- Email: [email protected]
The validity of the heat tolerance test in prediction of recurrent exertional heat illness events
G Model
ARTICLE IN PRESS
JSAMS-1720; No. of Pages 5
Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Journal of Science and Medicine in Sport journal homepage: www.elsevier.com/locate/jsams
Original research
The validity of the heat tolerance test in prediction of recurrent exertional heat illness events Haggai Schermann a,b,c,∗ , Yuval Heled b , Chen Fleischmann a,b , Itay Ketko a,b , Nathan Schiffmann a,b , Yoram Epstein b , Ran Yanovich a,b a
Institute of Military Physiology, IDF Medical Corps, Israel Heller Institute of Medical Research, Sheba Medical Center, affiliated with Tel Aviv University, Israel c Division of Orthopedic Surgery, Tel Aviv Sourasky Medical Center, affiliated with Tel Aviv University, Tel Aviv, Israel b
a r t i c l e
i n f o
Article history: Received 5 May 2017 Received in revised form 25 June 2017 Accepted 5 October 2017 Available online xxx Keywords: Heat tolerance testing Exertional heat illness Screening Secondary prevention
a b s t r a c t Objectives: Heat-tolerance-testing (HTT) protocol is used as a screening test for secondary prevention of exertional heat illness (EHI) in the military. Subjects whose test results are positive (heat-intolerant, HI) are presumed to be at higher risk of repeated EHI events than heat-tolerant subjects (HT) and are therefore prevented from return to combat duty, but may return to unsupervised recreational activity. Our aim was to determine, whether HTT results predict the risk of repeated episodes of exertional heat illness (EHI). Design: Retrospective cohort. Methods: One-hundred-forty-five subjects (110 HT, 35 HI) who were diagnosed with an EHI event by a physician and underwent HTT during 2008–2015 were contacted and asked about recurrence of EHI. Incidence of recurrent events was reported as number of cases per 1000 person-years. Ratio of events among HI and HT individuals was presented as rate ratio (RR) and its 95% confidence interval. Results: Of the 145 patients, six (4.1%) had experienced recurrent EHI events (10.63 per 1000 PY): four HI subjects (11.4%, 26.6 per 1000 PY) and two HT (1.8%, 4.8 per 1000 PY) (RR = 5.504, CI 95% = 1.01–30, p = 0.027). Only one of the six recurrent events was a heat stroke (HT individual), other five were heat exhaustions. Sensitivity, specificity and diagnostic accuracy of HTT were 66.7%, 77.7% and 77.2%, respectively. Conclusions: The risk of EHI recurrence is measurable and can be discussed with patients before they return to sports. A referral to HTT can be considered, as negative HTT result is associated with substantial and significant EHI risk reduction. © 2017 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
1. Introduction On the spectrum of the exertional heat illness (EHI), exertional heat stroke (EHS) is a potentially fatal condition, resulting from excess heat accumulated in the body during physical exertion. It is an occupational hazard for young and healthy individuals: soldiers, manual laborers, and athletes .1,2 Residual neurologic damage, reduced exercise capacity, heat intolerance, and excess mortality have been reported among EHS survivors .3,4 Therefore, the prevention and treatment of EHS, as well as the decision to return an individual to active duty after an episode of EHS, receive high prior-
∗ Corresponding author. E-mail address: [email protected] (H. Schermann).
ity among other questions dealt with by sports and military training professionals. Heat intolerance is characterized by a reduced ability to sustain exercise-induced heat stress.5 The symptoms have been linked to physiological defect in the ability to effectively dissipate metabolic heat. This concept is often used to distinguish between individuals who will endure standardized exercise heat stress and those who will not.6 Various protocols have been suggested to assist informed return-to-duty (RTD) decisions after EHS. Some protocols focus on clinical recovery6 and some rely on physiological responses to an exercise heat test.7 For the last 40 years, RTD decisions of soldiers who had experienced an episode of EHS in the Israeli Defense Force (IDF) have been based on the results of a heat tolerance test (HTT) .7 In short, the results of the test are based on core body temperature and heart rate responses to a 2-h exercise–heat stress consisting
https://doi.org/10.1016/j.jsams.2017.10.001 1440-2440/© 2017 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
2
of a treadmill walk (5 km/h) in a climate chamber under controlled conditions of 40 ◦ C and 40% relative humidity. Testing is performed a few weeks after clinical recovery from the episode of EHS.7 The test is repeated, 2–3 months later, for those individuals who are considered heat intolerant (HI) during the 1st test. A positive result on the second test is a definitive indication for revision of the subjects’ medical profile grade and discontinuation of their combat service.7 Nevertheless, the sensitivity and specificity of the test have never been analyzed, mostly due to the fact that those who are diagnosed as HI do not return to regular physical activity. In this paper, using retrospective data, we attempted to quantitatively evaluate the HTT-based decision to return to duty, by its ability to predict a repeated episode of EHI, either heat stroke or heat injury. We have also assessed for any residual post-EHS exertional symptoms among subjects who underwent HTT.
2. Materials and methods The study was based on a cohort of 147 individuals who were referred to an HTT in our lab between 2008 and 2015 after sustaining an episode of EHS or suspected EHS (presentation with significant neurologic dysfunction, but with delayed measurement of core temperature, performed only after cooling and not reflective of core temperature at the time of collapse) and who were otherwise healthy. The diagnosis of EHS was made by a unit physician, based on the initial clinical presentation, rectal temperature value and emergency room laboratory results. Only individuals who performed the test at least 6 months prior to the survey where included in the cohort. This follow-up survey was approved by the IDF Medical Corps’ institutional review board. Demographic and contact information, details of the EHI event, and the HTT data of these individuals, were available from the clinical database of the Warrior Health Research Institute. Data collected included age at the time of the event, height, weight, type of activity preceding the event, first measured core temperature, time from collapse to temperature measurement (coinciding with the time when the subject was first examined by a medic and then cooling treatment with water was started), and time between the event and the HTT. Some subjects’ initial HTT was positive, but second or third HTT was negative. We used the latest HTT result to classify individuals as heat tolerant or heat intolerant, and reported the time between the event and the latest HTT. Of the 147 subjects, one refused to participate and one was excluded due to a history of recurrent syncope, unrelated to exertion. Remaining subjects reported no background medical conditions or chronic medications use. A physician who is familiar with EHI and the HTT completed the telephone interviews, which included questions about return to previous level of activity, recurrent episodes or symptoms of EHI, presence of any difficulties in performing exercise in the heat (i.e. heat intolerance symptoms), and any background medical conditions (Table 1). Each subject was classified as HI or HT, according to the HTT result. A recurrent episode of EHI was established based on subjective reports of any impairment of consciousness that occurred during exercise or work, and a participant’s description of an episode as
Table 1 The survey questionnaire. 1 2 3 4
Have you returned to the level of activity that you were capable of before the initial exertional heat illness event? Ever since the first event of exertional heat illness, have you experienced any recurrent event similar to the first one? Have you been experiencing any symptoms on exertion? (headache, dizziness, nausea, any other symptom) Do you have any background medical condition?
similar to the EHI event encountered in the past. The subjects were asked “Ever since the first event of exertional heat illness, have you experienced any recurrent event similar to the first one?” We further inquired about any medical documentation of the event, in order to obtain more clinical details. Residual post-EHI symptoms were defined by reports of any headache or dizziness on exertion, disturbed thermoregulatory function (e.g. change in sweating pattern or perception of ambient heat different from other people), and any new neurologic impairment that was not present prior to the first EHI event. Duration of follow-up was calculated as the time elapsed from the first EHI event to the telephone survey. Rate of the recurrent events was calculated as the number of events per 1000 person-years. Comparison of the event rates between the HT and HI individuals was done by using exact estimates of the rate ratio and their 95% confidence intervals.8 Screening utility of HTT was evaluated using standard contingency tables and by calculating sensitivity, specificity, and diagnostic accuracy of each classification, using recurrent EHI events as reference. Odds ratios of EHI events and their 95% confidence intervals were calculated from contingency tables using Wilson score.9 Statistical analysis was performed on R 3.3.0 opensource software. 3. Results Based on the HTT results, 35 subjects were identified as HI and 110 subjects as HT. Mean time of follow-up was 48 months, ranging from 8 to 108 months. Six recurrent EHI episodes were reported (4.1%, 95% CI: 1.7–8.4). Four events occurred in 4 heat-intolerant (11.4%) and 2 (1.8%) heat-tolerant subjects. (odds ratio = 6.85, 95% CI (1.2–39.8), p = 0.03,). The recurrent event incidence rates, the rate ratios of HI to HT subjects, and the screening utility measures of HTT are presented in Table 2. Only one event was registered in medical records as a heat stroke. It had occurred in an individual who was previously diagnosed as heat-tolerant, during reservist military training, while marching in full gear. Obvious risk factors for the event included high environmental heat load and inadequate hydration. Other five subjects described episodes of collapse due to fatigue, syncope or pre-syncope that were treated by cessation of activity, cooling with water and rest, and complete recovery occurring within minutes to hours. Only one of these events occurred during military training in an active service officer, who was diagnosed as heat-intolerant and was assigned an administrative role in a combat unit. He had violated the recommendations and participated in a training march
Table 2 Recurrent heat illness events.
No. of subjects tested (total n = 145) No. of recurrent cases (total n = 6) Duration of follow-up (total person-years for the group) Ratio (recurrent events ratio (cases per 1000 person-years)
HTT− (Heat-tolerant)
HTT+ (Heat intolerant)
Total/significance
110 2 416.96 4.832
35 4 147.38 26.59
145 6 564.34 0.0267
HTT — heat tolerance test.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model
ARTICLE IN PRESS
JSAMS-1720; No. of Pages 5
H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
3
Table 3 Background characteristics of HTT-positive vs HTT-negative subjects, and subjects with repeated exertional heat illness events vs those without. Heat tolerance testing result
Recurrent exertional heat illness events
HTT+ (n = 110)
HTT− (n = 35)
p-value
Recurrent events (n = 6)
No recurrent events (n = 139)
p-value
Age (years, mean ± SD) Height (m, mean ± SD) Weight (kg, mean ± SD) Type of activity: March or drill Physical test Selections Week of field training Running
20.4 ± 2.2 1.75 ± 0.08 78 ± 12.3
19.9 ± 2.4 1.75 ± 0.07 73 ± 11.4
0.32 0.92 0.09
20.2 ± 1.92 1.76 ± 0.11 74.5 ± 14.1
20 ± 2.4 1.75 ± 0.07 74 ± 11.7
0.82 0.82 0.94
50% 21% 12.5% 12.5% 4%
44% 22% 24% 3% 7%
0.3
0% 25% 25% 50% 0%
47% 22% 21% 5% 5%
0.09
Core temperature at the event (◦ C) Time to core temperature measurement (mins, mean ± SD) Time to HTTa (days, median, mean ± SD) Duration of follow-up (months) Residual symptoms at follow-upb (%)
39.1 ± 1.8 2.83 ± 4.16
39.4 ± 1.3 1.63 ± 7.8
0.45 0.41
20.2 ± 1.9 8 ± 12
20 ± 2.4 1.7 ± 4.7
0.8 0.32
48, 52 ± 93
47.5, 101 ± 207
0.12
60, 62 ± 13
47, 92 ± 192
0.18
54 ± 24 43%
45 ± 24 14.5%
26 ± 20 83%
49 ± 24 19%
0.14 0.0009
0.07 0.0017
a
HTT — heat tolerance test. Refers to any remaining exercise or heat intolerance, exercise-induced headache and dizziness, constant headache or changed pattern of sweating, reported at the follow-up. b
Table 4 Screening utility measures of HTT. Screening utility measures Rate ratio of events in HI vs HTa subjects (CI 95%b , p-value) Sensitivity (CI 95%) Specificity (CI 95%) Likelihood ratio of a positive test (CI 95%) Likelihood ratio of a negative test (CI 95%) Diagnostic accuracy (CI 95%) a b
5.502 (1.008–30.03, 0.0267) 66.7% (30–90.3) 77.7% (70.1–83.8) 2.99 (2.2–4.1) 0.43 (0.16–1.15) 77.2% (69.8–83.3)
HI — heat-intolerant, HT — heat-tolerant. 95% CI — 95% confidence interval.
voluntarily. Other four subjects described mild EHI events that occurred during running and tracking. Subjects’ baseline characteristics and the event and treatment details are presented in Table 3. The comparison between HTT+ and HTT− subjects and between those who had recurrent EHI and those who did not, showed that the groups were uniform with respect to age at the event, height, weight, type of activity preceding the event, maximum core temperature at the event, time of core temperature measurement and time to HTT. Residual symptoms were present in 31 subjects. They included mainly headache and dizziness on exertion (n = 19, 61%). Fewer subjects had constant headaches (n = 8, 26%), change in pattern of sweating (n = 2, 6.5%) and memory impairment (n = 2, 6.5). Symptoms were present in 14.5% of HTT− and in 43% of HTT+ subjects (OR = 4.4, p = 0.0009), and were also highly correlated with repeated EHI events (OR = 21.7, p = 0.0017) (Table 3). 4. Discussion In our study, we attempted to estimate the incidence of recurrent EHI events and to evaluate HTT-based screening as a diagnostic test, using reported recurrent EHI events as reference. We have found an increased incidence of heat exhaustion among heatintolerant individuals, but were unable to determine whether positive HTT result is predictive of recurrent heat stroke (Table 4). The estimated rate of first EHI events in the IDF today is about 0.5–1 cases per 1000 person-years (PY). This is substantially lower than the incidence rate reported recently in the US military — 1.44 (range 0.21–5.39 in different subgroups) cases per 1000 PY.2 In this study, the EHI survivors exhibited a rate of 10.64 cases of
recurrent events per 1000 PY, which appears to be significantly greater than first-event incidence reported by Medical Surveillance Monthly Report (p < 0.001). Similar findings were presented by a retrospective follow-up study of US military recruits, which compared incidence of hospitalizations for EHI among subjects who previously had EHI and were treated as inpatients, subjects who had EHI and were treated as outpatients and subjects who did not have a history of EHI. The incidence rates were 7.5, 1.7 and 0.5 per 1000 PY, respectively.10 The inpatient EHI group may be most similar to our cases, who were all evacuated and treated in medical centers, and their recurrence rates are close to ours. Together with several case reports,11,12 these studies provide a firm basis for the theory that a single EHI event is predictive of additional EHI events. The odds of recurrent events in subjects with a positive result in HTT was almost 7 times higher than for individuals with negative result in HTT, despite the fact that all individuals with positive HTT are instructed to refrain from strenuous physical activity, especially under unfavorable climatic conditions. Therefore, only those who disregard the recommendations were included in the recurrent events statistic. This fact strengthens the validity of the HTT, meaning that in reality, return to duty of those who were identified as HI without an HTT-based screening would have resulted in much higher incidence of recurrent events. Obviously, HTT results were not fully explanatory of the recurrent EHI events. The reason is that HTT is a functional, not a medical diagnostic test. Heat tolerance is defined clinically as an inability to adapt physiologically to exercise in heat.5 It is true that heat intolerant subjects are somewhat restricted in non-routine exercise in extreme conditions, which resembles a pathological or disease state. However, the heat tolerance status is highly correlated with physiological entities, such as aerobic fitness, acclimatization, weight, etc.11,13 Change in one of the latter would lead to increase or decrease of heat tolerance. Therefore, we believe that in most cases heat intolerance is a physiological state, while HTT is a functional test reflective only of the current state. Despite this, HTT result may still be prognostic of future heat tolerance, because other physiological states also tend to be trend-like. For example there are higher chances that an obese or unfit person would continue to be obese or unfit. There may be a small fraction of subjects who are able to modify other physiological parameters and still remain heat-intolerant due to some inherent pathological heat intolerance, but vast majority of subjects are heat intolerant due to inability to modify other modifiable physiological factors.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5 4
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
In this study, the subjects’ demographics and event details were not correlated with HTT results, nor with EHI recurrence. We propose two explanations for this. First and most probable is the sample size — heat tolerance is subject to influence by multiple known and unknown intrinsic and extrinsic factors. Therefore, research of the effect of the event-related factors on heat tolerance would likely require adjustment for multiple confounders and a sample size of hundreds or thousands. This is difficult, however, because EHS is a rare disease. Another, possibly complimentary, explanation is that in our study population, treatment was provided immediately and uniformly, consisting drenching the patient with water (but not cold-water immersion). This decreased variability of the event and treatment details, since none of the subjects were cooled later than 30 min after collapse. The HTT-based RTD protocol should be considered within the context of the corresponding US military policy.14 US army employs a complex protocol which emphasizes initial risk stratification, analysis of contributing factors and clinical follow-up of soldiers until recovery. Soldiers with repeated episodes of heat exhaustion, recurrent heat injury and heat injury with sequelae, and those who had sustained a complex heat stroke (“recurrent, or occurring in the presence of a non-modifiable risk factor”) are referred to the medical examination board (MEB).14 All other cases are subject to continued follow-up (heat injury and heat exhaustion) or to supervised gradual return to normal activity (heat stroke with and without sequelae). The goal of the follow-up is to detect any subjective complaints and symptoms of heat illness or work intolerance, that would preclude return to full duty. This decision-making process is justified by the fact that heat intolerance is defined clinically. In other words, subjects’ ability to tolerate exertion may be sufficient evidence of heat tolerance. In addition, analysis of contributing factors may also provide adequate grounds for medical clearance, because natural predisposition to EHI is not likely in a person who has not experienced any complaints prior to the event, and/or who was dehydrated or sick during that particular incident. Finally, there is no validated alternative to the MEB clinical judgement. However, the US military protocol lacks objectivity and is greatly influenced by the information provided by the soldier. Problems may arise in over-motivated individuals (e.g. professional athletes and combat soldiers) who may experience symptoms of heat intolerance but do not report them for fear of losing their position. Now, after the significant association between HTT results and recurrent heat exhaustion episodes has been established, we believe that the two protocols should be complimentary. Soldiers who sustained an EHS, should undergo HTT about two weeks after the event. Those determined as HT may resume the unrestricted service, while HI individuals should be recommended gradual return to duty. Residual exertional and non-exertional symptoms that were not present prior to the event are actually the only parameter that differs between subjects with positive and negative HTT. They may be regarded as a residual disability that reflects the severity of the event. Alternatively, they are likely to represent the clinical heat intolerance, which is part of the RTD protocol in the US military, as described above. The odds ratio (OR) of recurrent EHI events among subjects with these symptoms was 21.7. This finding highlights the importance of the clinical assessment and follow-up. Our study has several limitations. We used terms such as sensitivity and specificity to quantify the ability of the HTT to predict a future heat stroke/heat injury event. However, subjects with positive and negative HTT were assigned to different levels of activity and were not exposed to the same risk level. Furthermore, the reported occurrence of repeated EHI events is subject to recall bias and lacks the objectivity and reliability that a conventional gold standard measure requires. A major advantage of self-reported EHI recurrence, and the reason we chose this measure rather than
review of medical records, is mitigation of reporting bias: for one documented case of EHS, there were five cases of EHI not captured in the medical records. This is especially true regarding the residual symptoms. On the one hand, most subjects did not seek medical care for these nonspecific symptoms, because they were relatively subtle and did not interfere with daily routine. This would lead to underestimation of their incidence had we relied on medical records. On the other hand, it is an example of reporting bias that unequally affects the HTT+ and HTT− subjects. Those diagnosed as “heat intolerant” (HTT+) would surely be more attentive to any symptoms they experience during exertion or hot weather, than HTT− subjects. Therefore, this finding needs to be validated by additional studies with different design. Small sample size is another major limitation of our study. It was sufficient for estimation of recurrent EHI events, but inadequate for calculation of incidence of such rare occurrence as recurrent HS. In this cohort, only one subject had a registered recurrent heat stroke event, which may not serve as basis for any conclusions regarding HTT validity or even incidence of the recurrent HS. Finally, we were unable to derive any valid conclusions regarding the influence of subject’s baseline characteristics and the primary EHI event and treatment details on heat tolerance or HTT results. Investigation of such a rare yet multifactorial event as EHI requires large sample sizes to adjust for all possible confounding variables. This was not feasible with our study design. Prospective surveillance of larger cohorts of persons who experienced EHI, integrating several other types of predictors in addition to the HTT result, may eventually answer these questions. 5. Conclusion Our study provides quantitative evidence that HTT offers diagnostic utility and may serve as a tool for secondary prevention of EHI. HTT should not be regarded as a medical test, but rather as a functional test. It can be performed multiple times, the last test being most reflective of a subject’s current heat tolerance status. The test provides substantial new information for clinical judgement before return to sports, and enables risk stratification of athletes into high and low risk of recurrent EHI. Practical implications • Heat tolerance (HTT) test is significantly associated with recurrent heat exhaustion events. • It is still not clear whether HTT is predictive of recurrent heat stroke. • The major advantage of HTT is objective EHI risk stratification of over-motivated individuals. Funding There has been no financial assistance with the project. Acknowledgement None. References 1. Casa DJ, DeMartini JK, Bergeron MF et al. National athletic trainers’ association position statement: exertional heat illnesses. J Athl Train 2015; 50(9):986–1000. http://dx.doi.org/10.4085/1062-6050-50.9.07. 2. Update Heat injuries, active component, U.S. Armed Forces. Med Surveill Mon Rep 2015; 22(3):17–20. 3. O’Connor FG, Casa DJ, Bergeron MF et al. American College of Sports Medicine Roundtable on exertional heat stroke—return to duty/return to play. Curr Sports Med Rep 2010; 9(5):314–321. http://dx.doi.org/10.1249/JSR.0b013e3181f1d183.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
4. Wallace RF, Kriebel D, Punnett L et al. Prior heat illness hospitalization and risk of early death. Environ Res 2007; 104(2):290–295. http://dx.doi.org/10.1016/j.envres.2007.01.003. 5. Strydom NB. Heat intolerance: its detection and elimination in the mining industry. S Afr J Sci 1980; 76(4):154–156. 6. O’Connor FG, Williams AD, Blivin S et al. Guidelines for return to duty (play) after heat illness: a military perspective. J Sport Rehabil 2007; 16(3): 227–237. 7. Moran DS, Erlich T, Epstein Y. The heat tolerance test: an efficient screening tool for evaluating susceptibility to heat. J Sport Rehabil 2007; 16(3):215–221. 8. Martin DO, Austin H. Exact estimates for a rate ratio. Epidemiology 1996; 7(1):29–33.
5
9. Wallis S. Binomial confidence intervals and contingency tests: mathematical fundamentals and the evaluation of alternative methods. J Quant Linguist 2013; 20(3):178–208. http://dx.doi.org/10.1080/09296174.2013.799918. 10. Phinney LT, Gardner JW, Kark JA et al. Long-term follow-up after exertional heat illness during recruit training. Med Sci Sports Exerc 2001; 33(9):1443–1448. 11. Epstein Y. Heat intolerance: predisposing factor or residual injury? Med Sci Sports Exerc 1990; 22(1):29–35. 12. Keren G, Epstein Y, Magazanik A. Temporary heat intolerance in a heatstroke patient. Aviat Space Environ Med 1981; 52(2):116–117. 13. Lisman P, Kazman JB, O’Connor FG et al. Heat tolerance testassociation between heat intolerance and anthropometric ing: and fitness measurements. Mil Med 2014; 179(11):1339–1346. http://dx.doi.org/10.7205/MILMED-D-14-00169.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
ARTICLE IN PRESS
JSAMS-1720; No. of Pages 5
Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Journal of Science and Medicine in Sport journal homepage: www.elsevier.com/locate/jsams
Original research
The validity of the heat tolerance test in prediction of recurrent exertional heat illness events Haggai Schermann a,b,c,∗ , Yuval Heled b , Chen Fleischmann a,b , Itay Ketko a,b , Nathan Schiffmann a,b , Yoram Epstein b , Ran Yanovich a,b a
Institute of Military Physiology, IDF Medical Corps, Israel Heller Institute of Medical Research, Sheba Medical Center, affiliated with Tel Aviv University, Israel c Division of Orthopedic Surgery, Tel Aviv Sourasky Medical Center, affiliated with Tel Aviv University, Tel Aviv, Israel b
a r t i c l e
i n f o
Article history: Received 5 May 2017 Received in revised form 25 June 2017 Accepted 5 October 2017 Available online xxx Keywords: Heat tolerance testing Exertional heat illness Screening Secondary prevention
a b s t r a c t Objectives: Heat-tolerance-testing (HTT) protocol is used as a screening test for secondary prevention of exertional heat illness (EHI) in the military. Subjects whose test results are positive (heat-intolerant, HI) are presumed to be at higher risk of repeated EHI events than heat-tolerant subjects (HT) and are therefore prevented from return to combat duty, but may return to unsupervised recreational activity. Our aim was to determine, whether HTT results predict the risk of repeated episodes of exertional heat illness (EHI). Design: Retrospective cohort. Methods: One-hundred-forty-five subjects (110 HT, 35 HI) who were diagnosed with an EHI event by a physician and underwent HTT during 2008–2015 were contacted and asked about recurrence of EHI. Incidence of recurrent events was reported as number of cases per 1000 person-years. Ratio of events among HI and HT individuals was presented as rate ratio (RR) and its 95% confidence interval. Results: Of the 145 patients, six (4.1%) had experienced recurrent EHI events (10.63 per 1000 PY): four HI subjects (11.4%, 26.6 per 1000 PY) and two HT (1.8%, 4.8 per 1000 PY) (RR = 5.504, CI 95% = 1.01–30, p = 0.027). Only one of the six recurrent events was a heat stroke (HT individual), other five were heat exhaustions. Sensitivity, specificity and diagnostic accuracy of HTT were 66.7%, 77.7% and 77.2%, respectively. Conclusions: The risk of EHI recurrence is measurable and can be discussed with patients before they return to sports. A referral to HTT can be considered, as negative HTT result is associated with substantial and significant EHI risk reduction. © 2017 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
1. Introduction On the spectrum of the exertional heat illness (EHI), exertional heat stroke (EHS) is a potentially fatal condition, resulting from excess heat accumulated in the body during physical exertion. It is an occupational hazard for young and healthy individuals: soldiers, manual laborers, and athletes .1,2 Residual neurologic damage, reduced exercise capacity, heat intolerance, and excess mortality have been reported among EHS survivors .3,4 Therefore, the prevention and treatment of EHS, as well as the decision to return an individual to active duty after an episode of EHS, receive high prior-
∗ Corresponding author. E-mail address: [email protected] (H. Schermann).
ity among other questions dealt with by sports and military training professionals. Heat intolerance is characterized by a reduced ability to sustain exercise-induced heat stress.5 The symptoms have been linked to physiological defect in the ability to effectively dissipate metabolic heat. This concept is often used to distinguish between individuals who will endure standardized exercise heat stress and those who will not.6 Various protocols have been suggested to assist informed return-to-duty (RTD) decisions after EHS. Some protocols focus on clinical recovery6 and some rely on physiological responses to an exercise heat test.7 For the last 40 years, RTD decisions of soldiers who had experienced an episode of EHS in the Israeli Defense Force (IDF) have been based on the results of a heat tolerance test (HTT) .7 In short, the results of the test are based on core body temperature and heart rate responses to a 2-h exercise–heat stress consisting
https://doi.org/10.1016/j.jsams.2017.10.001 1440-2440/© 2017 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
2
of a treadmill walk (5 km/h) in a climate chamber under controlled conditions of 40 ◦ C and 40% relative humidity. Testing is performed a few weeks after clinical recovery from the episode of EHS.7 The test is repeated, 2–3 months later, for those individuals who are considered heat intolerant (HI) during the 1st test. A positive result on the second test is a definitive indication for revision of the subjects’ medical profile grade and discontinuation of their combat service.7 Nevertheless, the sensitivity and specificity of the test have never been analyzed, mostly due to the fact that those who are diagnosed as HI do not return to regular physical activity. In this paper, using retrospective data, we attempted to quantitatively evaluate the HTT-based decision to return to duty, by its ability to predict a repeated episode of EHI, either heat stroke or heat injury. We have also assessed for any residual post-EHS exertional symptoms among subjects who underwent HTT.
2. Materials and methods The study was based on a cohort of 147 individuals who were referred to an HTT in our lab between 2008 and 2015 after sustaining an episode of EHS or suspected EHS (presentation with significant neurologic dysfunction, but with delayed measurement of core temperature, performed only after cooling and not reflective of core temperature at the time of collapse) and who were otherwise healthy. The diagnosis of EHS was made by a unit physician, based on the initial clinical presentation, rectal temperature value and emergency room laboratory results. Only individuals who performed the test at least 6 months prior to the survey where included in the cohort. This follow-up survey was approved by the IDF Medical Corps’ institutional review board. Demographic and contact information, details of the EHI event, and the HTT data of these individuals, were available from the clinical database of the Warrior Health Research Institute. Data collected included age at the time of the event, height, weight, type of activity preceding the event, first measured core temperature, time from collapse to temperature measurement (coinciding with the time when the subject was first examined by a medic and then cooling treatment with water was started), and time between the event and the HTT. Some subjects’ initial HTT was positive, but second or third HTT was negative. We used the latest HTT result to classify individuals as heat tolerant or heat intolerant, and reported the time between the event and the latest HTT. Of the 147 subjects, one refused to participate and one was excluded due to a history of recurrent syncope, unrelated to exertion. Remaining subjects reported no background medical conditions or chronic medications use. A physician who is familiar with EHI and the HTT completed the telephone interviews, which included questions about return to previous level of activity, recurrent episodes or symptoms of EHI, presence of any difficulties in performing exercise in the heat (i.e. heat intolerance symptoms), and any background medical conditions (Table 1). Each subject was classified as HI or HT, according to the HTT result. A recurrent episode of EHI was established based on subjective reports of any impairment of consciousness that occurred during exercise or work, and a participant’s description of an episode as
Table 1 The survey questionnaire. 1 2 3 4
Have you returned to the level of activity that you were capable of before the initial exertional heat illness event? Ever since the first event of exertional heat illness, have you experienced any recurrent event similar to the first one? Have you been experiencing any symptoms on exertion? (headache, dizziness, nausea, any other symptom) Do you have any background medical condition?
similar to the EHI event encountered in the past. The subjects were asked “Ever since the first event of exertional heat illness, have you experienced any recurrent event similar to the first one?” We further inquired about any medical documentation of the event, in order to obtain more clinical details. Residual post-EHI symptoms were defined by reports of any headache or dizziness on exertion, disturbed thermoregulatory function (e.g. change in sweating pattern or perception of ambient heat different from other people), and any new neurologic impairment that was not present prior to the first EHI event. Duration of follow-up was calculated as the time elapsed from the first EHI event to the telephone survey. Rate of the recurrent events was calculated as the number of events per 1000 person-years. Comparison of the event rates between the HT and HI individuals was done by using exact estimates of the rate ratio and their 95% confidence intervals.8 Screening utility of HTT was evaluated using standard contingency tables and by calculating sensitivity, specificity, and diagnostic accuracy of each classification, using recurrent EHI events as reference. Odds ratios of EHI events and their 95% confidence intervals were calculated from contingency tables using Wilson score.9 Statistical analysis was performed on R 3.3.0 opensource software. 3. Results Based on the HTT results, 35 subjects were identified as HI and 110 subjects as HT. Mean time of follow-up was 48 months, ranging from 8 to 108 months. Six recurrent EHI episodes were reported (4.1%, 95% CI: 1.7–8.4). Four events occurred in 4 heat-intolerant (11.4%) and 2 (1.8%) heat-tolerant subjects. (odds ratio = 6.85, 95% CI (1.2–39.8), p = 0.03,). The recurrent event incidence rates, the rate ratios of HI to HT subjects, and the screening utility measures of HTT are presented in Table 2. Only one event was registered in medical records as a heat stroke. It had occurred in an individual who was previously diagnosed as heat-tolerant, during reservist military training, while marching in full gear. Obvious risk factors for the event included high environmental heat load and inadequate hydration. Other five subjects described episodes of collapse due to fatigue, syncope or pre-syncope that were treated by cessation of activity, cooling with water and rest, and complete recovery occurring within minutes to hours. Only one of these events occurred during military training in an active service officer, who was diagnosed as heat-intolerant and was assigned an administrative role in a combat unit. He had violated the recommendations and participated in a training march
Table 2 Recurrent heat illness events.
No. of subjects tested (total n = 145) No. of recurrent cases (total n = 6) Duration of follow-up (total person-years for the group) Ratio (recurrent events ratio (cases per 1000 person-years)
HTT− (Heat-tolerant)
HTT+ (Heat intolerant)
Total/significance
110 2 416.96 4.832
35 4 147.38 26.59
145 6 564.34 0.0267
HTT — heat tolerance test.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model
ARTICLE IN PRESS
JSAMS-1720; No. of Pages 5
H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
3
Table 3 Background characteristics of HTT-positive vs HTT-negative subjects, and subjects with repeated exertional heat illness events vs those without. Heat tolerance testing result
Recurrent exertional heat illness events
HTT+ (n = 110)
HTT− (n = 35)
p-value
Recurrent events (n = 6)
No recurrent events (n = 139)
p-value
Age (years, mean ± SD) Height (m, mean ± SD) Weight (kg, mean ± SD) Type of activity: March or drill Physical test Selections Week of field training Running
20.4 ± 2.2 1.75 ± 0.08 78 ± 12.3
19.9 ± 2.4 1.75 ± 0.07 73 ± 11.4
0.32 0.92 0.09
20.2 ± 1.92 1.76 ± 0.11 74.5 ± 14.1
20 ± 2.4 1.75 ± 0.07 74 ± 11.7
0.82 0.82 0.94
50% 21% 12.5% 12.5% 4%
44% 22% 24% 3% 7%
0.3
0% 25% 25% 50% 0%
47% 22% 21% 5% 5%
0.09
Core temperature at the event (◦ C) Time to core temperature measurement (mins, mean ± SD) Time to HTTa (days, median, mean ± SD) Duration of follow-up (months) Residual symptoms at follow-upb (%)
39.1 ± 1.8 2.83 ± 4.16
39.4 ± 1.3 1.63 ± 7.8
0.45 0.41
20.2 ± 1.9 8 ± 12
20 ± 2.4 1.7 ± 4.7
0.8 0.32
48, 52 ± 93
47.5, 101 ± 207
0.12
60, 62 ± 13
47, 92 ± 192
0.18
54 ± 24 43%
45 ± 24 14.5%
26 ± 20 83%
49 ± 24 19%
0.14 0.0009
0.07 0.0017
a
HTT — heat tolerance test. Refers to any remaining exercise or heat intolerance, exercise-induced headache and dizziness, constant headache or changed pattern of sweating, reported at the follow-up. b
Table 4 Screening utility measures of HTT. Screening utility measures Rate ratio of events in HI vs HTa subjects (CI 95%b , p-value) Sensitivity (CI 95%) Specificity (CI 95%) Likelihood ratio of a positive test (CI 95%) Likelihood ratio of a negative test (CI 95%) Diagnostic accuracy (CI 95%) a b
5.502 (1.008–30.03, 0.0267) 66.7% (30–90.3) 77.7% (70.1–83.8) 2.99 (2.2–4.1) 0.43 (0.16–1.15) 77.2% (69.8–83.3)
HI — heat-intolerant, HT — heat-tolerant. 95% CI — 95% confidence interval.
voluntarily. Other four subjects described mild EHI events that occurred during running and tracking. Subjects’ baseline characteristics and the event and treatment details are presented in Table 3. The comparison between HTT+ and HTT− subjects and between those who had recurrent EHI and those who did not, showed that the groups were uniform with respect to age at the event, height, weight, type of activity preceding the event, maximum core temperature at the event, time of core temperature measurement and time to HTT. Residual symptoms were present in 31 subjects. They included mainly headache and dizziness on exertion (n = 19, 61%). Fewer subjects had constant headaches (n = 8, 26%), change in pattern of sweating (n = 2, 6.5%) and memory impairment (n = 2, 6.5). Symptoms were present in 14.5% of HTT− and in 43% of HTT+ subjects (OR = 4.4, p = 0.0009), and were also highly correlated with repeated EHI events (OR = 21.7, p = 0.0017) (Table 3). 4. Discussion In our study, we attempted to estimate the incidence of recurrent EHI events and to evaluate HTT-based screening as a diagnostic test, using reported recurrent EHI events as reference. We have found an increased incidence of heat exhaustion among heatintolerant individuals, but were unable to determine whether positive HTT result is predictive of recurrent heat stroke (Table 4). The estimated rate of first EHI events in the IDF today is about 0.5–1 cases per 1000 person-years (PY). This is substantially lower than the incidence rate reported recently in the US military — 1.44 (range 0.21–5.39 in different subgroups) cases per 1000 PY.2 In this study, the EHI survivors exhibited a rate of 10.64 cases of
recurrent events per 1000 PY, which appears to be significantly greater than first-event incidence reported by Medical Surveillance Monthly Report (p < 0.001). Similar findings were presented by a retrospective follow-up study of US military recruits, which compared incidence of hospitalizations for EHI among subjects who previously had EHI and were treated as inpatients, subjects who had EHI and were treated as outpatients and subjects who did not have a history of EHI. The incidence rates were 7.5, 1.7 and 0.5 per 1000 PY, respectively.10 The inpatient EHI group may be most similar to our cases, who were all evacuated and treated in medical centers, and their recurrence rates are close to ours. Together with several case reports,11,12 these studies provide a firm basis for the theory that a single EHI event is predictive of additional EHI events. The odds of recurrent events in subjects with a positive result in HTT was almost 7 times higher than for individuals with negative result in HTT, despite the fact that all individuals with positive HTT are instructed to refrain from strenuous physical activity, especially under unfavorable climatic conditions. Therefore, only those who disregard the recommendations were included in the recurrent events statistic. This fact strengthens the validity of the HTT, meaning that in reality, return to duty of those who were identified as HI without an HTT-based screening would have resulted in much higher incidence of recurrent events. Obviously, HTT results were not fully explanatory of the recurrent EHI events. The reason is that HTT is a functional, not a medical diagnostic test. Heat tolerance is defined clinically as an inability to adapt physiologically to exercise in heat.5 It is true that heat intolerant subjects are somewhat restricted in non-routine exercise in extreme conditions, which resembles a pathological or disease state. However, the heat tolerance status is highly correlated with physiological entities, such as aerobic fitness, acclimatization, weight, etc.11,13 Change in one of the latter would lead to increase or decrease of heat tolerance. Therefore, we believe that in most cases heat intolerance is a physiological state, while HTT is a functional test reflective only of the current state. Despite this, HTT result may still be prognostic of future heat tolerance, because other physiological states also tend to be trend-like. For example there are higher chances that an obese or unfit person would continue to be obese or unfit. There may be a small fraction of subjects who are able to modify other physiological parameters and still remain heat-intolerant due to some inherent pathological heat intolerance, but vast majority of subjects are heat intolerant due to inability to modify other modifiable physiological factors.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5 4
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
In this study, the subjects’ demographics and event details were not correlated with HTT results, nor with EHI recurrence. We propose two explanations for this. First and most probable is the sample size — heat tolerance is subject to influence by multiple known and unknown intrinsic and extrinsic factors. Therefore, research of the effect of the event-related factors on heat tolerance would likely require adjustment for multiple confounders and a sample size of hundreds or thousands. This is difficult, however, because EHS is a rare disease. Another, possibly complimentary, explanation is that in our study population, treatment was provided immediately and uniformly, consisting drenching the patient with water (but not cold-water immersion). This decreased variability of the event and treatment details, since none of the subjects were cooled later than 30 min after collapse. The HTT-based RTD protocol should be considered within the context of the corresponding US military policy.14 US army employs a complex protocol which emphasizes initial risk stratification, analysis of contributing factors and clinical follow-up of soldiers until recovery. Soldiers with repeated episodes of heat exhaustion, recurrent heat injury and heat injury with sequelae, and those who had sustained a complex heat stroke (“recurrent, or occurring in the presence of a non-modifiable risk factor”) are referred to the medical examination board (MEB).14 All other cases are subject to continued follow-up (heat injury and heat exhaustion) or to supervised gradual return to normal activity (heat stroke with and without sequelae). The goal of the follow-up is to detect any subjective complaints and symptoms of heat illness or work intolerance, that would preclude return to full duty. This decision-making process is justified by the fact that heat intolerance is defined clinically. In other words, subjects’ ability to tolerate exertion may be sufficient evidence of heat tolerance. In addition, analysis of contributing factors may also provide adequate grounds for medical clearance, because natural predisposition to EHI is not likely in a person who has not experienced any complaints prior to the event, and/or who was dehydrated or sick during that particular incident. Finally, there is no validated alternative to the MEB clinical judgement. However, the US military protocol lacks objectivity and is greatly influenced by the information provided by the soldier. Problems may arise in over-motivated individuals (e.g. professional athletes and combat soldiers) who may experience symptoms of heat intolerance but do not report them for fear of losing their position. Now, after the significant association between HTT results and recurrent heat exhaustion episodes has been established, we believe that the two protocols should be complimentary. Soldiers who sustained an EHS, should undergo HTT about two weeks after the event. Those determined as HT may resume the unrestricted service, while HI individuals should be recommended gradual return to duty. Residual exertional and non-exertional symptoms that were not present prior to the event are actually the only parameter that differs between subjects with positive and negative HTT. They may be regarded as a residual disability that reflects the severity of the event. Alternatively, they are likely to represent the clinical heat intolerance, which is part of the RTD protocol in the US military, as described above. The odds ratio (OR) of recurrent EHI events among subjects with these symptoms was 21.7. This finding highlights the importance of the clinical assessment and follow-up. Our study has several limitations. We used terms such as sensitivity and specificity to quantify the ability of the HTT to predict a future heat stroke/heat injury event. However, subjects with positive and negative HTT were assigned to different levels of activity and were not exposed to the same risk level. Furthermore, the reported occurrence of repeated EHI events is subject to recall bias and lacks the objectivity and reliability that a conventional gold standard measure requires. A major advantage of self-reported EHI recurrence, and the reason we chose this measure rather than
review of medical records, is mitigation of reporting bias: for one documented case of EHS, there were five cases of EHI not captured in the medical records. This is especially true regarding the residual symptoms. On the one hand, most subjects did not seek medical care for these nonspecific symptoms, because they were relatively subtle and did not interfere with daily routine. This would lead to underestimation of their incidence had we relied on medical records. On the other hand, it is an example of reporting bias that unequally affects the HTT+ and HTT− subjects. Those diagnosed as “heat intolerant” (HTT+) would surely be more attentive to any symptoms they experience during exertion or hot weather, than HTT− subjects. Therefore, this finding needs to be validated by additional studies with different design. Small sample size is another major limitation of our study. It was sufficient for estimation of recurrent EHI events, but inadequate for calculation of incidence of such rare occurrence as recurrent HS. In this cohort, only one subject had a registered recurrent heat stroke event, which may not serve as basis for any conclusions regarding HTT validity or even incidence of the recurrent HS. Finally, we were unable to derive any valid conclusions regarding the influence of subject’s baseline characteristics and the primary EHI event and treatment details on heat tolerance or HTT results. Investigation of such a rare yet multifactorial event as EHI requires large sample sizes to adjust for all possible confounding variables. This was not feasible with our study design. Prospective surveillance of larger cohorts of persons who experienced EHI, integrating several other types of predictors in addition to the HTT result, may eventually answer these questions. 5. Conclusion Our study provides quantitative evidence that HTT offers diagnostic utility and may serve as a tool for secondary prevention of EHI. HTT should not be regarded as a medical test, but rather as a functional test. It can be performed multiple times, the last test being most reflective of a subject’s current heat tolerance status. The test provides substantial new information for clinical judgement before return to sports, and enables risk stratification of athletes into high and low risk of recurrent EHI. Practical implications • Heat tolerance (HTT) test is significantly associated with recurrent heat exhaustion events. • It is still not clear whether HTT is predictive of recurrent heat stroke. • The major advantage of HTT is objective EHI risk stratification of over-motivated individuals. Funding There has been no financial assistance with the project. Acknowledgement None. References 1. Casa DJ, DeMartini JK, Bergeron MF et al. National athletic trainers’ association position statement: exertional heat illnesses. J Athl Train 2015; 50(9):986–1000. http://dx.doi.org/10.4085/1062-6050-50.9.07. 2. Update Heat injuries, active component, U.S. Armed Forces. Med Surveill Mon Rep 2015; 22(3):17–20. 3. O’Connor FG, Casa DJ, Bergeron MF et al. American College of Sports Medicine Roundtable on exertional heat stroke—return to duty/return to play. Curr Sports Med Rep 2010; 9(5):314–321. http://dx.doi.org/10.1249/JSR.0b013e3181f1d183.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001
G Model JSAMS-1720; No. of Pages 5
ARTICLE IN PRESS H. Schermann et al. / Journal of Science and Medicine in Sport xxx (2017) xxx–xxx
4. Wallace RF, Kriebel D, Punnett L et al. Prior heat illness hospitalization and risk of early death. Environ Res 2007; 104(2):290–295. http://dx.doi.org/10.1016/j.envres.2007.01.003. 5. Strydom NB. Heat intolerance: its detection and elimination in the mining industry. S Afr J Sci 1980; 76(4):154–156. 6. O’Connor FG, Williams AD, Blivin S et al. Guidelines for return to duty (play) after heat illness: a military perspective. J Sport Rehabil 2007; 16(3): 227–237. 7. Moran DS, Erlich T, Epstein Y. The heat tolerance test: an efficient screening tool for evaluating susceptibility to heat. J Sport Rehabil 2007; 16(3):215–221. 8. Martin DO, Austin H. Exact estimates for a rate ratio. Epidemiology 1996; 7(1):29–33.
5
9. Wallis S. Binomial confidence intervals and contingency tests: mathematical fundamentals and the evaluation of alternative methods. J Quant Linguist 2013; 20(3):178–208. http://dx.doi.org/10.1080/09296174.2013.799918. 10. Phinney LT, Gardner JW, Kark JA et al. Long-term follow-up after exertional heat illness during recruit training. Med Sci Sports Exerc 2001; 33(9):1443–1448. 11. Epstein Y. Heat intolerance: predisposing factor or residual injury? Med Sci Sports Exerc 1990; 22(1):29–35. 12. Keren G, Epstein Y, Magazanik A. Temporary heat intolerance in a heatstroke patient. Aviat Space Environ Med 1981; 52(2):116–117. 13. Lisman P, Kazman JB, O’Connor FG et al. Heat tolerance testassociation between heat intolerance and anthropometric ing: and fitness measurements. Mil Med 2014; 179(11):1339–1346. http://dx.doi.org/10.7205/MILMED-D-14-00169.
Please cite this article in press as: Schermann H, et al. The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport (2017), https://doi.org/10.1016/j.jsams.2017.10.001