Background
Staphylococcus aureus is an opportunistic pathogen that colonizes asymptomatically the skin and nares of approximately 1 in 3 people worldwide [
1,
2].
S. aureus is found in hospital settings, and with the emergence of antibiotic resistance, can cause life threatening infections. Recent studies have suggested that, in the United States, over 80,000 invasive infections and 11,000 yearly deaths are attributed to methicillin-resistant
S. aureus (MRSA) [
3]. While the number of invasive MRSA infections has declined slowly over the past decade, our group has identified reservoirs of MSSA (methicillin-susceptible
S. aureus) and MRSA in humans, animals, and the environment [
4‐
11]. Although colonization with
S. aureus is usually asymptomatic, it is a risk factor for active infection [
12] and enhances the ability of an individual to transmit
S. aureus to fomite surfaces [
13].
One location that has been associated with an increased risk of both infection and colonization with
S. aureus is the athletic fitness facility [
14,
15]. Over 50 million individuals in the United States support approximately 30,000 fitness facilities, and the number continues to rise [
14]. MRSA infections have been linked to contamination of athletic facilities due to shared exercise equipment [
15] and towels [
16]. Facility-associated MRSA infections have also been documented in both professional and collegiate athletic teams [
17‐
19], and even in high school athletes [
20,
21]. The link between fitness facilities and contaminated surfaces is unclear [
22], but Markley and colleagues [
15] found that approximately 10% of gym surfaces were contaminated with
S. aureus and these contaminated fomites may serve to spread
S. aureus. However, not all fitness facility types and surfaces may warrant the same scrutiny.
In the present study, we assessed the prevalence of S. aureus and MRSA across several fitness facility types to characterize the microbial environment and potential for S. aureus transmission, to identify potential risks associated with certain areas, environmental conditions, or types of exercise equipment, and to provide a more inclusive study addressing exercise facility type as a facilitator of S. aureus transmission.
Discussion
This study examined the prevalence and molecular characteristics of
S. aureus and MRSA sampled from 288 gym surfaces collected from 16 gyms across four different types of gym facilities in Northeast Ohio. From 288 samples, 110 were positive
S. aureus isolates and we had a 26.7% (77/288) and 11.5% (33/288) recovery of
S. aureus and MRSA, respectively. We found similar
S. aureus prevalence across community, traditional, CrossFit, and hospital-associated fitness facilities (40.0% vs 38.9% vs 38.9% vs 33.3%, respectively) (Table
1). However, our prevalence rates were higher than those identified previously [
15‐
21]. The prevalence rate difference may be attributed to fitness facility and/or patron type. As athletes and athletic personnel generally have a significantly higher incidence of both infections and over a ten-fold higher number of antibiotic prescriptions per year compared to the general public, many infections may remain unmonitored or unrecognized [
18,
33,
34]. Despite their continual occurrence, there has been little effort to identify and monitor contaminated surfaces and the role they may play in transmission, until recently [
35‐
39]. Though our study found similar rates of contamination across all fitness facilities that mirror common human carriage rates, the incidence of both
S. aureus and MRSA is higher in our environmental contamination study than what has been observed in the literature, such as in school settings, playgrounds, and beaches [
4‐
8,
15,
22,
40]. Despite other environmental contamination studies, studies of fitness facilities have received attention only recently.
For example, Ryan and colleagues [
22] found zero presence of
S. aureus in gym facility surfaces suggesting that all transmission was entirely via-person to person contact or at least ruling out that gyms were reservoirs of
S. aureus. Markley and colleagues [
15] sampled 16 different surface types at one large community center and found that 10% (10/99) of samples were contaminated with MSSA only. Due to the significantly limited size and scope of the study (one facility type was examined), their reported incidence may be underestimated. Prior to these studies, 5 players (9%) on the 2003 St. Louis Rams football team were found to have MRSA infections [
18]. Interestingly, they found zero nasal carriers and/or environmental reservoirs of MRSA, but did grow MSSA from whirlpool water and a gel-applicator stick used for taping ankles, suggesting that fomite surfaces have the potential to harbor and transmit
S. aureus. Although Ryan and colleagues [
22] surveyed three facilities (college, high school, and private gyms) before and after cleaning regiments, they found zero presence of MSSA and MRSA from their 240 samples. Their results may be attributed to differences in bacterial isolation and cultivation. Almost 40% of the population are carriers of
S. aureus [
41], thus, it is surprising that these studies found very few contaminated surfaces, while contamination in a hospital setting is sufficiently ubiquitous to sound alarm [
42‐
46]. For example, a hospital study found that 76% of skin and soft tissue infections were of
S. aureus etiology and 59% of those were attributable to MRSA [
47]. Of those presenting MRSA, 99% of isolates were community-associated (CA-MRSA), pointing to acquisition of MRSA strains from outside of the hospital setting, such as a gym facility. Likewise, hospital ward high touch surfaces areas were highly contaminated with
S. aureus concentration increasing by almost 80% over a 4-h period despite the use of hypochlorite. The addition of Quaternary Ammonium Compound surfactants (QAC) did drastically decontaminate surfaces to almost 10% of their original bacterial load count, pointing to potential bacterial decontamination strategies to reduce transmission [
46]. Additionally, through the use of sequencing techniques, small amounts of biomass collected from gym facilities were sufficient to identify community bacteria, as well as staphylococcal species present on athletic surfaces in the gym, with the composition modulated by interacting with human skin [
48]. Though our study did not track personnel or patron
S. aureus carriage or microbiome composition, provenance of contamination will be key for future studies addressing the movement, transmission, and potential antibiotic-resistant reservoirs of fitness facilities.
The increased prevalence of
S. aureus on fitness facility surfaces may also be a result of environmental co-evolution. As
S. aureus can tolerate high osmolarity stress (high saline environments), the production of sweat at gym facilities can even be extrapolated to other high intensity situations such as war and combat, which may select for
Staphylococcal species in the environment or individual [
49]. With ease of horizontal gene transfer, the acquisition of antibiotic resistance may be enhanced as a result. The incidence of MRSA in athletes is almost triple what is observed in the general population. Thus, it is not surprising that we observed higher contamination rates on gym surfaces than other surfaces [
50].
We found a total of 38 unique
spa types with t008 (14; 12.7%) and t267 (11; 10.0%) being the most common (Table
2; Fig.
2). Interestingly, some loosely identified livestock associated strains such as t548 and t338 were found in Crossfit, community, and hospital-associated strains but not in strains isolated from traditional gyms (Fig.
2). t548 is associated to upper Midwestern and northwestern regions of the US, including Ohio. Since it was found in hospital associated gyms, the line between the original provenance of
S. aureus strains and their site of contamination is becoming increasingly fluid. Approximately 8.2% (9/110) of strains were categorized as livestock-associated. A total of 6 isolates were t338 and were found in hospital, Crossfit, and community fitness facilities. Three isolates (2.7%) were t548 and found solely within Crossfit facilities. Additionally, t012 was the most common strain type found in hospital-associated facilities (4; 22.0%) and community fitness centers (1; 3.0%), but not traditional or Crossfit facilities. t012 is known to be less prevalent as the age of the individual increases [
51,
52]. However, its increased incidence in hospital- associated facilities may be a result of rehabilitation of both older and younger patients. Conversely, t002 was found in hospital-associated (2; 11.0%), community (1; 3.0%), and traditional facilities (1; 4.0%). t002 is often found in nursing homes and in older patients [
53]. As such, the hospital-associated facilities also had strains associated with older patients. These results suggest that age demographics may play a significant role in strain isolates found in various fitness facilities. We found t002 on the weight ball and weight bench bars in hospital, traditional, and community facilities. As it has the possibility to be present in cases of bacteremia [
52,
54], it is important to be careful in regards to lifting weights with any cuts present, which could contaminate gym equipment.
Looking across gym facilities, Crossfit had the most diverse range of
spa types (Table
2; Fig.
2). Of the 10
spa types found in Crossfit facilities, 6 were community-associated (t267, t377, t084, t282, t334, and t4371), two have been found in livestock (t548 and t338), and two have been associated in hospital settings (t189 and t346). Though other facilities sampled had some similar variations of these associations, none were as diverse as Crossfit types. This may be a result of the comparative lack of lifting machine structure in Crossfit gyms and/ or the wide range of people that attend them [
55,
56]. Furthermore, if common cleaning regimens are not followed, high hand-touch surfaces may harbor and easily disseminate pathogenic, antibiotic resistant bacteria to other people via hand contact, as hands are recognized as a primary mode of transmission of many diseases (Fig.
3), [
38,
45,
57].
To the best of our knowledge, this is the first study to evaluate systematically different gym facility types for contamination and molecular typing of S. aureus. The strength of our study resides within our large sample size both across fitness facility types, as well as across fitness surfaces sampled. In addition, we also carried out molecular genotyping of S. aureus isolates, further strengthening our epidemiological study of S. aureus contamination on athletic gym surfaces. However, there are limitations to our study that included convenience sampling in Northeast Ohio fitness facilities only. In addition, we only sampled surfaces at one point in time, we did not sample surfaces after a cleaning regimen, and we did not sample and type isolates found on patrons and facility employees. Future studies should evaluate the patron microbiome, as well as the collective microbiota impact on fomite contamination and transmission. Our results indicate not only the presence of putatively dangerous isolates of S. aureus, but also that increased cleaning regimens and enhanced hygiene practices should be followed in fitness facilities as is practiced in the hospital or work place.