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| ORIGINAL ARTICLE |
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| Year : 2021 | Volume
: 64
| Issue : 5 | Page : 225-231 |
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Visual hallucinations in 246-km mountain ultra-marathoners: An observational study
Ming-Kun Huang1, Kuo-Song Chang2, Wei-Fong Kao3, Li-Hua Li4, Chorng-Kuang How5, Shih-Hao Wang6, Yen-Kuang Lin7, Yuh-Shyan Hwang8, Ding-Kuo Chien9, Yu-Hui Chiu10
1 Department of Emergency Medicine, Mackay Memorial Hospital; Department of Electronic Engineering, National Taipei University of Technology, Taipei; Department of Medicine, Mackay Medical College, New Taipei City, Taiwan
2 Department of Emergency Medicine, Mackay Memorial Hospital; Department of Medicine, Mackay Medical College, New Taipei City, Taiwan
3 Department of Emergency and Critical Care Medicine, Taipei Medical University Hospital; Department of Emergency, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
4 Department of Pathology and Laboratory Medicine, Taipei Veterans General Hospital; Program of Medical Biotechnology, Taipei Medical University, Taipei, Taiwan
5 Department of Emergency Medicine, Taipei Veterans General Hospital; Department of Emergency Medicine, School of Medicine, National Yang Ming Chiao Tung University, Taipei; Department of Emergency Medicine, Kinmen Hospital, Ministry of Health and Welfare, Kinmen, Taiwan
6 Leader Clinic, Taipei, Taiwan
7 Graduate Institute of Athletics and Coaching Science, National Taiwan Sport University, Taoyuan, Taiwan
8 Department of Electronic Engineering, National Taipei University of Technology, Taipei, Taiwan
9 Department of Emergency Medicine, Mackay Memorial Hospital, Taipei; Department of Medicine, Mackay Medical College, New Taipei City, Taiwan
10 Department of Emergency Medicine, Mackay Memorial Hospital; Department of Medicine, Mackay Medical College, New Taipei City; Department of Emergency, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
| Date of Submission | 20-Jun-2021 |
| Date of Decision | 05-Sep-2021 |
| Date of Acceptance | 11-Sep-2021 |
| Date of Web Publication | 27-Oct-2021 |
Correspondence Address:
Dr. Yu-Hui Chiu
Department of Emergency Medicine, Mackay Memorial Hospital, Taipei
Taiwan
 Source of Support: None, Conflict of Interest: None  | 3 |
DOI: 10.4103/cjp.cjp_57_21
Ultra-marathons are typically held over harsh terrains such as mountains, deserts, or other wilderness, and place severe demands on the physical and psychological capabilities of participants. Adventure-race competitors commonly report hallucinations. The goal of this study was to gain insight into visual hallucinations (VHs) during a mountain ultra-marathon. Thirty-one Taiwanese runners who participated in the 2018 Run Across Taiwan Ultra-Marathon, which spans 246 km with an altitude difference of 3266 m and an overall cut-off time of 44 h, volunteered for this study. Self-reported questionnaires on sleep duration, hallucinatory experiences, clinical symptoms of cold- and heat-related illnesses, and the 2018 Lake Louise Acute Mountain Sickness (AMS) Score were recorded prerace, during the summit, immediately postrace, and 3-days postrace. Hematological samples were collected 1 week before, immediately after, and 3 days after the race. Eight ultra-marathoners (six males and two females; seven finishers and one withdrawer) were recruited. Three out of eight (37.5%) subjects (two males and one female) reported experiencing VHs during the last 60 km. Three out of five (60%) lower-ranked subjects experienced VHs. All eight runners slept for <30 min during the race. None of the runners presented with headache either during or after the race to meet the criteria for AMS. None of the runners suffered an abnormal thermoregulatory response or a hypoglycemic episode throughout the ultra-marathon. The changes in blood osmolality immediately postrace were subclinical, despite being statistically significant. Among the three runners with VHs, none presented with severe dehydration or dysnatremia immediately postrace. High-altitude exposure, hyper/hypothermia, dehydration, dysnatermia, or hypoglycemia did not seem to contribute to hallucination onset in our subjects during the event. VHs of ultra-marathoners may be associated with excessive physical exertion and sleep deprivation.
Keywords: Excessive physical exertion, mountain ultra-marathon, sleep deprivation, visual hallucinations
How to cite this article:
Huang MK, Chang KS, Kao WF, Li LH, How CK, Wang SH, Lin YK, Hwang YS, Chien DK, Chiu YH. Visual hallucinations in 246-km mountain ultra-marathoners: An observational study. Chin J Physiol 2021;64:225-31 |
How to cite this URL:
Huang MK, Chang KS, Kao WF, Li LH, How CK, Wang SH, Lin YK, Hwang YS, Chien DK, Chiu YH. Visual hallucinations in 246-km mountain ultra-marathoners: An observational study. Chin J Physiol [serial online] 2021 [cited 2023 Nov 30];64:225-31. Available from: https://www.cjphysiology.org/text.asp?2021/64/5/225/329361 |
| Introduction | |  |
Mountain ultra-marathons (MUMs) place high demands on both the physical and psychological capabilities of runners.[1] Visual hallucinations (VHs), defined as the false perception of an external visual stimulus resulting from a wide variety of underlying etiologies, are commonly reported among ultra-runners.[2],[3] This study focused on the stressors during a MUM event that could contribute to the onset of VHs.
Research articles concluded that when sleep deprivation is combined with excess physical exertion, cognitive function is negatively affected.[2],[4] Other than serious symptoms of VHs, sustained sleep restriction has been shown to adversely affect alertness, vigilance, attention, memory, mood, and executive functioning.[5],[6],[7] Hyperthermia can occur when an athlete is vigorously active in a hot environment and when an athlete remains for too long in a cold environment wherein the body is unable to generate enough body heat to compensate for the heat loss to the environment.[8],[9] A cold or hot environment can also impact physical and mental capabilities during sustained, sleep-deprived exercise.[10],[11] Sleep deprivation itself could disrupt thermoregulation of the body, a process that is crucial for normal cognitive function.[12],[13]
Another important aspect of MUM is that neurocognitive functions can be affected by high altitude.[14],[15] Some mountaineers have reported cognitive deficits, increased reaction times, impaired memory encoding and retention at high altitudes (1500–3500 m), impaired learning, spatial and working memory at very high altitudes (3500–5500 m), and impaired memory retrieval at extreme altitudes (>5500 m).[16],[17] Many climbers exposed to very high or extreme altitudes have reported hallucinations.[18] In addition to these etiologies, ultra-marathoners can experience other causes that can lead to impairment in cognitive function. For example, excessive fluid consumption during endurance exercise can result in exercise-associated hyponatremia (EAH), and insufficient fluid supplementation can lead to dehydration and/or hypernatremia.[19],[20] Athletes who fail to consume sufficient carbohydrate before and during an event can experience a drastic drop in blood glucose to a very low level.[9],[21] All these conditions can negatively affect the runners' cognitive functions.
Cognitive impairment with VHs is a critical issue for mountain ultra-marathoners for both safety and competitiveness. Anecdotal evidence suggests that the VH experienced by ultra-endurance athletes could be due to excessive physical exertion and sleep deprivation. Only two published studies were found to have focused on this causal link, wherein the investigators evaluated cognitive and neurobehavioral performance in multi-day, single-handed sailors,[6] and 168-km mountain ultra-marathoners.[1] However, there are limited objective data that look into the correlation between VHs and actual biochemical changes in the body.
Thus, we designed an observational study and hypothesized that competing in a 246-km MUM may induce VHs in these runners. The goal of this study was to gain insight into VHs during a 246-km MUM and investigate whether stressors such as sleep deprivation, high altitude exposure, hyper/hypothermia, dehydration, dysnatremia, or hypoglycemia, contribute to its onset. To the best of our knowledge, this is the first study to evaluate acute biochemical changes in ultra-marathoners experiencing VHs during a MUM.
| Materials and Methods | | |
The study was conducted in accordance with the Declaration of Helsinki of the World Medical Association. Before conducting the observational study, ethical approval was obtained from the TMU-Joint Institutional Review Board (N201802069), and all participants provided written consent to participate in the study.
Study design and population
Registered runners of the 2018 Run Across Taiwan Ultra-Marathon were contacted by phone to explain the study protocol and to determine their willingness to participate in this study. Runners were excluded if they had a history of heart disease, renal dysfunction, seizure, or syncope of unknown origin. Thirty-one Taiwanese competitors volunteered for this study. The race, which is a 246-km ultra-distance race with an altitude difference of 3266 m, took place between 8 pm April 13, 2018, and 4 pm April 15, 2018, with an overall cut-off time of 44 h. Data from eight runners were included in the analysis.
Subject characteristics, medical history, and marathon/ultra-marathon records were collected using predesigned questionnaires that were filled out by the subjects prerace. The self-reported questionnaires on sleep duration, hallucinatory experiences, clinical symptoms of cold- and heat-related illnesses, and the 2018 Lake Louise Acute Mountain Sickness (AMS) score,[22] including headache, gastrointestinal symptoms, fatigue and/or weakness, and dizziness/light-headedness were recorded prerace, during the summit, immediately postrace, and 3-days postrace.
To assess sleep duration on the course, runners were asked to respond to the following questions (translated to English from Chinese): (1) “Have you taken naps during this race?” (2) “What was the duration of each nap period?,” (3) “Where was it?,” and (4) “What time was it?.” For the investigation of hallucinations, individual interview questions were as follows (translated to English from Chinese): (1) “Have you ever had a hallucination during this MUM?,” (2) “When and where did you experience the hallucination (s)?” and (3) “Please describe the hallucination (s) that you suffered from.”
Blood samples (10 ml) were collected from each subject 1 week before, immediately following and 3 days after the race. The official race records of this 246-km race were obtained to document each subject's performance. All runners were permitted to rest and to freely consume water and food throughout the race, according to standard ultra-marathon regulations.
Laboratory assessment
Blood samples were drawn from the antecubital vein using sterile techniques. All specimens were refrigerated and transported to the laboratory within 8 h of sampling. Plasma glucose (PGlu) and sodium (PNa) were analyzed using Modular Analytics Roche Cobas 702 (Roche Diagnostics GmbH, Mannheim, Germany) with proprietary reagents. Plasma osmolality (POsm) was determined using the freezing point depression method using the Advanced Model 3D3 Single-Sample Osmometer (Advanced Instruments, Norwood, MA, USA).
Track briefing and weather condition
Traversing Formosa (Taiwan), an island with mountain ranges stretching from the north to the south, is a run track from Taiwan's west coast rising to Wuling, Hehuan Mountain (3275 m above sea level) and descending to the east coast. The first 80 km were on wide, flat, well-lit roads, followed by 40 km of alternate ascents and descents. From 113 km onward, there was a 44-km unremitting uphill ascent on a narrow road, followed by an 86-km steady downhill descent. The final 25 km of the race was along rocky cliffs riddled with tunnels.
The participants ran from the general lowlands in the humid subtropical region to the high mountain summit. During the competition, the weather was sultry with a temperature of 26°C at the lowland during the night of April 13. The temperature gradually dropped from 20s to a single digit, with a foggy and windy weather on the summit of Hehuan Mountain on April 14. On April 15, the weather was cool and breezy with a light shower. Air temperature, relative humidity, and wind speed throughout the MUM are shown in [Figure 1] (data provided by the Central Weather Bureau, Taiwan). | Figure 1: Weather conditions throughout the 246-km mountain ultra-marathon.
Click here to view |
Statistical analysis
The Shapiro–Wilk test (P > 0.05) and an inspection of the participants' histograms, normal Q-Q plots, and box plots were used to test the normality of our data. Descriptive results are reported as mean ± standard deviation (SD). Fisher's exact test was applied for categorical data and independent-samples t-test (or Mann–Whitney U test when appropriate) for numerical data to compare demographic differences between runners who experienced VH (VH runners) and those who did not (non-VH runners). Repeated measures analysis of variance with LSD as post hoc was applied to evaluate the biochemical association between the three time points (pre-, immediately post-, and 3-days postrace). Commercially available statistical software (SPSS version 21.0, IBM Corp, Armonk, NY, USA) was used for statistical analysis. Differences were considered statistically significant when the two-tailed P value was <0.05.
| Results | | |
Race details
One hundred and six runners were registered for this race, but 11 runners withdrew, resulting in only 95 runners competing. The average age of the runners was 45.7 years (SD 6.4 years). Eighty-two of the 95 (86.3%) runners were male. Thirty-three out of 95 runners (34.7%) crossed the finish line. Twenty-five of the 33 finishers (75.8%) were male. The average finishing time was 40.6 (30–43.9) hours. Thirty-one out of 95 (32.6%) competitors volunteered to participate in this study and completed the prerace hemodynamic assessment and questionnaire. Eight out of 31 participants (six males and two females) completed the postrace hemodynamic assessment and questionnaire. Seven subjects crossed the finishing line, whereas one runner only completed 240 km and failed to cross the finish line [Figure 2].
Race performance and demographic characteristics
The race duration and running pace of the eight subjects are summarized in [Table 1]. Three of eight (37.5%) subjects had VHs. On average, the VH runners ranked lower than non-VH runners. Runner D described that he saw distorted stones and experienced disorientation in the tunnel between 198 km and the finish line. Runner G stated seeing stones lined up like animals and pictographs of female faces on the tunnel walls between 183 km and 225 km. Runner H felt she was being stalked and saw the shadow of a human figure in the tunnel at approximately 240 km. The characteristics and comparison between the VH and non-VH groups are shown in [Table 2]. There were no statistical differences between the two groups in age, sex, prerace body weight, height, body mass index, years of running marathon, years of running ultra-marathon, training distance, personal best marathon time, personal best 100-km ultra-marathon time, and this MUM finishing time.
Questionnaires and clinical symptoms
The self-reported questionnaires on sleep duration, hallucinatory experiences, clinical symptoms of cold- and heat-related illnesses, and 2018 AMS score were recorded at four different time points: prerace, during the summit, immediately postrace, and 3-day postrace. All eight runners claimed to have <30 min of sleep during the race. No subjects reported headaches during or after the race. No subjects suffered from heat-related illnesses, such as cramps, exertional hyperthermia, heat syncope, or body temperature >40.0°C (104.0 °F) that fulfills the definition of heat stroke. None of the runners had cold injuries, such as hypothermia with core body temperature below 35°C (95 °F), chilblain, trench foot, or frostbite.
Osmotic, sodium, and glucose concentration
POsm, PNa, and PGlu concentrations were measured at three different time points: before the race, immediately after the race, and 3 days after the race. VH and non-VH runners had similar data for the prerace plasma values of POsm, PNa, and PGlu [Table 2]. The exact osmolality values of the VH and non-VH runners are shown in [Figure 3]. POsm (P = 0.032) showed a significant increase in the immediate postrace values compared to the prerace values in the non-VH group. As for PNa concentrations [Figure 4], two non-VH runners expressed hyponatremia (Runner B: Na+ =130 mmol/L; Runner F: Na+ =133 mmol/L) immediately postrace. None of the subjects presented with hypernatremia (Na+ >145 mmol/L) either immediately or 3-days postrace. With regard to PGlu concentrations [Figure 5], no significant hypoglycemia was observed in the eight ultra-marathoners in terms of postrace values. POsm, PNa, and PGlu concentrations did not differ between VH runners and non-VH runners from prerace to all postrace measurements. | Figure 3: Changes in plasma osmolality during the 246-km mountain ultra-marathon. Osmolality levels were measured at 3 different timepoints: before the race (prerace), immediately after (postrace), and 3 days after the race (post-3-d).
Click here to view |
 | Figure 4: Changes in plasma sodium levels during the 246-km mountain ultra-marathon. Sodium levels were measured at 3 different timepoints: before the race (prerace), immediately after (postrace), and 3 days after the race (post-3-d).
Click here to view |
 | Figure 5: Changes in plasma glucose levels during the 246-km mountain ultra-marathon. Glucose levels were measured at 3 different timepoints: before the race (prerace), immediately after (postrace), and 3 days after the race (post-3-d).
Click here to view |
| Discussion | | |
This study presented the following findings: (1) 37.5% of the included subjects experienced VHs during the MUM; (2) all VHs took place in the last 60 km where multiple tunnels are present; (3) all subjects reported to have <30 min of sleep during the race; (4) other stressors, such as high-altitude exposure, hyper/hypothermia, dehydration, dysnatremia, or hypoglycemia, did not seem to contribute to the onset of VHs.
Excessive physical exertion and sleep deprivation
Despite the fact that evidence suggests a strong correlation between sleep deprivation and impaired cognitive function, it is common that ultra-runners tend not to have sufficient sleep to accomplish these endurance races in the allocated time.[1],[4] In a study conducted during the North-Face Ultra-Trail du Mont-Blanc (UTMB) 2013, Poussel et al. reported that among 303 finishers with a mean (SD) race finish time 39.5 (5.1) hours, only 28% of the runners took at least one break for sleep during the race.[23] Martin et al. have also focused on sleep habits and strategies used among 636 French, Italian, and American ultra-marathoners. Seventy-five out of 456 runners (16.4%) reported sleeping during a race that lasted one night, 120 out of 216 runners (55.6%) reported sleeping during a race that lasted two nights, and 88 out of 93 (94.6%) reported sleeping during a race that lasted more than two nights.[24] All eight subjects (100%) with a mean (SD) race finish time 41.1 (3.8) hours in our study reported to have brief naps of <30 min throughout the race. One explanation would be that the 2018 Run Across Taiwan Ultra-Marathon started at 20:00, while UTMB 2013 started at 16:30, and lasted for 2 nights. A 246-km MUM imposed heavy physical and psychological loads on the participants.
Previous studies have linked sleep management strategies to performance in ultra-endurance athletes. Nonsleepers were significantly faster than finishers who slept in ultra-marathons and ultra-cyclings.[23],[25] However, a study by Hurdiel et al. on UTMB 2015 indicated that self-reported sleepiness increased and cognitive performance decreased across the course.[2] In our study, three subjects experienced VHs between early morning and approximately 16:00 after a lack of sleep for two nights. The VHs all occurred in the last 60 km, where multiple tunnels are present. Although there was no statistical difference between VH and non-VH subjects in running speed (P = 0.143), three of five (60%) lower-ranked subjects experienced VHs. Our results are in line with the study by Hurdiel et al. on UTMB 2013, which indicated that acute lack of sleep compounded with strenuous exercise increases vulnerability to VHs.[1] To decrease the risk of accidents due to sleep deprivation and excessive physical exertion, we suggest to take 8–20 min naps on the course based on recommendations from the UTMB organization.[2]
High altitude
Wilson et al. (2009) reported hallucinations in 32% of climbers above 7500 m, while Hüfner et al. (2018) reported hallucinations in 42% (35/83) of climbers at a mean altitude of 7280 m, and Brugger et al. (1999) found hallucinatory experiences in seven of eight (88%) world-class climbers who reached altitudes above 8500 m.[18],[26],[27] It seems that hallucinations, one of the core features of high-altitude psychosis, were most likely to occur at heights exceeding 7000 m above sea level. It should be noted that in the study by Hüfner et al., they also observed that extreme hallucinations cannot be fully explained as a side effect of altitude sickness or brain swelling.[18] In this study, these mountain ultra-marathoners were only exposed to 3275 m, and none of the eight subjects presented with headaches either during or after the race to meet the criteria of AMS. This implies that VH is a separate condition that cannot be linked to AMS.
Hydration status
Dehydration is a common physiological state that can have profound implications on exercise performance, and exceeding 2% in Posm (∼5 mOsm/kg) is consistent with negative physiologic outcomes.[28] Although Cheuvront et al. recommended that a POsm value of 301 ± 5 mOsm/kgH2O be used clinically as the threshold of dehydration, previous data have shown that a POsm value of 301 ± 5 mOsm/kgH2O represents a body mass loss of ~4.5% in healthy, young males; a marked level of dehydration is hardly a threshold for dehydration.[28],[29] In our study, there were only two non-VH runners who had POsm values >300 mOsm/kgH2O (Runner A: POsm = 307 mOsm/kgH2O; Runner C: POsm = 304 mOsm/kgH2O). Interestingly, three of five (60%) non-VH runners presented a >5 mOsm/kg increase in POsm (Runner A: 5.1% increase; Runner C: 4.8% increase; Runner E: 5% increase) and only one of three (33.3%) VH runners had a >5 mOsm/kg increase in Posm (Runner D: 2.1% increase) immediately postrace. Our results suggest that such a level of dehydration is not related to VHs in mountain ultra-marathoners.
Environmental temperature and hyponatremia
Extreme ambient temperatures and electrolyte imbalances can also induce cognitive impairment.[11],[30],[31] In 2012, Knechtle et al. reported that approximately 8% of competitors in the “Swiss Jura Marathon,” a MUM held in a temperate climate, developed EAH.[32] Conversely, Lebus et al. investigated the “Rio del Lago 100-Mile Endurance Run,” held in 2008 in a hot-summer Mediterranean climate and reported an EAH rate of over 50%.[33]
The race route of “2018 Run Across Taiwan Ultra-Marathon” has a drastic change in elevation. This race was held in the sub-tropical and mountain climate zone with outdoor temperatures, in °C, ranging between single digits to the high 20s. None of the subjects reported any body temperature abnormalities. Notably, EAH was defined as a PNa level of 135 mmol/l or lower.[20],[34] Two of our eight subjects (25%) met the criteria of EAH with immediately postrace PNa levels of 130 and 133 mmol/l, respectively. However, clinical symptomatology of EAH is generally expected with a PNa concentration of <120 mmol/L and symptoms at a PNa concentration >125 mmol/L are rare. These two hyponatremic subjects did not experience VHs, which could imply that there was no correlation between VHs and EAH.
Hypoglycemia
Carbohydrates are the main energy source in endurance athletes. The general estimation is that an ultra-marathoner burns 47–71 kilocal per km in a race. However, humans can only store approximately 2000 cal of glucose and absorb only 240–280 cal per hour.[20],[35] Over time, runners are likely to exhibit a net calorie loss that will cause a decrease in blood glucose levels, resulting in exercise-induced hypoglycemia. This is most commonly seen in distance events lasting more than 4 h, wherein endurance athletes can experience a dramatic alteration in their level of consciousness.[21] From our data, the PGlu levels of all eight subjects did not fall to a level that would result in hypoglycemia and VH.
This study has some limitations. First, the relatively small sample size and observational design of the study limits the capability of producing a statistically powerful analysis. However, MUM is an extreme sport with far fewer participants than traditional marathon races. We believe our study is of noteworthy importance. Second, the questionnaires were on a self-report basis without specific electronic devices to record the subject's sleeping duration. Finally, hallucinations were diagnosed based on runners' memory. Only two of eight (25%) subjects had witnessed hallucinations. However, ultra-marathoners may forget that they experienced a hallucination because they are only partially conscious during some parts of the race. To date, no prior literature has explored acute biochemical changes in ultra-marathoners experiencing VHs during a MUM. Our data, although far from conclusive, provides additional information regarding the hallucinatory phenomenon in long-distance running sports. We anticipate that further data on ultra-marathons could provide additional insights into this issue.
| Conclusion | | |
In conclusion, we report that VHs of mountain ultra-marathoners may be caused by excessive physical exertion and sleep deprivation. The results suggest that AMS, hyper/hypothermia, dehydration, dysnatremia, or hypoglycemia are not associated with VHs in runners during the 246-km MUM. Hence, athletes should actively take breaks and manage their sleep during MUMs.
Acknowledgments
We thank all the ultra-marathon runners who participated in this study and all the doctors, nurses, and emergency medical technicians who provided professional care at this ultra-marathon race. We also express gratitude to the Chinese Taipei Association of Ultra Runners, all of which assisted at the ultra-marathon event.
Financial support and sponsorship
This study was supported by Mackay Memorial Hospital, Taiwan (MMH107129/11061).
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2]
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