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. Author manuscript; available in PMC: 2025 Feb 1.
Published in final edited form as: Sleep Med Rev. 2023 Nov 1;73:101868. doi: 10.1016/j.smrv.2023.101868

Maternal sleep disordered breathing and offspring growth outcome: a systematic review and meta-analysis

Laura Sanapo 1,2, Sandra Hackethal 3, Margaret H Bublitz 1,2,4, Kelsey Sawyer 5, Corrado Garbazza 6, Arabhi Nagasunder 7, Marian Gonzalez 1, Ghada Bourjeily 1,2
PMCID: PMC11000747  NIHMSID: NIHMS1945909  PMID: 37956482

Summary

Sleep disordered breathing is extremely common in pregnancy and is a risk factor for maternal complications. Animal models demonstrate that intermittent hypoxia causes abnormal fetal growth. However, there are conflicting data on the association between maternal sleep disordered breathing and offspring growth in humans. We investigated this association by conducting a systematic review and meta-analysis. Sixty-three manuscripts, and total study population of 67,671,110 pregnant women were included. Thirty-one studies used subjective methods to define sleep disordered breathing, 24 applied objective methods and eight used international codes. Using a random effects model, habitual snoring, defined by subjective methods, and obstructive sleep apnea, diagnosed by objective methods, were associated with an increased risk for large for gestational age (OR 1.46; 95%CI 1.02–2.09 and OR 2.19; 95%CI 1.63–2.95, respectively ), while obstructive sleep apnea, identified by international codes, was associated with an increased risk for small for gestational age newborns (OR 1.28; 95%CI 1.02–1.60). Our results support that maternal sleep disordered breathing is associated with offspring growth, with differences related to the type of disorder and diagnostic methods used. Future studies should investigate underlying mechanisms and whether treatment of sleep disordered breathing ameliorates the neonatal growth.

Keywords: Maternal sleep disordered breathing, snoring, obstructive sleep apnea, sleep, fetal growth, neonatal growth, small for gestational, large for gestational age, low birthweight

Introduction

Maternal sleep disordered breathing (SDB) is a spectrum of disorders, common in pregnancy, characterized by snoring, airflow limitation, and intermittent hypoxia. Snoring and obstructive sleep apnea (OSA), two common SDB disorders, affect 33% of all pregnancies, and up to 70% of high-risk pregnancies, respectively [1–3]. The incidence of these maternal conditions is likely to increase given the global rise in obesity, a major risk factor for SDB [4]. Prenatal exposure to SDB is an independent risk factor for adverse pregnancy outcomes, such as gestational diabetes [2,5,6], perinatal depression [7], hypertensive disorders [2,6,8], cesarean delivery [9], and severe maternal cardiovascular complications and intensive care unit admission [8], especially among women with high-risk pregnancies [10]. In addition, pregnancies complicated by maternal SDB present a higher risk for adverse neonatal outcomes, including preterm birth, congenital abnormalities, stillbirth, and postnatal medical complications requiring hospitalization [9,11]. Despite this evidence, data from human studies on SDB in pregnancy and abnormal offspring growth are limited, and evidence conflicting.

Animal models of OSA show that exposure to gestational intermittent hypoxia leads to fetal growth restriction, and complications in the offspring, such as abnormal glucose metabolism, an increase in adipose tissue [12], cardiac hypertrophy and arterial stiffness [13]. Underlying mechanisms, proposed by animal studies, include an impairment of placental function through adverse effects on the vasoreactivity of the uterine arteries, increase in oxidative and inflammatory markers, and abnormal production of placental angiogenic and growth factors [14]. However, most of the previous human studies on SDB in pregnancy and neonatal outcomes, including systematic reviews, provided conflicting results, with data showing a possible association with fetal growth restriction, macrosomia, or neither [6,8,15]. While it is biologically plausible that SDB would be associated with growth restriction, other maternal conditions associated with SDB (e.g., diabetes, obesity) may slow or accelerate fetal growth depending on time at onset of the condition and severity [16].

Growth restriction and macrosomia are the two main outcomes of abnormal fetal growth, a condition affecting 20% of all pregnancies [16,17]. Abnormal offspring growth is a major cause of neonatal mortality and morbidity [16,18,19]. Identifying modifiable prenatal risk factors of abnormal fetal growth allows appropriate antenatal surveillance of fetal development and ultimately improves the outcomes of those newborns at highest risk for either decreased or accelerated growth in-utero [20]. Based on current practice, prenatal ultrasound evaluation of fetal growth after mid gestation is not universally performed [21]. Given that maternal SDB, compared to other obstetric factors [16], is amenable to non-invasive and non-pharmacological treatment [22], this condition may represent a modifiable risk factor for abnormal fetal growth in utero. Therefore, establishing whether maternal SDB affects fetal growth can help identify those pregnancies in need for fetal surveillance, to improve neonatal outcome.

In the proposed study, we aim to examine whether maternal SDB in pregnancy is a risk factor for abnormal offspring growth, by conducting a systematic review and meta-analysis of the available evidence.

Methods

We searched PubMed, Cochrane Library, Embase, CINAHL, and Web of Science, with terms related to SDB in pregnancy and fetal growth outcome. The full search is available as a supplemental file (Table S1). Studies were included based on the inclusion and exclusion criteria presented in Table S2.

The literature search was completed on July 13, 2023. Two investigators (LS and MB) screened each title and abstract independently using the online program Covidence (https://app.covidence.org/) and then they reviewed the full text of the manuscripts of the included abstracts. Discrepancies were discussed and verified by a third investigator (GB). For data extraction we generated a detailed coding system form which included sample size, study design, inclusion and exclusion criteria of the enrolled population, diagnostic criteria used to determine SDB, gestational age or trimester at diagnosis, methods used to define offspring growth outcome, including the fetal or neonatal reference ranges to derive birthweight percentile values, obstetric complications, and type of statistical analysis conducted. We performed quality assessment by using the Newcastle-Ottawa Scale (NOS), a scoring system originally designed for case-control and cohort studies, and more recently applied to cross-sectional studies [23,24]. This method evaluates three dimensions of a study: the selection of study population; the comparability of study groups and the assessment of exposure and outcome. When applied to case-control and cohort studies, the NOS score has a maximum value of nine and a score of seven or more is considered of high methodological quality. In case of cross-sectional studies, the maximum value of NOS is seven.

The study protocol was registered to the International prospective register of systematic review (CRD42022381065).

Statistical Analysis

The final manuscripts included in the systematic review were divided in three groups based on the method used to identify maternal SDB. Specifically, the first group included those studies using subjective methods or questionnaires, the second included those studies using objective methods or sleep test and the final group was composed by those reports that applied international classification of diseases (ICD) codes related to diagnosis of SDB. In each group, we identified subgroups presenting similarities regarding diagnostic methods (such as a specific questionnaires, or type of sleep test device), cut-off and scoring system for the diagnosis of maternal SDB and definitions of offspring growth outcomes. When at least three studies were available using the same or comparable methods assessing the presence of SDB, fixed- and random-effects model meta-analysis was performed. To evaluate the difference between birth weight of infants born to either cases of the SDB-spectrum and controls, we pooled the mean and standard deviation of the respective studies and used weighted mean difference (MD) with the corresponding 95% confidence interval (95% CI) for absolute differences of continuous outcomes. For dichotomous outcomes (example: small for gestational age or SGA, low birthweight, or LWB, defined by birthweight <2500 g, and large for gestational age, or LGA), the odd ratio (OR) with 95% CI were used to estimate the pooled effects. Since there was considerable variability among the studies regarding availability of adjusted ORs and the individual chosen confounders, we limited our analysis to unadjusted ORs. Heterogeneity of the chosen studies was investigated using I2 and Cochrane’s Q test with a P-values of Cochrane’s Q test < 0.01 or the <di>I2 > 50% indicating significant between study heterogeneity. Since we only regarded and discussed the random effects models of the analysis, Venetian heterogeneity was already accounted for. Funnel plots and Eggeŕs linear regression test were used to evaluate publication bias. In the case of asymmetrical funnel plots upon visual inspection and Eggert`s test p <0.05, a “trim and fill” analysis was conducted [25]. All statistical tests were performed in R 4.2.2 [26], using the meta (version 6.2–1) [27] and metasens (version 1.5–2) [28] libraries. Two-sided significance tests were used and results considered statistically significant if the p value was <0.05.

Results

Literature Search and general characteristics of included studies

We initially identified 1,327 references from the five databases selected. After excluding duplicates (n=238), we screened titles and abstracts of 1,089 records (Figure 1), 856 were excluded, and the remaining 233 reports were reviewed as full text. Among those, 63 manuscripts met the inclusion and exclusion criteria (Tables S3-S5). Thirty-one (49%) were cohort longitudinal studies, 19 (30%) were cross-sectional and 13 (21%) case-control. Thirty-one (49%) manuscripts used subjective methods to define SDB, 24 (38%) applied objective methods and eight (13%) used ICD codes to identify pregnancies complicated by SDB. The 63 selected manuscripts identified a total study population of 67,671,110 pregnant women. The prevalence of SDB in pregnant women varied among the studies, and was 23.22%, 16.98% and 0.04% for studies using subjective, objective and ICD codes, respectively.

Figure 1.

Figure 1.

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PRISMA 2020 flow diagram.

Study quality

The median (range) NOS score for the longitudinal and case-control studies were 6 (4–7) and 5 (2–9) respectively, with 19 (43%) manuscripts having a score of seven or higher, indicating high quality. For the cross-sectional studies, the median (range) of NOS was 4 (2–6) and none reached the highest score for this study design category.

Gestational age at diagnosis of maternal SDB and definition of exposure among the studies using subjective methods.

A total of 28,556 pregnant subjects were enrolled in these 31 studies, and 6,631 women (23.22%) were diagnosed with SDB by using subjective methods (Table S3). Screening for maternal SDB was performed at the time of delivery or post-partum in twelve studies (43%) [1,30,33–35,39,49,51,56,58,62,63], in the second and third trimester in thirteen studies (39%) [40,42–46,48,50,52,54,55,65,66], while only a minority included participants in the first trimester of pregnancies (14%) [29,37,57,60] or did not specify any gestational age or trimester (4%) [59,61]. While the type of questionnaire varied among the reports, 54% of the studies based the exposure on self-reported snoring, with habitual snoring defined as a frequency of at least three-four times per week in the majority of cases [1,35,37,40,43–46,48,54,56,57,62,63,66]. Other questionnaires used included the Berlin, Epworth sleepiness scale, Stop-BANG, Pittsburgh sleep quality index, and Basic Nordic Sleep Questionnaire (Table S3).

Definition of fetal growth outcomes and covariates of the studies using subjective methods

The definition of fetal growth outcome varied among the 31 studies with subjective methods for SDB assessment, with 14 studies using a single definition of fetal growth outcome, and 17 using more than two different criteria. The two most common methods, used in 23 studies (74%) were neonatal birthweight expressed as raw or percentile value and number of SGA newborns, defined by birthweight below 10th percentile for gestational age, however only some studies specified the fetal or neonatal normal reference range used to derive percentile values of the birthweight [1,37,40,45,46,48,52,56,63]. Moreover, each of these studies used a different normal reference range. Other fetal growth outcomes included LBW, based on birthweight below 2,500 grams regardless of gestational age at birth, and LGA, defined by birthweight above the 90th percentile for gestational age. None of the subjective studies used fetal growth velocity to assess fetal growth outcome.

Fifteen studies (48%) [29,33–35,37,40,42,45,46,48,50,54,59,61,66], among the 31 using subjective methods, controlled the results for covariates, with the majority adjusting the results for maternal age, body mass index, smoking exposure in pregnancy, and only a minority included other factors affecting fetal growth outcome, such as maternal obstetric complications [29,40,46,50,59], race and ethnicity [29,40,59] or fetal sex [40].

Gestational age at maternal SDB diagnosis and definition of exposure among the studies using objective methods

These 24 studies included a total study population of 6,555 pregnant women (Table S4). Of those, 16.98% were diagnosed with OSA. Most assessed maternal SDB in the second or third trimester. The device used to identify OSA varied, with eveln studies using a level III device [69,70,73,75,79–81,89,91,98,99], six preforming overnight sleep studies with level I device [67,78,88,90,92,96], and three using more than one device [76,94,100]. The remaining studies used a level II [83] or level IV [82,101], and the sleep apnea monitor used was not specified in one case [22]. As shown in Table S4, most of the studies used a cut-off of AHI equal or greater than five to define OSA, however, both the scoring system applied and definition of hypopnea varied, while in some reports this information was not specified. The majority of OSA cases diagnosed were mild, with average values of AHI ranging from 5.4 to 15 events per hour.

Definition of fetal growth outcomes and covariates of the studies using objective methods

The methods and diagnostic criteria used to assess fetal growth outcome varied among this group of studies, with the majority using more than one method. The most common diagnostic criteria were birthweight expressed as raw or percentile value and SGA, defined by birthweight below the 10th percentile for gestational age at delivery. Fourteen (58%) of the 24 studies of this group reported the fetal or neonatal normal reference range used to derive percentile values. Less common criteria used included LBW, fetal abdominal circumference below the 10th percentile, birthweight below the 5th, or above the 90th and 95th percentile, fetal growth velocity or estimated fetal weight, based on prenatal ultrasound, below the 3rd or 10th percentile for gestational age at testing.

Among the 24 studies using objective methods, eleven controlled the results for covariates [22,70,73,75,76,79,80,82,83,96,99], which included maternal BMI in all eleven cases, obstetric complications [22,73,75,76,79,82], and maternal ethnicity in limited reports [75,82,83]. Some report also controlled for fetal sex [83] or applied sex-specific normal reference range of the fetal growth [22,76,94,100].

Results of subgroups analysis

Subjective measures of SDB and small for gestational age at birth

Nine studies [29,37,42–44,46,48,56,63] defined SGA as birthweight below 10th percentile for gestational age and provided number of SGA newborns among subjects with and without SDB. The statistical heterogeneity in this subgroup was low (I2= 0%; p=0.52). The random effects model showed a trend toward a higher risk for SGA newborns among pregnancies without SDB, however it did not reach statistical significance (OR 0.84; 95%CI 0.72–1.01) (Figure 2). When the studies were divided based on the type of questionnaire used to identify maternal SDB, the results were similar among the seven studies using self-reported snoring (OR 0.88; 95%CI 0.72–1.08) [37,43,44,46,48,56,63] (Figure 3).

Figure 2.

Figure 2.

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Subjective sleep disordered breathing assessment and risk of small for gestational age newborns.

Figure 3.

Figure 3.

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The studies previously included in Figure 2 are divided into two subgroups, based on type of questionnaire used to assess sleep disordered breathing. Subgroup 1: self-reported snoring assessment. Subgroup 2: Berlin questionnaire.

Subjective measures of SDB and birthweight

Seven studies [43–46,56,62,65] compared the birthweight between pregnant women with and without SDB assessed by subjective methods. Based on these studies, women with and without SDB delivered at term (gestational age of 37 weeks or above), at a similar gestational age. As represented in Figure 4, the heterogeneity between these studies was statistically significant (I2= 54%; p=0.04). When we included only the five studies [43,44,46,56,63] using a similar questionnaire assessing snoring frequency and same cut-off (three or four times per week) to define habitual snorers, the heterogeneity between studies decreased (I2= 27%; p=0.24) (Figure 5). The mean difference in birthweight between newborns born to mothers with SDB and newborns to mothers without SDB was not significant. As represented by the funnel plot (Figure S1), publication bias was unlikely, given a similar distribution of positive and negative correlations between maternal SBD assessed by subjective methods and fetal growth outcome.

Figure 4.

Figure 4.

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Subjective sleep disordered breathing assessment and mean difference in birthweight.

Figure 5.

Figure 5.

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Subjective sleep disordered breathing assessment and mean difference in birthweight. The studies previously presented in Figure 4 have been divided in subgroups based on type of questionnaire used. Subgroup 1: questionnaire different from self-reported snoring. Subgroup 2: self-reported snoring.

Subjective measures of SDB and large for gestational age at birth

In four studies [37,46,48,56] habitual snoring in pregnancy was associated with an increased risk for LGA newborns (OR 1.46; 95%CI 1.02–2.09, p=0.037) (Figure 6). However, the heterogeneity across these studies was elevated (I2= 73%; p=0.01).

Figure 6.

Figure 6.

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Subjective sleep disordered breathing assessment and risk for large for gestational age newborns.

Subjective measures of SDB and low birthweight

Habitual snoring was not associated with an increased risk for LBW, based on the random effects analysis of the three studies [37,45,49] using similar questionnaires to define SDB (OR 1.38; 95%CI 0.72–2.66, p=0.335). Heterogeneity across these studies was not significant (I2= 46%; p=0.16) (Figure 7).

Figure 7.

Figure 7.

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Subjective sleep disordered breathing assessment and risk for low birthweight.

Objective measures of SDB and small for gestational age

Among the 24 studies using objective methods of SDB, eight studies [22,69,73,76,79,90,91,99] used a cut-off value of five of the apnea-hypopnea index (AHI) or respiratory disturbance index (RDI) to define maternal OSA, in the second or third trimester of gestation, and a birthweight value below the 10th for gestational age to define SGA newborns. The heterogeneity across this subgroup was I2= 9% (p=0.36). The random effects model did not show any significant risk for SGA (OR 0.77; 95%CI 0.51–1.15, p=0.201) (Figure 8). We then divided the above seven studies in two subgroups, based on which guidelines were used to score the sleep studies (Figure 9). Four studies [69,76,91,99] used the criteria established by the American academy of sleep medicine in 2007, with hypopnea defined as a reduction in airflow of at least 50%, and the heterogeneity across these subgroup was low (I2 = 24%, p=0.27). The remaining reports used different criteria or did not specify how hypopnea events were defined [22,73,79,90] (I2 = 0%, p=0.70). The random effects model confirmed a non-significant association between OSA and SGA in both subgroups (Figure 9). As represented by the funnel plot (Figure S2), no publication bias was detected.

Figure 8.

Figure 8.

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Obstructive sleep apnea diagnosed by sleep test and risk for small for gestational age newborns.

Figure 9.

Figure 9.

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Obstructive sleep apnea diagnosed by sleep test and risk for small for gestational age newborns. The studies previous represented in Figure 8 are divided in two subgroups, based on the guidelines used to score the sleep studies. Subgroup 1: studies using criteria different from the 2007 American Academy of Sleep Medicine, or definition of hypopnea not specified. Subgroup 2: studies using the 2007 American Academy of Sleep Medicine.

Objective measures of SDB and birthweight

Seven studies with OSA defined by AHI or RDI equal or greater than 5 and fetal growth outcome reported as birthweight were identified [69,76,78,81,90,92,98]. The participants included in these studies delivered at term, with gestational age at birth similar among study groups. This subgroup had low heterogeneity (I2 = 0%, p=0.80) and the mean difference in birthweight did not reach significance (−88.42; 95%CI −193.56–16.71) (Figure 10).

Figure 10.

Figure 10.

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Obstructive sleep apnea diagnosed by sleep test and mean difference in birthweight.

These results were confirmed when we included only the five studies defining OSA by AHI values of 5 or above events per hour [69,81,90,92,98] (Figure S3).

We further divided the above five studies in two subgroups, by excluding two studies that did not specify the scoring system used [81,90] to define OSA. Similarly, the results of the random effects model of the remaining studies [69,92,98], which used the 2007 American Academy of Sleep Medicine criteria, were not statistically significant (MD −71.06; 95%CI −187.44–45.32) (Figure S4).

Objective measures of SDB and large for gestational age at birth

Three studies reported data on LGA [73,79,99] (Figure 11). This group presented low heterogeneity (I2 = 0%, p=0.42). The random effects model showed an association with LGA newborns (OR 2.19; 95%CI 1.63–2.95, p<0.0001). Only one study reported data on newborns with low birthweight [88], preventing the performance of this meta-analysis.

Figure 11.

Figure 11.

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Obstructive sleep apnea diagnosed by sleep test and risk for large for gestational age newborns.

Studies using ICD codes and association with small for gestation age newborns

Eight reports [8,11,103,106,108,110–112] identified maternal SDB through ICD codes for OSA included in delivery discharge hospital records (Table S5). These studies differed in study population size, ranging from 190 to 55,781,965, and included a total of 67,635,999 pregnant subjects. Given the intrinsic limitations of defining a condition by using ICD codes, none of these studies reported information on time at diagnosis of SDB, type of testing used to identify OSA, disease severity or therapy. Only one study [108] specified that, in the database used, ICD codes for OSA implied completion of polysomnograms in ambulatory setting within one year prior to delivery. The most common offspring growth outcome investigated was small for gestational age, defined by birthweight <10th percentile and/or identified by ICD codes. Six studies reported data on number of SGA of pregnancies with and without OSA [11,103,108,110–112] and were included in the meta-analysis. Based on the random effects model, prenatal exposure to OSA was associated with an increased risk for SGA (OR 1.28; 95%CI 1.02–1.60, p=0.029), however the heterogeneity across this subgroup was elevated I2= 77% (p=0.01) (Figure 12). Less common outcomes were birthweight above the 90th percentile, reported by two studies [11,103], and low birthweight, presented only in one report [108], preventing additional analysis.

Figure 12.

Figure 12.

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Obstructive sleep apnea identified by the international classification of diseases codes and risk for small for gestational age newborns.

Discussion

We conducted a systematic review and meta-analysis examining whether prenatal exposure to maternal sleep disordered breathing is a risk factor for abnormal offspring growth. Most of the studies included in our analysis identified maternal SDB in late pregnancy or post-partum, while only a minority assessed frequency of this maternal condition in the first trimester of pregnancy, which is a critical time for the developing fetus and placenta [29,37,57,81,88].

The meta-analysis on the association between maternal SDB and offspring growth outcome led to different results, depending on the type of exposure used, subjective, objective, or ICD defined SDB. Maternal snoring, identified by subjective methods, and OSA, diagnosed by objective assessment, were associated with an increased risk for LGA, while maternal OSA, identified by ICD codes, was associated with an increased risk for SGA. Underlying reasons for variability in results may be related to the fact the spectrum of SDB disorders includes conditions that vary in clinical severity and that may present different impact on placenta function and fetal wellbeing. For example, habitual snoring may have a lesser impact on fetal development compared to severe sleep apnea as data from non-pregnant individuals suggest that compared to snorers with sleep apnea, non-apneic snorers are unlikely to present nocturnal episodes of oxygen desaturation [113]. Hence, though snoring is associated with a biological cascade leading to adverse pregnancy outcomes [1,114,115], it is possibly that nocturnal hypoxemia may be an essential component to growth restriction. However, it is noteworthy that studies included in this systematic review that have used snoring as an exposure, did not exclude the presence of OSA, hindering the assumption that patients with snoring only have snoring but OSA. Our group [56] has previously documented that maternal serum levels of markers of fetal growth restriction [116], such as alpha fetoprotein, pregnancy-associated plasma protein A and inhibin A, of pregnant participants with habitual snoring are similar to those described among controls. Despite this evidence, the effects of maternal snoring on offspring growth remains controversial. Previous reports have documented that chronic maternal snoring, with onset before conception, represents an independent risk factor for small for gestational age newborns [46,66], while pregnancy-onset snoring is an independent risk factor for large for gestational age newborns [37,48] among women without a previous history of SDB or additional sleep disturbances. This suggests that time of onset of habitual snoring in relation to pregnancy may be an important factor in the association with fetal growth. A recent study documented that chronic and pregnancy onset snoring lead to different maternal blood pressure trajectories, suggesting that these two conditions are associated with different maternal cardiovascular effects [115]. Similar mechanisms may be involved in the association with offspring growth outcome; however, underlying pathophysiology needs to be investigated.

It is important to mention that our meta-analysis of the subgroup of the studies with similar snoring questionnaires administered and similar definition of large for gestational age, included cases diagnosed with habitual snoring, without distinguishing between chronic versus pregnancy-onset snoring. This is related to the fact that not all the manuscripts reported data on the offspring growth outcome based on time at onset of maternal snoring. Despite this limitation, this subgroup of studies presented overall higher number of pregnancy-onset snoring compared to chronic snoring. Therefore, our results may mainly reflect the effect of pregnancy-onset snoring rather than chronic snoring. Another important consideration is that pregnancies complicated by maternal snoring of the subgroup of studies we investigated, compared to controls, also presented higher maternal BMI, hypertensive disorders [37,46,48,56] and higher frequency gestational diabetes [48,56], which are known to affect growth outcome. However, the details of these factors in relation to the subgroup of pregnancies complicated by large for gestational age newborns were not available, limiting the possibility of adjusting the results of our meta-analysis.

Animal models of OSA support that intermittent hypoxia reduces the maternal uterine vascular function [14], and impairs fetal growth, by affecting offspring metabolism, fat distribution and the production of growth factors [12]. A pilot human study found differences in cord blood levels of fetal growth regulators between pregnancies complicated by objectively defined maternal OSA and controls [76], with newborns among cases being at higher risk for impaired fetal growth. Maternal disease severity may also impact offspring growth outcomes. Pamidi et al. [83] demonstrated that objectively defined OSA in the third trimester is associated with impaired fetal growth and increases the risk for small for gestational age newborns only in patients with moderate and severe OSA. On the other hand, other studies have shown that mild OSA was associated with greater birthweight percentile and placenta weight [80] and smaller head circumference at birth but accelerated adiposity acquisition in early infancy, compared to no OSA [70]. Discrepancies between animal models of sleep apnea and different forms of OSA in pregnant women may be due to the fact animal models are more representative of the pathophysiology of severe forms of OSA described in humans [13].

It is important to highlight that most of the studies using objective methods included in our systematic review identified mild forms of OSA, with AHI values less than 15 events per hour. Therefore our results may confirm that mild OSA is associated with large for gestational age newborns, rather than increasing risk for SGA, and this is in agreement with the previous studies focusing on mild forms of OSA [70,80]. Further, in our meta-analysis, most of the studies that performed objective testing in pregnancy could not determine whether OSA predated pregnancy or developed de novo during pregnancy, limiting the examination differential effects on maternal biological adaptations depending on timing of exposure to OSA.

Our results of the meta-analysis of those studies using ICD codes did find an association between maternal OSA and SGA newborns. While hospital administrative databases are commonly used in research in pregnancy, it is known the correct identification of specific maternal prenatal conditions and offspring outcomes, through international codes from discharge records, depend on several factors [117]. Based on previous studies, these databases present high accuracy in identifying those maternal and neonatal conditions of great severity, or high prevalence, and characterized by established diagnostic criteria, such as small for gestational age [117–119]. These reasons may explain that, in our metanalysis, OSA defined by sleep testing in pregnancy and maternal OSA identified by ICD codes presented different results regarding offspring growth outcome. As OSA is underdiagnosed in pregnancy, we can postulate that the use of codes may have identified the most severe forms of maternal OSA and hence the association. It is also possible, however, that sample size may have impacted differences in findings between cohort studies that tested OSA objectively and the much larger population-based studies that used ICD coding. Only two studies, among the reports using ICD codes [11,103], investigated the association between OSA and LGA newborns, with conflicting results, and preventing the performance of the meta-analysis. This limits the understanding of possible association between OSA defined by international codes and other types of abnormal offspring growth outcomes.

Our meta-analysis also highlighted that heterogeneity across studies varied based on the methods used to define SDB. Specifically, among the studies using objective methods, we performed subgroups analysis by selecting those reports using similar cut-off values of AHI and/or RDI and scoring systems to define OSA. This resulted in null or low heterogeneity across the objective studies included in the subgroups analysis. Although we used a similar approach for the analysis of the studies using subjective methods and ICD codes, by including only those with similar methods to define SDB and the specific offspring growth outcomes, subjective and ICD codes manuscripts presented high heterogeneity (with I2 up to 77%). It is important to consider that, despite we divided the studies in subgroups based on the specific subjective method to define SDB, (Figure 5) some differences persisted in relation to the characteristics of the study population enrolled. Some studies [43,44,62] enrolled low-risk pregnancies, while others included both high-and low-risk pregnancies [46,56]. Also, the frequency of prenatal exposure to tobacco, which is known to affect fetal growth outcome [120], varies among the studies reporting this data [43,45]. These factors may have contributed to the high heterogeinity of the results between the subgroups of studies using subjective methods (Figure 5).

Great heterogeneity has also been highlighted by previous systematic reviews on maternal SDB and pregnancy outcome. Pamidi et al. [6] reported high heterogeneity of the studies on maternal SDB with birthweight data available, however, they did not test whether subgroups based on similar diagnostic SDB criteria presented a lower heterogeneity. The systematic review and meta-analysis conducted by Brown et al. [9] on maternal SDB and multiple perinatal outcomes, found that the heterogeneity between the studies with offspring growth outcome was moderate. Brown et al. reported a trend for birthweight being lower among pregnancies complicated by OSA, identified by objective methods, although results did not reach statistical significance. They did not investigate the possible association with LGA, and they did not report sub-analysis based on the specific diagnostic criteria or scoring system used to define OSA. In a recent systematic review and meta-analysis on several sleep disturbances in pregnancy, Lu et al. [121] reported that maternal SDB, defined by subjective symptoms, but not OSA, was a risk factor for LGA. They also described high heterogeneity between the studies using subjective methods. An additional consideration is that the questionnaires used to screen for SDB in pregnancy present different sensitivity and sensibility, and for each questionnaire, accuracy may vary depending on gestational age at admistration, specific characteristics of the study population and severity of the disorders in the SDB spectrum [122,123]. The Berlin questionnaire, one of the most common screening tool, has a better performance in the second half of pregnancy and when applied to a general pregnant population, rather than high-risk pregnancies [122]. Moreover, it is affected by overweight and obesity [124]. Underlying reasons are that overweight and obesity, which are known risk factors for SDB [4], are very common in pregnancy, affecting almost 30% of women entering pregnancy and one third of those subjects with a normal BMI at conception but excessive gestational weight gain [125,126]. These considerations highlith the need for a specific screening method for SDB in pregnancy.

Methodology used to assess the offspring growth outcome varied significantly among studies. We identified more than 15 definitions, with the two most common being SGA, defined by birthweight below the 10th percentile for gestational age, and birthweight expressed as raw values in grams or kilograms. Although the use of birthweight percentile was common, the type of normal reference range of the fetal or neonatal weight used to derive percentile values was not always reported. In addition, the type of nomogram used, when reported, varied among the studies, with more than eighteen different reference ranges used. These represent important limitations, since as we and others have demonstrated, the frequency of abnormal offspring growth outcomes is affected by the definition and nomogram used [127–129]. Moreover, although the use of birthweight, as raw values or percentile, is commonly used to describe neonatal growth, this method can miss up to 90% of those infants with abnormal fetal growth, who are at risk for developing associated morbidities later in life, such as obesity, metabolic and cardiovascular diseases [17]. Most of the newborns with abnormal fetal growth, especially impaired in-utero growth, are born with birthweight above the 10th percentile for gestational age, therefore above the cut-off commonly used to define SGA newborns [17]. Underlying reasons are that fetal growth is a dynamic process and, under normal circumstances, is based on a specific fetal weight gain over time [130]. Therefore, a single measurement of the offsping size, either in pregnancy or at birth, cannot correctly detect those fetuses who fail to reach their growth potential [131]. In addition, a single evaluation of the fetal size may miss possible temporal associations between prenatal exposure to risk factors and onset of abnormal growth [132]. There is evidence that more accurate methods are those providing a comprehensive and longitudinal evaluation of placenta and fetal development, such as Doppler vascular biomarkers and fetal growth velocity [133]. In our systematic review, only two studies [22,76] defined impaired fetal growth as birthweight below the 10th centile or decreased third trimester fetal growth velocity. Both studies reported a higher frequency of impaired fetal growth among pregnancies complicated by OSA, and in one study [22] this remained statistically significant after controlling for several covariates. The same authors [22] also described that, among those cases treated with positive airway pressure, there was not an increased risk for impaired fetal growth, suggesting that therapy of OSA in pregnancy may ameliorate offspring growth outcome.

Clinical and research implications

The results of this systematic review and meta-analysis support that SDB in pregnancy is associated with adverse offspring growth, with differences based on the type and severity of SDB. Further studies would need to investigate the underlying pathophysiology. In addition, it would be necessary to identify those factors moderating this association, including time at onset of the specific SDB (before or during gestation), and maternal comorbidities often coexisting with OSA and habitual snoring, and affecting offspring outcome, such as obesity, diabetes, and hypertensive disorders [16]. At present, there are no universal guidelines on screening and treatment of SDB in pregnancy, and whether prenatal management of this maternal condition improves offspring outcomes. There is biological plausibility and limited preliminary data to support that maternal use of continuous positive airway pressure (CPAP) may positively impact fetal growth outcome [22,134]. A larger study has recently demonstrated that use of CPAP among pregnant women with OSA and obesity, is associated with lower vascular resistance of the uterine arteries, compared to controls, supporting that treatment of SDB is associated with an improvement in placenta function [135]. However, a recent systematic review by Migueis et al [136] emphasizes the overall limited number of existing trials on use of CPAP in pregnancy and offspring outcome, especially growth outcome. Moreover, the previous trials presented great heterogenicity in population enrolled, and duration of the therapy with CPAP, ranging from a single night, to several weeks. As SDB is a modifiable risk factor, there is urgent need in better understanding the association with fetal growth outcomes and testing new interventions.

Strengths and limitations

Our study presents several strengths. It includes a large study population size. We conducted the meta-analysis for subgroups of studies with similar methods and diagnostic criteria used to define specific conditions of the SDB spectrum [137], allowing for lower heterogeneity among subgroups of studies, compared to previous systematic reviews [6]. In case of manuscripts using objective methods, we were able to also distinguish between the scoring systems applied in the definition of OSA, given the fact that differences in scoring system may affect prevalence of this condition [138].

Our study also presents limitations. Less than 50% of the cohort and case-control studies were high quality based on the NOS system. None of the cross-sectional studies reached the highest NOS value for this study design category. There was paucity of studies with data on SDB in early pregnancy, limiting our understanding of the possible effects of this maternal condition on the developing fetus and placenta. Also, preterm birth was often an exclusion criterion of the reports, and this may have affected the number of pregnancies complicated by abnormal fetal growth, given that growth restriction and maternal conditions affecting neonatal outcome are often indications for induction of labor before term [139]. In addition, although 63 manuscripts met the inclusion criteria, a lower number was eligible for meta-analysis. Moreover, most of the studies reported neonatal birthweight expressed as raw value or frequency of SGA newborns, with only a minority including data on LGA newborns. This limitation prevented the meta-analysis of the association between OSA defined by ICD codes and LGA. Additionaly, while some studies controlled the results for covariates, information on covariates for the specific growth outcomes we investigated were not available. Therefore, the results of our meta-analysis were not adjusted for factors that may affect offspring growth outcomes.

Conclusions

Our systematic review and meta-analysis support that exposure to sleep disordered breathing in pregnancy is associated with abnormal offspring growth outcome, with differences related to the type of the disorders, diagnostic methods used, and possibly the severity and timing of the exposure. Further studies are needed to identify the underlying pathophysiology, by applying comprehensive assessment of fetal and placenta development and by analyzing whether time at onset of sleep disordered breathing affect this association. In addition, our study supports the need for trials on the effects of prenatal management of this maternal condition and offspring outcomes.

Supplementary Material

1

Figure S1. Publication bias assessment for studies using subjective methods.

2

Figure S2. Publication bias assessment for studies using objective methods.

3

Figure S3. Obstructive sleep apnea diagnosed by sleep test and mean difference in birthweight. Forest plot including only the studies defining obstructive sleep apnea by apnea-hypopnea index values of five or above events per hour.

4

Figure S4. Obstructive sleep apnea diagnosed by sleep test and mean difference in birthweight. Studies of figure S3 are divided in two subgroups, based on the scoring system used. Subgroup 1: no scoring system specified. Subgroup 2: studies using the 2007 American Academy of Sleep Medicine criteria.

5

Table S1. Search Strategy

6

Table S2. Inclusion and exclusion criteria

7

Table S3. Characteristics of the studies using subjective methods to identify maternal sleep disordered breathing.

8

Table S4. Characteristics of the studies using objective methods to identify maternal sleep disordered breathing.

9

Table S5. Characteristics of the studies using international classification of diseases codes to identify maternal sleep disordered breathing.

Practice Points.

  1. Maternal sleep disordered breathing affects the offspring growth outcome, with differences related to the type of disorder, diagnostic methods used, and possibly the severity and timing of the exposure.

  2. The existing scientific literature on this topic is characterized by great heterogeneity in methods used to identify sleep disordered breathing in pregnancy, gestational age at testing, diagnostic criteria of abnormal offspring growth and normal reference ranges of fetal and neonatal weight.

Research Agenda.

  1. Elucidate underlying mechanisms of the association between prenatal exposure to sleep disordered breathing and offspring growth outcome, by applying comprehensive and longitudinal assessment of fetal and placenta development.

  2. Evaluate whether time at onset of maternal sleep disordered breathing (example: chronic versus pregnancy-onset) and maternal comorbidities affect the association with offspring growth outcome.

  3. 3. Establish whether maternal treatment of sleep disordered breathing ameliorates neonatal growth.

Acknowledgements:

We would like to thank Ms. Beth Hott for her assistance with manuscript preparation.

Conflicts of interest:

The authors declare that they do not have any conflicts of interest related to the data presented in this manuscript. This work is supported by research grants from the Rhode Island Foundation and Chest Foundation (PI: Sanapo), and by grants from the national heart lung and blood institute (R01HL157288, PI: Bublitz; R01 HL130702, PI: Bourjeily).

Glossary of terms

AHI

apnea-hypopnea index

BMI

body mass index

CI

confidence interval

CPAP

continuous positive airway pressure

ICD

international classification of diseases

LBW

low birthweight

LGA

large for gestational age

MD

mean difference

NOS

Newcastle-Ottawa scale

OR

odds ratio

OSA

obstructive sleep apnea

RDI

respiratory disturbance index

SDB

sleep disordered breathing

SGA

small for gestational age

Footnotes

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

1

Figure S1. Publication bias assessment for studies using subjective methods.

NIHMS1945909-supplement-1.pdf (120.5KB, pdf)
2

Figure S2. Publication bias assessment for studies using objective methods.

NIHMS1945909-supplement-2.pdf (674.2KB, pdf)
3

Figure S3. Obstructive sleep apnea diagnosed by sleep test and mean difference in birthweight. Forest plot including only the studies defining obstructive sleep apnea by apnea-hypopnea index values of five or above events per hour.

NIHMS1945909-supplement-3.pdf (762.5KB, pdf)
4

Figure S4. Obstructive sleep apnea diagnosed by sleep test and mean difference in birthweight. Studies of figure S3 are divided in two subgroups, based on the scoring system used. Subgroup 1: no scoring system specified. Subgroup 2: studies using the 2007 American Academy of Sleep Medicine criteria.

NIHMS1945909-supplement-4.pdf (1.1MB, pdf)
5

Table S1. Search Strategy

NIHMS1945909-supplement-5.docx (26.5KB, docx)
6

Table S2. Inclusion and exclusion criteria

NIHMS1945909-supplement-6.docx (13.6KB, docx)
7

Table S3. Characteristics of the studies using subjective methods to identify maternal sleep disordered breathing.

NIHMS1945909-supplement-7.docx (70.3KB, docx)
8

Table S4. Characteristics of the studies using objective methods to identify maternal sleep disordered breathing.

NIHMS1945909-supplement-8.docx (92.6KB, docx)
9

Table S5. Characteristics of the studies using international classification of diseases codes to identify maternal sleep disordered breathing.

NIHMS1945909-supplement-9.docx (32.5KB, docx)

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