Amercan Journal of Epdemology Copyrght 2004 by the Johns Hopkns Bloomberg School of Publc Health All rghts reserved Vol. 160, No. 10 Prnted n U.S.A. DOI: 10.1093/aje/kwh304 Incdence and Rsk Factors for Concusson n Hgh School Athletes, North Carolna, 1996 1999 Mark R. Schulz 1, Stephen W. Marshall 2,3, Frederck O. Mueller 3,4, Jngzhen Yang 5, Nancy L. Weaver 6, Wllam D. Kalsbeek 7, and J. Mchael Bowlng 5 1 Department of Publc Health Educaton, School of Health and Human Performance, Unversty of North Carolna at Greensboro, Greensboro, NC. 2 Departments of Epdemology and Orthopedcs, School of Publc Health, Unversty of North Carolna at Chapel Hll, Chapel Hll, NC. 3 Injury Preventon Research Center, School of Publc Health, Unversty of North Carolna at Chapel Hll, Chapel Hll, NC. 4 Department of Exercse and Sport Scence, Unversty of North Carolna at Chapel Hll, Chapel Hll, NC. 5 Department of Health Behavor and Health Educaton, School of Publc Health, Unversty of North Carolna at Chapel Hll, Chapel Hll, NC. 6 Health Communcaton Research Laboratory and the Department of Communty Health, Sant Lous Unversty, Sant Lous, MO. 7 Survey Research Unt, Department of Bostatstcs, School of Publc Health, Unversty of North Carolna at Chapel Hll, Chapel Hll, NC. Receved for publcaton July 24, 2003; accepted for publcaton June 4, 2004. A prospectve cohort study was used to quantfy rsk factors for sports concussons. Analyss was based on a stratfed cluster sample of North Carolna hgh school athletes followed durng 1996 1999. Clusterng was by school and sport, and the sample ncluded 15,802 athletes wth 1 8 seasons of follow-up per athlete. Concusson rates were estmated for 12 sports, and rsk factors were quantfed usng generalzed Posson regresson. Concusson rates ranged from 9.36 ( : 1.93, 16.80) per 100,000 athlete-exposures n cheerleadng to 33.09 ( : 24.74, 41.44) per 100,000 athlete-exposures n football, where athlete-exposure s one athlete partcpatng n one practce or game. The overall rate of concusson was 17.15 ( : 13.30, 21.00) per 100,000 athlete-exposures. Cheerleadng was the only sport for whch the practce rate was greater than the game rate. Almost two thrds of cheerleadng concussons nvolved two-level pyramds. Concusson rates were elevated for athletes wth a hstory of concusson, and they ncreased wth the ncreasng level of body contact permtted n the sport. After adjustment for sport, body mass ndex, and year n school, hstory of concusson(s) remaned a moderately strong rsk factor for concusson (rate rato = 2.28, : 1.24, 4.19). The fact that concusson hstory s an mportant predctor of concusson ncdence, even n ths young populaton, underscores the mportance of prmary preventon efforts, tmely dentfcaton, and careful clncal management of these njures. athletc njures; bran concusson; Posson dstrbuton; rsk factors; sports; students Abbrevatons: NCHSAA, North Carolna Hgh School Athletc Assocaton; NCHSAIS, North Carolna Hgh School Athletc Injury Study. Because partcpaton n sports nvolves the potental for mpact to the head, athletes are at partcular rsk for concusson. Permanent bran damage and even death can result f sports-related concussons are not dagnosed and treated properly. Second-mpact syndrome, a condton wth a mortalty rate of nearly 50 percent, may occur when an athlete who has sustaned even a mld concusson sustans a second concusson before symptoms assocated wth the frst have resolved (1). Hgh school athletes, who numbered nearly 7 mllon n 2000 2001, are the largest group of athletes at rsk of concusson (2). An estmate of the annual number of sports- and physcalactvty-related concussons s derved from data collected n the Injury Supplement to the 1991 Natonal Health Intervew Correspondence to Dr. Mark Schulz, 437 HHP Buldng, P.O. Box 26170, Unversty of North Carolna at Greensboro, Greensboro, NC 27402-6170 (e-mal: mrschulz@uncg.edu). 937 Am J Epdemol 2004;160:937 944
938 Schulz et al. Survey. Usng data from ths survey, Sosn et al. (3) estmated a total of 1.54 mllon traumatc bran njures that nvolved loss of conscousness n the year pror to the ntervew. Of these njures, 306,000 (95 percent : 262,000, 354,000) were attrbuted to sports or physcal actvty. A key lmtaton of these natonal survellance data s that data on concussons not resultng n loss of conscousness were not avalable (4). Many more sportsrelated concussons would lkely be dentfed f the estmates produced from the Natonal Health Intervew Survey data were supplemented by data on concussons not resultng n loss of conscousness. A survey of 242 certfed athletc traners employed by hgh schools and colleges reported that 90 percent of ther football-related concussons dd not nvolve loss of conscousness (5). Much of the attenton that concusson has receved (5 10) has focused on concussons n football. Recent studes have estmated concusson rates n other collson sports, such as hockey (11) and rugby (12), and two large, natonal studes have documented how concusson rates vary by sport and exposure type (games vs. practces) (13, 14). Stll, for some sports, such as women s track and compettve cheerleadng, no publshed concusson rates are avalable. Several of the football studes have ndcated a strong assocaton between concusson hstory and ncdent concusson (5, 9). However, ths assocaton has not been demonstrated n any other sport, and no studes have been publshed that examned how the relaton between concusson hstory and the concusson rate s affected by covarates. Several varables such as age, body sze and type, access to proper facltes, and educaton of coaches have been postulated as determnants of athletc njures (15 19), but these varables have not been explored emprcally as determnants of concusson n sports. The purpose of ths study was to examne the ncdence rate of sports-related concussons by sport and to estmate the assocaton between hstory of prevous concusson(s) and concusson rate, adjusted for varables that have been postulated to affect the concusson rate. MATERIALS AND METHODS Sample selecton Data were collected as part of the North Carolna Hgh School Athletc Injury Study (NCHSAIS), a prospectve cohort study of the njury experence of North Carolna hgh school athletes (20). Weaver et al. (21) descrbed the selecton of the study populaton n detal. The study populaton was selected usng a stratfed two-stage cluster-samplng desgn. In the frst stage, 100 schools were selected from among the 324 hgh schools that are members of the North Carolna Hgh School Athletc Assocaton (NCHSAA). In the second stage at each partcpatng school, sx teams were randomly selected for follow-up from the 12 sports (football, cheerleadng, wrestlng, volleyball, baseball, softball, boys and grls basketball, boys and grls soccer, and boys and grls track) ncluded n the study. The samplng process attempted to ensure that all NCHSAA athletes had the same selecton probablty. The samplng probabltes and data on nonresponse at the frst and second levels were used to construct samplng weghts for the purpose of estmatng ncdence for the populaton of all NCHSAA athletes. Data collecton The selected varsty teams were followed for 3 years, and one contact person at each school, ether an athletc traner or athletc drector, had ultmate responsblty for ensurng the tmely and accurate completon of data forms. Varsty athletes were enrolled n the NCHSAIS 1 day after they receved a consent letter to share wth ther parents. Besdes nformng parents of what ther chld s partcpaton would ental, the letter offered parents a toll-free number to contact the project staff (f parents had questons or declned partcpaton n the study). Because there was lttle rsk to the athletes and gven the extreme logstc challenges, wrtten consent was not requred. The consent letter and the protocol of the NCHSAIS were approved by the Insttutonal Revew Board of the Unversty of North Carolna School of Publc Health. Each varsty athlete partcpatng n a selected sport completed a demographc form at the begnnng of each season. The form requested nformaton regardng sport, grade n school, sex, weght, heght, and hstory of prevous concussons regardless of the cause of concusson. Each head coach also completed a demographc form that asked for nformaton about educatonal attanment. To document the number of players who partcpated n each game or practce durng the preseason and regular season, partcpaton forms smlar to attendance sheets were completed weekly for each team. If an athlete partcpated n any part of a game or practce, he or she was consdered to have partcpated, and nformaton was not collected on the degree of partcpaton. An njury report form requested nformaton on njury event crcumstances (whether the njury occurred durng a game or practce and whether the njury occurred durng preseason, regular season, or postseason) and nature of the njury (type of njury and body part njured). A reportable njury was defned as one that occurred as a result of partcpaton n varsty hgh school sports and that ether lmted the student s full partcpaton n the sport the day followng the njury or requred medcal attenton by a health professonal. In addton, all bran concussons were defned as reportable njures. Multple njures were reported for any gven njury event wth a separate njury form beng completed for each separate njury. Ascertanment of concussons Am J Epdemol 2004;160:937 944 Although there s no generally agreed upon defnton of concusson, a commonly referenced defnton s a clncal syndrome characterzed by mmedate and transent posttraumatc mparment of neural functons, such as alteraton of conscousness, dsturbance of vson, equlbrum, etc., due to bran stem nvolvement (22, p. 388). For ths study, ncdent concusson was operatonalzed wth two questons. Frst, concusson was one of 16 possble responses that school contacts could use to descrbe the type of njury. The second queston elcted nformaton about sgns and symp-
Incdence and Rsk Factors for Concusson 939 whether or not he or she had ever experenced a concusson. We dd not ask about the severty of past concussons. FIGURE 1. Exact wordng of questons used to dentfy concussons among 19,903 hgh school athletes who competed durng the preseason and regular season, North Carolna, 1996 1999. toms consstent wth concusson, such as the length of dsorentaton/confuson, the absence or presence of short-term memory loss, and the duraton of lost conscousness assocated wth the njury. The exact wordng of the questons appears n fgure 1. If an njury was desgnated as a concusson n response to queston 1, the njury was counted as a concusson. If an njury type other than concusson was desgnated on an njury form but sgns and symptoms consstent wth a concusson were reported n response to the second queston, the entre njury form was revewed by one of the authors (M. S.), wth specal focus on responses to the questons about the nature of the njury event. After revew of the njury form, the same author (M. S.) determned whether the concusson-related sgns and symptoms were most lkely due to a sport-related concusson or another njury or health condton, such as heat stress. Injures determned to be concussons after the revew were combned wth the njures desgnated as concussons n the frst queston. Fnally, as mentoned above, retrospectve self-reported lfetme hstory of concusson was obtaned at the begnnng of each season, when each ndvdual athlete completed the athlete demographc form. The queston used smply asked the athlete Am J Epdemol 2004;160:937 944 Data analyss Because the study was a 3-year prospectve cohort study, many of the hgh school athletes partcpated for more than one athlete-season (one athlete partcpatng for one season), and therefore there were multple observatons for many athletes. The resultng data structure was a longtudnal data set comprsng between one and eght observatons for each athlete. Because of dffcultes n collectng complete postseason partcpaton data, all concusson rate estmates and models were lmted to preseason and regular season data. To compare concusson ncdence between sports, sportspecfc concusson ncdence densty rates per athletegame (one athlete n one game), per athlete-practce (one athlete n one practce), and per athlete-exposure (one athlete partcpatng n one practce or game) were estmated as follows: Game rate (r g ) = weghted sum of game concussons ( wn g )/weghted sum of athlete-games ( we g ). Practce rate (r p ) = weghted sum of practce concussons ( wn p )/weghted sum of athlete-practces ( we p ). Overall rate (r) = weghted sum of concussons ( wn a )/ weghted sum of athlete-exposures ( we a ), where athlete-exposures (e a ) = the sum of athlete-games (e g ) and athlete-practces (e p ), total concussons (n a ) = the sum of game concussons (n g ) and practce concussons (n p ), and = the sum over all atheletes. The 95 percent s of the rates were calculated usng the formula, 95 percent of rate = rate ± 1.96 (varance of the rate) 1/2 (23). The weghts n the equatons above account for complex survey desgn and dfferental nonresponse at dfferent levels of the survey desgn, and they serve to estmate results for all NCHSAA athletes on the bass of the athletes ncluded n the study (21). For the purposes of multvarate adjustment of the assocaton between prevous concusson and concusson rate, a Posson regresson model was developed that ncluded several athlete-level covarates (sport, body mass ndex, year n school), calendar tme, school sze (as a proxy for access to facltes and resources), and hghest educatonal attanment by head coach. Sports were grouped as contact (football and wrestlng), lmted contact (basketball, soccer, baseball/softball), and noncontact (track, cheerleadng, and volleyball) and as collson (football) versus noncollson (all other study sports). Grade n school, hghest educatonal attanment by coach, and body mass ndex were categorzed n several dfferent ways n bvarate analyses to determne the shape of ther relatons to the concusson rate before ncluson n the multvarate model. Snce the objectve of the Posson model was to descrbe the concusson rate as a functon of the covarates whle accountng for the complex sample survey used to collect the
940 Schulz et al. TABLE 1. Rate of concusson by sport among 19,903 hgh school athletes who competed durng the preseason and regular season, North Carolna, 1996 1999 * Annual statewde ncdence n North Carolna Hgh School Athletc Assocaton hgh schools. Athlete-exposure s one athlete partcpatng n one practce or game; athlete-game s one athlete n one game; athlete-practce s one athlete n one practce. IRR g/p, njury rate rato where the practce rate s the referent. data, SUDAAN, verson 8.0 (24), software was used to ft the Posson regresson model. Generalzed Posson models account for the correlaton of teams wthn schools and athletes wthn teams that s expected n data clustered by school and team when they were collected (25). RESULTS Actual no. of concussons Annual weghted no. of concussons* Of the 2,750 reported njures n the NCHSAIS, 206 were ascertaned to be concussons. Only 8 percent of the concussons resulted n a loss of conscousness. Eghty-two concussons were ascertaned by the school contacts responsble for ensurng the completon of the njury forms. An addtonal 124 concussons were ascertaned by one of the study authors (M. S.) through a revew of the njury event crcumstances surroundng 135 njures for whch concusson sgns and symptoms were reported on njury forms but the njury type was not desgnated as concusson. Of the total concussons, 168 occurred durng the 1,024,636 regular and preseason athlete-exposures. These data were weghted, and the number of concussons and concusson rates per 100,000 athleteexposures for specfc sports and all sports combned are reported n table 1. Sport- and sex-specfc njury rates Annual weghted no. of athleteexposures ( 10 5 ) Rate/ 100,000 athleteexposures Football had the hghest overall and game concusson rate (table 1). In contrast, the football practce rate was exceeded Rate/ 100,000 athletegames Rate/ 100,000 athletepractces IRR g/p by the practce rate n cheerleadng. The njury rate rato comparng the game rate wth the practce rate was greater than one for both sexes and for all sports except cheerleadng. Besdes beng substantally less than one, the of the game/practce rate rato for cheerleadng dd not overlap wth those of half the other sports (table 1). Posson regresson models of the concusson rate Sport Football 75 280 8.48 33.09 24.74, 41.44 148.84 102.82, 194.87 8.47 3.90, 13.04 17.57 8.87, 34.83 Boys soccer 24 69 2.95 23.31 8.40, 38.22 59.34 18.10, 100.58 2.67 0, 6.39 22.23 4.41, 111.98 Grls soccer 6 18 1.38 13.21 0, 27.30 19.91 0.43, 39.39 7.94 0, 19.84 2.51 0.86, 7.35 Boys basketball 12 33 3.21 10.25 4.20, 16.29 25.92 10.05, 41.78 1.89 0, 4.53 13.75 3.15, 59.95 Grls basketball 10 52 2.97 17.49 0.80, 34.18 46.66 0, 94.19 1.74 0, 5.08 26.78 2.65, 270.81 Baseball 9 30 2.49 11.98 3.10, 20.86 16.99 3.00, 30.97 8.37 0, 19.72 2.03 0.40, 10.18 Softball 6 21 2.04 10.14 1.48, 18.80 19.99 0, 41.90 4.09 0, 9.48 4.88 0.79, 30.36 Wrestlng 13 29 3.05 9.36 0, 19.21 15.96 0, 34.00 7.08 0, 15.21 2.25 0.92, 5.58 Cheerleadng 7 21 2.27 9.36 1.93, 16.80 3.38 0, 9.99 11.32 1.84, 20.81 0.30 0.04, 2.51 Boys track 4 25 2.48 10.14 0, 25.16 48.66 0, 122.08 0 Grls track 2 29 2.03 14.34 0, 43.23 59.30 0, 181.18 0 Total 168 607 35.40 17.15 13.30, 21.00 46.22 33.90, 58.55 5.20 3.22, 7.17 8.90 5.67, 13.96 Gender Males 137 466 22.60 20.61 15.31, 25.91 61.50 42.00, 80.99 5.81 3.30, 8.31 10.59 6.28, 17.86 Females 31 141 12.80 11.04 4.30, 17.78 24.92 4.78, 45.06 4.01 1.25, 6.77 6.22 1.97, 19.64 Unadjusted estmates ndcated that havng a hstory of one or more prevous concussons was a moderately strong predctor of the concusson rate (table 2). Almost 4.5 percent of the athletes had a hstory of prevous concussons. Lkewse, partcpaton n contact sports was a moderately strong predctor of the concusson rate (table 2). Beng a nnth grader or havng a body mass ndex n the bottom quntle of the study athletes was a moderately strong protectve predctor of the concusson rate. Although beng a nnth grader appeared to be protectve, the concusson rate dd not ncrease monotoncally wth grade n school. Lkewse, the concusson rate dd not ncrease monotoncally wth quntles of athlete body mass ndex. Nether school sze nor the hghest educatonal level acheved by the head coach appeared to have a predctve nfluence on the concusson rate, but concusson rates were notceably hgher n the second year of the study compared wth ether year 1 or 3. Am J Epdemol 2004;160:937 944
Incdence and Rsk Factors for Concusson 941 TABLE 2. Rate ratos and s for concusson among 19,903 hgh school athletes who competed durng the preseason and regular season, North Carolna, 1996 1999 Exposure Unadjusted rate rato Multvarateadjusted rate rato (full model) Adjusted rate rato (parsmonous model) Athlete-level varables Concusson hstory No hstory of concusson(s) 1.00 Referent 1.00 Referent 1.00 Referent Hstory of concusson(s) 2.95 1.67, 5.24 2.25 1.14, 4.44 2.28 1.24, 4.19 Degree of contact Partcpaton n noncontact sports 1.00 Referent 1.00 Referent 1.00 Referent Lmted contact sports 1.73 0.67, 4.48 1.89 0.68, 5.25 2.01 0.70, 5.73 Full contact sports 3.13 1.18, 8.29 3.28 1.26, 8.58 3.84 1.42, 10.40 Body mass ndex Athletes wth hghest 80% of body mass ndexes 1.00 Referent 1.00 Referent 1.00 Referent Athletes wth lowest 20% of body mass ndexes 0.26 0.12, 0.59 0.44 0.20, 0.99 0.40 0.18, 0.90 13.3 <19.6 (bottom quntle) 1.00 Referent 19.6 <21.0 (second quntle) 2.78 1.18, 6.48 21.0 <22.6 (thrd quntle) 4.21 1.86, 9.57 22.6 <25.1 (fourth quntle) 3.59 1.36, 9.44 25.1 <52.0 (top quntle) 4.47 1.79, 11.17 Grade Sophomores to senors 1.00 Referent 1.00 Referent 1.00 Referent Nnth graders 0.45 0.22, 0.91 0.61 0.29, 1.27 0.60 0.30, 1.20 Senors 1.00 Reference Junors 0.70 0.40, 1.23 Sophomores 0.75 0.42, 1.36 Nnth graders 0.37 0.17, 0.81 Calendar tme 1998 1999 1.00 Referent 1.00 Referent 1997 1998 2.53 1.49, 4.29 2.32 1.24, 4.32 1996 1997 1.19 0.67, 2.13 1.41 0.82, 2.44 School level Class 4A (1,314 2,600 students) 1.00 Referent 1.00 Referent Class 3A (967 1,308 students) 0.63 0.36, 1.12 0.97 0.51, 1.84 Class 2A (668 957 students) 1.10 0.61, 1.99 1.58 0.75, 3.31 Class 1A (<668 students) 0.74 0.39, 1.40 1.26 0.62, 2.58 Head coach qualfcatons Master s degree 1.00 Referent 1.00 Referent No master s degree 0.74 0.48, 1.13 0.94 0.60, 1.49 When all these varables hstory of concusson, sport by contact level, body mass ndex (top 80 percent vs. bottom 20 percent), grade n school (12th grade vs. 9th 11th grades), calendar year, school sze, hghest educatonal degree completed by head coach were ncluded n a model, hstory of prevous concusson(s) was stll assocated wth a greater than twofold elevaton of the concusson rate, and the assocaton of the other varables wth the concusson rate changed lttle (table 2). Besdes hstory of concusson(s), partcpaton n contact sports, beng n the bottom quntle of study athlete body mass ndexes, and year 2 of the study appeared to be the strongest predctors of the concusson rate. Because the assocaton between concusson hstory and ncdent concusson was of nterest, further modelng Am J Epdemol 2004;160:937 944
942 Schulz et al. TABLE 3. Concusson ncdence comparng athletes wth and wthout a hstory of prevous concusson(s) among 19,903 hgh school athletes who competed durng the preseason and regular season, North Carolna, 1996 1999* Sport One or more prevous concussons No. of ncdent concussons No. of athleteexposures Incdence rate/10,000 athleteexposures No. of ncdent concussons No prevous concusson No. of athleteexposures Incdence rate/10,000 athleteexposures Rate rato Football,# 151 126,542 11.92 691 2,416,272 2.86 4.17 1.70, 10.23 Nonfootball 50 300,689 1.66 930 7,775,166 1.20 1.38 0.56, 3.44 All sports 201 427,231 4.70 1,621 10,191,439 1.59 2.95 1.67, 5.24 focused on obtanng a parsmonous estmate of ths assocaton. The confoundng effect of each varable was determned by removng varables from the model on a one-byone bass; a varable was retaned n the model f ts removal changed the rate rato for hstory of concusson by more than 10 percent. The fnal model ncluded only a three-level term for sport (contact, lmted contact, noncontact), a dchotomous term for body mass ndex (lowest quntle vs. top four quntles), and a dchotomous term for grade n school (nnth grader vs. all others) as mportant confounders of the relaton between prevous concusson(s) and the concusson rate (table 2). The parsmonous, adjusted estmate of the concusson rate rato of those wth a hstory of concusson(s), compared wth those wth no reported hstory, was nearly dentcal to the rate rato estmated for the full model (table 2). Partcpaton n football, the only collson sport n the study, was a bologcally plausble effect measure modfer of the assocaton between hstory of concusson(s) and the concusson rate (table 3). In unadjusted analyss, n a comparson of the concusson rate of those wth a hstory of concusson(s) wth the rate of those wth no reported hstory, the rate rato was greater than 4 among football players and only slghtly greater than 1 among all other study athletes. Data were too sparse to permt an assessment of other covarates as modfers. DISCUSSION * Weghted data. Not adjusted for any other varables. Athletes sustanng one or more concussons wthn a season. An athlete-exposure s one athlete partcpatng n one practce or game. The rate rato for those athletes partcpatng n football wth no hstory of prevous concusson(s) relatve to those not partcpatng n football wth no hstory of prevous concusson(s) was 2.4 ( : 1.5, 3.8). # The rate rato for those athletes partcpatng n football wth a hstory of prevous concusson(s) relatve to the referent group of those not partcpatng n football wth no hstory of prevous concusson(s) was 10.0 ( : 4.22, 23.55). Multple concussons Rsk of concusson was elevated more than twofold among athletes wth a hstory of concusson(s) relatve to athletes wthout a hstory of concusson(s) even after adjustng for sport, body mass ndex, and grade n school. Ths s the frst prospectve study to dentfy hstory of concusson(s) as a potental rsk factor for future concussons. Hstory of concusson(s) was also observed to be a potental rsk factor for subsequent concussons by Gerberch et al. (9) and more recently by Guskewcz et al. (5) n ther studes of football players. Several aspects of the current study lend weght to the dentfcaton of retrospectve hstory of concusson as a rsk factor for subsequent ncdent concusson. Frst, both ncdent concussons and exposure tme were assessed prospectvely, reducng the probablty of recall bas; second, the regresson models used account for ndvdual exposure dfferences at the level of athlete-exposure; and thrd, mportant potental confounders, sport, body mass ndex, and grade n school, were consdered and elmnated as alternatve explanatons of the observed assocaton. Two explanatons can be consdered for why a retrospectve hstory of concusson s assocated wth elevated rsk of prospectve ncdent concusson. Frst, t s possble that the ablty of the bran to respond to traumatc nsults may be compromsed n prevously concussed athletes, makng them more susceptble to another concusson. Ths scenaro s the chronc analog to second-mpact syndrome, except that the second njury n second-mpact syndrome s not a concusson but rather a serous traumatc bran njury that can result n death (1). Ths compromsed state of the bran, f present, s not easly detected by current methods. Collns et al. (8) found some evdence of long-term cogntve defcts among football players wth two or more concussons compared wth those wth none, but Maccocch et al. (10) dd not fnd smlar defcts among football players wth two concussons compared wth those wth one concusson. Lkewse, Guskewcz et al. (26) reported no assocaton between chronc cogntve mparment and a hstory of mld concussons among collegate soccer players. Alternatvely, t may be that the rsk of concusson s greater among those wth a hstory of concusson for envronmental and behavoral reasons. Some athletes are exposed to more athletc actvty because they play more mnutes wthn games or practces, and some athletes are Am J Epdemol 2004;160:937 944
Incdence and Rsk Factors for Concusson 943 exposed to more ntense athletc actvty (n terms of the number and force of the collsons that athletes experence) because of ther ndvdual or team style of play. These same athletes may contnue to be exposed to more mnutes or more ntense athletc actvty for the same reasons, even after havng the frst concusson. The current study lends some support to ths argument. It ndcates that the effect estmate for hstory of concusson wthn the football strata s much stronger than the effect estmate for hstory of concusson for the other sports, and football players would appear to be exposed to more collsons and more forceful collsons than athletes n the other study sports. Sgnfcance Because the study was based on a stratfed two-stage cluster sample and examned 12 sports (ncludng sx grls sports), the current study broadens the understandng of sports concussons. Most of the concusson lterature has focused on football; for grls track and cheerleadng, concusson rates have not prevously been reported n the lterature. Interestngly, cheerleadng was the only sport for whch the concusson rate rato comparng the game rate wth the practce rate was less than one. One possble explanaton for ths fndng s that cheerleaderng teams n competton are judged on the bass of both the dffculty and the form of ther routnes; ths scorng method could nfluence cheerleader behavor so as to reduce rsk n games relatve to practces. Another possble explanaton would be that more and stronger spotters (ndvduals assgned to spot and catch fallng performers) are avalable for compettons than for practce (27). Several nvestgators (28, 29) have hghlghted the mportance of collectng specfc and accurate exposure data to measure tme at rsk of njury for populatons of athletes. For njury rates to be comparable between studes, comparable measures of tme at rsk, as well as comparable defntons of njury and comparable methods of njury ascertanment, must be utlzed. The measure of tme at rsk used n ths study, the athlete-exposure (.e., one athlete partcpatng n one practce or game), s a detaled measure of tme at rsk that can be collected (albet wth a good deal of work) at ths level. Obvously, snce each athlete-game and each athletepractce are assocated wth dfferent actvtes and varyng mnutes of actvty, t would be deal to capture a more precse estmate of the mnutes of each athlete (athletemnutes) spent on each type of sport-specfc actvty (e.g., offense, defense, runnng, tacklng, sdelne cheerng, partner stunts, and so on). However, ths level of detal was beyond the scope of the study. The approach taken n ths study may underestmate game concusson rates per athletemnute for sports n whch many athletes partcpate for bref perods of tme relatve to sports n whch fewer players partcpate for longer tme perods. The current study used athletc traners where they were avalable to document njures, whch was n only 33 percent of the schools. The choce of data collector was manly drven by the fact that the majorty of hgh schools do not have certfed athletc traners. Consequently, some concussons may have gone uncounted. Ths lmtaton was n part remeded by Am J Epdemol 2004;160:937 944 ncludng a bref queston about head njury symptoms, whch allowed the concussons, not orgnally dentfed by our data collectors, to be dentfed n the analyss. Calendar year of the concusson remaned an mportant predctor of the overall concusson rate n the full model, but t dd not affect the relaton between hstory of concusson and the concusson rate. Snce no other covarate appeared to confound the assocaton between calendar year and the overall concusson rate, t may be that concusson ascertanment was more complete for the second year of the study (1997 1998) compared wth ether the frst or thrd year. Ths explanaton s bolstered by the fact that the njury rate for athletc njures of all types was elevated for year 2 relatve to the other years n the NCHSAIS (20). Ascertanment of concusson hstory and possblty of bas n effect estmate Recall decay regardng events n the more dstant past may have led to an underestmaton of the number of prevous concussons suffered by athletes n ths study. Harel et al. (30) descrbed how the njury rates of chldren and adolescents based on nformaton provded by ther mothers declned as the recall perod that mothers were reportng became more dstant n tme. In the current study, the athlete reported hs or her own njury hstory so we are concerned wth the recall of the athlete rather than that of a proxy. The prmary nterest of ths study was to estmate the assocaton between a hstory of prevous concussons and the current concusson rate. Ths effect estmate would only have been based by the athletes recall decay f ther recall decay was assocated wth the ascertanment of concussons durng the study perod (31). Snce concusson ascertanment was done by school contacts who were unaware of the athlete s responses regardng hstory of prevous concussons, t s unlkely that the recall decay of the athletes regardng ther prevous concussons would be assocated wth the ascertanment of ncdent concussons. However, as Gerberch et al. (9) suggested, athletes who recalled a past concusson were more vgorous n reportng concusson symptoms than those wth no recall of past concusson, perhaps because the former were more aware of concusson symptoms and the attendant dangers. To help quantfy the extent to whch underreportng of concussons n those wth a negatve concusson hstory could have ntroduced a bas, we conducted a small senstvty analyss usng smple determnstc methods (31). The workng assumpton for the senstvty analyss was that specfcty was 100 percent (.e., all recorded concussons represented true concussons). If the dfference n underreportng between those wth and wthout a hstory of concusson was up to 10 percent, only a modest degree of bas was present. Under ths scenaro, the corrected rate rato (for the unadjusted rate rato of 2.96) ranged from 2.70 to 3.29 for hstory of concusson. Even f the dfference n underreportng was up to 20 percent, the range of the corrected rate rato expanded to only 2.37 3.70. Ths suggests that underreportng of concussons s not a major threat to the valdty of ths fndng as long as t s nondfferental or moderately dfferental wth respect to hstory of concusson.
944 Schulz et al. Concluson The results of ths study broaden the knowledge base regardng concusson n hgh school athletes, especally wth respect to cheerleadng and grls track. Cheerleadng appears to be exceptonal n that t s the only sport n whch the rsk of concusson s greater n practce than t s n competton, pontng to a need to focus cheerleadng concusson preventon efforts on practces. In multvarate regresson models, the relaton between hstory of concusson and the concusson rate remaned strong after adjustment for several covarates n the multvarate model, but when sports were categorzed as collson sports (football) versus noncollson sports (the 11 other sports), the assocaton of hstory of concusson wth the concusson rate was found to be much stronger for the collson sport (football) than for the noncollson sports. ACKNOWLEDGMENTS Ths study was supported by grants from the Natonal Insttute of Arthrts, Musculoskeletal, and Skn Dseases (R01AR42297) and the Natonal Center for Injury Preventon and Control (R49/CCR402444) to the Unversty of North Carolna Injury Preventon Research Center. The authors express ther apprecaton to Dr. Dana P. Looms, Dr. Carol W. Runyan, John Sderas, Bran Sutton, the Advsory Board (especally, Dck Knox and Dr. Wllam E. Prentce, Jr.), and the athletc traners and athletc drectors who partcpated n ths project. REFERENCES 1. Cantu RC. Second-mpact syndrome. Cln Sports Med 1998;17: 37 44. 2. Natonal Federaton of State Hgh School Assocatons. NFHS 2001 hgh school athletcs partcpaton survey. Kansas Cty, MO: Natonal Federaton of State Hgh School Assocatons, 2001. 3. Sosn DM, Snezek JE, Thurman DJ. Incdence of mld and moderate bran njury n the Unted States, 1991. Bran Inj 1996;10: 47 54. 4. Thurman DJ, Branche CM, Snezek JE. 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