DOI: 10.1161/CIRCULATIONAHA.115.015431

Harmon et al.; Sudden Cardiac Death in NCAA Athletes: 10-Years Kimberly G. Harmon, MD1; Irfan M. Asif, MD2; Joseph J. Maleszewski, MD3; David S. Owens, MD, MS1; Jordan M. Prutkin, MD, MHS1; Jack C. Salern Salerno, rn no, M MD D1; Monica L. Zigman, MPH1; Rachel Ellenbogen, MS4; Ashwin Rao, MD1; Michael M Mi chael J. Ackerman, MD, PhD hD3; Jonathan A. Drezne Drezner, nerr, MD1 ne

1

University Un y ooff Wa Washington, W shiing gton n, Seattle, Se e WA; WA; 2Un University Unive erssity y ooff So South outh Carolina Carolin Ca na Gr Greenville, reeenvillle,, Gr Greenville, reeenvillee, SC;; 3Ma SC Mayo yo C Clinic, lini li nic, ni c, R Rochester, oche oc hest he ster st er,, MN er MN;; 4Br Brown Brow own ow n Un University, Univ iver iv ersi er sity si ty,, Pr ty Providence, Prov ovid ov iden id ence en ce,, RI ce

Kimberly G. Harmon, MD University of Washington 3800 Montlake Blvd. Seattle, WA 98195 Tel: 206-598-3294 Fax: 206-598-6144 E-mail: [email protected] Etiology:[8] Epidemiology, Cardiovascular (CV) surgery:[41] Pediatric and congenital heart disease, including cardiovascular surgery, Treatment:[121] Primary prevention, Treatment:[122] Secondary prevention 1 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

Background The incidence and etiology of sudden cardiac death (SCD) in athletes is debated with hypertrophic cardiomyopathy (HCM) often reported as the most common etiology. Methods and Results—A database of all NCAA deaths (2003 – 2013) was developed. Additional information and autopsy reports were obtained when possible. Cause of death was adjudicated by an expert panel. There were 4,242,519 athlete-years (AY) and 514 total student athlete deaths. Accidents were the most common cause of death (257, 50%, 1:16,508 AY) followed by medical causes (147, 29%, 1:28,861 AY). The most common medical cause of death was SCD (79, 15%, 1:53,703 AY). Males were at higher risk than females 1:37,7 1:37,790 790 A AY Y vs. vs 1:121,593 AY (IRR 3.2, 95% CI, 1.9-5.5, p < .00001), and black k athletes were at higher risk than white whit te at athletes athl hlet hl etes et es 1:2 1:21,491 21, 1 491 AY vs. 1:68,354 AY (IRR RR 3.2, 3.2, 95% CI, 1.9-5.2, 2, p < .00001). The incidence nciidence of SCD CD inn Division Divi visi vi sion si on 1 male mal alee basketball b sket ba ettball baa athletes ath th hletees was waa 1:5,200 1::5, 5 20 00 AY AY. Th The he mo most st com common ommo om mon mo n findings fi ind ndin ings in g at au autopsy aut top psy we were eree aut autopsy top opsy sy nnegative e attiv eg ve su sudden udden n uunexplained nexp xplain xp in ned ed ddeath eaath h (AN (AN-SUD) AN-S SUD UD) in n 16 16 (2 ((25%) 5%) an and nd definitive dde efi fini fi niti iti tive ve eevidence viidenc vide ncee fo ffor orr HC HCM M wa wass se seen en iinn 5 (8%). (8%) (8 %). Me %) Media M edi diaa reports di repo re port rts ts id identified iden enti tifi ti fied fi ed dm more oree de or ddeaths eat aths ths iin n hi high higher gher herr divisions (87%, 61%, and 44%) while percentages from the internal database did not vary (87%, 83%, and 89%). Insurance claims identified only 11% of SCDs. Conclusions The rate of SCD in NCAA athletes is high, with males, black athletes and basketball players at substantially higher risk. The most common finding at autopsy is AN-SUD. Media reports are more likely to capture high profile deaths, while insurance claims are not a reliable method for case identification.

sudden cardiac death, epidemiology, pathology, sudden cardiac arrest, athlete

2 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

Sudden cardiac death (SCD) in an athlete is a tragic event with far-reaching impact. Those directly impacted by SCD struggle to understand why more effective screening techniques were not utilized as part of preparticipation exams required of nearly all US athletes. The rationale for the current screening model is that although SCD is shocking and often highly publicized, it is relatively rare and therefore not cost-effective to invest additional resources toward prevention.1 However, the incidence of SCD in athletes in the US is vigorously debated with much of the variation attributable to study methodology, specifically the accuracy of case identification and ascertainment of the population studied (denominator).2 Estimates of the rate of SCD in athletes range from 1:3,000 athlete-years (A (AY) Y) iin n National Collegiate Athletic Association (NCAA) Division I male basketball athletes3 to 1:917,000 1:91 17, 7,00 000 00 0 AY re reported eported in Minnesota high school epo ol aathletes; t letes;4 a differencee of th o over 300-fold. Traditional T raaditional ad estimates estiima matess of SCD SCD incidence incid ncid ideenc ence in US US athletes athlettes are are re usually usu uallly l aaround roun ro und un d 1:200,000 1:20 200 20 0,00 000 00 0 AY5, 6 although al lth thou ough ou g studies stu udi d es sp specifically peciificcally y examining ex xam min inin ng college c llleg co ge at athletes thlletees sho show ow hi hhigher gherr ra gh rates atees ooff S SCD CD w with ith a relatively ela lati tive ti vely ly cconsistent onsi on sist isten tentt es esti estimate tima ti mate te ooff 1: 11:43,000 :43 43,000 000 – 11:67,000 :6 :67 67,00 000 00 0 AY AY.3, 7,, 8 T These hese he se S SCD CD rrates attes in ates in college coll co lleg ll egee athletes represent a pooled risk of both high and low risk groups, with higher rates identified in male, black, and basketball athletes.3 The most common cause of SCD in athletes is also questioned. Hypertrophic cardiomyopathy (HCM) is identified as the leading cause of death by the US National Registry of Sudden Death in Athletes (USNRSDA).8-11 However, studies in athletes in other countries,12-16 the US military,17, 18 and in US college athletes19 have found autopsy-negative sudden unexplained death (AN-SUD) to be the most frequent finding associated with SCD. A precise understanding of the etiology of SCD is important to devise effective screening strategies.

3 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

This study examines the incidence and etiology of forensically confirmed SCD in NCAA athletes over ten years and is a continuation of five years of previously published data.3

The NCAA tracks participation data as well as the sex and ethnicity of more than 450,000 student-athletes annually. Deaths in NCAA athletes were identified during the school years (July 1 to June 30) from 2003-2004 to 2012-2013 through: 1) the NCAA Resolutions List, 2) the Parent Heart Watch database, and 3) NCAA insurance claims. The NCAA Resolutions List is compiled annually to honor NCAA student-athletes who have died of any cause. It is created by monitoring of national media and by institu institutions tuti tu tion ti onss on voluntarily providing names to the NCAA after email solicitations in November of every school year. year r. Th There Ther eree ar er aaree no no causes of death associated wi with ith tthe h NCAA Resolution he Resolutions onss list. Parent Heart on Watch Wat Wa tch (PHW) is a national natio iona ona nall no non nonprofit npro rofi ro fitt organization fi org gani nizaation ni n ddedicated edi diica cate ateed to t tthe he pprevention reeve v ntio on an and d aw awar awareness aren ar nes esss ooff sudden udd dden e cardi cardiac diaac aarrest di rrrest (S (SCA)) in n tthe hee yyoung. ou ung ng. PH PHW W ma maintains ainttaiins an oongoing ngo oing n ddatabase atab basse from om sy systematic ystemaatiic search ear arch ch h ooff media medi me diaa re di reports. repo port rts ts. T The he ddatabase he attabas atab basee wa wass queried queeried qu riied d ffor or S SCA/SCD CA/S CA /SCD /S CD among amo mong ng aathletes thle th lete tess 17 tto o 24 yea years ears rs of age, and each case reviewed to determine if the athlete was a member of an NCAA team. All NCAA athletes are covered by the NCAA Catastrophic Injury Insurance Plan which provides a death benefit of $25,000 for athletes who die during a competition, practice or conditioning activity organized or supervised by the institution. Claims related to SCA/SCD during the study period were retrieved. The data sources were combined into a single data set. Missing information regarding deaths was acquired through Internet searches and media reports, or emails and telephone calls to sports information directors, head or team athletic trainers, next-of-kin, coroners, medical

4 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

examiners and physicians involved in the case. SCD was defined as a sudden unexpected death due to cardiac cause, or a sudden death in a structurally normal heart with no other explanation for death and a history consistent with cardiac-related death that occurred within 1 hour of symptom onset or an unwitnessed death occurring within 24 hours of the person having been alive. Unwitnessed deaths were not included as cardiac unless additional information such as autopsy, negative toxicology screen or other information was available that could verify the death was cardiac in nature. Deaths were categorized broadly as accident, homicide, suicide, drug/alcohol overdose, or medical. If a drug overdose appeared to be intentional it was included as a suicide; if it was unknown or accidental the death was included in the drug/alcohol overdose categ category. gor ory y. T The he medical causes were further broken down into cardiac, cancer, heat stroke, sickle cell trait, sportrelated elate ted te d he head ad iinjury, nju ury, meningitis, and other. If the ca ury cause cau use of death could nnot ot be reasonably ddetermined, eteermined, it i w was a rec as recorded ecorrde ec ded d as ““unknown.” unkn un know kn own.”” Activi Activity A c ity y att ti time me of of death deat de ath at h wa was listed listted aass “e “exertional”, “exe xeertio ona nal” l”,, l” “rest “r rest “, “slee “sleep”, eeep” p , or “un “unknown”. nknow wn” n”.. De Demographic emo m graaphi aphi hic dataa in in NCAA NC A ath athletes t lettess w th were erre obtained obt btai a ned d ffrom rom m the NCAA NC AA SSports ports t SSponsorship ponsorshi hip and hi dP Participation arti ticiipati tion R Rates attes R Report eportt20 aand nd d tthe he NC he NCAA AA Student-Athlete Stud dentt-Ath Ath thllette Ethnicity Report.21 Definitions for pathological determination of cause of death were agreed upon using previously accepted definitions.22-26 (

). When more than one pathologic abnormality was

present, the pathology most likely related to the athlete’s death was considered primary. Autopsy reports were reviewed independently by a panel of experts consisting of 4 sports medicine physicians, a cardiovascular pathologist, a cardiomyopathy specialist, an adult and pediatric electrophysiologist, and a channelopathy/genetic specialist all with expertise in SCD in athletes. Differences of opinion were adjudicated through panel discussion. This study was approved by

5 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

the Division of Human Subjects, University of Washington.

Data were analyzed for overall death rate and etiology, as well as death rate according to sex, ethnicity, sport, and NCAA division. Incidence rates and 95% confidence intervals (CIs) were reported as incidence of death/AY. Incidence rates were also calculated for risk over 4 years representing the risk of an athlete death over a typical 4-year athletic career by multiplying the number of annual cases by 4 and using the same denominator. The relative risk of SCD and specific disease etiology was estimated with an incidence rate ratio (IRR). A priori analysis of the relative risk between white athletes vs. black athletes, male athletes vs. female athletes, risk between divisions, males vs. female basketball athletes and basketball athletes com compared ompa om pare pa red re d to oother ther th sports ports was performed based on previous work suggesting a higher rate of SCD in those groups. For ca cause caus usee of ddeath us eaath comparison significant results resultts were were presented. A cap capture-recapture ptu ture-recapture analysis was w ass performed to eestimate sttim imat atee th at thee number numb nu mberr ooff deaths mb deatths tha de that haat may may have hav ha ve bbeen eeen mi miss missed, sed,, al allow all low fo low fforr comparison co omp mparison n ooff th the he cap capture ptu ure ra rate ate bbetween etwe w en we n ddivisions iviisio is ons an and nd es est estimate tim matte po potential oten enti en t all iintra-divisional ntrra-d divisi sio si on bbias. onal ias. A All ll p-values p-va valu lues es wer were eree tw ttwo wo o side sided si ided d an and d sign significance si ignif ific if ican ance ce sset ett aatt p = 50% expected mean based on gender, age, and body size for weight (using the Mayo nomograms) without myocyte disarray o LV wall < 10 mm o Left ventricular chamber diameter > 3.0 cm (note: agonal dilatation should be excluded by examining for cell separation and other post-mortem artifact histologically) If absolute chamber diameter not measured, then comments about gross chamber dilation (without agonal dilatation from autolysis) o Histologically, myocyte hypertrophy with variable interstitial fibrosis (usually pericellular-type) Autopsy Negative-Sudden Unexplained Death Normal heart pathologica pathologically all llyy No obvious explanation ffor or ddeath eaathh Presumed arrhythmia Myocarditis Related Active lymphocytic myocarditis o Inflamma Inflammatory mato ma tory infiltrates of the to myocardium myocardi my ium with associated myocyte iinjury/necrosis inju n ury ry/n /nnec ecro rosis Borderline Bor Bo rdeerline nee m myocarditis yocaardditiss o IInflammatory nfflammaatoory inf infiltrates filtratees ooff th the he myocardium myoc my occar a dium mw without i ho it hout aassociated sssociaatedd myocyte my yocytte iinjury/necrosis. nju jury/nec ecro ec rosi ro sis. Healed Heal He aled al ed m myocarditis yoca yo card ca rdit rd itis it is Coronary A C Artery t Abnormalities Ab liti Coronary artery anomalies Myocardial bridging Tunneled coronary arteries Coronary artery dissections SCD due to Coronary Artery Disease Atherosclerotic coronary arteries > 70% lumen occlusion More likely than not that this was primary cause of death Commotio Cordis SCD after blunt trauma to the chest No other cardiac pathology

Hypertrophic Cardiomyopathy Heart weight > = 50% of expected mean based on gender, age, and body size for weight (using the Mayo nomograms) plus at least one of the following: o Histologic myocyte disarray, o Septal mitral valve contact lesion (implying systolic anterior motion of the anterior mitral valve leaflet), o Asymmetric LV hypertrophy, particularly ventricular septal – left ventricular free wall ratio 1.3 Significant (>75% of the area of a section) myocyte disarray in a basal or mid-ventricular section but not meeting weight criteria. Arrythmogenic Cardiomyopathy Gross fibrofatty replacement of either ventricular free wall (excluding anterior RV in older individuals The fatty change should appear “infiltrative” with a perpendicular pattern with respect to the epicardial surface Variable degrees of fibrosis, vacuolization, and/or lymphocytic myocarditis Idiopathic diopa path pa thic th ic L LVH/ VH/ Po VH Possible ossib i le Cardiomyopathy He weig Heart weight igh ig ht > = 50% of the expected mean based b sed on gen ba gender, e de derr, age age, gee, and an nd bo body y ssize izee fo iz forr we w weight i htt ig (using the May Mayo yo nnomograms) omo ogrrams)) Heart H He art weig weight ght h < = 50% %o off the expe ex expected xp cted m mean ean n base ba s d on se n ssex, ex, ag age,, and d body bod o y si size ize z ffor or w weight eigh ght h based ((using (u sing g Mayo Mayo nomo nomograms), ogr grams), ) but wi with: ith th:: o Fe Features Feat atur at ures ur es suggestive sug ugge gest ge stiv st ivee (but iv (but not not d diagnostic) iagn ia gnos gn osti os tic) ti c) ooff CM, iincluding: CM l di LV wall ll > 16 mm, interstitial fibrosis (non-replacement type), significant histologic myocyte hypertrophy. o No specific features of CM Cardiomyopathy NOS Heart weight does not meet weight criteria There are histologic changes such as hypertrophy or fibrosis No/ minimal myocyte disarray not meeting criteria for HCM Does not meet criteria for DCM No pathologic features suggestive of HCM

22 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

Breakdown of accidental death type.

automobile drowning fall motorcycle pedestrian bus head injury plane accidental overdose skateboarding fire bike boating horse snow now mobile electrocution choking jet et sk ski ki logging ogg ggiing otheer other total otaal

158 23 18 17 6 5 4 4 3 3 2 2 2 2 2 1 1 1 1 1 256

61.72% 8.98% 7.03% 6.64% 2.34% 1.95% 1.56% 1.56% 1.17% 1.17% 0.78% 0.78% 0.78% 0.78% 0.78% 0.39% 0.39% 0.39% 0.39% 0.39% 0.39 39% 39 % 100.00 100.00% 00% 00 %

* Total Tota To taal numb number ber of NCAA NC athlete-years ath hlete-y year year arss is 44,242,519 ,24 42,5 ,519 ,5 9

23 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

1 in 26,851 1 in 184,457 1 in 235,696 1 in 249,560 1 in 707,086 1 in 848,503 1 in 1,060,629 1 in 1,060,629 1 in 1,414,173 1 in 1,414,173 1 in 2,121,256 1 in 2,121,256 1 in 2,121,256 1 in 2,1 2,121,256 ,121 ,1 2 ,2 21 256 1 in 22,121,256 , 21 ,1 21,2 ,2 256 1 in 4,242,519 4,2 242,519 1 in 4,242,519 1 in 4,242,519 1 in 4,242,519 1 in 44,242,519 ,242 ,2 4 ,5 42 ,519 9

DOI: 10.1161/CIRCULATIONAHA.115.015431

Incidence of sudden cardiac death in NCAA athletes. Athlete-Years 4,242,519 2,418,563 1.823,899

SCD 79 64 15

Incidence per Athlete-Year 1 in 53,703 1 in 37,790 1 in 121,593

IRR 3.22 1.00

95% CI 1.9 – 5.5 Reference

p-value >0.0001*

Division Division 1 Division 2 Division 3

1,663,441 930,434 1,648,128

38 22 19

1 in 43,775 1 in 42,292 1 in 86,744

1.98 2.05 1.00

1.1 - 3.6 1.1 - 4.0 Reference

0.0131* 0.0231*

Race

3,075,942 644,715 168,763 353,042

45 30 3 1

1 in 68,354 1 in 21,491 1 in 56,254 1 in 353,042

1.00 3.18 1.22 0.19

Reference 1.9 - 5.2 0.2 - 3.8 0.005 - 1.1

Characteristic Overall Sex Male Female

White Black Hispanic Other

24 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

>0.0001* 0.6974 0.049 0.0491*

DOI: 10.1161/CIRCULATIONAHA.115.015431

Incidence of sudden cardiac death in male basketball athletes

Division I male basketball Division II male basketball Division on III male basketball asketball Overall ll male basketball ball

7

30,660

1 in 4,380

1 in 1,095

3

15,689

1 in 5,230

1 in 1,307

10

51,995

1 in 5,200

1 in 1,300

3

24,723

1 in 8,241

1 in 2,060

1

18,016

1 in 18,016

1 in 4,504

4

47,530

1 in 15,843

1 in 3,961

4

19,623

1 in 4,906

1 in 1,227

1

46,368

1 in 46,368

1 in 11,592

5

71,332 71,3 332

1 in in 14 14,266 14,2 ,266 ,2 66

1 in 3,567

14

74,866

1 in 5,348

1 in 1,337

5

79,972

1 in 15,994

1 in 3,999

19

170,590 90

1 in in 8,978 8,97 9788

1 in 2,245

25 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

DOI: 10.1161/CIRCULATIONAHA.115.015431

Incidence of sudden cardiac death in sports .

Men’s basketball Men’s soccer Men’s Football Men’s Swimming Men’s Cross-country Men’s Lacrosse Women’s Cross-country Women’s Volleyball Men’s Baseball NCAA Athletes Women’s Swimming Women’s basketball Men’s track

19 9 18 2 3 2 3 3 6 79 2 2 2

170,590 213,205 647,125 85,568 128,570 91,699 141,268 147,653 300,137 4,242,519 115,221 154,121 241,041

1 in 8,978 1 in 23,689 1 in 35,951 1 in 42,784 1 in 42,857 1 in 45,850 1 in 47,089 1 in 49,217 1 in 50,023 1 in 53,703 1 in 57,611 1 in 77,061 1 in 120,521

1 in 2,245 1 in 5,922 1 in 8,988 1 in 10,696 1 in 10,714 1 in 11,463 1 in 11,772 1 in 12,304 1 in 12,505 1 in 13,426 1 in 14,402 1 in 19,265, 19, 9,26 265, 26 5, 1 iin n 30 30,1 30,130 130

*Sports Sports with one death: men’s crew, women’s golf, women’s softball, women’s tennis, men’s tennis, women’s track, rack, wrestling, women’s lacrosse Other Oth her ssports port po rtss ha rt hhad d no no iidentified dentified SCDs

Source Sou urc r e off inf information forrmattion tion for ddetermination etterrmin nattion off ca cause aus use of dea death. ath h.

A Autopsy confirmed fi d Coroner/medical examiner/ medical team Medical/legal report of autopsy Personal/Family history and history consistent with SCD Exertional collapse without other explanation Discussion with next of kin Death certificate

26 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

58 8 4 3 3 1 2

DOI: 10.1161/CIRCULATIONAHA.115.015431

Causes of Death in NCAA Athletes 2003 – 2013.

A. Etiologies of sudden cardiac death in athletes. B. Etiology and activity at time of death*. *One person figure equals one death; female figures follow male figures unless no male deaths were present.

27 Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

Figure 1

Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

Figure 2A

Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

Figure 2B

Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015

Incidence, Etiology, and Comparative Frequency of Sudden Cardiac Death in NCAA Athletes: A Decade in Review Kimberly G. Harmon, Irfan M. Asif, Joseph J. Maleszewski, David S. Owens, Jordan M. Prutkin, Jack C. Salerno, Monica L. Zigman, Rachel Ellenbogen, Ashwin Rao, Michael J. Ackerman and Jonathan A. Drezner Circulation. published online May 14, 2015;

Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 2015 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7322. Online ISSN: 1524-4539

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://circ.ahajournals.org/content/early/2015/05/14/CIRCULATIONAHA.115.015431

Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Circulation can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: http://www.lww.com/reprints Subscriptions: Information about subscribing to Circulation is online at: http://circ.ahajournals.org//subscriptions/

Downloaded from http://circ.ahajournals.org/ by guest on May 16, 2015