Extreme pregnancy: maternal physical activity at Everest Base Camp

Abstract

High-altitude natives employ numerous physiological strategies to survive and reproduce. However, the concomitant influence of altitude and physical activity during pregnancy has not been studied above 3,700 m. We report a case of physical activity, sleep behavior, and physiological measurements on a 28-yr-old third-trimester pregnant native highlander (Sherpa) during ascent from 3,440 m to Everest Base Camp (~5,300 m) over 8 days in the Nepal Himalaya and again ~10 mo postpartum during a similar ascent profile. The participant engaged in 250–300 min of moderate to vigorous physical activity per day during ascent to altitude while pregnant, with similar volumes of moderate to vigorous physical activity while postpartum. There were no apparent maternal, fetal, or neonatal complications related to the superimposition of the large volumes of physical activity at altitude. This report demonstrates a rare description of physical activity and ascent to high altitude during pregnancy and points to novel questions regarding the superimposition of pregnancy, altitude, and physical activity in high-altitude natives.

INTRODUCTION

Early last century, Sir Joseph Barcroft asserted that the hypoxia associated with intrauterine fetal life was analogous to the hypobaric hypoxia experienced by those standing at the highest terrestrial point on earth, the summit of Mount Everest (8,848 m). During early fetal development, we are physiologically on Everest in utero (2, 17). In other words, fetuses reach a level of hypoxia in utero that rivals the peak of Everest. Yet, the fetus adapts to survive and thrive in this intrauterine environment. However, the superimposition of pregnancy and altitude exposure and/or residency remains largely unstudied (7, 12, 13, 15) with limited information available on the concurrent influence of maternal physical activity.

Guidelines for physical activity during pregnancy from multiple developed countries recommend women without contraindication exercise at a moderate to vigorous intensity for ~150 min/wk (8). These guidelines are based on objective evidence of improved maternal-fetal health outcomes, including reduced risk of gestational diabetes, caesarean sections, and large for gestational age babies (22, 32). However, many international guidelines recommend limiting physical activity to altitudes below 1,800 m in lowlander populations and that adequate acclimatization and reduced physical activity are required for travel above 2,500 m (1, 6, 8, 12). These cautions are based on concerns that lowlanders who exercise at altitude may cause critical reductions in oxygen delivery to the fetus, concurrent with increased maternal oxygen demand during physical activity (7). Native highlanders are not considered in these guidelines. Currently, there is limited information regarding adaptation of lowlanders to altitude during pregnancy, and particularly activity patterns and responses to increased maternal physical activity. Thus, the safety of exercise for lowlander pregnant women has not been established at higher altitudes (>1,800 m). Nonetheless, based on previous estimations (4), ~200 million people worldwide currently live at altitudes above 2,500 m. Many of these populations live in rural and developing countries where occupation and activities of daily living are more physically demanding than in developed countries. However, the impact of prenatal exercise in lowlander or native highlander women residing at altitude is unknown.

In this unique report, we present a series of quantitative measurements of physical activity, sleep behavior, and cardiorespiratory function in a late-term pregnant high-altitude native (Sherpa) woman voluntarily working as a trekking guide during incremental ascent from 3,400 to 5,300 m in the Nepal Himalaya. This is the first known assessment of pregnancy physiology above 3,700 m and physical activity during pregnancy above 1,800 m.

MATERIALS AND METHODS

Participant Recruitment and Ethical Approval

Our participant was a pregnant woman of Sherpa ethnicity working with a family-run guiding company leading a high-altitude research expedition in the Nepal Himalaya in May 2016. The research expedition sought to investigate the responses and adaptations during incremental ascent to altitude. However, this case was not an a priori study on the expedition but rather an opportunity that arose by serendipity because of the participant’s voluntary employment as a trekking guide while pregnant. Upon meeting the participant at 3,440 m and learning of her pregnancy, our intent was to monitor her for safety and make measurements during ascent that we understood would be highly novel. The participant was university educated and fluent in written and spoken English. The intended measurements and protocol were explained via verbal and written communication, and subsequent written, free, and informed consent was obtained before her participation, and remained ongoing throughout the expedition. This study abided by the Canadian Government Tri-Council policy statement on research ethics with human participants and was consistent with the relevant sections of the Declaration of Helsinki. Ethical approval was received in advance, including approval for testing both lowlanders and local Sherpa guides, through the Mount Royal University Human Research Ethics Board (MRU HREB; Protocol 2015–26b) and was harmonized with the Nepal Health Research Council (NHRC; Protocol 96/2015). In May 2017, a second research expedition using the same guiding team and ascent profile was undertaken, and follow-up measurements were obtained in the participant at 10 mo postpartum (MRU HREB Protocol 100012 and NHRC Protocol 109–2017).

Participant History and Demographics

The participant was a late-term pregnant (~31 wk) 28-yr-old primiparous female Sherpa native to the Nepal Himalaya. She received an ultrasound between 5 and 6 mo gestation at Kunde Hospital (~3,800 m), confirming gestational age and approximate due date. The entirety of her pregnancy was spent between 3,800 and 4,200 m. When the participant joined the expedition on May 7, 2016, she was 69.5 kg, 160 cm tall, with a body mass index (BMI) of 27.2 kg/m² and ~31wk gestation during a singleton pregnancy. Her estimated date of delivery was July 10, 2016.

She had no reported serious health concerns throughout pregnancy but self-reported prepregnancy hypotension and ongoing gastritis, which was managed with prescription medications when required (common in rural Himalayan communities; see Ref. 27). She was otherwise healthy with a prepregnancy BMI of 22.8 kg/m². Interview records indicated that her grandparents were born in the Tibet (paternal) and Nepal (maternal) Himalaya. Her mother lived in Thamo, Nepal (3,450 m), during her pregnancy with a highest altitude exposure in utero of 4,250 m. Our participant lived the majority of her life above 3,450 m but lived in Kathmandu from ages 18 to 21 yr. From age 24 to 28 yr she was actively trekking and guiding tourists from Namche (3,440 m) to Everest Base Camp (5,300 m) approximately four times per year. She is an elite competitive endurance athlete and was the first woman from her village to work as a trekking guide and ascend to Everest Base Camp.

Participant Ascent Profile and Experimental Protocol

Figure 1 describes the ascent profile from 3,440 m to Everest Base Camp (5,300 m) and return descent to 3,440 m over 11 days, before she departed back to 3,800 m separately from the expedition team. The portion of the trek reported covered ~65 km with a net gain in altitude of 1,840 m. The participant repeated a portion of this ascent 10 mo postpartum (3,440–4,370 m).

Fig. 1.

Ascent-descent profile and physical activity in a pregnant Sherpa during high-altitude trekking. Line and scatter represent sleeping altitudes during 11 days of trekking. Location of measurements is indicated below each day. Broken line indicates day hike to Everest Base Camp (EBC). Light gray hatched bars indicate objective moderate-vigorous physical activity (MVPA) during pregnancy measured using wrist-worn accelerometry (Actigraph), averaging ~270 min/day throughout. Black cross-hatched bars indicate MVPA values postpartum, ~10 mo later. Values above each location indicate time spent in MVPA in %, with values in brackets indicating postpartum values. Horizontal broken line indicates the North American guidelines for recommended low-altitude MVPA during pregnancy (150 min/wk; ~21 min/day).

Instrumentation and Data Collection

Physical activity and sleep quality were assessed daily, and all other measurements were made the morning following at least one night at each altitude.

Actigraphy.

An Actigraph (Pensacola, FL) triaxial accelerometer (model wGT3X-BT) worn on the nondominant wrist for the duration of the trek collected 24-h physical activity and sleep behavior in 60-s time intervals (epochs). These data indicate the intensity (magnitude of the acceleration) and duration (summed duration of the accelerations) of activity (18). Freedson accelerometer count ranges were used to determine time spent sedentary [<100 counts of movement/min (cpm)], engaging in light activity (100–1,951 cpm), and engaging in moderate to vigorous physical activity (MVPA; ≥1,952 cpm; see Ref. 9). Daily physical activity is reported in both total minutes and percent of total daytime activity.

Actigraph sleep analysis was performed using the Cole-Kripke algorithm, with sleep times determined based on sleep logs. Movement index (MI) was calculated as the number of epochs (60 s) with one or more movements and expressed as a percentage of total time in bed. The fragmentation index (FI) was determined as the number of sleep periods >1 min in duration terminated by movements as a percentage of total sleep time. Sleep fragmentation index (SFI; sum of MI and FI) was used to indicate the total volume of restlessness and fragmentation of the sleep period. The movement density (i.e., volume of fragmentation; SFI) has been previously validated against polysomnography in patients with sleep apnea syndrome in lowland populations (26).

Physiological variables.

Each morning (0600–0800) noninvasive fasted measures were made, including weight (digital scale; Omron model OMRHBF514C), hemoglobin concentration (hemoglobinometer; Hemocue HB201+), and hematocrit (hearinized capillary tube, minicentrifuge; StatSpin, CritSpin microhemaotocrit system, model M960). The participant was then seated in a private and quiet room and provided with white noise through head phones to minimize distraction. Subsequently, respiratory rate and the pressure of end-tidal CO₂ was measured using a portable calibrated capnograph (Masimo EMMA, Danderyd, Sweden) with a personal mouthpiece and nose clip. Heart rate and peripheral oxyhemoglobin saturation (SpO₂) were measured with a portable finger pulse oximeter (Masimo SET Rad-5). Arterial blood pressure (i.e., systolic, diastolic) was measured using an automated blood pressure cuff (model BP786n; Omron) and used to calculate pulse pressure (systolic-diastolic) and mean arterial pressure (1/3 systolic + 2/3 diastolic). The participant filled out the Lake Louise acute mountain sickness (AMS) questionnaire to assess self-reported AMS symptoms (25).

RESULTS

Physical Activity

The ascent profile and Actigraph daily physical activity data (i.e., MVPA) are presented in Table 1 and Fig. 1. The participant was extremely active on all days during the expedition. Mean MVPA was ~270 min/day (20–30% of waking hours). Postpartum data collected at the same altitudes 10 mo later indicated similar, if not slightly lower, levels of MVPA.

Table 1.

Physical activity, physiological measurements, and sleep behaviors collected during altitude ascent/descent in a pregnant (~31–32 wk gestation) high-altitude native (Sherpa)

	Day 1 Namche	Day 2 Tengboche (Deboche)	Day 3 Tengboche (Deboche)	Day 4 Pheriche	Day 5 Pheriche	Day 6 Lobuche	Day 7 Gorak Shep	Day 8 Pheriche	Day 9 Pangboche	Day 10 Khunde	Day 11 Namche
Altitude, m	3,440	3,860 (3,820)	3,860 (3,820)	4,370	4,370	4,910	5,160	4,370	3,985	3,840	3,440
Partial pressure of O2, mmHg	107	101	101	95	95	89	86	95	100	102	107
Physical activity, %/day
Sedentary	18 (21)	16 (16)	11 (24)	12 (26)	14	23	24	17	15	24	18
Light activity	60 (59)	53 (53)	63 (57)	60 (53)	54	45	47	50	55	55	60
MVPA	22 (20)	31 (31)	26 (19)	28 (21)	31	32	29	33	30	21	22
Physiological measures
Hematocrit, %	36	38	*	34	*	40	*	*	*	*	42
Hemoglobin concentration, g/l	140	118	*	114	*	129	*	*	*	*	129
Peripheral hemoglobin saturation, %	94 (95)	92 (92)	93	90 (91)	90	83	83	90	91	92	93
Mean blood pressure, mmHg	85	77	76	80	82	86	86	80	76	79	85
Systolic pressure, mmHg	106	93	91	98	102	105	103	101	93	99	104
Diastolic pressure, mmHg	75	69	69	71	72	76	77	69	67	69	75
Respiratory rate, breaths/min	18 (17)	19 (14)	19	21 (16)	18	19	20	19	16	19	18
$\mathrm{P}\mathrm{E}{\mathrm{T}}_{\mathrm{C}{\mathrm{O}}_{\mathrm{2}}}$, mmHg	23 (23)	19 (24)	19	21 (20)	18	21	21	22	19	18	18
Heart rate, beats/min	67 (71)	69 (64)	69	64 (66)	68	72	69	82	69	66	58
Sleep behavior
Movement index %	16 (17)	24 (18)	16 (8)	21	29	16	21	16	17	21	*
Fragmentation index, %	27 (7)	22 (0)	8 (0)	13	29	33	17	10	21	23	*
Sleep fragmentation index	43 (22)	46 (17)	24 (8)	35	58	49	37	26	37	44	*
AMS score (0–15)	0	0	0	0	0	0	0	0	0	0	0

$\mathrm{P}\mathrm{E}{\mathrm{T}}_{\mathrm{C}{\mathrm{O}}_{\mathrm{2}}}$, pressure of end-tidal CO₂; AMS, acute mountain sickness. Data in parentheses were collected during postpartum follow-up (~10 mo postpartum). Sleep behavior data represent those collected the evening before physical activity and physiological measures. Postpartum data were only collected during the first 4 days of ascent, and the location of testing on days 2 and 3 (Deboche) varied slightly from where pregnancy assessments were carried out (Tengboche). Note that Tengboche and Deboche are adjacent villages within 1 km of each other with only 40 difference in altitude between locations.

^*Pregnancy data that were not available for a given location.

Physiological and Qualitative Variables

Physiological data are presented in Table 1. The participant’s weight ranged between 68 and 70 kg with a BMI of 26.6–27.3 kg/m². While pregnant, respiratory rate ranged between 16 and 21 breaths/min with an end-tidal Pco₂ between 18 and 23 Torr, indicating appreciable hyperventilation compared with postpartum values. This is consistent with normal responses to both altitude exposure and pregnancy. The participant was normotensive with a mean arterial pressure that ranged from 76 to 86 mmHg with no clear change evident with ascent or descent. Similarly, pregnancy heart rate ranged from 69 to 77 beats/min and was similar to postpartum values, counter to the tachycardia that is typical in the third trimester in lowlanders (5). Hematocrit and hemoglobin concentrations during pregnancy were consistent with known Sherpa physiology and normal pregnancy-induced hemodilution (10). There were similar SpO₂ values during pregnancy compared with postpartum (measured up to 4,370 m). Increasing elevation was associated with an appreciable reduction in SpO₂, reaching a nadir of 83% at rest after one night at 5,160 m.

No AMS symptoms were reported at any time point during ascent and descent. The participant reported a qualitative reduction in fetal activity when visiting 5,300 m (i.e., Everest Base Camp), which returned to normal once descending to 4,370 m, but this was not assessed clinically.

Sleep Disturbances

Actigraph sleep behavior data are reported in Table 1. Although the MI, FI, and SFI were relatively unchanged with ascent, the values were indicative of sleep fragmentation during pregnancy. Although unconfirmed in this case, these data suggest the likely existence of obstructive sleep apnea (OSA; see Ref. 23), since her values were consistently higher than the mean of these values for nonpregnant lowlander women during ascent (data not shown). The participant’s values tended to be lower postpartum, suggesting resolution of OSA following pregnancy.

Birth Outcomes and Postpartum Assessment

Birth outcomes were collected via personal communication with the participant. The participant traveled to Kathmandu at ~40 wk gestation because of reconstruction activities at the hospital in Khunde (3,860 m). She gave birth at ~42 wk gestation by emergency caesarean section because of a nuchal cord and associated fetal distress. The female infant weighed 3.2 kg (7.1 lbs) at birth and had no subsequent health concerns. The infant has appeared to have normal growth and development, with the research team meeting the mother and child the following year when follow-up measures were made. However, clinical assessment of developmental milestones has not been performed.

DISCUSSION

A Remarkable Report of Physical Activity during Pregnancy at Altitude

Pregnancy is influenced by a mother’s lifestyle and interaction with her environment. While the responses and adaptations to prenatal physical activity are well described in lowlander populations below 1,800 m (5), little is known regarding high-altitude pregnancy (13, 15). Although millions of high-altitude residents become pregnant each year, the combined impact of pregnancy, altitude, and physical activity has not been described. This case report is the first known characterization of the physical activity and physiological responses of a pregnant high-altitude native resident ascending to 5,300 m.

In lowlander populations, fewer than 15% of pregnant women achieve a minimum of 150 min of MVPA per week [i.e., 2.5 metabolic equivalent of task (MET) hours]. Our participant ascended ~1,800 m over ~65 km in 11 days and accumulated an average of ~270 min of MVPA each day, nearly double the minimum North American weekly guidelines. Kardel (14) previously described activity patterns in elite high-volume endurance athletes training during pregnancy, who accumulated 8.4 h of training and 50 MET hours of MVPA in a week. By contrast, our participant accumulated over 30 h of MVPA in 1 wk during ascent, which we conservatively calculate as 180 MET hours (using 6 METs for MVPA intensity).

Complications in High-Altitude Pregnancies

Pregnancy at high altitude above 2,500 m is accompanied by a host of possible complications, including preeclampsia, birth defects, intrauterine growth restriction, and increased risk of neonatal mortality (15, 21, 24). However, Sherpa/Tibetans have lower rates of pregnancy complications compared with lowlander populations at altitude, including reductions in intrauterine growth restriction and reproductive loss (19). Studies of Tibetan high-altitude natives implicate increases in uterine artery blood flow, which facilitates a larger convective delivery of oxygen, despite a reduced carrying capacity within the blood (i.e., both Sherpa and pregnancy-induced hemodilution; see Refs. 3, 10, and 20). In a retrospective study of Sherpa women who gave birth in Kathmandu, the mean gestational weight gain was 12.8 ± 3.4 kg, and the mean birth weight was 3.46 ± 0.41 kg (29), irrespective of their residence during their antenatal period. The female newborn in our case report weighed 3.2 kg, in line with previous reports.

Prenatal visits among Sherpa women in the Khumbu region have enabled early detection of high-risk pregnancies. Residents of the Khumbu region visit health clinics in either Khunde (3,840 m) or Namche (3,440 m) for antenatal checkup and delivery. Although both facilities are able to conduct a normal delivery, neither has the resources to perform caesarean sections. There have been some rare occurrences of spontaneous abortion and stillbirth in both Sherpas and lowlanders (nonnative) in the Khumbu region, but the causes remain unknown. Unfortunately, no systematic studies on preeclampsia have been performed in Sherpa, but anecdotal evidence from the Kunde hospital (3,840 m) suggests that cases requiring antihypertensive medication and evacuation to Kathmandu for caesarian section are rare. Our participant was relatively hypotensive during pregnancy, and her descent to Kathmandu and subsequent caesarian section were unrelated to factors attributed to high-altitude ascent in the antenatal period.

Recommendations for Physical Activity during Pregnancy

Based on a lack of data, current guidelines recommend limiting altitude exposure and physical activity at altitude during pregnancy in lowlander populations (8, 12) but do not address permanent high-altitude residents. Our report and measurements not only highlight a case of extreme physiology and behavior during high-altitude pregnancy but also highlight a lack of data in these populations. These current deficits in understanding include: 1) physical activity patterns in pregnant women living at altitude, 2) the physiological responses in pregnant women to physical activity in mountainous regions, and 3) the linkages between physical activity patterns and pregnancy outcomes in active high-altitude natives. We know that, in overly sedentary populations (e.g., North Americans), increased maternal physical activity has positive benefits for short- and long-term maternal-fetal health (28), but we do not yet know about the upper limits or potential harms associated with high intensities or large volumes of physical activity.

Physiological Tolerance to Altitude During Pregnancy

Exposure to high-altitude hypoxia is a profound physiological stressor for lowlanders associated with myriad physiological adaptations (30) and risk of development of AMS (16). In contrast, high-altitude ancestry (>2,500 m) is associated with physiological adaptations that promote reproductive success at altitude (3, 10). As a native high-altitude resident, our participant spent the first ~40 wk of gestation living at or above 3,450 m and only descended to 1,400 m (Kathmandu) for the 2 wk before delivery. Physiologically, she demonstrated the following adaptations typically observed during pregnancy: increased ventilation, hypocapnia, and hemodilution. However, resting heart rate did not appear to be significantly elevated with ascent, or during pregnancy, compared with the postpartum state. This is unexpected, and it is unclear if this is typical of Sherpa women or a result of her status as an elite athlete. Her oxygen saturation reduced with ascent similarly while pregnant and postpartum, reaching a nadir of 83% at rest after one night sleep at 5,160 m [pressure of inspired O₂ ($P{I}_{O_2}$) 86 mmHg]. Interestingly, she performed some of the highest volumes of MVPA (~300 min) the day prior during the trek to and from Everest Base Camp [Lobuche (4,910 m) to Gorak Shep (5,160 m) to Everest Base Camp (5,300 m) to Gorak Shep (5,160 m)], likely leading to substantial desaturation during exercise.

West and Barcroft Revisited

Based on alveolar gas samples and oxygen consumption obtained on the summit of Mount Everest, John West speculated that this altitude (8,848 m; $P{I}_{O_2}$ 53 mmHg; ~33% of sea level) may represent the limit of human tolerance (31). However, this speculation may vary between populations (e.g., lowland vs. highland natives), duration of exposure (e.g., extent of acclimatization), and intensity of physical activity while at altitude. Similarly, the threshold altitude/$P{I}_{O_2}$ where placental blood flow and exchange may become insufficient during human pregnancy remains unclear. In addition to the caveats regarding absolute altitude tolerance in humans, altitude tolerance during human pregnancy is likely to be a complex determination, including variations in convective blood flow, placental efficiency, and fetal metabolic rate, which also may vary between populations (e.g., lowland vs. highland natives; see Refs. 3 and 20). Limited data from animal models suggest a threshold of between 13 and 10% $F{I}_{O_2}$ ($P{I}_{O_2}$ 99 and 76 mmHg, respectively) whereby the placenta can no longer adapt to supply adequate resources to support fetal development, resulting in intrauterine growth restriction (11). Interestingly, the equivalent altitude for this threshold is between 4,000 and 6,000 m, roughly the altitude range where our participant spent ∼5 days while performing between ~250 and 300 min MVPA/day. There were no apparent or reported pregnancy- or birth-related complications. This natural experiment leads to many remaining questions regarding 1) activity patterns during pregnancy in high-altitude natives, 2) the influence of physical activity at altitude on fetal well being, and 3) tolerable limits of altitude exposure for pregnancy in low- and high-altitude natives. Unfortunately, no systematic data exist in humans on these questions.

Given the high numbers of pregnancies that occur in mountainous regions, further understanding of not only physiological adaptation to pregnancy at altitude, but responses to physical activity while pregnant at altitude, will serve to inform better clinical management of these populations and aid our broader understanding and guidance related to prenatal maternal physical activity across all populations. Thus, Barcroft’s “Everest in utero” perspective may provide novel insight to the superimposition of multiple metabolic stressors, including pregnancy, high-altitude residency and/or ascent, and maternal physical activity. However, the reality of these superimposed stressors in large populations of high-altitude natives and the perspective afforded us by this rare case report serve as a reminder of the remarkable ability of high-altitude natives to adapt to all aspects of life in thin air.

GRANTS

Financial support for this work was provided by Natural Sciences and Engineering Research Council of Canada Discovery grants [RGPIN-04915 (T. A. Day); RGPIN-06637 (C. D. Steinback)], a Heart and Stroke Foundation of Canada Improving Women’s Heart Health National New Investigator Award (M. H. Davenport), an Alberta Innovates Health Solutions Summer studentship (K. J. Borle), a Women and Children’s Health Research Institute Summer Studentship (B. A. Matenchuk), the Alberta Government Student Temporary Employment Program (E. R. Vanden Berg, E. M. de Freitas, and A. M. Linares), and the Department of Physiology, University College Cork, Cork, Ireland (K. D. O’Halloran).

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the authors.

AUTHOR CONTRIBUTIONS

M.H.D., C.D.S., K.J.B., K.D.O., and T.A.D. conceived and designed research; M.H.D., C.D.S., K.J.B., B.A.M., E.R.V.B., E.M.d.F., A.M.L., and T.A.D. analyzed data; M.H.D., C.D.S., B.A.M., K.D.O., M.T.S., and T.A.D. interpreted results of experiments; M.H.D., C.D.S., and T.A.D. prepared figures; M.H.D., C.D.S., K.D.O., and T.A.D. drafted manuscript; M.H.D., C.D.S., K.J.B., B.A.M., E.R.V.B., E.M.d.F., A.M.L., K.D.O., M.T.S., and T.A.D. edited and revised manuscript; M.H.D., C.D.S., K.J.B., B.A.M., E.R.V.B., E.M.d.F., A.M.L., K.D.O., M.T.S., and T.A.D. approved final version of manuscript; K.J.B., E.R.V.B., E.M.d.F., A.M.L., K.D.O., and T.A.D. performed experiments.