A 20-yr-old cross-country runner presents to your sports medicine clinic to be cleared for return to practice after recovering from an exertional heat stroke (EHS) event during a race 2 wk earlier. He experienced an EHS event at the finish line and was unable to recall or describe any premonitory warning signs. A maximal rectal temperature of 108°F was recorded, but he was successfully treated with cold water immersion. He was subsequently transferred to an emergency room, where he was hospitalized for 4 d and treated for moderate rhabdomyolysis. His peak creatine kinase (CK) was 23,000 IU·L−1, and he was found to have a comorbid acute kidney injury with a peak creatinine of 2.2 mg·dL−1 (normal, 0.6–1.1 mg·dL−1). He denied any illness or supplement use at the time of or before the event. Follow-up laboratories, to include liver functions tests, BUN and creatinine, and CK, were normal. He wants a “green light” to return to practice. However, this was his second EHS event in the last 2 yr.
Exertional heat stroke is a syndrome associated with hyperthermia, potentially complicated by a systemic inflammatory response syndrome and tissue damage leading to multiple-organ failure (1). Unfortunately, although EHS is often preventable, it is one of the top three leading causes of death in both athletic and military populations (2). Core questions in the return to play/duty (RTP/D) decision process are as follows:
- What is the status of the individual's clinical recovery?
- What are the risks of a second event if the individual returns to play/duty (RTP/D) too early?
- What clinical tools, if any, can assist in predicting future risk and managing the individual's status after the RTP/D decision?
Although clear guidelines have been established for successful treatment of EHS, the process of safely returning individuals to play/duty is not well established (3–5). This gap in clinical knowledge is due largely to the practical and ethical challenges of systematically researching potential assessment and treatment approaches in a human population. This special communication reviews current guidance on RTP/D decisions after an EHS event, discusses the current literature and evidence base for addressing heat tolerance, and examines the risks of further EHS events. In particular, we address the potential role of heat tolerance testing in the decision process.
The Problem: EHS and the Risk of Recurrence
Because individuals who sustain an EHS may be at higher risk for a subsequent event, the clinician must contemplate the RTP/D decision especially carefully, since knowledge of the potential risk for a second event is a critical factor. In one of a number of studies of EHS epidemiology and heat tolerance published by the French military (6,7), 15.4% of the 182 military members who were hospitalized after experiencing EHS reported a previous episode of EHS (7). The U.S. military also has extensively tracked exertional heat illness (EHI) epidemiology, for it can dramatically impact operational readiness. In 2016 alone, there were 2536 incident diagnoses of EHI (heat exhaustion and EHS) among active component service members (incidence rate, 1.96 cases per 1000 person years [p-yr]). The overall crude incidence rates of heat stroke and “other heat illness” were 0.31 and 1.65 per 1000 p-yr, respectively. Subgroup-specific incidence rates of heat stroke were highest among men and service members ages 19 years or younger, Asian/Pacific Islanders, Marine Corps and Army members, recruit trainees, and those in combat-specific and “other” occupations (8).
A few studies in the U.S. military have addressed the issue of heat injury recurrence. This is a cornerstone issue because a history of EHS generally requires a medical waiver, which is a barrier to military enlistment. Phinney et al. (9) evaluated the subsequent risk for rehospitalization in Marines who suffered EHI during basic training (BT) as outpatients (n = 872) or inpatients (n = 50) and completed at least 6 months of service. They compared these EHI cases to 1391 noncases, followed them all for 4 yr. The EHI cases had about 40% higher subsequent hospitalization rates in military hospitals than noncases; these differences declined over time, and diagnoses showed little relationship to EHI. Although the authors concluded that hospitalizations for EHI are uncommon during BT, the numbers are too small (five hospitalizations) to provide an accurate comparison.
Nelson et al. recently studied a large cohort of active duty soldiers, observing 238,168 subjects for a total 427,922 p-yr of service. Among clinically focused variables, a prior serious EHI event was associated with a 4.02 greater odds of experiencing a mild EHI event later, and a mild EHI was associated with a 1.77 greater risk of having a serious EHI event later. These observations strongly confirm the likelihood that a prior EHI event is associated with an increased risk of a subsequent EHI event (10).
The RTP/D Decision After EHS
The RTP/D decisions may be the most challenging component of athlete injury management, because it is both complex and demanding (3). Although the final decision is most commonly left to the attending physician, assessments frequently require input and assistance from the athletic trainer, physical therapist, coach, family members, and the athlete. An American College of Sports Medicine (ACSM) guideline on RTP identified several key considerations (3):
- status of anatomical and functional healing;
- status of recovery from acute illness and associated sequelae;
- status of chronic injury or illness;
- whether the athlete poses an undue risk to the safety of other participants;
- restoration of sport-specific skills;
- psychosocial readiness;
- ability to perform safely with equipment modification, bracing, and orthoses;
- compliance with applicable federal, state, local, school, and governing body regulations.
The RTP/D decision-making process requires a fundamental understanding of both the pathophysiology of the EHS and how the affected tissues, organs, and/or body systems recover. Exertional heat stroke RTP/D is especially challenging because our understanding of the pathophysiological processes involved in the development and recovery from EHS is incomplete (11). Current research suggests that most individuals recover completely within a few weeks, especially when patients are treated promptly and cooled aggressively (i.e., cold water immersion) (11,12). However, some patients experience long-term complications that may include multisystem organ (liver, kidney, muscle) and/or neurologic damage, and/or reduced exercise capacity and heat intolerance (12–15). The most concerning complication is the risk of a recurrent event.
As for any other injury, post-EHS RTP/D guidelines should involve a carefully planned, progressively increasing physical challenge closely supervised by an athletic trainer and/or physician. Although clinicians can use basic hematologic parameters and blood chemistries to assess a return to normal function for renal, hepatic, and coagulation disorders, potential exercise-heat tolerance deficits, neuropsychological impairments, and/or the altered fitness/acclimatization status can offer far more complex challenges. The absence of a clear, evidence-based guidance further complicates decision making for sports medicine professionals who must guess at the best decision for an individual who has experienced an EHS event. Moreover, the lack of consistency and clinical agreement can negatively affect not only individual athletes and warfighters but also directly influence athletic success and military readiness.
Nonetheless, current civilian and military RTP/D guidelines are largely based on anecdotal observations and caution (3–5). Most guidelines are simply common sense, requiring an asymptomatic state and normal laboratory findings that target end organs (e.g., liver and kidney) coupled with a cautious reintroduction of activity and gradual heat acclimatization. Although current guidance states that EHS patients may return to practice and competition when they have reestablished heat tolerance, clear clinical definitions of heat tolerance/intolerance are distinctly lacking. Suggested recovery periods vary from 7 d to 15 months before EHS victims return to full activity (4). In addition, both the role of heat tolerance testing and the potential effect of EHS on the thermoregulatory system are areas of scientific question and controversy (2).
While there are presently no definitive, high-level evidence-based guidelines regarding RTP/D, ACSM has published recommendations (5), summarized below:
- Refrain from exercise for at least 7 d after release from medical care.
- Follow up about 1 wk postincident for a physical examination and laboratory testing or diagnostic imaging (biomarkers) of the affected organs. This will address the clinical course of the heat stroke incident.
- When the individual has been cleared for return to activity, he or she should begin exercise in a cool environment and gradually increase the duration, intensity, and heat exposure over 2 wk to demonstrate heat tolerance and initiate acclimatization.
- If return to vigorous activity is not accomplished within 4 wk, a laboratory exercise-heat tolerance test should be considered.
- If the athlete proves heat tolerant, he/she may be cleared for full competition between 2 and 4 wk after the return to full training.
While the ACSM guidance is indisputably useful, many gaps remain. Importantly, the current ACSM process does not address the true risk of recurrence. Core questions confronting the provider with an EHS patient who requires a RTP/D decision include the following:
- What constitutes heat tolerance?
- When is a heat tolerance test required?
What is Heat Tolerance?
Body temperature is determined by the balance between heat production and dissipation. During vigorous physical exercise, metabolic heat production can increase 15 to 20 times above resting levels. If metabolic heat production exceeds heat dissipation, hyperthermia will occur, potentially resulting in a heat-related injury. The mechanisms of heat dissipation include radiation, convection, and evaporation. The integration of these mechanisms is complex, comprising both vasomotor and sudomotor (sweat) activities controlled by a functional thermoregulatory center located in the preoptic/anterior area of the hypothalamus (16).
The ability to sustain workloads under conditions of heat stress varies widely across individuals (9). Under extreme conditions of exertion in the heat, even healthy, well-acclimated, and physically fit individuals will ultimately be unable to dissipate the excessive heat, such that body temperature rises, and a heat injury may ensue. Some individuals may not respond properly to heat stress: their body temperature starts rising earlier and at a higher rate than others under the same conditions. We have defined these individuals as heat intolerant (17). Heat intolerance is therefore the “inability to efficiently dissipate heat as expected by normal average individuals under similar conditions.” The factors that underlie heat intolerance can be categorized as congenital, functional, or acquired (Table).
Heat intolerance has been observed in those who experienced an EHS episode from a few weeks to as long as 5 yr later; thus, heat intolerance may be considered as either temporary or permanent (13). It has been suggested that heat intolerance may reflect inherent or genetic characteristics and possibly a consequence of a previous EHS event (11). In a large-scale survey conducted on participants recruited from South African gold mines, 2% to 4% of the population were found to be heat intolerant yet manifested no apparent disease process (18).
When Is Heat Tolerance Testing Required?
The Heat Tolerance Test (HTT), as originally developed by the Israeli Defense Force, was designed to determine a Service member's ability to RTD after an EHS (13,17). The EHS victims who are treated appropriately and aggressively tend to have uncomplicated recoveries as long as they are otherwise healthy (19). However, the recovery process can become quite complicated if appropriate, optimal care is not provided (2,20). Unfortunately, objective measures or procedures that specifically evaluate the body's ability to handle exercise heat stress (“heat tolerance”) after an EHS have not yet been agreed on. The clinical challenge is thus analogous to RTP/D testing after a concussion, where consensus for an objective test to determine severity or prognosis does not yet exist. However, even where some limitations may be indicated, we believe that a successful HTT should be considered a reliable tool when incorporated into a decision making process that considers other factors impacting an individual's ability to safely return to a pre-EHS lifestyle.
Heat tolerance depends on many factors, both within and outside the individual's control, and no biological markers to assess recovery or future risk for EHS have been identified. The HTT relies on thermoregulatory and cardiovascular function as surrogates. Although the data are currently insufficient to support HTT as a diagnostic test, HTT can still serve as a functional test to assess an individual's responses under the test conditions within a given time frame.
Importantly, the HTT does not account or adjust for factors, such as sex, aerobic capacity, training, acclimatization status, and/or body fat, which have all been put forward as predictors of HTT outcomes. Accurate assessments of an individual's ability to RTP/D can thus differ across and among military and athletic populations, where men and women of varying exercise capabilities must perform similar tasks under similar conditions. Additionally, it is currently impossible to determine whether risk factors following an EHS event were a result of or present before the event.
For the last few decades, the standard practice in the Israel Defense Force (IDF) Medical Corps has been that all EHI patients undergo a standard exercise HTT about 6 wk postevent as part of the RTD process (13,17). Testing is performed during the early hours of the morning, but for practical reasons time of year and patient acclimatization are not accounted for. However, the test is not performed before complete clinical recovery. The IDF HTT criteria are based primarily on changes in rectal temperature (Trec) and heart rate (HR) during the test. Before testing, subjects undergo a general medical examination and assessment of their baseline core temperature, which should be lower than 37.5°C (99.5°F) to be cleared for testing. Subjects are instructed to avoid tobacco and caffeine before the test; not to perform any exercise or drink any alcohol for at least 24 h before the test; to sleep at least 7 h during the night; and to drink 0.5 L of water in the hour before the test. During the test, the subject wears light clothing: shorts and no shirt for men, shorts and sports bra for women. The HTT is performed in a controlled environmental chamber with the temperature set at 40°C (104°F) and a relative humidity of 40%.
Body weight is measured before and after the test. During the test, the subject walks on a treadmill for 120 min at 5 km·h−1 (3.1 mph) at a 2% incline, while core body temperature and heart rate are continuously monitored and recorded (21,22). Additionally, fluid intake and urine output are measured to compute sweat rate in combination with pre/post-body weight. Heat intolerance is defined as a Trec above 38.5°C, or HR above 150 bpm, or when either does not reach a plateau (17). A plateau is consistent with a <0.45 °C·h−1. increase in core temperature, or a Trec/HR ratio (>0.279°C·bpm−1). The Figure presents the Trec dynamics in a heat tolerant and a heat intolerant individual (13). Sweat rate is expected to be 0.5 to 1 L·h−1.
Under the IDF protocol, if the thermoregulatory response is abnormal (~5% to 10% of cases), the soldier is scheduled for a second test that can be performed between 1 and 3 months later, depending on the test results and severity of the prior heat injury. If the second HTT is abnormal according to IDF standards, the subject is defined as heat intolerant and cannot continue service in a combat military unit. After decades of experience and hundreds of cases, the IDF process has yielded almost no indications of heat intolerance after return to duty. A recent study by the IDF military demonstrated that only 6 (4.1%) of 145 subjects who underwent HTT because of a prior EHS experienced recurrent EHI events: 4 (11.4%) of 35 had been classified as heat intolerant and 2 (1.8%) of 110 as heat tolerant (21). Only one of the six recurrent events was diagnosed as EHS and involved a heat-tolerant individual; the other five were diagnosed as heat exhaustions. Based on these data, the sensitivity, specificity, and diagnostic accuracy of the HTT were 66.7%, 77.7%, and 77.2%, respectively.
Importantly, not all HTT results are straightforward. Although the final Trec and HR are classification criteria, the dynamics of these measures, even when below intolerance thresholds, may be important: the “tendency to plateau” in borderline cases may be subjectively interpreted. Therefore, additional measures have been suggested by the IDF Institute of Military Physiology to account for the physiologic dynamics. The first dynamic measure is the Thermal-Circulatory Ratio (TCR) index, calculated as the ratio between Trec and HR, which directly influence the thermoregulatory processes (22). A maximum TCR value of 0.279°C·bpm−1 or less at the end of the 120-min test has been suggested as the cutoff to distinguish between heat tolerance and heat intolerance. The specificity and sensitivity are 89% and 100%, respectively. In addition, a TCR value of 0.320°C·bpm−1 or higher, calculated at 60 min into the test was found to classify heat intolerance with 100% sensitivity and 69% specificity. Although the latter threshold may allow for shortening the HTT for those individuals whose TCR value matches this criterion, the data are currently limited. Overall, the TCR index should contribute to preventing misdiagnosis of heat intolerance (false negatives), with adequate specificity to account for false positives.
The magnitude of increase in Trec during the HTT provides a second dynamic measure to refine the distinction between heat-tolerant and heat-intolerant individuals during HTT (22). An increase of more than 0.45°C in Trec during the second hour of the test can be helpful in distinguishing between a positive and negative test. A value higher than 0.45°C reflects an inability for Trec to plateau during the HTT, which again may help identify heat-intolerant individuals.
It should be emphasized that the IDF HTT criteria were established for relatively young and moderately fit individuals (soldiers). Therefore, older, unfit, ill, and/or obese individuals may need different criteria. Moreover, in many cases, heat intolerance is a consequence of low or inappropriate functional or physiological capabilities, in particular cardiovascular health, and not thermoregulatory dysfunction. However, although HTT results may point to certain thermoregulatory-related pathologies, sound RTP/D decisions do not require criteria for each clinical condition or disease. Heat tolerance test would flag such individuals to exclude from further participation in activities that could compromise their well-being.
The Way Ahead
EHS cases present clinicians with a daunting challenge, particularly when the athlete or warfighter wants to return to vigorous training. Since no consensus regarding a valid tool to expedite this process is currently available, physicians must rely on the patient's postrecovery clinical outcomes and subjective judgments during the progression back to training. Heat tolerance testing provides an intriguing alternative, particularly using the protocol successfully incorporated into the IDF medical corps for many years. Ideally, research will be able to identify molecular markers that reflect both inherent EHS susceptibility and postevent recovery status, and clinicians will pair those laboratory assessments with the dynamics of the HTT. Although the task of discovering such markers is indeed complicated, it is likely an achievable mission.
Importantly, the IDF HTT experience is limited to a specific population with relatively narrow age and physical conditioning range. Moreover, the classification of heat intolerance remains a general and somewhat arbitrary decision that can yield both false-positive and false-negative outcomes. Although HTT's limitations emphasize the need to develop better evidence-based criteria and guidelines to assist clinicians in RTP/D decisions, in many cases, it will be clear that the individual would have difficulty performing the tasks inherent to his/her job if the test criteria are not met. Where an HTT classification as heat intolerant reflects low fitness and/or anthropometric measures rather than inherent thermoregulatory dysfunction, the clinical decision not to allow RTP/D may still be legitimate, for such individuals may not be able to safely meet the rigorous demands of competitive sports or military training.
The RTP/D decision for the athlete or warfighter who sustains an EHS is challenging and requires an attentive and astute clinician. There is no evidence-based, consensus guideline or tool at this time, and estimating the actual risk of recurrence is limited. It is our collective opinion that clinicians should be encouraged to use as many reliable tools as possible: a detailed assessment of the patient's history, clinical biomarkers, and objective measures that may include HTT protocols. As with all clinical decisions, physicians must carefully weigh the data to make the tough calls. We will continue to incorporate the HTT into our challenging clinical decisions and use the data for future changes to assist in updating evidence-based decisions.
The authors declare no conflict of interest and do not have any financial disclosures. The views of this article are those of the authors and are not to be construed as official or as reflecting the views of the U.S. Army, the U.S. Navy, U.S. Air Force, the Uniformed Services University of the Health Sciences, or the Department of Defense.
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