The use of mobile phones provides many advantages; however, it may be a source of pathogen contamination, such as with S. aureus [1]. S. aureus has emerged as a major pathogen for both hospital and community-acquired infections. It can contaminate food or material products during preparation and processing. S. aureus can survive in dry and stressful environments such as the nose, skin, clothing, and surfaces [15]. These characteristics support the growth of S. aureus in many food products [9]. In addition, S. aureus can remain viable on hands and environmental surfaces for a long time after contact [16]. Hands may contaminate mobile phones at the time of use, especially when it is hot and humid and the hands are sweaty [17]. For all these reasons, there is no doubt that S. aureus is possibly present on the mobile phones of people in various occupations, such as healthcare workers, hospital staff, medical students [18], university students [19], or even the food vendors in this study. However, no study has previously assessed the contamination of S. aureus on the mobile phones of food vendors. Our study showed that 12.8% of mobile phones were contaminated with S. aureus among the ready-to-eat food vendors; this is within the prevalence range reported for previously studied samples. This result also agreed with the detection of isolates in ready-to-eat food samples in northeast Thailand [4]. Accordingly, many of the advantages of mobile phones including 1) the better quality and flexibility of service offered to customers, 2) the ability to accept payments wirelessly, 3) increased ability to communicate in and out of the workplace, 4) greater access to modern apps and services, and 5) improved networking capabilities resulted in their contamination by S. aureus among food vendors either on walking streets (11.5%) or in food centers (14.2%); the prevalence in these two settings was not significantly different (p > 0.05). It is concluded that the mobile phone is one of the potential vehicles for S. aureus dissemination into food during food preparation regardless of the size of the food shop.
S. aureus enterotoxin is the major cause of food poisoning and other public health problems in developing countries [20]. In Thailand, many episodes of foodborne disease outbreaks have occurred without investigation of the causative agents due to 1) not being able to immediately collect the relevant food samples and 2) a much higher incidence as sporadic cases of S. aureus infection are not adequately reported. It is only known that S. aureus is the third most common causative agent of foodborne illness in Thailand [21]. Conversely, several studies have assessed the detection rates of SEs in food samples such as ready-to-eat foods [22] and retail chicken meat [23]. In this study, SE genes were detected in 61.2% (30/49) of all isolates from samples collected from the mobile phones of food vendors. The sea gene was found at a higher frequency than others. The present results agreed with several previous studies reporting that sea was the most common gene in S. aureus isolated from food [22, 23, 24]. However, sed, sej, and ser were not detected in our study, which did not agree with a previous study reporting the presence of these genes in food poisoning cases and food. Additionally, sed, sej, and ser are known to be located on plasmids. In our study, eight se genotypes were observed and 23.4% of isolates possessed more than one SE gene: sea-sec (6.7%), sea-sem (6.7%), seb-sem (6.7%), and sec-sel-seq (3.3%). However, the onset of S. aureus-mediated food poisoning is abrupt. Abdominal cramps, nausea, and vomiting are the most common symptoms but the infection is generally self-limiting and resolves within 24–48 h. The conclusive diagnostic criteria of S. aureus food poisoning are based on the detection of SEs in food or exposure to at least 105 cell/g from food [25]. Therefore, the toxigenic S. aureus detected on mobile phones should be further analyzed for the phenotypes of toxin production and also detected in the relevant food samples for food safety.
The growing problem of AMR is a major public health concern. Although most studies of AMR surveillance have focused on healthcare and agriculture settings, AMR in humans and environments has also been reported. Staphylococci are commonly found in built environments. Multiple studies have indicated that AMR bacteria, including S. aureus, can be transmitted to humans in public environments including on buses [26], at railway stations [27], and in classrooms [28]. Presently, much evidence of AMR S. aureus contaminating mobile phones has been derived from healthcare settings where it causes nosocomial infection. S. aureus resistant to ampicillin, oxacillin, ceftazidime, vancomycin, and amoxicillin was isolated from the mobile devices of students in the health sector [29]. Additionally, S. aureus isolates resistant to ceftazidime (50%), gentamycin (40.9%), ciprofloxacin (40.9%), tetracycline (36.4%), chloramphenicol (31.8%), imipenem (27.3%), and azithromycin (27.3%) were isolated from the mobile phones of healthcare workers in Bangladesh [2]. However, there is no known surveillance of AMR S. aureus on the mobile phones of food vendors. Only S. aureus isolates resistant to erythromycin, ciprofloxacin, oxacillin, and cefoxitin were detected in processed raw meat/fish samples of ready-to-eat foods in other settings [30]. This study’s results regarding the AMR of S. aureus on the mobile phones of food vendors were quite similar to those of previous reports in other settings. It is remarkable that the frequency of penicillin resistance was quite high at 75%, and 28.6% of isolates harbored mecA. These were defined as MRSA variants detected on the mobile phones of food vendors on walking streets and in food centers. These results agreed with those from ready-to-eat foods, humans, pork, and beef [30]. Conversely, the prevalence of MDR S. aureus was quite high (51.0%) in this study. Most of the MDR isolates were methicillin-sensitive S. aureus and diverse. Only MRSA and VRSA isolates having MDR profiles of PEN-OXA-TET-GEN-RIF-CLI-CHL and VAN-PEN-OXA-DAP-LZD-ERY-TEI-RIF-CLI-CHL were detected in this study. It seemed that the AMR profiles in this study were quite different from those in previous studies [29]. This may be due to the antimicrobial agents used in different settings and the different environments, times, or samples. Thus, the results of one study may not be comparable with those of other studies. Within the same study, the AMR of S. aureus from the mobile phones of food vendors on walking streets and in food centers was quite similar. Only the percent resistance to each drug was different but not so significantly. However, MRSA isolate having MDR profile and carrying seb was detected on a mobile phone from a food shop at a food center in this study. It is not known whether this isolate was derived from food vendors, food materials, or other related environments in the shop. Generally, food is also an important factor in the transfer of AMR. Recently, MRSA strains were isolated from several food-producing animals including pigs, cattle, chickens, and other animals [25]. Additionally, this strain could produce enterotoxin when exposed to optimal conditions, leading to food poisoning outbreaks. It is concluded that the diversity of the S. aureus population on the mobile phones of food vendors regarding their toxigenic potential and AMR sheds light on the quality and safety of ready-to-eat foods on walking streets and in food centers.