Background
Moderate intensity aerobic exercise throughout pregnancy is known to result in lower caesarean delivery rates, lower incidence of gestational diabetes and hypertensive disorders, decreased maternal weight gain, and improvements in antenatal and postnatal depression, and has not been found to negatively affect birth weight [
1‐
3]. However, studies investigating the effects of vigorous intensity exercise on birth weight have been mixed [
4‐
8]. This is clinically important as birth weight is the single most important predictor of neonatal morbidity and mortality [
9]. Research has shown that fetal hypoglycemia in hypoxic conditions can result in infants born small for gestational age [
10]. So while moderate intensity exercise throughout pregnancy is beneficial, it is not known whether vigorous intensity exercise is detrimental, particularly in the third trimester when the needs of the fetus are greater.
Decreases in utero-placental blood flow occurs during vigorous intensity exercise, and has been shown to result in fetal bradycardia [
11]. Physical exertion demands greater substrate utilisation, and as such re-directs blood to the working muscles, whilst also generating heat and excess by-products [
12]. The combination of these adaptations challenges the greater demands required by the fetus during pregnancy. Indeed, reduced fetal movement after vigorous intensity exercise in the third trimester has been shown in studies with both conditioned and unconditioned mothers [
13]. It seems likely that the increasing physiological demands during each trimester of pregnancy require variation in exercise training accordingly. However, current guidelines for pregnancy are not trimester-specific.
The American College of Sports Medicine (ACSM) recommend moderate intensity exercise throughout pregnancy; however, the guidelines around vigorous intensity exercise are not as clear [
14]. Vigorous and high-intensity exercise is defined as being at least 70% of maximum heart rate (MHR), or an activity in which a conversation generally cannot be maintained [
15]. There is limited participation in vigorous intensity exercise in pregnancy [
16], perhaps due to the fact it requires a significant increase in workload of greater than 6–9 times resting levels of metabolism (6–9 METs) [
15]. This is thought to be due to an increase in discomfort in progressing pregnancy [
16], or, potentially is indicative of a lack of consensus around the safety of participating in this type of training. The threshold for achieving vigorous intensity exercise during pregnancy is considered to be lower than the non-pregnant population due to autonomic nervous system modulation and subsequent attenuation of maximum heart rate and elevation of resting heart rate [
17]. Indeed, if women are trying to achieve vigorous intensity workload based on an aerobic capacity of 60–80% heart rate reserve or VO
2peak, it is recommended by the Canadian Guideline for Physical Activity throughout Pregnancy that women target a heart rate of between 142 and 169 bpm, depending on their age [
18]. This range is lower than the target heart rate of non-pregnant populations. The haemodynamic variances throughout the stages of pregnancy, which are also dependent on age and fitness, provides insight to the lack of guidance behind vigorous intensity exercise prescription in pregnant populations. Moreover, it highlights the need for a subjective measure of intensity to be used concurrent to any objective measure [
17]. It is currently recommended that if patients are completing vigorous intensity exercise before pregnancy they should be able to continue throughout pregnancy, but with caution. This is also the recommendation by The Royal Australian and New Zealand College of Obstetricians and Gynaecologists [
19].
The current understanding of the benefits of vigorous intensity exercise during pregnancy lie predominantly in decreased maternal weight gain. Moreover, it has been suggested that vigorous intensity exercise is an important goal for pregnant women, especially among the overweight or obese, previously inactive, or those with gestational diabetes [
20,
21]. A study by Clapp, et al. [
22], found that the offspring of women who were randomly assigned to a high volume of moderate-vigorous intensity exercise in mid-late pregnancy were significantly lighter than infants born to women who did lower volumes of exercise. Despite vigorous intensity exercise having potential benefits in minimising maternal weight gain, trimester-specific evidence needs to be pooled for an improved synthesis of existing evidence before vigorous intensity exercise can safely be prescribed throughout pregnancy.
More specific guidelines are needed on vigorous intensity exercise in each trimester; and particularly in the final trimester, as this appears to be the most controversial within the literature. This is the first analysis of its kind to pool the evidence for studies reporting vigorous intensity exercise specifically in the third trimester. The primary aim of the study was to investigate the effects of vigorous intensity exercise during pregnancy on birth weight. The secondary aim was to investigate the effects on incidence of small for gestational age (SGA), low birth weight (LBW), prematurity, gestational age at delivery and maternal weight gain.
Discussion
The findings from the meta-analysis indicated no significant difference in birth weight from mothers who completed vigorous intensity exercise in the third trimester compared with controls. Further, no significant mean difference was observed between vigorous intensity exercise and control groups on incidence of SGA, LBW, or maternal weight gain. However, women undertaking vigorous intensity to third trimester did have a small, but significant, increase in gestational age at delivery and decreased risk of prematurity.
Clapp, et al. [
55] suggested that the intermittent periods of hypoxia inherent in vigorous exercise, as blood is re-directed to the working muscles, may actually be advantageous to the fetus in the first and second trimester, as this is the time when the growth of the placenta at the level of the intermediate villi is greatest [
55]. Indeed, periods of hypoxia can increase placenta vascularisation through angiogenesis in the placenta [
56]. As such, vigorous intensity exercise in the first and second trimesters can result in a healthier placenta. However, the needs of the fetus are greater in the third trimester, with blood flow to the uterus increasing from 50 mL/min in the first trimester to 500 mL/min in the third trimester [
57]. It is postulated that fetus compensatory sympathetic responses are in place to deal with a reduction in blood flow [
58], exemplified by what occurs transiently during vigorous exercise. This is supported in the study by Collings, et al. [
36], who reported an increase in fetal heart rate responses during and after vigorous intensity exercise. Indeed, the findings from this meta-analysis indicate an absence of detrimental effects of vigorous intensity exercise in the third trimester on markers which may reflect outcomes of reduced blood flow, such as incidence of SGA, LBW and prematurity. There also appeared to be no difference between groups in the women who suffered miscarriages in the RCTs. However, there is a lack of detail in the reporting of adverse events in the cohort and case-control studies, and caution is required.
A meta-analysis by Leet and Flick [
59] found endurance exercisers who continued exercise into the third trimester delivered infants who weighed 212.2 g less than active controls (in six studies), and 436.5 g less than sedentary controls (in two studies). However, the weight loss was insufficient to be considered as a diagnosis of SGA. Notably, only one of these studies provided exercise descriptions that were considered adequate to be defined as vigorous intensity exercise. Reduced birth weight without diagnosis of SGA was also found in two other reviews [
60,
61]. The lower birth weight that is shown in some studies is thought to be due to reduced fetal fat deposition, rather than a reduction in lean mass [
22]. However, it would seem pertinent to suggest that women who are carrying fetuses on the lower end of the weight chart in the later stages of pregnancy should be cautious about undertaking vigorous exercise in the third trimester, as, although not significant, the pooled results from the RCTs demonstrated slightly lower birth weight than controls.
Every paper reported vigorous intensity exercise in a different way, making it difficult to compare studies. It is hard to differentiate if it is intensity, frequency, duration, or volume (total exercise workload which can be a factor of intensity, frequency and duration) of exercise sessions, that contributes to the lower birth weight reported in some of the studies. Bell, et al. [
35] identified that frequency of vigorous intensity exercise may relate to birth weight, with findings indicating a decrease in birth weight with increasing number of exercise sessions (3 sessions = 3682 g birth weight, and 5/6/7 sessions = 3049 g birth weight). On the other hand, the study by Kuhrt, et al. [
43] showed that neither average weekly kilometers (i.e., volume), or trimester that women ran to, influenced birth weight percentiles. The retrospective survey by Zeanah and Schlosser [
44] also showed no effect of higher volume (> 80 min/week) or higher intensity (> 150 bpm) exercise during third trimester, on birth weight. The study by Takami, et al. [
62], divided 92,796 women into very low, low, medium and high levels of physical activity, based on met-hours per week. The equation for met-hours per week uses a weighting for intensities, therefore looking at volumes of exercise rather than specific intensities. However, this study found no detrimental effects of high-volume exercise on infant outcomes. Conversely, a significant increase was reported in prematurity in the very low volume exercise group. This is in line with our own findings, which found a reduction in prematurity in women undertaking vigorous intensity exercise. Rather than vigorous intensity exercise having a physiological effect on reducing prematurity, it is more likely to indicate women participating in vigorous intensity exercise and/or choosing to be involved in an exercise research study, are likely to be healthier with lower risk pregnancies.
It is important to note that most studies in this systematic review reported intensities below 90% MHR (or equivalent). Indeed, according to the terminology reported in Norton, et al. [
15], most studies included in this review described exercise considered vigorous intensity (< 90% MHR) and
not high-intensity (≥90% MHR). This is significant to highlight as a study in elite athletes showed normal fetal heart rate responses to an acute bout of exercise conducted at 23–29 weeks of gestation,
until the intensity reached above 90% MHR [
63]. Only two of the seven athletes reached an intensity greater than 90% MHR, and in both of these athletes the mean uterine artery blood flow was less than 50% of the initial value with fetal bradycardia occurring (indicating fetal distress). However, fetal heart rate returned to normal upon cessation of the exercise. It is not clear what the long-term impact of this transient fetal bradycardia from acute strenuous exercise is. It could be that this extreme high-intensity exercise undertaken by some women is what is driving the tendency to lower birth weight in some studies. The study by Kardel and Kase [
64], did report women reaching heart rates of 170–180 bpm (likely equivalent of greater than estimated 90% MHR) in two exercising groups (one with higher volume). This study reported measuring fetal heart rate and movement after a 10-min interval training session, assessed 6–7 times throughout the pregnancy, and used as a prognostic value for detection of fetal distress and antenatal hypoxia. However, the results from these measures are not reported in the article. As both studies were conducted with a small sample size, the impact of exercising at levels above 90% MHR warrants further investigation. Three studies included in this review demonstrated no negative effects of vigorous intensity exercise on fetal heart response [
36,
41] and mean uterine arteries pulsatility index [
31].
Due to the difficulty in accurate assessment of MHR during pregnancy (as a result of haemodynamic changes), associations of exercise intensity with ratings of perceived exertion are recommended [
65]. The use of non-pregnant intensity guidelines [
15] as an inclusion criteria for vigorous intensity exercise studies in this review is likely to represent pregnant women completing exercise at an intensity higher than vigorous intensity guidelines in non-pregnant guidelines. However, the purpose of this meta-analysis is to demonstrate the safety of an intensity that is likely prescribed as vigorous intensity exercise in research and clinical practice. As such, the lack of adverse events using non-pregnant vigorous intensity guidelines (i.e. the upper limit) provides reassurance of the safety of this intensity of exercise. Future research should validate pregnancy specific target heart rates throughout each trimester of pregnancy, alongside the varying changes in maternal haemodynamics, so the safety of adjusted intensities can be assessed.
It has been recommended by the Canadian Guidelines Consensus Panel for Physical Activity Throughout Pregnancy that chronic high-intensity exercise, above the target heart rates recommended, is only undertaken in a monitored environment [
18]. Of the 15 included studies, only five reported exclusively supervised exercise sessions. Whilst these studies are considered vigorous intensity, not high-intensity exercise, the lack of adverse events in the studies that reported unsupervised exercise sessions should provide reassurance as to the safety of this type of exercise in most low-risk pregnancies.
Moderate intensity exercise is well reported to reduce gestational weight gain in normal weight, overweight and obese pregnant women [
66]. However, the lack of benefit of vigorous intensity exercise on maternal weight gain in this meta-analysis is an interesting finding. The lack of additional benefit of maternal weight gain may suggest that vigorous intensity exercise in the third trimester is not necessary above and beyond moderate intensity exercise. It is important to note that the two RCTs in this review that recruited a cohort of overweight and obese pregnant women, did in fact find a benefit of vigorous intensity exercise on maternal weight gain compared to a control group [
31,
34]. This perhaps indicates a benefit of vigorous intensity exercise in limiting maternal weight gain in overweight and obese populations, rather than in healthy weight women. Future research should identify any additional benefits on infant and maternal outcomes of vigorous intensity exercise in the third trimester, such as to antenatal anxiety and depression and gestational diabetes. It is also pertinent that studies conducted during pregnancy should document and report all adverse events occurring throughout the pregnancy and birth. Indeed, the original design of this systematic review was to compare the effects of vigorous intensity exercise ceased at each trimester, and the subsequent benefit or detriment of continuing vigorous exercise into the third trimester. Unfortunately, a lack of evidence precluded this sub-analysis.
Strengths and limitations
There are both strengths and limitations to this meta-analysis. The main strengths of the paper are that it is the first of its kind to pool the evidence for studies reporting vigorous intensity exercise specifically in the third trimester. Further, by including both randomized, cohort and case-control studies we have been able to capture the scope of evidence in this area. Indeed, by doing so we have been able to identify an important discrepancy in reporting of lower birth weight in RCTs compared with cohort and case-control studies. However, the heterogeneity of the research designs is also a limitation in synthesising the evidence [
67]. A random effects meta-analysis attempts to account for this by estimating the effects from similar interventions that operate on a similar outcome. The results from the moderator analyses did not demonstrate significant heterogeneity, however it is acknowledged that samples were small in some of these analyses. While point estimates of heterogeneity were often modest, the small number of studies meant the confidence intervals for heterogeneity were very wide. This means there may be heterogeneity in the outcomes that could not be explained by the studies in this review.
Further research on the effects of vigorous intensity exercise on maternal and infant outcomes is still needed, particularly in separating the benefits or detriments of high-intensity exercise versus high volume of exercise in the third trimester of pregnancy. Thorough documentation of adverse events should be prioritised, and future studies should also examine placenta function and growth in combination with birth weight. More evidence is needed on the impact of higher intensity on birth outcomes in elite athletes, who are the population likely to be exercising at > 90% MHR [
68]. It is also important to note that in the studies included in this systematic review, the mode of exercise was not always reported. However, in most cases the vigorous intensity mode was aerobic exercise. Future research is still needed to assess the safety of high-intensity resistance training regarding changes in musculature (such as pelvic floor dysfunction and diastasis recti) during pregnancy.
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