The Probability of Giving Birth among Women Who Were Born Preterm or with Impaired Fetal Growth: A Swedish Population-based Registry Study

K. Ekholm1, J. Carstensen2, O. Finnström3 and G. Sydsjö1

1 Division of Obstetrics and Gynecology, Department of Molecular and Clinical Medicine, Faculty of Health Sciences, Linköping University, Linköping, Sweden
2 Department of Health and Society, Linköping University, Linköping, Sweden
3 Division of Pediatrics, Department of Molecular and Clinical Medicine, Faculty of Health Sciences, Linköping University, Linköping, Sweden

Correspondence to Katarina Ekholm, Division of Obstetrics and Gynecology, Department of Molecular and Clinical Medicine, University Hospital, SE-581 85 Linköping, Sweden (e-mail: katarina.ekholm{at}lio.se).

Received for publication September 9, 2004. Accepted for publication December 2, 2004.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The primary aim of this study was to investigate whether women born prematurely or with impaired fetal growth have a reduced probability of giving birth. Using Swedish population-based registries, the authors identified 148,281 women born in 1973–1975 for follow-up until 2001. Of these women, 4.1% were born preterm and 0.32% very preterm, 0.29% were born with a very low birth weight, and 5.4% were small for gestational age. Outcome measures were the hazard ratios for giving birth during the study period. Adjustments were made for socioeconomic factors. Very-low-birth-weight women displayed a reduced probability of giving birth (hazard ratio = 0.74, 95% confidence interval: 0.60, 0.91), most apparent among women aged 25 or more years. There were also tendencies of reduced hazard ratios of giving birth among women born preterm or very preterm in this age interval. Women born small for gestational age (below –2 standard deviations) seemed to be more likely to have given birth (hazard ratio = 1.09, 95% confidence interval: 1.04, 1.14), but when a more extreme group of small-for-gestational-age women (below –3 standard deviations) was defined, the association was less evident (hazard ratio = 1.04, 95% confidence interval: 0.94, 1.16). The results suggest that very-low-birth-weight women and, possibly, women born preterm or very preterm have a reduced probability of giving birth, while the results regarding small for gestational age are less clear.

infant, small for gestational age; infant, very low birth weight; premature birth; registries; reproduction; women


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Preterm birth and impaired fetal growth seem to be associated with several long-term consequences. Preterm children and children with very low birth weights have higher rates of neurosensory impairment, lower mean intelligence quotient, and poorer school performances compared with normal birth weight controls during school age and early adulthood (1Go–5Go). Low birth weight, a crude marker of impaired fetal growth, seems to be associated with an increased risk of hypertension, type 2 diabetes and, to some extent, obesity and cardiovascular disease in women (6Go–14Go).

Intrauterine growth restriction and preterm birth can alter organ structure and functioning (15Go, 16Go). Researchers have speculated about a connection between impaired fetal growth and risk of reduced fertility in women (17Go, 18Go). The primary aim of this study was to investigate if prematurely born women and women born with impaired fetal growth have a subsequently reduced probability of giving birth. In addition to biologic factors, other factors of importance must be considered when investigating the probability of giving birth. These include factors related to lifestyle and socioeconomic status (19Go–23Go), some of which seem to be related to impaired fetal growth and premature birth (24Go–28Go). Swedish population-based registries provide a unique opportunity to study the effect of birth-related variables on the probability of giving birth. By use of population-based registries, we retrieved information on socioeconomic characteristics to include in the analyses.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The Swedish Medical Birth Registry was established in 1973 and covers approximately 99 percent of all births (29Go). The registry continuously receives information on births, including previous reproductive history, as well as complications during pregnancy, delivery, and the neonatal period. The Total Population Register contains information on births, deaths, and marital status, as well as on migration and country of origin for Swedish residents born abroad (30Go). The Causes of Death Register records information on all deceased persons registered in the country at the time of death (31Go) and, by use of the Multi-Generation Register (32Go), it is possible to identify the parents of the children registered in the Medical Birth Registry and the Total Population Register. Information on the educational level of the study population and their parents was retrieved from the Education Register (33Go) and the Population and Housing Census 1970 (34Go).

A total of 155,494 female births were registered in Sweden during the years 1973, 1974, and 1975 according to both the Medical Birth Registry and the Total Population Register. Information available in the other registries (presented above) was retrieved by use of the infant's or mother's unique personal identification number. Women who were alive and still living in Sweden at 13 years of age served as the study population (n = 150,425). Women with missing values on birth weight and gestational length (n = 1,029) were excluded, as were those with extremely high birth weights compared with the length of gestation (n = 126). We excluded those born in the gestational week of less than or equal to 28 with birth weights more than 2,000 g and those with a gestational length of 29 or 30 weeks whose birth weights were more than 2,500 g. Women with gestational lengths of 31 or 32 weeks who weighed more than 3,000 g were also excluded, as were those who weighed more than 3,500 g and were born in week 33 or 34. In 48 cases, the mothers of the studied women could not be identified, and in 956 cases, the fathers. The final cohort therefore consisted of 148,281 index women who could be followed until 2001 with respect to the cumulative incidence of giving birth to one child or more during the study period.

"Preterm birth" was defined as less than 37 completed weeks' gestation, and "very preterm birth" was defined as less than 32 completed weeks. "Very low birth weight" was defined as a birth weight of less than 1,500 g, and "small for gestational age" was defined as a birth weight of less than 2 standard deviations below the mean weight for the gestational length according to the Swedish standard (35Go). The growth curves used are based on ultrasound estimations of fetal weight and were calculated in 1996. As the mean birth weight among girls born in Sweden was about 50–60 g lower when the index women were born (36Go), the results including small for gestational age were validated by accounting for this mean increase in birth weight. This was done by computing a birth weight adjusted for the weight gain among all newborn female children registered in the Medical Birth Registry (36Go) between 1973–1975 and 1996 (i.e., when the growth curves were calculated). We subtracted the mean weight among all female children born in 1973, 1974, and 1975, respectively, from the mean weight among all female children born in 1996 and added these differences in weight to the original birth weights in our study cohort. These adjusted weights were then used to calculate an adjusted small for gestational age, which was analyzed in the same way as the original variable. The results of these analyses did not differ substantially from the ones presented. The growth curves used were based on singleton births, but we used them for twin births as well. As postnatal small-for-gestational-age standards exist that are specially designed for multiple births, it was possible to validate the results concerning small for gestational age by using one of the small-for-gestational-age standards on the twins in this study (37Go). Again, the results of these analyses did not differ substantially from the ones presented.

Information on socioeconomic background characteristics of both the index women and their parents was retrieved from the registries, as socioeconomic characteristics have been shown to be related to both the exposures (24Go, 25Go, 27Go, 28Go, 38Go) and the main outcome of this study (21Go, 22Go). There also seems to be an association between birth weight and subsequent educational levels and marital status (3Go, 4Go, 39Go, 40Go). The variables were tested as potential confounders both individually (table 1) and simultaneously before being included in the analyses. All parental background variables were measured in 1970, which is close to the time of the index women's births. Data on the index women's socioeconomic characteristics were collected when the women in the study cohort were aged 25 years. The educational levels of both the parents and the index women were coded according to the Swedish educational system: elementary school (9 or 10 years of education), high school (11–13 years), and graduate and postgraduate education (14 years or more). Information on the parents' country of origin was coded to indicate if at least one of the parents had been born outside the Nordic countries or if both parents had been born in the Nordic countries. The marital status of the mothers was coded as married, unmarried, and divorced or widowed, and the marital status of the index women was coded as unmarried or married. The mothers' parity at the time of giving birth to the index women was split into two categories: no previous children and one or more previous children; and the mothers' age was split into four categories: 13–19, 20–26, 27–33, and 34 years or more. The year of birth of the index women and the classification of the birth as twin birth or not twin birth were also included as background variables.


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TABLE 1. Birth characteristics and probability of giving birth before the year 2001 in relation to the background characteristics of Swedish index women born in 1973–1975*

 
Information on the educational levels of the mother and the father was missing for 16,163 and 10,234 index women, respectively. The parents of index women for whom data on the educational level in 1970 were missing were younger and born outside the Nordic countries to a significantly greater extent (p < 0.001). Therefore, the groups for which values were missing were added as separate categories in the analyses. Missing values on other background variables (<1 percent on each variable) were assigned to the largest category on each variable.

Statistical analyses
The effects of parental background variables on the index women's birth characteristics (i.e., preterm birth, very preterm birth, very low birth weight, and small for gestational age) were estimated through multiple logistic regression analysis. The odds ratios were adjusted for all parental background variables in the study. All variables were treated as categorical. Multiple logistic regression analysis was also used when the relations between the birth characteristics and subsequent educational level and marital status of the index women were analyzed. The effects of the background variables of both the parents and the index women on the index women's probability of giving birth during the study period were estimated using Cox's proportional hazards model. The hazard ratios were adjusted for all background variables included in the models.

The data were also modeled through Cox's proportional hazards model to estimate the effect of the index women's birth characteristics (i.e., preterm birth, very preterm birth, very low birth weight, and small for gestational age) on subsequent probability of giving birth. The time dimension in the models was defined as age. Subjects exited from risk when they gave birth to the first child, emigrated for the first time, died, or reached the end of follow-up, whichever took place first. During the study period, 6,307 (4.3 percent) of the index women were censored from the analyses because of emigration; the corresponding number of deceased was 427 (0.3 percent). Crude and adjusted hazard ratios and 95 percent confidence intervals were calculated for each analysis. Adjustments were made for the socioeconomic background variables of the parents, as well as for the year of birth of the index women and whether or not the index women were born as a result of twin birth. The twin group is problematic because the individuals in this group are statistically dependent. As the effect of this nonindependence on the results is minor, we did not account for this in the analyses. Since the index women's own educational levels and marital status were measured at 25 years of age, we included these variables only in the last stratum of the analyses in which the time variable was stratified in three strata: 13–19 years, 20–24 years, and 25 years or more.

Two-way interaction terms between the four birth characteristics and the background variables were created to evaluate the models. The interaction terms were determined by means of forward stepwise regression. The data were also checked for proportionality by creating interaction terms between the time variable and each of the four birth characteristics.

This study was approved by the Human Research Ethics Committee, Faculty of Health Sciences, Linköping University.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Of the index women, 6,071 (4.1 percent) were born preterm, 474 (0.32 percent) were born very preterm, 436 (0.29 percent) were born with very low birth weight, and 7,942 (5.4 percent) were small for gestational age. All parental background variables were associated with the birth characteristics of the index women (table 1). When the effects of parental background variables were estimated simultaneously, they were all significantly associated with the occurrence of being born small for gestational age (data not shown). Preterm birth and very preterm birth were related to all parental background variables except for the educational level of the father, whereas only the mother's marital status, parity, and age were associated with the occurrence of very low birth weight among the index women. Being born as a result of twin birth was related to the birth characteristics of the index women, while year of birth seemed to be related only to preterm birth (table 1).

Index women who were born preterm, very preterm, small for gestational age, or with a very low birth weight had reached, at the age of 25 years, the highest level of education (i.e., ≥14 years) to a lesser extent than had women born at term or whose intrauterine growth was not affected (table 2). However, the birth characteristics of the index women did not influence the probability of being married at the age of 25 years.


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TABLE 2. Birth characteristics in relation to the Swedish index women's educational level and marital status at the age of 25 years for those born in 1973–1975*{dagger}

 
Among the women in the study cohort, 41,038 had given birth to one child or more before the year of 2001, and the cumulative incidence of giving birth was 30.2 percent, adjusted for the mortality and emigration among the index women. All parental background variables were associated with the probability of giving birth by the index women (table 1). When analyzed simultaneously, they were all significantly associated with the index women's probability of giving birth during the study period (table 3), as were the educational level and marital status of the index women (data not shown).


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TABLE 3. Background characteristics in relation to the Swedish index women's probability of giving birth during the study period from their birth in 1973–1975 until 2001*

 
In table 4, the effects of birth characteristics on the index women's probability of giving birth during the period of study are presented. The hazard ratio of giving birth to one child or more during the study period was 25 percent lower among index women born with a very low birth weight than among women with higher birth weights. Adjustments for parental socioeconomic characteristics did not markedly change the results. Neither preterm birth nor very preterm birth was significantly associated with the probability of giving birth during the study period. On the other hand, index women born small for gestational age had a significantly higher hazard ratio for giving birth during the period of study than did women born at a size appropriate for gestational age.


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TABLE 4. Birth characteristics in relation to the Swedish index women's probability of giving birth during the study period from their birth in 1973–1975 until 2001*

 
Validation of the models containing the four birth characteristics mentioned above (i.e., preterm birth, very preterm birth, very low birth weight, and small for gestational age) showed no evidence of significant interactions between the parental socioeconomic background variables and the studied birth characteristics. There was, however, a negative interaction between very low birth weight and twin birth (p = 0.050). Thus, the analyses concerning the very-low-birth-weight women presented in table 4 were also performed separately for singletons and twins. Very-low-birth-weight women still had significantly reduced hazard ratios for giving birth during the period of study, irrespective of whether or not the women were results of twin births. Although the adjusted hazard ratio for twins (hazard ratio = 0.37, 95 percent confidence interval: 0.18, 0.78) was lower than that for singletons (hazard ratio = 0.80, 95 percent confidence interval: 0.65, 0.99), there was no significant difference between these two groups of index women. Therefore, we decided not to separate twins and singletons in the analyses presented.

The model validation also revealed that the assumption of proportional hazards could not be met in all of the models. The hazard ratios decreased significantly by time for preterm birth (p < 0.001) and very low birth weight (p = 0.005), and tendencies in the same direction were seen for very preterm birth (p = 0.053) and small for gestational age (p = 0.11). The results of these analyses, together with the fact that the index women's own educational levels and marital status were measured at the age of 25 years, concluded in a stratification of the time variable into three groups, as shown in table 5. Table 5 demonstrates that the reduced probability of giving birth among very-low-birth-weight women was significant only in the last time stratum (i.e., among index women aged 25 years or more). In this stratum, there were also tendencies of reduced hazard ratios of giving birth among index women born preterm and very preterm. However, index women born small for gestational age still had a significantly higher probability of giving birth than did women born appropriate for gestational age, and this was evident in all three time strata. In order to better understand the results concerning this variable, we created a more extreme group of small-for-gestational-age women. The new variable was defined as a birth weight below –3 standard deviations of the Swedish standard (35Go), and the results of this additional classification are presented in table 6. Index women who were categorized in this more extreme group did not have a higher probability of giving birth during the period of study. On the contrary, there were tendencies toward a decrease in the probability of the outcome when stratifying the time variable, although none of the corresponding p values reached statistical significance.


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TABLE 5. Birth characteristics in relation to the Swedish index women's probability of giving birth during the study period from their birth in 1973–1975 until 2001, stratified by time*

 

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TABLE 6. Swedish index women's probability of giving birth during the study period from their birth in 1973–1975 until 2001 among small-for-gestational-age women*{dagger}

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
We found an association between very low birth weight and subsequently reduced probability of giving birth among Swedish women aged 25–27 years. This association was most evident among women aged 25 years or more, at which point there also were tendencies of a reduced probability of giving birth among women born prematurely or very prematurely. Women born small for gestational age seemed to be more likely to have given birth during the whole period of study, but when defining a more extreme group of small-for-gestational-age women, we found the association to be less clear. Consistent with previous Swedish studies (24Go, 25Go, 27Go, 28Go, 38Go), this study, also, found that parental socioeconomic characteristics were associated with the birth weight and gestational length of the children (index women). Low socioeconomic status of both the index women and their parents increased the probability of giving birth, as was found in previous studies (21Go, 22Go). As stated in other studies (3Go, 4Go), our study found that very low birth weight, small for gestational age, and moderately and very preterm birth were negatively related to subsequent educational levels. Low birth weight has previously been shown to be associated with subsequent marital status in men but not in women (39Go, 40Go). In this study, no connection between birth weight or gestational length and marital status at the age of 25 years was found.

The women in the present study were identified and followed up through population-based registries that are known to provide standardized and reliable data. Although the precision of the birth weights registered in the Medical Birth Registry is generally good (29Go), approximately 9 percent of the very low birth weights are wrongly entered, and these infants are also slightly underestimated in the registry (41Go). The analyses of preterm and very preterm birth may involve some errors as the estimations of gestational length at delivery were less precise in 1973–1975 (29Go), which is before the method of dating pregnancies by ultrasound examination came into use. We tried to reduce the errors by excluding individuals with extremely high birth weights compared with the length of gestation.

Another limitation of this registry study is the restricted number of possible confounding variables that can be controlled for. We were not able to investigate the effects of factors such as smoking and adult weight in the analyses, as these variables were not present in the Medical Birth Registry in 1973–1975. In addition, it is not possible to retrieve information from the registries used concerning factors such as whether or not the women were cohabiting. In the analyses, adjustments were made for parental socioeconomic factors, and some analyses were also adjusted for the index women's own educational level and marital status. At the age of 25 years, all women had theoretically been able to reach the highest category of educational attainment, and assessing the educational level when the index women were younger would have led to less informative and accurate data. The same holds true for the index women's marital status. The disadvantage in retrieving the educational level and marital status of the index women relatively late during the period of study is that it is more difficult to adjust for these variables in the analyses because of the possible bias due to reversed causality (e.g., the educational level could affect the probability of giving birth, but giving birth before age 25 could also affect the educational level at 25 years). Thus, these variables were adjusted for only when investigating index women aged 25 years or more.

Although controlling for the socioeconomic characteristics of the parents probably restricted the impact of confounding by other factors, such as the ones mentioned above, it is possible that the limited information on the index women's own socioeconomic characteristics may lead to residual confounding. This could, perhaps, be one explanation for the observed increased probability of giving birth among women born small for gestational age, as small for gestational age seems to be associated with socioeconomic characteristics to a greater extent than the other birth characteristics studied (table 1). The association between small for gestational age and subsequent probability of giving birth persisted, even after the results regarding small for gestational age were validated by adjusting for the mean increase in birth weight between 1973–1975 and 1996 and by using separate standards for twins and singletons. However, when a more extreme group of small-for-gestational-age women was created, the positive association was no longer present. Instead, the results followed the same pattern as the analyses made on the other birth characteristics.

The Medical Birth Registry was established in 1973, which makes the follow-up period relatively short when estimating the probability of giving birth. We were able to follow up the study population until 2001, at which point the women were 25–27 years of age. The mean age of giving birth to the first child among Swedish women in the year of 2000 was 27.7 years (36Go). Given the relatively short follow-up period, it is theoretically possible that women born prematurely or with very low birth weights postpone their pregnancies but eventually will have the same number of children as women born with higher birth weights or longer lengths of gestation. However, the model validation showed that the hazard ratios decreased significantly by time (i.e., age) when analyzing women born preterm and with very low birth weights, and tendencies in the same direction were seen for women born very preterm and for those born small for gestational age. This implies that a longer follow-up period could yield greater differences between the exposed and unexposed women in the groups mentioned.

A recent study showed that fewer very-low-birth-weight women than controls had had intercourse, been pregnant, or delivered a liveborn infant at the age of 20 years, even when controlling for sociodemographic status (4Go). They also displayed a lower use of alcohol and drugs. Thus, the potentially postponed pregnancies could be related to differences in behavioral factors.

Impaired fetal growth can alter organ structure and functioning (15Go), and it is plausible that it also affects the reproductive organs. Studies on adolescent girls have shown that there seems to be a connection between being born small for gestational age and subsequent risk of reduced fertility (17Go, 18Go), but our findings do not support such an association. These differences in the results may arise because our study was population based, unlike the studies made by Ibanez et al., and because of differences in the definition of small for gestational age. In addition, we estimated the probability of giving birth, whereas Ibanez et al. studied factors related to reduced fertility.

In conclusion, the results of this study suggest that women born with very low birth weights and, possibly, women born preterm or very preterm have a reduced probability of giving birth, while the results regarding small for gestational age are less clear. Therefore, further studies with longer follow-up periods are necessary.


    ACKNOWLEDGMENTS
 
This study was supported by grants from the Swedish Council for Working Life and Social Research and the Health Research Council in Southeast Sweden (FORSS).

The authors would like to acknowledge Rolv Skjaerven for help in providing data on postnatal small-for-gestational-age standards for female twins. They would also like to thank the National Board of Health and Welfare and Statistics Sweden for help and access to the registries.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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