Original Article
An Outbreak of Herpes Gladiatorum at a High-School Wrestling Camp
N Engl J Med 1991; 325:906-910September 26, 1991
- Abstract
- Abstract
Background and Methods.
Herpes simplex virus type 1 (HSV-1) has been identified as a cause of cutaneous or ocular infection among athletes involved in contact sports; in this context it is known as herpes gladia-torum. In July 1989, we investigated an outbreak among 175 high-school wrestlers attending a four-week intensive-training camp. Cases of infection were identified by review of medical records, interview and examination of the wrestlers, and culture of skin lesions. Oropharyngeal swabs were obtained for HSV-1 culture, and serum samples for HSV-1 serologic studies. HSV-1 isolates were compared by restriction-endonuclease analysis.
Results.
HSV-1 infection was diagnosed in 60 wrestlers (34 percent). The lesions were on the head in 73 percent of the wrestlers, the extremities in 42 percent, and the trunk in 28 percent. HSV-1 was isolated from 21 wrestlers (35 percent), and in 39 (65 percent) infection was identified by clinical criteria. Five had conjunctivitis or blepharitis; none had keratitis. Constitutional symptoms were common, including fever (25 percent), chills (27 percent), sore throat (40 percent), and headache (22 percent). The attack rate varied significantly among the three practice groups, ranging from 25 percent for practice group 1 (lightweights) to 67 percent for group 3 (heavyweights). Restriction-endonuclease analysis identified four strains of HSV-1 among the 21 isolates. All 10 isolates from practice group 3 were identical (strain A), and 5 of 7 isolates from practice group 2 (middleweights) were identical (strain B), which suggested concurrent transmission of different strains within different groups. HSV-1 was not isolated from any oropharyngeal swabs.
Conclusions.
Herpes gladiatorum may cause substantial morbidity among wrestlers, and it is primarily transmitted by direct skin-to-skin contact. Prompt identification and exclusion of wrestlers with skin lesions may reduce transmission. (N Engl J Med 1991; 325:906–10.)
Article Activity
- Article
CUTANEOUS and ocular infection with herpes simplex virus type 1 (HSV-1) was initially recognized as a health risk for wrestlers in the mid-1960s.1 2 3 4 Several clusters of primary cutaneous HSV-1 infection were recognized, and transmission was also documented in rugby players.5 The condition was labeled "herpes gladiatorum." Previous reports of this illness have emphasized its clinical features. Because of the small number of athletes in each cluster, epidemiologic data on modes of transmission and risk factors for infection are limited. Recent surveys of athletic trainers suggest that infection with herpes gladiatorum is endemic among high-school and college wrestlers,6 but the incidence of disease and optimal control methods remain unknown. This infection may represent a real public health problem: during the 1990–1991 school year, there were more than 230,000 male and 130 female participants in competitive high-school wrestling (McGinness F, National Federation of State High School Associations: personal communication).
In July 1989, we investigated a large outbreak of herpes gladiatorum among high-school wrestlers attending a four-week intensive-training camp. Using both clinical and molecular epidemiology, we sought to define the modes of transmission and the risk factors for infection.
Methods
Background
On July 24, 1989, the Minnesota Department of Health was notified of an outbreak of cutaneous HSV-1 infection among high-school wrestlers attending an intensive-training camp in Minneapolis. The camp was held from July 2 to July 28 and was attended by 175 wrestlers from 26 states and 1 Canadian province. The typical daily schedule included five activity sessions: a run before breakfast, a session on wrestling technique later in the morning, an intensive wrestling practice in the afternoon, a "motivation" session after dinner, and another run later in the evening. On some days, the evening run was replaced by a second session devoted to wrestling technique. The wrestlers were divided into three practice groups according to weight. Most wrestling occurred within groups, although some contact between groups occurred during the evening sessions on technique.
During practice sessions the wrestlers were required to wear jerseys, but the use of headgear was optional. The wrestling mats were mopped twice daily with a disinfectant solution. Trainers were responsible for the initial evaluation of medical problems, but they did not perform routine skin examinations. Skin lesions were detected primarily when the wrestlers reported them. All wrestlers who required medical care were referred to the emergency department at the University of Minnesota Hospital.
After the initial notification of the outbreak, a review of the diagnoses by the emergency department indicated that herpes gladiatorum infection had already developed in at least 40 wrestlers. Because additional cases were being identified daily, the Minnesota Department of Health recommended that all wrestling be suspended for the remaining three days of the camp session to prevent further transmission.
Epidemiologic Investigation
Infections were defined by the isolation of HSV-1 from the involved skin or mucous membranes or by the presence of cutaneous vesicles as noted by an examining physician. Only infections with an onset from July 1 through August 5 were considered related to the outbreak.
We conducted a clinic at the field house during the final two days of camp to identify infected wrestlers and collect epidemiologic data. After parental consent was obtained, all wrestlers were asked to provide a blood sample voluntarily for the determination of HSV-antibody status and an oropharyngeal swab for HSV culture. The skin of consenting wrestlers was examined if they had skin lesions during the last week of camp, and cultures of suspicious skin lesions were obtained.
Additional cases of infection were identified by reviewing the records of the emergency department to which the affected wrestlers were referred for medical care. Pertinent history and physical-examination data were abstracted from the records of the emergency department; laboratory records were reviewed in the case of wrestlers who had a specimen sent from the emergency department for HSV-1 culture.
During the month after the conclusion of camp, the parents of all the wrestlers were contacted by telephone, and the athletes were interviewed with use of a standardized questionnaire. Information was elicited about the appearance and onset of skin lesions, constitutional symptoms, history of herpes labialis (fever blisters), and specific wrestling activities at camp. Since the investigation was carried out after wrestling had ceased, no cultures of mats or other shared equipment were obtained.
Laboratory Investigation
Oropharyngeal swabs and swabs of skin or mucous membrane were obtained on Culturettes (Baxter Health Care, McGaw Park, I11.) and inoculated within one hour onto rabbit skin cells and human foreskin fibroblasts. High-titer virus stocks were produced from positive cultures by subculture in rabbit skin cells as described.7 Viral DNA was isolated from infected rabbit skin cells by ultracentrifugation through sodium iodide gradients.8 The HSV DNA was cleaved with restriction enzymes BamHI, KpnI, EcoRI, SalI, and HindIII. The endonuclease-cleaved DNA was subjected to electrophoresis in 0.8 percent agarose gels along with DNA from prototype strains HSV-1 17syn+ and HSV-2 HG52. The gels were stained with ethidium bromide.
Serum samples were tested for IgG antibodies to HSV-1 by an enzyme immunoassay (Herpes Stat, Whittaker Bioproducts, Walk-ersville, Md.).
Statistical Analysis
Relative risks, MantelHaenszel summary relative risks, and 95 percent confidence intervals were calculated with standard microcomputer software (Epi-Info, Centers for Disease Control, Atlanta). Chi-square tests or two-tailed Fisher's exact tests were used to test differences in categorical variables.
Results
Epidemiologic Investigation
We obtained clinical data and questionnaire results for 171 of the 175 athletes who attended the camp (98 percent). The median age was 16 years (range, 14 to 18), 153 (89 percent) were white, and 137 (80 percent) were high-school juniors or seniors. The median duration of competitive wrestling was 4 years (range, 1 to 12).
Illness that met the case definition developed in 60 wrestlers (35 percent). Of these, 13 (22 percent) became symptomatic during the first two weeks of camp, and 47 (78 percent) during the final two weeks (Fig. 1). HSV-1 was cultured from 21 of 27 wrestlers (78 percent) who had cultures of suspicious skin lesions. Thirty-nine affected wrestlers were identified on the basis of clinical criteria without confirmation by culture. Two wrestlers had recurrences of previously evident HSV infections during the first week of camp. One had an episode of recurrent herpes labialis, and one had recurrent cutaneous HSV-1 infection. Fiftyeight affected wrestlers (97 percent) had their first clinically apparent HSV-1 infection during the outbreak. In addition, 31 other wrestlers (18 percent of the total group for whom data were obtained) had skin rashes that were not typical of HSV-1 (i.e., that lacked vesicles) or were not described in the medical record with sufficient clarity to determine whether vesicles were present. Because these wrestlers could not be classified clinically as either infected or noninfected, they were excluded from the epidemiologic analysis. A total of 140 wrestlers (60 affected and 80 unaffected) were included in this analysis.
The location of the skin lesions differed markedly from the usual orolabial site of HSV-1 infections (Fig. 2Figure 2
Typical Herpes Gladiatorum (HSV-1) Lesions on the Head and Neck of One of the High-School Wrestlers during the Outbreak.). Forty-four affected wrestlers (73 percent) had involvement of the head, 17 (28 percent) had involvement of the trunk, and 25 (42 percent) had involvement of the extremities. In addition, five had herpetic conjunctivitis or blepharitis; none had keratitis. Thirty-four (57 percent) had skin lesions limited to the right side of the body; 5 (8 percent) had lesions limited to the left side; and 21 (35 percent) had lesions on both sides. Constitutional symptoms were common and included fever (in 25 percent), chills (in 27 percent), sore throat (in 40 percent), and headache (in 22 percent). Thirty-six (60 percent) had tender regional lymphadenopathy on the basis of history or physical examination. The median time reported between onset and complete eschar formation was 6 days (range, 2 to 21). Thirty affected wrestlers (50 percent) were treated with oral acyclovir; the duration of treatment and the clinical response were not assessed.The attack rate was 25 percent ( 12 of 48) in practice group 1 (lightweights), 37 percent (17 of 46) in practice group 2 (middleweights), and 67 percent (31 of 46) in practice group 3 (heavyweights) (relative risk, 2.7; 95 percent confidence interval, 1.6 to 4.6; P<0.001 for the comparison of group 3 with group 1). The attack rate was 28 percent (9 of 32) among wrestlers who reported having had episodes of herpes labialis before attending camp, and 47 percent (51 of 108) among wrestlers who reported no previous vesicular lip lesions (relative risk, 0.6; 95 percent confidence interval, 0.3 to 1.1; P = 0.06). The protective effect of previous herpes labialis was not statistically significant after adjustment for practice group (MantelHaenszel summary relative risk, 0.7; 95 percent confidence interval, 0.4 to 1.2; P = 0.28).
The attack rates were 57 percent (29 of 51) and 29 percent (21 of 73), respectively, in wrestlers who did and those who did not recall wrestling with someone who had a noticeable rash (relative risk, 2.0; 95 percent confidence interval, 1.3 to 3.1; P = 0.002). Thirteen affected wrestlers (22 percent) continued to wrestle for two or more days after the onset of the vesicular skin rash. Because each wrestler had frequent contact with many other members of the practice group during drills, it was not possible to evaluate the effect of the number of wrestling partners as a risk factor. The risk of developing herpes gladiatorum infection on the head was the same (31 percent) in wrestlers who routinely wore headgear and those who did not. There was no association between illness and sharing a water bottle or between illness and the use of antibacterial soap. Twenty-nine of the affected wrestlers (48 percent) recalled having an abrasion or break in the skin at the location of the vesicular rash before the rash developed.
Laboratory Investigation
We performed restriction-endonuclease analysis on all 21 isolates of HSV-1 that were obtained from lesions of the skin or mucous membranes. Four distinct HSV-1 strains were identified with KpnI (Fig. 3Figure 3
Gel Electrophoresis of HSV-1 DNA after Cleavage with the Restriction Enzyme KpnI.) and BamHI (not shown). All 10 isolates from wrestlers in practice group 3 (heavyweights) were identical (strain A) (Fig. 4). In contrast, a different strain of HSV-1 (strain B) was found predominantly in practice group 2 (middleweights); five of the seven isolates from this group were strain B. Practice group 1 had the lowest attack rate, and no single predominant strain was identified. The first illness in practice group 2 occurred in a wrestler with recurrent herpes labialis, and strain B was cultured from his lip.Oropharyngeal swabs for HSV-1 culture were obtained from 34 affected wrestlers and 43 unaffected wrestlers who agreed to participate. The specimens were obtained within seven days of the onset of illness from 20 of the affected wrestlers (59 percent). All oropharyngeal swabs from either affected or unaffected wrestlers were negative for HSV.
Serologic testing was performed on specimens obtained during the final week of camp from 34 unaffected wrestlers and 12 affected wrestlers with a recent onset of symptoms (duration, ≤1 week). The affected wrestlers were more likely to have a nonreactive or weakly reactive enzyme immunoassay than the unaffected wrestlers, but the difference was not statistically significant (odds ratio, 4.0; 95 percent confidence interval, 0.44 to 190; P = 0.25) (Table 1). The occurrence of weakly reactive enzyme immunoassays among the affected wrestlers may represent an early primary serologic response to infection.
Discussion
This outbreak of herpes gladiatorum was unusual because of the large number of cases, the high attack rate in one practice group, and the transmission of a number of distinct viral strains. Behavioral factors contributed to the risk of transmission. Several wrestlers continued to wrestle after the onset of skin lesions, and practice drills were often organized so that most wrestlers in one practice group would have contact with each other. Decreased skin integrity as a result of frequent mat burns may also have contributed. The reason for the unusually high attack rate in practice group 3 is unknown. It may have been due to differences in host susceptibility or in the risk of exposure. Both factors have been independently associated with the transmission of other communicable skin diseases in high-school athletes.9
The results of this investigation support the long-standing hypothesis that herpes gladiatorum is transmitted primarily by direct skin-to-skin contact. The epidemiologic investigation found no evidence of substantial viral transmission by fomites, but the potential contribution of contact with the mat could not be assessed. Each practice group used a separate mat for most workouts, and the moist environment of the mats could have prolonged viral survival. The absence of HSV-1 in the oropharyngeal swabs suggests that saliva was not a major source of transmission. The swab results may underestimate the true prevalence of viral shedding in saliva, however, since shedding may be transient and the swabs were obtained only at the conclusion of the outbreak. In addition, half the affected wrestlers had been treated with acyclovir, which may have reduced viral shedding.
We had expected to find a single strain of HSV-1 common to all the affected wrestlers. Instead, we identified two strains that accounted for most cases and that were transmitted within different practice groups. Strain B was isolated from a wrestler in practice group 2 who initially had a recurrent episode of herpes labialis, and primary skin infections with the same strain subsequently developed in four other wrestlers in that group. No culture was obtained from the wrestler who first had herpetiform skin lesions in practice group 3, but he was the most likely source of the initial transmission of strain A.
Although many wrestlers had typical vesicular skin lesions, there was great variability in the appearance of the rash. It is likely that additional cases were not identified because the vesicular stage was not observed and HSV-1 culture was not obtained. Since the clinical appearance may be unreliable, all suspicious skin and eye lesions should be cultured for HSV-1. In this outbreak, infection of the conjunctiva or eyelid developed in five wrestlers, but the cornea was not affected. The risk of an ocular recurrence is approximately 36 percent within five years,10 and such a recurrence may subsequently involve the cornea after an initial infection of the lid or conjunctiva. Risk factors for ocular involvement have not been defined, but they may include direct contact and autoinoculation.
Strategies to control herpes gladiatorum have not been systematically evaluated. We believe that control efforts should emphasize the early identification of skin lesions and the prompt exclusion of potentially infected wrestlers. Routine skin examinations by coaches or trainers may be helpful, since some athletes are reluctant to report skin lesions that would bar them from competition. During the subsequent (1990) camp session, all the wrestlers were regularly examined by their trainers and encouraged to report all skin lesions promptly. No outbreak was identified.
In response to reports of the transmission of herpes gladiatorum among high-school wrestlers in the 1990–1991 season, the Minnesota State High School League initiated a policy requiring all wrestlers to be examined before competing in regional or state wrestling tournaments. The wrestlers are examined at the time of weighing in by the tournament manager or by another designated person, such as an athletic trainer. Wrestlers with open skin lesions are not allowed to compete until they have obtained a physician's statement indicating that the condition is not communicable.
Further investigation is needed to determine the incidence of herpes gladiatorum infection in high-school wrestlers, to assess the long-term sequelae, and to evaluate control strategies such as those described above. In addition, it is necessary to educate wrestlers, parents, and coaches to increase their awareness of herpes gladiatorum as a serious health risk.
The inclusion of trade names is for identification only and does not imply endorsement by the Department of Health and Human Services, the U.S. Public Health Service, or the Minnesota Department of Health.
We are indebted to the following persons who contributed to this investigation: Richard Danila, Ph.D., Kristen Ehresman, M.P.H., Jan Forfang, M.P.H., Linda Gabriel, Jean Jacobs, David Jones, M.S., Jack Korlath, M.P.H., Jean Kramber, Kristine MacDonald, M.D., Lynne Pearson, Dorothy Reier, M.P.H., John Soler, M.P.H., Don Stiepan, M.P.H., John Thomas, M.P.H., and Susan Turner, M.S.; and to the staff of the Clinical Virology Laboratory at the University of Minnesota.
Source Information
From the Division of Field Services, Centers for Disease Control, and the Acute Disease Epidemiology Section, Minnesota Department of Health (E.A.B.); the University of Minnesota Hospital and Clinic (J.L.G., E.J.H., C.W.A., S.R.H., R.L.M., M.W.M., A.E.); and the Acute Disease Epidemiology Section, Minnesota Department of Health (M.T.O.); all in Minneapolis. Address reprint requests to Dr. Osterholm at the Acute Disease Epidemiology Section, Minnesota Department of Health, 717 S.E. Delaware St., Box 9441, Minneapolis, MN 55440.
- References
References
1
Selling
Full Text | Web of Science | Medline2
Porter
CrossRef | Web of Science | Medline3
Wheeler
CrossRef | Web of Science | Medline4
Dyke
CrossRef | Web of Science | Medline5
White
CrossRef | Web of Science | Medline6
Becker
CrossRef | Web of Science | Medline7
Goodman
CrossRef | Web of Science | Medline8
Walboomers
CrossRef | Web of Science | Medline9
Sosin
CrossRef | Web of Science | Medline10
Liesegang
Web of Science | Medline
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CrossRef3
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CrossRef8
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CrossRef14
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CrossRef20
A. Schuchat. (2000) Microbes without borders: infectious disease, public health, and the journal. American Journal of Public Health 90:2, 181-183
CrossRef21
Mark S. Dworkin, Phyllis C. Shoemaker, Christopher Spitters, Anne Cent, Ann C. Hobson, Jeff Vieira, Lawrence Corey, Lyn R. Frumkin. (1999) ENDEMIC SPREAD OF HERPES SIMPLEX VIRUS TYPE 1 AMONG ADOLESCENT WRESTLERS AND THEIR COACHES. The Pediatric Infectious Disease Journal 18:12, 1108-1109
CrossRef22
Thomas N. Helm, Wilma F. Bergfeld. (1998) Sports dermatology. Clinics in Dermatology 16:1, 159-165
CrossRef23
Israel Potasman, Neora Pick. (1997) Primary Herpes Labialis Acquired during Scuba Diving Course. Journal of Travel Medicine 4:3, 144-145
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CrossRef25
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