Considerations for the Pregnant Endurance Athlete

Abstract

It is well known that moderate exercise during pregnancy benefits maternal and fetal well-being. The benefits of more vigorous exercise for pregnant women are less clear. The boundaries of safe exercise during pregnancy remain a matter for continued research, which is important to the growing number of female athletes who plan on becoming pregnant. The purpose of this article is to discuss the existing research related to the physiological concerns of the pregnant endurance athlete specifically. Because endurance training includes prolonged and repetitive exercise bouts at varying intensities, topics will include the effect of high-intensity exercise on uterine blood flow and thermoregulation, metabolic, and musculoskeletal changes in pregnancy.

INTRODUCTION

Guidelines for exercise during pregnancy used to be quite conservative. In 1985, the American College of Obstetricians and Gynecologists (ACOG) recommended pregnant women limit their exercise heart rates (HRs) to 140 bpm and the overall duration of their exercise to 15 minutes (¹). In addition, women who were not active before their pregnancy were discouraged from beginning an exercise program. Since that time, research has shown that such limitations are restrictive and potentially counterproductive. As research on exercise and pregnancy grew in the 1980s and 1990s, the benefits and safety of exercise started to become clearer (⁵¹). We now know that many types of exercise can be beneficial for a healthy pregnant woman. Moderate exercise throughout pregnancy helps women maintain recommended gestational weight gain (GWG), reduces the likelihood of developing gestational diabetes mellitus (GDM) and hypertension, and could have positive effects on childbirth outcomes (^19,37,38,59). Regular moderate-intensity exercise during pregnancy also has positive effects on birth weight and infant neuromotor skills (^41,59).

The benefits of more vigorous exercise for pregnant women are less clear. Identifying the boundaries of safe exercise during pregnancy remains a matter for continued research, and such research is important to the growing number of female athletes who plan on becoming pregnant. Unfortunately, the guidelines for exercise during pregnancy are not intended for the athletic population and there is a paucity of research on the effect of strenuous exercise on maternal and fetal well-being. The safety of training for competitive sport and/or competing in sport while pregnant is not well understood.

Training for endurance sport presents some unique challenges to the pregnant athlete. Typically, endurance sport training involves long duration and moderate-intensity to high-intensity bouts of exercise (^21,33). The current ACOG guidelines for healthy pregnant women, updated most recently in 2020, are now similar to the exercise recommendations for the general population—150 minutes per week of moderate-intensity exercise (^2,58). The moderate intensity of exercise recommended is equivalent to brisk walking—an activity far less demanding than the training bouts of avid or elite endurance athletes. The recommended duration of 150 minutes per week or 30 minutes, 5 times a week is also much shorter than a typical endurance training session. Thus, endurance sport training does not fit well with the current guidelines for duration or intensity. For women who want to do more than the recommended exercise, the United States Department of Health and Human Services (USDHHS, 2018) guidelines state, “Women who habitually engaged in a vigorous-intensity aerobic activity or who were physically active before pregnancy can continue these activities during pregnancy and the postpartum period” (58, p. 9). At the same time, however, the most recent 2020 ACOG guidelines caution that “More data are needed from athletes who may exert beyond the accepted 'vigorous' definition of up to 85% of capacity, and it is possible that there is an absolute level of intensity (or duration, or both) that exists, and if exceeded, could place the fetus at risk” (2, e180).

Owing to the inherent risks to both the mother and the fetus involved in the process of identifying how much is too much exercise, there is limited scholarly information available. The purpose of this study is to discuss the existing research related to the physiological concerns of a pregnant endurance athlete. Because the number of female endurance athletes is growing, more women will need information related to training during pregnancy (^26,29). Understanding how physiological adaptations to pregnancy meet with exercise responses can clarify the benefits and risks of endurance sport training. Topics will include issues related to endurance training including the effect of high-intensity exercise on uterine blood flow and thermoregulation, metabolic, and musculoskeletal changes in pregnancy.

EFFECT OF HIGH-INTENSITY EXERCISE ON UTERINE BLOOD FLOW

During pregnancy, there are vast changes to the cardiovascular system that occur for the body to meet the increased metabolic demands and circulatory requirements of the mother and fetus (⁴⁹). These changes begin as early as 5 weeks and most persist throughout pregnancy and in some cases, into the postpartum period (^10,49). In the first trimester, an increase in systemic vasodilation causes a 35–40% decrease in peripheral resistance (⁴⁹). The decrease in vascular tone is likely related to elevated estrogen levels and the associated increase in the vasodilator nitric oxide (^20,61). In addition, the hormone relaxin, which circulates during pregnancy, has a vasodilatory effect on the endothelium (⁵). The systemic vasodilation that occurs during pregnancy is related to the decrease in resting blood pressure (BP) (5–10 mm Hg), which occurs at 6–8 weeks and peaks during the second trimester (³⁹).

The decrease in peripheral resistance reduces afterload and contributes to an increase in resting cardiac output (Q) by as much as 45–50% (^10,28,45,49). The substantial elevation in resting Q is also related to the changes in HR, stroke volume (SV), blood volume (BV), and ventricular remodeling that occur during pregnancy. The 10–20 bpm increase in resting HR occurs progressively throughout pregnancy and peaks in the final trimester (^16,49). The augmented HR is mediated by a reduction in parasympathetic/vagal tone (⁴). Resting SV also increases by as much as 10% up until the second trimester further contributing to the elevation in Q (⁴⁹). Total BV increases by 45–50% within the first 2 weeks of pregnancy. The change is a result of increases in both plasma volume (PV) and red blood cell (RBC) mass. Plasma volume expansion occurs because of enhanced renin-angiotensin system activity. Specifically, the elevated levels of estrogen seen during pregnancy are associated with higher levels of renin. This change leads to more angiotensin that stimulates the release of aldosterone. Aldosterone increases cause sodium and water retention and contribute to BP maintenance and the increase in PV. In addition, relaxin enhances the activity of antidiuretic hormone further contributing to PV expansion (⁴⁹). A 40% increase in RBC mass occurs because of higher levels of erythropoiesis (⁴⁹). The increased BV as well as the increased vascular distensibility and decreased aortic stiffness due to systemic vasodilation create a volume overload on the heart. This volume overload leads to increases in left ventricular wall thickness and wall mass (³⁵).

Despite the dramatic changes to the cardiovascular system that occur during pregnancy to ensure adequate fetal circulation, concerns still exist regarding fetal well-being during strenuous exercise. During aerobic exercise, there is a redistribution of blood flow from the splanchnic region to skeletal muscle to meet the metabolic demand. Skeletal muscle may receive 80–90% of cardiac output during high-intensity exercise (³⁰). Because blood flow to the skeletal muscle is preferred during exercise, researchers concerned with fetal circulation have investigated the effect of exercise on uterine blood flow in pregnancy. Early research in animals did find a compromise in uterine blood flow during exercise to exhaustion (¹⁴). Interestingly, fetal well-being was preserved because of the maintenance of uterine oxygen uptake. The findings in human studies are equivocal with some researchers reporting no change in uterine blood flow (^22,42,46) and others reporting decreased uterine blood flow with no associated fetal compromise (^43,54,56). A systematic review by Skow et al. (⁵⁰) concluded that acute or chronic exercise does not negatively affect fetal HR and uterine blood flow. The results of these studies confirm that the current ACOG recommendations for exercise in pregnancy, which suggest that moderate exercise is safe for both the mother and the fetus, are appropriate. Unfortunately, the effect of exercise above the recommended intensities is not as well studied.

A typical bout of exercise for an endurance athlete may include efforts from lactate threshold to V̇o₂max (²⁵). Because the lactate threshold of some trained endurance athletes is above the current ACOG guidelines, it is critical to understand more about high-intensity exercise in pregnancy (⁴⁰). To determine whether strenuous exercise compromises fetal well-being, Szymanski and Satin (⁵⁵) investigated fetal responses during a graded exercise test in healthy pregnant women. Fetal HR (FHR), as well as umbilical and uterine artery flow after exercise to volitional fatigue in nonexercisers and regularly active and highly active women, was measured. In a subset of highly active women, postexercise FHR was depressed and uterine and umbilical Doppler indices were elevated—indicating resistance to flow. The changes were transient (average 2:37 minutes) and fetal well-being was reassured thereafter. The normal FHR response to maternal exercise is a slight increase likely related to a decrease in blood flow. A decrease in FHR (<110 bpm) is a marker of fetal distress (⁵⁰). The effect of transient fetal bradycardia is not well understood and thus Szymanski and Satin (⁵⁵) urged caution for athletes who may want to push themselves beyond the recommendations for moderate intensity. In a similar study, Salvesen et al. (⁴⁸) examined the effect of strenuous exercise on fetal well-being and uterine volume blood flow in highly trained, Olympic-level endurance athletes. The pregnant women exercised on a treadmill for intermittent bouts at 60–90% V̇o₂max. Uterine volume blood flow decreased during exercise by 40–75%, but FHR remained in the normal range (110–160 bpm) for subjects who exercised below 90% of maximal maternal HR (MHR). In women who exercised above 90% of MHR, transient fetal bradycardia and higher resistance to uterine flow occurred. Salvenson et al. (⁴⁸) concluded that because fetal well-being can be compromised after exercise above 90% of MHR in highly trained women, exercise intensity should not exceed 90% MHR with associated decreases to uterine blood flow.

To continue training safely while pregnant, endurance athletes may wonder what the boundaries are for exercise intensity. It seems that fetal well-being is reassured when exercise is performed at moderate intensities (⁵⁰). Although more research needs to be performed to completely understand how higher-intensity exercise affects pregnancy, some research indicates fetal compromise above 90% MHR. The conclusion may be particularly interesting to the pregnant endurance athlete as the data suggest that even with a high level of fitness (subjects were Olympic and world champion endurance athletes), and likely associated enhanced prepregnancy total BV, fetal circulation was still compromised at high exercise intensities.

THERMOREGULATION CHANGES IN PREGNANCY

Fetal temperature is based on maternal temperature, fetal metabolism, and uterine blood flow (^10,36). Fetal temperature is 0.5°C above maternal temperature because of heat production from ongoing fetal metabolism (³⁶). Animal studies have concluded that when maternal core temperature rises, the transplacental maternal-fetal temperature gradient, which helps fetal heat dissipation, may be compromised (⁵³). The results of various animal studies have led the scientific community to conclude that maternal core temperature should not exceed 39°C or increase 1.5–2.0°C from the baseline because of potential teratogenic effects (^3,47,53). The fetal neural tube is the most vulnerable to compromised thermoregulation. Because fetal neural tube development occurs 35–42 days from the last menstrual period, it is recommended that pregnant women not exceed core temperatures >39°C or 1.5°C–2.0°C from the baseline particularly early in pregnancy (^3,10). Indeed, the ACOG guidelines state that pregnant women should exercise in thermoneutral environments and avoid prolonged exposure to heat (²).

During exercise, core temperature rises as a result of metabolic heat production and external environmental conditions. Thermoregulation during exercise requires a constant balance between this internal heat source and external, environmental heat sources. An increase in core temperature is sensed by the cells of the anterior hypothalamus, which initiates the thermoregulatory response. Heat dissipation mechanisms include peripheral vasodilation and evaporation. Peripheral vasodilation enhances blood flow so that heat can be transferred from the core to the periphery. Once there, the heat can be removed through the evaporation of sweat. The increase in sweating moves water from the vasculature to the eccrine sweat glands, which may decrease PV as well (⁶⁰). Thus, during exercise, the cardiovascular system has competing demands—the need for thermoregulation and the need for muscle metabolism (⁶⁰). Endurance athletes have an advantage in the heat because aerobic training improves heat dissipation because of an increased sweat response and increased PV and Q (¹²). Pregnancy is associated with improved heat dissipation as well. The mechanisms for the enhanced heat dissipation are in part related to the increase in PV and decrease in vascular tone found in pregnancy and the associated improvements to skin blood flow circulation (¹⁰). Unfortunately, the threat to the fetus is most concerning in the early days of pregnancy, and these adaptations progress as pregnancy advances.

In nonpregnant women, core temperature has been found to increase to 37.3°C during light exercise (50% V̇o₂max) and 38.5°C during moderate exercise (75% of V̇o₂max) (⁵³). The combination of hot environmental conditions and increased intensity and duration can cause core temperature to increase more—marathon runners, for example, can tolerate core temperatures above 40°C (¹³). Because inducing heat stress in pregnant women can be harmful to fetal well-being, less is known about thermoregulation during strenuous exercise in pregnancy. Soultanakis et al. (⁵²) did examine the effect of prolonged exercise on core temperature although the effort was considerably lower than a typical bout of exercise in endurance-trained individuals. Specifically, Soultanakis et al. (52) examined the effect of 60 minutes of exercise at 55% V̇o₂max on core temperature. Pregnant subjects demonstrated effective thermoregulation as core temperature did not increase by more than 0.6°C. This suggests that pregnant women can thermoregulate effectively at low-to-moderate intensities for up to 60 minutes. Similarly, a systematic review by Ravanelli et al. (⁵²) concluded that pregnant women could exercise for as long as 35 minutes at 80–90% of maximum MHR in warm or thermoneutral conditions without surpassing the teratogenic temperature threshold (⁴⁷).

It is disappointing, but understandable that there is a lack of research investigating the effect of both high-intensity and long-duration exercise on thermoregulation in pregnancy. For ethical reasons, the information we do have is mostly derived from animal studies. Because of the potential adverse effects on fetal development, it is recommended the pregnant endurance athlete follow the ACOG's guidelines and exercise in thermoneutral environments. In addition, they should avoid prolonged heat exposure and should be mindful of proper hydration during exercise to maintain effective evaporative cooling. The practice of other types of exercises that affect thermal balance—namely, “hot yoga” or similar—is contraindicated. Because the adverse effects of heat can occur so early in pregnancy—sometimes before a woman knows she is pregnant—athletes should be mindful of these recommendations when training while trying to become pregnant and during pregnancy.

METABOLIC CHANGES IN PREGNANCY

Significant metabolic changes occur during pregnancy to meet the demands of the developing fetus. In early pregnancy, increases in estrogen, progesterone, and human placental lactogen stimulate insulin release from the β cells of the pancreas increasing circulating insulin levels. The increased insulin levels help to increase fat storage, which serves as an alternate fuel for the mother while sparing glucose for the fetus. Insulin levels eventually increase by as much as 250% of prepregnancy levels (¹⁶). As pregnancy progresses, there is an increase in maternal insulin resistance (³⁴). Because the major energy source for the fetus is maternal carbohydrates, the increased maternal insulin resistance ensures more glucose availability for the fetus (¹⁰). Despite the increase in circulating insulin, liver glucose production through gluconeogenesis and glycogenolysis in pregnant women is elevated (³⁴). As pregnancy progresses, however, circulating blood glucose levels decrease by as much as 10–20%, which may indicate increased fetal use (^16,34).

Exercise in general is associated with an increase in glucose uptake by skeletal muscle. The combination of glucose demand by exercising muscle and the fetal demand of maternal glucose could result in maternal hypoglycemia and, theoretically, decreased glucose availability for the fetus. In the nonpregnant state, the combination of epinephrine, norepinephrine, glucagon, and cortisol works to ensure adequate plasma glucose for the working muscles. Epinephrine, norepinephrine, and glucagon stimulate glycogenolysis in the liver and the muscles, and cortisol increases gluconeogenesis. As exercise intensity increases, catecholamine release increases and so does the rate of glycogenolysis. During short-term exercise, plasma glucose is elevated. During prolonged exercise, however, plasma glucose remains close to resting levels as the rate of glucose release from the liver matches the skeletal muscle metabolic need. Once liver glycogen levels decrease (as occurs with prolonged exercise without supplemental nutrition), plasma glucose levels decrease and glucagon levels increase in an attempt to increase gluconeogenesis. In steady-state exercise lasting longer than 3 hours, proper nutrition becomes critical to maintain sufficient fuel. Insulin levels decrease with prolonged exercise, but insulin sensitivity increases because of the increased blood flow (^15,27). Because pregnancy is associated with an increase in insulin resistance and a decrease in blood glucose, it is important to consider how these changes affect the pregnant endurance athlete's ability to exercise—particularly during higher-intensity, longer-duration work.

During exercise in pregnancy, blood glucose decreases more than that in nonpregnant women (^8,17). The decrease may be related to impaired hepatic gluconeogenesis or glycogenolysis, increased maternal glucose utilization, or a disparity between glucose use and production (^8,17). Bessinger et al. (⁷) examined the plasma glucose response to moderate-intensity exercise in women at 22 and 32 weeks of pregnancy and at 14 weeks postpartum. The women exercised on a treadmill for 30 minutes at 65% of MHR. The decreases in plasma glucose were significantly higher at 22 and 33 weeks pregnant versus postpartum. To assess how a longer duration of moderate exercise could affect blood glucose, Soultanakis et al. (⁵²) investigated glucose homeostasis in pregnant versus nonpregnant women during 60 minutes of cycling at 55% V̇o₂max. Blood glucose concentrations of pregnant women decreased faster and to a lower level at 45-minute and 60-minute exercise. Perhaps more relevant to the pregnant endurance athlete, Mottola et al. (⁴⁴) assessed metabolic responses to longer, more intense exercise in physically active women. Both pregnant (16–20 weeks) and nonpregnant women completed 40 minutes of vigorous (95% of ventilatory threshold) treadmill exercise. No differences in blood glucose concentration were found at rest and at 20-minute exercise. Blood glucose concentration decreased significantly more in the pregnant group by 40 and 15 minutes into the recovery period. Mottola et al. (⁴⁴) speculated the preservation of blood glucose in the nonpregnant women was due to the normal increases in glycogenolysis and gluconeogenesis that occur during exercise and recommended that exercising pregnant women be especially aware of the need for a carbohydrate-rich diet.

Despite the theoretical possibility that exercise may reduce fetal carbohydrate, evidence suggests that chronic exercise does not contribute to low birth weights. Exercise in pregnancy improves GWG and decreases the risk of developing GDM and the incidence of macrosomia (^19,37,38,59). A systematic review by Davenport et al. (¹⁷) found the incidence of maternal hypoglycemia to be low during and after prenatal exercise. The pregnant endurance athlete and their coach should be cautious in interpreting these results because more research is needed on high-intensity, long-duration exercise. Because blood glucose levels decline more during exercise in pregnancy than in the nonpregnant state, the pregnant endurance athlete should be mindful of the amount of carbohydrates in their diet and their fuel needs during exercise (⁴⁴).

MUSCULOSKELETAL CHANGES IN PREGNANCY

Weight gain goals for pregnant women are based on body mass index (BMI). According to the ACOG, women with a normal BMI (18.5–24.9 kg/m²) should gain 25–35 pounds, overweight individuals (BMI 25–29.9 kg/m²) should gain 15-25 pounds, and obese individuals (BMI > 30 kg/m²) should gain 11–20 pounds during pregnancy. Gestational weight gain includes the increase in maternal fat stores (including breast tissue) and increased BV, extracellular fluid, the fetus, placenta, and amniotic fluid (¹⁰). Pregnant women experience a progressive anterior shift in the center of gravity (COG) with the expansion of the uterus, the enlargement of the breasts, and the general redistribution of their weight (^10,24,32). The anterior shift in COG is associated with an increase in anterior flexion of the spine and exaggerated lumbar lordosis (^10,23). In addition, hormonal changes—particularly the release of relaxin from the corpus luteum—increase joint laxity. Altered gait patterns emerge with the postural changes including decreased step length, increased double support (the time during the gait cycle when both feet are in contact with the ground), and a wider stance (²⁴).

These musculoskeletal changes affect balance and proprioception and could thus affect the performance of certain types of exercise. In addition, the changes are associated with symptoms such as low back pain (LBP), pelvic girdle pain (PGP), and joint pain, which cause discomfort in general and could affect high-impact endurance exercises such as running (^10,32). Low back pain and PGP are common in pregnancy. Wu et al. (⁶²) reported LBP and PGB in 45% of pregnancies. Pregnant elite athletes are also susceptible. Bo and Backe-Hansen (⁹) investigated the prevalence of LBP and PGP in elite national team players and reported 18.5% of the athletes experienced LBP and 29.6% experienced PGP during pregnancy. Throughout pregnancy, women's musculoskeletal changes affect exercise to varying degrees.

Running is one of the most common endurance modes of exercise, but the high-impact nature of the activity can be particularly challenging as pregnancy progresses. Tenforde et al. (⁵⁷) surveyed competitive runners during pregnancy and found 70% of the women ran while pregnant, but only 31% ran during the last trimester. The average volume and intensity for the subjects were reduced by half compared with training before pregnancy. Although the most common reasons to stop running were feeling “poorly” or “uncomfortable,” only 3% reported sustaining a running injury related to training while pregnant. Some women can tolerate high-volume running throughout their entire pregnancies. Davies et al. (¹⁸) examined the training habits of an elite marathoner during a twin pregnancy. The athlete reported running an average of 155 km/wk before pregnancy. The average weekly miles were reduced during pregnancy, but only to 107 ± 19 km/wk.

If the high-impact nature of running causes discomfort, other low-impact modes of activity could be appropriate. Swimming is a recommended exercise while pregnant because the buoyancy of the water decreases pressure on exercising joints. In addition, the increase in central BV when immersed in water may help maintain fetal circulation during exercise (³¹). Because water conducts heat more effectively than air, thermoregulation is also improved while swimming (⁵³). Cycling is another mode of endurance exercise that is low-impact in nature. It is important to be aware though of how the shift in COG affects balance and proprioception. Changes to bicycle fit may improve the ability to ride comfortably throughout pregnancy, and there is anecdotal evidence to support safe cycling in each trimester. However, the fall risk has led the ACOG to recommend stationary cycling and to list “off-road” cycling as an activity to avoid during pregnancy.

CONCLUSION

It is well determined that exercise during pregnancy has many benefits for both mother and fetus. Unfortunately, because research investigating how much exercise is too much may cause maternal and fetal harm, less is known about the safety of high-intensity and long-duration exercise in pregnancy. In the update to their guidelines in 2020, the ACOG included information specifically for athletes. Although they concluded that “vigorous-intensity” exercise seems to be safe in the third trimester of pregnancy, they called for more research investigating the effect of more strenuous exercise in early pregnancy (^2,6). In addition, they have cautioned against exercising at intensities above the current guidelines (specifically >90% of MHR) because of the potential fetal risk.

The prolonged nature of endurance exercise also requires pregnant athletes to be mindful of thermoregulation during exercise. Current guidelines recommend that pregnant women exercise in thermoneutral environments because research has found that maternal core temperature exceeding 39°C or increasing 1.5°C–2.0°C from the baseline could compromise fetal well-being (^2,3,47,53). The prolonged nature of endurance training and the fact that blood glucose has been found to decrease more in exercising pregnant women also necessitates that these athletes carefully assess their nutrition before, during, and after exercise (⁴⁴). Finally, owing to the repetitive nature of endurance exercise, athletes must also pay attention to the biomechanical changes that occur during pregnancy that could lead to discomfort or injury. Pregnant endurance athletes should work closely with a multidisciplinary team including their physician, coach, athletic trainer, exercise physiologist, and nutritionist to create an exercise prescription that meets their individual needs.