INTRODUCTION

Preeclampsia is a pregnancy complication recognized by the new onset of hypertension (HTN) and proteinuria after the 20th gestational week [1]. This syndrome is one of the most serious complications of pregnancy and a leading cause of maternal and perinatal morbidity and mortality [1]. Women with preeclampsia are at an increased risk of acute renal insufficiency, hepatic failure, cerebral edema, and hemolysis. On the fetal side, intrauterine growth restriction, oligohydramnios, and stillbirth are serious complications of preeclampsia [2].

Globally, the prevalence of preeclampsia is stimated to be about 4.6%, however, the prevalence differs between different regions [3]. According to the systematic review by Kharaghani et al. [4] the prevalence of preeclampsia in Iran increased from 4% during 1996 to 2005 to 7% during 2010 to 2013.

The triad of intravascular inflammation, endothelial dysfunction, and syncytiotrophoblast stress forms the common pathophysialogical pathway through which many risk factors with various pathological mechanisms contribute to this condition [5]. Gestational diabetes mellitus, maternal obesity, certain endocrinopathies such as hyperparathytoidism and hyperaldosteronism, fetal distress and some types of sleep disorders are important risk factors for this syndrome [5]. Considering lethal consequences of this syndrome, better recognition of its risk factors and effort to correct them are crucial.

Sleep plays an essential role in maintaining physical and mental health. The association of sleep disturbances with metabolic and cardiovascular disease has been reported in previouse studies [6]. Epidemiological cross-sectional and cohort studies have demonstrated a strong association between HTN and abnormalities in short sleep duration and poor sleep quality [7,8].

Sleep disturbances are highly prevalent during the pregnancy. In a meta-analysis of data from 11 002 pregnant women, Sedov et al. [9] showed that 45.7% of participants had poor sleep quality and sleep quality decreased further by advancing pregnancy. In other epidemiological studies, a 26.2% prevalence of short sleep duration [10], 38.2% of insomnia [11], and 15% of obstructive sleep apnea (OSA) [12] were reported in pregnant women.

Among various sleep-related abnormalities, the role of sleep breathing disorders in the development of preeclampsia is more established. In a meta-analysis by Lu et al. [13], subjective sleep-breath disorders and OSA were associated with 2.36 times and 1.74 times higher risk of pre eclampsia, respectively.

Despite the abundant evidence on the role of sleep breathing disorders in preeclampsia development, there are limited studies on the influence of other aspects of sleep (e.g., sleep quality or duration on preeclampsia). In a cohort study conducted by Williams et al. [14], pregnant women with short sleep duration in early pregnancy were about 9 times more likely to develop preeclampsia in the later months. In another cohort study by Zhu et al. [15], low sleep efficiency in early pregnancy was a risk factor for HTN development but not preeclampsia in later months. Since most other studies on the association of sleep quality with preeclampsia are cross-sectional, causality cannot be inferred from their results.

Due to the limited and inconsistent data available concerning the research topic, this study investigated the impact of sleep quality and duration in early pregnancy on the development of preeclampsia in the following months.

METHODS

Study Participants

This research was conducted by secondary analysis of Qazvin Maternal and Neonatal Metabolic Outcomes Study (QMNMS) data. QMNMS is a cohort study on 821 Iranian pregnant women in Qazvin province of Iran from September 2018 to May 2020 and from February 2021 to June 2021. Pregnant women with gestational age ≤14 weeks who received prenatal care at the obstetrics and gynecology clinic were included in the study. Inclusion criteria were age ≥18 years and gestational age ≤14 weeks based on ultrasonography or the date of the last menstrual period. Women with known depressive disorders before pregnancy, any painful chronic disease like active rheumatological disease, severe allergic rhinitis or asthma interfering with sleep quality, shift workers, not completing the Pittsburgh Sleep Quality Index (PSQI) questionnaire, miscarriage or loss to follow-up were excluded from the final analysis of the present study. The objectives and details of the study were explained to the participants individually.

Sleep Assessment

Sleep quality was assessed at the first prenatal visit (gestational age ≤14 weeks) using the PSQI questionnaire [16]. Short and long sleep durations were defined as night sleep durations less than 6 hours and more than 9 hours, respectively [17,18]. Sleep quality was categorized in two groups; groups 1: very good (PSQI score 1 to 4) or fairly good (PSQI score 5 to 9), group 2: fairly bad (PSQI score 10 to 14 ) or very bad (PSQI score ≥15) [19].

Sleep efficiency was calculated as the ratio of total sleep time at night to time in bed, and low sleep efficiency was defined as ≤85% [20]. Sleep latency was expressed as the time the participant took to fall asleep. Prolonged sleep latency was defined as sleep latency of more than 30 minutes 3 times a week or more than 60 minutes more than once a week [21,22].

For components of sleep quality without pre-defined classifications (i.e., daytime dysfunction, subjective sleep quality, and frequently using sleep medications), a score ≥2 (fairly bad or very bad) was defined as an impairment in that component.

Outcomes

According to the American College of Obstetricians and Gynecologists guideline [23], preeclampsia is defined as systolic blood pressure ≥140 mmHg or diastolic blood pressure ≥90 mmHg on two occasions 4 hours apart after 20 weeks of pregnancy in a previously normotensive woman and proteinuria ≥300 mg/24 hr urine or protein to creatinine ratio ≥0.3 or positive urine dipstick reading ≥1+ (if a quantitative method was not available). In the absence of proteinuria, preeclampsia was diagnosed as a new onset of HTN with a new onset of any of the following conditions: thrombocytopenia (thrombocyte count <100 000/µL), serum creatinine concentration of ≥1.1 mg/day, or a doubling serum creatinine concentration in the absence of other kidney disease, elevated liver transaminases to twice normal levels, pulmonary edema, and cerebral or visual symptoms.

Covariates

At the time of enrollment in the study, a structured questionnaire including information on demographic characteristics, smoking, history of chronic diseases, use of medications, and daily habits (including daytime napping) was recorded by two trained interviewers. Gestational age was calculated using the last menstrual period or ultrasound done in the first trimester. Body mass index was calculated as pre-pregnancy weight in kg per square of height in meters. Physical activity and depression scores were evaluated using Baecke and Beck Depression Inventory-II (BDI-II) questionnaires, respectively [24,25].

Statistical Analysis

The normality of continuous data was examined by the Kolmogorov-Smirnov test. Quantitative data with normal and non-normal distribution were expressed as mean±standard deviation (SD) and median (interquartile range) and were compared between preeclampsia and non-preeclampsia groups by t-test and Mann-Whitney test, respectively. Categorized data were expressed as numbers (percentages). All four graded components of sleep quality (i.e., very good, fairly good, fairly bad, very bad) were compared between preeclampsia and non-preeclampsia groups using the chi-square (χ²) test.

Logistic regression analysis was run to evaluate the independent association of each abnormal component of sleep quality with the development of preeclampsia. The analysis was adjusted as follows:

Model 1: Adjusted for variables with significant difference among two groups (pre-pregnancy body mass index, and smoking) and age.

Model 2: Included variables from model 1 plus variable that could potentially affect sleep quality or preclampsia risk (education, occupation, parity, pre-pregnancy diabetes mellitus, weight gain during pregnancy, daytime napping, physical activity, and depression score).

Statistical analysis was performed using SPSS version 24 (IBM Corp., Armonk, NY, USA), where p-value <0.05 was considered statistically significant.

Ethics Statement

Participation in the study was voluntary, and all participants signed a written informed consent. The QMNMS was approved by the Ethics Committee of Qazvin University of Medical Sciences (code: IR. QUMS. REC.1394.819).

RESULTS

Of the 821 women participating in this study, 245 participants were excluded from the final analysis due to the following reasons: being a shift worker (n=2), known depressive disorders before pregnancy (n=46), active rheumatologic disease, severe allergic rhinitis or asthma that interfered with sleep quality (n=41), uncompleted PSQI questionnaire (n=7), and miscarriage or loss to follow-up (n=149). Overall, the final analysis was performed on the data of 576 participants (Supplemental Material 1). Preeclampsia occurred in 20 women (3.5%). Baseline characteristics of the participants are presented in Table 1. The frequencies of smoking or being overweight or obese were higher in the preeclampsia group compared to the non-preeclampsia group (p=0.019 and 0.021, respectively). The two groups did not differ in terms of other variables, including age, education level, parity, history of pre-pregnancy diabetes, depression score, physical activity score, and PSQI score.

A comparison of categories of each sleep component between preeclampsia and non-preeclampsia groups is shown in the Supplementl Material 2. Sleep duration, subjective sleep quality, and PSOI score distributions were significantly different between preeclampsia and non-preeclampsia groups (p=0.034, 0.002, and 0.001, respectively).

A comparison of the frequencies of abnormalities in each component of sleep quality between preeclampsia and non-preeclampsia groups is shown in Table 2. Short sleep duration (<6 hours) was associated with a 5.5-time higher risk of developing preeclampsia (95% CI, 1.5 to 20.9; p=0.011). Long sleep duration (>9 hours) was not associated with a higher risk of preeclampsia. Prolonged sleep latency was associated with a 3.5-time higher risk of developing preeclampsia (95% CI, 1.2 to 10.1; p=0.019). Considering the total PSQI score, fairly bad or very bad sleep quality was a risk factor for developing preeclampsia, with a relative risk of 4.9 (95% CI, 1.4 to 17.8; p=0.014).

Table 3 presents adjusted associations of abnormalities in each sleep component with the development of preeclampsia in two models. All three sleep components abnormalities that showed a significant association with preeclampsia in univariate analysis, remained significant predictors either in the model 1 or model 2. In the fully adjusted model, short sleep duration and prolonged sleep latency were associated with 7.2 times and 4.5 times higher risk of preeclampsia, respectivey (95% CI, 1.6 to 33.1; p=0.011 and 95% CI, 1.4 to 14.6; p=0.012, respectively). In this model, pregnant women with fairly bad or very bad sleep quality had 5.9 times higher risk of preeclampsia development (95% CI, 1.5 to 22.8; p=0.011).

DISCUSSION

This study showed the important roles of sleep duration and poor sleep quality in preeclampsia development. Prolonged sleep latency and short sleep duration in the first trimester were the most important components of sleep quality affecting preeclampsia risk.

Evidence of the relationship between sleep quality and preeclampsia is limited such that most studies are case-control or cross-sectional. In a study on 313 pregnant women, Takmaz et al. [26] compared the sleep quality in 3 groups of preeclampsia, preterm labor, and control. The average enrollment time of the participant was about 225 days of pregnancy (about gestational week of 32 weeks). The frequency of poor sleep quality in the preeclampsia group was significantly higher than in the control group (87.5 vs. 74.8%; p=0.01, respectively). In a cross-sectional study by Khazaie et al. [27] the frequency of initial insomnia, fragmented sleep, and snoring were significantly higher in the preeclampsia group compared to the healthy pregnant group. In a case-control study in 150 women with preeclampsia and 150 healthy pregnant women, Kordi et al. [28] showed that the frequency of poor sleep quality in the preeclampsia group was significantly higher than in the healthy pregnant group (79.3 vs. 60.7%, respectively).

Considering the impact of critical illnesses (e.g., preeclampsia) on sleep quality [29], causality cannot be inferred in these cross-sectional illnesses or control cases.

Despite extensive studies on the research topic, we found only one cohort study on the association of poor sleep quality and preeclampsia. In a study conducted on more than 5000 pregnant women, Zhu et al. [15] assessed sleep quality in early pregnancy and the participants were followed until delivery. Despite the association of low sleep efficiency with gestational HTN, snoring was the only predictor of preeclampsia among sleep quality components.

Sleep duration is another important aspect of sleep characteristics. In the present study, short sleep duration (less than 6 hours) was associated with an approximately 7 times higher risk of preeclampsia in the adjusted model. More evidence of this association is available from cohort studies. In a cohort study by Williams et al. [14], the relationship between sleep duration and preeclampsia was evaluated in 1272 pregnant women. In this study, very short sleep duration (less than 5 hours) was independently associated with a higher risk of preeclampsia (OR, 9.52; 95% CI, 1.83 to 49.40) [14]. In the study by Zhu et al. [15], sleep duration in early pregnancy was not associated with preeclampsia. However, this study’s cut-off for defining short sleep duration was 7 hours.

The association of poor sleep quality and abnormal sleep duration with HTN in non-pregnant populations has been established in previous studies [8]. Among the components of sleep quality, several studies have shown difficulty in falling asleep (i.e., prolonged sleep latency) as the most common sleep problem [30] and reported its impact on the development of HTN or resistant HTN [31-34]. Since some of these studies used objective methods such as actigraphy to assess sleep quality, their results are more reliable [33,34].

The association between abnormal sleep duration and HTN in the non-pregnant population has also been reported in many studies. Excessively long or too short sleep duration can affect blood pressure [18]. In a meta-analysis conducted by Wang et al. [18] in 2015, a U-shaped relationship was found between sleep duration and HTN. In this research, a sleep duration of ≤5 hours or ≥9 hours was associated with a higher risk of HTN (OR, 1.61 and 1,29, respectively). Nevertheless, in other studies, this association was less consistent for long than short sleep duration. In another meta-analysis of 11 cohort studies, only short sleep duration was a risk factor for HTN development [7].

The proposed mechanisms involved in the pathophysiology of the effects of sleep disturbances on HTN and preeclampsia are multifactorial. The main pathophysiological processes in the development of preeclampsia are placental ischemia, systemic inflammation, and endothelial dysfunction [35]. Sleep disturbances are associated with endothelial dysfunction and increased inflammatory markers. In a meta-analysis of seventy-two cohort or experimental studies (more than 50 000 participants), Irwin et al. [36] identified higher levels of C-reactive protein and interleukin 6 in sleep disturbances. Endothelial dysfunction is another consequence of sleep disturbances reported in experimental and observational studies [37,38].

According to the above considerations, sleep quality and duration can play an important role in the development of cardiovascular abnormalities (including preeclampsia) in non-pregnant and pregnant people.

The present study had some limitations and some strengths. The main limitation of our study was the relatively low number of preeclampsia events. The main strength of our study was its prospective cohort design, which allowed for the evaluation of sleep quality in the first trimester, providing a stronger basis for establishing a causal relationship between poor sleep quality and preeclampsia. The second strength was the adjustment of preeclampsia risk associated with poor sleep quality for multiple risk factors, such as daytime napping, depression, and physical activity. In this respect, previous cohort studies on the relationship between preeclampsia and sleep quality have not evaluated the above-mentioned important confounding variables.

In conclusion, our cohort study demonstrated the role of short sleep duration and prolonged sleep latency as the main components of poor sleep quality in preeclampsia development. Other prospective cohort studies are suggested to investigate the causal role and pathophysiologic mechanisms of influencing sleep disturbances on the development of preeclampsia.

Supplemental Materials

Notes

Conflict of Interest

The authors have no conflicts of interest associated with the material presented in this paper.

Funding

None.

Acknowledgements

None.

Author Contributions

Conceptualization: Hashemipour S. Data curation: Ghasemi A, Esmaeili Kelishomi S, Mirzaeei Chopani S. Formal analysis: Hashemipour S, Ghafelehbashi SH. Funding acquisition: None. Methodology: Hashemipour S, Kolaji S, Modarresnia L. Project administration: Hashemipour S, Lalooha F. Writing – original draft: Kolaji S, Hashemipour S, Badri M, Abasi M. Writing – review & editing: Hashemipour S, Badri M. Ghasemi A, Esmaeili Kelishomi S, Mirzaeei Chopani S, Ghafelehbashi SH, Lalooha F, Abasi M, Kolaji S, Modarresnia L.

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