Risks of Heat Illness in Athletes With Spinal Cord Injury: Current Evidence and Needs

It has been well documented that spinal cord injury (SCI), especially with resultant tetraplegia or high level paraplegia (T6 and above) (Price and Campbell, 2003), leads to disrupted somatic, sensory and autonomic functions below the level of lesion (Cruz and Blauwet, 2018; Walter and Krassioukov, 2018) and thereby compromised heat dissipation mechanisms (Price and Trbovich, 2018). The current consensus when it comes to exercise and sports in the heat is that athletes with SCI, multiple sclerosis, or cerebral palsy (another neuromuscular disorder affecting thermoregulation) are more susceptible to hyperthermia than able-bodied athletes (Lepretre et al., 2016). Empirical evidence to date, however, is notably limited regarding the assumed risks of heat injury among this cohort (Price, 2016), which could be due to a very small incidence, lack of resources, or failures to collect data (Trbovich et al., 2019).Grobler et al. (2019), for the first time, reported accurate medical records (level III evidence) during the 2015 IPC Athletics World Championships held in the heat (venue wet-bulb globe temperature 24.6-36.0°C). According to their field data, not only was the incidence rate of all illnesses (37.6 per 1000 para athletes) low in comparison to that from outdoor IAAF World Championships between 2009 and 2017 (50.2 per 1000 able-bodied athletes) (Edouard et al., 2019), but also it was explicitly low in heat illness (seven recorded cases of heat illness, of which there was only one case of athlete with SCI). This shouldn’t be surprising though.The discrepancy between hypothesis and observation is that the cause of the elevated body temperature (which ultimately leads to heat illness) during the time course of exercise and sports is not solely attributed to the body’s heat dissipation mechanisms. Rather, the absolute heat production rates and the capacity of the body to transport heat and the environment to absorb the heat generated by the body are the real issue among this cohort (Zhang, 2019). This is akin to what economists called an “identification problem”. For instance, Olympic caliber marathoners reached a V̇O2max of 79.6 mlkg-1min-1 and they ran at an average of 89.7% V̇O2max (resultant oxygen consumption ~71 mlkg-1min-1) during 10-km time trial (Billat et al., 2001). In contrast, Paralympic caliber SCI racers showed considerably lower V̇O2max, 46.4 mlkg-1min-1, as well as substantially lower percentage of V̇O2max, 73.7% (resultant oxygen consumption ~34 mlkg-1min-1) during 25-km time trial (Edwards et al., 2018). Furthermore, the duration of endurance sports is typically longer among able-bodied events. Therefore, given the same body mass, the metabolic energy expenditure and thereby accumulated heat production is clearly lower among para athletes, which is a proximate cause of heat illness.In terms of competition environments, many para sports, such as wheelchair basketball, are held at indoor stadiums where the venue temperature is typically controlled at 19-21°C. Such temperate environments could partially offset the deleterious effects of the autonomic nervous system related dysfunction in thermoregulation. Certain para athletes participating in outdoor endurance events (e.g., T54 wheelchair athletes competing in 5000m, 10000m, marathon, H1-5 para cyclists) could be subject to the negative influence of heat on performance and health when competitions are held in hot and humid environments. However, the nature of these sports allows para athletes to get some thermoregulatory relief in the form of enhanced convection and evaporation from air movement. While Olympic caliber marathoners ran at 18.8 kmh-1 pace (Billat et al., 2001), Paralympic caliber SCI racers showed an average race speed at 30.7 kmh-1 (Edwards et al., 2018), which results in significantly faster air motion from the wheelchair movement relative to the environment. It has been reported that an air velocity of 33.5 kmh-1 could reduce heat storage by 60% compared with a no-wind condition (Saunders et al., 2005). Despite the compromised heat dissipation mechanisms, SCI athletes generally carry less than expected accumulated thermal burden as a result of both relatively lower heat production rate and higher heat convective transfer to the environment. Therefore, the circumstances of SCI sports competition may largely mitigate any compromise of heat dissipation in these athletes, leading to the low incidence rate of heat illness.It is worth noting that the ability to maintain core body temperature within normothermia, while exercising in the heat would be affected by the varying degrees of sympathetic integrity in this cohort. There is consistent reporting of continual increases in core body temperature during rest (Griggs et al., 2019a) and exercise (Price and Trbovich, 2018) among persons with tetraplegia. For example, competitive wheelchair rugby match play (4 × 8-min quarter; ambient temperature, 18.4-20.9°C; relative humidity, 31.1-45.1%) resulted in 39.3°C core body temperature in elite players with a cervical spinal cord injury (C5/6-C7) (Griggs et al., 2017). A popular perception therefore is that athletes with tetraplegia who exhibits greater disruption of evaporation (sweating) and convection (cutaneous vasodilation) should be prepared with appropriate cooling strategies during exercise in the heat provided they demonstrate heightened thermal strain (Griggs et al., 2019b; Trbovich et al., 2019). While this increase in core body temperature, especially if greater than 39.0°C, could be materially alarming, yet trained tetraplegic athletes who whether participate in indoor events (e.g., wheelchair basketball, rugby, fencing), or outdoor sports like H1 para-cycling, exhibit no expected higher incidence rate of heat injury. True exertional heat injury is primarily triggered by a pathological elevation of the core body temperature, usually greater than 40.5°C (Casa et al., 2015). Additionally, severe heat injury including exertional heat stroke could have resulted from excessive endogenous thermogenesis, leading to widespread muscle necrosis and even organ failure (Rae et al., 2008). To date, none of these unfortunate medical comorbidities has been documented in this cohort. Furthermore, another important catalyst for exertional heat injury is prolonged duration of continuous exercise. Athletes with tetraplegia usually compete in much shorter durations compared with able-bodied endurance events such as marathon and triathlon that incur more frequent cases of heat injury. Therefore, despite severe interruption of effector sympathetic pathways in athletes with tetraplegia, the hypothesized higher risks of heat injury (Price, 2016) is not supported by the available epidemiological data.However, the low incident rate of illness including heat-related illness among para athletes (Grobler et al., 2019) should not be celebrated if preventive measures and post-incident medical strategies are not well developed to ensure overall health, especially if events are held in hot and humid environments. No one is immune from heat illness and para athletes are no exception. An alarming report of paratriathlon races held in hot environments (33°C ambient temperature, 35-41% relative humidity, 25-27°C water temperature) has revealed that 78.6% of studied para athletes displaying a core body temperature greater than 39.5°C, including 28.6% of para athletes showing a core body temperature greater than 40.0°C (Stephenson et al., 2019). This exertional hyperthermia was further tied to 57% of studied para athletes experiencing self-reported symptoms of heat illness (Stephenson et al., 2019). Should a framework for early recognition, diagnosis, and treatment of heat illness symptomatology not be well prepared by the governing bodies and event organizers, persistent severe hyperthermia could lead to thermoregulatory collapse, resulting in heat injury in any type of athlete.Across a variety of organized sports that SCI athletes are eligible to compete in, wheelchair marathon, triathlon, and tennis, usually lasting over 60 minutes, result in overall high metabolic heat production, which make SCI athletes vulnerable to heat injury in warm/hot weather. Despite this potential health risk, policy regarding safe competition under heat exposure for SCI athletes have only been implemented by the International Tennis Federation (Regulations for Wheelchair Tennis 2019, September 2019) , which still lacks specific guidelines for the risk management of heat illness.Moreover, it is crucial to understand that SCI athletes display unique patterns of thermoregulatory responses as a consequence of their underlying physiology. Cutaneous temperature sensation has been studied extensively, including in persons with SCI (Price and Trbovich, 2018). In response to the stimulus, nerve impulses regarding the thermal state of the body and the environment are sent to the spinal cord, the major bidirectional connection between the body and the brain, where neural signals are transmitted upwards until they are blocked at the level of the lesion. Reduced afferent input from the insensate portion of the body, especially at those regions (i.e., chest, forearm, hand, finger, and thigh) rich in warm thermoreceptors (Arens and Zhang, 2006), results in altered thermal sensation. Griggs and colleagues (2019a) presented data showing that active persons with SCI undergoing passive heat exposure (37°C ambient temperature; initially 20% relative humidity, with an increase by 5% every 7 minutes thereafter), despite displaying higher mean skin temperature, were not able to perceive the magnitude of thermal strain as measured via thermal sensation. Should athletes present higher level (tetraplegia vs. paraplegia) of SCI, or completeness (vs. incompleteness) of SCI, the resultant thermal sensation in the heat is expected to be further disrupted.In summary, abnormal somatic, sensory, and autonomic functions after SCI present significant challenges for these individuals participating in competitive sports. Despite the overall low incidence rate of heat illness in para athletes, the nature and distinct risks of heat illness of any SCI athlete competing in warm to hot environments underline the need for specific guidelines aimed at improving knowledge and medical support for athletes with SCI or other neuromuscular disorders. Continued research to evaluate heat tolerance among all athletes in all sports is vital to safe sports competition. For the upcoming Tokyo 2020 Paralympics, the environmental conditions are expected to pose a challenge to para athletes’ performance and health (Kakamu et al., 2017). Accordingly, a systematic heat policy addressing appropriate preventive measures (Griggs et al., 2015; Griggs et al., 2019b), early recognition and correct diagnosis (Casa et al., 2015; Trbovich et al., 2019), and effective treatment strategies (Casa et al., 2015) of heat illness would be essential to uphold safe and successful sports participation for this special population.

This article reviews the risks of heat illness in athletes with spinal cord injury.