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Asthma deaths during sports
Asthma deaths during sports: Report of a 7-year experience Asthma, rhinitis, other respiratory diseases
Jack M. Becker MD,a James Rogers, BS, AT,C,b Gregory Rossini, MD,c Haresh Mirchandani, MD,d and Gilbert E. D’Alonzo, Jr, DOb Philadelphia and Lancaster, Pa Background: Asthma mortality and the mortality of athletes during sports have been described separately in detail in the medical literature. However, asthma has not been reported as a cause of death in competitive athletes. Objective: The object of this study was to raise the awareness of physicians, coaches, trainers, and parents that children and adults can have fatal asthma exacerbations during and immediately after participating in sports. Methods: The Temple Sports Asthma Research Center identified athletes from 1993 until 2000 who died during or after sporting activity by using the nationwide Burrell’s Information Service. Once a possible asthma-related sports death was identified, the autopsy report was requested from the coroner or medical examiner, and an attempt was made to contact the family. Contact with the family was limited to information about the death, medical history, sports involvement, and any medication usage by the person who had died. Secondary sources, including news reports, were used to confirm whether the subject died of asthma during or immediately after a sporting activity. Results: Two hundred sixty-three possible cases were identified. Sixty-one deaths met the criteria for study inclusion. White deaths outnumbered black deaths by 2 to 1. Deaths among male subjects predominated. Most subjects were younger than the age of 20 years, with the most prevalent age group being between 10 to 14 years old. Fifty-one percent (18 of 35) of the competitive athletes had their fatal event while participating in organized sport, 14 in a practice situation and 4 deaths during a game or meet setting. Basketball and track were the 2 most frequent activities performed at the time of the fatal event. Conclusion: The subjects who had fatal asthma exacerbations were usually white male subjects between the ages of 10 and 20 years. Mild intermittent or persistent asthma by history was commonly identified. Sudden fatal asthma exacerbations occur in both competitive and recreational athletes and can be precipitated by sporting activity. (J Allergy Clin Immunol 2004;113:264-7.)
From athe Section of Allergy, Asthma and Immunology, Department of Pediatrics, St. Christopher’s Hospital for Children, Drexel University College of Medicine, Philadelphia; bthe Division of Pulmonary and Critical Care Medicine, Department of Medicine, and the Department of Sports Medicine, Temple University School of Medicine, Philadelphia; cPulmonary Associates of Lancaster, LTD; and dChief Medical Examiner’s office, Philadelphia. Supported by an unrestricted educational grant from GlaxoSmithKline Inc, Triangle Park, NC. Received for publication August 19, 2003; revised October 16, 2003; accepted for publication October 24, 2003. Reprint requests: Jack M. Becker, MD, Section of Allergy, Department of Pediatrics, Drexel University College of Medicine, St. Christopher’s Hospital for Children, Front Street at Erie Avenue, Philadelphia, PA 19134. 0091-6749/$30.00 © 2004 American Academy of Allergy, Asthma and Immunology doi:10.1016/j.jaci.2003.10.052
264
Key words: Asthma, competitive athlete, recreational athlete, asthma mortality, sudden death, cardiac death, mild intermittent asthma
Investigators have separately reported asthma mortality and the mortality of athletes during sports, but there have been no studies published to date that suggest that the competitive athlete is at risk for death from asthma while playing sports.1-7 It is considered uncommon that a professional athlete has asthma, but when one is identified, he or she is held out as a role model for children. The professional athlete is used to promote optimal asthma care. Competitive athletes do have asthma. In the 1996 Summer Olympic games, 50% of cyclists, 30% of swimmers, 25% of rowers, and 18% of track and field athletes reported that they have asthma.8 Up to 10% of high school athletes have undiagnosed asthma.9,10 However, asthma is generally not considered as a possible etiology for morbidity or death during sports.6,11 In this study we examined the deaths of participants in athletic activities to determine whether asthma can be a cause of death in the competitive athlete.
METHODS The Temple Sports Asthma Research Program initially identified subjects who died during or immediately after a sporting or athletic event between July 1993 and December 2000, regardless of cause, by using the Burrell’s Clipping Service. This news release service reviews newspapers from throughout the country by using specified search criteria and forwards the articles on request. We used the search terms asthma, sports, and death related to sports or asthma. This service reviews 1871 general and special interest daily newspapers as well as 8335 non-daily newspapers. In addition, we received reports of other sport-related deaths directly from physicians who were aware of our interest. Once a possible sports-related asthma death was identified, a request for autopsy records was made to the local coroner or medical examiner. An attempt was made to contact the family as well. One of the investigators would call the family and request information about the death, medical history, sports involvement, and any medication usage by the person who had died. We did not attempt to confirm medications prescribed or compliance; most families were unwilling or unable to provide such information. Secondary sources, including information published in the press, were used to determine whether the subject died of asthma during or immediately after an athletic or sporting activity. Subjects were considered eligible for further analysis only if the following criteria were met. The subject had to be participating in physical activity at the time of development of symptoms. A review of the newspaper report or family information had to indicate that the subject appeared well immediately before the event. The coroner or medical examiner had to have concluded that the subject died of asthma; asthma had to have been listed as the only cause of death on the death certificate. Subjects were excluded if a complete histo-
Becker et al 265
J ALLERGY CLIN IMMUNOL VOLUME 113, NUMBER 2
RESULTS We identified 263 potential asthma-related athletic deaths between July 1993 and December 2000. To ensure that only subjects who died of asthma during sports events were included, 202 (77%) were excluded for 1 or more of the following reasons: (1) death was not attributed to asthma at the time of autopsy; (2) the autopsy listed the cause of death as asthma, but concurrent cardiac or other disease was noted; (3) the subject’s history or autopsy had signs, symptoms, or findings that could be classified as consistent with anaphylaxis; (4) the subject was not participating in a sporting activity immediately before the fatal event; and (5) information about the subject’s autopsy or the activities of the subject before the subject’s death was unattainable or not verifiable. We were able to obtain useful information from a family member in 10 of 61 (16%) of the cases included in the study. Most families were either unwilling or unable to provide us with additional information. Sixty-one deaths were identified that met these criteria of an asthma death occurring in close association with a sporting event or physical activity. Eighty-one percent (49 of 61) of the subjects were younger than 21 years of age; approximately half (32) of all the subjects were between the ages of 13 and 17 years. Sixty-nine percent of the subjects were male, and they outnumbered female subjects 42 versus 19. The white to black subject ratio was almost 2:1, 39 white subjects versus 20 black subjects. Ninety-one percent (55 of 61) of the subjects had a known history of asthma (Table I). Competitive athletes (defined as those who played for either a professional team or one directly related to an educational institution) had a slightly higher incidence of sudden death from asthma, 57% (35 of 61), than subjects who competed recreationally, 43% (26 of 61). Fifty-one percent (18 of 35) of the competitive athletes had their fatal event while participating in their organized sport, 14 of the 18 in a practice situation and 4 deaths during a game or meet setting. Basketball and track were the 2 most frequent sports at the time of the fatal event. This is similar to the recreational athletes, who died most frequently while playing basketball (Table II). Ninety percent of the subjects had a history of asthma as obtained from news reports or family members. In an effort to assess asthma severity, we relied on reports from either the medical examiner or a family member. Although suboptimal, this approach was the only one available because of generalized family reticence. We inferred the overall group’s asthma severity by the number of subjects taking either inhaled steroids or sodium cromoglycate. Only 3 subjects were using this type of medication; 2 were
TABLE I. Demographics of the study subjects (N = 61)
Age at time of death (y) Less than 9 10 to 14 15 to 20 21 to 30 Older than 31 Gender Male Female Race Black White Other Subjects with medical history of asthma Asthma history No known asthma history
n
Percent
4 26 19 10 2
7 43 31 16 3
42 19
69 31
20 39 2
33 64 3
55 6
91 9
TABLE II. Event characteristics Event characteristic
Type of sport participation Organized sport Recreational sport Season of fatal event Spring Summer Fall Winter Sport at time of fatal event Basketball Track/running Gym class Football Recreational play Baseball Soccer Swimming Cheerleading Other
n
Percent
35 26
57 43
13 19 24 5
22 31 39 8
13 7 6 5 5 3 3 2 2 16
21 12 10 8 8 5 5 3 3 26
TABLE III. Reported use of long-term control medications Reported use
Yes No Unknown
n
Percent
3 47 11
5 77 18
using cromolyn and one an inhaled corticosteroid; none were taking a leukotriene modifier. Two of 3 athletes receiving medication were black (Table III).
DISCUSSION There is little information concerning asthma death in association with sport, especially in the context of the competitive athlete. This paucity of data partially stems from a societal belief that athletes rarely become afflicted with a disease. This study highlights a previously unrec-
Asthma, rhinitis, other respiratory diseases
ry or autopsy was unavailable or if severe asthma symptoms began more than 1 hour after the cessation of athletic activity. Subjects were also excluded if the autopsy could not exclude exerciseinduced anaphylaxis, cardiac disease, trauma, or any other potential cause that might have contributed to the subject’s death. The data were then stratified according to race, sex, age, severity of disease, timing of the death, and type of activity.
266 Becker et al
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ognized group of subjects who die of asthma, the competitive and noncompetitive athlete. Several reviews of asthma deaths, as well as a review of death in the competitive athlete, have not considered the possibility that athletic activity can trigger a fatal asthmatic attack.6,12,13 This current study indicates that there might be a risk of such death. The Morbidity Mortality Weekly Report reported the 1993 death rate for asthma as 3.7 per million.4 Cantu et al11 estimated that there are 22 million competitive high school and college athletes. With even more strict criteria and by using only those cases in which we could review the actual autopsy records and not rely on a death certificate alone, we documented 5 deaths per year in the competitive athlete for an approximate death rate of 0.23 deaths per population of million competitive athletes. This is probably an underestimation because of our study entry criteria and screening mechanism.4 The racial distribution in our study differed from that of other studies of asthma mortality. In our study those athletes with asthma who died during sporting activities were primarily white, at nearly a 2:1 ratio to blacks. This is in contrast to other studies that show a much greater asthma death rate in the black population; in those studies roughly 80% of all asthma deaths occurred among blacks. It is unknown whether this difference is due to whites having a greater rate of activity-induced asthma deaths, or whether they are reported more often and therefore are found to be higher in this study. The gender ratio also differed slightly from previously reported studies on asthma mortality. Male subjects died at a 2:1 ratio to female subjects in our study compared to the generally reported ratio of 1.5 to 1.4,14 The severity of disease might also have differed in our subjects compared to that reported with mortality from asthma in general. Although it is possible that a subject with mild asthma might die suddenly of asthma, generally asthmatic deaths occur in the severely afflicted population, in those who are poorly compliant, and in those who have had recent hospitalizations as a result of severe attacks.12,13,15-17 None of the athletes who died could have been classified as severe from the information that was available, but an underestimation of their disease severity is certainly possible, and this lack of knowledge of the exact asthma severity of the subjects is a limitation of the study. The times of the year that the deaths were reported correlate more closely with those seen with sports injuries and fatalities and do not differ substantially from those seen in asthma in a comparable age group. Sports deaths generally occur in late summer through fall, corresponding with football and basketball seasons, whereas asthma deaths for comparable age group are usually seen during the summer months.18 Our study showed that the peak time for asthma deaths is fall > summer > spring > winter. There are several unavoidable limitations to this study. It is impossible, even with the history and autopsy information, to be assured that the cause of death in every subject was asthma. A subject could have had exerciseinduced anaphylaxis or an undetectable cardiac condition. However, in exercise-induced anaphylaxis the subject usu-
J ALLERGY CLIN IMMUNOL FEBRUARY 2004
ally has generalized pruritus, urticaria, flushing, and angioedema.19 None of these signs or symptoms was reported in any of our subjects. It is also possible that a cardiac death was classified incorrectly as an asthma death. However, autopsied cardiac deaths reveal structural cardiac abnormality in more than 90% of the subjects, and the subject is usually reported to have collapsed suddenly at the time of the fatal event.20 That was not the case in any of the deaths included in this study. All of our subjects had documented respiratory symptoms immediately before their terminal event. We do not attempt to deduce a physiologic pathway for these subjects’ deaths. There have been several theories proposed for the cause of this type of fatal asthma attack. These include sudden severe asphyxia as well as a reduced chemosensitivity to hypoxia and blunted perception of dyspnea by the patient.21-23 Exercise has been shown to trigger a more severe sudden exacerbation.24 In conclusion, this study indicates that sudden fatal asthma can occur in competitive and recreational athletes during sporting activities. These subjects are usually white male subjects between the ages of 10 and 20 years. Female subjects are also affected, albeit at a lower rate. Many of these subjects had mild asthma. Therefore, extra care is needed to ensure that the athlete with asthma is receiving proper care and therapy. This study underscores the need to make asthma a reportable disease as a cause of death. This would allow better understanding of the epidemiology and appropriate measures for prevention. It is certainly plausible that more aggressive management of these subjects with asthma might have altered the outcome. This work also suggests that all individuals involved in organized sports should be cognizant of the risk of a severe asthmatic attack. Coaches, trainers, and team physicians should be specifically trained. Healthcare providers who care for competitive athletes who have asthma should be apprised of the risk of a sports-induced asthma death. Healthcare providers must make sure that their patients with asthma are properly medicated and stress the need for rescue medication to be immediately available during any sports activity. It is critical, however, that this work not be misinterpreted to bar athletes with asthma from exercising or competing. The aim of this work establishes that asthma can be a cause of death during exercise in the athlete. The positive benefits to an active lifestyle have been clearly documented in asthma and other chronic diseases25-31 and cannot be negated by the risks outlined here. This work is in memory of Theodore C. Quedenfeld, MEd, whose passion and dedication have improved the health and care of children and athletes nationwide.
REFERENCES 1. Strunk RC, Nicklas RA, Milgrom H, Ikle D. Fatal and near-fatal asthma questionnaire: prelude to a national registry. J Allergy Clin Immunol 1999;104:763-8. 2. McFadden ER, Warren EL. Observations on asthma mortality. Ann Intern Med 1997;127:142-7. 3. Campbell MJ, Cogman GR, Holgate ST, Johnston SL. Age specific
4.
5. 6.
7. 8.
9.
10. 11.
12. 13. 14. 15. 16. 17. 18.
trends in asthma mortality in England and Wales, 1983-95: results of an observational study. BMJ 1997;314:1439-41. Center for Disease Control and Prevention. Asthma mortality and hospitalization among children and young adults: United States, 1980-1993. MMWR Morb Mortal Wkly Rep 1996;45:350-3. Sly R. Changing asthma mortality. Ann Allergy 1994;73:259-68. Maron BJ, Shirani J, Poliac LC, Mathenge R, Roberts WC, Mueller FO. Sudden death in young competitive athletes: clinical, demographic and pathological profiles. JAMA 1996;276:199-204. Maron BJ. Sudden death in young athletes: lessons from the Hank Gathers affair. N Engl J Med 1993;329:55-7. Weiler JM, Layon T, Hunt M. Asthma in United States Olympic athletes who participated in the 1996 Summer Games. J Allergy Clin Immunol 1998;102:722-6. Kukufka DS, Lang DM, Porter S, Rogers J, Ciccolella D, Polanski M, et al. Exercise-induced bronchospasm in high school athletes via a free running test: incidence and epidemiology. Chest 1998;116:1613-22. Rupp NT, Brudno DS, Guill MF. The value of screening for risk of exercise-induced asthma in high school athletes. Ann Allergy 1993;70:339-42. Cantu RC, Mueller FO. Fatalities and catastrophic injuries in high school and college sports, 1982-1997. The Physician and Sports Medicine 1999;27:35-48. Robertson C, Rubinfeld A, Bowes G. Pediatric asthma deaths in Victoria: the mild are at risk. Pediatr Pulmonol 1992;13:95-100. Kunitoh H, Yahikozawa H, Kakuta T, Ono K, Hamabe Y, Kuroki H, et al. Fatal and near fatal asthma. Ann Allergy 1992;69:111-5. Thomas SD, Whitman S. Assessing the burden of asthma and asthma care. Chest 1999;116:135-41. Benatar SR. Fatal asthma. N Engl J Med 1986;318:423-9. McFadden ER Jr, Warren EL. Observations on asthma mortality. Ann Intern Med 1997;127:142-7. Strunk RC. The fatality-prone asthmatic child and adolescent. Immunol Allergy Clin North Am 1998;18:85-97. Weiss KB. Seasonal trends in US asthma hospitalizations and mortality. JAMA 1990;263:2323-8.
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19. Shadick NA, Liang MH, Partridge AJ, Bingham C, Wright E, Fossel AH, et al. The natural history of exercise-induced anaphylaxis: survey results from a 10-year follow-up study. J Allergy Clin Immunol 1999;104:123-7. 20. Maron BJ, Epstein SE, Roberts WC. Causes of sudden death in competitive athletes. J Am Coll Cardiol 1989;7:204-14. 21. Molfino NA, Nannini LJ, Martelli AN, Slutsky AS. Respiratory arrest in near-fatal asthma. N Engl J Med 1991;324:285-8. 22. Wasserfallen JB, Schaller MD, Feihl F, Perret CH. Sudden asphyxic asthma: a distinct entity? Am Rev Respir Dis 1990;142:108-11. 23. Kikuchi Y, Okabe S, Tamura G, Hida W, Homma M, Shirato K, et al. Chemosensitivity and perception of dyspnea with a history of near-fatal asthma. N Engl J Med 1994;330:1329-34. 24. Barr RG, Woodruff PG, Clark S, Camargo CA Jr. Sudden-onset asthma exacerbations: clinical features, response to therapy, and 2-week followup—Multicenter Airway Research Collaboration (MARC) investigators. Eur Respir J 2000;15:266–73. 25. Paluska S, Schwenk T. Physical activity and mental health: current concepts. Sports Med 2000;29:167-80. 26. O’Grady M, Fletcher J, Ortiz S. Therapeutic and physical fitness exercise prescription for older adults with joint disease: an evidence-based approach. Rheum Dis Clin North Am 2000;26:617-46. 27. Bourjeily G, Rochester CL. Exercise training in chronic obstructive pulmonary disease. Clin Chest Med 2000;21:763-81. 28. Ades PA, Coello CE. Effects of exercise and cardiac rehabilitation on cardiovascular outcomes. Med Clin North Am 2000;84:251-65, x-xi. 29. Sothern M. Exercise as a modality in the treatment of childhood obesity. Pediatr Clin North Am 2001;48:995-1015. 30. Neder JA, Nery LE, Silva AC, Cabral AL, Fernandes AL. Short-term effects of aerobic training in the clinical management of moderate to severe asthma in children. Thorax 1999;54:202-6. 31. Counil FP, Varray A, Matecki S, Beurey A, Marchal P, Voisin M, et al. Training of aerobic and anaerobic fitness in children with asthma. J Pediatr 2003;142:179-84.
Asthma, rhinitis, other respiratory diseases
J ALLERGY CLIN IMMUNOL VOLUME 113, NUMBER 2
Jack M. Becker MD,a James Rogers, BS, AT,C,b Gregory Rossini, MD,c Haresh Mirchandani, MD,d and Gilbert E. D’Alonzo, Jr, DOb Philadelphia and Lancaster, Pa Background: Asthma mortality and the mortality of athletes during sports have been described separately in detail in the medical literature. However, asthma has not been reported as a cause of death in competitive athletes. Objective: The object of this study was to raise the awareness of physicians, coaches, trainers, and parents that children and adults can have fatal asthma exacerbations during and immediately after participating in sports. Methods: The Temple Sports Asthma Research Center identified athletes from 1993 until 2000 who died during or after sporting activity by using the nationwide Burrell’s Information Service. Once a possible asthma-related sports death was identified, the autopsy report was requested from the coroner or medical examiner, and an attempt was made to contact the family. Contact with the family was limited to information about the death, medical history, sports involvement, and any medication usage by the person who had died. Secondary sources, including news reports, were used to confirm whether the subject died of asthma during or immediately after a sporting activity. Results: Two hundred sixty-three possible cases were identified. Sixty-one deaths met the criteria for study inclusion. White deaths outnumbered black deaths by 2 to 1. Deaths among male subjects predominated. Most subjects were younger than the age of 20 years, with the most prevalent age group being between 10 to 14 years old. Fifty-one percent (18 of 35) of the competitive athletes had their fatal event while participating in organized sport, 14 in a practice situation and 4 deaths during a game or meet setting. Basketball and track were the 2 most frequent activities performed at the time of the fatal event. Conclusion: The subjects who had fatal asthma exacerbations were usually white male subjects between the ages of 10 and 20 years. Mild intermittent or persistent asthma by history was commonly identified. Sudden fatal asthma exacerbations occur in both competitive and recreational athletes and can be precipitated by sporting activity. (J Allergy Clin Immunol 2004;113:264-7.)
From athe Section of Allergy, Asthma and Immunology, Department of Pediatrics, St. Christopher’s Hospital for Children, Drexel University College of Medicine, Philadelphia; bthe Division of Pulmonary and Critical Care Medicine, Department of Medicine, and the Department of Sports Medicine, Temple University School of Medicine, Philadelphia; cPulmonary Associates of Lancaster, LTD; and dChief Medical Examiner’s office, Philadelphia. Supported by an unrestricted educational grant from GlaxoSmithKline Inc, Triangle Park, NC. Received for publication August 19, 2003; revised October 16, 2003; accepted for publication October 24, 2003. Reprint requests: Jack M. Becker, MD, Section of Allergy, Department of Pediatrics, Drexel University College of Medicine, St. Christopher’s Hospital for Children, Front Street at Erie Avenue, Philadelphia, PA 19134. 0091-6749/$30.00 © 2004 American Academy of Allergy, Asthma and Immunology doi:10.1016/j.jaci.2003.10.052
264
Key words: Asthma, competitive athlete, recreational athlete, asthma mortality, sudden death, cardiac death, mild intermittent asthma
Investigators have separately reported asthma mortality and the mortality of athletes during sports, but there have been no studies published to date that suggest that the competitive athlete is at risk for death from asthma while playing sports.1-7 It is considered uncommon that a professional athlete has asthma, but when one is identified, he or she is held out as a role model for children. The professional athlete is used to promote optimal asthma care. Competitive athletes do have asthma. In the 1996 Summer Olympic games, 50% of cyclists, 30% of swimmers, 25% of rowers, and 18% of track and field athletes reported that they have asthma.8 Up to 10% of high school athletes have undiagnosed asthma.9,10 However, asthma is generally not considered as a possible etiology for morbidity or death during sports.6,11 In this study we examined the deaths of participants in athletic activities to determine whether asthma can be a cause of death in the competitive athlete.
METHODS The Temple Sports Asthma Research Program initially identified subjects who died during or immediately after a sporting or athletic event between July 1993 and December 2000, regardless of cause, by using the Burrell’s Clipping Service. This news release service reviews newspapers from throughout the country by using specified search criteria and forwards the articles on request. We used the search terms asthma, sports, and death related to sports or asthma. This service reviews 1871 general and special interest daily newspapers as well as 8335 non-daily newspapers. In addition, we received reports of other sport-related deaths directly from physicians who were aware of our interest. Once a possible sports-related asthma death was identified, a request for autopsy records was made to the local coroner or medical examiner. An attempt was made to contact the family as well. One of the investigators would call the family and request information about the death, medical history, sports involvement, and any medication usage by the person who had died. We did not attempt to confirm medications prescribed or compliance; most families were unwilling or unable to provide such information. Secondary sources, including information published in the press, were used to determine whether the subject died of asthma during or immediately after an athletic or sporting activity. Subjects were considered eligible for further analysis only if the following criteria were met. The subject had to be participating in physical activity at the time of development of symptoms. A review of the newspaper report or family information had to indicate that the subject appeared well immediately before the event. The coroner or medical examiner had to have concluded that the subject died of asthma; asthma had to have been listed as the only cause of death on the death certificate. Subjects were excluded if a complete histo-
Becker et al 265
J ALLERGY CLIN IMMUNOL VOLUME 113, NUMBER 2
RESULTS We identified 263 potential asthma-related athletic deaths between July 1993 and December 2000. To ensure that only subjects who died of asthma during sports events were included, 202 (77%) were excluded for 1 or more of the following reasons: (1) death was not attributed to asthma at the time of autopsy; (2) the autopsy listed the cause of death as asthma, but concurrent cardiac or other disease was noted; (3) the subject’s history or autopsy had signs, symptoms, or findings that could be classified as consistent with anaphylaxis; (4) the subject was not participating in a sporting activity immediately before the fatal event; and (5) information about the subject’s autopsy or the activities of the subject before the subject’s death was unattainable or not verifiable. We were able to obtain useful information from a family member in 10 of 61 (16%) of the cases included in the study. Most families were either unwilling or unable to provide us with additional information. Sixty-one deaths were identified that met these criteria of an asthma death occurring in close association with a sporting event or physical activity. Eighty-one percent (49 of 61) of the subjects were younger than 21 years of age; approximately half (32) of all the subjects were between the ages of 13 and 17 years. Sixty-nine percent of the subjects were male, and they outnumbered female subjects 42 versus 19. The white to black subject ratio was almost 2:1, 39 white subjects versus 20 black subjects. Ninety-one percent (55 of 61) of the subjects had a known history of asthma (Table I). Competitive athletes (defined as those who played for either a professional team or one directly related to an educational institution) had a slightly higher incidence of sudden death from asthma, 57% (35 of 61), than subjects who competed recreationally, 43% (26 of 61). Fifty-one percent (18 of 35) of the competitive athletes had their fatal event while participating in their organized sport, 14 of the 18 in a practice situation and 4 deaths during a game or meet setting. Basketball and track were the 2 most frequent sports at the time of the fatal event. This is similar to the recreational athletes, who died most frequently while playing basketball (Table II). Ninety percent of the subjects had a history of asthma as obtained from news reports or family members. In an effort to assess asthma severity, we relied on reports from either the medical examiner or a family member. Although suboptimal, this approach was the only one available because of generalized family reticence. We inferred the overall group’s asthma severity by the number of subjects taking either inhaled steroids or sodium cromoglycate. Only 3 subjects were using this type of medication; 2 were
TABLE I. Demographics of the study subjects (N = 61)
Age at time of death (y) Less than 9 10 to 14 15 to 20 21 to 30 Older than 31 Gender Male Female Race Black White Other Subjects with medical history of asthma Asthma history No known asthma history
n
Percent
4 26 19 10 2
7 43 31 16 3
42 19
69 31
20 39 2
33 64 3
55 6
91 9
TABLE II. Event characteristics Event characteristic
Type of sport participation Organized sport Recreational sport Season of fatal event Spring Summer Fall Winter Sport at time of fatal event Basketball Track/running Gym class Football Recreational play Baseball Soccer Swimming Cheerleading Other
n
Percent
35 26
57 43
13 19 24 5
22 31 39 8
13 7 6 5 5 3 3 2 2 16
21 12 10 8 8 5 5 3 3 26
TABLE III. Reported use of long-term control medications Reported use
Yes No Unknown
n
Percent
3 47 11
5 77 18
using cromolyn and one an inhaled corticosteroid; none were taking a leukotriene modifier. Two of 3 athletes receiving medication were black (Table III).
DISCUSSION There is little information concerning asthma death in association with sport, especially in the context of the competitive athlete. This paucity of data partially stems from a societal belief that athletes rarely become afflicted with a disease. This study highlights a previously unrec-
Asthma, rhinitis, other respiratory diseases
ry or autopsy was unavailable or if severe asthma symptoms began more than 1 hour after the cessation of athletic activity. Subjects were also excluded if the autopsy could not exclude exerciseinduced anaphylaxis, cardiac disease, trauma, or any other potential cause that might have contributed to the subject’s death. The data were then stratified according to race, sex, age, severity of disease, timing of the death, and type of activity.
266 Becker et al
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ognized group of subjects who die of asthma, the competitive and noncompetitive athlete. Several reviews of asthma deaths, as well as a review of death in the competitive athlete, have not considered the possibility that athletic activity can trigger a fatal asthmatic attack.6,12,13 This current study indicates that there might be a risk of such death. The Morbidity Mortality Weekly Report reported the 1993 death rate for asthma as 3.7 per million.4 Cantu et al11 estimated that there are 22 million competitive high school and college athletes. With even more strict criteria and by using only those cases in which we could review the actual autopsy records and not rely on a death certificate alone, we documented 5 deaths per year in the competitive athlete for an approximate death rate of 0.23 deaths per population of million competitive athletes. This is probably an underestimation because of our study entry criteria and screening mechanism.4 The racial distribution in our study differed from that of other studies of asthma mortality. In our study those athletes with asthma who died during sporting activities were primarily white, at nearly a 2:1 ratio to blacks. This is in contrast to other studies that show a much greater asthma death rate in the black population; in those studies roughly 80% of all asthma deaths occurred among blacks. It is unknown whether this difference is due to whites having a greater rate of activity-induced asthma deaths, or whether they are reported more often and therefore are found to be higher in this study. The gender ratio also differed slightly from previously reported studies on asthma mortality. Male subjects died at a 2:1 ratio to female subjects in our study compared to the generally reported ratio of 1.5 to 1.4,14 The severity of disease might also have differed in our subjects compared to that reported with mortality from asthma in general. Although it is possible that a subject with mild asthma might die suddenly of asthma, generally asthmatic deaths occur in the severely afflicted population, in those who are poorly compliant, and in those who have had recent hospitalizations as a result of severe attacks.12,13,15-17 None of the athletes who died could have been classified as severe from the information that was available, but an underestimation of their disease severity is certainly possible, and this lack of knowledge of the exact asthma severity of the subjects is a limitation of the study. The times of the year that the deaths were reported correlate more closely with those seen with sports injuries and fatalities and do not differ substantially from those seen in asthma in a comparable age group. Sports deaths generally occur in late summer through fall, corresponding with football and basketball seasons, whereas asthma deaths for comparable age group are usually seen during the summer months.18 Our study showed that the peak time for asthma deaths is fall > summer > spring > winter. There are several unavoidable limitations to this study. It is impossible, even with the history and autopsy information, to be assured that the cause of death in every subject was asthma. A subject could have had exerciseinduced anaphylaxis or an undetectable cardiac condition. However, in exercise-induced anaphylaxis the subject usu-
J ALLERGY CLIN IMMUNOL FEBRUARY 2004
ally has generalized pruritus, urticaria, flushing, and angioedema.19 None of these signs or symptoms was reported in any of our subjects. It is also possible that a cardiac death was classified incorrectly as an asthma death. However, autopsied cardiac deaths reveal structural cardiac abnormality in more than 90% of the subjects, and the subject is usually reported to have collapsed suddenly at the time of the fatal event.20 That was not the case in any of the deaths included in this study. All of our subjects had documented respiratory symptoms immediately before their terminal event. We do not attempt to deduce a physiologic pathway for these subjects’ deaths. There have been several theories proposed for the cause of this type of fatal asthma attack. These include sudden severe asphyxia as well as a reduced chemosensitivity to hypoxia and blunted perception of dyspnea by the patient.21-23 Exercise has been shown to trigger a more severe sudden exacerbation.24 In conclusion, this study indicates that sudden fatal asthma can occur in competitive and recreational athletes during sporting activities. These subjects are usually white male subjects between the ages of 10 and 20 years. Female subjects are also affected, albeit at a lower rate. Many of these subjects had mild asthma. Therefore, extra care is needed to ensure that the athlete with asthma is receiving proper care and therapy. This study underscores the need to make asthma a reportable disease as a cause of death. This would allow better understanding of the epidemiology and appropriate measures for prevention. It is certainly plausible that more aggressive management of these subjects with asthma might have altered the outcome. This work also suggests that all individuals involved in organized sports should be cognizant of the risk of a severe asthmatic attack. Coaches, trainers, and team physicians should be specifically trained. Healthcare providers who care for competitive athletes who have asthma should be apprised of the risk of a sports-induced asthma death. Healthcare providers must make sure that their patients with asthma are properly medicated and stress the need for rescue medication to be immediately available during any sports activity. It is critical, however, that this work not be misinterpreted to bar athletes with asthma from exercising or competing. The aim of this work establishes that asthma can be a cause of death during exercise in the athlete. The positive benefits to an active lifestyle have been clearly documented in asthma and other chronic diseases25-31 and cannot be negated by the risks outlined here. This work is in memory of Theodore C. Quedenfeld, MEd, whose passion and dedication have improved the health and care of children and athletes nationwide.
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