**2. When do** *S. aureus* **outbreaks occur in athletes?**

Outbreaks of SA infections in an athletic setting have also occurred during the regular season (with the term "regular season" referring to the sport's league competitive period) [15]. During the regular season, there are likely to be more opportunities for contact with the others that subsequently result in wounds. Creech et al. examined an American men's football team and found a high rate of SA infection during the regular season [15]. Kazakova et al. also reported an outbreak of MRSA in a men's football team during the regular season [1]. Thus, evaluations of players taking part in physical contact sports during the regular season are critical for prevention and control of SA infections. In addition, individuals with SA-infected abscesses need to be carefully evaluated, as they may also serve as an SA "reservoir" that facilitates transmission to uninfected players. Our current analyses indicated that the regular season is intrinsically associated with risk factors for SA outbreaks (**Figure 2A**). Individuals with SA-infected abscesses might also be SA reservoirs that facilitate transmission to uninfected players.

#### **3. The role of fomites in SA infection outbreaks in athletes**

Data suggest that athletes with SA skin infection are more likely to experience a recurrence if the fomites were contaminated with SA. For example, an investigation of an outbreak of a MRSA infection in two different football teams revealed that the responsible MRSA clone was not found in the nares of any of the infected players, uninfected teammates/staff, or the environment [1, 3]. In a retrospective study that examined community-onset MRSA skin infections among professional football players, Kazakova et al. [1] did not find any MRSA in the nasal swabs or environmental cultures, even though 42% of the players were nasal carriers of the MSSA strains. Apart from these highly selected populations, it remains questionable whether the results from these studies can be extrapolated to the general population [16]. These findings suggest that the strain responsible for the infection was acquired from a nonnasal endogenous source or environmental sources. Moreover, the MRSA infection observed in these outbreaks was associated with exposures to various contaminated fomites, including whirlpools, shared razors, and shared towels. Other fomites implicated in the outbreaks of sports team-associated MRSA infections include benches, body sites worn by fencers, and even a bar of soap [1, 12, 17]. In non-outbreak settings, it has been reported that close contact with a person who has a skin infection was also associated with the SA infection [11].

Aggressive control of SA strains in the environment has contributed to effective strategies that can be used to prevent SA infection. For example, the National Collegiate Athletic Association (NCAA) has implemented prevention programs [18] that encourage hand hygiene [9], surveys of environmental contamination [12], showering the entire body with an antimicrobial soap and water immediately after each practice and game [19], discouraging cosmetic body shaving [3], and cleaning and disinfecting shared items [18]. As a result of active surveillance (a way of carefully monitoring of SA nasal carriage), consensus has been reached concerning the optimal ways for controlling infection among athletes [15], with nares screening for SA critical for preventing skin and soft tissue infection.

#### **4. Nasal carriage and SA infection in athletes**

After the reports of the initial studies on SA infection, sports medicine scientists have focused on the SA nasal carriage and skin infection. In human beings, the nose is the main ecological niche where SA resides [20]. The primary reservoir of SA is thought to be the anterior nares, and 30% of individuals carry nasal SA at any given time [6]. The association between SA nasal carriage and staphylococcal disease was first reported by Danbolt in 1931, who studied furunculosis [21].

subsequently result in wounds. Creech et al. examined an American men's football team and found a high rate of SA infection during the regular season [15]. Kazakova et al. also reported an outbreak of MRSA in a men's football team during the regular season [1]. Thus, evaluations of players taking part in physical contact sports during the regular season are critical for prevention and control of SA infections. In addition, individuals with SA-infected abscesses need to be carefully evaluated, as they may also serve as an SA "reservoir" that facilitates transmission to uninfected players. Our current analyses indicated that the regular season is intrinsically associated with risk factors for SA outbreaks (**Figure 2A**). Individuals with SA-infected abscesses might also be SA reservoirs that facilitate transmission to uninfected players.

Data suggest that athletes with SA skin infection are more likely to experience a recurrence if the fomites were contaminated with SA. For example, an investigation of an outbreak of a MRSA infection in two different football teams revealed that the responsible MRSA clone was not found in the nares of any of the infected players, uninfected teammates/staff, or the environment [1, 3]. In a retrospective study that examined community-onset MRSA skin infections among professional football players, Kazakova et al. [1] did not find any MRSA in the nasal swabs or environmental cultures, even though 42% of the players were nasal carriers of the MSSA strains. Apart from these highly selected populations, it remains questionable whether the results from these studies can be extrapolated to the general population [16]. These findings suggest that the strain responsible for the infection was acquired from a nonnasal endogenous source or environmental sources. Moreover, the MRSA infection observed in these outbreaks was associated with exposures to various contaminated fomites, including whirlpools, shared razors, and shared towels. Other fomites implicated in the outbreaks of sports team-associated MRSA infections include benches, body sites worn by fencers, and even a bar of soap [1, 12, 17]. In non-outbreak settings, it has been reported that close contact

with a person who has a skin infection was also associated with the SA infection [11].

critical for preventing skin and soft tissue infection.

**4. Nasal carriage and SA infection in athletes**

Aggressive control of SA strains in the environment has contributed to effective strategies that can be used to prevent SA infection. For example, the National Collegiate Athletic Association (NCAA) has implemented prevention programs [18] that encourage hand hygiene [9], surveys of environmental contamination [12], showering the entire body with an antimicrobial soap and water immediately after each practice and game [19], discouraging cosmetic body shaving [3], and cleaning and disinfecting shared items [18]. As a result of active surveillance (a way of carefully monitoring of SA nasal carriage), consensus has been reached concerning the optimal ways for controlling infection among athletes [15], with nares screening for SA

After the reports of the initial studies on SA infection, sports medicine scientists have focused on the SA nasal carriage and skin infection. In human beings, the nose is the main ecological

**3. The role of fomites in SA infection outbreaks in athletes**

36 Frontiers in Frontiers in Staphylococcus Aureus *Staphylococcus aureus*

Epidemiologic studies found higher SA nasal carriage rates and skin lesions in players of various sports. Sports activities that can cause skin lesions are also correlated with higher SA nasal carriage rates. These include river rafting [22] and football [1]. Decker et al. reported that higher nasal carriage rates were correlated with SA skin infections [22]. They postulated that maceration of the skin caused by prolonged contact with water in conjunction with repeated small cuts or skin injuries might have been the cause of the infections. Begier et al. [3] examined the sports activity of the players for an American football team and found that 97 of 100 players were positive for SA nasal carriage. Supporting these data is a further study that found repeated skin punctures in drug users and diabetics appeared to be the source of higher SA nasal carriage rates [6]. In addition, a retrospective analysis demonstrated that infection rates tended to peak among rugby forwards [23], American football linemen [1, 12, 14], cornerbacks, and wide receivers [3], all of whom have frequent contact with other players. All of these athletes play in the front lines, engage in frequent and aggressive skin-to-skin contact during matches, and are expected to engage the opposing team in the blind side of the scrum and tackle other players. This high-frequency, rough physical contact causes the skin abrasions that are associated with SA soft tissue infections [8].

Persistent SA nasal carriage is an established risk factor for cutaneous infection in physical contact sports [15]. Despite various proposals, there has yet to be a standard definition regarding the number of cultures that need to be taken or what fraction should be positive when determining the carrier status [24]. However, attempts to define persistent carriers have been problematic, as most SA infections originate from lines that are specific to carriers and hands, which are often the primary vectors for transmitting nasal bacteria in athletes [13]. Moreover, there are a number of infectious diseases that can be spread from one person to another by contaminated hands and body sites in athletes [13]. Therefore, the current consensus is that SA resides in the anterior nares of individuals and which serve as reservoirs that predispose players to subsequent infections.

The quantity of the SA colony-forming units (CFU) that can be recovered from swabs used to examine the noses of carriers varies widely, with numbers reported to range from the single digits to millions [25, 26]. In addition, other studies have reported that there is a strong association between high cell counts and persistent carriage [24, 27, 28]. Furthermore, evidence from various studies has led to the postulate that persistent carriers represent a separate group that is distinct from the intermittent and noncarriers [27, 29]. (Most studies that have examined SA nasal carriage have used a cross-sectional design with a single-nasal culture in order to determine whether an individual is a carrier. However, longitudinal studies have distinguished at least three SA nasal carriage patterns in healthy individuals: persistent carriage, intermittent carriage, and non-carriage [6, 30–32]. In addition, some studies make a further distinction between occasional and intermittent carriers [33, 34].) Even though the reasons remain unknown, the basic determinants of persistent and intermittent carriage are thought to be different. Persistent carriers are often colonized by a single strain of SA over long time periods, whereas intermittent carriers may carry different strains over time [31, 33, 35]. Furthermore, the load of SA is higher in persistent carriers, which results in increased dispersal and a higher risk of infection [24, 29]. Nasal carriers who are also persistent carriers are reported to have higher SA loads and disperse more SA [21, 36, 37].

Approaches that use high-throughput nasal swab data can also be applied to help in our understanding of the bacterial spread. While many studies have focused on nasal swab data, it is still unknown whether nasal SA colonization alone can trigger an SA outbreak. By achieving a deeper understanding of the repercussions of carrying nasal SA, this should help to refine and optimize strategies for risk control among athletes, thereby reducing SA infections.
