromycin, doxycycline, ciprofloxacin, levofloxacin, clindamycin and rifampin. Furthermore, animal-based biotypes harbored higher prevalence of resistance against animal-based antibiotics or those which are routine in veterinary medicine including penicillin, gentamicin, erythromycin, tetracycline, trimethoprim-sulfamethoxazole and chloramphenicol. Poultry-based biotypes of the MRSA strains had a higher prevalence of resistance against chloramphenicol (P < 0.05). It may be due to the higher prescription of chloramphenicol in aviculture. MRSA strains of our study harbored the highest prevalence of resistance against antibiotics of the penicillins, cephems and tetracyclines groups. There were no previously published data about the relations between biotypes and prevalence of antibiotic resistance in the MRSA strains. Similar antibiotic resistance patterns of the MRSA strains isolated from different types of food and clinical samples have also been reported against aminoglycosides [29,30,31,32,33], cephems [29, 31,32,33], penicillins [29, 31,32,33], macrolides [29,30,31,32,33], tetracyclines [29, 31, 32], fluoroquinolones [29,30,31,32,33], lincosamides [29,30,31,32], folate inhibitors [29,30,31,32,33], phenicols [29, 31, 32] and ansamycins [29, 31, 32] groups of antibiotics. Fowoyo and Ogunbanwo (2017) [34] reported that the S. aureus strains isolated from ready to eat foodstuffs exhibited the high prevalence of resistance against ampicillin (86.70%), trimethoprim–sulfamethoxazole (74.90%), amoxicillin–clavulanic acid (52.50%), cefotaxime (3.50%), oxacillin (35.70%), ciprofloxacin (23.90%), erythromycin (15.70%), gentamicin (11.40%) and ofloxacin (7.10%). Rong et al. (2017) [35] reported that the prevalence of antibiotic resistance in the S. aureus strains isolated from different types of food samples against ampicillin, penicillin, amoxicillin–clavulanic acid, cefoxitin, ceftazidime, cefepime, kanamycin, streptomycin, amikacin, gentamicin, norfloxacin, ciprofloxacin, erythromycin, tetracycline, clindamycin, chloramphenicol, trimethoprim-sulfamethoxazole, vancomycin and rifampicin were 88.20, 88.20, 73.90, 8.40, 10.90, 8.40, 22.70, 14.30, 1.70, 4.20, 6.70, 5.00, 53.80, 26.90, 12.60, 7.507.50, 0 and 2.50%, respectively. MRSA strains should resist completely against all types of beta-lactams and penicillins [17], but it is surprising that some studies show that the MRSA strains isolated from food and also clinical samples don’t have complete resistance against several types of beta-lactams and also penicillins [36, 37].
Most of the tetracycline-resistant MRSA strains harbored tetK and tetM genes. Prevalence of aacA-D gene was high among gentamicin, amikacin and kanamycin-resistant MRSA strains. Prevalence of msrA, ermA and ermC and linA were also significant among the macrolide, erythromycin and clindamycin-resistant MRSA strains. Therefore, the pattern of the antibiotic resistance of the MRSA strains of hospital food samples was confirmed by the PCR amplification of the specific antibiotic resistance genes. MRSA strains of our study had considerable prevalence of resistance against clindamycin (48.64%). The most imperative mechanism involving resistance against clindamycin is modulated by methylase enzyme which often encoded by ermA and ermC genes [38]. Prevalence of ermA and ermC antibiotic resistance genes among the MRSA strains of our research were 72.97 and 27.02%, respectively. Majority of our isolates carried two tetracyclines, two erythromycins, one macrolide and several streptogramin resistance determinants reveals a great diffusion of these types of resistance. TetK, ermA, msrA and aacA-D which encode resistance against tetracycline, erythromycin, macrolides and aminoglycosides were the most commonly detected antibiotic resistance genes in the MRSA strains isolated of hospital food samples. The literature survey did not indicate any report on the prevalence of vatA, vatB, vatC, msrA, ermA, ermC, linA, aacA-D, tetK and tetM genes among the MRSA strains of hospital food samples. Kumar et al. (2010) [39] reported that the most commonly identified antibiotic resistance genes among the S. aureus isolates of food samples were linA (51.60%), msrB (46.10%), tetK (34.40%), tetM (34.40%), msrA (26.60%) and aacA-D (26.60%). Karataş et al. (2017) [40] revealed the higher prevalence of ermA than ermc antibiotic resistance genes among the clindamycin, erythromycin and telithromycin-resistant and also higher prevalence of tetM than tetK antibiotic resistance genes among the tetracycline-resistant MRSA strains which were similar to our findings. Our results were also similar with those of the previous research which was conducted by Simeoni et al. (2008) [41]. They reported that the prevalence of tetM, tetO, tetK, ermA, ermB, ermC, aac, blaZ and mecA antibiotic resistance genes amongst the S. aureus strains isolated from meat samples were 100, 0, 91.66, 16.66, 33.33, 58.33, 0, 100 and 58.33%, respectively. High prevalence of tetK and tetM antibiotic resistance genes in the MRSA isolates can be clarified by their usual genetic locations. Presence of tetK gene on small multicopy plasmids and tetM on conjugative transposons contributes to the spread of these determinants [42]. Some of the MRSA strains harbored ermC gene. This gene is often located on small multicopy plasmids which are present in many different staphylococcal species [42]. The ermA gene is usually carried by transposons which could explain its high prevalence amongst the MRSA strains. Resistance to aminoglycosides (43.24 to 81.08%) which encode by the aacA-D gene (62.16%) is more prevalent amongst the human-based biotypes. It is because of this gene is usually more diffused in staphylococci of human origin [42]. Johler et al. (2011) [42] reported that prevalence of ermC, tetK and tetM antibiotic resistance genes among the S. aureus strains isolated from cases of food poisoning, milk and pork were 25, 4.87 and 0%, 50, 0 and 12.82 and 0%, 12.19, and 53.84%, respectively. Podkowik et al. (2012) [43] reported that the prevalence of tetracycline resistance genes (tetO, tetK and tetM) and erythromycin resistance methylase gene (ermA, ermB and ermC) among the S. aureus strains isolated from ready to eat meat products were 44 and 60%, respectively.