Background. Athletics-associated methicillin-resistant Staphylococcus aureus (MRSA) infections have become a high-profile national problem with substantial morbidity.
Methods. To investigate an MRSA outbreak involving a college football team, we conducted a retrospective cohort study of all 100 players. A case was defined as MRSA cellulitis or skin abscess diagnosed during the period of 6 August (the start of football camp) through 1 October 2003.
Results. We identified 10 case patients (2 of whom were hospitalized). The 6 available wound isolates had indistinguishable pulsed-field gel electrophoresis patterns (MRSA strain USA300) and carried the Panton-Valentine leukocidin toxin gene, as determined by polymerase chain reaction. On univariate analysis, infection was associated (P < .05) with player position (relative risk [RR], 17.5 and 11.7 for cornerbacks and wide receivers, respectively), abrasions from artificial grass (i.e., “turf burns”; RR, 7.2), and body shaving (RR, 6.1). Cornerbacks and wide receivers were a subpopulation with frequent direct person-to-person contact with each other during scrimmage play and drills. Three of 4 players with infection at a covered site (hip or thigh) had shaved the affected area, and these infections were also associated with sharing the whirlpool ⩾2 times per week (RR, 12.2; 95% confidence interval, 1.4–109.2). Whirlpool water was disinfected with dilute povidone-iodine only and remained unchanged between uses.
Conclusions. MRSA was likely spread predominantly during practice play, with skin breaks facilitating infection. Measures to minimize skin breaks among athletes should be considered, including prevention of turf burns and education regarding the risks of cosmetic body shaving. MRSA-contaminated pool water may have contributed to infections at covered sites, but small numbers limit the strength of this conclusion. Nevertheless, appropriate whirlpool disinfection methods should be promoted among athletic trainers.
Staphylococcal skin infections due to methicillin-susceptible Staphylococcus aureus (MSSA) are a well-documented complication of participation on athletic teams [1–4]. Recently, community-acquired methicillin-resistant S. aureus (MRSA) infections have been increasingly reported among athletes and, in some cases, have required hospitalization and surgery [5–7]. Transmission via person-to-person contact during practice or competitive play has been implicated in outbreaks involving wrestling and rugby football teams [5–7]. The sharing of equipment (i.e., sensor wires) has been linked to transmission of MRSA among fencers .
Football teams, in particular, have emerged as a common population in which MRSA outbreaks occur, with several high-profile outbreaks publicized during 2003 . High school, college, and professional players have been affected [8–10]. A recent report described 2 outbreaks among college football players; possible risk factors were abrasions due to artificial grass (i.e., “turf burns”), skin shaving, and sharing unwashed bath towels, balms, and lubricants . We describe an MRSA outbreak among members of a college football team to inform clinicians and public health practitioners and to guide related policy.
The Connecticut Department of Public Health was notified on 3 September 2003 about a cluster of skin infections due to MRSA among members of a college football team and, at that time, initiated enhanced surveillance for MRSA skin infections among players and the community. All athletes with skin lesions were evaluated at the student health center. Health center staff obtained swab specimens from the anterior nares of players, trainers, and coaching staff to identify individuals with nasal carriage. Swab samples from the groin, axillae, and nares of patients with recurrent infections were obtained for culture. We contacted nearby hospital laboratories to identify cultures of wound specimens obtained from persons 15–25 years during the period of July through September 2003 that yielded MRSA. We called student health facilities of the 3 opposing teams that were played during the outbreak to identify individuals with skin infections.
We visited the athletic center and interviewed athletic trainers, coaching staff, and infected players regarding player routines and hygienic practices at the athletic center. We performed a retrospective cohort study of members of the 2003 football team by use of a face-to-face questionnaire to assess skin injuries, hygienic practices (e.g., sharing of towels and equipment), and other exposures during the interval between the arrival at football camp and the announcement of the outbreak (i.e., from 6 August through 6 September 2003). We also asked about known risk factors for MRSA (e.g., health care contacts [such as physician visits, surgery, or hospitalization] and skin conditions). We reviewed training room charts to obtain more-detailed information regarding whirlpool use.
We defined a case as culture-confirmed MRSA cellulitis or skin abscess diagnosed in a player during the period from 6 August through 1 October 2003. Univariate relative risks were calculated with use of Stata 7 software (Stata) . We investigated confounding by use of stratified analysis and bivariate logistic regression. MRSA isolates were subtyped at the Minnesota Department of Health's Public Health Laboratory (Minneapolis) by PFGE. Methicillin resistance was confirmed at the Minnesota Department of Health's Public Health Laboratory by detection of the mecA gene with PCR. The genetic element carrying the mecA gene—staphylococcus cassette chromosome mec (SCCmec)—was typed by PCR [12, 13]. Antibiotic susceptibility results from clinical laboratories were obtained. A subset of isolates underwent quantitative susceptibility testing by broth microdilution and testing for inducible clindamycin resistance by the “D test” at the Minnesota Department of Health's Public Health Laboratory. All PFGE-indistinguishable wound and colonization isolates were tested at the Centers for Disease Control and Prevention (Atlanta, GA) for enterotoxins A-E and H by ELISA, for toxic shock syndrome toxin 1 by reverse passive latex agglutination, and for the presence of Panton-Valentine leukocidin toxin gene by PCR.
We identified 10 of 100 players who had skin infections due to MRSA (attack rate, 10%). Skin infections due to MRSA were not identified among trainers and coaching staff, non-football players (i.e., other students and local residents), or members of opposing teams. Primary MRSA infections occurred during a 3-week period (between 16 August and 17 September) (figure 1).
Laboratory findings. Wound isolates were available from 6 of 10 case patients, and 3 colonization isolates were available from the 2 hospitalized patients described below. PFGE showed that all isolates had indistinguishable PFGE patterns indicative of community-associated USA300 strain  and carried mecA and SCCmec type IVa methicillin resistance gene alleles and Panton-Valentine leukocidin toxin gene. Production of enterotoxins A-E and H and toxic shock syndrome toxin 1 were not identified. Clinical laboratory testing revealed that all wound isolates had identical susceptibility patterns revealing resistance to cephalothin, erythromycin, oxacillin, and penicillin and susceptibility to ciprofloxacin, clindamycin, gatifloxacin, gentamicin, levofloxacin, linezolid, rifampin, tetracycline, trimethoprim-sulfamethoxazole, and vancomycin. This pattern was confirmed by quantitative broth microdilution testing. Isolates were negative for inducible clindamycin resistance by D test.
Patient characteristics. All case patients were males and aged 17–22 years. Ten case patients had 13 infections (9 cases of abscess and 4 cases of cellulitis) at the following sites: elbow, 4 cases; thigh, 2; hip, 2; chin, 1; forearm, 1; wrist, 1; knee, 1; and tibial plateau, 1. Eight players were treated as outpatients only; all but 1 required ⩾7 days of frequent visits (median, 10 days; range, 1–21 days) for wound care (i.e., irrigation and packing).
Hospitalized patients. One player was hospitalized initially in early September because of cellulitis and possible septic arthritis. Gram stains of synovial fluid specimens obtained from this patient showed rare WBCs and no organisms (fluid cell count was not performed). Culture of the synovial fluid yielded negative results, but arthrocentesis was performed several hours after receipt of the first dose of ciprofloxacin. The patient received intravenous vancomycin for 3 weeks to treat presumed septic arthritis due to MRSA. Three weeks after completing antibiotic treatment, he developed a chin abscess due to MRSA strain USA300. After diagnosis of the second infection, samples obtained from the groin and axillae were obtained for culture, which also yielded MRSA USA300. Results of nasal culture, which were initially negative during the team-wide survey, again did not yield S. aureus.
Another case patient who originally presented with a thigh abscess subsequently developed cellulitis of the elbow. After receipt of oral ciprofloxacin for a total of 5 weeks and resolution of the second infection, he was hospitalized because of an abscess on his forearm due to MRSA (which again was susceptible to ciprofloxacin) and received intravenous vancomycin for 14 days. Swab samples were obtained from the axillae, groin, and nares for culture, but only nares culture yielded MRSA USA300; the patient's initial nares culture had yielded MSSA.
Colonization results. A total of 97 of 100 players had nares swab specimens obtained for culture. Forty-three cultures yielded MSSA. No MRSA was found. All 29 members of the athletic training and coaching staff had nares swabs obtained for culture: 6 cultures yielded MSSA, and 0 yielded MRSA.
Disease risk factors. Ninety players (90%) (including all 10 case patients) completed face-to-face interviews. Cornerback defensive backs and wide receivers had the highest infection risk (50% and 33%, respectively), accounting for 8 of 10 case patients (table 1). Remaining case patients were a linebacker and a tight end.
Players who sustained turf burns had a risk of infection that was 7 times higher than that for players without turf burns (relative risk [RR], 7.2; 95% CI, 1.0–54.5). An additive interaction was seen between player position and turf burns, suggesting that players in high-risk positions were particularly at risk if they sustained such abrasions (table 2). Times to wound cleaning, wound coverage, and receipt of wound care by team trainers were not predictive of infection risk. Only 10 players used protective elbow pads. Use of such pads was associated with a trend toward a higher risk of infection (RR, 3.2; 95% CI, 0.6–17.9).
Overall, 25 players (28%) reported body shaving (i.e., shaving an area of the body other than the face). Players reported shaving the following sites: chest, 12 players; groin, 7; arms, 6; legs, 2; abdomen, 2; ankle/foot, 2; and axillae, 1. Seven of these 25 players shaved 2 sites. Players who reported body shaving were 6.1 times more likely to develop MRSA infections. Shaving genitals or the groin was associated with a higher infection risk (43%) than shaving other body sites (RR, 9.3; 95% CI, 2.3–37.6). Three of 4 players with infections of covered sites (areas normally covered by the football uniform, including hips and thighs) had recently shaved these areas. The fourth player reported shaving the affected area before the start of camp. No case patients reported sharing razors. As with turf burns, additive interaction was seen between player position and body shaving, suggesting that players in high-risk positions increased their risk by body shaving (table 2).
Training room charts recorded only therapeutic whirlpool use. Chart reviews documented that only 5 players were directed by athletic trainers to use the whirlpool, whereas 38 players reported whirlpool use on the questionnaire. Players who reported sharing the cold whirlpool in the training room with another athlete were 2 times as likely to have an MRSA infection (RR, 2.4; 95% CI, 0.8–7.7), although this difference was not statistically significant. However, for infections of covered sites, risk increased significantly with more-frequent whirlpool sharing. Those who shared the whirlpool ⩾2 times a week were 12 times more likely to have infections due to MRSA on covered sites than were those who never shared the whirlpool (RR, 12.2; 95% CI, 1.4–109.2) (table 3). Infections of covered sites occurred throughout the outbreak, and whirlpool maintenance practices were not altered from those described below until the end of September.
Health care-associated risk factors for MRSA, such as antibiotic use and surgery or hospitalization during the previous year, and hygienic practices were not significantly associated with infection risk. Additional risk factors not found to be associated with disease were having a football player as a roommate, dormitory of residence, and locker location. Sharing of personal items was relatively infrequent (towels, 4% of players; creams and ointments, 6% of players; nonspray deodorant, 6% of players; and bar soap, 20% of players) and not associated with infection.
Skin infections due to MSSA. In addition to skin infections due to MRSA, 6 minor skin infections due to MSSA were identified during active surveillance. Nasal carriage of MSSA and other assessed exposures were not statistically associated with MSSA infection (P > .05).
Facility inspection and staff interviews. No soap was available in showers used by the athletes. Water used to wash towels was 44.4°C rather than 71°C , and chlorine bleach was not used. Wound care and coverage was optional and left to the discretion of the players. Several case patients reported having played football with open wounds.
Two 416-L (100-gallon) whirlpools in the athletic trainers' room were filled in the morning, and povidone-iodine was added as a disinfectant (30 mL per 75.7 L [1 fluid ounce per 20 gallons] of water). Usually, 2 players used a pool at once. Pool water was unchanged throughout the day. Players were instructed to shower before use, and players with open wounds were reportedly not allowed in the whirlpool, although case patients with turf burns described having used the whirlpool. Whirlpools were drained and cleaned with heptagon at the end of each day. Whirlpools were kept at temperatures of 7°C–15.5°C (cold pool) and 35°C–40.5°C (hot pool; used only at the end of the outbreak).
We hypothesize that MRSA was spread between players largely by frequent direct contact between cornerbacks and wide receivers during practice scrimmage and drills. Whirlpools may have provided an additional mechanism for the spread of MRSA, because of unproven and limited water disinfection practices. Infection appears to have been facilitated by interruptions of skin integrity, including turf burns and microabrasions likely sustained while body shaving. Nasal colonization with MRSA does not appear to have played a role in this outbreak.
Despite prompt recognition of methicillin resistance by the treating clinician, these previously healthy players experienced significant morbidity from their infections, with nearly all requiring daily wound care for >1 week and 2 requiring hospitalization. Outbreak wound isolates carried mecA and SCCmec type IVa gene alleles for methicillin resistance, as well as the Panton-Valentine leukocidin toxin gene. This gene allele combination has been frequently identified in community-associated MRSA isolates, particularly those from patients with primary skin infections and necrotizing pneumonia [16–18]. Whether Panton-Valentine leukocidin toxin or other associated exotoxins are responsible for increased clinical virulence requires study .
The strong association with certain player positions provides evidence for person-to-person spread, because cornerbacks and wide receivers were a subpopulation with frequent direct person-to-person contact with each other during scrimmage play and drills. Two other investigations of MRSA outbreaks among athletes implicated person-to-person spread during prolonged close contact [6, 7]. One occurred among wrestlers, in which teammates passed MRSA to each other during practice but not to opponents exposed only for a brief 3-min match . An outbreak among rugby players was attributed to person-to-person contact during play because of a high attack rate among those playing the position of forward . An increased rate of infection among rugby forwards has also been seen in outbreaks of cutaneous herpes simplex .
We did not find evidence that playing with uncovered wounds increased the risk of infection. However, several case patients reported having played football with uncovered wounds that were subsequently diagnosed as MRSA infections, which likely provided the opportunity for such patients to pass MRSA to others before diagnosis. Before the outbreak, athletic staff left wound care largely to the discretion of the players, allowing the players to seek care and wound coverage if they wished. As a control measure, we required the exclusion of case patients from all play until the wounds healed, and all players were required to cover open wounds during play. These interventions have been routinely used in similar outbreaks [1, 2, 5]. We recommend that players routinely and consistently comply with covering wounds as a participation requirement to limit the potential for and extent of future outbreaks of infection.
MRSA infection appears to have been facilitated by interruptions of skin integrity, including those caused by body shaving. Although some athletes (e.g., swimmers) practice body shaving to enhance performance, body shaving is largely a cosmetic practice among football players and other young men . Body shaving is likely to produce microabrasions. Surgical literature has documented increased risk of postoperative infection associated with shaving surgical sites [21, 22]. Body shaving has not previously been conclusively linked to infections among athletes, although it was a possible risk factor in an MRSA outbreak among college football teammates in 2000 . This emerging cosmetic behavior among young men may contribute to the risk of infection in populations of athletes, especially in areas covered by clothing (e.g., the groin and thighs). Education regarding the risks of body shaving for participants in contact sports should be considered.
Open wounds [3, 4] and possibly turf burns  have been associated with staphylococcal infections, including MRSA, during past outbreaks among football players. We found increased risk associated with turf burns, although these abrasions were not always directly adjacent to infection. We did not find an association with the type and timing of care of turf burns, suggesting that avoiding such abrasions entirely would be the best way to prevent infection. Although the negative impact of artificial turf on the rates and severity of more debilitating injuries such as concussions [23, 24] and musculoskeletal injuries [25, 26] has been described, the specific effects of the characteristics of artificial turf on the risk of abrasion warrants study. Additionally, the impact of wearing uniforms that cover more skin merits testing , particularly given recent advances in textiles that likely improve the tolerability of such clothing.
We found a trend toward increasing risk of infection associated with the use of elbow pads. Investigation of 2 previous MSSA outbreaks found that use of elbow pads significantly increased the risk of infection [3, 4]. Although pads should prevent abrasions, it is possible that they promote moisture buildup and bacterial growth or skin breaks due to chafing. Study is needed to better define the positive and negative effects of elbow pads.
In our initial survey, we found no MRSA nasal colonization among players or staff. We did identify a high rate of colonization with MSSA, suggesting that nasal swabs were a sensitive means of detecting staphylococcal colonization. Two other investigations of outbreaks of MRSA among athletic teams found similarly low rates of nasal carriage of the outbreak strain [6, 7]. We identified axilla and groin (but not nasal) colonization with the outbreak strain in 1 player with a well-documented MRSA skin infection following a possible MRSA joint infection, suggesting that alternative carriage sites may have played a role in infection, including recurrent infection. Additionally, at the time of this player's second infection, after the outbreak period, his roommate (a running back on the same football team) became infected with the outbreak strain. We also found a higher risk associated with groin shaving, compared with shaving of other body sites, again suggesting that groin carriage of MRSA by athletes should be investigated further.
Given the full-body nature of the players' routine contact, particularly in hot weather promoting perspiration, sites of carriage among participants in contact sports might reasonably differ from those among health care workers, who predominantly have hand contact with patients. In an MRSA outbreak in a child care center, culture of throat and anal swab specimens were found to have a higher sensitivity for identifying MRSA carriage than was culture of nares specimens . Because no new cases occurred after initial control measures were implemented, groin and axilla swab samples for culture were not obtained from the entire team. Such a survey involving a 20-member rugby team was conducted during an MRSA outbreak. No axilla or groin carriage was identified , but small numbers limit firm conclusions based on those findings.
We found that an increasing infection risk was associated with an increased frequency of sharing the cold whirlpool in the trainer's room and with unproven water disinfection practices that did not meet Connecticut regulations. All public pools, even therapeutic whirlpools, must be disinfected with an automatic disinfection feeder . In this study, povidone-iodine was added only in the morning, and whirlpool water remained unchanged all day. Research concerning hydrotherapy whirlpools has documented that staphylococci can persist in whirlpools even when water is changed between users  and when chlorine disinfection is performed to enable use by multiple people . Furthermore, transmission of MRSA has been linked to contaminated hydrotherapy equipment  and bathtubs  in nosocomial outbreaks. Athletic trainers were instructed to empty, disinfect, and refill whirlpools after each use, because pools lacked recirculation and filtration equipment, including automatic disinfection feeders. Because informal conversations with athletic trainers suggested that use of dilute povidone-iodine for disinfection of whirlpools was a common practice, we sent a communication to similar Connecticut facilities to clarify whirlpool maintenance practices that comply with Connecticut's public health code.
We found several practices that did not accord with basic principles of good hygiene and infection prevention (e.g., soap not available in showers), as has been the case in other outbreaks [3, 5]. We recommended installing soap dispensers with antibacterial soap in team showers and washing towels with water consistently ⩾71°C. Players were urged to shower immediately after practice and to clean and dress cuts and turf burns as soon as possible. Although all of these measures were implemented in the days after the outbreak report, the end of the outbreak was most closely temporarily associated with the installation of soap dispensers, and recurrent cases coincided with times at which the dispensers were temporarily empty and awaiting refill.
Given repeated findings of inadequate routine hygienic practices and increased risk of infection associated with skin breaks, disseminating guidelines for schools and universities via the American College Health Association or other national health organizations would be appropriate to publicize the best effective practices to prevent outbreaks of MRSA. Such measures would enable trainers and athletic department staff to use straightforward approaches to prevent or limit the extent of MRSA outbreaks.
There are several study limitations. The outbreak's small size—only 10 case patients—made full multivariate analysis impossible; however, bivariate analysis did not suggest that confounding explains our results. We also could not ascertain the actual number of days of whirlpool use by case patients. With such information, we could have more conclusively determined the risk of infection associated with whirlpools. Additionally, whirlpool water and surfaces were not sampled for culture, so we cannot say if MRSA was actually present in these whirlpools.
In summary, in this high-morbidity outbreak of MRSA infection among young healthy athletes, we identified both modifiable risk factors for infection and breaks in adherence to standard hygiene recommendations. Because of increasing reports of virulent community-acquired MRSA nationwide, athletic and coaching staff should note the special risk associated with athletes, and common-sense prevention guidelines should be implemented.
Study Group Members
The Connecticut Bioterrorism Field Epidemiology Response Team members involved in the investigation include Brenda Esponda, Diana Mlynarski, Ava Nepaul, and Terry Rabatsky-Ehr.
We thank Arthur Leffert, Sands Cleary, MariJo Panettieri, Matt Cartter, Richard Dicker, Bill Sawacki, Bob Howard, Arjun Srinivasan, Joanne Bartkus, Ruth Lynfield, Nolan Lee, Tim Naimi, Andre Weltman, Virginia Dato, Eddy Bresnitz, Corey Robertson, Dan Jernigan, and members of the university administration and athletic department staff. We also thank George Killgore and Gregory Fosheim (Centers for Disease Control and Prevention; Atlanta, GA) for performing toxin testing on the outbreak-associated MRSA isolates and Jeff Hageman for facilitating this analysis.
Potential conflicts of interest. All authors: No conflict.