Maternal Physical Activity During Pregnancy and the Effect on the Mother and Newborn: A Systematic Review

in Journal of Physical Activity and Health

Background: The practice of physical exercise during pregnancy has benefits for both the mother and baby. Currently, there is scientific evidence that supports the inclusion of a monitored physical activity program in the daily activities of pregnant women. The objective of this study is to provide an overview of the current status of the association between physical activity during pregnancy and the effects on the mother and the newborn. Methods: A systematic review of the literature, assessing each study using the Scottish Intercollegiate Guidelines Network, from different databases PubMed, Embase, or ScienceDirect, on the association between maternal physical activity and its effects on the mother and the newborn published from 2010 until 2018 was conducted. Results: About 25 studies were identified and divided into categories according to the health problems affecting the mother or newborn. It was found that 8% of all the studies received a grade B, 68% obtained a grade C, and the remaining 24% obtained less than a grade C. Improved cardiovascular function, decreased risk of gestational diabetes mellitus, hypertension, and the limitation of weight gain are among the benefits to the mother with lower percentage of body fat, increased gestational age, and potentially improved neurodevelopment as benefits for the child. Conclusions: The realization of physical activity during pregnancy is supported by most of the studies reviewed. However, given the vulnerability of the studied populations, more studies on the association between physical activity and pregnancy are necessary.

Pregnancy is a period of significant physiological and psychological change in the life of women that can promote sedentary behavior and/or low level of physical activity. These behaviors have been associated with an elevated risk of gestational diabetes, gestational hypertension, diabetes mellitus type 2, and other cardiovascular diseases.1 Recent data indicate that only 15% of pregnant women follow the minimum recommendations of 150 minutes per week of moderate-intensity physical activity.1,2 In addition, until recently, interventions to promote physical activity in pregnancy have been scarce and may be due to the symptoms associated with pregnancy (nausea, fatigue, weight gain, low motivation, complications, and fear) and the variety of social and personal beliefs related to pregnancy. The measurement of physical activity during pregnancy has methodological challenges, making it difficult to obtain accurate results on the level of physical activity performance and the real impact on the mother and the newborn. Considering all these points, it is not surprising that physicians are interested in making recommendations and in how to effectively, efficiently, and safely promote physical activity during pregnancy.

In 2002, the American Congress of Obstetricians and Gynecologists published an opinion that recommended 30 minutes of moderate-intense physical exercise almost every day for pregnant women without medical or obstetric complications and suggested that participation in a wide range of physical leisure activities was safe.3 Previous early studies provided strong scientific evidence to promote the safety of moderate-intense exercise, not identifying an increased risk of adverse effects for the mother or the newborn, such as low birth weight, preterm delivery, or miscarriage.47 In addition, physical exercise during pregnancy reduces the risk of some complications associated with pregnancy (preeclampsia and gestational diabetes) and the duration of delivery.810

In order to incorporate recent evidence regarding the benefits and risks of physical activity and exercise during pregnancy and the postpartum period and provide greater specificity, defining moderate-intense exercise and clarifying the impact of intense physical activity on the health of the mother and the newborn, the American Congress of Obstetricians and Gynecologists recently revised its 2002 guidelines11 and published a new committee opinion on the subject.12 Also recently, the Society of Obstetricians and Gynaecologists of Canada and the Canadian Society for Exercise Physiology published the 2019 Canadian Guideline for Physical Activity throughout Pregnancy, which represents a foundational shift in the view of prenatal physical activity from a recommended behavior to improve quality of life, to a specific prescription to reduce pregnancy complications and optimize health across the lifespan of 2 generations.13

In light of this and the growing global epidemic of obesity, new globally established and accepted guidelines that take into account obesity in pregnant women are required. This highlights the need for new guidelines on physical activity with the aim of reducing the intergenerational impact of obesity.14

In the last 25 years, the evidence on the impact of physical activity on pregnancy has greatly increased. However, currently, there is still some concern among gynecologists and obstetricians about the possible consequences of physical activity performed by the mother during pregnancy, as well as the type of exercise or program most appropriate for a period with so many peculiarities.

Therefore, in this systematic review, the objective was to evaluate the association between maternal physical activity during pregnancy and the effects on the mother and newborn; to provide a comprehensive analysis of current data and a context on how to advise pregnant women trying to improve their health during this period and that of the newborn.

Methods

Type of Study

A systematic review of the scientific literature was carried out and the following question was posed: is the physical activity carried out during pregnancy associated with effects on the health of the mother and the newborn?

Identification of Studies and Eligibility Criteria

All the studies published in PubMed, EMBASE, and Web of Science from 2010 to November 2018 were collected. Figures 1 and 2 show the search strategy used. A second bibliographic search was carried out, specifically the references of the publications identified were searched in a search of studies on the subject that were not in the first search. Two investigators independently completed the bibliographic search and consensus was sought in relation to the finally eligible studies. Conflicting decisions were resolved by consensus with a third investigator. The studies were included if they fulfilled the following criteria: (1) articles from 2010 to 2018, (2) studies on results of performing different degrees of physical activity during pregnancy in the health of the mother and the newborn, and (3) studies in humans published in English. When the same article was repeated in different databases, only one of them was taken into account. Of the eligible articles, those that by the title or abstract did not meet the selection criteria, or that by the content of the article did not conform to the parameters of the study, were discarded. Finally, publications were only included in the analysis if they met all the eligibility criteria.

Figure 1
Figure 1

—Search strategy.

Citation: Journal of Physical Activity and Health 18, 1; 10.1123/jpah.2019-0348

Figure 2
Figure 2

—Flow diagram.

Citation: Journal of Physical Activity and Health 18, 1; 10.1123/jpah.2019-0348

The methodological norms established for the publication of systematic reviews and the elements of preferred reports for systematic reviews and meta-analysis were followed.

Internal Validity of the Studies

To evaluate the selected articles and guide the assessment of the results included in them, the publications were classified using the scale proposed by the Scottish Intercollegiate Guidelines Network15 to establish levels of evidence (Table 1) and recommendations (Table 2). This scale was chosen following the principles of evidence-based medicine (EBM) that emphasizes the use of scientific evidence in well-designed and performed research. EBM is about making sure that when a decision is made, it is based on the most up-to-date, reliable, and scientifically sound evidence available about the particular situation being studied.16

Table 1

Levels of Evidence15

LevelDescription
11++High-quality meta-analyses, systematic reviews of RCTs, or RCTs with a very low risk of bias.
1+Well-conducted meta-analyses, systematic reviews of RCTs, or RCTs with a low risk of bias.
1-Meta-analyses, systematic reviews, or RCTs with a high risk of bias.
22++High-quality systematic reviews of case-control or cohort or studies.

High-quality case-control or cohort studies with a very low risk of confounding or bias and a high probability that the relationship is casual.
2+Well-conducted case-control or cohort studies with a low risk of confounding or bias and a moderate probability that the relationship is casual.
2-Case-control or cohort studies with a high risk of confounding or bias and a significant risk that the relationship is not causal.
3Nonanalytic studies, eg, case reports, case series.
4Expert opinion.

Abbreviation: RCT, randomized controlled trials.

Table 2

Grades of Recommendation15

GradeDescription
AAt least one meta-analysis, systematic review, or RCT rated as 1++, and directly applicable to the target population

A body of evidence consisting principally of studies rated as 1+, directly applicable to the target population, and demonstrating overall consistency of results
BA body of evidence including studies rated as 2++, directly applicable to the target population, and demonstrating overall consistency of results Extrapolated evidence from studies rated as 1++, or 1+
CA body of evidence including studies rated as 2+, directly applicable to the target population, and demonstrating overall consistency of results

Extrapolated evidence from studies rated as 2++
DEvidence level 3 or 4

Extrapolated evidence from studies rated as 2+

Abbreviation: RCT, randomized controlled trials.

Results

Characteristics of the Studies

Twenty-five publications that met the established criteria were selected from a total of 133 identified articles. There are some differences in the size of the samples studied (ranging from 30 patients to over 3000 patients). Regarding the methodology of collecting information on physical activity carried out by the mother during pregnancy, some studies were based on surveys carried out after childbirth or months later, and other studies were based on sessions of physical exercise where blood pressure, heart rate, and so on were directly measured. In general, the studies can be divided into 2 main groups: those that included an exercise program as part of a regimented and supervised intervention and those that relied on self-reported physical activity assessed through several different questionnaires. The countries where studies have been conducted on this subject are largely in Europe and North America, but studies from other countries, for example Colombia or New Zealand were also found.

A division of studies has been established in such a way that 5 are focused on overweight and gestational diabetes during pregnancy (Table 3A), 9 on the risks to the baby of performing maternal physical activity (Table 4A), 6 to treat the benefits of physical activity on maternal hypertension (Table 5A), and finally 5 refer to miscarriage, premature delivery, and maternal depression (Table 6A). As for the studies on overweight and gestational diabetes during pregnancy, 3 obtained a grade C, 1 a grade D, and another a grade B (Table 3B). Of the studies on the health of the newborn, 6 obtained a grade C and 3 a grade D (Table 4B). Those studies dealing with maternal gestational hypertension 4 grade C and 2 grade D were assigned (Table 5B). Finally, the studies on maternal depression and the risk of miscarriage, 4 obtained a grade C and 1 a grade B (Table 6B).

Table 3

Relationship Between Maternal Physical Activity, Weight Gain, Overweight, and GDM During Pregnancy

A
AuthorCountryNDesignObjectiveMethodologyPhysical activity
Haakstad y Bo17NorwayCohort of 105 pregnant women were randomized into a CG and an EG.Randomized control trial in patients recruited between 2007 and 2008.Evaluation of the effects of an aerobic exercise program for 12 wk on weight gain in pregnant women.The EG was subjected to sessions of aerobic dance 2 per week of 60 min each with a minimum of 12 wk and without supervision of physical activity the rest of the week.Physical activity was part of a regimented and supervised intervention.
Ramírez-Vélez18ColombiaCohort of 855 pregnant women who were randomized into an EG consisting of 429 pregnant women and another CG consisting of 426 pregnant women.It is a randomized controlled trial with concealment in distribution and evaluation.The aim is to find out if a series of 12-wk workouts is able to prevent gestational diabetes mellitus during the second trimester of pregnancy.All study participants received written advice on diet to follow, exercises to strengthen the pelvic floor, and possible lumbar pain in the area. Apart from this, the EG was subjected to 12 wk of activities directed by a physiotherapist. They were also encouraged to do 2 sessions per week of 45 min each in their own homes.Physical activity was part of a regimented and supervised intervention.
Kraschnewski et al19United StatesLongitudinal cohort of 2767 pregnant women, who were classified in BMI before pregnancy and if they subsequently exceeded or not the recommended weight during pregnancy according to their BMI.Longitudinal cohort study of 34 wk in patients recruited between 2009 and 2011.Analyze the relationship between the amount of physical exercise performed during pregnancy and the weight gain that occurs during pregnancy.All these women completed an initial survey in early pregnancy to know the level of physical activity prior to pregnancy, type, and weekly sessions. Throughout each quarter they were interviewed by telephone, continuing with these interviews until 3 y after childbirth.Regular physical activity, defined as >150 min of moderate-intensity activity per week was self-reported.
Sanabria-Martínez et al20Spain13 articles on the influence of physical activity in pregnant women.Selection of articles published in 1990 until May 2014.Study the effectiveness of performing physical exercises to prevent gestational diabetes during the second and third trimesters.A meta-analysis of randomized clinical trials is carried out.Physical activity was part of regimented and supervised interventions.
Nasiri-Amiri et al21IranCases: 100 pregnant women with gestational diabetes diagnosed after 20 wk of pregnancy.

Controls: 100 healthy pregnant women.
Case-control study in patients recruited between 2012 and 2015.Analyze the type and intensity of physical activity performed by pregnant women in the first 20 wk of pregnancy.All participants performed a blood glucose test. In turn, they filled out 3 forms on demographic data and physical activity details so far, while the physical tests performed in those 20 wk were evaluated at the time of registration.Physical activity was self-reported using the PPAQ.
B
AuthorResultsConclusionsLEGR
Haakstad and Bo17In the EG, a significant weight difference after delivery of 0.8 + 1.7 kg was observed only among women who had completed 24 exercise sessions, while the CG presented a gain of 3.3 + 4.1 kg.Women who performed moderate-intensity aerobic activity during the last 6 mo of pregnancy reduced the weight gain and did not exceed the weight established by the Institute of Medicine of the United States.2+C
Ramírez-Vélez18There was no significant difference in the prevalence of gestational diabetes between both groups with an HOMA-IR of −0.15; 95% CI, 0.33 to 0.03. Or in the oral glucose tolerance tests −0.13 mmol/L; IC = 95% CI: −0.28 to 0.03 in women with a normal-range BMI in the second trimester of pregnancy.A 12-wk project during the second trimester does not decrease the prevalence of diabetes in healthy pregnant women with a normal-range BMI.2+C
Kraschnewski et al19A small percentage did not participate in any physical session (28.1%). With this, the difference in weight gain of the active mothers was statistically significant with OR (95% CI) of 0.97 (0.79 to 1.2) among women with sessions of <1 h and of 0.72 (0.57 to 0.88) for women with sessions longer than 150 min. It is also observed that women with overweight and obesity were those who gained more weight during their pregnancy with an OR (95% CI) of OR = 5.11 (4.08 to 6.4) and OR = 2.35 (1.91–2.89), respectively.Women with a BMI greater than 25 have the highest odds of exceeding the weight gain values during pregnancy. However, women who exercise a physical activity with a minimum of 150 min/wk were less likely to exceed the recommendations of the Institute of Medicine of the United States on weight gain during pregnancy.2+C
Sanabria-Martínez et al20There is a strong association between exercise and risk of gestational diabetes that allows to reduce it by 31% with the greatest benefits when starting physical exercise in early pregnancy.Performing physical exercise at the beginning of pregnancy decreases the incidence of gestational diabetes mellitus, and weight gain thus improving the health of the offspring.2++B
Nasiri-Amiri et al21Women who had low levels of physical activity had a higher odds ratio to develop gestational diabetes mellitus (OR = 4.12; 95% CI, 2.28 to 7.43). Women with a BMI < 25 kg/m² before pregnancy had an 84% lower risk of developing GDM compared with BMI > 30 kg/m².There is a significant statistical correlation between the magnitude of moderate effort of a physical activity and a lower risk of developing gestational diabetes mellitus despite independent predictive factors such as BMI prior to pregnancy and family history.2-D

Abbreviations: BMI, body mass index, CG, control group; CI, confidence interval; EG, exercise group; GDM, gestational diabetes mellitus; GR, grade of recomendation; HOMA-IR, Homeostatic Model Assessment of Insulin Resistance; LE, level of evidence; OR, odd ratios; PPAQ, Pregnancy Physical Activity Questionnaire.

Table 4

Relationship Between Maternal Physical Activity and the Health of the Newborn

A
AuthorCountryNDesignObjectiveMethodologyPhysical activity
Szymansky and Satin22United StatesCohort of 45 healthy pregnant women distributed in 3 different groups of 15. These 3 groups were classified into nonactive groups, regularly active group, and highly active group.Study with patients recruited between 2010 and 2011.To analyze how the fetus reacts to a series of physical activity sessions between week 28 and 32 of gestation according to the current guidelines.All the sessions were done in a period of 2 wk. The 3 groups were subjected to a progressive ergometric test to volitional fatigue. In turn, the 3 groups repeated a half hour exercise on the tape. Finally, the 2 EGs (regular and high) repeated this last 30-min session.Physical activity 6 mo prior to pregnancy or during pregnancy was self-reported. Exercise test were continuously monitored.
Bisson et al23CanadaCohort of 65 women. All of them in gestation and recruited between week 15 and 17 of pregnancy.Study with patients recruited between 2010 and 2011.Check that fitness levels after 16 wk of gestation are related to physical levels prior to pregnancy, and how the birth weight of the newborn is related to this physical condition.The physical activity of the mother was estimated 3 mo prior to pregnancy and during the month before the 16th week of gestation independently, both through the questionnaire of physical activity of pregnancy. In terms of life habits and sociodemographic characteristics, they were extracted through interviews, and data on delivery and the baby were collected through maternal medical records.Physical activity during the 3 mo prior to pregnancy and during the month prior to testing were assessed separately and self-reported using the PPAQ.
Ferland et al24CanadaCohort of 94 women who were divided into 3 groups in relation to their frequency of physical activity. A first CG (N = 15), a second group that performs between 2 and 4 activities per month (N = 36) and a last group with more than 4 activities (N = 43).This is a secondary analysis of a prospective study of cohorts of women recruited between 2009 and 2010.Study the influence of sport during the first trimester of pregnancy on the growth of the fetus and the placental function.Blood samples were taken between week 11 and 13 of pregnancy together with Doppler study of the bilateral uterine artery and 3D examination of the placenta. In turn, during the 22nd and 23rd weeks of gestation, a questionnaire was administered through which detailed lifestyle information was obtained during the first 3 mo.Physical activity (20–30 min) during the 3 mo prior to assessment at 22/23 wk gestation was self-reported using a questionnaire.
Barakat et al25Spain320 pregnant women were chosen from a hospital database and randomly distributed in 2 different groups of 160 each, being identified as a CG and EG.It is a randomized controlled study with patients recruited between 2008 and 2011.Demonstrate that physical activity during pregnancy does not cause premature birth.The EG performed a physical schedule of 3 classes/wk (exercises that work the main muscle groups of the body) of a duration of 60 min, which begin between week 8 and 10 of gestation and end in weeks 38–39. Each participant had a heart rate meter to confirm that the activity that took place was of moderate intensity.Physical activity was part of a regimented and supervised intervention.
Harrod et al26United StatesCohort of 826 women who were studied together with their neonate children.Longitudinal trial of healthy Start with patients recruited between 2012 and 2013.To analyze how the neonate is influenced with regard to fat mass, fat-free mass, birth weight, and gestational age when the mother is subjected to physical activity during pregnancy.All the participants were invited to 3 medical visits to the respective research center. These 3 visits occurred during the first trimester, the second was performed around week 27 of gestation and the last one after delivery. In all of them, they filled out questionnaires to examine a general week of physical exercise.Physical activity during early pregnancy, mid-pregnancy and late pregnancy was assessed separately and self-reported using the PPAQ.
Seneviratne et al27New Zealand75 participants with a BMI > 25 kg/m2 were randomized into 2 groups, 1 EG (n = 38), and 1 CG (n = 37).Study with patients recruited between 2013 and 2014.To analyze how exercise could affect pregnancy in obese and overweight women on the results of the mother and the newborn.The CG was not subjected to any type of physical test but the EG made a total of 67 sessions during weeks 20 and 35 of gestation of a duration of half an hour using fixed magnetic bicycles.Physical activity was part of a regimented and supervised intervention.
Onoyama et al28United StatesCohort of 373 women in 2 cycles. A first cycle of n = 199 and a second cycle of n = 174.Study with patients recruited between 2004 and 2012.The main purpose was to assess whether the performance of prepregnancy exercise and during this increases the concentrations of stem cells in the umbilical cord and subjected to a flow cytometry.The participants were asked when they were in their respective delivery rooms. In addition, they filled in the International Physical Activity Questionnaire to obtain the maximum information about life habits prior to pregnancy and during the first 6 mo of pregnancy. In addition, blood samples were collected from the umbilical cord during delivery.Physical activity during the 12 mo before pregnancy, during first trimester, and during second trimester were assessed separately and self-reported using a semiquantitative questionnaire, modeled after the IPAQ.
Rêgo et al29BrazilBreeze cohort of 1380 pregnant women.Cohort study with patients recruited between 2010 and 2011.Analyze the possible relationship between physical activity during pregnancy and possible outcomes such as low birth weight, premature birth, and uterine growth restriction.All the participating women filled in 2 questionnaires. The first of them during the second trimester of pregnancy and in which it was intended to know the sociodemographic characteristics of the mother and her pattern of physical activity. In the second, carried out during the first 24 h after delivery, information about delivery and possible complications that may have occurred during the third trimester of pregnancy were recorded.Physical activity (<10 min) during the previous 7 d was self-reported using the IPAQ.
Reyes and Davenport30CanadaArticles about physical exercise as a therapeutic intervention to improve the weight of the fetus.Selection of published articles.Study the relationship between performing physical exercise during pregnancy and the risk of being underweight, the baby during pregnancy.A nonsystematic review was carried out.N/A
B
AuthorResultsConclusionsLEGR
Szymansky and Satin22In maternal terms, the lowest resting heart rate was found in the most active women.

Regarding measures of fetal well-being, no differences were found between the groups regarding the umbilical artery Doppler index; neither in terms of fetal heart rate (N-E: 149.5 [9.5], RA: 146.5 [10.8], and HA: 146.9 [7.3]).
The programs have been correctly accepted by both the mother and the baby without suffering any acute fetal adverse effect, thus allowing healthy mothers to follow an exercise program during pregnancy.2+C
Bisson et al23The level of activity was evaluated on average energy spent weekly (EE). There was a decrease in physical activity between the prepregnancy periods until the first trimester (37% [15%] of total EE at 30% [14%], P < .0001). There was also a positive correlation (r = .60, P < .0001) that all those mothers who exercised before pregnancy remained so at the end of the first trimester. Despite the decrease in activity during pregnancy, in infants of women with regular physical activity prior to pregnancy, a mean birth weight of 3326 (509) g with birth weight z score of −0.160 (0.956) was observed.Women physically active before pregnancy have greater facility to exercise a program of physical activity during pregnancy, this being recommended from the first 3 mo of pregnancy as they promote fetal development and a correct body composition of the newborn with weights at birth within the optimal values.2-D
Ferland et al24A significant reduction of the PIGF component was observed as the level of physical activity in the first trimester increased with a difference compared with the CG of −0.252 (−0.479 to 0.026) MoM with P = .03 in the case of the second group and with a difference of −0.330 (−0.552 to 0.108) MoM with P = .003 in the case of the third group.

However, no significant differences were found in the gestational age of the fetus at birth, in birth weight, or placental weight between groups.
Physical exercise is not recommended during the first 3 mo of pregnancy as it affects placental growth and the development of pregnancy.2+C
Barakat et al25The gestational age of the newborns was not altered by physical activity (39.7 [1.3] wk in the EG vs 39.6 [1.1] wk in the CG with P = .81). In turn, the state of the baby was not altered because there were no differences in the pH of umbilical cord blood (EG = 7.31 [0.7], CG = 7.30 [0.7]) nor in Apgar scores at minute and 5 min.Healthy, low-risk women during pregnancy can perform a sports plan whenever it is reviewed by a specialist staff because it does not affect gestational age or their fetal well-being.2+C
Harrod et al26The neonates that were found above the highest quartile of energy expenditure had a lower fat mass (249.4 vs 290.5 g, P = .03) with respect to those of the lowest quartile. Among these same quartiles, it was observed that there was a greater probability of having small newborns for their gestational age 3.0 (95% CI, 1.4 to 6.7). Of the 826 neonates, 107 were born with a small size with respect to their gestational age, while on the contrary, 30 were born with a size greater than their gestational age.The increase in energy expenditure during the last stage of pregnancy is related to a decrease in adiposity of the newborn but related to free fat mass and not to neonatal fat mass. An increase in neonates with a size smaller than their gestational age but related to the decrease in adiposity and not the limitation of growth at a systemic level has also been observed.2+C
Seneviratne et al27Birth weight was practically similar with similar weight percentiles (52% [33%] vs 43% [26%], P = .12). There were also no significant differences between the weight gained during pregnancy between the EG and the CG (12 [5.3] vs 13.2 [5.8], respectively, with 95% CI, 1.6 to 39 with P = .397). However, no more than 33% of the participants in the EG exceeded more than 30 sessions of the 67 that had been scheduled.Maternal physical exercise without moderate weight lifting in women with a BMI > 25 kg/m2 improved the aerobic conditions of the mother but had no impact on birth weight.2-D
Onoyama et al28It has been seen that vigorous exercise prior to pregnancy significantly increases 4 types of endothelial progenitor cell populations (P = .02, .01, .001, .003) but not with hematopoietic stem cells.

It has also been observed that moderate exercise during pregnancy is associated with a decrease in breast stem cells (which can subsequently lead to tumorigenesis), a discovery that can be a great step against breast cancer.
An increase in endothelial cells in umbilical cord blood has been observed after physical exercise prior to pregnancy, which could improve the cardiovascular well-being of the newborn.2+C
Rêgo et al29No association harmful to the fetus was detected between high levels of physical activity and low levels with respect to low birth weight with RR = 0.94; 95% CI, 0.54 to 1.63 and RR = 0.88; 95% CI, 0.57 to 1.35; P = .833, respectively.

There was also no significant relationship between high levels of physical activity and low relative to prematurity with a RR = 0.86; 95% CI, 0.48 to 1.55 and RR = 0.82; 95% CI, 0.53 to 1.26; P = .640. Therefore no relationship was detected between physical activity during the 9 mo of gestation and effects harmful to the fetus.
Any physical activity, whatever the level, is not related during the second quarter with harmful perinatal results.2+C
Reyes and Davenport30Adopting a healthy life during pregnancy, such as exercising, decreases the excess accumulation of fat in the fetus, and could improve the risk of cardiovascular disease, later, in the life of both mother and child.Physical exercise for pregnant women is healthy and beneficial for both the mother and the fetus. Prenatal physical exercise does not increase the risk of low birth weight in the baby. On the contrary, prenatal exercise is associated with the prevention of excessive accumulation of fat in the newborn and the maintenance of muscle mass.2-D

Abbreviations: BMI, body mass index, CG, control group; CI, confidence interval; EG, exercise group; ESW, energy spent weekly; IPAQ, International Physical Activity Questionnaire; GR, grades of recommendation; HA, highly active; LE, level of evidence; MoM, multiple of median; N-E, non-exercisers; PIGF, placental growth factor; PPAQ, Pregnancy Physical Activity Questionnaire; RA, regularly active; RR, rate ratio.

Table 5

Relationship Between Maternal Physical Activity and Development of Hypertension During Pregnancy

A
AuthorCountryNDesignObjectiveMethodologyPhysical activity
Martin and Brunner Huber31United StatesCohort of 3348 pregnant women of which 421 were diagnosed with hypertensive complications during pregnancy.Observational study of patients between 2004 and 2006.To analyze the association between physical activity and hypertensive complications through the use of a population-based surveillance system.A series of surveys is conducted for the North Carolina Monitoring System pregnancy risk assessment from 2 to 6 mo after delivery plus additional collection of birth certificates.Physical activity (30 min) 3 mo prior to pregnancy and during the last 3 mo of pregnancy was self-reported on questionnaires.
Kawabata et al32Japan17 women with normal pregnancy who were compared with 81 matched controls.Study of patients recruited during the first half of 2008.To analyze how exercise performance during the second and third semester influences arterial stiffness in order to avoid arterial function disturbances through ankle-brachial measurements (baPWV).All participants visited their clinic on a regular basis throughout the pregnancy until delivery. All of them were routinely evaluated for blood pressure, body weight, and pregnancy status. The EG performed aerobic sessions after week 16 of gestation in sessions of 60 min and at least 3 sessions per week.Physical activity was part of a regimented and supervised intervention.
Barakat et al33SpainCohort of 765 pregnant women, which were randomly distributed into 2 groups. One group exercised with 382 participants and a CG with 383 participants. In turn, each group was divided into waves, each of which was made up of 10 or 12 women.Randomized clinical trial with patients recruited between 2011 and 2015.To examine the result of a program of controlled physical activities during the gestation period and its repercussion in hypertension induced by pregnancy itself.The CG received guidance on their care during pregnancy and the positive effects of exercise. In turn, the EG received the same advice in addition to 3 sessions per week of physical activity of about 50 min per session from week 11 of pregnancy until weeks 38 or 39 with an initial planning of 85 sessions.Physical activity was part of a regimented and supervised intervention.
May et al34United StatesGroup of pregnant women divided into 2 groups. A CG consisting of a total of 30 members and a group exercising 26 women.Part of a longitudinal study.Evaluate whether physical exercise during pregnancy can affect the functioning of the maternal and fetal autonomic nervous system.Both groups completed the physical activity questionnaire that could be modified twice during the 12 mo of the study. The first time was to report on the 3 mo prior to pregnancy, to classify the participants in the 2 CGs and the second time at the end of the pregnancy. During weeks 28, 32, and 36 of pregnancy all groups were subjected to sessions of 18 min along with a magnetocardiogram to record both the variability and possible fluctuations of heart rate.Physical activity was self-reported twice by each subject in the 3 mo prior to conception and throughout the pregnancy using the Modifiable Physical Activity Questionnaire.
Haakstad et al35NorwayCohort of 51 pregnant women, all inactive, distributed in: EG: 35 members.

CG: 26 members.
Randomized controlled trialTo assess how the resting heart rate varies in pregnant women and how the heart rate varies during moderate-intensity physical activity in which the counselor and participants were blinded.Sociodemographic data of the participants were taken in addition to extraction of more data such as systolic or diastolic pressure. These measurements took place during the second trimester of pregnancy (initial visit) and between week 36 and 38 after physical activity. In these sessions, the EG performed 2 sessions per week of 60 min with an expert in aerobic exercises and with a minimum time of 12 wk.Physical activity was part of a regimented and supervised intervention.
Santos et al36Brazil28 healthy pregnant women with a single fetus with a fetal viability of 26 wk.Transversal studyEvaluation of acute effects in the hemodynamics of the fetus and the mother of low-risk exercises.The investigation was carried out in 3 phases. An initial one in which blood pressure, heart rate, and cardiotocography were measured; a second phase in which fetal growth was evaluated and an exercise session and a last phase of measurement of the same elements as at the beginning.Women with no regular physical activity prior to pregnancy underwent regimented and supervised aerobic physical exercise sessions at 2 different moments with an interval of at least 4 wk.
B
AuthorResultsConclusionsLEGR
Martin and Brunner Huber31A 47% reduction was observed in women with physical activity between 1 and 4 d/wk (OR = 0.63; 95% CI, 0.45 to 0.95) while women with equal or greater activity at 5 d/wk it was reduced by 54% the odds of hypertensive complications during pregnancy (OR = 0.46; 95% CI, 0.2 to 1.02).Both inactive and physically active women before pregnancy can take advantage of exercise during pregnancy to reduce the development of hypertensive complications during their course.2+C
Kawabata et al32It has shown that in the CG there was a significant increase in arterial stiffness from 1116.7 (87.9) cm·second−1 in the early second trimester to 1160.2 (109.1) cm·second−1 1-month after delivery. In contrast, in the EG the increase is not significant, going from 1122.7 (100.2) cm·second−1 to 1145.9 (88.1) cm·second−1.Maternal trainings performed regularly during pregnancy without any contraindication decrease arterial stiffness, which can help prevent hypertensive disorders during pregnancy.2-C
Barakat et al33Physical activity decreased the rates of hypertension from 2.1% to 5.7% in the CG with a P = .009. Likewise, it also reduced preeclampsia levels from 0.5% in the EG to 2.3% in the CG with P = .03. On the other hand, pregnant women who did not perform any physical activity were 3 times more likely to develop hypertension during pregnancy (OR [95% CI] = 2.96 [1.29 to 6.81], P = .01).The risk of hypertension has been reduced, there has not been an excessive increase in gestational weight without varying the gestational age. The number of premature births has not increased as well as the incidence of macrosomia in the newborn has been diminished.2+C
May et al34The results show a significant increase in parasympathetic control measures over time at weeks 28, 32, and 36 of pregnancy with P values of .01, .002, and.03, respectively, indicating that autonomic tone improves throughout pregnancy. However, only a significant decrease with respect to heart rate was observed at week 28. With a value of 85.3 (8.9) pulses/min in the CG compared with 79.7 (7.3) in the EG. Even so, regardless of whether the pregnant mother exercises physical activities, there is a progressive increase in the maternal heart rate.Maternal exercise during pregnancy shows improvements in cardiac autonomic control, such as reducing heart rate and increasing the variability of heart rate, which helps reduce effects such as gestational hypertension or preeclampsia.2-D
Haakstad et al35As a primary data, the resting blood pressure was analyzed. Regarding systolic blood pressure, a difference of 7.5 mm Hg (95% CI, 1.5 to 12.6; P = .013) and diastolic pressure 3.9 mm Hg (95% CI, −0.07 to 7.8; P = .054) was observed. The same happened with blood pressure during exercise, finding differences of 5.9 mm Hg (95% CI, 4.4 to 16.1 P = .254) and 5.5 mm Hg (95% CI, −0.2 to 11, 1 P = .059), respectively, giving evidence that hypertension can be prevented during the 9 mo of pregnancy by exercise.Regular exercise after the second trimester of pregnancy decreases blood pressure in inactive women and may be useful in the prevention of hypertension caused by pregnancy.2+C
Santos et al36The fetal heart rates did not show significant variations before and after physical exercise. But instead the heart rates and maternal blood pressure before and after exercise showed significant values, giving an increase in both parameters.Pregnant women at low risk undergoing regular exercise, performed gradually and not exceeding 85% of the maximum heart rate, presented minimal hemodynamic changes such as vasodilatation of the umbilical artery to ensure fetal homeostasis.2-D

Abbreviations: BMI, body mass index, CG, control group; CI, confidence interval; EG, exercise group; OR, odd ratios; PWV, pulse wave velocity.

Table 6

Mental Health, Abortion, Premature Birth, and Maternal Physical Activity

A
AuthorCountryNDesignObjectiveMethodologyPhysical activity
Songøygard et al37NorwayCohort of 855 pregnant women who were randomized into 2 groups: CG and intervention group. Within which they also separated when lifting in blocks of 30.Randomized control trial with patients recruited between 2007 and 2009.Demonstrate whether physical activity during pregnancy can reduce the risks of postpartum depression.Both groups received advice from their midwife about diet, pelvic floor, and possible pain. The intervention group, on the other hand, from the 20th week of gestation to the 36th week, participated in sports classes led by a physiotherapist in 60-min sessions. Three months after birth, the participants were asked to complete the Edinburgh Postnatal Depression Scale.Physical activity was part of a regimented and supervised intervention.
Barakat et al38SpainCohort of 290 White pregnant women chosen from a hospital database, separated into 2 different groups at random. A group of 138 women, exercise group, and CG formed by 152.Randomized controlled trialFind out how the type of delivery is affected after a program of physical activities that are carried out throughout the entire pregnancy (9 mo).The EG was subjected to 3 sessions on a weekly basis lasting around 45 min from week 6 of pregnancy to week 38. During these sessions, supervised by a specialist in the subject and with the presence of a gynecologist, the main muscle groups in the extremities and abdomen were strengthened and with the presence of a gynecologist.Physical activity was part of a regimented and supervised intervention.
Perales et al39SpainA total of 167 pregnant women accepted participation in the study. All of them were distributed randomly in 2 groups, a CG of 77 participants and a group exercise of 90 participants.Randomized clinical trial carried out by 3 different authors to make the blinding of the process and results analysis simpler.Analyze whether a controlled and supervised exercise program may be able to reduce the symptoms of depression in pregnant women.Both groups received the frequent information offered by their midwives or health professionals. In addition, the EG participated from week 9–12 of pregnancy until week 39–40 in 3 sessions per week supervised by a specialized trainer staff and the presence of an obstetrician to facilitate full participation in the program.Physical activity was part of a regimented and supervised intervention.
Hegaard et al40Brazil5 articlesSelection of articles.Establish the possible dangers of physical activity during the first trimester of pregnancy.A systematic review is carried out.Physical activity description and measurement varied and was either measured with a portable ECG or self-reported as type of exercise and minutes of exercise per week, dichotomized (≥30 min ≥2 times per week) or categorized (number of times engaging in physical activity/strenuous exercise per week).
Shakeel et al41Norway643 pregnant women.Cohort study with pregnant women (58% ethnic minorities) during pregnancy and after childbirth between 2008 and 2010.To investigate whether physical activity during pregnancy was inversely associated with symptoms of postpartum depression in a multiethnic sample.Demographic data and health outcomes were collected through standardized interviews. The symptoms of postpartum depression were defined by a total score ≥10 on the Edinburgh Postnatal Depression on Scale, 3 mo after birth. Physical activity was recorded in the week of gestation 28 and defined as moderate to vigorous intense, accumulated in periods of ≥10 min.Physical activity was recorded with Sense Wear™ Pro3 Armband (Body Media Inc., Pittsburgh, PA).
B
AuthorResultsConclusionsLEGR
Songøygard et al37No significant differences were found between the 2 groups, since they only found a 3.2% score of Postnatal Depression Scale of Edinburgh equal to or greater than 13. However, a subgroup within the intervention group that does not exercise consistently prior to pregnancy has a lower risk of postpartum depression.It has not been possible to assure that the accomplishment of physical exercise during the childbirth diminishes the probability of suffering postpartum depression.2+C
Barakat et al38Yes, it is true that there was a lower number of cesarean sections in the EG with a total of 5 compared with 27 in the CG, but the difference was not significant according to the statistics. Although the number was lower, a relative risk was seen in the group performing cesarean sections compared with the CG (0.69; 95% CI, 0.42 to 0.82). There was also a lower number of instrumental births in the EG compared with the CG (16 vs 29).Given the results, a sports program of moderate intensity is recommended for healthy pregnant mothers as it reduces the rate of cesareans and of instrumented deliveries.2+C
Perales et al39At the beginning of the study, the levels of depression in both groups were practically similar (EG: 9.87 [8.9] vs CG: 9.38 [8.10], t165 = 0.36 and P = .71). In contrast, in the third quarter, the differences between both groups were significant (EG: 7.67 [6.30] vs CG: 11.34 [9.74]; t126 = 2.83, P = .005) demonstrating that physical activity during pregnancy decreases the chances of suffering depression.The development of moderate-intensity physical activity supervised during the months of pregnancy has decreased levels of depression without having consequences on maternal and fetal life.2+C
Hegaard et al40High intensity exercise such as running or ball games are related to a greater danger of spontaneous abortion. In contrast exercise such as cycling or swimming were not associated with spontaneous abortion in a statistical way. It should be noted that exercise does not increase the risk of abortion once the first 3 and a half months of pregnancy have passed.During early pregnancy, physical exercise performed for more than 2 d increases the risk of spontaneous abortion. The same happens between active pregnant women and nonactive women. However, the danger of abortion is not increased after the first 3 mo of pregnancy.2+C
Shakeel et al41Women who accumulated ≥150 min/wk of moderate–vigorous physical activity had a significantly lower risk (OR = 0.2, 95% CI, 0.06 to 0.90), for symptoms of postpartum depression, compared with those who had not accumulated.Women who meet the recommendations (150 min/wk of moderate–vigorous physical activity) during pregnancy have a lower risk of having symptoms of postpartum depression compared with women who are not active during pregnancy.2++B

Abbreviations: CG, control group; CI, confidence interval; ECG, electrocardiogram telemetry system; EG, exercise group; OR, odd ratios.

Data Analysis

Table 3A shows that 51721 of the 25 studies are based on the analysis of the benefits of performing physical exercise during pregnancy in overweight mothers or those with gestational diabetes mellitus. Three studies18,20,21 analyze the development of gestational diabetes mellitus: in one20 they find greater benefit if exercise occurs early in pregnancy and in another21 they find a relationship between higher level of physical exercise with a lower incidence of gestational diabetes mellitus during the 9 months of gestation, with this benefit increasing when the values of body mass index are <25 kg/m2. However, the third study18 does not find significant results. The other 2 studies17,19 analyze the relationship between weight gain during pregnancy and the realization of a physical exercise program: in one of them,17 they find that mothers who performed physical activity during the last 6 months of pregnancy presented the least weight gain after childbirth; and in the other,19 focused on the time dedicated to exercise, the group of women who devoted more than 150 minutes per week was less likely to exceed the recommendations on weight gain during pregnancy.

Table 4A shows that 9 studies2230 of the 25 that meet the requirements are based on the analysis of maternal physical activity and the health of the newborn. None of the studies conclude against performing exercise during pregnancy, with the exception of Ferland et al,24 which concludes that no physical activity should be performed during the first trimester of pregnancy because the levels of the growth factor may decrease during this period of time as a result of physical activity. However, the rest of the selected studies have not found harmful effects on the health status of the newborn.

Among the authors who study the birth weight of the newborn,24,25,2730 none of them observed significant variations in weight. The slight weight variations observed were caused by the decrease in the adiposity of the baby, which is why these studies do not oppose the performance of physical exercise during pregnancy.

Six of the studies3136 deal with the relationship that can be established between pregnant mothers with hypertension during pregnancy and the performance of physical activity without danger to the baby (Table 5A). In 5 of the studies,3135 performing physical exercise can reduce the risk of high blood pressure. Barakat et al33 goes further concluding that the physical activity programs carried out have no impact on the newborn. For Santos et al,36 physical exercise does not cause changes that are detrimental to the normal development of pregnancy.

In relation to the studies3741 on physical exercise during pregnancy and postpartum depression, miscarriage, and preterm birth shown in Table 6A, not all the studies were directed towards the same objective. Three of them investigate whether performing physical exercise during pregnancy is associated with symptoms of postpartum depression.37,39,41 For 2 of the studies,39,41 performing physical exercise during pregnancy decreases the risk of depression, while the third37 concludes that it has not been possible to ensure that the performance of physical exercise during pregnancy reduces the likelihood of suffering postpartum depression. Barakat et al38 focused on the type of delivery after a sports program throughout the pregnancy with the exception of the first month, thus decreasing the number of instrumented and cesarean section deliveries. Finally, it is worth highlighting Hegaard et al40 does not recommend physical exercise during the first trimester of pregnancy as it increases the risk of spontaneous abortion.

Discussion

In the present study, a review of the literature on physical activity during pregnancy and its effects on the health of the mother and the newborn was carried out. It was identified that most of the studies support the performance of moderate-intensity exercise due to its multiple benefits; and that a good physical form prior to pregnancy improves the symptoms associated with pregnancy and ensures a good predisposition of the mother to physical activity during pregnancy. Among the benefits to the mother of physical activity during pregnancy are the improvement of cardiovascular function, a decrease in the risk of gestational diabetes mellitus, hypertension caused by childbirth, the limitation of weight gain during pregnancy, fewer complications in childbirth as well as the increased release of endorphins produced during the practice of physical exercise because a high level of these is considered a natural analgesic. On the other hand, regarding benefits on the child, lower percentage of body fat, increased gestational age, and potentially improved neurodevelopment have been described.42

Obesity is one of the most important health problems worldwide due to the exponential growth that it is having in recent years, manifesting more in the female gender. The importance of having a prepregnancy body mass index <25 is noteworthy, as it is associated with a lower weight gain during pregnancy.19 Haakstad and Bo17 adds that this reduction in weight gain is favored with the performance of moderate-intensity aerobic activities during the last 6 months of pregnancy. Therefore, it could be recommended that in the case of a body mass index >5, the performance of physical exercise should be a main part of the weight-loss program with a minimum of 30 minutes of duration and 5 days of moderate intensity.

Another of the metabolic changes that may favor obesity is gestational diabetes, which can lead to diabetes mellitus type 2 in up to 40% of cases with the corresponding health risks.43,44 During gestational diabetes, there are failures in the secretion of insulin, caused by placental hormones responsible for maintaining high blood glucose levels so that it is available to the fetus, which may cause hyperglycemias and increase insulin resistance.45 In these cases, the performance of physical activity can play an important role because it increases the energy requirements of glucose by the muscles, decreases the blood glucose and the insulin necessary for this glucose to be absorbed by the cells. Sanabria-Martinez et al20 associates physical activity at the beginning of pregnancy with a decrease in the incidence of diabetes mellitus, unlike Ramírez-Vélez18 who does not find an association between physical exercise and gestational diabetes during the second trimester. These results highlight the importance of when in pregnancy it may be more beneficial to perform physical exercise to reduce the incidence of gestational diabetes.

Gestational hypertension is the most frequent medical complication during pregnancy, it occurs in 8% to 10% of all pregnancies and is the leading cause of maternal mortality in the world.46,47 A decrease in uterine blood flow has been observed when pregnant women performed a moderate-intensity physical activity, and this decrease intensifies as the intensity of the effort increases. This decrease in blood flow reduces the availability of oxygen; however, oxygen delivery to and utilization by the fetoplacental unit is maintained by several mechanisms.48 Considering the studies focused on the relationship between physical activity and arterial hypertension, the results do not diverge with different authors31,32,35,38 establishing that physical exercise during pregnancy reduces the risk of arterial hypertension. Martin and Brunner Huber31 may present information bias as information on the physical activity of pregnant mothers during their pregnancy and was obtained through surveys 2 to 6 months after delivery. Physical exercise reduces the risk of preeclampsia and stimulates the growth and vascularization of the placenta, the reduction of oxidative stress, and benefits on endothelial function.49 Barakat et al33 found a decrease in the risk of hypertension during pregnancy, a lower risk of macromia among women who exercised during pregnancy and did not identify a reduction in the weeks of gestation. Physical activity is, therefore, important as a preventive measure, which can cause gestational hypertension to go no further, thus avoiding the need for medication, for example, beta-blockers such as atenolol and metoprolol, which should be avoided before week 27 of gestations as their use has been associated with low birth weight placentas and delayed fetal growth.50 The same happens with angiotensin-converting enzyme inhibitors and angiotensin II receptor antagonists, which are contraindicated, as their use has been associated with neonatal anuria, pulmonary hypoplasia, and neonatal death.51

For Barakat et al,38 a program of physical exercise during pregnancy after the 6th week would allow reduction of both premature birth and the need for cesarean section. The rate of cesarean sections recommended by the World Health Organization is between 10% and 15%52 compared with 25% in Spain.53,54 The instrumentalization of delivery and cesarean section favors an increased risk of infection, hemorrhage, and intense blood clots as well as an increased risk of placenta previa.55 For all these reasons, maternal physical exercise during pregnancy could be an alternative in the prevention of these complications. The same results are described by Barakat et al,38 which has seen reduced rates of premature births with maternal physical activity programs during pregnancy.

In the studies reviewed, it is described that pregnant mothers’ greatest concern with performing physical exercise during pregnancy refers to the risk of miscarriage. Hegaard et al40 confirms this risk of miscarriage during the first trimester, which may be due to the fact that this period is when the division and implantation of the fertilized ovum takes place, in addition to the formation of the first structures and vital organs in the baby. However, after 12 weeks of gestation, a physical exercise plan could be followed safely.

Mental health during pregnancy is a topic of growing interest because during pregnancy hormonal changes may favor the development of mental health problems, which are estimated to affect as many as 1 in 5 pregnant women.56 Perales et al39 analyzed the possible relationship between the practice of physical exercise and mental health, concluding that it was beneficial for the mother as well as for the fetus. Another worrisome symptom among mothers is postpartum depression. Shakeel et al41 concludes that women who meet the physical activity recommendations during pregnancy (150 min/wk of moderate–vigorous physical activity) have a lower risk of having symptoms of postpartum depression compared with women who are not active during pregnancy. The specific causes are unknown, but the hormonal levels of estrogen and progesterone, as well as sadness and lack of sleep can lead to physical discomfort and exhaustion.56 However, Songøygard et al37 found no association between postpartum depression and the practice of physical activity.

Overall, the studies reviewed are limited in terms of the quality of the research, out of the 25 articles selected only 8% obtained sufficient experimental rigor to be considered as grade B studies (2 ++). Second, the different studies reviewed show large differences in sample size and the methodology used in obtaining information on physical exercise is very variable, all of which makes it difficult to integrate the results. Clinical tests that pose any risk to the health of the pregnant women or to the fetus cannot ethically be performed, which limits the designs that can be applied to this subject. Given all this, this review may be limited, and it is necessary to carry out more exhaustive studies on this subject.

Conclusions

The practice of physical exercise during pregnancy has benefits for both the mother and baby. Currently, there is scientific evidence that supports the inclusion of a monitored physical activity program in the daily activities of pregnant women.

Acknowledgment

This work received no specific funding.

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If the inline PDF is not rendering correctly, you can download the PDF file here.

Morales-Suárez-Varela, Peraita-Costa, Llopis-Morales, and Llopis-González are with the Area of Preventive Medicine and Public Health, Department of Preventive Medicine and Public Health, Food Sciences, Toxicology and Legal Medicine, Faculty of Pharmacy, Universitat de València, Burjassot, Valencia, Spain. Morales-Suárez-Varela, Peraita-Costa, and Llopis-González are also with the CIBER in Epidemiology and Public Health (CIBERESP), Madrid, Madrid, Spain. Clemente-Bosch is with the IES Federica Montseny, Burjassot, Valencia, Spain. Martínez is with the Department of Nursing, Faculty of Nursing and Podiatry, Universitat de València, Valencia, Valencia, Spain.

Morales-Suárez-Varela (maria.m.morales@uv.es) is corresponding author.
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    Hegaard HK, Ersbøll AS, Damm P. Exercise in pregnancy: first trimester risks. Clin Obstet Gynecol. 2016;59(3):559567. PubMed ID: 27042797 doi:10.1097/GRF.0000000000000200

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    Shakeel N, Richardsen KR, Martinsen EW, Eberhard-Gran M, Slinning K, Jenum AK. Physical activity in pregnancy and postpartum depressive symptoms in a multiethnic cohort. J Affect Disord. 2018;236:93100. PubMed ID: 29723768 doi:10.1016/j.jad.2018.04.081

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    Prather H, Spitznagle T, Hunt D. Benefits of exercise during pregnancy. PM&R. 2012;4(11):845850. doi:10.1016/j.pmrj.2012.07.012

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    Moore LE. Pathophysiology of insulin resistance. In: Diabetes in Pregnancy. Cham, Switzerland: Springer; 2018:15.

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    Lo JO, Mission JF, Caughey AB. Hypertensive disease of pregnancy and maternal mortality. Curr Opin Obstet Gynecol. 2013;25(2):124132. PubMed ID: 23403779 doi:10.1097/GCO.0b013e32835e0ef5

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    Roberts JM, Pearson G, Cutler J, Lindheimer M. Summary of the NHLBI working group on research on hypertension during pregnancy. Hypertension. 2003;41(3):437445. PubMed ID: 12623940 doi:10.1161/01.HYP.0000054981.03589.E9

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    Clapp III JF. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur J Obstet Gynecol Reprod Biol. 2003;110:S80S85. PubMed ID: 12965094 doi:10.1016/S0301-2115(03)00176-3

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    Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS. Association of maternal endothelial dysfunction with preeclampsia. JAMA. 2001;285(12):16071612. PubMed ID: 11268269 doi:10.1001/jama.285.12.1607

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    • PubMed
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    Bayliss H, Churchill D, Beevers M, Beevers D. Anti-hypertensive drugs in pregnancy and fetal growth: evidence for “pharmacological programming” in the first trimester? Hyperten Pregnancy. 2002;21(2):161174. doi:10.1081/PRG-120013785

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    Bullo M, Tschumi S, Bucher BS, Bianchetti MG, Simonetti GD. Pregnancy outcome following exposure to angiotensin-converting enzyme inhibitors or angiotensin receptor antagonists: a systematic review. Hypertension. 2012;60(2):444450. PubMed ID: 22753220 doi:10.1161/HYPERTENSIONAHA.112.196352

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    World Health Organization Department of Reproductive Health and Research. WHO statement on caesarean section rates. https://apps.who.int/iris/bitstream/handle/10665/161442/WHO_RHR_15.02_eng.pdf;jsessionid=6E4502491B76AAD3580EE81F560B833C?sequence=1. Updated 2015.

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    Ministerio de Sanidad Servicios Sociales e Igualdad. Informe anual del sistema nacional de salud 2017: Actividad y calidad de los servicios sanitarios. 2018;14.

    • Search Google Scholar
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    Ministerio de Sanidad Consumo y Bienstar Social. Portal estadístico área de inteligencia de gestión. https://pestadistico.inteligenciadegestion.mscbs.es/publicoSNS/Comun/Cubo.aspx?IdNodo=14041. Updated 2018.

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    MedlinePlus. C-section. https://medlineplus.gov/ency/article/002911.htm. Updated 2019. Accessed June 18, 2019.

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    • Export Citation
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