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Maximal Exercise Testing in Late Gestation: Fetal Responses

From the School of Physical and Health Education and the Departments of Obstetrics and Gynaecology and Physiology, Queen’s University, Kingston, Ontario, Canada.

Address reprint requests to: Larry A. Wolfe, PhD School of Physical and Health Education Queen’s University Kingston, ON K7L 3N6 Canada

	Abstract

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Objective: To determine the fetal response to and safety of maximal maternal exercise in the third trimester.

Methods: Twenty-three active women with uncomplicated pregnancies (singleton gestations) underwent maximal exercise testing in late gestation using a progressive maximal cycle ergometer protocol. Fetal heart rate (FHR) responses were monitored and classified using National Institute of Child Health and Human Development guidelines. Statistical analyses involved use of the Student t test, repeated measures analysis of variance with Tukey-Kramer multiple comparisons posttest, and the ² test.

Results: There was an increase in baseline FHR in the 20-minute posttest period compared with the 20-minute pretest period. There were significantly fewer accelerations in the second posttest 10-minute segment compared with the second pretest 10-minute segment. Variability was reduced in both posttest periods compared with the first 10-minute pretest period. Time to reactivity increased after testing. Mild tachycardia was noted in two tracings and bradycardia occurred in a fetus with previously undiagnosed growth restriction. There were no abnormal neonatal outcomes.

Conclusion: Maximal exercise testing in late gestation led to minimal changes in FHR. Fetal bradycardiac responses were not seen in appropriate for gestational age fetuses, suggesting that brief maximal maternal exertion for research or diagnostic purposes is safe in this group.

Research on exercise in pregnancy has increased over the years, resulting in more specific and less conservative guidelines for physical activity for healthy women with normal pregnancies.^1,2 Because most studies have focused on moderate exercise, limited information is available about the effects of strenuous exercise on the fetus. Such information is needed so that female athletes and women with occupations involving strenuous exertion (eg, military service, police work, or firefighting) can be advised on the safe limits of exercise throughout pregnancy and, in particular, during late gestation.

Fetal heart rate (FHR) characteristics are important indicators of fetal well-being or distress. Fetal heart rate responses associated with hypoxia include tachycardia, bradycardia, reductions in variability or accelerations, and increases in decelerations.³ Fetal heart rate tracings have been analyzed inconsistently in the past because of different definitions of normal FHR patterns, interpreter variability, and incorrect assessment of motion artifacts (from Doppler ultrasound recording) as bradycardia.^4,5 These drawbacks, combined with poor descriptions of the exercise engaged in and incomplete clinical and physical descriptions of subjects, have resulted in knowledge gaps about the effects of strenuous maternal exercise on FHR responses.⁴

Strenuous maternal exercise involves metabolic and cardiovascular changes that have the potential to compromise fetal well-being.⁴ Studies of laboratory animals suggest that redistribution of blood flow from visceral organs to contracting maternal skeletal muscle could compromise uterine, umbilical, and fetal blood flow, causing fetal hypoxia.⁶ The combined effects of reduced maternal liver glycogen storage,⁷ blunted maternal sympathoadrenal responses,⁸ and recruitment of fast-twitch motor units in maternal skeletal muscle at high work rates also could contribute to maternal hypoglycemia⁸ and reduced fetal glucose availability immediately after exercise.⁹ Finally, maternal blood lactate accumulation during strenuous exercise could, in theory, reverse the transplacental gradient for hydrogen ion concentration, possibly contributing to fetal asphyxia.³

A growing body of evidence also supports the existence of maternal-fetal protective mechanisms that could help to prevent fetal hypoxia and preserve fetal glucose availability in association with strenuous exertion. As discussed in a recent review from this laboratory,⁴ these might include redistribution of uterine blood flow to favor the cotyledons rather than the myometrium, exercise-induced hemoconcentration, and increased fetal arteriovenous oxygen extraction.

The purpose of this study was to examine the effects of maximal maternal exercise testing on FHR responses using standardized subject inclusion criteria, a testing protocol tailored to pregnant women, fetal monitoring before and immediately after exercise, and analysis of tracings using standard measurement criteria recently proposed by the National Institute of Child Health and Human Development.¹⁰ The hypothesis tested was that FHR responses to a single bout of strenuous exercise by aerobically conditioned women in late gestation are minimal and transient. Results are discussed in relation to maternal physiologic data obtained through the same exercise tests (unpublished data).¹¹

	Materials and Methods

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Twenty-three subjects were recruited through newspaper advertisements, posted announcements, and contact with physicians, midwives, and community agencies that provide services to women in Kingston, Ontario, Canada. Prospective subjects were screened by their obstetricians, family physicians, or midwives using the Physical Activity Readiness Medical Examination for Pregnancy,² a standardized medical screening questionnaire designed to determine whether exercise in pregnancy is safe for the individual responding to the questionnaire. Inclusion criteria were the following: gestational age 31–38 weeks, singleton gestation, non-smoker, physically active throughout pregnancy (minimum energy expenditure equivalent to walking 30 minutes three times per week), nonobese (body mass index less than 27), age 20–40 years, parity 0–2, not taking medications or supplements other than prenatal vitamins, and absence of absolute or relative contraindications to exercise in pregnancy based on response to the Physical Activity Readiness Medical Examination for Pregnancy administered by a physician. Written informed consent was obtained before entry into the study. The study design and informed consent form were approved by the Research Ethics Board, Faculty of Medicine, Queen’s University, and by the Human Subjects Protection Branch, US Army Medical Research and Materiel Command.

Baseline FHR was chosen as the most important and fundamental experimental variable. A minimum sample size for adequate statistical power was estimated using a paired subject formula for comparison of means (SPSS, Inc., Chicago, IL). The sample was selected as adequate to detect a change in baseline FHR of five beats per minute with an expected standard deviation (SD) of seven beats per minute.¹² Using this formula, the critical sample size (80% power) was estimated as 18 subjects. Therefore, a sample size of 23 women was considered adequate.

Before exercise testing, subjects abstained from caffeine for at least 6 hours and strenuous physical activity for at least 12 hours. They also consumed a standard meal (350 kcal) 2 hours before testing. Subjects exercised on a constant work-rate cycle ergometer at 20 W for 4 minutes, and this was followed by a ramp increase in work rate of 20 W per minute until volitional fatigue (unpublished data).^11,13,14 Subjects were monitored by an experienced obstetric nurse using a cardiotocometer (model 8041-A; Hewlett-Packard, Avondale, PA) for 20 minutes before and 20 minutes immediately after the maximal exercise test. Any significant abnormalities identified by the nurse were referred to the on-call obstetrician for further assessment.

Fetal heart rate tracings were interpreted independently by two researchers (GALD and RV) experienced in the interpretation of FHR tracings in both clinical and research situations. Measurements were made of the baseline heart rate, frequency of accelerations and decelerations, and variability using research guidelines for interpretation of electronic FHR monitoring developed by the National Institute of Child Health and Human Development.¹⁰

The FHR tracing was separated into two pretest 10-minute segments and two posttest 10-minute segments. According to the National Institute of Child Health and Human Development guidelines, the baseline FHR is the approximate mean FHR rounded to increments of five beats per minute during a 10-minute segment. To be interpretable, the baseline FHR must be of at least 2-minutes’ duration within the 10-minute segment, without periodic or episodic changes, or periods of marked variability or segments of the baseline that differ by more than 25 beats per minute. Bradycardia is considered present when baseline FHR is less than 110 beats per minute. In tachycardia, baseline FHR is more than 160 beats per minute. Accelerations are defined as abrupt increases in FHR from baseline of at least 15 beats per minute, lasting at least 15 seconds and no longer than 2 minutes before the return to baseline. Variable decelerations are defined as abrupt decreases in FHR below baseline of at least 15 beats per minutes, lasting at least 15 seconds and no longer than 2 minutes before the return to baseline. Prolonged decelerations are defined as decreases in the baseline heart rate of at least 15 beats per minute, lasting more than 2 minutes but less than 10 minutes from onset to return to baseline.

The National Institute of Child Health and Human Development guidelines also include definitions of early and late decelerations. However, none of the exercising patients were contracting or in labor. Because these definitions depend on the fetal heart response to uterine contractions, they are not included. The National Institute of Child Health and Human Development guidelines do not differentiate between beat-to-beat (short-term) and long-term variability. Baseline FHR variability is defined as fluctuations in baseline FHR of two or more cycles per minute. The fluctuations are irregular in amplitude and frequency and are determined visually by noting the amplitude of the peak-to-trough in beats per minute (amplitude range undetectable: absent FHR variability; amplitude range detectable but less than five beats per minute: minimal FHR variability; amplitude range six to 25 beats per minute: moderate FHR variability; and amplitude range more than 25 beats per minute: marked FHR variability). Time to reactivity is defined as the time in minutes required for two accelerations from baseline of more than 15 beats per minute lasting at least 15 seconds.¹⁵

Data from four 10-minute FHR segments, two before exercise and two after, were available for interpretation. These were analyzed for baseline FHR, number of accelerations from baseline, number of decelerations from baseline, and degree of FHR variability. The time to a reactive FHR was determined both before and after exercise testing. Values obtained by the two evaluators were not significantly different (paired Student t test); therefore, the mean of the data obtained by the two interpreters was used for the assessment of continuous variables (baseline FHR, accelerations, decelerations, and time to reactivity). Data obtained by a single interpreter (GALD) was used for the categoric definition of variability. Repeated measures analysis of variance was used to compare continuous data during the four 10-minute periods. Application of the Tukey-Kramer multiple comparisons followed posttest. ² analysis was used for comparison of categoric data. Results were considered statistically significant if P < .05.

	Results

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Twenty-three women with uncomplicated pregnancies (singleton gestations) underwent a graded-cycle ergometer test until volitional fatigue. Mean (± SD) gestational age was 35.0 ± 1.6 weeks. Maternal physical characteristics are listed in Table 1. All pregnancies resulted in live births. Neonatal characteristics are given in Table 2. Fetal heart rate tracings were available for all subjects for at least 20 minutes before and after maximal exercise testing. A summary of FHR characteristics stratified by the four 10-minute periods, two pretest and two posttest, can be found in Table 3.

	Discussion

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This study was conducted to characterize the effects on FHR characteristics of an acute bout of strenuous exercise engaged in by healthy, physically active women in late gestation. Particular attention was paid to standardization of inclusion criteria, exercise protocol and testing, and analysis of fetal responses. As hypothesized, FHR responses were minimal and transient under these conditions.

The results of this study confirm that the most common FHR response to an acute bout of strenuous exercise is an increase in FHR immediately after exercise.^12,16–24 Mild tachycardia was noted on 9% of tracings. Baseline FHR was significantly higher (approximately six beats per minute) in the second posttest 10-minute segment than in the first and second 10-minute pretest segments. This difference is not likely to be clinically significant. Mean baseline FHR did not return to the pre-exercise value within 20 minutes after exercise. Others have reported a return to pre-exercise baseline within 20–30 minutes.^{4,17,19,22–24} Integrated fetal chemoreceptor, baroreceptor, and adrenal responses appear to influence transient increases in FHR, resulting in increased fetal cardiac output and hence increased oxygen availability.²¹ This may be a protective mechanism or reflex response to compensate for relative hypoxia resulting from reduced uterine blood flow during maternal exercise.^21,25

Postexercise fetal bradycardia has been reported to occur in 15–20% of fetuses after strenuous exercise.^{4,17,19,22,26} Except for the case of significant FGR no episodes of fetal bradycardia occurred in our study. Bradycardia is a reflex vagal response to significant hypoxia due to maternal hypotension and/or reduced uterine blood flow during recovery. It protects the fetus by preserving blood flow and oxygen delivery to vital organs including the brain and the heart.³

There are several possible reasons for the infrequent occurrence of bradycardia in this study. Subjects were conditioned, and thus there may have been maternal and fetal compensatory mechanisms to prevent fetal hypoxia.^4,12,22,27 Such women might be able to perform at a higher work rate before inducing fetal hypoxic stress as less cardiac output is redistributed toward skeletal muscle and away from the placenta,^12,22 and they might have greater placental volume.²⁷ The exercise protocol of this study was shorter than that of other studies such as the study by Manders et al²⁴ and involved the use of a cycle ergometer instead of modes requiring greater muscle mass. Shorter duration and reduced percentage of maternal muscle mass both contribute to smaller reductions in uterine blood flow, thereby maintaining greater fetal oxygen pressure (tension).⁶ Another reason bradycardia has been reported in some studies but not in others is the varied definitions of this FHR characteristic.⁴

Variability was reduced after exercise but returned toward pretest values in the second 10-minute period after exercise cessation. Reduced variability was observed by Artal et al¹⁷ in 22.5% of cases, lasting 6–7 minutes, and by Manders et al²⁴ in association with bradycardiac incidents, for 20 minutes after exercise. Carpenter et al²⁶ observed bradycardia with normal FHR variability within 3 minutes of cessation of exercise in 16.2% of maximal cycle ergometer tests (bradycardia was defined as FHR less than 110 beats per minute for more than 10 seconds). No change in variability occurred in fetuses of healthy pregnant women in studies by O’Neill²³ or van Doorn et al.²⁰ Variability is thought to indicate central nervous system integrity, adequate oxygenation, and fetal well-being.^3,4 However, a reduction in variability in the absence of other ominous findings such as decelerations might not imply an asphyxial insult.³

In the present study, we observed a reduction in accelerations, no change in decelerations, and a nonsignificant increase in time to achieve reactivity after exercise. Few investigators have reported information about these fetal characteristics. O’Neill²³ observed no FHR decelerations or reduction in accelerations with strenuous maternal exercise. Accelerations in the study by Artal et al¹⁷ were similar before and after strenuous exercise. van Doorn et al²⁰ found no change in pattern pre- to postexercise. Carpenter et al²⁶ noted normal reactive tracings within 30 minutes after exercise.

An important advantage of the present study over previous investigations of fetal responses to maximal exercise testing is the availability of detailed information on maternal physiologic responses to the same maximal exercise tests.⁴ In this regard, Kemp et al¹¹ used a modern physicochemical approach to study acid-base responses of nine of the present study subjects, and our group (unpublished data) used state-of-the-art breath-by-breath methodologies to study metabolic and respiratory responses of the remaining 14 subjects during and after the exercise test. Both studies found no significant differences in the peak work rate achieved among healthy active pregnant subjects compared with nonpregnant controls.

Our group (unpublished data) also observed no significant differences between pregnant and nonpregnant subjects in absolute maximal oxygen uptake (expressed in liters per minute), oxygen uptake at the ventilatory anaerobic threshold, oxygen uptake at the point of respiratory compensation, or calculated working efficiency. However, the respiratory exchange ratio at peak exercise was reduced significantly during pregnancy, suggesting reduced carbohydrate utilization. These findings were also consistent with the earlier reports by Lotgering et al,^13,14 who studied the exercise responses of healthy pregnant women using the same cycle ergometer testing protocol. In association with the blunted respiratory exchange ratio at peak exercise, our group (unpublished data) also reported significantly lower values during pregnancy in terms of peak postexercise lactate concentrations and excess postexercise oxygen consumption (ie, oxygen debt). All of these results suggest that maternal ability to use carbohydrates and produce lactic acid during heavy exercise above the point of respiratory compensation is reduced in late gestation. This was attributed to augmented insulin resistance caused by gestational hormones and might be an important mechanism to maintain fetal glucose availability from the maternal blood glucose pool.⁴

In a parallel study by Kemp et al,¹¹ pregnant subjects were able to maintain lower plasma hydrogen ion concentrations (higher pH) compared with nonpregnant controls, in the resting state, at peak exercise, and during the immediate 15-minute postexercise recovery period, through a combination of respiratory and metabolic adaptations. Thus, maternal capacity for weight-supported work is well preserved and the ability to regulate acid-base balance during and after brief strenuous exercise is maintained in healthy active pregnant women in late gestation.

Considered in relation to the maternal data just summarized, the present study results suggest that maternal exercise testing using a brief cycle ergometer testing protocol is safe in this group under carefully controlled conditions, but additional study involving the testing of a larger number of subjects is necessary to confirm this hypothesis. The single episode of bradycardia demonstrates the need for screening, including estimates of fetal weight before maximal exercise testing. Also, the use of maximal exercise intensities in chronic physical conditioning might not be safe and could result in altered fetal growth.^4,28

	Footnotes

 
Supported by the US Army Medical Research and Materiel Command (contract no. DAMD17-96-C-6112), the Ontario Thoracic Society, and the Natural Sciences and Engineering Research Council of Canada.

PII S0029-7844(99)00940-6

Received November 22, 1999. Received in revised form March 14, 2000. Accepted March 24, 2000.

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