Nutrition-Related Adverse Outcomes in Endurance Sports Competitions: A Review of Incidence and Practical Recommendations

few years, the numbers of competitors in endurance and ultra-endurance sports modalities have increased signi cantly. This type of competition is an extreme challenge for athletes. Therefore, they have an increased the risk of developing medical and nutritional problems. The aim of the work is to estimate the incidence of nutrition-related adverse outcomes in endurance and ultra-endurance sports, considering the variables that in uence them. A critical review was carried out based on the PubMed database, by means of a search strategy based on keywords separated by Boolean connectors. For all the results obtained in a period from 2008 to 2019, a series of inclusion/exclusion criteria was applied to select only the studies that tted the objective of the present study. Results and discussion: Of the 871 publications identi ed, 33 met the inclusion criteria. The adverse outcomes found included exercise-associated hyponatremia (EAH), heat stroke by exertion (EHS), gastrointestinal (GI) problems, dehydration, and hypothermia; the provision of misinformation to athletes about nutrient intake and hydration during competition was identi ed as the main cause. Conclusions: The

objective of the present study. Results and discussion: Of the 871 publications identi ed, 33 met the inclusion criteria. The adverse outcomes found included exercise-associated hyponatremia (EAH), heat stroke by exertion (EHS), gastrointestinal (GI) problems, dehydration, and hypothermia; the provision of misinformation to athletes about nutrient intake and hydration during competition was identi ed as the main cause. Conclusions: The main adverse outcomes in endurance and ultra-endurance sports modalities are EAH, GI inconveniences, and EHS. These problems can a ect the performance and health status of the athlete during and post-competition. Several nutritional guidelines have been suggested that can prevent these adverse outcomes, and it is essential to individualize and adjust the nutritional intake and hydration status according to the characteristics of each competition. Keywords: heat stroke; hyponatremia; dehydration; hypothermia; gastrointestinal diseases; sport; athletic performance 1. Introduction Endurance sport modalities requires competitors to complete a set distance or amount of work in the shortest time possible (time trial) or a maximal amount of work in a xed amount of time [1] with the predominance of an energy metabolism dependent on oxidative processes [2,3]. In this sense the Int. J. Environ. Res. Public Health2020,17, 4082; doi:10.3390 /ijerph17114082 /journal/ijerph

Int. J. Environ. Res. Public Health2020,17, 4082 2 of 19 more important performance variables in endurance sport modalities is the maximal aerobic power, lactate threshold and economy [4] and the duration of the competition are higher than 5 min [1]. Within these modalities, there are ultra-endurance sports, those competitions with a duration of more than 6 h [5]. In recent years there has been a notable and widespread increase in the number of ultra-endurance events (triathlons, marathons, cycling competitions, mountain races, etc.), in which athletes test their physical and mental abilities to the limit [5]. The ultra-endurance competitions pose extreme challenges for athletes, since during them they may be under extreme conditions—for example, due to changes in altitude or extreme temperatures - that increase physical demands and nutritional requirements, as well as psychological conditions that should be regulate to facilitate their performance [5,6]. These competitions require the athletes to focus on di erent factors such as the distance of the competition, the pro le of the tests, or the di erent stages or aspects related to the environment (for example, temperature, humidity, and altitude). Therefore, proper training, individualized nutritional preparation, and adequate equipment are essential to successfully complete the event [7]. Thus, athletes that are poorly prepared for these types of competitions have an increased risk of injuries and illnesses [8]. Among these problems and diseases to which athletes are exposed, those related to nutrition, and hydration must be highlighted [9]. These adverse outcomes refers to all the e ects that can occur to athletes during a competition or training that are related to their nutrition and that a ects the athlete's health. Dehydration (DH) is the problem of greatest concern to date, being caused by inadequate uid intake and/or a signi cant loss of body uid through sweat [10]. However, it should be noted that in some environments overhydration is almost as frequent, being a key stimulus for the development of symptomatic hyponatremia associated with exercise (EAH) [11], which in some endurance and ultra-endurance competitions has a ected as many as 30% of the participants [12]. The appearance of

a signi cant loss of body uid through sweat [10]. However, it should be noted that in some environments overhydration is almost as frequent, being a key stimulus for the development of symptomatic hyponatremia associated with exercise (EAH) [11], which in some endurance and ultra-endurance competitions has a ected as many as 30% of the participants [12]. The appearance of EAH can be prevented and treated if it is detected quickly and appropriate measures are taken, thus avoiding the complications and side e ects that, in extreme cases, can lead to death [13]. The weather conditions constitute a very important factor in endurance and ultra-endurance sports, and may lead to problems for athletes during the competition [14]. During prolonged e ort in a hot condition, exercise hyperthermia cause an important challenge at thermoregulatory level [15]. Therefore, the thermic energy associated to the mechanical work caused by muscle contractions increase body temperature and considering that a higher environmental temperature than skin temperature di cult dissipate the thermic energy produced, exercise in hot conditions can provoke stress heat stroke (EHS) [16], an adverse outcome with important consequences, being a potentially dangerous condition for the athletes and one of the rst three causes of sudden death in sports [17]. At the opposite, another potentially dangerous weather condition is the cold, together with competitions in a low-temperature aquatic environment, since athletes are exposed to frostbite and hypothermia (HT) [18]. Nevertheless, these situations can be minimized by nutrition. Therefore, the dehydration diminish the ability to dissipate body heat and a correct uid reposition during exercise could diminish a possible EHS associated to exercise [19]. Likewise, even in cold weather the active body still sweats and needs uids, and warm uids or at room temperature can help to protect against hypothermia [20]. Gastrointestinal (GI) problems are also very common in endurance athletes, and it can inhibit sport performance and/or recovery. In general, studies suggest that between 30 and 70% of athletes experience gastrointestinal problems during competition [21]. Most gastrointestinal symptoms during exercise are mild and do not carry any health risks, but hemorrhagic gastritis or intestinal

help to protect against hypothermia [20]. Gastrointestinal (GI) problems are also very common in endurance athletes, and it can inhibit sport performance and/or recovery. In general, studies suggest that between 30 and 70% of athletes experience gastrointestinal problems during competition [21]. Most gastrointestinal symptoms during exercise are mild and do not carry any health risks, but hemorrhagic gastritis or intestinal ischemia can be serious medical problems [22]. The most common complaints of the upper gastrointestinal tract include heartburn, nausea, abdominal cramps, vomiting, epigastric pain, and diarrhea. Each of these symptoms may be present in multiple disease states at di erent levels of severity [23]. An adequate nutritional strategy, according to the characteristics of the athlete and the events he/she participates in, will help to reduce the problems described above, in turn allowing the athlete to successfully complete the events [10]. Thus, the aim of this study is to carry out a critical review to

Int. J. Environ. Res. Public Health2020,17, 4082 3 of 19 estimate the incidence of nutrition-related adverse outcomes during competition of endurance and ultra-endurance sports. 2. Materials and Methods The work comprised a descriptive study, involving a critical review, to answer the research question, “what is the incidence of the di erent nutrition-related adverse outcomes that occur in endurance/ultra-endurance competitions and sports?” A structured search was performed in the PubMed database. To nd the largest number of available articles related to the research question, the words of the search strategy were established considering: 1) The descriptors of the Medical Subjects Headings (MeSH); 2) other terms described in MeSH as “entry terms”, which include the terminology prior to the setting-up of the MeSH register; and 3) the terms [tiab] or [Title/Abstract] attached to the “entry terms” or MeSH, in singular or plural, which allow the localization of these terms in the title and summary of the articles. The words and the search strategy were in Appendix. The articles selected for the literature review met the following inclusion criteria: Human studies related to adverse outcomes that occur in endurance and ultra-endurance athletes during competitions. Type of study: cohort-study, case studies or clinical trials. Published in English or Spanish. Articles published from 2008 to 2019. Dates were limited to o er a most recent and updated information according to the scienti c advances in sports nutrition eld, because in the lasts 10 years the number of endurance and ultra-endurance competition events has increased substantially and in parallel, nutritional recommendations for sports people have undergone signi cant changes. Articles in review format, non-human studies, and studies that were not related to athletes or that analyzed sports that did not belong to the endurance or ultra-endurance modalities were excluded. The screening of the articles was carried out independently by two researchers, reviewing the titles and summary, accessing the full text in case of doubt, and agreeing on the inclusion or exclusion of the articles. The article selection protocol for this study was composed of the following variables: Study: authors and year of publication Objective: purpose for

modalities were excluded. The screening of the articles was carried out independently by two researchers, reviewing the titles and summary, accessing the full text in case of doubt, and agreeing on the inclusion or exclusion of the articles. The article selection protocol for this study was composed of the following variables: Study: authors and year of publication Objective: purpose for which the study was carried out. Sample: number of subjects trained for the activities, sports discipline, and sex. Sports competition: type of competition where adverse outcomes detected, place and year of occurrence. Adverse outcomes: type of adverse e ect found. - Incidence: number or % of cases of adverse outcomes su ered by athletes during the competition. - Causes: established after the investigation, triggers of said problems su ered during the competition Conclusions: obtained from the research and reached by the authors themselves. 3. Results The number of publications identi ed was 871. After eliminate duplicate articles (n=6), 865 articles were identi ed for this review, of which only 33 (18 cohort-study articles, 11 case studies, and 4 randomized clinical trials) remained after applying thee exclusion criteria (see Figure).

Int. J. Environ. Res. Public Health2020,17, 4082 4 of 19Int. J. Environ. Res. Public Health 2020, 12, x FOR PEER REVIEW 4 of 22 Figure 1. Flow diagram showing the process used to select the studies. Tables 1–3 describe the variables used to analyze the adverse outcomes that arose during competitions and were reported in the studies used in the review. In this way, Table 1 groups the cohort studies, Table 2 shows the randomized clinical trials, and Table 3 the studies based on case studies. Figure 1.Flow diagram showing the process used to select the studies. Tables–3 competitions and were reported in the studies used in the review. In this way, Table studies, Table

Int. J. Environ. Res. Public Health2020,17, 4082 5 of 19 Table 1.Nutrition-related adverse outcomes in endurance and ultra-endurance competitions and sports, in cohort studies. Study Objectives Sample Sporting Competition Adverse Outcomes Incidence Causes Conclusions Parkkali et al. (2017) [24] -To determine the origin and prevalence of GI problems in participants in triathlon y duathlon -To adopt preventative measures for future events. 239 athletes -80 F -159 M Triathlon and duathlon, The Netherlands (2015) Acute GI illnesses GI illnesses: 73 cases (30.5%) -Stomach pain: 52 cases (71%) -Nausea: 56 cases (77%) -Diarrhea: 43 cases (59%) -Vomiting: 28 cases (38%) Consumption of energy drinks and ingestion of sips of water from the canal in which the swimming event took place. -The rate of appearance of the symptoms in the 2 days after the event suggested a viral origin, which was con rmed by the detection of norovirus in feces samples. -The open-water swimming events were the most probable source of the infection. -No food or drink, except the energy drinks, was associated with the GI illnesses.Meyer et al. (2017) [25] -To evaluate the incidence of diarrhea in a hiking trail. -To determine the seriousness and causes of this GI problem. 737 athletes -281 F -420 M -36 unspeci ed John Muir Trail (JMT), long-distance hiking trail, USA (2014) GI problems: diarrhea. Diarrhea: 121 cases (16.4%) -Mild: 99 cases (82%) -Moderate: 16 cases (13%) -Severe: 6 cases (5%) Fecal contamination of the natural sources of water ingested, together with poor handwashing on the trail. -The incidence of diarrhea is relatively low compared with other long-distance trails in the USA. -By following standard hygiene recommendations and using ltration or treatment methods for the water, the prevalence of GI problems in this type of event could be reduced. Magee et al. (2017) [26] To evaluate the hydration and physical state of university athletes according to the sports and disciplines practiced. 429 athletes Runners: -54 M Cyclists: -7 F -22 M -Runners: 5 cycles of 2 km on uneven terrain. -Cyclists: cycles of 100 km with a rise in altitude of 1000 m. Ireland (2016) DH

could be reduced. Magee et al. (2017) [26] To evaluate the hydration and physical state of university athletes according to the sports and disciplines practiced. 429 athletes Runners: -54 M Cyclists: -7 F -22 M -Runners: 5 cycles of 2 km on uneven terrain. -Cyclists: cycles of 100 km with a rise in altitude of 1000 m. Ireland (2016) DH Total DH: 187 cases (43.6%) -Runners, post-training: 6 cases (12%) -Cyclists, post-training: 13 cases (45%) Lack of knowledge about the liquid requirements and nutritional values of the athletes. -Many athletes consume insu cient liquid during physical exercise. -The opportunities to drink water and other liquids during the events are too limited. -There are more drinks-breaks during team sports; even so, the participants do not consume enough water to avoid DH. Brustia et al. (2016) [27] -To obtain information about the risks involved in mountain sports, so that adequate information can be supplied. -To develop recommendations for health and safety teams. 202 athletes Endurance sports in the French Alps, at 2500 m altitude. (2013) Injuries due to cold and HT. Injuries due to cold: 13 cases (6.4%) Due to HT: 9 cases (4.4%) Exposure to high altitudes for long periods of time, in addition to the use of thermal protection inferior to that used by climbers in winter. -The medical risks and trauma cases produced at high altitude a ected 1% of the participants. -Head injuries and traumas are the most frequent types at high altitude. -Altitude sickness and cold-related injuries are more frequent in summer, during climbing activities. Chl½bkov¡et al. (2016) [28] To determine the state of hydration before and after a competition and the incidence of EAH in ultra-endurance athletes. 113 athletes -25 F -88 M Ultra-endurance in the Czech Republic. (2012–2013) -4 cycle races of 24 h in the mountains. -3 foot races: 2 of 24 h and 1 of 100 km DH and EAH. EAH: 13 cases (11.5%) DH: 30 cases (27%) Loss of sodium in the sweat during the races. Over-ingestion of drinks and greater retention of liquids. -Incidence of EAH greater than that reported previously

Czech Republic. (2012–2013) -4 cycle races of 24 h in the mountains. -3 foot races: 2 of 24 h and 1 of 100 km DH and EAH. EAH: 13 cases (11.5%) DH: 30 cases (27%) Loss of sodium in the sweat during the races. Over-ingestion of drinks and greater retention of liquids. -Incidence of EAH greater than that reported previously in ultra-endurance athletes. -Hyper-hydration before the race did not protect the athletes. -The results obtained indicate that the concentration of sodium [Na + ] in the blood is still the only viable way of determining EAH in endurance athletes.

Int. J. Environ. Res. Public Health2020,17, 4082 6 of 19 Table 1.Cont. Study Objectives Sample Sporting Competition Adverse Outcomes Incidence Causes Conclusions Danz et al. (2016) [13] To evaluate the rates of EAH in an Ironman competition. 1089 athletes -157 F -932 M Ironman championships held in Europe (2005–2013) EAH. EAH: 115 cases (10.6%) -Mild: 95 cases (8.7%) -Severe: 17 cases (1.6%) -Critical: 3 cases (0.3%) Association between: -EAH and F -EAH and those that took longer to complete the events. -EAH has a high incidence among Ironman competitors. -F competitors and those that took 9 h seem to be more susceptible to EAH. Joslin et al. (2016) [29] To determine the number of medical complications related to EHS and the number of competitors who, for this reason, did not complete the race. 326 athletes Ultra-marathons of various stages, in the Amazonian jungle, Brazil (2008–2013) EHS. Heat related problems: 29 cases (8.9%) Incorrect acclimatization before the event and inappropriate rest between stages. Obligatory rests during ultra-endurance competitions in tropical conditions are probably the best way to improve the safety of the athletes and their acclimatization to the heat. Stuemp e et al. (2015) [30] To examine the incidence, the seriousness, and the time of appearance of symptoms of GI problems in athletes who complete the event, and in those who do not. 272 athletes -56 F -216 M Ultra-marathon of 161 km, USA. (2013) GI illnesses. GI symptoms: 261 cases (96%) -Nausea: 157 cases (60.3%) -Vomiting: 92 cases (35.4%) -Stomach cramps: 83 cases (31.9%) -Intestinal cramps: 63 cases (24.1%) -Diarrhea: 58 cases (22.2%) -GI hemorrhages: 4 cases (1.5%) Multifactorial origin, including an altered physiology, mechanical factors, and the intake of water and food before the competition. -GI symptoms were experienced by most of the runners (96.0%). -The results obtained seem to con rm that GI symptoms are very common during ultra-marathons; in particular, nausea, a key problem that can determine whether or not a competitor can complete the event. Cairns et al. (2015) [12] -To examine the incidence of EAH during and after an ultra-marathon. -To evaluate the non-osmotic stimuli

The study reviews nutrition-related issues in endurance sports competitions.