Abstract
In this chapter, physiological adaptations to pregnancy are summarised as knowledge of the fundamental; physical adaptations that occur during pregnancy are important to understand the influence of physical activity on maternal and foetal outcomes. Cardiovascular, respiratory, musculoskeletal and endocrine adaptations that occur during pregnancy are briefly explained while metabolic adaptations are specifically addressed due to the importance of the energy balance during pregnancy. Measuring physical activity during pregnancy, subjective versus objective, forms an integral part of the energy balance and is presented, specifically longitudinally; physical activity patterns are poorly understood and concurrently reviewed. Physical activity tends to decrease during pregnancy in spite of the conclusive evidence in the literature of the benefit of regular physical activity during pregnancy. The findings are not always communicated to pregnant women and this has led to a misconception that physical activity might be detrimental during pregnancy. The possible risk associated with physical activity is therefore discussed, as well as the guidelines for physical activity during pregnancy to ensure a beneficial and safe antenatal period. The importance of understanding the role of habitual physical activity in high-risk pregnancy is presented. Finally, the influences of physical activity during pregnancy on birth outcomes are addressed based on the hypothesis set by the “theory of foetal origins” that states that the maternal environment influences foetal growth.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
Introduction
Regular physical activity during pregnancy benefits both maternal and infant health [1]. Regardless of the physiological changes women undergo during pregnancy, pregnant women benefit from physical activity just as much as nonpregnant women [2]. The complexity of assessing physical activity during pregnancy hampers the determination of the optimal amount of recreational physical activity for pregnant women [3] and has led to broad physical activity guidelines being proposed for pregnant women. Concurrently, pregnancy is characterised by a reduction in physical activity [4] resulting in discrepancies between physical activity during pregnancy and the guidelines set by various institutional and governmental entities [5–12].
Physiological Adaptations to Pregnancy
The duration of a pregnancy averages 266 days (38 weeks) after ovulation, or 280 days (40 weeks) after the first day of the last menstrual cycle. This period equals 10 lunar months, or just over 9 calendar months [13]. Physiological changes during pregnancy are divided into a series of stages and sub-stages, and the entire process is then subdivided into three relatively equal trimesters [14].
All maternal physiological systems adapt to the demands of pregnancy; however, the quality, degree and timing of the adaptation varies from one individual to the next and from one organ system to another [15–16]. The adaptations are mostly mediated due to the effects of progesterone and oestrogen that are produced, predominantly by the ovary in the first 12 weeks of pregnancy and thereafter by the placenta [15]. These adaptations enable the foetus and placenta to grow and prepare the mother and baby for parturition [15, 17].
Physiological changes, as a result of pregnancy, represent a serious challenge to all body systems [17]. While these adaptations do not pose major risks for healthy women, the normal physiological changes of pregnancy can place significant strain on already compromised systems, threatening the lives of both the mother and the foetus during parturition [17] .
Cardiovascular Adaptations During Pregnancy
Profound physiological changes occur in the cardiovascular system during pregnancy [17]. Circulating blood volume increases in order to meet the demands of the developing foetus and placenta. During pregnancy, there are major alterations in blood volume, constituents of cells and coagulation factors [16, 17]. A substantial part of maternal weight gain during pregnancy results from fluid accumulation, specifically plasma volume [16]. This increase in plasma volume supplies the necessary nutrients to the uterus and the placenta and ensures the removal of waste products from the uterus and placenta [14]. The increase in the plasma volume is to counter the decrease in the low pressure circulatory system that resulted due to the increase in vascular dilatation. Overall blood pressure decreases too, more specifically diastolic blood pressure to a greater extent than systolic blood pressure [14]. Blood pressure decreases despite an increase in blood volume and cardiac output, due to a decrease in systemic and pulmonary vascular resistance [18]. In addition to the previously mentioned changes, change to the cardiovascular system includes an increase in cardiac output, the product of heart rate and stroke volume [14, 19]. Initially, the increase in cardiac output is mediated by the increase in stroke volume. As pregnancy progresses, an increase in heart rate becomes the dominant factor to increase the cardiac output [18].
Respiratory Changes During Pregnancy
Numerous changes occur in the maternal respiratory system during pregnancy to ensure sufficient oxygen supply to the placenta for increased foetal energy demands and for foetal physiology [15–17]. The net physiologic change in the respiratory system is a lowering of the maternal PCO2 to facilitate effective exchange of CO2 from the foetus to the mother [16, 17]. The oxy-haemoglobin dissociation curves of foetal haemoglobin and adult haemoglobin allow the foetus to extract oxygen effectively from the maternal circulation [16]. The effects are mediated by hormonal factors that influence the respiratory centre, specifically progesterone [20]. An increase in progesterone stimulates the respiratory centre to increase minute volume, lowers the threshold of carbon dioxide concentrations [20] and may also decrease airway resistance, facilitating a greater airflow during maternal respiration [21, 22].
Musculoskeletal Changes During Pregnancy
Hormonal changes, specifically, changes in progesterone and relaxin levels, lead to increased joint laxity and hyper-mobility [23], which could potentially raise the risk of injury during exercise in pregnancy [10] . Increased body weight, as a result of foetal growth , increases the forces imposed on the joints such as the hips and knees [24]. Since the abdomen expands anterior during foetal growth, the centre of gravity shifts during pregnancy, resulting in postural adjustments, specifically an extension of the lumbar spine [14], which realigns the body mass above the base of support [25]. Elongation and decreased tone of the abdominal muscles may ensue because of the prolonged maintenance of the abovementioned position [14]. The combination of weight gain, altered postural alignment and ligamentous laxity causes changes in proprioception and postural balance in pregnant women [26]. The postural changes associated with pregnancy result in pregnant women adapting their stance and gait with a longer double limb support time and changes in the angles of hip, knee and ankles, suggesting an adaptation in locomotion to become more efficient [27] that might also influence energy expenditure of gait during pregnancy.
Endocrine Changes During Pregnancy
Since the development of the foetal origin of disease in later life hypotheses (described later in this chapter) , plenty of research focused on the intra-uterine environment, specifically with regard to hormonal changes during gestation as summarised by Kuijper et al. [28] in a systematic review that found both endogenous and maternal hormones to influence the foetus. Foetal development and sustained essential physiological functions for both mother and foetus are mediated by an increase in the release of specific hormones [29] such as oestrogen, progesterone, human chorionic gonadotropin, prolactin, adrenocorticotropic hormone, thyroid-stimulating hormone, cortisol and thyroid hormones [30]. The mass of cells that forms on the ovaries, the corpus luteum, is the main source of pregnancy-sustaining hormones during the first 6–8 weeks of gestation [31]. As previously mentioned, the majority of hormonal changes in pregnancy are related to the activity of the placenta [30]. The placenta takes over the role of the corpus luteum later in the pregnancy. The changes to hormones during pregnancy and their effects include:
-
Oestrogen, which stimulates glandular tissue and ducts in the breast and increases prostaglandin and oxytocin production [13].
-
Progesterone, which mediates vital physiological function during pregnancy, including an increased mobility of the joints [13].
-
Relaxin, which functions synergistically with progesterone to decrease uterine activity during pregnancy and to suppress oxytocin release [14]. Relaxin also affects the connective tissue to increase the mobility of the joints, in a similar way to progesterone [26].
-
Cortisol secretion, which increases from the second trimester of pregnancy to meet the body’s extra metabolic workload [30].
-
Human chorionic gonadotropin levels increase, which is linked to changes in appetite, sleep patterns and food tolerance in the first trimester [30].
-
Thyroid hormones, both T3 and T4, increase, causing the basal metabolic rate to increase during pregnancy [32].
In summary, the changes observed in the physiological systems during pregnancy (Fig. 16.1) simulate the adaptations observed in nonpregnant women who perform regular aerobic exercise to a large degree.
Summary of the physiological adaptations during pregnancy
Metabolic Adaptations to Pregnancy
Energy Intake During Pregnancy
The physiological changes that occur during pregnancy cause an increased demand for dietary energy as a result of increased oxygen consumption, respiration, circulation and renal function of the foetus during development [33]. From conception to birth, all the growth of the foetus is possible because of the nutrients the mother consumes [34]. The nutrient needs during pregnancy and lactation are higher than any other time in a woman’s life [34]. This high nutrient demand during pregnancy is met with an increased energy intake, as well as help from the mother’s body that maximises absorption and minimises energy expenditure [34].
The energy needs of pregnant women exceed those of nonpregnant women by an additional 340 kilocalories per day during the second trimester and extra 450 kilocalories per day during the third trimester [34]. The additional kilocalories represent 15–20 % more food than before pregnancy for an average 2000-kilocalorie daily intake. Ample carbohydrates are essential for fuel to the foetal brain, which ensures that the protein needed for growth is catabolised and used to synthesise glucose [34]. The extra energy demands of pregnancy can be met by an increase in food intake or by the mobilisation of energy fat stores of the mother, particularly those mothers with sufficient energy reserves [35].
The additional energy requirements during pregnancy can be described as the energy needed for maternal tissue and foetal growth , as well as the energy required for the rise in basal metabolic rate and the changes in physical activity [35]. Energy requirements during pregnancy remain controversial because of conflicting data on maternal fat deposition and putative reductions in the mother’s physical activity as the pregnancy advances [36].
Energy Expenditure During Pregnancy
Total daily energy expenditure (TDEE) consists of three general factors: resting metabolic rate, thermogenic effect of feeding and physical activity [34, 37]. TDEE for the nonpregnant healthy woman is calculated as the energy expended on resting metabolic rate (60–75 %), thermogenic effect of feeding (10 %) and physical activity (25–30 %). TDEE increases during pregnancy because of tissue growth, an elevated basal metabolic rate and the increased energy costs of moving a heavier body [38].
Resting metabolic rate (RMR) accounts for all the metabolic activities in the human body [34]. Human metabolism involves all the body’s chemical reactions of biomolecules that cause anabolism and catabolism. RMR varies dramatically from person to person and for the same individual with a change in circumstances or physical condition (with pregnancy being an extreme physiological condition) [34]. Pregnancy is a dynamic, anabolic state where the human body obtains energy for growth and maintenance [39].
The enhanced work of pregnancy raises the RMR dramatically and demands extra energy [40, 41]. This is calculated by Prentice et al. [42] as 20 % in late pregnancy. Forty percent of this variability is explained by the percentage of total body fat before pregnancy and the gain in body weight during pregnancy [35, 41]. Body fat gain accounts for about 55.5 ± 20 % of total weight gain during pregnancy [43]. According to Löf et al. [41], factors that are responsible for the variability in RMR response during pregnancy differ in the earlier and later trimesters of pregnancy . Most of the total body fat mass is deposited during the second trimester, with little change taking place in the first and third [44]. Chamberlain and Popkin [33] developed a theoretical model to estimate energy requirements during pregnancy (Fig. 16.2) [45], assuming an average gestational weight gain (GWG) of 12.5 kg (≈ 0.925 kg protein, ≈3.8 kg fat, and ≈ 7.8 kg water), which is associated with an increase in RMR [41].
Estimated factors contributing to weight gain during pregnancy. (Based on data from [45])
The thermogenic effect of food is attributed to the digestion process and the energy cost of storage of the exogenous macronutrient is proportional to the food energy that is consumed [34]. This diet-induced thermogenesis seems to be unaltered [36, 42, 46–49] or even reduced [44, 50, 51] during pregnancy.
The most varying factor that determines total energy expenditure is physical activity and is dependent on three factors: muscle mass, body weight and level of activity [34]. The interaction between physical activity and energy metabolism is complex. For example, pregnant women may reduce physical activity energy expenditure by selecting less demanding activities or reducing the pace of activity, although the actual cost might be higher, because of moving a heavier body [38]. However, all pregnant women might not reduce their physical activity because of the knowledge they have of the health benefits of regular physical activity during pregnancy. Over the past 2 years, more studies have focused on the energy expenditure during pregnancy, especially in the wake of the rapid increase in obesity, globally. The measurement of total energy expenditure during pregnancy is controversial, mainly because of conflicting data on the extent of reduction in physical activity as pregnancy advances [35] and the collection of physical activity information with self-report questionnaires.
The energy cost that is attributed to physical activity during pregnancy is generally lower [40, 52–55] and tends to decrease as pregnancy advances [56–60]. Studies show that pregnant Scottish [61] and Dutch [60] women had a slight decrease in absolute energy cost of physical activity , observed in activity diary studies, as their pregnancy advanced. The same results were found in British women by Prentice et al. [42] by means of whole body indirect calorimetry methodology. However, Melzer et al. [35] found this decrease in active energy expenditure insignificant in pregnant women in Sweden and America, but when expressed as per unit of body weight to account for weight differences, this result became significant. Other studies from Sweden and the UK report similar decreases in active energy expenditure per kilogram in the pregnant compared to the nonpregnant state [42, 54]. Preliminary findings of the Habitual Activity Patterns during PregnancY (HAPPY)-study in Potchefstroom, South Africa, indicate a 25 % reduction in activity energy expenditure from the first to the third trimester of pregnancy. The study included participants from white, black and coloured ethnic groups as well as low-, middle- and high socioeconomic groups [62]. The physical activity levels (PAL) reported can be classified as low activity to sedentary behaviour from the first to the third trimester of pregnancy.
Reasons for this decrease in physical activity are explained in the following section. However, physical activity cannot be observed in isolation when activity energy expenditure is discussed because the energy intake is also important in the energy balance . More details regarding behavioural changes in activity patterns are discussed in the following section.
To better understand the associations between energy intake, energy storage and energy expenditure during pregnancy, studies should be carried out during free-living conditions applying the most objective and reliable methodology [38]. The correct measuring tool is essential to quantify physical activity during pregnancy.
Measurement of Physical Activity During Pregnancy
Critical appraisal of the physical activity during pregnancy and the influence of recreational or habitual physical activity on birth outcomes and maternal health are dependent on valid and reliable objective measurements of physical activity [3]. The relationship between physical activity and birth outcomes is likely to be modest, therefore it is essential to measure recreational physical activity accurately to minimise the possibility that no effect is observed because of a measurement error [3]. The majority of information on physical activity in the pregnant and nonpregnant population is based on subjective physical activity questionnaire-collected data. The current guidelines for physical activity are therefore also based on the research based on the subjective data. Changes in technology have given rise to the development of more objective instruments to determine habitual physical activity, not only in the general population but also in pregnancy.
Subjective Physical Activity Measurements
A great variety of physical activity questionnaires have been developed and validated over the past 20 years. The accuracy of self-reporting questionnaires is influenced by the subjective nature of the term “intensity of physical activity” [63]. Physical activity questionnaires emphasise participation in moderate to vigorous sports while not including household or childcare activity [64]. Indeed, women spend considerable time and energy in moderate intensity activities related to household chores, their job and family care [65]. Interestingly, the accuracy of short- and long-term recollections of physical activity patterns by pregnant women is not known [66]. According to Poudevigne and O’Conner [66] there is a lack of knowledge regarding how accurately women can recall their physical activity patterns during pregnancy.
Direct measurements of the metabolic cost of energy expenditure among pregnant women, as opposed to relying upon values collected among nonpregnant populations, will objectively define the intensity of recreational activity among pregnant women [3]. For this purpose, double-labelled water and indirect calorimetry [67, 68] are used to measure physical activity, but because of the costs, invasiveness and technical sophistication of these methods, their suitability for the general population decreases.
In large samples and population-based studies, questionnaires have been the instrument of choice. Hermann et al. [69] determined the validity of two questionnaires, namely the International Physical Activity Questionnaire (IPAQ) [70, 71] and the Global Physical Activity Questionnaire version 2 (GPAQ) [72]. The GPAQ shows short- and long-term retest reliability and modest validity [69], although it has not been validated in the pregnant population. Specifically during pregnancy , four validated questionnaires are currently being used to determine physical activity [73–76]. A validated, self-administered questionnaire, the Pregnancy Physical Activity Questionnaire (PPAQ) has been used to assess the physical activity levels of pregnant women [74]. Categories in this questionnaire include: household/care-giving, occupational, sport/exercise, transportation and inactivity [77] and asks women to estimate the duration and frequency of time spent per activity during the current trimester of pregnancy. The reliability of the PPAQ for total physical activity was strong (r = 0.78), with the highest reliability for moderate intensity activity (r = 0.82). With regards to activity type, the highest reliability was found for occupational activity (r = 0.93), followed by household/care-giving (r = 0.86) and sports/exercise (r = 0.83). The validity of the PPAQ was determined against accelerometry (ActiGraph). The overall correlations between the PPAQ and average counts per minute were within the range of values observed for the published cut points (r = 0.27 for total activity), while validity coefficients for vigorous activity (r = 0.37) and sports/exercise (r = 0.48) were higher using average counts per minute. PPAQ provides an easy method of assessing physical activity patterns in women with uncomplicated pregnancies [77].
Objective Physical Activity Measurements
Both accelerometers [55, 78] and heart rate monitors [79] have been used to measure daily physical activity accurately. However, when these devices are used separately, they have disadvantages [80]. Heart rate is influenced by temperature, humidity, fatigue and emotional stress. [81]. Additional challenges are the loss of data from signal interruptions and delayed heart rate responses [82, 83]. Accelerometers on the other hand are not waterproof and cannot monitor activities in water [80]. Also, static physical activity, such as weight lifting, generates less body movement but requires energy expenditure, which can be problematic when accelerometers are used [84, 85].
To continually measure free-living physical activity, a combination of the abovementioned accelerometers and heart rate monitors are used and could provide more accurate activity profiles by overcoming individual sources of error [84, 86–89]. One such device that combines heart rate and accelerometry is the ActiHeart® (CamNTech, UK) [80], which was first used by Melzer et al. [35] to measure changes in resting and activity-related energy expenditure during pregnancy. The device is currently the only commercially available device that combines acceleration and heart rate, therefore increasing the practical applicability to improve energy estimates compared to traditional acceleration devices [90]. ActiHeart® is a 10 g, waterproof, self-contained logging device that allows activity to be measured synchronously with heart rate at between 15–60 s epochs [91]. The device is worn on the chest and consists of two electrodes that are connected by a short lead and clip onto two standard electrocardiograph (ECG) pads. Free-living data, as assessed by the ActiHeart® and calculated according to branched models, is essential to determine behavioural changes in activity patterns in pregnant women [35]. The ActiHeart® device has shown accurate estimates of energy expenditure versus indirect calorimetry over a wide range of activities (varying from sedentary behaviours to vigorous physical activity) in men and nonpregnant women, although it is not validated specifically for pregnant women [35]. Brage et al. [92] conclude that the ActiHeart® is a reliable and valid tool for the measurement of movement and heart rate in humans at rest and during walking and running. Overall, the ActiHeart® is reliable in measuring and categorising intensities of physical activity [80] in addition to increased monitor-wear compliance in adolescents [93] (Fig. 16.3).
Combined heart rate and accelerometer device (ActiHeart®, CamNtech, UK) placement for the measurement of habitual activity energy expenditure in pregnancy
The complexity of assessing physical activity in general, and in particular, during pregnancy, a demanding period characterised by changing physiology, hampers the determination of the optimal dose of recreational physical activity for pregnant women [3]. Because of the well-documented advantages of regular exercise in nonpregnant women, similar findings are expected during pregnancy. A lack of measuring instruments limits studies on the direct effect of physical activity levels on the growth of the foetus and maternal and foetal birth outcomes. The results are that health professionals have been very conservative in the volume (intensity x duration) and frequency of exercise and physical activity that are recommended to pregnant women. These guidelines have therefore impacted directly on habitual activity patterns during pregnancy.
Physical Activity Patterns During Pregnancy
The physical activity patterns of pregnant women are poorly described [66]. Maternal physical activity tends to decrease during pregnancy because of the minor discomforts that are associated with pregnancy, such as leg cramps, swelling, fatigue, shortness of breath [94], difficulties in movement related to a larger body mass [2] and, sometimes, because of the perception that physical activity may be damaging to the foetus [95, 96].
Physical activity patterns vary across the duration of pregnancy and are generally at a lower level when compared to pre-pregnancy [3, 97]. Prospective studies indicate that recreational, occupational and overall physical activity declines during pregnancy [52, 55]. Physical activity is usually constrained in the first trimester because of nausea, vomiting and profound fatigue [8, 66]. These symptoms usually decrease in the second trimester. Physical limitations—like uterine enlargement and changes in weight distribution [66]— also lead to a decrease in physical activity in the third trimester [8]. Reductions in physical activity, especially in the third trimester, might also be a method to meet the increased energy demands of pregnancy [98]. Physical activity often decreases the most during the third trimester of pregnancy. This decrease in physical activity has sometimes been referred to as the “nesting effect”, as pregnant women prepare their home for the arrival of a new baby [66].
Psychological changes, such as a declining body image and depression may make physical activity less attractive during pregnancy [99]. In contrast to this, some of the barriers to physical activity during pregnancy, such as depression and fatigue, can be attenuated by regular exercise [66]. Exercise intensity decreases as many women cease vigorous sport activities when pregnant [100–102]. Evidence indicates that the primary mode of physical activity by pregnant women is low intensity walking [103, 104]. There is a shift in the nature of the activities pregnant women usually perform, to activities that are less vigorous, more comfortable or perceived as safer, like walking and swimming and less bicycling [66, 105, 106]. Work-related physical activity also decreases as pregnancy proceeds [66].
A study done by Löf [38] found that pregnant women, compared with nonpregnant controls, spend less time (1.5 h/24 h) standing and performing moderate activities and more time (1.5 h/24 h) on sedentary activities such as sitting and reclining. Additionally, absolute active energy expenditure decreased by 18 % [38]. The PAL was also significantly lower than the corresponding value for nonpregnant controls per 24-h period [38]. However, as stated by Prentice et al. [42], the use of PAL on pregnant women is not advisable because even if active energy expenditure (total energy expenditure—basal metabolic rate) is unchanged, PAL will still decrease as basal metabolic rate increases during pregnancy. These findings correspond with an American study that confirmed a decrease in active energy expenditure by 13 % as recorded with activity records [40]. However, another study on healthy Swedish women indicated no major effect of pregnancy on activity patterns or on active energy expenditure [54] (Fig. 16.4).
Energy expenditure for nonpregnant versus pregnant women at different physical activity levels. PAL physical activity level, AEE activity energy expenditure, EE energy expenditure, TEE total energy expenditure, NP nonpregnant; REE resting energy expenditure, kcal kilocalories, kcal/d kilocalories per day, kg kilogram
While all of the abovementioned factors contribute to the decreased pattern of physical activity during pregnancy , the strongest predictor of physical activity during pregnancy is the level of physical activity during the year prior to pregnancy [107, 108]. If pregnant women were active as teenagers, they were 13 times more likely to engage in high intensity physical activity during pregnancy as compared to sedentary teens [107]. Highly active women may be more aware of the health benefits of exercise and may have more confidence in their ability to choose an appropriate mode and intensity of exercise [66]. As with women who were sedentary before pregnancy, some started becoming physically active when they were pregnant, according to a few studies [97, 100, 108, 109]. This indicates that these women consider their pregnancy to be a chance to change their lifestyle [100]. Few studies document longitudinal changes in physical activity during all three trimesters [102, 110, 111]. It is expected that the majority of pregnant women would have low levels of physical activity since PALs of the general nonpregnant population are globally reported to be low.
Very limited research exists pertaining to the physical activity patterns of South African women [112]. Results from a single South African study, determining physical activity subjectively during pregnancy [112], found no change in PALs between the second and third trimester. This contradicts previously mentioned studies that found a decline in physical activity as pregnancy progressed. This contradiction can be explained by the fact that the patients in the study were recruited from a gynaecologist who advocated exercise during pregnancy [112].
Hegaard et al. [100] found that women with a higher body mass index (BMI; more than 25 kg/m2) decreased their physical activity during pregnancy more than pregnant women with a normal weight (BMI 18.5–24.99 kg/m2). Changes in physical activity during pregnancy are extremely detrimental because this decrease results in an even higher risk of gestational diabetes, pre-eclampsia or preterm delivery than in women who continued their normal level of physical activity [113–115].
The most extreme type of physical inactivity is bed rest, which is recommended by obstetrics and gynaecology physicians in 20 % of all pregnancies [66]. Bed rest is recommended in the hope of preventing or treating a wide variety of conditions, including spontaneous abortion, preterm labour, foetal growth retardation, oedema and pre-eclampsia [116]. Little evidence exists regarding the effectiveness of bed rest on the treatment of these conditions [117]. The adverse effects of bed rest may be even more detrimental than the conditions it is meant to prevent or treat, like decreased sex steroids, insulin resistance, systemic inflammation, mood disturbances and even progressive bone and muscle loss compromising the ability to perform tasks of daily living [118]. Additionally, Poudevigne and O’Conner [66] state that a combination of biological, psychological, social and environmental factors interacts to contribute to changes in physical activity during pregnancy.
Physical activity in the postpartum period is usually decreased, because of the added fatigue of delivery and newborn care [8]. However, less is known about physical activity during the postpartum period and in the change in activity from pregnancy to postpartum [119]. Data from the HAPPY-study that objectively determined physical activity indicate the activity counts in a sample of 70 women decreased by 20 % from the third trimester to 3 months postpartum [62]. According to Pereira et al. [102], walking as a physical activity modality might remain unchanged from pre-pregnancy to postpartum. Usually care-giving physical activity in the postpartum period constitutes the largest proportion of total physical activity [119].
In summary, a reduction in physical activity during pregnancy augments the need to promote regular physical activity of pregnant women as a necessary part of their lifestyle due to the minimal risk and numerous short- and long-term benefits for both the mother and the baby. Education about the benefits of regular physical activity during pregnancy must be included in the planning and implementation of health promotion programmes by medical personnel and physical education staff [120].
Benefits of Regular Physical Activity During Pregnancy
Physical activity is a major determinant of lifelong health [121, 122] and has been associated with reduced morbidity and mortality [123–125] by serving as a primary preventive behaviour for several chronic health conditions including coronary heart disease [126–128], cancer [128], type 2 diabetes [129], [130], stroke [131], metabolic syndrome [132] and osteoporosis [133].
Maternal benefits of physical activity appear to be both physical and psychological in nature [10]. Physical benefits during pregnancy include shorter labour and a lower incidence of operative abdominal and vaginal deliveries and acute foetal distress [2, 128, 134–136]. Benefits for pregnant women also include improved cardiovascular function [2], reduced incidence of muscle cramps and lower limb oedema [137, 138], attenuation of gestational diabetes mellitus [139, 140] and gestational hypertension [24].
Physical activity does not only have physical benefits but also improves psychological health and provides wellbeing benefits [105, 141, 142]. An increased level of physical activity is known to have a protective effect against insomnia, stress, anxiety and depression [143–146], relieve job strain [147] and provide mood stability [66, 148] as well as increased perceived levels of energy during the day [149]. These benefits carry over to the postpartum period [149] and do not compromise infant breast milk acceptance of infant growth [150] .
Kalisiak and Spitznagle [151] reviewed clinically controlled trials that demonstrate that there is a moderate amount of evidence proving that exercise during pregnancy in healthy females has positive effects on both the mother and the foetus. While many studies conclude a positive relationship between physical activity and pregnancy outcome, the majority of the studies applied subjective questionnaires to determine the relationships. Therefore, accurate and objective methods to measure levels of physical activity are important when defining an appropriate relationship between physical activity and health outcomes for both the mother and foetus [90].
Recent meta-analyses of randomised control trails determining the effect of structured and supervised exercise during pregnancy report that pregnant women who exercised gained significantly less weight (− 1.13 kg) than women in the control group. The birth weight was however not significantly reduced in the exercise group compared to the control group [152].
Risks Associated with Physical Activity During Pregnancy
Physical activity was discouraged until the early twentieth century on the basis of theoretical concerns about exercise-induced injury and adverse foetal and maternal outcomes [31, 144]. These concerns were based on the potentially detrimental effects of exercising on the mother and the foetus, secondary to increases in maternal body temperature, circulating stress hormones, caloric expenditure, decreased blood flow and biomechanical stress [153, 154] as seen in Fig. 16.5 [155].
Possible risks associated with physical activity during pregnancy. (Courtesy of Andries Fourie van Oort, M.Sc.)
Biological mechanisms that might contribute to reduced birth weight and length of gestation were theorised by [156]. They suggest that these effects are mediated by the sympathetic nervous system and may also be associated with the release of prostaglandins into the maternal circulation. Physical strain may lead to the release of catecholamines, which may increase maternal blood pressure and uterine contractility and decrease placental function [157].
Another concern of physical training during pregnancy is the subsequent teratogenic effect of hyperthermia in the first trimester [7, 155, 158]. However, this has not been shown to occur in studies of exercising women [8], because an increase in minute ventilation and skin blood flow augment heat dissipation and somewhat inhibit the potential hyperthermic effects of exercise [159]. Even so, exercising while pregnant should preferably take place in a well-ventilated and temperature-controlled environment [7].
The theoretical risk of foetal hypoxia is another concern for the exercising pregnant woman. It was once believed that the demands of exercising muscles divert blood flow from the uteroplacental unit [10]. However, compensatory changes with exercise, such as raised maternal haematocrit and oxygen extraction, appear to prevent the impairment of foetal oxygenation [135, 160]. Takito et al. [161] found that maintaining specific standing postures for a prolonged period could potentially reduce uteroplacental blood flow and lead to decreased foetal growth . Decreased visceral blood flow is suggested to cause potential adverse outcomes, such as congenital malformation, growth retardation, premature labour, brain damage, difficult labour, haemorrhage and maternal musculoskeletal injury [153].
Takito et al. [161] identified high total energy expenditure to potentially be associated with low birth weight, preterm birth and intrauterine growth restriction under the supposition that higher caloric expenditures could withhold energy from the foetus. The risk of maternal musculoskeletal injury due to changes in posture and centre of gravity or fetoplacental injury caused by blunt trauma or stress effects from sudden motions is also a concern [162].
Recommendations of physical activity during pregnancy before the twentieth century were overly conservative [162–171]. Recently, the guidelines have evolved as more reliable research has emerged [14]. The American College of Obstetricians and Gynaecologists (ACOG) found no scientific support that normal pregnant women should limit their exposure to physical activity based on the risks to the foetus and/or mother. However, some studies found that higher daily physical activity is inversely associated with foetal growth [172] and birth weight [173].
Campbell and Mottola [174] found that excessive physical exercise, at a frequency greater than 5 days a week, resulted in a low birth weight. However, their results also showed an equally harmful effect on foetal growth in the group of women who exercised less than two times per week. Magann et al. [175] supported the abovementioned results and found that less energy expenditure, at work and during leisure time, was associated with an increased risk of preterm birth and low birth weight (< 10th and < 3rd percentile).
The risk–benefit balance of physical activity during pregnancy needs to be assessed. During pregnancy, the risk of a sedentary lifestyle may be more detrimental than an active one [7], since a sedentary lifestyle includes loss of muscular and cardiovascular fitness, excessive weight gain, raised risk of gestational diabetes or pre-eclampsia, development of varicose veins and an increased risk of physical complaints such as dyspnoea, lower back pain and poor psychological adjustment [115, 139, 176]. According to Takito et al. [161], both excessive and insufficient physical activity impact negatively on pregnancy outcomes. Physical activity, done at an appropriate level for the physical condition of the woman, is beneficial to foetal growth , with the extremes being inactivity/sedentarism and a prolonged duration of vigorous intensities, which are potentially harmful to the supply of oxygen for adequate foetal growth [160]. However, women with complicated pregnancies have been discouraged from participating in exercise activities for fear of impacting the underlying disorder or maternal or foetal outcomes [8]. Some publications indicate that high levels of strenuous, high-intensity activity may result in preterm labour in susceptible individuals as well as babies with a low birth weight [177–179].
Absolute contraindications to exercise in pregnancy include haemodynamically significant heart disease, restrictive lung disease, incompetent lung disease, multiple gestation at risk for premature labour (≥ triplets), persistent second- or third-trimester bleeding, placenta praevia after 26 weeks’ gestation, ruptured membranes, preterm labour, pre-eclampsia, uncontrolled type-1 diabetes and thyroid disease or other serious systemic disorders like chronic bronchitis and uncontrolled seizures [8]. Relative contraindications to exercise include anaemia (defined by the World Health Organization as < 19 g/dL in pregnant women), unevaluated maternal cardiac arrhythmia, extreme morbid obesity and extreme underweight (BMI 8] (Table 16.1).
However, pregnant women should be advised that adverse pregnancy or neonatal outcomes are not increased for exercising pregnant women [7, 180–186], and maternal and infant health can even be enhanced [144, 180, 187–191]. Table 16.2 provides evidence regarding the effects of physical activity on foetal growth and birth outcomes.
Guidelines for Physical Activity During Pregnancy
The ACOG [5] recommends that healthy pregnant women exercise at moderate intensity for at least 30 min, most days of the week [24] while the American College of Sports Medicine [7] encourages an accumulation of 30 min or more of moderate physical activity per day on most, if not all, days of the week. Yet, another recommendation set forth by the US Department of Health and Human Service states in the document “2008 Physical Activity Guidelines for Americans” that pregnant women should engage in a minimum of 150 min of moderate-intensity aerobic activity a week, even if they were not physically active prior to pregnancy [12]. Recommendations in Australia [11], Canada [8], the UK [10] and Norway [9] are similar to the abovementioned American [120]. A recent South African Position Statement [7] supports the guidelines set out by the ACOG [5], the Society of Obstetricians and Gynaecologists of Canada (SOGC) and the Canadian Society of Exercise Physiology [8], but focuses on exercise and does not give guidelines regarding general physical activity during pregnancy (Table 16.3) .
The question remains whether pregnant women adhere to these guidelines. Due to the uncertainty regarding the benefits and risks of exercise during pregnancy [199], the adherence of pregnant women to exercise is not reflective of the recommended ACOG guidelines [55, 104, 200]. Additionally, pregnant women often receive mixed messages from friends, family and even their doctors about exercise during pregnancy [199]. While scientific data support the safety of exercise during pregnancy, this knowledge is not always communicated to pregnant women. According to Price et al. [199], exercise must be prescribed to pregnant women in a similar way as the prescription of medicine. In addition, more reliable quantitative-determined data are warranted to provide an evidence-based exercise regimen for pregnant women .
The recommendations for physical activity for pregnant women, as presented in Table 16.3, are similar to the guidelines for nonpregnant women. The only exception is the intensity of the activity. In the guidelines, “moderate activity” is given as the intensity, but the definition for moderate-intensity activity is not defined. When the presented guidelines are compared to the guidelines for maintaining weight after weight loss, which is 60–90 min of activity, it is understandable that women do not comply with the guidelines due to the inherent discrepancies. Finally, the guideline for heart rate should be clarified in consideration with the fitness level of the pregnant women and previous exercise experience and level of fitness prior to pregnancy.
Birth Outcomes
Foetal Growth Parameters and Confounders Thereof
Monitoring the growth of the foetus is a major purpose of antenatal care [201]. The overall term “foetal growth parameters” includes: head and abdominal circumference, femur length, ponderal index (weight in grams x100 divided by length in cubic centimetres), placental weight and expected birth weight [202]. While birth weight is a crude measurement of foetal growth, the measurement of head size and length at birth gives an insight into the timing of growth retardation during intrauterine life [203].
Birth Weight
Although birth weight is not the most objective measurement of foetal growth , it is important with regards to public health [3]. Birth weight is an amalgam of multiple determinants and is a proxy for the many different processes that occur in the months preceding delivery [204]. Birth weight is associated with a broad range of short- and long-term maternal complications (e.g. pre-eclampsia, premature labour), foetal complications (e.g. stillbirth, malformations), neonatal complications (e.g. respiratory distress, infant mortality) and long-term complications (e.g. behavioural disorders, cerebral palsy) [205, 206].
Foetuses delivered with a lower birth weight than expected might become healthy, thriving infants, while others are small because their growth in utero was impaired and have an increased risk for perinatal morbidity and mortality [207, 208]. The cut-off for small-for-gestational-age is a birth weight below the tenth percentile [209]. Low birth weight and foetal growth impairment may be multifactorial in origin, therefore it is vital to have knowledge of possible associations between specific risk factors, pre- and postnatal growth patterns and specific adult health parameters like smoking and physical activity habits [210].
Over the last decade, a new paradigm evolved from the notion that environmental factors in early life and in utero can have profound influences on lifelong health [204]. Reduced foetal growth might also be the origin of cardiovascular disease later in life through programming in foetal life and infancy [203].
Theory of Foetal Origins
Time in the womb can be seen as a critical window during which maturation must be achieved, because failure of maturation is to some extent irrecoverable [203]. The maternal environment influences these critical stages of early life and leads to long-term changes in the body’s structure, physiology or metabolism—this is called programming [211, 212]. Relationships between foetal experiences and later risk for adult chronic disease, including cardiovascular disease and its risk factors, cancer, osteoporosis , diabetes, neuropsychiatric outcomes and respiratory diseases, have been demonstrated by a large number of studies [213–216]. The abovementioned relationship, the foetal origins hypothesis, was first proposed by the British epidemiologist David Barker as the “thrifty gene hypothesis” [217]. The foetal origin hypothesis was developed by linking records of births in the early twentieth century with health in later life from the Hertfordshire records [203, 217–225].
The theory of foetal origins suggests that associations with body size at birth underestimate the influence of intrauterine development on later disease. Prevention of coronary heart disease and non-insulin-dependent diabetes may be related to the choices of the mother. Therefore, chronic disorders that manifest later in life may be related to poverty (malnourished mothers give birth to malnourished infants with low birth weight) and prosperity (exposure of an infant with low body weight phenotype to a high caloric diet) [226] In this way, both a low and high birth weight is associated with negative outcomes in later life, showing a U-shaped relationship as observed by Rich-Edwards et al. [227]. Newborns that are small-for-gestational-age tend to preserve body fat at the expense of lean body mass [228], whereas large newborns may also have relatively increased body fat. Hammani et al. [229] suggest that associations between foetal growth and later adiposity are complex. The findings that a low and high birth weight is a strong predictor of diabetes and cardiovascular disease in later life has led to continuing debate about the significance of nature and nurture [230].
Environmental Pollution
Environmental air pollution has been shown to have associations with a low birth weight and its determinants, preterm delivery and intrauterine growth restriction [231–238]. Exposure to an air pollutant like carbon monoxide could lead to decreased oxygen delivery to tissues, including the foetus [239]. Inhaling air pollution particles may lead to increased blood viscosity, which may have an adverse effect on placental function, thereby restricting foetal growth [233] . However, the effect of air pollution on foetal growth is smaller than the effect of high-risk behaviours [239].
Lifestyle
Tobacco smoking, alcohol consumption and illicit drug abuse are increasing among women of childbearing age [240]. Intrauterine growth restriction and low birth weight are the most consistent effect of these high-risk behaviours [240]. Maternal smoking during pregnancy is an extremely important, modifiable risk factor that is associated with adverse perinatal outcomes [241–243], such as intrauterine growth retardation [243, 244], low birth weight [245–248], preterm and very preterm delivery [249], ectopic pregnancy [250], placental pathologies [251] and a significant higher risk of perinatal and infant mortality [252–255]. Specifically, smoking has negative effects on multiple foetal growth parameters including body weight, femur length, limb length, total length, head circumference, chest circumference and abdominal circumference [256–259]. According to Hernandéz-Martínez et al. [261], maternal smoking during pregnancy is also related to cognitive, emotional, temperamental and behavioural problems throughout the child’s life.
The effects of smoking could be mediated by the direct toxic effect on the foetus, leading to metabolic alterations, as well as by mechanisms resulting in decreased oxygen delivery [255]. Cigarette smoke contains more than 2500 chemicals and some of these are harmful to the developing foetus and cause adverse pregnancy outcomes [261, 262]. Carbon monoxide readily crosses the placental barrier by passive diffusion, causing a fourfold increase in the level of carboxyhaemoglobin in umbilical cord blood, which inhibits the release of oxygen into foetal tissues [263–266]. This chronic hypoxia alters the physiological development of organs and tissues [261, 267]. Therefore, cigarette smoking during pregnancy is a strong dose-dependent risk factor for small-for-gestational-age [268, 269]. Second-hand smoke showed a similar relationship, according to Horta et al. [248].
Cigarette smoking may confound the relationship between birth weight and later body size [204]. Multiple studies have demonstrated a clear inverse relationship between maternal smoking and childhood weight [270, 271], although [272] suggest an increased risk of obesity later in life among offspring of mothers who smoked during pregnancy. [255] analysed body composition and found that lean body mass was more affected than body fat, and proportional body distribution of subcutaneous fat was not affected in infants from mothers who smoked during pregnancy.
Alcohol consumption during pregnancy has been associated with various pregnancy complications such as miscarriage [273], stillbirth [274] and other multiple birth defects [275–279] such as foetal alcohol syndrome [280, 281] and an increased risk of low birth weight [282, 283].
Drug abuse during pregnancy may lead to complications for the foetus, the newborn and later during childhood [240]. Cannabis, cocaine and heroin specifically have been studied in relation to their effects on foetal growth [240, 284], and findings have proposed that cannabis abuse during pregnancy decreases foetal growth , but this has not been confirmed in follow-up studies [285–287]. Poor pregnancy outcomes, including premature birth and abnormalities of behavioural testing in the offspring, have been associated with cocaine use during pregnancy [240]. Associations with heroin use during pregnancy and an increased incidence of pregnancy complications, including premature delivery , premature rupture of the membranes, intrauterine foetal growth retardation and perinatal mortality have also been confirmed [240].
Another confounder between birth weight and later adiposity may be social and economic factors [204]. Vagero et al. [289] found that babies born to women with a lower social status had lower birth weights. As such, neighbourhood factors that have been associated with an increased risk for a low birth weight include a negative perception of the neighbourhood [290], an average income [291, 292], economic hardship, low housing costs [293] and, interestingly, neighbourhood crime rates [294]. How these factors relate to birth weight remains speculation, but there have been explanations that focus on the stress-related hormonal factors and birth outcomes through biological mechanisms [295–299], whereas others researched the association with maternal health behaviours, such as smoking [300–302]. Although environmental factors play an important role in determining foetal growth , genetics must also be considered.
Genetics
Both genetic and environmental factors are important determinants of foetal growth [230, 303, 304]. As stated by Tower and Baker [305], the growth potential of any foetus is likely to be genetically determined. As an example, Knight et al. [304] found that paternal height is an important, independent determinant of foetal linear growth. Knight et al. [304] concludes that skeletal size is regulated by genetic information, while the adiposity of the newborn is reflected by the maternal intrauterine environment. Another example is that offspring birth weight has a strong association with parental adiposity [306, 307]. Therefore, the associations of maternal and paternal birth weight with offspring birth weight suggest genetic or intergenerational environmental influences [204, 308, 309].
Foetal growth restriction is a complex trait for which no single susceptibility gene can be identified [305]. There are between 100 and 200 imprinted genes and there is increasing evidence that many are involved in pre- and postnatal growth [310]. When the normal imprint is disrupted, malformations in the development of the foetus occur [310]. Vaessen et al. [230] postulate that the Insulin-like Growth Factor-1 (IGF-1) gene imprint disruption may lead to low circulating IGF-1 concentrations, reduced height in adulthood, diminished insulin secreting capacity and a high risk of type-2 diabetes and myocardial infarction. Although genetically established expression of IGF-1 and insulin are important determinants of growth during the foetal period, they do not play a major role in the regulation of body weight in postnatal life [230]. Additionally, the postnatal environment that includes adverse eating and activity habits shared by family members may also lead to a higher birth weight and higher adiposity later in life. Other genetic and environmental factors such as diet and physical activity have more relevant effects on the regulation of weight [230]. A summary of the interactions can be seen in Fig. 16.6 that has been composed from the existing literature.
Multifactorial influences on foetal growth. + positive influence/effect, − negative influence/effect
Labour
Natural birth seems to be the best conclusion of the pregnancy for both the mother and the baby [311] and should therefore be seen as a major goal for all pregnant women [120]. Other methods of childbirth, including a caesarean section, should only be used when justified by the circumstances [120]. From a public health perspective, there is concern regarding the increased rate of caesarean sections during the last decade because this procedure is not risk-free [312]. One possible explanation for this recent rise in caesarean sections includes a rise in maternal obesity [313]. However, this rise cannot be attributed entirely to a worsening of maternal or foetal risk factors [314–316]. Therefore, caesarean sections may be not justified medically, exposing women and babies to surgical risks without proved benefit [317, 318]. Reducing rates of caesarean sections should be a public health priority [312].
In recent years, prenatal physical activity has increasingly been recommended to promote natural birth [99, 120, 134, 165, 319]. Regular physical activity during pregnancy may have other beneficial effects on multiple aspects of the course and outcome of labour and delivery [120] including a shorter delivery [134, 320–323], less frequent need for anaesthesia [134, 324], a lower rate of induction of labour [134, 320], amniotomy [134], episiotomy and perineum lacerations [134, 321, 325] and improved neonatal outcome directly after birth [134]. Based on these findings, it is clear that physical activity during pregnancy has physiological benefits on labour. However, as stated by Guskowska [326], pregnant women often experience fear about labour and delivery , which is undoubtedly detrimental. Physical activity might produce anti-anxiety effects that will help to reduce labour anxiety [326].
To conclude, Ghodsi et al. [322] state that physical activity can result in shorter labour, fewer medical interventions, less exhaustion during labour and might also reduce the fear associated with giving birth. Encouraging pregnant women to be physically active could represent a low-cost, low-risk approach to reduce the number of caesarean deliveries [312].
Body Composition at Birth Related to Disease in Later Life
Early environmental influences, as early as in the womb, have long-term effects on body composition and musculoskeletal development as evidenced by the prevalence of obesity, sarcopenia and osteoporosis in later life [327]. This phenomenon is explained by means of foetal programming as previously mentioned, and more specifically, to the body composition of the baby, referred to as developmental plasticity [327]. Developmental plasticity is defined as the ability of a single genotype to produce more than one alternative form of structure, physiological state or behaviour in response to early environmental conditions [327].
During embryonic life, bone and muscle develop from the mesoderm layer, differentiate during the first trimester into dermatomes containing bone and muscle cell precursors [327]. Muscle development starts between 6 and 8 weeks of gestation and progresses until about 18 weeks [328]. Adipose cell formation is determined much later, the critical period varying from 30 weeks of gestation to the first year of postnatal life [329]. These major phases of the developing of muscle and fat are important, because of the high vulnerability of foetal programming occurring during this period of rapid cell division, the so-called critical periods [330].
A low birth weight has implications on fat, muscle and bone distribution in later life [327]. An association between low birth weight and increased adult central distribution of fat exists and has been evident in a couple of studies [327, 331, 332]. Reduced muscle mass and strength have also been implicated due to small size at birth [327]. These abovementioned effects are mediated by mechanisms that include a direct effect on cell number, altered stem cell function and resetting of regulatory hormonal axis [327].
Overall, evidence indicates that a higher birth weight is associated with increased risk of adiposity in childhood and adulthood, as reflected by BMI [204]. According to findings from Silverman et al. [333], increased adiposity was apparent at birth and progressively after the age of 4 years, but not from ages 1 to 3 years. Numerous studies have found direct associations between a higher birth weight and a higher adult BMI [227, 271, 334–339]. Specifically, the magnitude ranges from 0.5 to 0.7 kg/m2 for each 1-kg increment in birth weight [339, 340].
Maternal Weight Gain During Pregnancy
Women often express concern about weight gain during pregnancy ; however, it is important to remember that during pregnancy, all women gain weight due to foetal and maternal health . This weight gain also corresponds directly with foetal birth weight, which is a strong precursor of the health and development of the infant [34]. However, desirable weight gain also depends on BMI before pregnancy. Siega-Riz et al. [341] recommend GWG ranges for women on the basis of BMI as outlined in Table 16.4. The recommended ranges are derived from the observed weight gains of women delivering full-term, healthy infants without complications [40]. The total amount of weight gained in normal-term pregnancies varies considerably between women [41]. Studies show that about one third of mothers in the USA gain more or less the recommended weight; however, there is a lack in current research regarding the effects of physical activity on weight gain during pregnancy in the South African context [112]. One cross-sectional South African study found physically active pregnant women tend to gain less weight than relatively inactive pregnant women [112]. The findings are also supported by a recent meta-analysis from Domenjoz et al. [152] who reported a 1.3 kg less weight gain in women participating in physical activity compared to a non-active control group .
Weight gain during pregnancy is an important factor to consider to determine long-term obesity [342] and predict other health risks such as pre-eclampsia and adverse birth outcomes [343]. Women are usually very self-conscious or concerned about weight gain during pregnancy [344]. Brunette et al. [112] conclude that leading a moderately active lifestyle during pregnancy can have definite weight-control benefits, therefore women should be advised to be physically active during their pregnancies to reap the benefits and possibly to prevent the development of postnatal obesity. On the other hand, adopting a sedentary lifestyle, a common trend among pregnant women, results in women gaining weight above the recommended weight gain ranges [345].
Physical Activity in Infertility-Related Conditions
Polycystic Ovarian Syndrome
The most common endocrinopathy affecting women of reproductive age are polycystic ovarian syndrome (PCOS) . The condition affects between 4–12 % [346, 347] of women in America. Various diagnostic criteria are used, with the most common being an increase in insulin resistance compared to non-PCOS women independent of obesity [348]. Women suffering from PCOS experience reduced fertility, morphological changes of the ovaries and increased abdominal visceral fat [349]. Although the link between insulin resistance and infertility have not been completely resolved, various studies have indicated in the general population that regular physical activity increases insulin sensitivity, reducing insulin resistance. Researchers were therefore prompted to investigate the effect of physical activity on insulin resistance of women suffering from PCOS. A systematic review including premenopausal women diagnosed with PCOS who were exposed to between 12–24 weeks of exercise reported an improvement of between 23–30 % in fasting insulin [350]. When the effect of diet alone and diet combined with exercise was analysed, an overall improvement in ovulation and/or menstrual cycle was reported in 49 % of the participants. No difference between diet only and diet plus exercise intervention groups were found. The findings from the review suggest that regular physical activity may improve ovulation rates independent of dietary restrictions and changes in body fat. The physical activity interventions seem to enhance the insulin sensitivity which restores the reproductive function.
Amenorrhea
Amenorrhea is considered the most severe form of menstrual abnormality that causes infertility and is reported to be present in 1–44 % of female athletes [351] . The prevalence tends to be higher in athletes of sports where a very low BMI is required or in sports with a large strength component [352]. The mechanism through which exercise disturbs the menstrual cycle is described as a disruption of the hypothalamic–pituitary–ovarian axis. The consequence is that the hypothalamic pulsatile release of gonadotropin-releasing hormone (GnRH) is supressed, which consequently reduces the release of gonadotropins follicle-stimulating hormones (FSH) and luteinizing hormone (LH). An anovulatory and hypoestrogenic state results as a lack of ovarian stimulation [353].
Results from a population-based study in Norway during the mid-1980s with a follow-up one decade later focussing on infertility indicated that an increase in frequency, duration or intensity of physical activity was related to an increase in difficulty conceiving. A 3.2-fold greater chance of being infertile was reported for women exercising most days of the week. Independent of age, smoking and BMI, the risk of infertility increased 2.3 times when exercising to exhaustion [354].
Although regular physical activity and exercise is highly beneficial for most women, adverse effects related to fertility can and do occur. Current evidence indicates that the mechanism appears to be via an energy deficit that is created through a high intensity training program with a concomitant deficit in energy intake [355]. The energy deficit results in a catabolic state, shutting down the reproductive system in order to maintain health .
Summary
Early environmental influences, as early as in the womb, have long-term effects on an individual’s health. The maternal environment influences critical stages of early life and leads to long-term changes in the body’s structure, physiology and metabolism . A healthy lifestyle during pregnancy, which includes regular physical activity, no smoking and alcohol consumption, is essential. The physical and psychological benefits of regular physical activity during pregnancy are plentiful. Regular physical activity not only provides maternal benefits (decreased GWG, reduced risk of gestational diabetes and pre-eclampsia) but also foetal benefits (decreased risk for small- or large-for-gestational-age) and improved birth outcomes (lower incidence of operative abdominal and vaginal deliveries and a shorter labour period).
Physical activity tends to decrease as pregnancy progresses despite these known benefits. Although scientific data supports the safety of physical activity during pregnancy, this knowledge is not always communicated to pregnant women. The lack of objective and quantitative research regarding physical activity and pregnancy might have led to these uncertainties. Determining physical activity during pregnancy remains problematic due to methodological difficulties. However, the combined heart rate and accelerometer available on the market is a valid and reliable tool for the measurement of physical activity. Free-living data can be assessed and is essential to determine behavioural changes in activity patterns during pregnancy. Accurately determining physical activity will minimise possible inaccuracies of subjectively determined habitual activity patterns by means of questionnaires and could provide better insights into the effect of these patterns on foetal growth.
Determining the influence of habitual physical activity on foetal growth is difficult. Multiple determinants influence foetal growth and these factors have thoroughly been researched. One exception is the influence of habitual physical activity on foetal growth, possibly because of a relatively small relationship. Regular physical activities tend to decrease the risk of small- and large-for-gestational-age. Regular physical activity, in addition, also appears to have advantages for women suffering from infertility due to PCOS , since the restoration of insulin sensitivity improves ovulation rates.
Various institutional and governmental entities have set guidelines specifically for physical activity during pregnancy, but few women follow these guidelines because of uncertainty of the benefits and risks associated with physical activity during pregnancy. These guidelines are not based on longitudinal studies on pregnant women and might be unnecessarily conservative. Future research needs to be aimed at objectively determining the habitual physical activity patterns during pregnancy, as well as guiding governmental organisations to set specific physical activity guidelines and educating women about these guidelines. In addition, the safety of regular physical activity during pregnancy must also be addressed with doctors and health workers.
References
Downs DS, Chasan-Taber L, Evenson K, Jenn L, Leo S. Physical activity and pregnancy: past and present evidence and future recommendations. Res Quart Exerc Sport. 2012;83(4):485–502.
Melzer K, Schutz Y, Boulvain M, Kayser B. Physical activity and pregnancy: cardiovascular adaptations, recommendations and pregnancy outcomes. Sport Med. 2010;40(6):493–507.
Chasan-Taber L, Evenson KR, Sternfeld B, Kengeri S. Assessment of recreational physical activity during pregnancy in epidemiologic studies of birthweight and length of gestation: methodologic aspects. Women Health. 2007;45(4):85–107.
Evenson KR, Wen F. Prevalence and correlates of objectively measured physical activity and sedentary behaviour among US pregnant women. Prev Med. 2011;53(1):39–43.
ACOG (American College of Obstetricians and Gynecologists). Exercise during pregnancy. and the postpartum period. ACOG Committee Opinion. Int J Gynaecol Obstet. 2002;77(1):79–81.
ACSM (American College of Sports Medicine), editor. ACSM’s guidelines for exercise testing and prescription. 9th ed. Philadelphia: Lippincott Williams and Wilkins; 2014.
Barsky E, Smith T, Patricios J, Collins R, Branfield A, Ramagole M. South African Sports Medicine Association position statement on exercise in pregnancy. S Afr J Sport Med. 2012;24(2):69–71.
Davies GA, Wolfe LA, Mottola MF, Mackinnon C. Joint SOGC/CSEP clinical practice guideline: exercise in pregnancy and the postpartum period. J Obstet Gynaecol Can. 2003;28(3):329–41.
Holan S, Mathiesen M, Petersen KA. National Clinical Guideline for Antenatal Care. [Internet]. Oslo, Norway: Directorate for Health and Social Affairs; 2005. http://helsedirektoratet.no/publikasjoner/retningslinjer-for-svangerskapsomsorgen-kortversjon/Publikasjoner/a-national-clinical-guideline-for-antenatal-care%E2%80%93short-version.pdf. Accessed 8 July 2013.
Royal College of Obstetricians and Gynaecologists [Internet]. RCOG; [updated 2006 Jan 1; cited 2012 Jul 2]. Exercise in Pregnancy (Statement 4); [about 8 screens]. http://www.rcog.org.uk/womens-health/clinical-guidance/exercise-pregnancy.
Sports Medicine Australia. Exercise in pregnancy [Internet]. Victoria: Sport and Recreation; 2009. http://sma.org.au/wp-content/uploads/2009/10/WIS-ExPreg.pdf. Accessed 8 July 2013.
US Department of Health and Human Services. Physical activity guidelines for americans [Internet]. Office of Disease Prevention and Health Promotion; 2008. http://www.health.gov/paguidelines/pdf/paguide.pdf. Accessed 8 July 2013.
Blackburn ST. Maternal, fetal, and neonatal physiology: a clinical perspective. 2nd ed. St. Louis: Mosby; 2003.
Kawaguchi JK, Pickering RK. The pregnant athlete, part 1: anatomy and physiology of pregnancy. Athlet Ther Today. 2010;15(2):39–43.
Heidemann BH, McClure JH. Changes in maternal physiology during pregnancy. Brit J Anaesth. 2003;3(3):65–8.
Norwitz ER, Edusa V, Park JS. Maternal physiology and complications of multiple pregnancy. Semin Perinatol. 2005;29(5):338–48.
Carlin A, Alfirevic Z. Physiological changes of pregnancy and monitoring. Best Prac Res Clin Obstet. 2008;22(5):801–23.
Capeless EL, Clapp JF. Cardiovascular changes in early phase of pregnancy. Am J Obstet Gynecol. 1989;161(6):1449–53.
Holschen JC. The female athlete. Southern Med J. 2004;97(9):852–8.
Jensen D, Webb KA, O’Donnell DE. Chemical and mechanical adaptations of the respiratory system at rest and during exercise in human pregnancy. Appl Physiol Nutr Metab. 2007;32(6):1239–50.
Garcia-Rio F, Pino JM, Gomez L, Alvarez-Sala R, Villasante C, Villamor J. Regulation of breathing and perception of dyspnoea in healthy pregnant women. Chest. 1996;110(2):446–53.
Jensen D, Wolfde LA, Slatkovska L, Webb KA, Davies GAL, O’Donnell DE. Effects of human pregnancy on ventilator chemoreflex response to carbon dioxide. Am J Physiol Regul Integr Comp Physiol. 2005;288(5):1369–75.
Calguneri M, Bird HA, Wright V. Changes in joint laxity occurring during pregnancy. Ann Rheum Dis. 1982;41(2):126–8.
Artal R, O’Toole M. Guidelines of the American College of Obstetricians and Gynaecologists for exercise during pregnancy and the postpartum period. Brit J Sport Med. 2003;37(1):6–12.
Whitcome KK, Shapiro LJ, Lieberman DE. Fetal load and the evolution of lumbar lordosis in bipedal hominins. Nature. 2007;450(7172):1075–8.
Wang TW, Apgar BS. Exercise during pregnancy. Am Fam Physician. 1998;57(8):1847–52.
Branco M, Santos-Rocha R, Aguiar L, Vieira F, Veloso A. Kinematic analysis of gait in the second and third trimesters of pregnancy. J Preg. 2013;718095. doi:101155/2013/718095.
Kuijper EAM, Ket JCF, Caanen MR, Lambalk CB. Reproductive hormone concentrations in pregnancy and neonates: a systematic review. Reprod Biomed Online. 2013;27(1):33–63.
Lewis B, Avery M, Jennings E, Sherwood N, Martinson B, Crain AL. The effects of exercise during pregnancy on maternal outcomes: practical implications for practice. Am J Lifestyle Med. 2008;2(5):441–55.
Wylie L. Essential anatomy and physiology in maternity care. 2nd ed. United Kingdom: Churchill Livingstone; 2005.
Mittlemark RA, Wiswell RA, Drinkwater BL. Exercise in pregnancy. 2nd ed. Baltimore: Lippincott Williams & Wilkins; 1991.
Glinoer D. The regulation of thyroid function during normal pregnancy: importance of the iodine nutrition status. Best Prac Res Clin Endocrinol Metab. 2004;18(2):133–52.
Chamberlain G, Popkin FB. Clinical physiology in obstetrics. 3rd ed. Nottingham: Blackwell Scientific Publisher; 1998.
Whitney E, Rolfes SR. Understanding nutrition. 11th ed. Belmont: Thomson Wadsworth; 2008.
Melzer K, Schutz Y, Boulvain M, Kayser B. Pregnancy-related changes in activity energy expenditure and resting metabolic rate in Switzerland. Eur J Clin Nutr. 2009;63(10):1183–91.
Poppitt SD, Prentic AM, Jequier E, Schults Y, Whitehead RG. Evidence of energy sparing in Gambian women during pregnancy: a longitudinal study using whole-body calorimetry. Am J Clin Nutr. 1993;57(3):353–64.
McArdle WD, Katch FI, Katch VL. Exercise physiology: nutrition, energy, and human performance. 7th ed. Baltimore: Lippincott Williams & Wilkins; 2010.
Löf M. Physical activity pattern and activity energy expenditure in healthy pregnant and non-pregnant Swedish women. Eur J Clin Nutr. 2011;65(12):1295–301.
Mojtahedi M, De Groot LCP, Boekholt HA, Van Raaij JMA. Nitrogen balance of healthy Dutch women before and during pregnancy. Am J Clin Nutr. 2002;75(6):1078–83.
Butte NF, Wong WW, Treuth MS, Ellis KJ, Smith EO. Energy requirements during pregnancy based on total energy expenditure and energy deposition. Am J Clin Nutr. 2004;79(6):1078–87.
Löf M, Olausson H, Bostrom K, Janerot-Sjöberg B, Sohlstrom A, Forsum E. Changes in basal metabolic rate during pregnancy in relation to changes in body weight and composition, cardiac output, insulin-like growth factor I, and thyroid hormones in relation to fetal growth. Am J Clin Nutr. 2005;81(3):678–85.
Prentice AM, Spaaij CJ, Goldberg GR, Poppitt SD, Van Raaij JM, Totton M, Swann D, Black AE. Energy requirements of pregnant and lactating women. Eur J Clin Nutr. 1996;50(1):82–111.
Okereke NC, Huston-Presley L, Saeid BA, Kalhan S, Patrick MC. Longitudinal changes in energy expenditure and body composition in obese women with normal and impaired glucose tolerance. Am J Physiol Endocrinol Metab. 2004;287(3):E472–9.
Kopp-Hoolihan LE, Van Loan MD, Wong WW, King JC. Longitudinal assessment of energy balance in well-nourished, pregnant women. Am J Clin Nutr. 1999;69(4):697–704.
IOM (Institute of Medicine) and NRC (National Res earch Council) editor. Weight gain during pregnancy: reexamining the guidelines. Rasmussen KM, Yaktine AL. editors. Washington, DC: The National Academic Press; 2009.
Bronstein MN, Mak RP, King JC. The thermic effect of food in normal-weight and overweight pregnant women. Brit J Nutr. 1995;74(2):261–75.
Nagy LE, King JC. Postprandial energy expenditure and respiratory quotient during early and late pregnancy. Am J Clin Nutr. 1984;40(6):1258–63.
Piers LS, Diggavi SN, Thangam S, Van Raaij JM, Shetty PS, Hautvast JG. Changes in energy expenditure, anthropometry, and energy intake during the course of pregnancy and lactation in well-nourished Indian women. Am J Clin Nutr. 1995;61(3):501–13.
Spaaij CJ, Van Raaij JN, Van der Heijden LJ, Schouten FJ, Drijvers JJ, De Groot LC, et al. No substantial reduction of the thermic effect of a metal during pregnancy in well-nourished Dutch women. Brit J Nutr. 1994;71(1):335–44.
Contaldo F, Scalfi L, Coltorti A, Palo MR D, Martinelli P, Guerritore T. Reduced regulatory thermogenesis in pregnant and ovariectomized women. Int J Vitam Nutr Res. 1987;57(3):299–304.
Illingworth PJ, Jung RT, Howie PW, Isles TE. Reduction in postprandial energy expenditure during pregnancy. BMJ (Res C editor). 1987;294(6587):1573–7.
Clarke PE, Rousham EK, Gross H, Halligan AW, Bosio P. Activity patterns and time allocation during pregnancy: a longitudinal study of British women. Ann Hum Biol. 2005;32(3):247–59.
Lawrence M, Whitehead RG. Physical activity and total energy expenditure of child-bearing Gambian village women. Eur J Clin Nutr. 1988;42(2):145–60.
Löf M, Forsum E. Activity patterns and energy expenditure due to physical activity before and during pregnancy in healthy Swedish women. Brit J Nutr. 2006;95(2):296–302.
Rousham EK, Clarke PE, Gross H. Significant changes in physical activity among pregnant women in the UK as assessed by accelerometry and self-reported activity. Eur J Clin Nutr. 2006;60(3):393–400.
Forsum E, Kabir N, Sadurkis A, Weterterp K. Total energy expenditure of healthy Swedish women during pregnancy and lactation. Am J Clin Nutr. 1992;56(2):334–42.
Heini A, Scuhtz Y, Diaz E, Prentice AM, Whitehead RG, Jequier E. Free-living energy expenditure measured by two independent techniques in pregnant and nonpregnant Gambian women. Am J Physiol. 1994;261(1 Pt 1):E9–17.
Lawrence M, Singh J, Lawrence F, Whitehead RG. The energy cost of common daily activities in African women: increased expenditure in pregnancy? Am J Clin Nutr. 1985;42(5):753–63.
Singh J, Prentice AM, Diaz E, Coward WA, Ashford J, Sawyer M. Energy expenditure of Gambian women during peak agricultural activity measured by the doubly-labelled water method. Brit J Nutr. 1989;62(2):315–29.
Van Raaij JM, Vermaat-Miedema SH, Schonk CM, Peek ME, Hautvast JG. Energy requirements of pregnancy in the Netherlands. Lancet. 1987;2(8565):953–5.
Durnin JV, McKillop FM, Grant S, Fitzgerald G. Energy requirements of pregnancy in Scotland. Lancet. 1987;2(8564):897–900.
Moss SJ, Van Oort AF, De Boer MR, Schutz Y. Objectively determined activity energy expenditure during pregnancy and changes in body mass: the HAPPY-study. Oral presentation at the 22nd European College of Sport Science Conference; 2014 Jul 2–5; Amsterdam, The Netherlands.
Shephard RJ. Limits to the measurement of habitual physical activity by questionnaires. Brit J Sport Med. 2003;37(3):197–206.
Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, et al. Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sport Exerc. 2000;32(9):498–504.
Ainsworth BE, Richardson M, Jacobs DR, Leon AS. Gender differences in physical activity. Women Sport Phys Activ J. 1993;2(1):1–17.
Poudevigne MS, O’Conner PJ. A review of physical activity patterns in pregnant women and their relationship to psychological health. Sport Med. 2006;36(1):19–38.
Ainslie PN, Reilly T, Westerterp KR. Estimating human energy expenditure; a review of techniques with particular reference to doubly labelled water. Sport Med. 2003;33(9):683–98.
Speakman JR. The history and theory of the doubly labelled water technique. Am J Clin Nutr. 1998;68(4):932–8.
Herrmann SD, Heumann KJ, Der Ananian CA, Ainsworth BE. Validity and reliability of the global physical activity questionnaire (GPAQ). Meas Phys Educ Exerc Sci. 2013;17(3):221–35.
Bauman AE, Sallis JF. Global problems require global studies. Am J Prev Med. 2008;34(6):544–5.
Guthold R, Ono T, Strong KL, Chatterji S, Morabia A. Worldwide variability in physical inactivity: a 51-country survey. Am J Prev Med. 2008;34(6):486–94.
Armstrong T, Bull F. Development of the World Health Organization Global Physical Activity Questionnaire (GPAQ). J Public Health. 2006;14(2):66–70.
Aittasalo M, Pasanen M, Fogelholm M, Ojala K. Validity and repeatability of a short pregnancy leisure time physical activity questionnaire. J Phys Activ Health. 2010;7(1):109–18.
Chasan-Taber L, Schmidt MD, Roberts DE, Hosmer D, Markenson G, Freedson PS. Development and validation of a pregnancy physical activity questionnaire. Med Sci Sport Exerc. 2004;36(10):1750–60.
Evenson KR, Wen F. Measuring physical activity among pregnant women using a structured one-week recall questionnaire: evidence for validity and reliability. Int J Behav Nutr Phys Activ. 2010;7(21):1–12.
Schmidt MD, Freedson PS, Pekow P, Roberts D, Sternfeld B, Chasan-Taber L. Validation of the Kaiser physical activity survey in pregnant women. Med Sci Sport Exerc. 2006;38(1):42–50.
Cohen TR, Plourde H, Koski KG. Use of the pregnancy physical activity questionnaire (PPAQ) to identify behaviors associated with appropriate gestational weight gain during pregnancy. J Phys Activ Health. 2013;10(7):1000–7.
Stein AD, Rivera JM, Pivarnik JM. Measuring energy expenditure in habitually active and sedentary pregnant women. Med Sci Sport Exerc. 2003;27(5):634–40.
Perkins CC, Pivarnik JM, Paneth N, Stein AD. Physical activity and fetal growth during pregnancy. Obstet Gynecol. 2007;109(1):81–7.
Barreira TV, Kang M, Caputo JL, Farley RS, Renfrow MS. Validation of the Actiheart monitor for the measurement of physical activity. Int J Exerc Sci. 2009;2(2):60–71.
Eston RG, Rowlands AV, Ingledew DK. Validity of heart rate, pedometry, and accelerometry for predicting the energy cost of children’s activities. J App Physiol. 1998;84(1):362–71.
Janz KF. Use of heart rate monitors to assess physical activity. In: Welk GJ, editor. Physical activity assessments for health-related research. 1st ed. United States: Human Kinetics; 2002. pp. 143–61.
Strath SJ, Swartz AM, Basset DR, O’Brien WL, King GA, Ainsworth BE. Evaluation of heart rate as a method for assessing moderate intensity physical activity. Med Sci Sport Exerc. 2000;32(9):465–70.
Freedson PS, Miller K. Objective monitoring of physical activity using motion sensors and heart rate. Res Quart Exerc Sport. 2000;71(2):21–9.
Welk GJ. Use of accelerometry-based activity monitors to assess physical activity. In: Welk GJ, editor. Physical activity assessments for health-related research. 1st ed. United States: Human Kinetics; 2002. pp. 125–40.
Corder K, Brage C, Mattocks C, Ness A, Riddoch C, Wareham NJ, Ekelund U. Comparison of two methods to assess PAEE during six activities in children. Med Sci Sports Exerc. 2007;39(12):2180–8.
Sallis JF, Saelens BE. Assessment of physical activity by self-report: status, limitations, and future directions. Res Quart Exercise Sport. 2000;71(2):1–7.
Strath SJ, Bassett DR, Thompson DL, Swarts AM. Validity of the simultaneous heart rate-motion sensor technique for measuring energy expenditure. Med Sci Sport Exerc. 2002;34(5):888–94.
Treuth MS. Applying multiple methods to improve the accuracy of activity assessments. In: Welk GJ, editor. Physical activity assessments for health-related research. 1st ed. United States: Human Kinetics; 2002. pp. 213–24.
Spierer DK, Hagins M, Rundle A, Pappas E. A comparison of energy expenditure estimates from the Actiheart and Actical physical activity monitors during low intensity activities, walking and jogging. Eur J App Physiol. 2011;111(4):659–68.
Brage S, Brage N, Franks PW, Ekelund U, Wareham NJ. Reliability and validity of the combined heart rate and movement sensor Actiheart. Eur J Clin Nutr. 2005;59(4):561–70.
Brage S, Brage N, Ekelund U, Franks PW, Wareham NJ. Effect of combined movement and heart rate monitor placement on physical activity estimates during treadmill locomotion and free-living. Euro J Appl Phys. 2006;96(5):517–24.
Campbell N, Prapavessis H, Gray C, McGowan E, Rush E, Maddison R. The Actiheart in adolescents: a doubly labelled water validation. Pediatr Exerc Sci. 2012;24(4):589–602.
Horns JF, Ratcliffe LP, Leggett JC, Swanson MS. Pregnancy outcomes among active and sedentary primiparous women. J Obstet Gynaecol Neonat Nurs. 1996;25(1):49–54.
Cioffi J, Schmied V, Dahlen H, Mills A, Thornton C, Duff M, et al. Physical activity in pregnancy: women’s perceptions, practices, and influencing factors. J Midwifery Women Health. 2010;55(5):455–61.
Duncombe D, Wertheim EH, Skouteris H, Paxton SJ, Kelly L. Factors related to exercise over the course of pregnancy including women’s beliefs about the safety of exercise during pregnancy. Midwifery. 2007;25(4):430–8.
Hinton PS, Olson CM. Predictors of pregnancy-associated change in physical activity in a rural white population. Matern Child Health J. 2001;5(1):7–14.
Agarwal S, Agarwal A, Agarwal KN, Agarwal DK, Bansal A. Physical activity and pregnancy outcome in rural undernourished women. Indian Pediatr. 2001;38:1017–22.
Bungum TJ, Peaslee DL, Jackson AW, Perez MA. Exercise during pregnancy and type of delivery in nulliparae. J Obstet Gynecol Neonat Nurs. 2000;29(3):258–64.
Hegaard HK, Damm P, Hedegaard M, Henriksen TB, Ottesen B, Dykes A, et al. Sports and leisure time physical activity during pregnancy in nulliparous women. Matern Child Health J. 2011;15(6):806–13.
Mottola MF, Campbell MK. Activity patterns during pregnancy. Can J App Physiol. 2003;28(4):642–53.
Pereira MA, Rifas-Shiman SL, Kleinman KP, Rich-Edwards JW, Peterson KE, Gillman MW. Predictors of change in physical activity during and after pregnancy. Am J Prev Med. 2007;32(4):312–9.
Albright C, Maddock JE, Nigg CR. Physical activity before pregnancy and following childbirth in a multiethnic sample of healthy women in Hawaii. Women Health. 2005;42(3):95–110.
Evenson KR, Savits DA, Huston SL. Leisure-time physical activity among pregnant women in the U.S. Paediatr Perinat Epidemiol. 2004;18(6):400–7.
Costa D D, Rippen N, Dritsa M, Ring A. Self-reported leisure-time physical activity during pregnancy and relationship to psychological well-being. J Psychosom Obstet Gynaecol. 2003;24(2):111–9.
Hatch MC, Ji BT, Shu XO, Susser M. Does standing, lifting, climbing or long hours of working during pregnancy have an effect during fetal growth? Epidemiol. 1997;8(5):530–6.
Ning Y, Williams MA, Dempsey JC, Sorensen TK, Frederick IO, Luthy DA. Correlates of recreational physical activity in early pregnancy. J Matern Fetal Neonatal Med. 2003;13(6):385–93.
Zhang J, Savits DA. Exercise during pregnancy among US women. Ann Epidemiol. 1996;6(1):53–9.
Domingues MR, Barros AJ. Leisure-time physical activity during pregnancy in the 2004 Pelotas Birth Cohort Study. Rev Saude Publ. 2007;41(2):173–80.
Barnes DL, Adair LS, Popkin BM. Women’s physical activity and pregnancy outcome: a longitudinal analysis from the Philippines. Int J Epidemiol. 1991;20(1):162–72.
Lui J, Blair SN, Teng Y, Ness AR, Lawlor DA, Riddoch C. Physical activity during pregnancy in a prospective cohort of British women: results from the Avon longitudinal study of parents and children. Eur J Epidemiol. 2010;26(3):237–47.
Brunette EL, Kotze J, Wood PS, Du Toit PJ, Grant CC. An epidemiological study of physical activity patterns and weight gain in physically active and sedentary pregnant women in Tshwane, South Africa. Afr J Phys Health Educ Recr Dance. 2012;18(1):132–43.
Dempsey JC, Sorensen TK, Williams MA, Lee IM, Miller RS, Dashow EE, et al. Prospective study of gestational diabetes mellitus risk in relation to maternal recreational physical activity before and during pregnancy. Am J Epidemiol. 2004;159(7):663–70.
Juhl M, Anderson PK, Olsen J, Madsen M, Jørgensen T, Nøhr EA, et al. Physical exercise during pregnancy and the risk of preterm birth: a study within the Danish National Birth Cohort. Am J Epidemiol. 2008;167(7):63e1–8.
Sørenson TK, Williams MA, Lee IM, Dashow EE, Thompson ML, Luthy DA. Recreational physical activity during pregnancy and risk of preeclampsia. Hypertension. 2003;41(6):1273–80.
Goldenberg RL, Cliver SP, Bronstein J, Cutter GR, Andrews WW, Mennemeyer ST. Bed rest in pregnancy. Obstet Gynecol. 1994;84(1):131–6.
Crowther CA, Han S. Hospitalisation and bed rest for multiple pregnancy. Cochrane Database Syst Rev. 2010;7:CD000110. doi:10.1002/14651858.CD000110.pub2.
Biolo G, Heer M, Nirici M, Strollo F. Microgravity as a model of ageing. Curr Opin Clin Nutr Metab Care. 2003;6(1):31–40.
Borodulin K, Evenson KR, Herring AH. Physical activity patterns during pregnancy through postpartum. BMC Women Health. 2009;19(9):32–9.
Szumilewicz A, Wojtyla A, Zarębska A, Drobnik-Kozakiewicz I, Sawczyn M, Kwitneiwska A. Influence of prenatal physical activity on the course of labour and delivery according to the new Polish standard for perinatal care. Ann Agric Environ Med. 2013;20(2):380–9.
Aaron DL, Jekal YS, LaPorte RE. Epidemiology of physical activity from adolescence to young adulthood. Word Rev Nutr Diet. 2005;94:36–41.
Wahlqvist ML. Physical activity for health: an overview. Word Rev Nutr Diet. 2005;95:62–72.
Helmrich SP, Ragland DR, Leung RW, Paffenbarger RS. Physical activity and reduced occurrence of non-insulin-dependent diabetes mellitus. N Engl J Med. 1991;325(3):147–52.
Kushi L, Fee R, Folsom AR, Mink PJ, Anderson KE, Sellers TA. Physical activity and mortality in postmenopausal women. J Am Med Assoc. 1989;277(16):1287–92.
Sandvik L, Erikssen J, Thaulow E, Erikssen G, Mundal R, Rodahl K. Physical fitness as a predictor of mortality among healthy, middle-aged Norwegian men. N Engl J Med. 1993;328(8):533–7.
Hu G, Jousilahti P, Barengo NC, Qiao Q, Lakka TA, Tuomilehto J. Physical activity, cardiovascular risk factors, and mortality among Finnish adults with diabetes. Diabetes Care. 2005;28(4):799–805.
Lee CD, Blair SN, Jackson AS. Cardiorespiratory fitness, body composition, and all-cause and cardiovascular disease mortality in men. Am J Clin Nutr. 1999;69(3):373–80.
Paisley TS, Joy EA, Price RJ. Exercise during pregnancy: a practical approach. Curr Sport Med Rep. 2003;2(6):325–30.
Burchfiel CM, Sharp DS, Curb JD, Rodriguez BL, Hwang LJ, Marcus B. Physical activity and incidence of diabetes: the Honolulu heart program. Am J Epidemiol. 1995;141(4):360–8.
Sigal JR, Kenny GP, Wasserman DH, Castaneda-Sceppa C, White RD. Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care. 2006;29(6):1433–8.
Ellekjær H, Holmen J, Ellekjaer E, Vatten L. Physical activity and stroke mortality in women: ten-year follow-up of the Nord-Trøndelag health survey, 1984–1986. Stroke. 2000;31(1):14–8.
Laaksonen DE, Lakka HM, Lynch J, Lakka TA, Kishanen L, Rauramaa R, et al. Cardiorespiratory fitness and vigorous leisure-time physical activity modify the association of small size at birth with the metabolic syndrome. Diabetes Care. 2003;26(7):2156–64.
Warburton DE, Nicol CW, Bredin SS. Health benefits of physical activity: the evidence. Can Med Assoc J. 2006;174(7):801–9.
Clapp JF. The course of labor after endurance exercise during pregnancy. Am J Obstet Gynecol. 1990;163(6):1799–805.
Sternfeld B. Physical activity and pregnancy outcome: review and recommendations. Sport Med. 1997;23(1):33–47.
Wolfe LA, Hall P, Webb KA, Goodman L, Monga M, McGrath MJ. Prescription of aerobic exercise during pregnancy. Sport Med. 1989;8(5):273–301.
Arena B, Maffulli N. Exercise in pregnancy: how safe is it? Sport Med Arthroscop Rev. 2002;10(1):15–22.
Wallace AM, Boyer DB, Dan A, Hol, Aerobic exercise K. Maternal self-esteem, and physical discomforts during pregnancy. J Nurs-Midwifery. 1986;31(6):255–62.
Bung P, Artal R, Khodiguian N, Kjos S. Exercise in gestational diabetes: an optional therapeutic approach? Diabetes. 1991;40(2):182–5.
Bung P, Artal R. Gestational diabetes and exercise: a survey. Semin Perinatol. 1996;20(4):328–33.
Borg-Stein J, Dugan SA, Gruber J. Musculoskeletal aspects of pregnancy. Am J Phys Med Rehab. 2005;84(3):180–92.
Hutchinson SL. Physical activity, recreation, leisure, and sport: essential pieces of the mental health and well-being puzzle [Internet]. Halifax: Recreation Nova Scotia; 2012 [cited 2012 July 6]. http://www.recreationns.ns.ca/wp-content/uploadhere/2012/05/MentalHealthLit.pdf.
Adams TB, Moore MT, Dye J. The relationship between physical activity and mental health in a national sample of college females. Women Health. 2007;45(1):69–85.
Clapp JF, Rockey R, Treadway JL, Carpenter MW, Artal RM, Warrnes C. Exercise in pregnancy: a short review. Med Sci Sports Exerc. 1992;24(6):294–300.
Kritz-Silverstein D, Barrett-Conner E, Corbeau C. Cross-sectional and prospective study of exercise and depressed mood in the elderly. Am J Epidemiol. 2001;153(6):596–603.
Strawbridge WJ, Deleger S, Roberts R, Kaplan GA. Physical activity reduces the risk of subsequent depression for older adults. Am J Epidemiol. 2002;156(4):328–34.
Yang X, Telama R, Hirvensalo M, Hintsanen M, Heintsa T, Pulkki-Raback, et al. The benefits of sustained leisure-time physical activity on job strain. Occ Med. 2010;60(5):369–75.
Poudevigne MS, O’Conner PJ. Physical activity and mood during pregnancy. Med Sci Sport Exerc. 2005;37(8):1374–80.
Mottola MF. Exercise in the postpartum period: practical applications. Curr Sport Med Rep. 2002;1(6):362–8.
Carey GB, Quinn TJ. Exercise and lactation: are they compatible? Can J App Physiol. 2001;26(1):44–74.
Kalisiak B, Spitznagle T. What effect does an exercise program for healthy pregnant women have on the mother, fetus, and child? Am Acad Phys Med Rehab. 2009;1(3):261–7.
Domenjoz I, Kayser B, Boulvain M. Effect of physical activity during pregnancy on mode of delivery. Am J Obstet Gynecol. 2014; 21(4):401.e1–11.
Clapp JF. Exercise during pregnancy: a clinical update. Clin Sports Med. 2000;19(2):273–86.
Shangold MM. Exercise during pregnancy: current state of the art. Can Fam Physician. 1989;35:1675–80.
Van Oort AF. The relationship between habitual physical activity patterns of pregnant women and foetal growth parameters: a longitudinal observational study [dissertation]. Potchefstroom: North-West University; 2014.
Luke B, Papiernik E. The effects of lifestyle on prematurity. In: Elder MG, Lamont RF, Romero R, editors. Preterm labor. New York: Churchill Livingstone; 1997. pp. 127–52.
Mozurkewich EL, Luke B, Avni M, Fredric MW. Working conditions and adverse pregnancy outcome: a meta-analysis. Obstet Gynecol. 2000;95(4):623–35.
Edwards MJ. Hyperthermia as a teratogen: a review of experimental studies and their clinical significance. Teratog Carcinog Mutagen. 1986;6(6):563–82.
Milunsky A, Ulcickas M, Rothman KJ, Willett W, Jick SS, Jick H. Maternal heat exposure and neural tube defects. J Am Med Assoc. 1992;268(7):882–5.
Stevenson L. Exercise in pregnancy: part 2: recommendations for individuals. Can Fam Physician. 1997;(43):107–111.
Takito MY, Benício MH, Neri LC. Physical activity by pregnant women and outcomes for newborns: a systematic review. Revis Saúd Públic. 2009;43(6):1059–69.
Clapp JF, Little KD. The interaction between regular exercise and selected aspects of women’s health. Am J Obstet Gynecol. 1995;173(1):2–9.
Clapp JF. The effects of maternal exercise on early pregnancy outcome. Am J Obstet Gynecol. 1989;161(6):1453–7.
Clapp JF, Lopez B, Harcar-Swvcik R. Neonatal behavioural profile of the offspring of women who continued to exercise regularly throughout pregnancy. Am J Obstet Gynecol. 1999;180(1):91–4.
Clapp JF, Simonian S, Lopez B, Appleby-Wineberg S, Harcar-Sevcik R. The one-year morphometric and neurodevelopmental outcome of the offspring of women who continued to exercise regularly throughout pregnancy. Am J Obstet Gynecol. 1998;178(3):594–9.
Hall DC, Kaufmann DA. Effects of aerobic and strength conditioning on pregnancy outcomes. Am J Obstet Gynecol. 1987;157(5):1199–203.
Hatch MC, Shu XO, Mclean DE, Levin B, Begg M, Reuss L, et al. Maternal exercise during pregnancy, physical fitness, and fetal growth. Am J Epidemiol. 1993;137(10):1105–14.
Kardel KR, Kase T. Training in pregnant women: effects on fetal development and birth. Am J Obstet Gynecol. 1998;178(2):280–6.
Klebanoff MA, Shiono PH, Carey JC. The effect of physical activity during pregnancy on preterm delivery and birth weight. Am J Obstet Gynecol. 1990;163(5 Pt 1):1450–6.
Kulpa PJ, White BM, Visscher R. Aerobic exercise in pregnancy. Am J Obstet Gynecol. 1987;156(6):1395–403.
O’Neill ME. Maternal rectal temperature and fetal heart rate responses to upright cycling in late pregnancy. Brit J Sport Med. 1996;30(1):32–5.
Sternfeld B, Quesenberry CP, Eskenazi B, Newman LA. Exercise during pregnancy and pregnancy outcome. Med Sci Sport Exerc. 1995;27(5):634–40.
Magann EF, Evans SF, Weitz B, Newnham J. Antepartum, intrapartum, and neonatal significance of exercise on healthy low-risk pregnant working women. Obstet Gynecol. 2002;99(3):466–72.
Rao S, Kanade A, Margetts BM, Yajnik CS, Lubree H, Rege S, et al. Maternal activity in relation to birth size in rural India: the Pune Maternal Nutrition Study. Eur J Clin Nutr. 2003;57(4):531–42.
Campbell MK, Mottola MF. Recreational exercise and occupational activity during pregnancy and birth weight: a case-control study. Am J Obstet Gynecol. 2001;184(3):403–8.
Magann EF, Evans SF, Newnham JP. Employment, exertion, and pregnancy outcome: assessment by kilocalories expended each day. Am J Obstet Gynecol. 1996;175(1):182–7.
Wolfe LA, Mottola MF. Validation of guidelines for aerobic exercise in pregnancy. In: Kumbhare DA, Basmajian JV, editors. Decision making and outcomes in sport rehabilitation. New York: Churchill Livingstone; 2000. pp. 205–22.
Bell RJ. The effect of vigorous exercise during pregnancy on birth weight. J Sci Med Sport. 2002;5(1):32–6.
Derbyshire E, Davies GJ, Costarelli V, Dettmar PW. Habitual patterns of physical activity during pregnancy and postnatally. Matern Health. 2008;16(1):20–4.
Riemann MK, Kanstrup Hansen IL. Effects on the foetus of exercise in pregnancy. Scand J Med Sci Sport. 2000;10(1):12–9.
Artal R. Exercise and pregnancy. Clin Sport Med. 1992;11(2):363–77.
Bell RJ, O’Neill M. Exercise and pregnancy: a review. Birth. 1994;21(2):85–9.
Dewey KG, McCrory MA. Effects of dieting and physical activity on pregnancy and lactation. Am J Clin Nutr. 1994;59(2S):446-53.
Jarski RW, Tripett DL. The risks and benefits of exercise during pregnancy. J Fam Prac. 1990;30(2):185–9.
Lokey EA, Tran ZV, Wells CL, Meyers BC, Tran AC. Effects of physical exercise on pregnancy outcomes: a meta-analytic review. Med Sci Sport Exerc. 1991;23(11):1234–9.
Schick-Boschetto B, Rose NC. Exercise in pregnancy. Obstet Gynecol Sur. 1991;47(1):10–3.
Snyder JL. Aerobic exercise during pregnancy. J Am Board Fam Prac. 1990;3(1):50–3.
Clapp JF. Exercise and fetal health. J Develop Physiol. 1991;15(1):9–14.
Hutch R, Erkkola R. Pregnancy and exercise-exercise and pregnancy. A short review. Brit J Obstet Gynaecol. 1990;97(3):208–14.
McMurray RG, Mottola MF, Wolfe LA, Artal R, Millar L, Pivarnik JM. Recent advances in understanding maternal and fetal responses to exercise. Med Sci Sport Exerc. 1993;25(12):1305–21.
Revelli A, Durandom A, Massobrio M. Exercise and pregnancy: a review of maternal and fetal effects. Obstet Gynecol Sur. 1992;47(6):355–67.
Warren MP. Exercise in women: effects on reproductive system and pregnancy. Clin Sport Med. 1991;10(1):131–9.
Alderman BW, Zhao H, Holt VL, Watts DH, Beresford AA. Maternal physical activity in pregnancy and infant size for gestational age. Ann Epidemiol. 1998;8(8):513–9.
Bell RJ, Palma S. Antenatal exercise and birth weight. Aus N Z J Obstet Gynaecol. 2000;40(1):70–3.
Clapp JF, Kim H, Burciu B, Lopez B. Beginning regular exercise in early pregnancy: effect on fetoplacental growth. Am J Obstet Gynecol. 2000;183(6):1484–8.
Clapp JF, Kim H, Burciu B, Schmidt S, Petry K, Lopez B. Continuing regular exercise during pregnancy: effect of exercise volume on fetoplacental growth. Am J Obstet Gynecol. 2002;186(1):142–7.
Haakstad LAH, Bø K. Exercise in pregnant women and birth weight: a randomized controlled trial. BMC Pregnancy Childbirth. 2011;(11):66–73.
Marquez-Sterling S, Perry AC, Kaplan TA, Halberstein RA, Signorile JF. Physical and psychological changes with vigorous exercise in sedentary primigravidae. Med Sci Sport Exerc. 2000;32(1):58–62.
Prevedel T, Calderon I, Abadde J, Borges V, Rudge M. Maternal and perinatal effects of hydrotherapy in pregnancy. Rev Brasil Ginecol Obstet. 2003;25(1):53–9.
Price BB, Amini SB, Kappeler K. Exercise in pregnancy: effect on fitness and obstetric outcomes—a randomized trial. Med Sci Sport Exerc. 2012;44(12):2263–70.
Macera CA, Ham SA, Yore MM, Jones DA, Ainsworth BE, Kimsey CD, et al. Prevalence of physical activity in the United States: behavioral risk factor surveillance system. Prev Chron Dis. 2001;2(2):A17.
Hall MH, Chng PK, MacGillivray I. Is routine antenatal care worthwhile? Lancet. 1980;2(8185):78–80.
Juhl M, Olsen J, Anderson PK, Nøhr EA, Anderson AN. physical exercise during pregnancy and fetal growth measures: a study within the Danish National Birth Cohort. Am J Obstet Gynecol. 2010;202(1):1e1–8.
Barker DJP, Osmond C, Simmonds SJ, Wield GA. The relation of small head circumference and thinness at birth to death from cardiovascular diseases in adult life. BMJ. 1993;306(6875):422–6.
Oken E, Gillman MW. Fetal origins of obesity. Obes Res. 2003;11(4):496–506.
Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2003. Nat Vital Stat Rep. 2005;54(2):1–116.
Massett HA, Greenup M, Ryan CE, Staples DA, Green NS, Maibach EW. Public perceptions about prematurity: a national survey. Am J Prev Med. 2003;24(2):120–7.
Gardosi J, Mul T, Mongelli M, Fagan D. Analysis of birthweight and gestational age in antepartum stillbirths. Brit J Obstet Gynaecol. 1998;105(5):524–30.
Lobos H, Rennie JM, Lees C. The natural history of fetal growth restriction in women with abnormal uterine artery Doppler. Prenat Diag. 2005;25(4):331–2.
Breeze ACG, Lees CC. Prediction and perinatal outcomes of fetal growth restriction. Semin Fetal Neonat Med. 2007;12(5):383–97.
Vielwerth SE, Jensen RB, Larsen T, Greisen G. The impact of maternal smoking on fetal and infant growth. Early Hum Dev. 2007;83(8):491–5.
Lucas A. Programming by early nutrition in man. In: Bock GR, Whelan J, editors. The childhood environment and adult disease. Chichester: Wiley; 1991. pp. 38–50.
Lucas A. Role of nutritional programming in determining adult morbidity. Arch Dis Child. 1994;71(4):288–90.
Ekbom A, Hsieh CC, Lipworth L, Wolk A, Pontén J, Adami HO, et al. Perinatal characteristics in relation to incidence of and mortality from prostate cancer. BMJ (Res C editor). 1996;313(7053):337–41.
Innes K, Byers T, Schymura M. Birth characteristics and subsequent risk for breast cancer in very young women. Am J Epidemiol. 2000;152(12):1121–8.
Karter AJ, Rowell SE, Ackerman LM, Mitchell BD, Ferrara A, Selby JV, et al. Excess maternal transmission of type 2 diabetes. Diabetes Care. 1999;22(6):938–43.
Shaheen SO, Sterne JA, Montgomery SM, Azima H. Birth weight, body mass index and asthma in young adults. Thorax. 1999;54(5):396–402.
Barker DJP. Fetal origins of coronary heart disease. BMJ. 1995;311(6998):171–4.
Barker DJP, Osmond C, Golding J, Kuh D, Wadsworth MEJ. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298(6673):564–7.
Barker DJP, Winter PD, Osmond C, Margetts B. Weight in infancy and death from ischemic heart disease. Lancet. 1989;2(8663):577–80.
Gupta R, Gupta VP. Meta-analysis of coronary heart disease in India. Indian Heart J. 1996;48(3):241–5.
Hales CN, Barker DJP, Clark PMS, Cox LJ, Fall CHD, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;303(6809):1019–22.
Law CM, Shiell AW. Is blood pressure inversely related to birth-weight? The strength of evidence from a systematic review of the literature. J Hypertension. 1996;14(8):935–41.
Mckeigue PM, Shah B, Marmot MG. Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asia. Lancet. 1991;377(8738):330–6.
Stien CE, Fall CHD, Kumaran K, Osmond C, Cox V, Barker DJP. Fetal growth and coronary heart disease in South India. Lancet. 1996;348(9037):1269–73.
Yajnik CS, Fall CHD, Vaidya U, Pandit AN, Bavdekar A, Bhat DS, et al. Fetal growth and glucose and insulin metabolism in four year old Indian children. Diabetic Med J Brit Diabetic Assoc. 1995;306(4):422–6.
Nair L, Nair MKC, Chacko DS. Markers of fetal onset adult diseases. Indian Pediatr. 2009;46:S48–54.
Rich-Edwards JW, Colditz GA, Stampfer MJ, Manson JE, Rosner B, Hankinson SE, et al. Birth-weight and the risk for type 2 diabetes mellitus in adult women. Ann Int Med. 1999;130(4 Pt 1):278–84.
Hediger ML, Overpeck MD, Kuczmarski RJ, McGlynn A, Maurer KR, Davis WW. Muscularity and fatness of infants and young children born small- or large-for-gestational-age. Pediatrics. 1998;102(5):E60–7.
Hammami M, Walters JC, Hockman EM, Koo WW. Disproportionate alterations in body composition of large for gestational age neonates. J Pediatr. 2001;138(6):817–21.
Vaessen N, Janssen JA, Heutink P, Hofman A, Lamberts SWJ, Oostra BA, et al. Association between genetic variation in the gene for insulin-like growth factor-I and low birthweight. Lancet. 2002;359(9311):1036–7.
Bobak M. Outdoor air pollution, low birth weight, and prematurity. Environ Health Perspect. 2000;108(2):173–6.
Dejmek J, Selevan SG, Benes I, Solansky I, Sram RJ. Fetal growth and maternal exposure to particulate matter during pregnancy. Environ Health Perspect. 1999;107(6):475–80.
Ha EH, Hong YC, Lee BE, Woo BH, Schwartz J, Christiani DC. Is air pollution a risk factor for low birth weight in Seoul? Epidemiology. 2001;12(6):643–8.
Maisonet M, Bush TJ, Correa A, Jaakkola JK. Relation between ambient air pollution and low birth weight in the northeastern United States. Environ Health Perspect. 2001;109(3):351–6.
Ritz B, Yu F. The effect of ambient carbon monoxide on low birth weight among children born in Southern California between 1989 and 1993. Environ Health Perspect. 1999;107(1):17–25.
Ritz B, Yu F, Chapa G, Fruin S. Effect of air pollution on preterm birth among children born in Southern California between 1989 and 1993. Epidemiol. 2000;11(5):502–11.
Wang X, Ding H, Ryan L, Xu X. Association between air pollution and low birth weight: a community-based study. Environ Health Persp. 1997;105(5):514–20.
Xu X, Ding H, Wang X. Acute effects of total suspended articles and sulphur dioxides on preterm delivery: a community-based cohort study. Arch Environ Health. 1995;50(6):407–15.
Maisonet M, Correa A, Misra D, Jaakkola JJK. A review of the literature on the effects of ambient air pollution on fetal growth. Environ Res. 2004;95(1):106–15.
De Santis M, De Luca C, Mappa I, Quattrocchi T, Angelo L, Cesari E. Smoking, alcohol consumption and illicit drug use in an Italian population of pregnant women. Eur J Obstet Gynecol Reprod Biol. 2011;159(1):106–10.
Jauniaux E, Greenough A. Short and long term outcomes of smoking during pregnancy. Early Hum Dev. 2007;83(11):697–8.
Pollack H, Lantz PM, Frohna JG. Maternal smoking and adverse birth outcomes among singletons and twins. Am J Pub Health. 2000;90(3):395–341.
Samper MP, Jiménez-Muro A, Nerín I, Marqueta A, Ventura P, et al. Maternal active smoking and newborn body composition. Early Hum Dev. 2012;88(3):141–5.
Figueras F, Meler E, Eixarch E, Francis A, Coll O, Gratacos E, et al. Association of smoking during pregnancy and fetal growth restriction: subgroups of higher susceptibility. Eur J Obstet Gynecol Reprod Biol. 2008;138(2):171–5.
Barker DJP, Gluckman PD, Robinson JS. Conference report: fetal origins of adult disease-report of the first international study group. Placenta. 1995;16(3):317–20.
Bernstein IM, Mongeon JA, Badger GJ, Solomon L, Heil SH, Higgins ST. Maternal smoking and its association with birth weight. Obstet Gynecol. 2005;106(5):986–91.
Källen K. The impact of maternal smoking during pregnancy on delivery outcome. Eur J Pub Health. 2001;11(3):329–33.
Horta BL, Victora CG, Menezes AM, Halpern R, Barros FC. Low birth weight, preterm births and intrauterine growth retardation in relation to maternal smoking. Paediatr Perinat Epidemiol. 1997;11(2):140–51.
Fantuzzi G, Aggazzotti G, Righi E, Faccinetti F, Bertucci E, Kanitz S. Preterm delivery and exposure to active and passive smoking during pregnancy: a case-control study from Italy. Paediatr Perinat Epidemiol. 2007;21(3):194–200.
Dekeyser-Boccara J, Milliez J. Smoking and ectopic pregnancy: is there a causal relationship? J Gynecol. 2005;34(1):119–23.
Jauniaux E, Burton GJ. Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev. 2007;83(11):699–706.
Cnattingius S, Lambe M. Trends in smoking and overweight during pregnancy: prevalence, risk of pregnancy complications and adverse pregnancy outcomes. Semin Perinatol. 2002;26(4):286–95.
Kyrklund-Blomberg NB, Genuser G, Cnattingius S. Placental abruption and perinatal death. Paediatr Perinat Epidemiol. 2001;15(3):290–7.
Mitchell EA, Milerad J. Smoking and the sudden infant death syndrome. Rev Environ Health. 2006;21(2):81–104.
Wisborg K, Kesmodel U, Henriksen TB, Olsen SF, Secher NJ. Exposure to tobacco smoke in utero and the risk of stillbirth and death in the first year of life. Am J Epidemiol. 2001;154(4):322–7.
Andersson K, Arner P. Systemic nicotine stimulates human adipose tissue lipolysis through local cholinergic and catecholaminergic receptors. Int J Obes Metab Dis. 2001;25(8):1225–33.
Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan B. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction: the Vermont Oxford Network. Am J Obstet Gynecol. 2000;182(1):198–206.
Cliver SP, Goldenberg MD, Cutter GR, Hoffman HJ, Davis RO, Nelson KG. The effect of cigarette smoking on neonatal anthropometric measurements. Obstet Gynecol. 1995;85(4):625–30.
Reeves S, Bernstein I. Effects of maternal tobacco-smoke exposure on fetal growth and neonatal size. Expert Rev Obstet Gynecol. 2008;3(6):719–39.
Hernández-Martínez C, Val VA, Subías JE, Sans JC. A longitudinal study on the effects of maternal smoking and secondhand smoke exposure during pregnancy on neonatal neurobehavior. Early Hum Dev. 2012;88(6):403–8.
Bruchova H, Vasikova A, Merkerova M, Milcova A, Topinka J, Balascak I, et al. Effect of maternal tobacco smoke exposure on the pacental transcriptome. Placenta. 2010;31(3):186–91.
Zhang J, Ratcliffe JM. Paternal smoking and birthweight in Shanghai. Am J Pub Health. 1993;83(2):207–10.
Eskenazi B, Prehn AW, Christianson RE. Passive and active maternal smoking as measured by serum cotinine: the effect on birthweight. Am J Pub Health. 1995;85(3):395–8.
Hansen C, Sorensen LD, Asmussen I, Autrup H. Transplacental exposure to tobacco smoke in human-adduct formation in placenta and umbilical cord vessels. Teratog Carcinog Mutagen. 1992;12(2):51–60.
Jauniaux E, Gulbis B, Acharya G, Thiry P, Rodeck C. Maternal tobacco exposure and cotinine levels in fetal fluids in the first half of pregnancy. Obstet Gynecol. 1999;93(1):25–9.
Luck W, Nau H, Hansen R, Stelding R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol Therap. 1985;8(6):384–95.
Lichtensteiger W, Ribary U, Schiumpf M, Odermatt B, Widemer HR. Prenatal adverse effects of nicotine on the developing brain. Prog Brain Res. 1988;73:137–57.
Rasmussen S, Irgens LM. The effects of smoking and hypertensive disorders on fetal growth. BMC Pregnancy Childbirth. 2006;6:16–23.
Windham GC, Hopkins B, Fenster L, Swan SH. Prenatal active or passive tobacco smoke exposure and the risk of preterm delivery or low birth weight. Epidemiol. 2000;11(4):427–33.
Morley R, Leeson PC, Lister G, Lucas A. Maternal smoking and blood pressure in 7.5 to 8 year old offspring. Arch Dis Child. 1995;72(2):120–4.
Williams S, Poulton R. Twins and maternal smoking: ordeals for the fetal origins hypothesis: a cohort study. BMJ. 1999;318(7188):897–900.
Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002;31(2):413–9.
Maconochie N, Doyle P, Prior S, Simmons R. Risk factors for the first trimester miscarriage—results from a UK-population-based case-control study. Int J Obstet Gynaecol. 2007;1114(2):170–86.
Burd L, Roberts D, Olson M, Odendaal H. Ethanol and the placenta: a review. J Matern-Fetal Neonat Med. 2007;20(5):361–75.
Barr HM, Bookstein FL, O’Malley KD, Connor PD, Huggins JE, Streissguth AP. Binge drinking during pregnancy as a predictor of psychiatric disorders on the structured clinical interview for DSM-IV in young adult offspring. Am J Psyc. 2006;163(6):1061–5.
Lazzaroni F, Bonassi S, Magnani M, Calvi A, Repetto E, Serra F, et al. Moderate maternal drinking and outcome of pregnancy. Eur J Epidemiol. 1993;9(6):599–606.
Little RE, Wendt JK. The effects of maternal drinking in the reproductive period: an epidemiologic review. J Subst Abuse. 1991;3(2):187–204.
O’Leary CM, Nassar N, Kurinczuk JJ, Bower C. The effect of maternal alcohol consumption on fetal growth and preterm birth. Int J Obstet Gynaecol. 2009;116(3):390–400.
Warren KR, Foudin LL. Alcohol-related birth defects—the past, present, and future. Alcohol Res Health. 2001;25(3):153–8.
Chiriboga CA. Fetal alcohol and drug effects. Neurologist. 2003;9(6):267–79.
Sokol RJ, Delaney-Black V, Nordstrom B. Fetal alcohol spectrum disorder. J Am Med Assoc. 2003;290(22):2996–9.
Henderson J, Gray R, Brocklehurst P. Systematic review of effects of low-moderate prenatal alcohol exposure on pregnancy outcome. Int J Obstet Gynaecol. 2007;114(3):243–52.
Henderson J, Kesmodel U, Nordstrom B. Systematic review of the fetal effects of prenatal binge-drinking. J Epidemiol Community Health. 2007;61(12):1069–73.
Hayatbakhsh MR, Kingsbury AM, Flenady V, Gilshenan KS, Hutchinson DM, Najman JM. Illicit drug use before and during pregnancy at a tertiary maternity. Drug Alcohol Rev. 2010;30(2):181–7.
Hatch EE, Bracken MB. Effect of marihuana use in pregnancy on fetal growth. J Ethnopharmacol. 1986;20(3):986–93.
Fried PA, Watkinson B, Willan A. Marijuana use during pregnancy and decreased length of gestation. Am J Obstet Gynecol. 1984;150(1):23–7.
Hingson R, Alpert JJ, Day N, Dooling E, Kayne H, Morelock S, et al. Effects of maternal drinking and marijuana. Pediatr. 1982;70(4):539–45.
Zuckerman R, Frank DA, Hingson R, Amaro H, Levenson SM, Kayne H, et al. Effects of maternal marijuana and cocaine use on fetal growth. Int J Gynecol Obstet. 1989;30(3):289–90.
Vagero D, Koupilova I, Leon DA, Lithell UB. Social determinants of birthweight, ponderal index and gestational age in Sweden in the 1920s and the 1980s. Acta Paediatr. 1999;88(4):445–53.
Collins J, David R, Symons R, Handler A, Wall S, Andes S. African-American mothers’ perception of their residential environment, stressful life events, and very low birthweight. Epidemiol. 1998;9(3):286–9.
Fang J, Madhavan S, Alderman M. Low birth weight: race and maternal nativity—impact of community income. Pediatr. 1999;103(1):1–6.
O’Campo P, Xu X, Wang M-C, Caughy M. Neighborhood risk factors for low birthweight in Baltimore: a multilevel analysis. Am J Pub Health. 1997;87(7):1113–8.
Roberts EM. Neighborhood social environments and the distribution of low birthweight in Chicago. Am J Pub Health. 1997;87(4):597–603.
Collins J, David R. Urban violence and African-American pregnancy outcome: an ecologic study. Ethnic Dis. 1997;7(3):184–90.
Copper R, Goldenberg R, Das A, Elder N, Swain M, Norman G, et al. The Preterm Prediction Study: maternal stress is associated with spontaneous preterm birth at less than thirty five weeks’ gestation. Am J Obstet Gynecol. 1996;175(5):1286–92.
Hickey CA, Cliver SP, Mulvihill FX, McNeal SF, Hoffman HJ, Goldenberg RL. Employment-related stress and preterm delivery: a contextual examination. Pub Health Rep. 1995;110(4):410–8.
Hoffman S, Hatch M. Stress, social support and pregnancy outcome: a reassessment based on recent research. Paediatr Perinat Epidemiol. 1996;10(4):380–405.
Sandman CA, Wadhwa PD, Chicz-DeMet A, Dunkel-Schetter C, Porto M. Maternal stress, HPA activity, and fetal/infant outcome. Ann NY Acad Sci. 1997;814(1):266–75.
Wadhwa P, Dunkel-Schetter C, Shicz-DeMet A, Porto M, Sandman C. Prenatal psychosocial factors and the neuroendocrine axis in human pregnancy. Psychosom Med. 1996;58(5):432–46.
LeClere FB, Wilson JB. Smoking behaviour of recent mothers, 18–44 years of age, before and after pregnancy: United States, 1990. Adv Data. 1997;288:1–11.
Wakefield M, Gillies P, Graham H, Madeley R, Symonds M. Characteristics associated with smoking cessation during pregnancy among working class women. Addiction. 1993;88(10):1423–30.
Walsh RA. Effects of maternal smoking on adverse pregnancy outcomes: examination of the criteria of causation. Hum Biol. 1994;66(6):1059–92.
Hattersley AT, Tooke JE. The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet. 1999;353(9166):1789–92.
Knight B, Shields BM, Turner M, Powell RJ, Yajnik CS, Hattersley AT. Evidence of genetic regulation of fetal longitudinal growth. Early Hum Dev. 2005;81(10):823–31.
Tower C, Baker P. The genetics of fetal growth restriction: implications for management. Rev Gynaecol Prac. 2006;6(1–2):99–105.
Guillaume M, Lapidus L, Beckers F, Lambert A, Björntorp P. Familial trends of obesity through three generations. Int J Obes Relat Metab Disord. 1995;19(3):5–9.
Okun N, Verma A, Mitchell BF, Flowerdew G. Relative importance of maternal constitutional factors and glucose intolerance of pregnancy in the development of newborn macrosomia. J Matern-Fetal Med. 1997;6(5):285–90.
Magnus P, Gjessing HK, Skrondal A, Skjaerven R. Paternal contribution to birth weight. J Epidemiol Community Health. 2001;55(12):873–7.
Skjaerven R, Wilcox AJ, Oyen N, Magnus P. Mothers’ birth weight and survival of their offspring. BMJ (Res C editor). 1997;314(7091):1376–80.
Preece MA, Moore GE. Genomic imprinting, uniparental disomy and foetal growth. Trends Endocrinol Metab. 2000;11(7):270–5.
Odent M. New reasons and new ways to study birth physiology. Int J Gynecol Obstet. 2001;75(1):39–45.
Bovbjerg ML, Siega-Riz AM. Exercise during pregnancy and cesarean delivery: north Carolina PRAMS, 2004–2005. Birth. 2009;36(3):200–7.
Chu SY, Bachman DJ, Callaghan WM, Whitlock EP, Dietz PM, Berg CJ, et al. Association between obesity during pregnancy and increased use of health care. N Engl J Med. 2008;3358(14):1444–53.
Bailit JL, Love TE, Mercer B. Rising caesarean rates: are patients sicker? Am J Obstet Gynecol. 2004;191(3):800–3.
Declercq E, Meacker F, Macdorman M. Maternal risk profiles and the primary cesarean rate in the United States, 1991–2002. Am J Pub Health. 2006;96(5):867–72.
Kabir AA, Steinmann WC, Myers L, Khan MM, Herrera EA, Yu S, et al. Unnecessary delivery in Louisiana: an analysis of birth certificate data. Am J Obstet Gynaecol. 2004;190(1):10–9.
Baicker K, Buckles KS, Chandra A. Geographic variation in the appropriate use of caesarean delivery. Health Aff. 2006;25(5):w355–67.
Shearer EL. Cesarean section: medical benefits and costs. Soc Sci Med. 1993;37(10):1223–31.
Melzer K, Schutz Y, Soehnchen N, Othenin-Girard V, Martinez de Tejada B, Irion O, et al. Effects of recommended levels of physical activity on pregnancy outcomes. Am J Obstet Gynecol. 2010;202(3):226.e1–6.
Beckmann CR, Beckman CA. Effect of a structured antepartum exercise program on pregnancy and labor outcome in primiparas. J Reprod Med. 1990;35(7):704–9.
Valgesoo T, Linkberg R. Effect of different physical exercises on pregnancy outcome. Acta Med Baltic. 1997;4(1):101–6.
Ghodsi Z, Asltoghiri M, Hajiloomohajerani M. Exercise and pregnancy: duration of labor stages and perineal tear rates. Proc Soc Behav Sci. 2012;(31):441–5.
Wong SC, Mkenzie DC. Cardiorespiratory fitness during pregnancy and its effect on outcome. Int J Sport Med. 1987;8(2):79–83.
Baciuk EP, Pereira RI, Cecatti JG, Braga AF, Cavalcante SR. Water aerobics in pregnancy: cardiovascular response, labor and neonatal outcomes. Reprod Health. 2008;21(5):10–21.
Salvesen KL, Mørkved S. Randomised controlled trial of pelvic floor muscle training during pregnancy. BMJ (Res C editor). 2004;329(7462):378–80.
Guszkowska M. Physical activity in relation to affetive states and labor anxiety in pregnant women. Med Sport. 2011;15(3):114–9.
Sayer AA, Cooper C. Fetal programming of body composition and musculoskeletal development. Early Hum Dev. 2005;81(9):735–44.
Barbet JP, Thornell LE, Butler-Browne GS. Immunocytochemical characterisation of two generations of fibres during the development of the human quadriceps muscle. Mech Dev. 1991;35(1):3–11.
Brook CG. Evidence for a sensitive period in adipose-cell replication in man. Lancet. 1972;2(7778):624–7.
McCance RA, Widdowson EM. The determinants of growth and form. P Roy Soc Lond. 1974;185(1078):1–17.
Law CM, Barker DJP, Osmond C, Fall CHD, Simmonds SJ. Early growth and abdominal fatness in adult life. J Epidemiol Community Health. 1992;46(3):184–6.
Rogers I. The influence of birthweight and intrauterine environment on adiposity and fat distribution in later life. Int J Obes Rel Metab Dis. 2003;27(7):755–77.
Silverman BL, Rizzo T, Green OC, Cho NH, Winter RJ, Ogata ES, et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes. 1991;40(Suppl 2):121–5.
Fall CHD, Osmond C, Barker DJP, Clark PM, Hales CN, Stirling Y, et al. Fetal and infant growth and cardiovascular risk factors in women. BMJ. 1995;310(6977):428–32.
Gale CR, Martyn CN, Kellingray S, Eastell R, Cooper C. Intrauterine programming of adult body composition. J Clin Endocrinol Metab. 2001;86(1):267–72.
Parsons TJ, Power C, Logan S, Summerbell CD. Childhood predictors of adult obesity: a systematic review. Int J Obes Relat Metabc Dis. 1999;23(8):1–107.
Parsons TJ, Power C, Manor O. Fetal and early life growth and body mass index from birth to early adulthood in 1958. British cohort: longitudinal study. BMJ. 2001;323(7325):1331–5.
Rich-Edwards JW, Stampfer MJ, Manson JE, Rosner B, HanKinon SE, Colditz GA, et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ. 1997;315(7105):396–400.
Sørenson HT, Sabroe S, Rothman KJ, Gillman M, Fischer P, Sørensen TIA. Relation between weight and length at birth and body mass index in young adulthood. BMJ (Res C editor). 1997;315(7116):1137.
Loos RJ, Beunen G, Fagard R, Derom C, Vlietinck R. Birth weight and body composition in young adult men—a prospective twin study. Int J Obes Relat Metab Disord. 2001;25(10):1537–45.
Siega-Riz AM, Viswanathan M, Moos MK, Deierlein A, Mumford S, Knaack J, et al. A systematic review of outcomes of maternal weight gain according to the Institute of Medicine recommendations: birthweight, fetal growth, and postpartum weight retention. Am J Obstet Gynecol. 2009;201(4):339.e1–14.
Rooney BL, Schauberger CW. Excess pregnancy weight gain and long-term obesity: one decade later. Obstet Gynecol. 2002;100(2):245–52.
Cedergren M. Effects of gestational weight gain and body mass index on obstetric outcome in Sweden. Int J Gynecol Obstet. 2006;93(3):269–74.
Devine CM, Bove CF, Olson CM. Continuity and change in women’s weight orientations and lifestyle patterns and the postpartum period: the influence of life course trajectories and transitional events. Soc Sci Med. 2000;50(4):567–82.
American Pregnancy Association [Internet]. Eating for two when over/or under weight. At what rate should I gain weight during my pregnancy? [updated 2014 Jun; cited 2013 Jan 22]. 2008. Promoting Pregnancy Wellness; [about 8 screens]. http://americanpregnancy.org/pregnancyhealth/eatingfortwo.html.
Azziz R, Woods KS, Reyna R, Key TJ, Knochenhauer ES, Yildiz BO. The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab. 2004;89(6):2745–49.
March WA, Moore VM, Willson KJ, Phillips DI, Norman RJ, Davies MJ. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod. 2010;25(2):544–51.
Teede HJ, Hutchison SK, Zoungas S. The management of insulin resistance in polycystic ovary syndrome. Trends Endocrinol Metab. 2007;18(7):273–9.
Lord J, Thomas R, Fox B, Acharya U, Wilkin T. The central issue? Visceral fat mass is a good marker of insulin resistance and metabolic disturbance in women with polycystic ovary syndrome. Brit J Obstet Gynaecol. 2006;113(10):1203–9.
Harrison CL, Lombard CB, Moron LJ, Teede HJ. Exercise therapy in polycystic ovary syndrome: systemic review. Hum Reprod Update. 2011;17(2):171–83.
De Souza MJ, Toombs RJ, Scheid JL, O'Donnell E, West SL, Williams NI. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod. 2010;25(2):491–503.
Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, Gupta N, Herzog DB, Klibanski A, Misra M. Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics. 2008;121(6):1127–36.
De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod Update. 2004;10:433–48.
Gudmundsdottir SL, Flanders WD, Augestad LB. Physical activity and fertility in women: the North-Trøndelag health study. Hum Reprod. 2009;24(12):3196–204.
Olive DL. Exercise and fertility: an update. Curr Opin Obstet Gynecol. 2010;22(4):259–63.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Science+Business Media New York
About this chapter
Cite this chapter
Moss, S., van Oort, A., Schutz, Y. (2016). Physical Activity and Pregnancy. In: Vaamonde, D., du Plessis, S., Agarwal, A. (eds) Exercise and Human Reproduction. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3402-7_16
Download citation
DOI: https://doi.org/10.1007/978-1-4939-3402-7_16
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4939-3400-3
Online ISBN: 978-1-4939-3402-7
eBook Packages: MedicineMedicine (R0)