Wilderness and Environmental Medicine, 16, 47 54 (2005) REVIEW Tibetans at Extreme Altitude Tianyi Wu, MD; Shupin Li, MD; Michal P. Ward, MD From the High Altitude Medical Research Institute, Xining, Qinghai, People s Republic of China (Dr Wu); the Chinese Mountaineering Association, Beijing, People s Republic of China (Dr Li); and the Society of Apothecaries of London, London, UK (Dr Ward). Between 1960 and 2003, 13 Chinese expeditions successfully reached the summit of Chomolungma (Mt Everest or Sagarmatha). Forty-five of the 80 summiteers were Tibetan highlanders. During these and other high-altitude expeditions in Tibet, a series of medical and physiological investigations were carried out on the Tibetan mountaineers. The results suggest that these individuals are better adapted to high altitude and that, at altitude, they have a greater physical capacity than Han (ethnic Chinese) lowland newcomers. They have higher maximal oxygen uptake, greater ventilation, more brisk hypoxic ventilatory responses, larger lung volumes, greater diffusing capacities, and a better quality of sleep. Tibetans also have a lower incidence of acute mountain sickness and less body weight loss. These differences appear to represent genetic adaptations and are obviously significant for humans at extreme altitude. This paper reviews what is known about the physiologic responses of Tibetans at extreme altitudes. Key words: Everest, altitude, Tibetan Introduction On May 29, 2003, people interested in high altitude celebrated Edmund Hillary and Tenzing Norgay s first ascent of Chomolungma 50 years earlier. That achievement was a landmark in high-altitude medicine and physiology. 1 One of the commemorative activities was the 2003 Chinese Chomolungma Expedition. On May 21 between 1:40 and 2:10 PM, 8 climbers reached the summit. Five of them were Tibetans, who were faster reaching the world s highest peak than the Han (ethnic Chinese) climbers. Between 1960 and 2003 in China, there were 13 expeditions to Mt Qomolungma (Everest) organized by the Chinese Mountaineering Association, including 5 international friendship expeditions, in which 80 climbers reached the summit. Among them, 45 climbers (56%) were Tibetan highlanders, and if 4 Sherpas are added, the percentage of summiteers that were Himalayan highlanders was 61%, compared to summiteers who were Han (11 persons [14%]) and the foreign climbers (20 persons [25%]). Impressive evidence indicates that Tibetans have de- Corresponding author: Wu Tianyi, MD, Department of Hypoxic Physiology and Mountain Sickness, High Altitude Medical Research Institute, Xining, Qinghai, 810012, People s Republic of China (e-mail:wutianyiqh@yahoo.com.cn). veloped an unusual degree of adaptation to high altitude. 2 This review deals with some of the clinical and physiological characteristics of Tibetans at high altitude and extreme altitude (above 18 000 feet or 5500 m). Sherpas, who are mainly of Tibetan origin, 3 are renowned for their work capacity at extreme altitude, and Sherpas have reached the summit of Everest on many occasions. 4 Their physiological characteristics can be referenced; less information is available on Tibetan and Han climbers. Various characteristics of Tibetan climbers at extreme altitude are discussed. PHYSICAL PERFORMANCE During the Chinese Everest expeditions (1960, 1975, 1988, 1990, 1992, 1993, 1997 twice, 1998 twice, 1999, 2002, and 2003), Tibetan climbers frequently carried heavy loads without supplemental oxygen and ascended as fast as those with oxygen. The Chinese Mountaineering Party does not completely support oxygenless climbing ; however, during the 1975 Chinese Mt Chomolungma Expedition, climbers used supplementary oxygen, but only during halts and not while actually climbing. 2,5 The expedition was brilliantly successful 9 climbers reached the summit on May 27, 1975. All of the summiteers but one (a Han) were Tibetans. In addition, 6 Tibetan women climbers reached 8000 m: 3
48 Wu, Li, and Ward reached 8200 m, and another 3 reached 8600 m, almost as high as some elite male climbers. 5 The expedition placed a survey tripod on the summit that allowed the altitude to be determined from the north side (the altitude was 8848.13 m 2,5 ) (Figure 1). However, from a physiological point of view, the more remarkable feature of the expedition was the Tibetan climbers ability to perform very heavy work drilling holes in rocks to install a metal tripod with legs as long as 3 m for the trigonometric survey. This work was carried out at an altitude of 8848 m for 70 minutes without supplemental oxygen. 5 The barometric pressure on the summit was about 251 mm Hg, 6 and the alveolar PO 2 was about 35 mm Hg. 7 The Tibetan climbers were on a physiological knife-edge and demonstrated an astonishing hypoxic tolerance. During the same expedition, the female climber Pan- Dou laid down under the tripod on the summit while an electrocardiogram (ECG, lead I) was telemetered to base camp (5154 m) and was noted to be normal 8 (Figure 2). This was the first medical measurement made on the summit of Mt Everest. 2 There is no doubt that humans at the highest point on earth are very close to the limit of hypoxic tolerance. During the 1988 China-Japan-Nepal Friendship Expedition to Chomolungma, a 29-year-old Tibetan climber, Ciren Daorji, was able to tolerate the summit altitude of 8848 m for 99 minutes without supplemental oxygen. 9 Tibetan women climbers tolerate hypoxia, cold, and stress as well as men. Four have summited Chomolungma: Pan-Dou (1975), Gui-Shang (1990, 1999), Jia-Zhen (1998), and Pubu-Drolkar (2003). Gui-Shang is the only female climber to have gained the summit on 2 occasions, and Pubu-Drolkar has climbed to more than 8000 m 3 times. LOW INCIDENCE OF ACUTE MOUNTAIN SICKNESS During the 1990 China-Japan Joint Medical Research Expedition to Mt Anymaqin (6282 m), a survey of acute mountain sickness (AMS) was carried out in mountaineers of 3 different nationalities: the lowland Han who had resided at moderate altitude (2261 m) for more than 10 years, the Japanese who had lived at sea level, and the Tibetans who had been born and lived at 3719 to 4520 m. The diagnosis of AMS was based on the Environmental Symposium Questionnaire. 10 Symptoms of AMS developed during a period of a few hours or days at 3719 m in the Japanese and at 4660 m in the Han. After ascent to 4904 to 5200 m and 5 days at this altitude, the incidence of AMS was significantly different in the 3 nationalities. In the Japanese, it was 55.6% (5/ 9), and in some individuals, it was severe. Two climbers were taken down to 4660 m and given oxygen, and 4 developed peripheral edema (periorbital, facial, or ankle). The incidence of AMS in the Han was 15.5% (2/ 15), but the disorders were mild. No Tibetans (12 subjects) suffered from AMS, even though physical exercise by the Tibetans was much greater than that performed by the Japanese and the Han. 11,12 The Sherpas, like the Tibetans, appear remarkably free from AMS when moving from low to high altitudes. In 1984, Hackett et al 4 reported 25 Sherpas with a history of 47 expeditions, during which they carried heavy loads to extreme altitudes. None had ever had AMS. In addition, although the Sherpas can now move from low altitudes to their homeland quickly by air transport, few cases of high-altitude pulmonary edema have been reported. High-altitude retinal hemorrhages are well-recognized phenomena at high altitude. During the Chinese Chomolungma expeditions, high-altitude retinal hemorrhages were found in 78% (7/9) of Han climbers who ascended to between 5000 and 7500 m but were not observed in 12 Tibetan mountaineers. 13 When Rennie and Morrissey 14 looked for retinal hemorrhages in 15 American climbers and 5 Sherpas at an altitude of 5880 m of Mt Dhaulagiri, such hemorrhages were seen in one third of the American climbers but in none of the Sherpas. While more data are needed to confirm that the Tibetans or the Sherpas are relatively immune from AMS and high-altitude retinal hemorrhage, their reported absence in these highlanders is another sign of excellent hypoxic tolerance. WEIGHT LOSS Humans can live at elevations considerably greater than 5500 to 5800 m for only short periods. Above that elevation, a progressive worsening in their mental and physical condition occurs and has been termed high-altitude deterioration. 15,16 However, Tibetans seldom develop high-altitude deterioration, even when they stay at higher altitudes for a relatively longer period. Loss of body weight is the most objective aspect of high-altitude deterioration. 17 During the 1990 Mt Anymaqin Expedition, after a 19- day trek to 4660 m and a 6-day stay at the laboratory camp near 5000 m, Chinese and Japanese mountaineers experienced an increasing loss of appetite despite a palatable diet. Twelve Han mountaineers lost an average of 2.56 1.11 kg during the trek and 3.37 1.09 kg during residence above 5000 m. Eight Japanese members had a mean 2.2-0.9-kg weight loss. However, 4
Tibetans at Extreme Altitude 49 Figure 1. Chinese climbers (8 Tibetans and 1 Han) drilling holes into rocks to install a metal tripod for a trigonometric survey at 8848 m for 70 minutes without supplemental oxygen. Adapted from Shunan et al. 5 of the Japanese developed AMS with peripheral edema, and the fluid retained lessened measured weight change. Twelve Tibetans had a good appetite and experienced a slight weight gain above 5000 m (average body weight of 59.8 7.2 kg during the trek and a mean of 60.7 4.2 kg at 5200 m over 6 days), even though they were working quite hard. 11,18 Skinfold measurements were used to estimate body fat. Fat loss accounted for 76.3% of the change in body weight during the trek and 54% of the change in body weight above 5000 m in Han members. Most of the weight loss occurred during the early phase of the expedition and represents the shedding of unnecessary fat. 16 At base camp (4660 m), Han members had slightly higher body fat (14.7%) than Tibetans (12.4%). 18 Boyer and Blume 19 reported that during the 1981 American Medical Research Expedition to Everest, the Sherpas lost no weight during the time spent above base camp (5400 m), most at or above 6300 m. By contrast, the western Caucasian members lost 2.7 kg of body weight during the trek to 5400 m and 3.9 kg during residence above 5400 m. Their weight losses were similar to those of the Han mountaineers. QUALITY OF SLEEP During the 1990 Anymaqin Medical Expedition, both the sea level Japanese and lowlander Han climbers at 4660 m developed during sleep severe hemoglobin oxygen desaturation and frequent sleep apnea. 11,20 Subsequently, a sleep study was performed at a simulated altitude of 5000 m 21 on 8 healthy young Tibetans aged 26 7 years and on 6 healthy young Han individuals aged 30.5 4 years. All subjects were living on the Tibetan plateau at an altitude of 4179 m (Zidou, Tibet). Investigations were performed in Xining (2261 m; barometric pressure, 581 mm Hg). Two full polysomnographies were performed in a hypobaric chamber, the first at the ambient altitude of 2261 m and the second during acute exposure to a simulated altitude of 5000 m (barometric
50 Wu, Li, and Ward rose from 21.8 (n/h) at 581 mm Hg to 24.3 at 405 mm Hg in the Han and from 6.8 to 25.8 (n/h) in the Tibetans. Periodic breathing increased from 0.003% of sleep time at 581 mm Hg to 44.6% at 405 mm Hg in the Han but from 0.04% to 53% in the Tibetans. These data indicate that the Tibetans preserved better sleep structure and higher arterial oxygenation than the Han during sleep at a simulated altitude of 5000 m. In addition, the Tibetans developed more periodic breathing than the Han. The data suggest that although ventilatory chemosensitivities play an important role in eliciting periodic breathing, climbers with high hypoxic ventilatory responses (HVRs) can better maintain their oxygenation during sleep by the hyperventilation associated with periodic breathing. 22 Figure 2. During the successful 1975 Chinese ascent of Mt Qomolungma, (a) Pan-Dou on the summit under the newly erected tripod while standard lead I of an electrocardiogram (ECG) was being telemetered to base camp. (b) ECG standard lead I: Pan-Dou from 50-m altitude to 8848 m and back to 50 m: a, 50 m; b, 6500 m; c, 8848 m; d, back to 5000 m; e, 2 months after returning to 50 m; and f, 3 months after returning to 50 m. Adapted from Shunan et al. 5 pressure, 405 mm Hg). Arterial O 2 saturation (SaO 2 ) averaged 92% at an atmospheric pressure of 581 mm Hg and 64.3% at an atmospheric pressure of 405 mm Hg in the Han. SaO 2 averaged 91.9% at an atmospheric pressure of 581 mm Hg and 68.3% at an atmospheric pressure of 405 mm Hg in Tibetans. Total sleep time decreased from 231 minutes at 581 mm Hg to 121.1 minutes at 405 mm Hg in the Han but decreased only from 197.1 minutes at 581 mm Hg to 171.2 minutes at 405 mm Hg in the Tibetans. Rapid eye movement sleep as a percentage of total sleep time decreased from 7.4% of sleep time at 581 mm Hg to 5.7% at 405 mm Hg in the Han and from 8.5% to 5.3% in the Tibetans. Arousals and awakenings VENTILATION AND HVRs Ventilatory function is particularly important during climbing at extreme altitude. Increasing ventilation (Ve) can better maintain oxygenation. During the 1966 Chinese Chomolungma Scientific and Mountaineering Expedition, studies of ventilatory function were conducted at base camp (5000 m). Huang et al 23 reported a similar resting minute Ve, respiratory frequency, tidal volume, and arterial blood gases in Tibetan highlanders and acclimatized Han newcomers. During the 1975 Chinese Chomolungma Scientific and Mountaineering Expedition, studies of HVR and hypercapnic ventilatory response (HCVR) were performed at 5000 m and at sea level. 23 The mean value of the ventilatory responses to hypoxia in Tibetans at sea level was similar to that of lowlanders ( Ve %, 16.5 12.9 vs 24.9 16.6, P.2), indicating that the Tibetans did not have significantly blunted hypoxic ventilatory drives. Moreover, the Tibetans had a CO 2 sensitivity similar to the lowlanders, both at high altitude and sea level, 24,25 indicating that Tibetans also have normal hypercapnic ventilatory drives. Two similar studies were carried out in Lhasa (3658 m), Tibet. Zhuang et al 26 compared 27 Tibetans with 30 acclimatized Han lowlanders matched for age, body size, and extent of exercise training. Between the Tibetan and the Han, resting Ve, SaO 2, and end-tidal PCO 2 (PETCO 2 ) did not differ. However, the Tibetan subjects had a higher HVR (parameter A) than did the Han. Paradoxically, while breathing 70% oxygen, Tibetans had increased minute Ve and decreased PETCO 2 that was not manifested by the Han subjects. Kobayashi et al 27 compared 17 healthy Tibetans with 5 Japanese lowlander trekkers matched in age and physical characteristics who were staying 2 to 3 weeks in Lhasa. The Tibetans had higher Ve, higher PETO 2, and
Tibetans at Extreme Altitude higher SaO 2 values and lower PETCO 2 values at rest than did the Japanese trekkers. The HVR ( Ve/ SaO 2 ) of the Tibetans was not as blunted as that of the Japanese, and the HCVR ( Ve/ PETCO 2 ) in the Tibetans was approximately the same as that in the Japanese. Recently, Beall et al 28 compared the Ve and HVR of 320 Tibetans aged 9 to 82 years with 542 Bolivian Aymara aged 19 to 94 years residing at a comparable altitude (3800 4065 m). They found that the Tibetan resting Ve was approximately 1.5 times higher and that the Tibetan HVR was approximately double that of the Aymara. These studies indicate that Tibetans have a higher Ve and a brisker HVR than acclimatized Han lowlanders and Andean natives, whose HVR and HCVR are similar to the sea level Japanese trekkers. These results fit with the studies of Hackett et al 4 and Masuyama et al, 29 who reported that Sherpas often do not have a blunted HVR, as initially believed. They also found that at rest and during exercise, Sherpas have a higher Ve than do lowland climbers. Climbers with a brisk HVR had greater exercise performance. During the 1981 American Medical Research Expedition to Everest, Schoene et al 30 found that the HVR measured before and during the expedition correlated well with performance high on the mountain. The climbers with the highest HVR reached and slept at higher altitudes. Masuyama et al 31 found that 5 climbers who reached an altitude of 8000 m on Kanchenjunga (8486 m) had a higher HVR than 5 climbers who did not. The Tibetans higher Ve and more brisk HVR would maintain higher SaO 2 and would be an important adaptation for performing well at extreme altitude. LUNG DIFFUSING CAPACITY AND LUNG VOLUME A relatively high lung diffusing capacity probably improves work capacity at very high altitude. During the 1966 Chinese Mt Chomolungma Scientific and Mountaineering Expedition, Huang et al 23 found that Tibetan natives at an altitude of 3890 m had a diffusing capacity for carbon monoxide slightly higher than did acclimatized Han lowlanders (27.6 2.0 ml min 1 mm Hg vs 25.3 1.6 ml min 1 mm Hg). However, limitation of oxygen transport in the lung by diffusion capacity became obvious during exercise at high altitude. 32 Although this limitation had great effects on lowlanders, the Tibetans were affected to a lesser extent. Zhuang et al 33 compared the alveolar to arterial O 2 differences, (A a)do 2, of 10 lifelong Tibetans and 9 Han acclimatized newcomer residents of Lhasa (3658 m) 51 at rest and at 3 levels of exercise. Resting blood gas tension and SaO 2 in the 2 groups were similar. During exercise, the Tibetans had lower total Ve, higher arterial PO 2, and higher SaO 2 than the Han at each level of exercise. The Tibetans ventilated less than the Han lowlanders, and their rate of increase in Ve with increasing work was similar, indicating their oxygen transport was more efficient. During heavy exercise, the Tibetans had a lower (A a)do 2 gradient than did the Han (14 1 mm Hg vs 20 1 mm Hg). The Tibetans had a larger diffusing capacity and a higher work rate during heavy exercise at high altitude than did the Han. The advantageous diffusing capacity of Tibetans may be related to their larger lung volumes. Droma et al 34 studied 38 Tibetan and 45 Han residents of Lhasa matched for age, height, weight, and smoking history. The Tibetan highlanders had larger chest circumference (85 1cmvs82 1 cm, P.05) and larger lung volumes (total lung capacity, 6.80 0.19 L vs 6.24 0.18 L, P.05; vital capacity, 5.00 0.08 L vs 4.51 0.10 L, P.05). Sun et al 35 also compared Tibetan natives and Han immigrants in Lhasa and found that the Tibetans had vital capacities significantly greater than the Han (5808 vs 4280 ml, P.01). Our own data 36 suggest that Tibetan children and adolescents also have significantly higher vital capacities than newcomer Han children and adolescents, both at 3417 m (3.39 0.14 L vs 2.66 0.14 L, P.01) and at 4300 m (3.44 0.17 L vs 2.58 0.12 L, P.01). These data are significant and are compatible with the concept that children born and raised at high altitude develop increased lung volume and diffusing capacity. The larger lung volumes may increase pulmonary diffusing capacity by increasing alveolar surface area and capillary blood volume, thus improving SaO 2 during exercise. The increased diffusing capacity may greatly benefit Tibetan climbers. MAXIMAL OXYGEN UPTAKE A commonly used measure of physical working capacity is VO 2max. A high VO 2max usually identifies persons with greater endurance during a climb. At the moderate altitude of 3658 m, Tibetans have a higher VO 2max than Han newcomers. 33 During the 1986 Qinghai Medical Research Expedition to Mt Anymaqin (6282 m), 37 measurements of VO 2max were made at various altitudes (2261, 4520, and 5620 m) by cycle ergometric exercise in 15 Tibetan natives and 10 Han newcomers. Both groups were young, healthy males and were matched for age, height, weight, and exercise training. The mean value of VO 2max decreases with increasing altitude in the Han. After exposure to 5620 m (baro-
52 Wu, Li, and Ward metric pressure, 374 mm Hg) for 20 days, the VO 2max fell from 49.7 1.2 ml kg 1 min 1 at 2261 m to 36.4 2.2 ml kg 1 min 1 O 2, which was equivalent to 2.6 L min 1 of O 2 for the Han. In contrast, the Tibetans had avo 2max of 48.8 1.3 ml kg 1 min 1, or about 4 L of O 2 per minute, much higher than the Han (P.05). During the same expedition, heart rate, stroke volume, cardiac output, and SaO 2 were determined at rest and during exercise at 3 different altitudes. During maximal exercise at 5620 m, the Tibetans had a higher maximal heart rate than did the Han (184.4 4.4 beats/min vs 148.8 4.6 beats/min, P.001), which was associated with a higher maximal cardiac output (20.96 0.56 L min 1 vs 12.31 0.37 L min 1, P.001) than that of the Han. Indeed, we demonstrated that the maximal cardiac output had a linear relationship with the VO 2max at high altitude (.694, P.01). As the work level was increased from rest to 1200 kg min 1, a progressive fall in SaO 2 occurred in Han newcomers, whereas Tibetans maintained slightly higher levels (Han vs Tibetan at 5620 m, 65.6 0.7% vs 78.8 0.6%, P.01). Our own data indicate that the enhanced VO 2max of the Tibetans was accompanied by a higher maximal Ve 35 and a greater maximal cardiac output, 36 which suggest that cardiopulmonary function at high altitude is closely related to VO 2max. During Operation Everest II, Reeves et al 38 also suggested that impaired cardiac function at high altitude contributes to a decline in maximal oxygen uptake. Some elite high-altitude climbers have only moderately high VO 2max levels at sea level, 39 which is an enigma but apparently an explanation of how Meissner and Habeler were able to reach the Everest summit without supplementary oxygen in 1978. 16 Obviously, the higher maximal heart rate, higher maximal cardiac output, and greater VO 2max in Tibetans indicate superior adaptation to high altitude. COLD TOLERANCE Tibetans are not only better adapted to hypoxia, but they also have an extraordinary tolerance to cold. For example, Tibetans walk barefoot at 4900 m in the snow for many hours without suffering frostbite. This ability may be related to their maintenance of relatively high metabolic rates and consistently high surface temperatures in their extremities. 40 42 However, during the 1990 China-Japan Joint Mt Anymaqin Expedition, a study of finger cooling was carried out. At 4860 m, the mean finger skin temperature during 20 minutes in 0 C water was measured in 7 male Japanese climbers and compared with that of 7 healthy male Tibetans who lived in the area. No significant difference between the 2 groups was found. Perhaps the Japanese newcomers had a temporary increase in plasma norepinephrine. 42 Whether some high-altitude populations such as Tibetans (or Sherpas) have benefited more from natural selection than other high-altitude populations, such as Andeans, Caucasians, and Chinese Han, is an issue in high-altitude physiology and biology. According to the historic, archaeological, and paleontological records, South American Indians probably have lived in the Andes for about 10 000 years. 44 Europeans began to settle high-altitude regions approximately 150 years ago in North America. 44 Paleoliths and microliths consistent with Northern Asia tool cultures of the Upper Paleoliths, dating to approximately 25 000 to 50 000 years ago, have been found at 4500- to 5200-m sites on the Northern Tibetan plateau. 45 The Chinese Han migrated to the Qinghai-Tibetan plateau only in the last 100 years. 46 The Tibetans may have lived at high altitude longer than any other population, which may be why the Tibetans are better equipped to deal with altitude than the Andeans, Caucasians, and Han. Preliminary data from the Tibetans (or Sherpas) at high or even extreme altitude are compatible with the concept that Tibetans are genetically adapted. However, most of these observations are relatively recent, and these findings deserve further investigation. CONCLUSION Even though Tibetan climbers are relatively new to mountaineering and a new emerging force of the Chinese Mountaineering Party, they demonstrate superior physical performance at extreme altitude and appear to be better adapted. The authors hope that this review article will excite interest in further research into the physiologic adaptation and performance of humans at extreme altitude. References 1. Ward MP. Everest 1953, first ascent: a clinical record. High Altitude Med Biol. 2003;4:27 37. 2. West JB. High Life: A History of High-Altitude Physiology and Medicine. New York, NY: American Physiological Society; 1998. 3. Gupta R, Basu A, Pawson IG, et al. Is high altitude a specialized environment in the human case? Analyses of some Eastern Himalayan data. Indian Statistical Institute, Technical Report No. Anthropology/2; 1985. 4. Hackett PH, Reeves JT, Grover RF, Weil JV. Ventilation in human populations native to high altitude. In: West JB,
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