Introduction

Exercise during pregnancy has become more popular during the last 10 years than it had previously (Brown, 2002; Mudd et al, 2009). As a result, the intensity and duration of physical activity (PA) performed by women with uncomplicated pregnancies is now arguably greater. The current guidelines from the American College of Obstetricians Gynaecologists (ACOG) encourage women to exercise without restriction for 30min on all or most days of the week (as per the population general), although no specific upper limits of intensity, duration and frequency are specified. As a result, most recommendations err on the side of moderate intensity for uncomplicated pregnancies. The type of exercise able to be performed safely does not have any restriction according to ACOG (2002), although there remains ambiguity over whether or not weight bearing activity is safe, particularly amongst less informed / educated populations (Mudd et al, 2009).

Therefore the aim of this review is to search the literature for contraindications / precautions for exercise during pregnancy, briefly review the maternal changes that occur in response to pregnancy and training whilst pregnant, and most importantly, investigate the efficacy and safety of the developing foetal-placental unit during moderate and vigorous PA.

Methods

A literature review using the Science Direct database was performed using the terms ‘pregnancy’ (title) and exercise (abstract, title, keywords), for articles published in the last 10 years. Additional articles, including older papers were sourced from the reference lists of selected studies. Three select websites were used also.

Results

Contraindications & Precautions: ACOG (2002) lists the following as absolute contraindications to aerobic exercise:

• Hemodynamically significant heart disease
• Restrictive lung disease
• Incompetent cervix
• Multiple gestation
• Premature labour in present pregnancy
• Ruptured membranes
• Pre-eclampsia / pregnancy induced hypertension
• Persistent second or third trimester bleeding
• Placenta previa

It may be that morbidity limits physical activity yet does not contraindicate altogether. For example, ‘growth retardation’, is cited by Sports Medicine Australia (2009), as a condition that they would advise against PA. Ertan et al (2004) investigated the effect of stationary bike exercise in the third trimester and doppler flow results of the foetal-placental unit in pregnancies complicated by intrauterine growth retardation (IUGR). The authors concluded that exercise does not significantly alter uterine and umbilical perfusion in pregnancies with IUGR. Bergmann et al (2004) speculates that weight bearing exercise during pregnancy may even have clinical value in such cases at risk for anomalous foetal-placental growth due to its positive influence on growth of the foetal-placental unit. Therefore, all women who fall pregnant, particularly those who posses a medical complication(s), are advised to seek individualised medical advice regarding participation in exercise.

If the following signs or symptoms appear during or after exercise, stop and contact your doctor immediately: uterine contractions, vaginal bleeding; amniotic fluid leakage; shortness of breath; decreased foetal movements; chest pain; calf pain;

palpitations; sudden swelling of the ankles, hands or face; back or pelvic pain or cramping in lower abdomen; high heart rate; dizziness; headache; nausea; muscle weakness; insufficient weight gain (SMA, 2009 & Better Health, 2009).

Considerations for Mother: For the mother, potential adverse outcomes of exercise in pregnancy are few (Lumbers et al, 2002). Some select considerations and their rationale include the following:

• Avoid supine positioning after the 14^th week. This may impede venous flow back to the heart (SMA, 2009). Exercising whilst lying on one side is safe.
• Avoid sudden positional and directional changes whilst exercising because of the risk of a fall due to an anterior shift in centre of gravity (SMA, 2009).
• Blood pressure becomes lower due to increased vasculature and the potential for a postural drop is increased (SMA, 2009), so therefore avoid exercises that involve getting up quickly off the ground such as burpees.
• Flexibility is increased due to increased secretion of the hormone relaxin. Stretch slow, avoiding bouncing movements. The sacroiliac joint and pubic symphysis appears most at risk of overstretching (Better health, 2009).
• Pelvic floor muscles become weakened by the weight of the uterus, resulting potentially in incontinence and prolapsed uterus. Pelvic floor exercises are very important during pregnancy to prevent these possible outcomes. It is suggested to contract the pelvic floor muscles for 10 seconds at a time, 3-6 times a day, lying, sitting or standing (Better health, 2009).

Benefits to Mother:

• Decreased labour duration + improved ability to withstand the physical demands of labour
• Decreased number of complications during labour
• Helps in reduction of excess maternal weight and post partum weight
• Decreased number of caesareans
• Improved posture
• Better sleep + management of insomnia

(SMA, 2009)

Risks to the Foetus:

Hyperthermia: The developing foetus has a higher temperature (0.5 degrees) than maternal, thus there is a gradient for heat transfer. Therefore, if maternal heat production is high and heat dissipation from the mother is slow (i.e. exercising in a hot, humid environment), then it is possible for the foetal-maternal heat gradient to be reversed (Lumbers et al, 2002). Sustained core temperature is associated with a slightly increased risk of congenital malformation (i.e. >39 degrees), however there is no evidence to suggest that transient spikes of core temperature causes foetal malformation. Core temperature does not increase though greater than 1.5 degrees during moderate submax exercise (Lumbers et al, 2002). Additionally, Brown (2002) states that there are compensatory mechanisms in humans to offset the effects of raised temperature such as an increase in minute ventilation and skin blood flow which help to dissipate heat during exercise. It is advised however, to wear appropriate (layers) of clothing so that layer(s) can be removed as dictated by the environment, exercise intensity and duration, and to remain well hydrated (Better health, 2009).

Risk of physical injury to the foetus: Sports Medicine Australia (2009) has developed guidelines for sports during pregnancy based on the risk of direct trauma. Non contact sports such as swimming, walking and jogging are safe right throughout pregnancy. Minimal contact sports such as racket sports and netball are safe during the first trimester and possibly the second. Contact and collision sports such as soccer and basketball are deemed safe during the first trimester only. Additional activities that SMA (2009) advises against due to risk of abdominal trauma include trampoline, gymnastics, parachuting, water skiing, and martial arts. Scuba diving is contraindicated due to the potential adverse effects of hyperbaric pressure (Clapp, 2003).

Effects of exercise on foetal growth: The maintenance and supply of the large foetal and placental mass is greatest during the third trimester, so therefore the effects of exercise are greatest during this time (Lumbers et al, 2002). During exercise, maternal cardiac output is redistributed away from the utero-placental unit to the skin and exercising muscles. This is hypothesised to compromise foetal oxygen and metabolic supply and removal of waste products, although there is limited evidence to suggest that this is the case (Lumbers et al, 2002). Clapp (2003) explains that the chronic effects of exercise such as increased foetal and maternal plasma volume, placental volume and intervillous space blood volume outweigh the acute effects of a reduction of oxygen and nutrient delivery to the foetus, resulting in a net increase in foetal growth and size at birth (given that exercise is reduced into the third trimester). Additionally, compensatory changes in placental oxygen extraction will prevent impairment of supply of essential nutrients and oxygen to the foetus (Brown, 2002).

Brown (2002) reports, that there is accumulating evidence to suggest that participation in moderate exercise throughout pregnancy may enhance birth weight, while more intense exercise maintained for longer into term may result in lighter babies. This was also demonstrated in studies by Clapp (2002 & 2003). Babies of mothers who continued to exercise vigorously into the third trimester were of a lighter weight compared to those who continued with a moderate intensity program through full term or those who ceased altogether after the second trimester. Interestingly, the decrease in weight was fat mass not lean tissue. The significance of this is unknown, although Clapp reported improved neurobehavioral outcomes in five day old infants whose mothers had exercised vigorously throughout their full term versus controls (1999), and also at five years old (1996).

A study by Bergmann et al (2004) also demonstrated that regular weight bearing activity during pregnancy stimulates placental growth, even whilst controlling for nutritional variables. This study showed significant changes in 11 subjects versus a control group for indices of cell proliferation. The authors therefore concluded that these findings may have implications for the prevention or treatment of pregnancies at risk of anomalous foetal-placental growth, specifically those with a history of growth

restriction or those with clinical evidence of poor placentation. Similarly, in a study comparing a training group of women using light resistance exercises versus non-exercising overweight controls, it was found that maternal body weight was positively and significantly associated with birth weight and length of their babies in the control group but not the training group. Gestational weight gain was mean 1300g greater in the non-exercising group which was above recommendations for gestational weight gain (Institute of Medicine, 1990) and is associated with multiple adverse newborn outcomes. Four babies of the non exercising group were over 4000g (macrosomnia). These children are more likely to become obese as children and as adults. Therefore, exercise during pregnancy may counteract the negative impact that excess maternal bodyweight before pregnancy has on the newborn’s birth size (Barakat et al, 2009).

Risk of premature birth: Pre-term birth (defined as delivery < 37weeks) is the leading cause of peri natal mortality (in North America and Europe) and a major predictor of neonatal and infant morbidity (Everson et al, 2002). Vigorous exercise has long been perceived as potentially unsafe for the developing foetus (Mudd et al, 2009). Everson et al (2002) speculates that vigorous exercise could increase the risk of preterm birth via triggering of uterine contractions as a result of a chain of unfavourable biological processes. Her subsequent study however, found that of women who participated in vigorous leisure time PA, the incidence of preterm delivery, versus less intense or sedentary controls, was less in the first trimester and even less of a risk during the second trimester. Risk was unaltered when taking duration of activity into account.

Duncombe (2006) examined the effects of intense exercise on birth weight and gestational age in 148 recreational exercisers. Although four women in the study gave birth to pre-term, low birth weight infants, only two exercised into the second trimester at all, therefore it was concluded that exercise was not a contributing factor, and additionally, it was noted that other risk factors such as maternal age, socioeconomic status, diet and obstetric complications were not accounted for. Similarly, Heggard et al (2008) investigated the relationship between presence and duration of vigorous activity and pre-term delivery. Pregnant women who competed in sport versus no sport and women who engaged in moderate to heavy leisure time

PA versus sedentary women both showed a significantly reduced risk of pre-term delivery. The authors concluded that there existed a strong association between sedentary lifestyle and pre-term delivery.

Mode of Exercise: Weight Bearing or Non Weight Bearing Exercise?

It is implied in some sources that weight bearing exercise such as running has an adverse effect on the developing foetus, although no specific outcomes have been targeted in studies and therefore no significance has been established. A retrospective study of all Danish pregnancies over a six year period by Madsen et al (2007), found when compared to non-exercisers and swimmers, weight bearing , high impact exercise was associated with a higher risk of miscarriage (foetal death <22 weeks) for the same amount of time (75-269 min per week). The number of subjects in this study was 92671, giving it good power, although the association pertained to the first 18 weeks of pregnancy only. The authors also warn though that part of the results may be explained by methodological bias, and to interpret the results with caution. Duncombe et al (2006), in opposition to a previous study using the same training variables, found no reduction in birth weight in vigorous exercisers. The only difference was that the Duncombe study used walking and cycling whereas the previous study included running and aerobics. Brown (2002) mentions that non-weight bearing activities such as cycling and swimming are beneficial late in term simply because performance will be maintained more efficiently as subjective effort becomes harder. There is little support aside from the aforementioned.

Clapp (2002) demonstrated increased birth size versus controls when using the treadmill exclusively throughout term, although growth decreased when exercising continued into the third trimester. Clapp (2003) also found that relatively strenuous swimming and cycling programs had no effect on size at birth, whilst beginning a moderate weight bearing regimen early in pregnancy resulted in increased mid trimester placental growth, placental volume at term and multiple indices of placental function by 20-25%. Additionally, increases in weight at birth were of lean tissue not fat. Bergmann’s findings relating to positive cell proliferation and placental component volume (2004) were underpinned by regular running throughout the full

term. Other benefits from weight bearing activity include a decrease in tumor necrosis factor, a naturally occurring protein produced in response to toxic substances, that is increased during pregnancy (Clapp et al, 2000), and a blunting effect of the acute response of blood flow redistribution away from splanchnic and uterine circulations, resulting from regular treadmill exercise (Clapp et al,2000).

Resistance training is also a form of weight bearing activity. Barakat et al (2009) investigated the effects of a program consisting of light resistance exercises using dumbbells, barbells and resistance bands. No significant differences were detected between the exercise and control groups in the study, although the authors state that the potential benefits from resistance exercise include decreased risk of insulin dependence in overweight women with gestational diabetes, improved posture, prevention of back pain, strengthening of the pelvic floor and prevention of diastasis recti (separation of the abdominal muscles at the midline). They also add that light resistance exercises may be better tolerated than aerobic training owing to lower cardiovascular stress and caloric expenditure (Barakat et al, 2009).

Table 1

Study	n	F	I	T	T	Stage of pregnancy	Sig. outcomes
Barakat (2009)	142	3/7 (3 times per wk)	< 80% age predicted max	36min	Free weights, resistance bands	Wks 12-38	(re: delivery type)= no ↑in pre-term births
Barakat (2009)	As above	As above	As above	As above	As above	As above	(re: growth) =unhealthily large infants born to controls
Bergmann (2004)	22	4/7	55-65% Vo2max	40-60min	Running	Through-out	↑ placental growth
Clapp (1996)	40	–	‘vigorous’	–	–	Through-out	Superior neurodevelopmental scores + less fat at 5yrs old.
Clapp (1999)	65	‘reg-ular’	–	–	–	Through-out	Superior neuro-developmental behaviour at 5days old
Clapp (2000)	12	‘reg-ular’	55%max	20min	Treadmill	Through-out	(Chronic) blunting of (acute) blood redistribution away from uterus
Clapp (2000)	–	≥4/7	–	–	‘weight bearing’	3 groups   (various)	Tumor necrosis factor ↓ in exercising groups
Clapp (2002)	75	‘mod-erate’	–	–	‘weight bearing’	3 groups   (various)	↑ fat free mass stopping after 2ndtrimester. ↓ fat mass only & weight when til end of 3rdtrimester.
Clapp (2003)	46	3-5/7	‘mod’   erate’	–	‘weight   bearing’	Through-   out	↑mid trimester   placental growth rate & function
Duncombe (2006)	148	1.≥3/7   2.≥3/7	1.≥50% max HR   2. >140bpm	1.≥30min   2.≥15min	1.Swim-ming, cycling, aerobics, running & walking   2.as above + circuit training, weights, martial arts & dance	Through-out	1 & 2: no asso-   ciation with ↓birth weight or ↑preterm infants. No diff. b/w groups
Ertan (2004)	10	1 bout	–	13min	Stationary   bike	During 3rd   trimester	Uterine &   umbilical perfusion unaltered with growth- retardation
Everson (2002)	1699   (retro spec-tive)	–	All intensities.Vigorous= ≥6METS	3hrs /   week	–	Until 29   weeks	↓risk of preterm delivery during 1sttrimester; ↓↓ risk during 2nd   trimester
Heggard (2008)	5749   (retro spec- tive)	–	All   intensities	0->3 hrs/ week	Light & moderate-   heavy leisure time PA; competet-ive sports	Until 16   weeks	Mod-to-heavy   Leisure time PA= sig ↓ risk of pre-term; >1 sport = sig↓ risk of pre-term v no sport
Lokey (1991)	2314   (meta analy-sis)	3/7	≤144bpm /   81%max HR	43min	Jogging;   bicycling; swimming; weights	Throu-   out	No adverse effects to mother or foetus
Madsen (2007)	92,   671 (retro spect-ive)	–	All   intensities	45-   >420 min/ week	‘high im-   pact’; ‘low im- pact’; gym based; bicycling; horseback riding; swimming	Until 22   weeks	All modes except swimming = ↑risk mis-   carriage (non sig) < 19wks. Swimming= ↓ risk. >45mins/wk =↑risk mis- carriage (non sig) < 19wks

Discussion

The 2002 ACOG guidelines for PA during pregnancy indicate that women with normal pregnancies can engage in exercise with almost no restriction without compromising foetal growth and development or complicating pregnancy, labour or delivery. The research conducted in this literature review supports this recommendation wholeheartedly. In further support of the safety of moderate-to-intense PA during pregnancy, Lokey (1991) and Duncombe (2006) demonstrate no adverse effects to the foetus whilst exercising at some of the most vigorous levels available in the literature. Lokey (1991) tested 2314 subjects working at a heart rate of up to 144bpm for 43 mins, 3 times per week using a variety of modes including jogging and weight training. The Duncombe study (2006), although testing just 34 subjects whilst cycling or vigorous walking, reached an intensity of 154bpm for an average of 22mins, 4.7 sessions per week.

In light of the above recommendations and data, concerning the uncomplicated pregnancy, it seems safe to endorse PA of any mode (with the exception of the stated contraindicated activities), for up to an hour on all or most days of the week, working at a maximal intensity that corresponds to 14-16 on the Borg scale of ratings of perceived exertion. This should be the case for the first two trimesters. The third trimester it is suggested to decrease the intensity and duration of exercise, as it appears that it is during this time that decrements in foetal growth are likely to occur, albeit via a reduction of fat mass not lean tissue. It has been shown that starting a moderate intensity program (Borg 12-14) in previously sedentary women is safe and

beneficial, as is maintaining a more vigorous program in the already active woman (Barakat et al, 2009; Bergmann et al 2004; Clapp, 1996, 1999, 2000, 2002 & 2003; Duncombe et al, 2006; Everson et al, 2002; Heggard et al, 2008; Lokey et al, 1991). It would be wise however not to commence a vigorous program of exercise if not already conditioned.

A major limitation of this study is not addressing the topic of nutrition. It was not within the scope of this literature review to do so, yet it is recognised that adequate nutrition for mother and foetus is essential to facilitate moderate-to-vigorous training, and assessment of intake via a dietician would be part of the preparation of commencement or continuation of exercise at the beginning and throughout pregnancy. Another limitation of studies included here is the possibility of self selection by participants. Generally, if not randomised, the subjects were healthy, active women without obstetric complication. This may alter the results of research favourably, however it was women with uncomplicated pregnancies that this review intended to focus on. A limitation placed on women is the lack of information and / or guidance regarding how much exercise they should undertake when pregnant.

Very few physicians counsel pregnant women on PA and much consumer based literature offers outdated advice (Mudd et al, 2009). As a result, perceptions of women remain guarded and conservative regarding what exercise is safe to perform, potentially missing out on the benefits regular PA during pregnancy offers mother and baby.

There are enough barriers to women’s continued participation in sport at this life stage without adding ones that are not based on scientific evidence. In the interests of public health, anything that encourages the continued participation in sport during pregnancy and after childbirth should be supported (Brown, 2002).

Training pre and post pregnancy is covered in the Certificate III in Fitness, Certificate IV in Fitness and Diploma of Fitness.

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