Best Practice & Research Clinical Obstetrics and Gynaecology 28 (2014) 159–168

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Sleep disorders in perinatal women Sabra M. Abbott, MD, PhD, Instructor *, Hrayr Attarian, MD, Associate Professor, Phyllis C. Zee, MD, PhD, Benjamin and Virginia T. Boshes Professor of Neurology Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA

Keywords: sleep obstructive sleep apnea restless legs syndrome insomnia narcolepsy circadian rhythm sleep disorders

Insufficient sleep is common in the general population, and can result from environmental and psychosocial factors, medical and psychiatric disorders, and sleep disorders, such as insomnia, circadian rhythm disorders, sleep apnoea and restless legs. Women are particularly at risk for sleep disorders, and complaints of sleep disturbance are more prevalent among women than men across the life span. During the perinatal period, many common sleep disorders, such as obstructive sleep apnoea or restless legs may be exacerbated, or in the case of insomnia or narcolepsy, treatment options may change. In addition, the role of circadian rhythms in fertility and perinatal health is just beginning to be appreciated. In this chapter, we provide an overview of the current knowledge of the unique aspects of diagnosis and treatment of sleep disorders during the perinatal period. Ó 2013 Elsevier Ltd. All rights reserved.

Introduction Sleep is an essential biological function in animals and humans. Sleep and wake cycles are governed by two major neural mechanisms: a sleep homeostatic process, which builds up as a function of time awake, and dissipates during sleep, and the daily circadian rhythm of sleep and wake propensity. Gonadotropic and sex hormones can also influence sleep quality and the risk for sleep disorders, such as insomnia and sleep-disordered breathing. Thus, a woman’s ability to sleep is influenced by hormonal and physiologic changes, particularly during pregnancy and the postpartum period. It is

* Corresponding author. Tel.: þ1 312 908 8549; Fax: þ1 312 695 5747. E-mail address: [email protected] (S.M. Abbott). 1521-6934/$ – see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.bpobgyn.2013.09.003

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estimated that 40% of pregnant women and 30% of postmenopausal women report only getting a good night’s sleep a few nights a month or less [1]. Mounting evidence shows that adequate sleep and wake function is imperative for health, performance, and overall quality of life. Laboratory studies have shown that even short-term partial sleep restriction adversely affects mood, appetite regulating hormones, insulin sensitivity, inflammation and autonomic function [2,3]; data from epidemiologic studies have shown an association between short sleep duration and increased risk of obesity, diabetes, hypertension, and mortality [4–6]. In addition, specific sleep disorders, such as sleep-disordered breathing, insomnia, circadian rhythm disorders, and restless legs syndrome (RLS) have been linked with higher risk of developing depression, cardiovascular, and metabolic diseases [7–9]. In light of these findings and the high prevalence of sleep disturbances in the perinatal period, it is important for obstetricians and gynaecologists to enquire about sleep quality in general, and identify and treat sleep disorders in the perinatal period (Table 1). Sleep is potentially a modifiable risk factor that can improve the health of both mother and infant. Obstructive sleep apnoea and pregnancy Pregnancy is a state of significant, albeit temporary, changes in respiratory physiology. Some of these alterations are conducive to the development of sleep-disordered breathing, whereas others are protective. First, obvious anatomical alterations occur as a result of gravid uterus, shifting of intra-abdominal organs, elevation of diaphragm, and an increase in intra-abdominal pressure. Second, both oestrogen and progesterone change sleep microstructure and basic respiratory physiology. Functional residual capacity gradually decreases by about 20% in the latter months of pregnancy, leading to an increase in minute ventilation and tidal volume, resulting in higher PaO2 and lower PaCO2 pressures [10]. This creates an O2 and CO2 differential gradient to shunt O2 to the fetus and allow CO2 excretion. This shunting leads to hypoxaemia and a drop in pulmonary oxygen stores [11]. Both of these phenomena exacerbate obstructive sleep apnoea (OSA). A decline also occurs in nocturnal oxygen saturation in normal late pregnancy, exacerbated by sleeping in the supine position, which may be related to upper airway collapse [12]. Finally, during pregnancy, there is a dramatic and rapid increase in weight, which can worsen preexisting OSA [13]. Rising oestrogen levels lead to upper-airway mucosal congestion and hyperaemia, leading to snoring. Up to 30% of women in their third trimester complain of nasal congestion [14], and oropharyngeal crowding increases in the third trimester compared with the first [15]. Oestrogen, however, decreases rapid eye movement sleep and progesterone increases non-rapid eye movement sleep, and OSA in young women is often worse in rapid eye movement sleep; therefore, reduction in time spent in that vulnerable state may be a protective mechanism [16]. Another potentially protective effect of progesterone is increased minute volume [17], which in itself is protective against airway occlusion. Habitual snoring increases from 4% in non-pregnant women to 25% with gestation [18]; however, the association between habitual snoring and adverse fetal outcomes in unclear. A trial of 350 pregnant

Table 1 Common sleep disorders encountered during the perinatal period: recommended diagnostic testing and treatment options. Disorder

Diagnosis

Non-pharmacologic treatment

Pharmacologic treatment

Obstructive sleep apnoea Restless legs syndrome

Polysomnogram.

Auto-continuous positive airway pressure. Exercise; massage.

None. Iron and folate.

Cognitive–behavioural therapy. Protected sleep; scheduled naps.

Diphenhydramine. None.

Regular sleep–wake schedule; bright light therapy.

None.

Insomnia Narcolepsy Shift work sleep disorder

Clinical history; ferritin (less useful in gestational restless leg syndrome). Clinical history. Polysomnogram with multiple sleep latency test. Clinical history.

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women did not show any adverse fetal outcomes with habitual pregnancy-related snoring [19]; however, two larger trials showed an association between lower birth weights and intrauterine growth retardation (IUGR) among habitual snorers after controlling for pre-pregnancy weight, age, parity, hypertension, education, and smoking [20,21]. An increase in inflammatory markers in umbilical cord blood was reported among habitual snorers [22]; however, this did not correlate with any adverse fetal outcomes [22]. Of note, the prevalence of polysomnographic-confirmed OSA among snorers has been reported to be only 11.4% [23]. Neither standardised questionnaires nor overnight oximetry measurements have high predictive value for OSA in pregnancy [24,25]. A recently developed four-variable model that includes pregestational hypertension (15 points), habitual snoring (15 points), obesity (measured by body mass index (BMI)), and age (in years) has shown the highest positive and negative predictive values. A score of 75 or more (15 þ 15 þ BMI þ age) conferred a high likelihood of OSA in pregnant women [26]. In women with OSA, IUGR in the form of both small for gestational age infants and low birth weight is the most common adverse outcome [27]. Other related complications of OSA include preterm birth, increased risk for caesarian sections, and low birth weight [27]. The most plausible mechanism for IUGR in OSA, derived from both animal data with intermittent hypoxaemia and human data in other chronic respiratory illnesses, is placental ischaemia owing to maternal hypoxaemia. Hypoxia associated with OSA and hypercarbia can lead to fetal hypoxia, increased sympathetic activation, endothelial dysfunction from oxidative stress, and fetal acidosis, resulting in impaired fetal growth [28]. A small study has shown lower Apgar scores along with IUGR, and prenatal heart rate decelerations associated with maternal hypoxaemia [29]. Obstructive sleep apnoea is also a major risk factor for pregnancy-induced hypertension, preeclampsia, and eclampsia [18,21]. Odds ratios for hypertension are 2.03 for any habitual snoring during pregnancy [21] and 2.36 with pregnancy-onset snoring [18] and 1.59 for pre-eclampsia [18]. Obstructive sleep apnoea is an independent and significant risk factor for preeclampsia and gestational hypertension, with odds ratios ranging from 1.6–7.5 [27,30,31]. The odds of gestational diabetes mellitus (GDM) also increase threefold with OSA in pregnancy [32]. A mean sleep duration of less than or equal to 7 h, daytime napping, and excessive daytime sleepiness, are all associated with high risk of GDM [32–34]. Severely curtailed sleep duration (equal or less than 4 h a night) increases the risk of GDM by 5.56 fold. The risk ratio for GDM among the lean cohort (prepregnancy BMI of less than 25 kg/m2) with snoring and short sleep was 3.23, whereas, among the overweight and obese cohort (pre-pregnancy BMI of 25 kg/m2 or more) was 9.83. When taking into consideration only habitual snoring, without factoring in sleep duration or weight, then the risk of GDM is still high, with a relative risk of 1.86. Finally, when considering weight and snoring without sleep duration, the relative risk for GDM among overweight and obese women who habitually snored was 6.9 compared with lean women who did not [35]. The potential mechanism for the development of GDM in OSA is most likely oxidative stress and sympathetic activation secondary to sleep fragmentation and intermittent hypoxaemia. Oxidative stress leads to insulin resistance and has been associated with a high risk for GDM [36]. Another mechanistic association between GDM and OSA could potentially be the pro-inflammatory lowering of adiponectin levels associated with insulin resistance [37,38]. The treatment for OSA in pregnancy is primarily continuous positive airway pressure (CPAP), preferably in an auto-titrating mode, because of the changes in weight and respiratory physiology between early and late pregnancy. Auto CPAP has the flexibility to adjust to the dynamic nature of the OSA in pregnancy. It tends to alleviate OSA and incrementally improve blood-pressure control, and may even improve fetal health [39–41]. Oral appliances are not practical because of the time needed to make and adjust them. Upper airway surgery has low efficacy and high risk in pregnancy, and OSA may resolve after delivery as weight and fluid distribution stabilise. In conclusion, pregnancy increases the risk of OSA, especially in obese women, which in turn can increases the likelihood of pregnancy-induced hypertension, GDM and IUGR. It is important to be clinically vigilant in screening pregnant women for symptoms of OSA, as routine questionnaires and overnight oximetry have low predictive values.

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Gestational restless legs syndrome Restless legs syndrome (RLS) is a movement disorder of dopaminergic dysfunction [42], characterised by primarily lower limb restlessness and dysesthesias occurring at night. Diagnosis is clinical, based on the four criteria of the international RLS study group. These include: (1) urge to move the legs, usually accompanied or caused by uncomfortable leg sensations; (2) temporary relief with movement; (3) onset or worsening of symptoms at rest or inactivity; and (4) worsening or onset of symptoms in the evening or at night [43]. Gestational RLS (gRLS) occurs in 12–26% of pregnant women, with symptoms worsening as the pregnancy progresses and improving or even resolving with delivery [44,45]. This is compared with 5– 8% in the general populations of the USA, Japan and Europe, with lower prevalence elsewhere [46]. Transient gRLS increases the risk for the subsequent development of chronic RLS fourfold, and gRLS reemerges during subsequent pregnancies in 60% of women [47]. Correlates of gRLS include family history, smoking, prior history of RLS or gRLS, and pre-pregnancy obesity [44,48]. Anaemia and ferritin levels correlated in one trial [48] but not in another, and oestrogen levels did not correlate at all with the occurrence of gRLS [44]. A clear pathophysiology of gRLS has yet to be established. Two attractive, albeit flawed hypotheses, are altered iron metabolism and hormonal changes. Low ferritin levels have been strongly associated with chronic RLS; however, in a group of pregnant women with gRLS, the overall ferritin levels were not lower than pregnant women without gRLS [44]. Furthermore, the rapid improvement of gRLS after delivery does not support this hypothesis, as iron stores take up to 3 months to replenish [49]. Fluctuations in prolactin, oestrogen and progesterone have been proposed as a cause of gRLS. Prolactin has antidopaminergic activity, and its levels rise throughout pregnancy. In breast-feeding women, prolactin continues to be secreted; however, gRLS resolves [50]. In addition, in both the general population and in pregnant women, RLS is not associated with any changes in diurnal prolactin rhythms [51], even though serum prolactin levels in RLS is closely correlated with the periodic limb movement index, the number of period limb movements per hour of sleep [52]. Exogenous oestrogen has been shown to correlate with risk of RLS in peri-menopausal women [53], but not in younger women of childbearing age [54]. The rise of oestradiol levels and their decline after delivery have been shown to correlate well with worsening and subsequent improvement in gRLS and related periodic limb movement indices [51]. Other larger studies, however, failed to find a relationship between oestradiol levels and gRLS [44]. Progesterone levels do not correlate with gRLS [51,55]. Treatment of gRLS poses significant challenges, as most medications used for RLS, and approved by the US Food and Drug Administration, have not been demonstrated to be safe for use in pregnancy. The only exceptions are pergolide and oxycodone. Pergolide is an ergot dopamine agonist and has fallen out of favor because of associated cardiac valvular fibrosis, whereas oxycodone is a high potency opiate with significant abuse risk. Current recommendations for gRLS include supplementation with iron and folate [56]. Other non-pharmacological methods of treatment include exercise, massages, infrared light exposure [57], pneumatic compression [58], intravenous magnesium [59], and hot baths. Untreated gRLS leads to severe sleep fragmentation, poor sleep quality, insomnia, and reduced quality of life. [44,48,60] Fragmented sleep, as discussed in the next section, can result in a host of peripartum complications. Insomnia and pregnancy Disrupted sleep, reduced total sleep time, and decreased sleep quality are common in pregnant women, especially in the third trimester. These complaints occur on an almost nightly basis in 52–61% of women during the last 8 weeks of pregnancy [61,62]. Moreover, they are strongly associated with both pre-existing and de-novo gestational depression [61–63]. History of smoking also predicts a higher prevalence of insomnia in late pregnancy [64]. As pregnancy progresses, an average of two to three nightly awakenings occur in the third trimester (30–45 min of wake after sleep onset), and a mean sleep duration of about 7 h per night, although some women report as little as 3–4 h of sleep. A commensurate increase in daytime napping occurs during late pregnancy [65]. Nulliparous women, and women over the age of 30 years, tend to sleep less (6 h or

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less) than their younger counterparts and those who have previously been pregnant [66]. As labour approaches, partly because of secretion of oxytocin (a wake promoting hormone) [67], insomnia generally worsens. Poor sleep quality and quantity affects the woman’s ability to tolerate and cope with labour pain [68]. Women, especially nulliparous women, have longer labours, higher chance of caesarean sections, and more spontaneous preterm deliveries if they average 6 h sleep or less compared with women who average over 7 h of nightly sleep [69,70]. Complaints of insomnia remain prevalent from delivery to 3 months postpartum, and tend to be more so among women who had undergone a caesarean section compared with those who have delivered vaginally [71]. Objective measures have shown an increase in total sleep duration by an average of 45 min in women who breast feed compared with those who bottle feed [72]. Co-bedding, however, increases maternal sleep disruptions [73]. Infant temperament also has a significant effect on maternal sleep during the first few months of life, as 20–30% of infants can become colicky [74]. Sleep loss during pregnancy is a risk factor for the subsequent development of postpartum depression (PPD), which can worsen sleep quality. Pre-partum sleep disruption and insomnia has been reported to increase the risk of PPD, with reported odds ratio as high as 7.7. Maternal sleep of less than 4 h between midnight and 6 am, and daytime naps of less than 60 min are independent risk factors for PPD [74], as is poor subjective sleep quality [75]. Treatment of pregnancy-related insomnia is primarily based on cognitive and behavioural approaches, because of the potential teratogenicity of sedative and hypnotic medications [76,77]. In summary, poor sleep quality in pregnant women, especially in the third trimester, is quite common. When coupled with short sleep duration, it can be a major risk factor for PPD, premature delivery, longer labours, and increased risk of caesarian sections. Most of these complications, in turn, affect sleep quality in the postpartum period. Narcolepsy and pregnancy Although narcolepsy is less common than sleep apnoea, insomnia, or restless legs syndrome, it is relevant to perinatal medicine because of the challenges in managing these women during pregnancy and postpartum. Narcolepsy is a sleep disorder characterised by excessive sleepiness, associated with cataplexy, sleep paralysis, and hypnagogic hallucinations [78]. Several considerations have to be taken into account when treating a pregnant woman with narcolepsy. Current treatment guidelines include the use of a daytime stimulant, such as either modafinil or an amphetamine to combat excessive daytime sleepiness, often along with either sodium oxybate or a selective serotonin reuptake inhibitor (SSRI) to treat cataplexy. None of these medications, have undergone human testing during pregnancy, and are not recommended to be used during pregnancy. In a recent review, however, no evidence was found for increased teratogenicity with the use of modafinil, sodium oxybate, methylphenidate and amphetamines, and case reports of narcoleptic women taking SSRIs during pregnancy did not show adverse outcomes [79]. Amphetamines have been associated with IUGR, and spontaneous miscarriages have been reported in women using sodium oxybate, although not at levels higher than in the general population. In a recent survey of 75 clinicians treating pregnant women with narcolepsy, most stopped narcolepsy medications at the time of conception or during pregnancy, and often reduced doses of medications during breast feeding [79]. In a large retrospective cohort study of 249 women with narcolepsy, among women who withdrew from all medications during the first trimester of pregnancy, 18.2% experienced an improvement in their symptoms, 40.1% had no change, and 40.1% had worsening of their symptoms [80]. If women are taken off their medication, non-pharmacologic options for treatment focus primarily on protecting the sleep period, so sleep is uninterrupted. In addition, brief scheduled naps during the day may also be beneficial. In addition to the treatment challenges, women with narcolepsy are at increased risk for adverse pregnancy outcomes. Women with narcolepsy had a significantly higher body mass index before pregnancy and a higher incidence of impaired glucose metabolism and anaemia during pregnancy [80]. During delivery, women with narcolepsy may develop cataplexy, which may contribute to a higher rate of emergency caesarian section [81]. In summary, narcolepsy is associated with higher BMI before pregnancy and an increased incidence of glucose intolerance during pregnancy. Treatment options during pregnancy and breast feeding are

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limited at this time; however, non-pharmacologic strategies including protected sleep at night and scheduled naps may be beneficial. Circadian rhythms and pregnancy The circadian system regulates internal timing with respect to the external environment. The primary circadian pacemaker in mammals is located in the hypothalamus, in the suprachiasmatic nucleus. The alignment of internal timing with the external environment can be disrupted owing to endogenous impairment of the circadian clock in individuals with intrinsic disorders of circadian timing, or far more commonly, owing to exogenous factors such as shift work and jet lag. With our increasing reliance on shift work, and greater exposure to artificial light during times of environmental darkness, resulting in circadian misalignment, interest in the role of circadian rhythms and their disruption on maternal health has increased. There is growing evidence that exposure to shift work is associated with increased risk of disorders ranging from cancer [82] to metabolic syndrome [83]; however, less is known about the role of circadian disruption on fertility and pregnancy. In women, the normal estrous cycle depends upon the appropriate timing of release of hormones from the anterior pituitary, with animal studies demonstrating that lesioning the suprachiasmatic nucleus disrupts this normal pattern [84], suggesting that a functioning circadian clock is important for a normal menstrual cycle. In studies looking at nurses exposed to shift work, the highest percentage of irregular menstrual cycles were seen in women working fixed night shifts [85]. Surveys comparing current and former flight attendants have found an increased risk of menstrual irregularities among the current flight attendants [86]. An association was also found in the flight attendants between menstrual irregularities and infertility. Similarly, a large multicentre European study looking at fertility found a greater incidence of sub-fecundity among women exposed to shift work [87]. These results suggest that, including a detailed history of an individual’s work and sleep schedule, should be considered an important part of the evaluation for infertility. Circadian disruption also seems to have detrimental effects during pregnancy. In animal studies, mice with a mutation in one of the genes regulating circadian rhythms have an increased risk of fetal resorption and fetal loss [88]. In genetically normal mice, exposure to repeated shifting of the environmental light dark cycle, similar to the schedule of an individual working rotating shift work, results in a significantly decreased number of term pregnancies [89]. In humans, several large cohort studies looked at pregnancy outcomes among women exposed to shift work. The National Birth Cohort in Denmark demonstrated an increased risk of small for gestational age babies in women exposed to shift work [90] and an increased risk of fetal loss among women working fixed night shifts [91]. The Lifeways cohort in Ireland also showed a trend towards lower birthweight among shift workers [92]. A meta-analysis of 17 studies found a pooled relative risk for preterm delivery of 1.16 among shift workers [93]. Additionally, during pregnancy, circadian dysfunction seems to be associated with pre-eclampsia. Normal arterial blood pressure peaks in the morning and dips at night; however, this is absent in women with pre-eclampsia [94,95]. No clear evidence, however, shows that circadian disruption from shift work or other factors increases the risk of pre-eclampsia [70]. Interestingly, in a study of 350 highrisk pregnant women, aspirin at a dose of 100 mg/day, started at 12–16 weeks gestation showed a significant reduction in blood pressure only if taken in the evening or at bedtime [96]. During labour, the circadian system also plays an important role. Spontaneous rupture of membranes occurs more often between midnight and 4 am [97], with onset of labour tending to peak around dawn and dusk, with a nadir in the middle of the day [98]. Interestingly, a randomisedcontrolled trial looking at women admitted for prostaglandin induction of labour, found that morning (8 am) inductions were less likely to require oxytocin and caesarean delivery than evening (8 pm) inductions [99]. This suggests that the appropriate timing of these interventions may improve outcomes. Finally some evidence shows that circadian disruption during pregnancy may have adverse effects on offspring. In rats, maternal exposure to shift work results in increased adiposity, impaired glucose tolerance, and insulin resistance, in offspring 12 months later [100]. Similar studies looking at the outcomes of human offspring exposed to shift work in utero are not available.

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In summary, the endogenous circadian system is important for normal pregnancy and delivery, with disruption to this system affecting fertility and pregnancy outcome; hence, it is important that work and sleep schedules are always considered when counselling women on peripartum health. Conclusion In this chapter we have outlined ways in which sleep quality and common sleep disorders can influence mental and physical health outcomes in the perinatal period, as well as how the changes in perinatal psychosocial factors and physiology can in turn increase the risk of disturbed sleep. One of the most common and often unrecognised disorders of pregnancy is OSA. When left untreated, OSA can lead to an increased risk for gestational hypertension low birth weight and gestational diabetes; however, most women can be easily treated with an auto-titrating CPAP. Pregnancy can also be associated with significant sleep fragmentation, both from restless legs syndrome and insomnia. Treatment options are limited, however. Some success has been made with using iron for RLS, and behavioural therapy for insomnia is often beneficial. Finally, given our increasing reliance on shift work, circadian disorders are an important consideration during the perinatal period. Circadian misalignment can result in decreased fertility and a possible increase in preterm delivery and fetal loss; however, data are still limited. Overall, prioritising sleep and identifying and treating common sleep disorders has the potential to improve mental and physical health outcomes in both mothers and children.

Practice points  Auto-CPAP is recommended for treating gestational OSA.  Iron is recommended for treating gRLS.  Most pharmacologic treatments for insomnia are potentially teratogenic, so management is primarily through cognitive and behavioural therapies.  Status cataplecticus during delivery is rare in women with narcolepsy, so the presence of narcolepsy alone should not be an indication for caesarian section.  Shift work status should be identified in all women, as this can affect fertility and pregnancy outcomes.

Research agenda  Adverse pregnancy outcomes associated with sleep-disordered breathing.  The effect of inadequate sleep and sleep disorders on depression during pregnancy and in the postpartum period.  The effect of treatment of sleep-disordered breathing in pregnancy on maternal–fetal outcomes.  Pathophysiology of gestational RLS.  The role of maternal circadian disruption on the health of offspring.

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