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Maximal Exercise Testing in Late Gestation:

Fetal Responses
ANNE MACPHAIL, BNSc, GREGORY A. L. DAVIES, MD, RAHI VICTORY, MD, AND
LARRY A. WOLFE, PhD

Objective: To determine the fetal response to and safety of fetus. Such information is needed so that female athletes
maximal maternal exercise in the third trimester. and women with occupations involving strenuous ex-
Methods: Twenty-three active women with uncomplicated ertion (eg, military service, police work, or firefighting)
pregnancies (singleton gestations) underwent maximal exer-
can be advised on the safe limits of exercise throughout
cise testing in late gestation using a progressive maximal
cycle ergometer protocol. Fetal heart rate (FHR) responses
pregnancy and, in particular, during late gestation.
were monitored and classified using National Institute of Fetal heart rate (FHR) characteristics are important
Child Health and Human Development guidelines. Statisti- indicators of fetal well-being or distress. Fetal heart rate
cal analyses involved use of the Student t test, repeated responses associated with hypoxia include tachycardia,
measures analysis of variance with Tukey-Kramer multiple bradycardia, reductions in variability or accelerations,
comparisons posttest, and the 2 test. and increases in decelerations.3 Fetal heart rate tracings
Results: There was an increase in baseline FHR in the have been analyzed inconsistently in the past because of
20-minute posttest period compared with the 20-minute
different definitions of normal FHR patterns, interpreter
pretest period. There were significantly fewer accelerations
variability, and incorrect assessment of motion artifacts
in the second posttest 10-minute segment compared with the
second pretest 10-minute segment. Variability was reduced (from Doppler ultrasound recording) as bradycardia.4,5
in both posttest periods compared with the first 10-minute These drawbacks, combined with poor descriptions of
pretest period. Time to reactivity increased after testing. the exercise engaged in and incomplete clinical and
Mild tachycardia was noted in two tracings and bradycardia physical descriptions of subjects, have resulted in
occurred in a fetus with previously undiagnosed growth knowledge gaps about the effects of strenuous maternal
restriction. There were no abnormal neonatal outcomes. exercise on FHR responses.4
Conclusion: Maximal exercise testing in late gestation led Strenuous maternal exercise involves metabolic and
to minimal changes in FHR. Fetal bradycardiac responses
cardiovascular changes that have the potential to com-
were not seen in appropriate for gestational age fetuses,
promise fetal well-being.4 Studies of laboratory animals
suggesting that brief maximal maternal exertion for research
or diagnostic purposes is safe in this group. (Obstet Gynecol
suggest that redistribution of blood flow from visceral
2000;96;56570. 2000 by The American College of Obste- organs to contracting maternal skeletal muscle could
tricians and Gynecologists.) compromise uterine, umbilical, and fetal blood flow,
causing fetal hypoxia.6 The combined effects of reduced
maternal liver glycogen storage,7 blunted maternal
Research on exercise in pregnancy has increased over sympathoadrenal responses,8 and recruitment of fast-
the years, resulting in more specific and less conserva- twitch motor units in maternal skeletal muscle at high
tive guidelines for physical activity for healthy women work rates also could contribute to maternal hypogly-
with normal pregnancies.1,2 Because most studies have cemia8 and reduced fetal glucose availability immedi-
focused on moderate exercise, limited information is ately after exercise.9 Finally, maternal blood lactate
available about the effects of strenuous exercise on the accumulation during strenuous exercise could, in the-
ory, reverse the transplacental gradient for hydrogen
From the School of Physical and Health Education and the Depart- ion concentration, possibly contributing to fetal asphyx-
ments of Obstetrics and Gynaecology and Physiology, Queens Univer- ia.3
sity, Kingston, Ontario, Canada. A growing body of evidence also supports the exis-
Supported by the US Army Medical Research and Materiel Command
(contract no. DAMD17-96-C-6112), the Ontario Thoracic Society, and tence of maternal-fetal protective mechanisms that
the Natural Sciences and Engineering Research Council of Canada. could help to prevent fetal hypoxia and preserve fetal

VOL. 96, NO. 4, OCTOBER 2000 0029-7844/00/$20.00 565


PII S0029-7844(99)00940-6
glucose availability in association with strenuous exer- adequate to detect a change in baseline FHR of five
tion. As discussed in a recent review from this labora- beats per minute with an expected standard deviation
tory,4 these might include redistribution of uterine (SD) of seven beats per minute.12 Using this formula,
blood flow to favor the cotyledons rather than the the critical sample size (80% power) was estimated as 18
myometrium, exercise-induced hemoconcentration, subjects. Therefore, a sample size of 23 women was
and increased fetal arteriovenous oxygen extraction. considered adequate.
The purpose of this study was to examine the effects Before exercise testing, subjects abstained from caf-
of maximal maternal exercise testing on FHR responses feine for at least 6 hours and strenuous physical activity
using standardized subject inclusion criteria, a testing for at least 12 hours. They also consumed a standard
protocol tailored to pregnant women, fetal monitoring meal (350 kcal) 2 hours before testing. Subjects exer-
before and immediately after exercise, and analysis of cised on a constant work-rate cycle ergometer at 20 W
tracings using standard measurement criteria recently for 4 minutes, and this was followed by a ramp increase
proposed by the National Institute of Child Health and in work rate of 20 W per minute until volitional fatigue
Human Development.10 The hypothesis tested was that (unpublished data).11,13,14 Subjects were monitored by
FHR responses to a single bout of strenuous exercise by an experienced obstetric nurse using a cardiotocometer
aerobically conditioned women in late gestation are (model 8041-A; Hewlett-Packard, Avondale, PA) for 20
minimal and transient. Results are discussed in relation minutes before and 20 minutes immediately after the
to maternal physiologic data obtained through the same maximal exercise test. Any significant abnormalities
exercise tests (unpublished data).11 identified by the nurse were referred to the on-call
obstetrician for further assessment.
Fetal heart rate tracings were interpreted indepen-
Materials and Methods
dently by two researchers (GALD and RV) experienced
Twenty-three subjects were recruited through newspa- in the interpretation of FHR tracings in both clinical and
per advertisements, posted announcements, and con- research situations. Measurements were made of the
tact with physicians, midwives, and community agen- baseline heart rate, frequency of accelerations and de-
cies that provide services to women in Kingston, celerations, and variability using research guidelines for
Ontario, Canada. Prospective subjects were screened by interpretation of electronic FHR monitoring developed
their obstetricians, family physicians, or midwives us- by the National Institute of Child Health and Human
ing the Physical Activity Readiness Medical Examina- Development.10
tion for Pregnancy,2 a standardized medical screening The FHR tracing was separated into two pretest
questionnaire designed to determine whether exercise 10-minute segments and two posttest 10-minute seg-
in pregnancy is safe for the individual responding to the ments. According to the National Institute of Child
questionnaire. Inclusion criteria were the following: Health and Human Development guidelines, the base-
gestational age 3138 weeks, singleton gestation, non- line FHR is the approximate mean FHR rounded to
smoker, physically active throughout pregnancy (min- increments of five beats per minute during a 10-minute
imum energy expenditure equivalent to walking 30 segment. To be interpretable, the baseline FHR must be
minutes three times per week), nonobese (body mass of at least 2-minutes duration within the 10-minute
index less than 27), age 20 40 years, parity 0 2, not segment, without periodic or episodic changes, or peri-
taking medications or supplements other than prenatal ods of marked variability or segments of the baseline
vitamins, and absence of absolute or relative contrain- that differ by more than 25 beats per minute. Bradycar-
dications to exercise in pregnancy based on response to dia is considered present when baseline FHR is less
the Physical Activity Readiness Medical Examination than 110 beats per minute. In tachycardia, baseline FHR
for Pregnancy administered by a physician. Written is more than 160 beats per minute. Accelerations are
informed consent was obtained before entry into the defined as abrupt increases in FHR from baseline of at
study. The study design and informed consent form least 15 beats per minute, lasting at least 15 seconds and
were approved by the Research Ethics Board, Faculty of no longer than 2 minutes before the return to baseline.
Medicine, Queens University, and by the Human Sub- Variable decelerations are defined as abrupt decreases
jects Protection Branch, US Army Medical Research and in FHR below baseline of at least 15 beats per minutes,
Materiel Command. lasting at least 15 seconds and no longer than 2 minutes
Baseline FHR was chosen as the most important and before the return to baseline. Prolonged decelerations
fundamental experimental variable. A minimum sam- are defined as decreases in the baseline heart rate of at
ple size for adequate statistical power was estimated least 15 beats per minute, lasting more than 2 minutes
using a paired subject formula for comparison of means but less than 10 minutes from onset to return to
(SPSS, Inc., Chicago, IL). The sample was selected as baseline.

566 MacPhail et al FHR Responses Obstetrics & Gynecology


The National Institute of Child Health and Human Table 1. Maternal Physical Characteristics
Development guidelines also include definitions of Variable Mean standard deviation
early and late decelerations. However, none of the
Maternal age (y) 32 4
exercising patients were contracting or in labor. Because Body height (cm) 162 6
these definitions depend on the fetal heart response to Body mass (kg) 74.3 7.9
uterine contractions, they are not included. The Na- Body mass index 28 2.6
tional Institute of Child Health and Human Develop- Sum of seven skinfolds (mm) 130 43
Resting heart rate (bpm) 91 11
ment guidelines do not differentiate between beat-to-
Peak heart rate (bpm) 176 6
beat (short-term) and long-term variability. Baseline Parity 0.7 0.9
FHR variability is defined as fluctuations in baseline Gestational age (wk) 35.0 1.6
FHR of two or more cycles per minute. The fluctuations Peak work rate (W) 184 28
are irregular in amplitude and frequency and are deter- Resting lactate level (mmol/L) 1.3 0.6
Peak postexercise lactate level (mmol/L) 9.8 2.4
mined visually by noting the amplitude of the peak-to-
Resting blood pressure (mmHg) 120/68 3.7/9.5
trough in beats per minute (amplitude range undetect-
able: absent FHR variability; amplitude range
detectable but less than five beats per minute: minimal
FHR variability; amplitude range six to 25 beats per stratified by the four 10-minute periods, two pretest and
minute: moderate FHR variability; and amplitude range two posttest, can be found in Table 3.
more than 25 beats per minute: marked FHR variabili- A significant difference in baseline FHR over the four
ty). Time to reactivity is defined as the time in minutes periods analyzed was noted on repeated measures
required for two accelerations from baseline of more analysis of variance. The Tukey-Kramer multiple com-
than 15 beats per minute lasting at least 15 seconds.15 parisons posttest identified a significantly higher base-
Data from four 10-minute FHR segments, two before line FHR in the second posttest 10-minute segment
exercise and two after, were available for interpretation. (mean 145 12 beats per minute) compared with the
These were analyzed for baseline FHR, number of first pretest 10-minute segment (mean 139 9 beats per
accelerations from baseline, number of decelerations minute, P .05) and the second pretest 10-minute
from baseline, and degree of FHR variability. The time segment (mean 139 10 beats per minute, P .01).
to a reactive FHR was determined both before and after There were significantly fewer accelerations in the sec-
exercise testing. Values obtained by the two evaluators ond posttest 10-minute segment (mean 1.5 1.2) com-
were not significantly different (paired Student t test); pared with the second pretest 10-minute segment
therefore, the mean of the data obtained by the two (mean 2.4 1.6, P .01). Fetal heart rate decelerations
interpreters was used for the assessment of continuous were uncommon regardless of the period, and no
variables (baseline FHR, accelerations, decelerations, significant differences were found between time seg-
and time to reactivity). Data obtained by a single ments. For each period, assessment of variability was
interpreter (GALD) was used for the categoric defini- categorized into either 1) undetectable or minimal or 2)
tion of variability. Repeated measures analysis of vari- moderate or marked. 2 analysis identified no signifi-
ance was used to compare continuous data during the cant differences in the amount of variability in the two
four 10-minute periods. Application of the Tukey- consecutive periods before or after maximal exercise
Kramer multiple comparisons followed posttest. 2 testing. However, there was a significant reduction in
analysis was used for comparison of categoric data. FHR variability between the first pretest time segment
Results were considered statistically significant if P
.05.
Table 2. Neonatal Characteristics
Variable
Results
1-min Apgar score 7.9 1.5
Twenty-three women with uncomplicated pregnancies Median 8
(singleton gestations) underwent a graded-cycle er- Range 39
gometer test until volitional fatigue. Mean ( SD) 5-min Apgar score 9.0 0.2
Median 9
gestational age was 35.0 1.6 weeks. Maternal physical
Range 8 9
characteristics are listed in Table 1. All pregnancies Birth weight (g) 3454 446
resulted in live births. Neonatal characteristics are given Birth length (cm) 51.0 2.5
in Table 2. Fetal heart rate tracings were available for all Head circumference (cm) 34.4 1.5
subjects for at least 20 minutes before and after maximal Cord artery pH/buffer base (base excess) 7.2 0.1/38.8 4.2
exercise testing. A summary of FHR characteristics Data are presented as mean standard deviation, median, or range.

VOL. 96, NO. 4, OCTOBER 2000 MacPhail et al FHR Responses 567


Table 3. Fetal Heart Rate Characteristics After Maximal Exercise
Time 1 Time 2 Time 3 Time 4
Characteristic (first 10 min pretest) (second 10 min pretest) (first 10 min posttest) (second 10 min posttest)

Baseline FHR (bpm) 139 9* 139 9 142 11 145 11


Accelerations 2.1 1.4 2.4 1.6 1.7 1.3 1.5 1.2
Decelerations 0.2 0.4 0.02 0.1 0.3 0.4 0.1 0.2
Variability
Absent/Minimal 2* 3 12 9
Moderate/Marked 21 20 11 14
Time to reactivity (min) 13.6 13.8 19.3 9.3
FHR fetal heart rate.
Data are presented as mean standard deviation.
* Significantly less than Time 4 at P .05.

Significantly less than Time 4 at P .01.

Significantly less than Time 2 at P .01.

Significantly less than Time 3 at P .01.

Significantly less than Time 3 at P .01.

and both the first posttest period (P .01) and the mately six beats per minute) in the second posttest
second posttest period (P .05). There was also a 10-minute segment than in the first and second 10-
significant decrease in FHR variability between the minute pretest segments. This difference is not likely to
second pretest period and the first posttest period (P be clinically significant. Mean baseline FHR did not
.01). Time to achieve reactivity was somewhat greater return to the pre-exercise value within 20 minutes after
after maximal exercise testing, but this effect did not exercise. Others have reported a return to pre-exercise
reach statistical significance. No fetuses demonstrated baseline within 20 30 minutes.4,17,19,2224 Integrated fe-
tachycardia or bradycardia before maternal exercise. tal chemoreceptor, baroreceptor, and adrenal responses
Posttest tachycardia was noted on two tracings, one at appear to influence transient increases in FHR, resulting
165 beats per minute for 20 minutes from a pretest in increased fetal cardiac output and hence increased
baseline of 150 beats per minute and a second at 163 oxygen availability.21 This may be a protective mecha-
beats per minute during the second 10-minute posttest nism or reflex response to compensate for relative
segment from a pretest baseline of 143 beats per minute hypoxia resulting from reduced uterine blood flow
and first 10-minute posttest baseline of 160 beats per during maternal exercise.21,25
minute. A single episode of transient bradycardia was Postexercise fetal bradycardia has been reported to
seen. Immediately after the test, the FHR was 60 beats occur in 1520% of fetuses after strenuous exer-
per minute and increased gradually to 120 beats per cise.4,17,19,22,26 Except for the case of significant FGR no
minute over 6 minutes. This subject underwent further episodes of fetal bradycardia occurred in our study.
medical evaluations that identified previously undiag- Bradycardia is a reflex vagal response to significant
nosed fetal growth restriction (FGR) and led to induc- hypoxia due to maternal hypotension and/or reduced
tion of labor 3 days after the test. 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
Discussion There are several possible reasons for the infrequent
This study was conducted to characterize the effects on occurrence of bradycardia in this study. Subjects were
FHR characteristics of an acute bout of strenuous exer- conditioned, and thus there may have been maternal
cise engaged in by healthy, physically active women in and fetal compensatory mechanisms to prevent fetal
late gestation. Particular attention was paid to standard- hypoxia.4,12,22,27 Such women might be able to perform
ization of inclusion criteria, exercise protocol and test- at a higher work rate before inducing fetal hypoxic
ing, and analysis of fetal responses. As hypothesized, stress as less cardiac output is redistributed toward
FHR responses were minimal and transient under these skeletal muscle and away from the placenta,12,22 and
conditions. they might have greater placental volume.27 The exer-
The results of this study confirm that the most cise protocol of this study was shorter than that of other
common FHR response to an acute bout of strenuous studies such as the study by Manders et al24 and
exercise is an increase in FHR immediately after exer- involved the use of a cycle ergometer instead of modes
cise.12,16 24 Mild tachycardia was noted on 9% of trac- requiring greater muscle mass. Shorter duration and
ings. Baseline FHR was significantly higher (approxi- reduced percentage of maternal muscle mass both con-

568 MacPhail et al FHR Responses Obstetrics & Gynecology


tribute to smaller reductions in uterine blood flow, ciency. However, the respiratory exchange ratio at peak
thereby maintaining greater fetal oxygen pressure (ten- exercise was reduced significantly during pregnancy,
sion).6 Another reason bradycardia has been reported in suggesting reduced carbohydrate utilization. These
some studies but not in others is the varied definitions findings were also consistent with the earlier reports by
of this FHR characteristic.4 Lotgering et al,13,14 who studied the exercise responses
Variability was reduced after exercise but returned of healthy pregnant women using the same cycle er-
toward pretest values in the second 10-minute period gometer testing protocol. In association with the
after exercise cessation. Reduced variability was ob- blunted respiratory exchange ratio at peak exercise, our
served by Artal et al17 in 22.5% of cases, lasting 6 7 group (unpublished data) also reported significantly
minutes, and by Manders et al24 in association with lower values during pregnancy in terms of peak post-
bradycardiac incidents, for 20 minutes after exercise. exercise lactate concentrations and excess postexercise
Carpenter et al26 observed bradycardia with normal oxygen consumption (ie, oxygen debt). All of these
FHR variability within 3 minutes of cessation of exer- results suggest that maternal ability to use carbohy-
cise in 16.2% of maximal cycle ergometer tests (brady- drates and produce lactic acid during heavy exercise
cardia was defined as FHR less than 110 beats per above the point of respiratory compensation is reduced
minute for more than 10 seconds). No change in vari- in late gestation. This was attributed to augmented
ability occurred in fetuses of healthy pregnant women insulin resistance caused by gestational hormones and
in studies by ONeill23 or van Doorn et al.20 Variability might be an important mechanism to maintain fetal
is thought to indicate central nervous system integrity, glucose availability from the maternal blood glucose
adequate oxygenation, and fetal well-being.3,4 How- pool.4
ever, a reduction in variability in the absence of other In a parallel study by Kemp et al,11 pregnant subjects
ominous findings such as decelerations might not imply were able to maintain lower plasma hydrogen ion
an asphyxial insult.3 concentrations (higher pH) compared with nonpreg-
In the present study, we observed a reduction in nant controls, in the resting state, at peak exercise, and
accelerations, no change in decelerations, and a nonsig- during the immediate 15-minute postexercise recovery
nificant increase in time to achieve reactivity after period, through a combination of respiratory and met-
exercise. Few investigators have reported information abolic adaptations. Thus, maternal capacity for weight-
about these fetal characteristics. ONeill23 observed no supported work is well preserved and the ability to
FHR decelerations or reduction in accelerations with regulate acid-base balance during and after brief stren-
strenuous maternal exercise. Accelerations in the study uous exercise is maintained in healthy active pregnant
by Artal et al17 were similar before and after strenuous women in late gestation.
exercise. van Doorn et al20 found no change in pattern Considered in relation to the maternal data just
pre- to postexercise. Carpenter et al26 noted normal summarized, the present study results suggest that
reactive tracings within 30 minutes after exercise. maternal exercise testing using a brief cycle ergometer
An important advantage of the present study over testing protocol is safe in this group under carefully
previous investigations of fetal responses to maximal controlled conditions, but additional study involving
exercise testing is the availability of detailed informa- the testing of a larger number of subjects is necessary to
tion on maternal physiologic responses to the same confirm this hypothesis. The single episode of brady-
maximal exercise tests.4 In this regard, Kemp et al11 cardia demonstrates the need for screening, including
used a modern physicochemical approach to study estimates of fetal weight before maximal exercise test-
acid-base responses of nine of the present study sub- ing. Also, the use of maximal exercise intensities in
jects, and our group (unpublished data) used state-of- chronic physical conditioning might not be safe and
the-art breath-by-breath methodologies to study meta- could result in altered fetal growth.4,28
bolic 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
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570 MacPhail et al FHR Responses Obstetrics & Gynecology

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