One of the major concerns in relation to the practice of exercise during pregnancy always has been the possibility of a negative effect on fetal growth. Part of the debate has focused on whether the redistribution of fetoplacental blood flow during physical exercise, in which blood flow is rerouted from the viscera to the muscles, may result in transitory fetal hypoxia with compensatory fetal tachycardia, leading to fetal growth restriction if the effect were to persist.1 This concern arose from experimental animal studies that showed a redistribution of cardiac output, with an increase in blood flow to the muscles and skin and a decrease to the viscera. This response may represent a reduction of approximately 35% in uteroplacental blood flow, which is consequently redistributed as a protective mechanism, favoring the placenta instead of the myometrium and resulting in hemoconcentration and a greater affinity of fetal blood to oxygen.2 , 3 It should be emphasized that this reduction in blood flow is directly proportional to the intensity of exercise and muscular strength used. Once exercise stops, blood flow rapidly returns to normal.4 , 5
Several studies have been performed in humans with the objective of demonstrating that exercise during pregnancy is healthy, both for the pregnant woman and for the fetus. Nevertheless, studies in this area are incipient and the effects of the practice of physical activity during pregnancy on fetal growth have yet to be established.6 – 8
The objective of the present study was to estimate the effect of an exercise program on uteroplacental and fetal blood flow during pregnancy, on fetal growth, the frequency of preeclampsia, blood pressure levels during pregnancy, and the weight and length of the newborn at birth. Outcomes were compared in accordance with the period of pregnancy in which systematic supervised walking was initiated (week 13 or 20) and with a control group of women who were not submitted to this intervention.
MATERIALS AND METHODS
This randomized controlled trial involved pregnant women attending public health care units in the city of Campina Grande, Brazil, between May 2008 and September 2010. The protocol was approved by the Internal Review Board of the State University of Paraíba (approval letter 324.0.133.000–07), and the study complied with the ethical guidelines for research in human beings published in Resolution 196/96 of the National Health Council. The study was registered with Clinical Trials (www.clinicaltrials.gov) under reference NCT00641550.9
The inclusion criteria consisted of: healthy pregnant women who were sedentary at admission to the study, gestational age 13 weeks or less confirmed by ultrasonography, and with the presence of a single live fetus. A sedentary lifestyle was defined as the absence of systematic routine physical exercise. Exclusion criteria consisted of women who smoked, those with chronic diseases, a history of premature delivery, the presence of fetal abnormalities, placenta previa, a history of vaginal bleeding, hematomas or areas of membrane detachment, and cervical length less than 2.5 cm as measured by transvaginal ultrasonography at admission to the study.
Sample size was calculated using the OpenEpi software program 2.1, using birth weight as the parameter and predicting a mean birth weight of 3,660±422.1 g in the group of women who initiated exercise in the first trimester of pregnancy and 3,430±440.9 g in the sedentary control group,7 resulting in a power of 80% and a significance level of 5%. Accordingly, 56 participants would be required for each of the three groups. The total sample was calculated as 168 pregnant women; however, this was increased to 187 women to compensate for any losses after randomization.
The pregnant women referred by the health care units were randomized in week 13 of pregnancy. Women at less than 13 weeks of gestation were submitted to ultrasonography to confirm gestational age. At this time, the objectives of the study were explained and the patient was instructed to return at 13 weeks of gestation if she was interested in participating in the study. Those who returned for the visit scheduled for gestational week 13 were once again submitted to ultrasonography to confirm fetal viability, and the inclusion and exclusion criteria were applied. If the women fulfilled these criteria and agreed to participate in the study, then they were asked to sign an informed consent form.
Next, each woman was randomized to one of three groups: group A, with exercise initiated at 13 weeks of gestation; group B, with exercise initiated at 20 weeks of gestation; and group C, which was a control group of women who were not submitted to supervised exercise. All the women continued to receive prenatal care at their health care unit of origin, with no interference from the research team. A randomization sequence was generated in blocks of 10 using the Random Allocation software program 1.0 by another investigator who did not participate directly in the study. This investigator also prepared the sealed opaque envelopes containing the randomization group for each participant. Group assignment was defined only after the woman had agreed to participate in the study, thus guaranteeing that allocation remained concealed until the participant had been admitted to the trial.
This was an open study because it was impossible to blind the investigators and the research participants; however, the investigators involved in monitoring the ultrasound variables and in the statistical analysis were unaware of the group to which the patient had been assigned. The CONSORT guidelines were applied in this study.10
The exercise program was developed by physical educators in accordance with the recommendations of the American College of Obstetricians and Gynecologists.11 All the women participating in the study performed a test on a treadmill at week 13 of gestation to determine their physical fitness levels, and this test was repeated at weeks 20 and 28.12 Maximal oxygen consumption (VO2max) was calculated using the following formula: VO2max=(0.055×heart ratemax)+(0.381×inclination)+(5.541×speed)+(−0.090×body mass index×time)−6.846. In the exercise groups, the supervised intervention was performed three times weekly. The initial duration of walking was 15 minutes, gradually increasing over the study period in accordance with the woman's previous physical fitness level. Before beginning the exercise, the women performed warming-up and stretching exercises.
During walking, two criteria were used to ascertain that the intensity of the exercise was indeed moderate: heart rate between 60% and 80% of maximum heart rate, corrected for age,13 and subjective perceived exertion of 12–16 on the Borg scale.14 Exercise was performed in the open air at a mild temperature (24°C), supervised by physical education professionals and medical, physiotherapy, and nursing students specifically trained for this purpose. Maternal heart rate was monitored continuously using a Polar S120 heart rate monitor to control the intensity of exercise.
Maternal blood pressure was measured at week 13 of gestation, at week 20, and thereafter every 4 weeks. Hypertension was defined as systolic pressure 140 mm Hg or more or diastolic pressure 90 mm Hg or more, or both.15 Blood pressure was measured before and after each exercise session using the palpation and auscultatory methods.16
To evaluate the ultrasonographic (fetal weight and cervical length) and Doppler velocimetry variables (pulsatility indices in the uterine, umbilical, and middle cerebral arteries), a Voluson 730 Expert ultrasound machine with a 2-MHz to 7-MHz convex probe was used. This is the standard scanner used in obstetric examinations. All scans were performed by the same fetal medicine specialist. Fetal growth was monitored every 4 weeks from weeks 20 to 36 of gestation and reevaluated at week 38.17 The fetuses were then classified according to their estimated weights for the respective gestational ages using the Brazilian curve as: less than the 10th percentile, between the 10th and the 90th percentiles, or above the 90th percentile.18
The uterine arteries were evaluated by transvaginal ultrasonography at week 13, taking into consideration the presence of notches and the pulsatility index.19 Subsequent evaluations were made by transabdominal ultrasonography at weeks 20, 24, 28, 32, 36, and 38. The umbilical arteries were evaluated at weeks 20, 24, 28, 32, 36, and 38 of gestation and the middle cerebral artery was evaluated at weeks 28, 32, 36, and 38.20 Fetal centralization was defined as when the ratio between the pulsatility index of the middle cerebral artery and the pulsatility index of the umbilical artery was less than 1 (pulsatility index middle cerebral artery/pulsatility index umbilical artery less than 1).21
All the women participating in the study answered a specific questionnaire about their habitual pattern of physical activity at the time of admission to the study (during week 13 of gestation) and during week 32 of gestation. Physical activity was measured by calculating the number of metabolic equivalents of task, a measure used to describe the total number of calories burned. A version of the Pregnancy Physical Activity Questionnaire validated for women in Brazil was used for this purpose.22
Any women with a cervix of less than 2.5 cm in length, as measured by ultrasonography in the first trimester of pregnancy (week 13), were excluded from the study. At this time, gestational age was estimated. A questionnaire about socioeconomic and obstetric issues was applied. The women's weights and heights were measured using Tanita digital scales and a Seca stadiometer, respectively. Body mass index was calculated as weight (kg)/[height (m)]2. The data referring to the newborns were collected on the day they were born. Weight was measured using digital scales with 10-g resolution. The newborns were classified according to their weights as: small for gestational age, appropriate for gestational age, or large for gestational age (LGA).23
The following variables were analyzed: physical fitness level, fetal growth as shown by serial evaluation of estimated fetal weight, pulsatility indices of the uterine, umbilical, and middle cerebral arteries by Doppler velocimetry, blood pressure levels throughout pregnancy, the frequency of preeclampsia, and the weight, length, and gestational age of the newborn at birth.
Data analyses were performed using the Epi-Info software program 3.3 and MedCalc. Initially, the Kolmogorov-Smirnov test was used to assess the normality of the distribution of the continuous numerical variables. The baseline characteristics of each group were compared with identify any differences that could represent biases for the study objectives. The categorical variables were evaluated according to their distribution of frequency. Measures of central tendency and dispersion were also calculated for the numerical variables. To evaluate the association between the practice of physical exercise and the numerical variables, tests of analysis of variance were used for the continuous variables and the Kruskall-Wallis test for discrete variables. This analysis was performed on an intention-to-treat basis.
Risk ratios, together with their 95% confidence intervals, were calculated as a measure of risk ratio for preeclampsia, fetal growth restriction, fetal macrosomia, LGA, and small for gestational age according to the exercise group (A or B), with a standard risk of 1.0 being attributed to the reference category (control group C). In addition, repeated measures analysis of variance was used to evaluate the association between physical exercise and the outcomes evaluated throughout pregnancy: fetal weight (weeks 20, 24, 28, 32, 36, and 38), systolic and diastolic blood pressures (weeks 13, 20, 24, 28, 32, 36, and 38), and the pulsatility index of the uterine arteries (weeks 13, 20, 24, 28, 32, 36, and 38), umbilical arteries (weeks 20, 24, 28, 32, 36, and 38), and middle cerebral arteries (weeks 28, 32, 36, and 38). The longitudinal nature of the variables permitted a pattern to be described over time. This type of analysis was adopted because of the nature of the variables (longitudinal with multiple observations). Sphericity was assumed in the case of all the study variables in a longitudinal manner, with P values being calculated for the time-by-intervention interaction. A significance level of 5% was adopted.
A total of 209 pregnant women were considered eligible for admission to the study during the period between May 2008 and September 2010. Of these, 22 refused to participate; therefore, 187 women were randomized. However, 16 of these women (8.6%) discontinued; therefore, 171 women were evaluated at week 20, with 32% belonging to group A (n=54), 35% belonging to group B (n=60), and 33% belonging to group C (n=57). In the subsequent evaluations, the number of women continuing follow-up decreased, with 140 women being evaluated at week 38. This decrease occurred for three reasons: because some of the newborns were born at 37–38 weeks; because some of the women failed to attend certain scheduled visits; and because others delivered their newborns prematurely. Because failure to attend a scheduled monthly visit was not considered to constitute loss to follow-up, the woman remained in the study as long as she continued attending the scheduled exercise classes and did not miss the subsequent follow-up visit. At delivery, 171 mothers and newborns were evaluated (Fig. 1). The mean number of days on which exercise was performed was 68 in group A and 46 in group B. All the women analyzed completed at least 85% of the scheduled exercise program.
The groups were homogenous at baseline (at week 13 of gestation) with respect to sociodemographic characteristics, weight, height, parity, body mass index, and habitual pattern of physical activity. The mean age of the women was 24.7 years, and most (58%) had already had at least one child. Mean weight at week 13 was 58.5±10.1 kg and mean metabolic equivalent of task was 1.5 (Table 1).
No difference was found in physical fitness level between the groups at weeks 13 or 20; however, at the evaluation conducted at week 28, a difference was found in mean VO2max: 27.3±4.3 in group A; 28±3.3 in group B; and 25.5±3.8 in group C (P=.03; Table 2). With respect to the pattern of routine physical activity evaluated at week 32, an improvement was found in the intervention groups (group A 3.2±0.43, group B 3.1±0.55, and group C 1.4±0.41 metabolic equivalents of task; P<.001).
Fetal growth was similar in all three groups at the six evaluation moments during pregnancy (weeks 20, 24, 28, 32, 36, and 38), with growth being appropriate in the majority of fetuses irrespective of whether exercise was being performed (P=.85; Fig. 2). No case of fetal growth restriction occurred in the intervention groups. No difference was found in the frequency of fetal macrosomia.
With respect to the outcome of birth weight, the overall percentage of LGA was 8.2%, with three in group A, four in group B, and seven in group C, whereas the overall percentage of small for gestational age was 7%, with four in each group. Mean birth weight was 3,279±453 g in group A, 3,285±477 g in group B, and 3,378±593 g in group C (P=.53; Table 2). Mean length at birth was 48 cm in all three groups (P=.86). Mean gestational age was similar in all three groups (39 weeks and 5 days in group A, 39 weeks and 6 days in group B, and 39 weeks and 4 days in group C; P=.49).
Uteroplacental blood flow was evaluated monthly, with results showing that moderate-intensity exercise had no effect on uteroplacental or fetal blood flow. A reduction was found in the pulsatility index of the uterine arteries (P=.75), umbilical arteries (P=.83), and middle cerebral arteries (P=.95) as pregnancy progressed, irrespective of the group (Fig. 3). There was no association between the presence of notches in the uterine arteries during pregnancy and the practice of physical exercise. No case of fetal centralization was found.
No association was found between the practice of physical exercise and preeclampsia. A total of 14 cases of preeclampsia occurred (corresponding to 8.4%), with three cases in group A, six in group B, and five in group C (Table 2). Likewise, no difference was found in systolic (P=.68) or diastolic (P=.17) blood pressure throughout pregnancy (Fig. 2).
A physical exercise program of moderate intensity initiated at different periods during pregnancy (at weeks 13 and 20) in previously sedentary women improved physical fitness level and did not affect uteroplacental or fetal blood flow resistance. Furthermore, there was no effect on fetal growth, preeclampsia, gestational age, or birth weight. The absence of unfavorable outcomes either for the pregnant woman or for the fetus can be considered a positive result, because no consensus has yet been reached on the effect of aerobic exercise initiated during pregnancy, with some studies suggesting an increase in the risk of uteroplacental blood flow redistribution, fetal growth restriction, and prematurity.2 – 4 , 6
A previous study showed that women who initiated physical exercise at the beginning of pregnancy had larger newborns as a result of the increased speed of placental growth and improved placental function.7 Those findings motivated the present study in which an effect was expected to be found on the outcomes of the placentation process, such as resistance in uteroplacental circulation, fetal growth, birth weight, blood pressure levels, and preeclampsia.
Contrary to what was expected, no differences were found in the pulsatility index of the uterine, umbilical, or middle cerebral arteries between the three groups; however, a reduction was found in pulsatility index as pregnancy progressed, irrespective of the group. As pregnancy progresses, a decreased resistance in the vessels evaluated is expected in healthy women and already has been documented.21 , 24 , 25
Studies evaluating the effect of physical exercise on uterine, placental, and fetal blood flow are incipient. In general, these studies evaluated blood flow during exercise testing, ie, they evaluated the short-term effect of exercise. Furthermore, blood flow was only evaluated immediately before and immediately after exercise. Results were conflicting and blood flow rapidly returns to normal soon after exercise has ceased.1 , 26 , 27
No differences were found in mean fetal weight or in the frequency of inappropriate fetal growth, evaluated every 4 weeks. Although no statistically significant differences were found, there was a decrease of approximately 50% in the percentage of LGA newborns in groups A and B. Because the sample size was calculated based on a difference in mean birth weight, the present study may not have had sufficient power to exclude the possibility of association with the lower rate of LGA newborns in the exercise group. Similar findings were encountered in two randomized clinical trials.8 , 28 It should be emphasized, however, that the newborns born to the women in the intervention group might have been lighter because of a reduced percentage of fat,29 which was not measured in the present study.
Another outcome studied was the frequency of preeclampsia and blood pressure levels monitored throughout pregnancy. This was evaluated using the same rationale with respect to the effect of exercise on the placentation process; nevertheless, no differences were found. Blood pressure levels were similar in all three groups, with a reduction in levels between weeks 24 and 32, irrespective of whether exercise was being performed.
One possible reason for the lack of an effect on the outcomes evaluated in this study may have been the gestational age at initiation of the exercise program (13 weeks in the present study compared with 8 or 9 weeks in the study conducted by Clapp et al).7 The initiation of physical activity early in pregnancy at the beginning of the placentation process would explain the stimulation of vascularization and placental growth and the consequent effect on fetal growth and birth weight that has been reported in several studies.5 , 7 , 29 The choice of week 13 as the time at which to initiate exercise in the present study was made because there is currently insufficient evidence to endorse the safe practice of exercise initiated at early stages of pregnancy, principally with respect to the fetus.6 The formation of a third group in which the women began the exercise program in week 20 of pregnancy was stimulated by the hypothesis that differences would be found in accordance with gestational age at the initiation of exercise (13 weeks compared with 20 weeks); however, this was not confirmed. New studies are required to evaluate the effect of physical exercise initiated in earlier phases of pregnancy at the beginning of the placentation process.
The present study shows that the physical fitness level of the women participating in the exercise program had improved by week 28 of pregnancy compared with the women in the control group, irrespective of gestational age at entry to the program. The majority of studies have suggested that the practice of physical exercise initiated during pregnancy, even in previously sedentary women, improves physical fitness level.30 – 32
One of the limitations of the present study that must be emphasized is the fact that physical fitness was evaluated indirectly and the pattern of physical activity was evaluated using a questionnaire instead of a pedometer. Although an improvement was found in physical fitness, this may have been insufficient to affect some of the outcomes evaluated. A Cochrane systematic review dealing with this subject corroborates the present findings, with the authors concluding that regular physical exercise during pregnancy appears to improve physical fitness; however, the data evaluated are insufficient to permit any conclusions to be made on any significant risks or benefits for the mother or the newborn.6
Nevertheless, the debate continues on whether a physical exercise program for previously sedentary women, initiated during pregnancy, would be sufficient to have an effect on important outcomes such as fetal growth, preeclampsia, and birth weight. It should be remembered that various physiologic alterations occur in women during pregnancy, in addition to the changes resulting from the physical exercise; therefore, it is essential to respect the limits of pregnant women.
Although this topic is not new and has recently been the subject of various publications, the possibility of reaching an evidence-based consensus remains distant. Further studies should be conducted to compare previously active pregnant women with those who were previously sedentary to evaluate both the short-term and long-term effects of various modalities of exercise, focusing not only on the mother but also on the fetus. In view of the lack of evidence of any harmful effects to the mother or fetus, the American College of Obstetricians and Gynecologists guidelines should be followed until new evidence is brought to light.
1. Rafla NM. Umbilical artery flow velocity waveforms following maternal exercise. J Obstet Gynaecol 1999;19:385–9.
2. Lotgering FK, Gilbert RD, Longo LD. Exercise responses in pregnant sheep: oxygen consumption, uterine blood flow, and blood volume. J Appl Physiol 1983;55:834–41.
3. Curet LB, Orr JA, Rankin HG, Ungerer T. Effect of exercise on cardiac output and distribution of uterine blood flow in pregnant ewes. J Appl Physiol 1976;40:725–8.
4. MacPhail A, Davies GA, Victory R, Wolfe LA. Maximal exercise testing in late gestation: fetal responses. Obstet Gynecol 2000;96:565–70.
5. Clapp JF. Influence of endurance exercise and diet on human placental development and fetal growth. Placenta 2006;27:527–34.
6. Kramer MS, McDonald SW. Aerobic exercise for women during pregnancy. The Cochrane Database of Systematic Reviews 2011, Issue 3. Art. No.: CD000180. DOI: 10.1002/14651858.CD000180.pub2.
7. Clapp JF 3rd, Kim H, Burciu B, Lopez B. Beginning regular exercise in early pregnancy: effect on fetoplacental growth. Am J Obstet Gynecol 2000;183:1484–8.
8. Barakat R, Lucia A, Ruiz JR. Resistance exercise training during pregnancy and newborn's birth size: a randomised controlled trial. Int J Obes (Lond) 2009;33:1048–57.
10. Boutron I, Moher D, Altman DG, Schulz KF, Ravaud P, CONSORT Group. Extending the CONSORT statement to randomized trials of nonpharmacologic treatment: explanation and elaboration. Ann Intern Med 2008;148:295–309.
11. Exercise during pregnancy and the postpartum period. Committee Opinion No. 267. American College of Obstetricians and Gynecologists. Obstet Gynecol 2002;99:171–3.
12. Mottola MF, Davenport MH, Brun CR, Inglis SD, Charlesworth S, Sopper MM. VO2 peak prediction and exercise prescription for pregnant women. Med Sci Sports Exerc 2006;38:1389–95.
13. Mesquita A, Trabulo M, Mendes M, Viana JF, Seabra-Gomes R. The maximum heart rate in the exercise test: the 220-age formula or Sheffield's table? [in Portuguese]. Rev Port Cardiol 1996;15:139–44, 101.
14. Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc 1982;14:377–81.
15. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol 2000;183:S1–22.
17. Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol 1985;151:333–7.
18. Cecatti JG, Machado MR, dos Santos FF, Marussi EF. [Curve of normal fetal weight values estimated by ultrasound according to gestation age]. Cad Saude Publica 2000;16:1083–90.
19. Plasencia W, Maiz N, Bonino S, Kaihura C, Nicolaides KH. Uterine artery Doppler at 11+0 to 13+6 weeks in the prediction of pre-eclampsia. Ultrasound Obstet Gynecol 2007;30:742–9.
20. Arduini D, Rizzo G. Normal values of Pulsatility Index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med 1990;18:165–72.
21. Wladimiroff JW, Tonge HM, Stewart PA. Doppler ultrasound assessment of cerebral blood flow in the human fetus. Br J Obstet Gynaecol 1986;93:471–5.
22. Silva FT. [Physical activity level evaluation during pregnancy]. Rev Bras Ginecol Obstet 2007;29:490.
23. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–8.
24. Cooley SM, Donnelly JC, Walsh T, MacMahon C, Gillan J, Geary MP. The impact of umbilical and uterine artery Doppler indices on antenatal course, labor and delivery in a low-risk primigravid population. J Perinat Med 2011;39:143–9.
25. Gramellini D, Folli MC, Raboni S, Vadora E, Merialdi A. Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 1992;79:416–20.
26. Kennelly MM, Geary M, McCaffrey N, McLoughlin P, Staines A, McKenna P. Exercise-related changes in umbilical and uterine artery waveforms as assessed by Doppler ultrasound scans. Am J Obstet Gynecol 2002;187:661–6.
27. Rafla NM, Etokowo GA. The effect of maternal exercise on uterine artery velocimetry waveforms. J Obstet Gynaecol 1998;18:14–7.
28. Haakstad LA, Bø K. Exercise in pregnant women and birth weight: a randomized controlled trial. BMC Pregnancy Childbirth 2011;11:66.
29. Clapp JF 3rd. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur J Obstet Gynecol Reprod Biol 2003;110:S80–5.
30. Marquez-Sterling S, Perry AC, Kaplan TA, Halberstein RA, Signorile JF. Physical and psychological changes with vigorous exercise in sedentary primigravidae. Med Sci Sports Exerc 2000;32:58–62.
31. Santos IA, Stein R, Fuchs SC, Duncan BB, Ribeiro JP, Kroeff LR, et al.. Aerobic exercise and submaximal functional capacity in overweight pregnant women: a randomized trial. Obstet Gynecol 2005;106:243–9.
32. Collings CA, Curet LB, Mullin JP. Maternal and fetal responses to a maternal aerobic exercise program. Am J Obstet Gynecol 1983;145:702–7.