The influence of socioeconomic status on stillbirth risk in Sweden

Olof Stephansson, Paul W Dickman, Anna LV Johansson and Sven Cnattingius

Department of Medical Epidemiology, Karolinska Institutet, Stockholm, Sweden.

Olof Stephansson, Department of Medical Epidemiology, Karolinska Institutet, PO Box 281, SE-171 77 Stockholm, Sweden. E-mail: olof.stephansson{at}mep.ki.se

Abstract

Background Low socioeconomic status (SES) is generally associated with increased risk of stillbirth, but the mechanisms have rarely been investigated. Our aim was to study the association between SES and risk of stillbirth, and to assess whether any differences in risk are mediated by other maternal socio-demographic or anthropometrical characteristics, differences in lifestyle, or attendance at antenatal care.

Methods Population-based individually-matched case-control study including 702 cases of stillbirth and 702 controls among Swedish primiparous women giving birth 1987–1996. We estimated the risk of stillbirth, and subgroups of stillbirth, for various categories of SES. Odds ratios (OR) with 95% CI, estimated by conditional logistic regression, were used to approximate the relative risk. The estimates were adjusted for maternal age, height, body mass index, cigarette smoking, and when necessary mother's country of birth.

Results Compared with women who were high level white-collar workers, the adjusted risks of stillbirth were as follows: unskilled blue-collar workers, 2.2 (95% CI : 1.3– 3.7), skilled blue-collar workers, 2.4 (95% CI : 1.3–4.1), low level white-collar workers, 1.9 (95% CI : 1.2–3.2), and intermediate level white-collar workers 1.4 (95% CI : 0.9–2.4). These risks were not substantially changed when we further adjusted for attendance at antenatal care, previous reproductive history, or excluded pregnancies with maternal diseases, and pregnancy-related disorders. Low social class was most associated with risks of term antepartum and intrapartum stillbirths.

Conclusions Low SES increases the risk of stillbirth. The association could not be explained by any of the factors we studied, and the underlying reasons remain unclear.

Keywords Stillbirth, socioeconomic status, maternal occupation, risk factors, pregnancy

Accepted 4 April 2001

An inverse relation between social class and stillbirth rates was reported by Baird 55 years ago.1 Most of the relatively few recent studies specifically focusing on stillbirth have demonstrated an increased risk of stillbirth with low socioeconomic status (SES),2–8 whereas others have not.9 However, many of these studies are register-based with census data for SES,3,4,6,8,9 and have included few co-variates in order to understand the reasons for the increase in risk.7

In this large population-based case-control study of stillbirth, we have used extensive information about maternal and pregnancy characteristics, recorded prospectively during pregnancy. The objective of this study was to investigate the association between SES and risk of stillbirth, and to possibly explain why social differences increase risk of stillbirth. Because stillbirth is not a homogeneous concept,5 we furthermore wanted to study the association between SES and risk in different subgroups of stillbirth.

Materials and Methods

Description of sample
From the population-based Swedish Medical Birth Register,10 we obtained information on all single births to primiparous women living and giving birth within a geographically defined area in central Sweden from 1987 through 1996. Of 220 712 births, there were 725 stillbirths (cases) occurring at >=28 weeks of gestation. For each case, we randomly selected two controls, matched by year of birth and delivery hospital. Using the unique national registration number assigned to all Swedish residents, the standardized antenatal and obstetric records were retrieved from each of the 25 delivery hospital archives and examined by one of us (OS) using a structured protocol. Of the 725 eligible cases, information on 702 (97%) was obtained: ten cases were missing in the archives, eight were incorrectly coded for delivery hospital, and five had an incorrect national registration number and were therefore impossible to trace. As for the controls, the second control was included only if the first selected control was not found. In order to obtain an equal number of cases and controls (n = 702), 25 second controls were included: 24 of the first controls were missing in the archives and one had an incorrect national registration number (retrieval rate of first controls 96%). Four cases and 2 controls had not attended antenatal care, and 12 cases and 4 controls did not have complete antenatal records.

Information for antenatal records is prospectively recorded from the first to the last antenatal visit. From registration for antenatal care we obtained information about maternal height, weight, number of previous miscarriages, induced abortions, ectopic pregnancies, occupation, cigarette smoking, years of involuntary childlessness, and gestational date at admission to antenatal care. History of maternal diseases at registration was noted and classified according to the Swedish version of the International Classification of Diseases, Ninth Revision (ICD-9), which was used during the study period.11 Information about expected date of delivery and gestational age at admission to antenatal care was calculated from the second trimester ultrasound examination (generally before 19 gestational weeks) when available (94% of cases and controls), otherwise the date of last menstrual period was used. Information on maternal country of birth was obtained from the Swedish Medical Birth Register.

Information on occupation was classified according to the Swedish Socio-economic Classification,12 and grouped as: unskilled and skilled blue-collar workers, low, intermediate and high-level white-collar workers, and others (self-employed n = 12, students n = 116 [comprehensive school n = 21, upper secondary school n = 31, post-secondary school n = 30 and unspecified n = 34] and not in labour force n = 54). Country of birth was categorized as Nordic (Sweden, Norway, Denmark, Finland and Iceland) or Non-Nordic. Body mass index (BMI) at registration to antenatal care was calculated as weight (kg) divided by height (m2). Women were categorized as lean (BMI <20.0), normal (BMI 20.0–24.9), overweight (BMI 25.0–29.9), or obese (BMI >=30.0). Maternal smoking was categorized as no daily smoking, 1–9 cigarettes per day, or >=10 cigarettes per day. First attendance at antenatal care was grouped as before week 13, weeks 13–15, and weeks 16 onwards. Number of visits to antenatal care until gestational week 24 was categorized as <=2, 3–6, and >6 visits. History of miscarriages, induced abortions and ectopic pregnancies were grouped as no event or at least one event. Involuntary childlessness was categorized as <1 year, 1–2 years, and >=3 years. Maternal diseases were grouped into pregestational diabetes, essential hypertension, other chronic diseases and infectious diseases.

During pregnancy, we obtained information about maternal blood pressure, proteinuria, blood glucose level, glucosuria, 75-g oral glucose tolerance test (when performed), and pregnancy complications. Pre-eclampsia and eclampsia were defined according to the criteria given by the National High Blood Pressure Education Program Working Group Report on High Blood Pressure in Pregnancy.13 Mild pre-eclampsia was defined as gestational hypertension (blood pressure of >=140/90 mmHg in >=2 readings >=6 h apart, occurring after 20 weeks of gestation) accompanied by mild or moderate proteinuria (two urinary dipsticks with 1+ or 2+, or 300 mg-3 g of protein in a 24-h urine collection). Severe pre-eclampsia was defined as gestational hypertension accompanied by severe proteinuria (two urinary dip sticks with 3+ or >=3 g of protein in a 24-h urine collection) or gestational hypertension with a diastolic blood pressure >=110 mmHg (in >=2 readings >=6 h apart), regardless of proteinuria. Eclampsia was defined as seizures in a patient with pre-eclampsia that could not be attributed to other causes. Gestational diabetes was defined as having a fasting blood glucose level >=6.7 mmol/l, or a 75-g oral glucose tolerance test value of >=9 mmol/l after 120 min. If blood glucose at any time during pregnancy exceeded 6.5 mmol/l, we defined this as suspect gestational diabetes. From the obstetric and paediatric records we obtained information about maternal age at delivery, gestational age at birth, and gestational age at time for diagnosis of antepartum death. Stillbirths were classified as antepartum or intrapartum, and preterm or term. Preterm birth was defined as gestational age less than 37 completed weeks.

The study was approved by the Research Ethical committee at Karolinska Institutet, Stockholm, Sweden.

Statistical analysis
We used standard statistical methods for the analysis of matched case-control studies, namely conditional logistic regression models estimated using SAS PROC PHREG.14 The data were individually matched, but some matched pairs had identical values for the matching variables. We therefore analysed the data as if they were N:M matched, i.e. each stratum contained N controls and M cases where neither N or M were necessarily 1. All 702 controls were eligible for the analysis, but were only included if they belonged to a stratum that contained at least one case. For each model, observations with missing values for explanatory variables were excluded from the analysis, although the corresponding matched case or control was included in the analysis if the stratum contained at least one case and one control with full covariate information. The number of observations excluded due to missing values was small (Table 1Go). In the multivariable models we initially included all variables. Maternal age, BMI, height and smoking have previously been shown to be independently associated with risk of stillbirth,15 and were therefore included in all final models. In addition, the final models also included other variables associated with the outcome (P < 0.1) in the multivariable model. Odds ratios (OR) with 95% CI were used to estimate the relative risk.


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Table 1 Characteristics of primiparous women with stillbirths and matched controls, crude odds ratios (OR), and 95% CI for risk of stillbirth, in Sweden 1987–1996
 
Results

Compared with high level white-collar workers, unskilled and skilled blue-collar workers, low level white-collar workers, and women in the ‘others’ group were at increased risk of stillbirth in the univariate analysis (Table 1Go). The risk of stillbirth increased with maternal age, BMI and cigarette smoking, and was also increased for women born outside the Nordic countries, women with >=3 years of involuntary childlessness, diabetes mellitus, severe pre-eclampsia or eclampsia. The risks of stillbirth related to short stature, few visits to antenatal care, and suspect gestational diabetes were of borderline significance. There was no increase in risk of stillbirth associated with late attendance at antenatal care, previous miscarriages, induced abortions, ectopic pregnancies, essential hypertension, other chronic or infectious diseases, or among women not living with the baby's father (data available on request).

High maternal age at first birth (>=35 years) was less common among blue-collar workers compared with high level white-collar workers (5% and 18%, respectively). Among unskilled blue-collar workers, 36% were daily smokers, while the corresponding figure among high level white-collar workers was 13%. Blue-collar workers generally had shorter stature and higher BMI compared to medium or high level white-collar workers. Compared to blue-collar workers, intermediate and high level white-collar workers had higher rates of involuntary childlessness, and also more visits to antenatal care (data available on request).

When we first adjusted for age, the risk of stillbirth related to low SES increased, and the OR for unskilled and skilled blue-collar workers compared with high level white-collar workers were 2.6 (95% CI : 1.7–4.2), and 2.3 (95% CI : 1.4–3.8) respectively (Table 2Go). When adjustments also were made for country of birth, BMI, height and smoking, some risks decreased, but were still higher than in the univariate analysis. In additional analyses, we also included number of visits to antenatal care and involuntary childlessness, and also excluded pregnancies with pregestational and gestational diabetes, pre-eclampsia or eclampsia, which only had minor influence in social risks of stillbirth. There were no major differences in the distribution of missing data for the variables used in the multivariate models with regard to SES (data available on request).


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Table 2 Socioeconomic status (SES) and adjusted odds ratios (OR) for stillbirth, in Sweden 1987–1996
 
When we performed analyses on the associations between SES and risk of fetal death in subgroups of stillbirths, we collapsed information about SES into three groups (Table 3Go). The risk of preterm antepartum stillbirth was slightly increased among women in the low SES group, although the result did not reach statistical significance, which may be due to the reduced sample size. Compared to the high SES group, the low SES group was at increased risk of term antepartum and intrapartum stillbirth.


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Table 3 Socioeconomic status (SES) and adjusted odds ratios (OR) for different categories of stillbirth, in Sweden 1987–1996
 
Discussion

The results from this study suggest a more than twofold increase in risk of stillbirth for women with the lowest SES compared with the highest. The increase in risk related to low social class was even higher for intrapartum and term antepartum stillbirths. Although we investigated an extensive number of maternal and pregnancy characteristics, we could not explain the increase in risk of stillbirth related to low social class.

This large population-based study included more than 700 cases and controls with a high retrieval rate (96–97%) of the medical records. Recall bias is almost inconceivable as exposure information was collected prospectively throughout pregnancy, thus before the outcome studied. We investigated primiparous women with singleton pregnancies and the conclusions can only be interpreted for this group. We were restricted to data found in the archive files, and could not study other potential covariates such as energy intake and expenditure, infections, the use of drugs other than tobacco, or the level of stress and physical strain during pregnancy. There were missing data for some of the variables used in the multivariate analyses. However, as the distribution of missing data was independent of social class, we have no reason to believe that this would have influenced the findings on the risk of stillbirth. Information on cigarette smoking was reported at the first visit to antenatal care, prior to the outcome, but we do not know whether reliability of self-reported smoking differs with regard to social class. Women from low social classes are more likely to continue to smoke during pregnancy compared to women from high social classes.16 Thus, residual confounding due to social differences in smoking cessation rates during pregnancy cannot be excluded. Another potential bias in this study is the risk of overmatching on delivery hospital. As the distribution of social class varies between hospital referral regions, an increased proportion of women of low SES may have been selected as controls. However, this potential bias would lead to an underestimation of the true association between SES and risk of stillbirth.

Increasing maternal age is a well-established risk factor for stillbirth, especially among primiparous women.17–19 Because women of low SES generally were of lower maternal age than women of high SES, risk of stillbirth related to a low SES increased when we adjusted for maternal age. We believe that an age-adjusted risk is the most accurate measurement of stillbirth risk related to low social class.

The present data permitted us to investigate whether the risk of stillbirth related to social class was mediated by differences in maternal demographic factors, anthropometric characteristics, smoking habits, whether the mother was living with the baby's father, reproductive factors, chronic diseases, pregnancy-related disorders, or compliance with antenatal care. We could however, only explain a small part of the more than twofold age-adjusted risk increase in stillbirth among blue-collar workers compared with high level white-collar workers.

The prevalence of cigarette smoking and high BMI increased with decreasing SES. In the present study, both smoking and high BMI were associated with an increased risk of stillbirth, which is in accordance with previous findings.5,18,20,21 However, when cigarette smoking and high BMI were included in the multivariate analysis they only accounted for a minor part of the increase in risk of stillbirth for women of low SES.

Our finding that term antepartum and intrapartum stillbirths were those deaths most associated with low social class is important, as these may have been the most potential preventable stillbirths. These increases in risk may be due to social differences in acting on signals of a pathological pregnancy, such as seeking care due to reduced fetal movements. Another possibility is that the quality, quantity or content of medical care may be affected by SES.22 On average, intermediate and high level white-collar workers had more visits to antenatal care compared with women of low SES. Although number of visits to antenatal care was not associated with stillbirth risk in the multivariate analyses, one can only speculate whether midwives and doctors may be more likely to understand subtle worrying signs from women of their own social class than from women of lower classes. In this study we were unable to investigate other more direct measures of quality of care, such as number of ultrasound investigations for suspected fetal growth retardation, number of referrals to hospitals or specialists, or supervision of asphyxia during labour.

What other mechanisms may then mediate the increased risk of stillbirth among women of low social class? In 1955, it was reported that primiparous women in Aberdeen, Scotland, who rose in social status at marriage were taller, healthier, and had lower rates of perinatal deaths, and vice versa.23 Illsley argues that this selective interchange between social classes at marriage may obscure the effects of social levelling.23 The causes of social differences in pregnancy outcome may lie in the environmental circumstances in which the mother grew up, acting as a cohort effect.24,25 Thus, disadvantaged mothers were borne by mothers who were similarly disadvantaged, and further improvement of perinatal health is dependent on the elimination of this continuity of social disadvantage. Rutter et al.26 explain social inequalities in pregnancy outcomes by material deprivation, which is due to an increase in negative life events with a lack of support and by a reduced level of education and access to information. Thus, women with low SES have increased emotional problems including stress, anxiety, depression and lowered self-esteem, as well as cognitive problems. The association between stress and stillbirth is not known, but psychological, emotional and job stress in pregnancy have been associated with preterm delivery,27 increased risks of malformations,28 and possibly also spontaneous abortion.29,30 In the present study we were unable to investigate the influences of stress and physical strain on stillbirth risk.

In summary, we found that the risk of stillbirth was markedly increased for women of low SES, despite our ability to control for a large number of covariates. This implies that there are substantial unexplained social differences in stillbirth risk in Sweden, a country where the population is regarded as relatively homogeneous, and where pregnant women should have equal opportunities to receive free antenatal and obstetric care. The finding that low social class was most associated with term antepartum and intrapartum stillbirths, which may be regarded as potential preventable deaths, suggests that the quality of care may differ with social class. From this study, we conclude that women of low social class may need more attention, support and observation at antenatal and obstetric clinics during pregnancy and labour.


KEY MESSAGES

  • Low socioeconomic status (SES) increases risk of stillbirth in Sweden.
  • Low SES is most associated with term antepartum and intrapartum stillbirth.
  • The increased risks cannot be explained by social differences in maternal age, height, body mass index (BMI), cigarette smoking or country of birth.
  • The reasons for the increased risk remain to be determined.

 

Acknowledgments

This study was funded by grants from The Swedish Council for Social Research (Project FO265/1998), and Karolinska Institutet.

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