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Reprinted from JAMA® The Journal of the American Medical Association

December 1, 1989, Volume 262

Copyright 1989, American Medical Association

An Outbreak of Nitrogen Dioxide—Induced Respiratory Illness Among Ice Hockey Players

Katrina Hedberg, MD; Craig W.Hedberg, MS; Conrad Iber, MD; Karen E.White, MPH; Michael T.Osterholm, PhD, MPH; David B.W.Jones; James R.Flink, MD; Kristine L.MacDonald, MD

During February 1987 an outbreak of nitrogen dioxide—induced respiratory illness occurred among players and spectators of two high school hockey games played at an indoor ice arena in Minnesota. The source of the nitrogen dioxide was the malfunctioning engine of the ice resurfacer. Case patients experienced acute onset of cough, hemoptysis, and/or dyspnea during, or within 48 hours of attending, a hockey game. One hundred sixteen cases were identified among hockey players, cheerleaders, and band members who attended the two games. Members of two hockey teams had spirometry performed at 10 days and 2 months after exposure; no significant compromise in lung function was documented. Nitrogen dioxide exposure in indoor ice arenas may be more common than currently is recognized; only three states require routine monitoring of air quality in ice arenas, and the respiratory symptoms caused by exposure to nitrogen dioxide are nonspecific and easily misdiagnosed.

(JAMA. 1989;262:3014–3017)

NITROGEN dioxide is a brownish gas produced as a by-product of combustion. Occupational exposures to nitrogen dioxide are frequent among silo fillers, arc welders, firefighters, and workers who manufacture missile fuels and explosives.1,2 The effects of nitrogen dioxide depend on the level and duration of exposure. Exposure to moderate levels (50 ppm) for brief periods may produce cough, hemoptysis, dyspnea, and chest pain.3 Exposure to high concen

   

From the Division of Field Services. Centers for Disease Control, Atlanta. Ga (Dr K.Hedberg); the Acute Disease Epidemiology Section, Minnesota Department of Health, Minneapolis (Drs K.Hedberg. Osterholm, and MacDonald and Ms White and Messrs C.W.Hedberg and Jones); the Department of Internal Medicine, Hennepin County Medical Center. Minneapolis (Dr Iber); and Pulmonary Health Associates, St Paul, Minn (Dr Flink).

Reprint requests to Acute Disease Epidemiology Section, Minnesota Department of Health, 717 Delaware St SE, Minneapolis, MN 55440 (Dr MacDonald).

trations of nitrogen dioxide (>100 ppm) can produce pulmonary edema, which can be acutely fatal or may lead to bronchiolitis obliterans.4,5 Bronchiolitis obliterans may result in chronic restrictive pulmonary disease; however, most patients recover, with few long-term sequelae. Treatment with corticosteroids may diminish the severity of disease.6,7 Exposure to low levels of nitrogen dioxide also may produce adverse pulmonary effects. Human volunteers exposed to 5 ppm of nitrogen dioxide for 15 minutes and 2.5 ppm for 2 hours demonstrated increased pulmonary airway resistance.8 Also, recent studies suggest that long-term exposure to low levels of nitrogen dioxide, in the environment or in the home, may predispose residents to respiratory infections and chronic obstructive pulmonary disease.915 The National Institute for Occupational Safety and Health recommends 1 ppm of nitrogen dioxide as a work-site standard.1

During February 1987, we investigated an outbreak of acute respiratory illness in participants and spectators of two high school hockey games played at an indoor ice arena located in a suburb of St Paul, Minn. The outbreak was caused by nitrogen dioxide gas emitted from the malfunctioning engine of the ice resurfacer, commonly referred to as a “Zamboni,” named after its inventor (Sports Illustrated. March 30, 1987:38–45). Because outbreaks of nitrogen dioxide—induced respiratory illness in this setting are reported rarely, our epidemiologic and clinical findings are presented herein.

BACKGROUND

On February 20, 1987, the Minnesota Department of Health, Minneapolis, was notified by a high school hockey coach that several members of two teams (A and B) experienced acute onset of cough, hemoptysis, and/or chest pain during or immediately after a game at an indoor ice arena on February 17, 1987. In addition, members of two hockey teams (C and D) that had played a game at the arena 5 days earlier (February 12, 1987) had developed similar symptoms during or shortly after their game at the arena. Three of the four hockey teams (A, B, and C) had played at the arena only one time; team D held daily practices and played weekly games at the arena.

The arena was community owned and operated. During practices, the ice was

Reprinted with permission from JAMA 262(21):3014–7, Copyright 1989, American Medical Association.



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Environmental Medicine: Integrating a Missing Element into Medical Education Reprinted from JAMA® The Journal of the American Medical Association December 1, 1989, Volume 262 Copyright 1989, American Medical Association An Outbreak of Nitrogen Dioxide—Induced Respiratory Illness Among Ice Hockey Players Katrina Hedberg, MD; Craig W.Hedberg, MS; Conrad Iber, MD; Karen E.White, MPH; Michael T.Osterholm, PhD, MPH; David B.W.Jones; James R.Flink, MD; Kristine L.MacDonald, MD During February 1987 an outbreak of nitrogen dioxide—induced respiratory illness occurred among players and spectators of two high school hockey games played at an indoor ice arena in Minnesota. The source of the nitrogen dioxide was the malfunctioning engine of the ice resurfacer. Case patients experienced acute onset of cough, hemoptysis, and/or dyspnea during, or within 48 hours of attending, a hockey game. One hundred sixteen cases were identified among hockey players, cheerleaders, and band members who attended the two games. Members of two hockey teams had spirometry performed at 10 days and 2 months after exposure; no significant compromise in lung function was documented. Nitrogen dioxide exposure in indoor ice arenas may be more common than currently is recognized; only three states require routine monitoring of air quality in ice arenas, and the respiratory symptoms caused by exposure to nitrogen dioxide are nonspecific and easily misdiagnosed. (JAMA. 1989;262:3014–3017) NITROGEN dioxide is a brownish gas produced as a by-product of combustion. Occupational exposures to nitrogen dioxide are frequent among silo fillers, arc welders, firefighters, and workers who manufacture missile fuels and explosives.1,2 The effects of nitrogen dioxide depend on the level and duration of exposure. Exposure to moderate levels (50 ppm) for brief periods may produce cough, hemoptysis, dyspnea, and chest pain.3 Exposure to high concen     From the Division of Field Services. Centers for Disease Control, Atlanta. Ga (Dr K.Hedberg); the Acute Disease Epidemiology Section, Minnesota Department of Health, Minneapolis (Drs K.Hedberg. Osterholm, and MacDonald and Ms White and Messrs C.W.Hedberg and Jones); the Department of Internal Medicine, Hennepin County Medical Center. Minneapolis (Dr Iber); and Pulmonary Health Associates, St Paul, Minn (Dr Flink). Reprint requests to Acute Disease Epidemiology Section, Minnesota Department of Health, 717 Delaware St SE, Minneapolis, MN 55440 (Dr MacDonald). trations of nitrogen dioxide (>100 ppm) can produce pulmonary edema, which can be acutely fatal or may lead to bronchiolitis obliterans.4,5 Bronchiolitis obliterans may result in chronic restrictive pulmonary disease; however, most patients recover, with few long-term sequelae. Treatment with corticosteroids may diminish the severity of disease.6,7 Exposure to low levels of nitrogen dioxide also may produce adverse pulmonary effects. Human volunteers exposed to 5 ppm of nitrogen dioxide for 15 minutes and 2.5 ppm for 2 hours demonstrated increased pulmonary airway resistance.8 Also, recent studies suggest that long-term exposure to low levels of nitrogen dioxide, in the environment or in the home, may predispose residents to respiratory infections and chronic obstructive pulmonary disease.9–15 The National Institute for Occupational Safety and Health recommends 1 ppm of nitrogen dioxide as a work-site standard.1 During February 1987, we investigated an outbreak of acute respiratory illness in participants and spectators of two high school hockey games played at an indoor ice arena located in a suburb of St Paul, Minn. The outbreak was caused by nitrogen dioxide gas emitted from the malfunctioning engine of the ice resurfacer, commonly referred to as a “Zamboni,” named after its inventor (Sports Illustrated. March 30, 1987:38–45). Because outbreaks of nitrogen dioxide—induced respiratory illness in this setting are reported rarely, our epidemiologic and clinical findings are presented herein. BACKGROUND On February 20, 1987, the Minnesota Department of Health, Minneapolis, was notified by a high school hockey coach that several members of two teams (A and B) experienced acute onset of cough, hemoptysis, and/or chest pain during or immediately after a game at an indoor ice arena on February 17, 1987. In addition, members of two hockey teams (C and D) that had played a game at the arena 5 days earlier (February 12, 1987) had developed similar symptoms during or shortly after their game at the arena. Three of the four hockey teams (A, B, and C) had played at the arena only one time; team D held daily practices and played weekly games at the arena. The arena was community owned and operated. During practices, the ice was Reprinted with permission from JAMA 262(21):3014–7, Copyright 1989, American Medical Association.

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Environmental Medicine: Integrating a Missing Element into Medical Education resurfaced for 10 minutes every hour; during games, the ice was resurfaced for 5 minutes after each 15-minute period. A Plexiglas shield surrounded the ice to protect spectators from airborne hockey pucks. Two ventilation systems were used in the arena: air vents for passive air exchange and exhaust fans. The ice resurfacer was powered by an internal combustion engine using propane fuel. If these engines are not properly tuned and the fuel mixture in the carburetor receives too little oxygen, elevated levels of carbon monoxide may be produced; if the mixture has too much oxygen, elevated levels of nitrogen dioxide may be produced.16 Ice arenas in Minnesota are required to measure ambient levels of carbon monoxide and nitrogen dioxide on a weekly basis during the months of operation. Measurements are taken 120 cm above the ice in the center of the arena. Ambient levels of nitrogen dioxide above 0.5 ppm are considered to be elevated and are required to be reported to the Minnesota Department of Health. METHODS Epidemiologic and Clinical Investigation Questionnaires were administered to all hockey team members who attended the two games. In addition, cheerleaders and band members, who were present during the second game, were interviewed. Information was obtained on symptoms (including cough, hemoptysis, shortness of breath, dyspnea, chest pain, headache, and weakness), onset and duration of each symptom, general health status (including history of asthma or other respiratory problems), length of time in the arena, and location in the arena during the games (in the stands or on the ice). For hockey players, information also was obtained on position played and length of time on the ice. All interviews were completed within 10 days after attending a game at the arena. A case was defined as acute onset of cough, hemoptysis, or dyspnea during a hockey game or within 48 hours of attending a hockey game at the arena. Attack rates for teams were compared using standard univariate analysis.17 Spirometry was performed within 10 days of exposure and again at 2 months after exposure for all members from two hockey teams: team C (with a single exposure) and team D (with multiple exposures). Spirometry also was performed on members of a basketball team from one of the schools, which served as an unexposed group for comparison. Pulmonary function testing was performed at the high schools that the players attended using a portable spirometer (Microloop, Medical Graphics Corp, St Paul, Minn). The best result of three attempts was recorded. Intermountain Thoracic Society predicted values (which control for age, height, and weight) were used to determine results by percent of predicted.18 We reviewed medical records for hockey players who reported seeing a physician. Information was obtained on physical examination, chest roentgenogram findings, and treatment prescribed during initial and follow-up clinic visits. Environmental Investigation Air quality records at the ice arena were reviewed for the hockey season. No measurements had been obtained during the two games in question. Therefore, to simulate conditions during the games, the ice resurfacer was operated for 30 minutes and levels of nitrogen dioxide and carbon monoxide in the arena were measured. The use of the ventilation systems during the two games also was reviewed. Survey of State Health Departments To evaluate air quality monitoring in indoor ice arenas nationally, and to obtain an estimate of the number of ice arenas located in each state, a telephone survey of all 50 state health departments was conducted. The Ice Skating Institute of America, the US Figure Skating Association, and the National Hockey Association also were contacted to obtain estimates of the number of indoor ice arenas located in the United States. RESULTS Epidemiologic Investigation Questionnaires were completed on 92 (94%) of 98 hockey players with a single exposure (teams A, B, and C), 34 (100%) of 34 players with multiple exposures (team D), 16 (76%) of 21 cheerleaders, and 25 (96%) of 26 band members. Overall, 116 cases were identified. Symptoms reported by at least 30% of the 69 case hockey players who had a single exposure are listed in Table 1. A typical case was characterized by acute onset of cough and dyspnea within 1 hour of playing a game at the arena. At the time of onset, the cough was frequently so severe that players had difficulty driving home after the game. The mean duration of cough was 16 days in players with acute exposure. The dyspnea was described most often as “aching lungs” or “a tightness in the chest” that made it difficult to inhale deeply. Hemoptysis was characterized by blood-tinged sputum. Similar symptoms were noted among players on team Table 1.—Symptoms Reported by 69 Case Patients With a Single Exposure to Nitrogen Dioxide, Minnesota, 1987 Symptom No. (%) of Patients Cough (acute onset) 67 (97) Shortness of breath (exertion) 45 (65) Chest pain 44 (64) Shortness of breath (rest) 31 (45) Headache 31 (45) Hemoptysis 24 (35) Weakness 22 (32) D. However, because many of the players on team D complained of chronic cough, they were not included as acute cases. The mean duration of cough for players on team D was 41 days. Eighteen (14%) of 126 hockey players reported a history of reactive airway disease (asthma). Of these, 16 (89%) reported an exacerbation of their asthma symptoms after playing at the arena. Attack rates for the groups are listed in Table 2. Although the attack rate for acute onset of symptoms for members of team D was only 56%, 11 (73%) of 15 players on team D who did not have acute onset of symptoms admitted to chronic respiratory symptoms (primarily cough). The attack rates for cheerleaders (who were on the ice) and band members (who sat in the stands) were similar to the attack rates for hockey players on teams A, B, and C. However, hockey players and cheerleaders were 3.2 times as likely as band members to develop hemoptysis (P=.05, Mantel-Haenszel χ2 test). Length of time spent in the arena, length of time spent on the ice, and position played did not substantially increase the risk of developing hemoptysis. Results of initial and follow-up spirometry performed on team C (single exposure), team D (multiple exposures), and the unexposed comparison group of basketball players are shown in Table 3. Overall, no differences in five lung function parameters at initial testing or at 2 months’ follow-up (when comparing percent of predicted) were noted between the two hockey teams and the basketball comparison group. Ninety-two hockey players sought medical attention; abnormal findings and treatment prescribed at the initial clinic visit are shown in Table 4. Ten patients had follow-up physician visits; none had ongoing signs or symptoms noted. Environmental Investigation Mechanics at the ice arena reported that the ice resurfacer had not been running properly during the preceding 6 months and that it had been emitting

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Environmental Medicine: Integrating a Missing Element into Medical Education Table 2.—Attack Rates Following Attendance at Hockey Games, Minnesota, 1987   No. (%) of Patients     Group Total Meeting Case Definition* With Hemoptysis Team A 33 27 (82) 9 (27) Team B 29 21 (72) 6 (21) Team C 30 21 (70) 9 (30) Team D 34 19 (56) 4 (12) Cheerleaders (teams A and B) 16 13 (81) 4 (25) Band members (team A) 25 15 (62) 2 (8) Total 167 116 (69) 34 (20) *Defined as acute onset of cough, hemoptysis, or dyspnea. Table 3.—Players Performing Below Normal on Initial and Follow-up Spirometry, Minnesota, 1987*   No. (%) of Players     Exposure Initial Follow-up Single n=30 n=26 FVC 0 (0) 0 (0) FEV1 1 (3) 2 (7) FEV1/FVC 5 (17) … FEF25–75 10 (34) 10 (34) Peak flow 6 (21) 4 (14) Multiple n=34 n=33 FVC 3 (9) 3 (9) FEV1 2 (6) 2 (6) FEV1/FVC 4 (12) … FEF25–75 12 (35) 10 (29) Peak flow 9 (26) 7 (21) Unexposed† n=24 … FVC 4 (17) … FEV1 3 (13) … FEV1/FVC 0 (0) … FEF25–75 7 (29) … Peak flow 4 (17) … *FVC indicates forced vital capacity; FEV1, forced expiratory volume in 1 second; and FEF25–75, forced expiratory flow at 25% to 75% of FVC. Below normal is less than 80% predicted for FVC, FEV1, FEF25–75, and peak flow and less than 95% predicted for FEV1/FVC. †No follow-up was performed in the unexposed group. Table 4.—Chest Auscultation and Chest Roentgenogram Findings and Treatment Prescribed for 92 Hockey Players After Nitrogen Dioxide Exposure, Minnesota, 1987 Finding and Treatment Total No.* No. (%) With Finding Chest auscultation: Rales, rhonchi, and wheezes 52 4 (8) Chest roentgenogram: Bilateral infiltrates 58 4 (7) “Increased bronchial markings” 58 8 (14) Treatment Antibiotics 92 22 (24) Corticosteroids 92 19 (21) Bronchodilators 92 7 (8) *Chest auscultation findings noted in 52 charts and chest roentgenogram results noted in 58 charts. elevated levels of nitrogen dioxide intermittently. Review of air quality measurements obtained between October 1986 and February 1987 indicated that a nitrogen dioxide level of 3 ppm had been recorded on November 23, 1986. At that time, exhaust fans had been turned on and subsequent measurements were within recommended limits (<0.5 ppm). All other measurements recorded in the logbook were within recommended limits. However, nitrogen dioxide levels were not measured during either of the two hockey games involved in the outbreak. During the games, the exhaust fans were not in use and, because the bleachers were not heated, the passive air vents had been blocked off to keep warm air from escaping. Responding to complaints from hockey players and spectators, arena operators turned on exhaust fans the morning after the second hockey game. When air quality measurements were obtained 2 days later, after operation of the ice resurfacer for 30 minutes, a nitrogen dioxide level of 4 ppm (eight times higher than the recommended limit) was detected. Survey of State Health Departments The survey of state health departments revealed that only 13 states (26%) had ever monitored indoor air quality in ice arenas. Of these, only 3 states (including Minnesota) monitor air quality on a routine basis. Although it was not possible to obtain an accurate count of the number of indoor ice skating rinks located in the United States, the Ice Skating Institute of America estimates that there are more than 800. These are located primarily in the Northeastern states, upper Midwestern states, Colorado, and California. Minnesota alone (population, 4.2 million) has 122 certified indoor ice arenas; each arena has an ice resurfacer. COMMENT Nitrogen dioxide exposure was the most likely cause of this outbreak of respiratory illness for the following reasons. First, the acute onset of respiratory symptoms in persons attending the two hockey games supports a toxic environmental exposure. Second, cough, hemoptysis, and dyspnea are symptoms that are typical of acute exposure to nitrogen dioxide. Finally, the ice resurfacer was found to be malfunctioning, as demonstrated by the elevated ambient levels of nitrogen dioxide detected in the ice arena after operation of the ice resurfacer 2 days later. No alteration in the machine’s engine had occurred between the hockey game and the time the measurements were obtained. Although the exact levels of nitrogen dioxide in the arena at the time of the hockey games are not known, the fact that a level of 4 ppm was detected, even after the arena ventilation system had been operating for 2 days, suggests that levels during the games may have been considerably higher. This also is supported by the following findings. High attack rates were noted for all groups interviewed. Between 21% and 30% of case hockey players experienced hemoptysis. Eighteen players reported a history of reactive airway disease (asthma), which is known to be exacerbated by nitrogen dioxide19; 89% of these players reported an exacerbation of their symptoms after exposure at the arena. Although attack rates were similar for all groups, rates of hemoptysis for persons who spent time on the ice (hockey players and cheerleaders) were higher than for persons who sat in the stands (band members). The concentration of nitrogen dioxide may have been higher near the ice surface because nitrogen dioxide is heavier than air and may have settled near the ice. Also, passive airflow near the ice may have been hindered by the Plexiglas shield surrounding the ice. In addition, the hockey players and cheerleaders were exercising and therefore had a higher minute ventilation and greater lung tissue exposure than persons in the stands. While symptoms were more severe for those on the ice, the attack rate for band members, who were seated in the stands, was greater than 50%, indicating that spectators also had a clinically important exposure. No data are available on the total number of spectators at the games or the number of cases among spectators; therefore, exposure for this group was not ascertained. Pulmonary function testing performed on members of one hockey team with a single exposure demonstrated no decrease in lung function parameters at either 10 days or 2 months after exposure. In addition, although players on the team with multiple exposures experienced more chronic respiratory symptoms than did players on the other teams, spirometry did not demonstrate a decrease in lung function in members of this team. This suggests that the level of nitrogen dioxide exposure during this outbreak, although sufficient to produce acute respiratory symptoms, was not high enough to cause long-term pulmonary damage. However, because baseline spirometry testing before exposure was not available, minor changes in pulmonary function in-

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Environmental Medicine: Integrating a Missing Element into Medical Education dicative of subtle small-airway damage may have remained undetected. Outbreaks of carbon monoxide intoxication in indoor ice arenas have occurred frequently20,21; however, outbreaks of nitrogen dioxide—induced respiratory illness in this setting are reported rarely. In addition to the current investigation, there are only two reports in the literature of illness compatible with nitrogen dioxide exposure in ice hockey players. In August 1969, a group of hockey players in Minnesota experienced chest tightness and difficulty breathing after playing a game.16 In February 1988, nine persons in Quebec, Canada, experienced cough, dyspnea, and “difficulty breathing” after attending a hockey game.22 Despite limited documentation of similar outbreaks, it is possible that the problem of nitrogen dioxide exposure in indoor ice arenas may be more common than is recognized currently. Although 800 indoor ice arenas are located in the United States, only three states monitor the air quality on a routine basis. In addition, because respiratory symptoms associated with exposure to nitrogen dioxide may be relatively mild and nonspecific, the correct diagnosis may remain unrecognized. To prevent future outbreaks from occurring, ice resurfacing equipment must be properly maintained and ice arenas must be adequately ventilated. In addition, regulations requiring routine exhaust emission checks of ice resurfacers may be necessary. When patients present with acute onset of pulmonary symptoms, particularly hemoptysis, with onset during or shortly after spending time in an indoor ice arena, physicians should consider the possibility of exposure to nitrogen dioxide. We thank Jack A.Korlath, MPH, William W. Joy, RN, Ray W.Thron, PhD, Karen A.Casale, BSN, Eileen M.Rooney, BSN, and Karen A.Kavan, BSN, for assistance with data collection; Peter A.Bitterman, MD, and Guiermo Dopico, MD, for advice; Robert A.Gunn, MD, MPH, for manuscript review; and the Twin Cities (Minn) medical community for providing information on patients. References 1. Criteria for a Recommended Standard… Occupational Exposure to Oxides of Nitrogen (Nitrogen Dioxide and Nitric Oxide). Washington, DC: National Institute for Occupational Safety and Health; 1976. Dept of Health, Education, and Welfare publication (NIOSH) 76–149. 2. Recommended Health-Based Occupational Exposure Limits for Respiratory Irritants. Geneva, Switzerland: World Health Organization; 1984. Technical report series 707. 3. Rosenstock L. Occupational Medicine: State of the Art Reviews . Philadelphia, Pa: Hanley & Belfus Inc; 1987;2:303–305. 4. Ramirez RJ, Dowell AR. Silo-fillers disease: nitrogen dioxide-induced lung injury. Ann Intern Med. 1971;74:569–576. 5. Milne JEH. Nitrogen dioxide inhalation and bronchiolitis obliterans. J Occup Med. 1969;11:538– 547. 6. Morgan WKC, Seaton A. Occupational Lung Disease. Philadelphia, Pa: WB Saunders Co; 1975. 7. Dorinsky PM, Davis WB, Lucas JG, Weiland JE, Gadek JE. Adult bronchiolitis: evaluation by bronchoalveolar lavage and response to prednisone therapy. Chest. 1985;88:58–63. 8. Kerr HD, Kulle TJ, McIlhany ML, Swidersky P. Effects of nitrogen dioxide on pulmonary function in human subjects: an environmental chamber study. Environ Res. 1979;19:392–404. 9. Melia RJW, Florey C, Morris RW, Goldstein BD, Clark D, John HH. Childhood respiratory illness and the home environment, I: relations between nitrogen dioxide, temperature and relative humidity. Int J Epidemiol. 1982;11:155–163. 10. Pearlman ME, Finklea JF, Creason JP, Shy CM, Young MM, Horton RJM. Nitrogen dioxide and lower respiratory illness. Pediatrics. 1971; 47:391–398. 11. Remijn B, Fischer P, Brunekreef B, Lebret E, Boliej JS, Noij D. Indoor air pollution and its effect on pulmonary function of adult non-smoking women, I: exposure estimates for nitrogen dioxide and passive smoking. Int J Epidemiol. 1985;2:215–220. 12. Detels R, Rokaw SN, Coulson AH, Tashkin DP, Sayre JW, Massey FJ. The UCLA population studies of chronic obstructive respiratory disease, I: methodology and comparison of lung function in areas of high and low pollution. Am J Epidemiol. 1979;109:33–58. 13. Wagner WD, Duncan BR, Wright PG, Stokinger HE. Experimental study of threshold limit of NO2. Arch Environ Health. 1965;10:455–466. 14. Shy CM, Creason JP, Pearlman ME, McClain KE, Benson FB. The Chattanooga school children study: effects of community exposure to nitrogen dioxide, I: methods, description of pullutant exposure and results of ventilatory function testing. J Air Pollut Control Assoc. 1970;20:539–545. 15. Shy CM, Creason JP, Pearlman ME, McClain KE, Benson FB. The Chattanooga school children study: effects of community exposure to nitrogen dioxide, II: incidence of acute respiratory illness. J Air Pollut Control Assoc. 1970;20:582–588. 16. Anderson DE. Problems created for ice arenas by engine exhaust. Am Ind Hyg Assoc J. 1971; 32:790–801. 17. Nie NH, Hull CH, Jenkins JG, Steinbrenner K, Bent DH. Statistical Package for the Social Sciences. 2nd ed. New York, NY: McGraw-Hill International Book Co; 1975. 18. Morris AH, Kanner RH, Crapo RO, Gardner RM. Clinical Pulmonary Function Testing. 2nd ed. Salt Lake City, Utah: Intermountain Thoracic Society; 1984. 19. Bauer MA, Utell MJ, Morrow PE, Speers DM, Gibb FR. Inhalation of 0.30 ppm nitrogen dioxide potentiates exercise-induced bronchospasm in asthmatics. Am Rev Respir Dis. 1986;134:1203– 1208. 20. Centers for Disease Control. Carbon monoxide intoxication associated with use of a gasoline-powered resurfacing machine at an ice-skating rink—Pennsylvania. MMWR. 1984;33:49–51. 21. Kwok PW. Evaluation and control of carbon monoxide exposure in indoor skating arenas . Can J Public Health. 1983;74:261–265. 22. Canadian Laboratory Centre for Disease Control. Nitrogen dioxide poisoning at a skating rink— Quebec. Can Dis Weekly Rep. 1988;14–15:61–62.