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Maternal and fetal risk factors for stillbirth
AbstractObjective To assess the main risk factors associated with stillbirth in a multiethnic English maternity population.Results Multivariable analysis identified a significant risk of stillbirth for parity (para 0 and para 3), ethnicity (African, African Caribbean, Indian, and Pakistani), maternal obesity (body mass index 30), smoking, pre existing diabetes, and history of mental health problems, antepartum haemorrhage, and fetal growth restriction (birth weight below 10th customised birthweight centile). As potentially modifiable risk factors, maternal obesity, smoking in pregnancy, and fetal growth restriction together accounted for 56.1% of the stillbirths. Presence of fetal growth restriction constituted the highest risk, and this applied to pregnancies where mothers did not smoke (adjusted relative risk 7.8, 95% confidence interval 6.6 to 10.9), did smoke (5.7, 3.6 to 10.9), and were exposed to passive smoke only (10.0, 6.6 to 15.8). Fetal growth restriction also had the largest population attributable risk for stillbirth and was fivefold greater if it was not detected antenatally than when it was (32.0% v 6.2%). In total, 195 of the 389 stillbirths in this cohort had fetal growth restriction, but in 160 (82%) it had not been detected antenatally. Antenatal recognition of fetal growth restriction resulted in delivery 10 days earlier than when it was not detected: median 270 (interquartile range 261 279) days v 280 (interquartile range 273 287) days. Stillbirth rates in the United Kingdom are among the highest in high income countries2 and have shown little improvement since the early 1990s.3Despite free availability of postmortem investigations in the English National Health Service as many as 50 70% of stillbirths have until recently been categorised as unclassified or unexplained4 and are, by implication, often considered unavoidable.5 Further investigation found that many stillborn fetuses had failed to reach their growth potential,6 7 8 and inclusion of fetal growth restriction as a category in stillbirth classifications resulted in imitation van cleef gold necklace a substantial drop to around 15% in the proportion of cases considered unexplained.8 9 This encouraged a renewed focus on understanding the underlying, mostly placental disease related, causes of fetal growth restriction. Recent reports of laboratory investigations10 and postmortem studies11 have confirmed the large contribution of placental failure in the cause of stillbirth.The clinical relevance of such findings van cleef alhambra necklace imitation is that although there are limited means by which to treat fetal growth restriction in utero, recognition that the fetus is at risk after appropriate maternal fetal investigations can lead to well timed delivery and improved perinatal outcome.12 13 However, there are currently no established and routinely used means to predict stillbirth, and risk factors known at the beginning of pregnancy are considered weak predictors of outcome.14We investigated the role of demographic, social, and medical risk factors that can be ascertained at the beginning of pregnancy together with those that become apparent as pregnancy progresses, and their respective contributions to the incidence of stillbirths in an NHS region in England with a multiethnic population.15 To focus on potentially avoidable factors we excluded congenital anomalies, as their contribution to stillbirth is contingent on incidence as well as cultural choices on antenatal screening, prenatal diagnosis, and decisions in response to positive results. We therefore explored the risk factors in pregnancies with normally formed singletons and estimated the respective contribution of these factors to the overall burden of stillbirth in our population.MethodsMaternity dataThe database was derived from the regional, NHSnet based perinatal episode electronic record (PEER) hosted and managed by the West Midlands Perinatal Institute.16 This electronic record was first implemented in April 2009 in the 19 maternity units in the West Midlands. For this study we used the data collected over a two year period, representing births between June 2009 and May 2011.The data originated from prospective records created in the standardised hand held maternity notes during pregnancy by the midwives and doctors.17 Trained data clerks in the respective hospitals transfer information from the notes on to the perinatal episode electronic record at the end of pregnancy. Quality was assured by central project staff through training workshops and regular on site data quality audits. The dataset contained 87 regionally agreed and defined data items,18 with information about maternal characteristics, including age, parity, ethnic origin, and maternal height and weight (expressed as body mass index); social factors, including employment status of the mother and her partner, consanguinity with the partner, and index of multiple deprivation; history of mental health problems, pre existing diabetes or hypertensive disease, or previous stillbirth; smoking status, alcohol consumption, non prescription drugs, folic acid intake, and time of first visit in pregnancy (the information for all these previous variables was usually recorded at the early pregnancy booking visit); complications in pregnancy, including gestational diabetes, antepartum haemorrhage, pregnancy induced hypertension, and pre eclampsia (defined as pregnancy induced hypertension with proteinuria); and fetal or neonatal characteristics, including sex, gestational age and weight at birth, and estimated weight during pregnancy. Gestational age was determined on the basis of routinely offered dating scans, which were carried out in the first or second trimester (The presence of intrauterine growth restriction was established on the basis of a birth weight below the 10th weight for gestational age centile, using the gestation related optimal weight standard (GROW),19 with coefficients derived from the West Midlands population. This method defines the fetal growth potential by excluding pathological factors such as smoking and diabetes, and individual adjustment or "customisation" for the baby's sex and the mother's height, weight, ethnic origin, and parity.20 21 A weight that is small for gestational age after such adjustment by growth potential has been shown to represent pathological smallness22 and is referred to as fetal growth restriction. We applied the 10th centile as the cut off, as it is in standard clinical use and has been validated through receiver operator curves as being close to optimal for predicting pathology by customised centiles.23The case notes were also examined for any recording of fetal growth problems. Fetal growth surveillance is usually done by a protocol of measuring fundal height at each antenatal visit in the third trimester, with referral for ultrasound assessment of estimated fetal weight when the serially plotted fundal height measurements do not follow the predicted curve. In pregnancies where assessment of fundal height is difficult (for example, maternal obesity) or where the risk of fetal growth restriction is considered increased (for example, due to obstetric history) serial estimated fetal weight measurements are done according to local protocols of varying scan frequency. Antenatal recognition of fetal growth restriction in pregnancies with birth weights below the 10th customised centile was defined as at least one antenatal entry with this diagnosis, usually based on one or more estimated fetal weights below the 10th customised centile, or an abnormal umbilical artery Doppler, or both. This assessment of the maternity record is part of routine ascertainment, as the proportion of pregnancies with antenatally detected fetal growth restriction is a regionally agreed key performance indicator.Linkage to mortality dataData on fetal, neonatal, and infant deaths and congenital anomalies were notified to the Perinatal Institute by a network of coordinators, and had a consistently high level of ascertainment. The information is held on secure NHS servers and is pseudonymised before any further analysis. Data linkage was established with the electronic maternity database, using the NHS number as unique identifier.Stillbirth was defined as a child born after the 24th week of pregnancy who did not, at any time after delivery, breathe or show any other signs of life. Along the lines of previously applied methods,6 we adjusted the gestational age of each stillborn fetus by deducting two days from the length of pregnancy at delivery, to correct for the estimated 48 hour average delay between intrauterine death and delivery.24Confidentiality and consentMaternal consent was obtained by provision of information and opt out. Mothers are informed at their first antenatal visit about the intention of collection and analysis of secondary data, and this is also explained in text printed in their standardised, hand held pregnancy notes. That this information has been given and explained is recorded in the notes and signed by the midwife. A mother can opt out at any time from her data being used, in which case her NHS number is added to an "opt out register" and further analysis is blocked. The Perinatal Institute's confidentiality and consent protocol has been reviewed and passed as appropriate by UK Connecting for Health, the NHS, and the Information Commissioner.Statistical analysesAfter initial exploratory analysis, we assessed the independent and multiple variable effects of explanatory variables on stillbirths in Poisson regression models. Variables entered in the multivariable analysis are those of known clinical relevance and from previous publications2 14 and included maternal age, parity, ethnic origin, place of birth, body mass index, history of mental health problems, pre existing hypertension, pre existing diabetes, cardiac disease, previous stillbirths, smoking in pregnancy, alcohol consumption, antenatal folic acid intake, late booking (13 weeks), gestational diabetes, pregnancy induced hypertension, pre eclampsia, antepartum haemorrhage, and fetal growth restriction. In addition to the index of multiple deprivation, we included maternal and paternal employment status as social factors in the multivariable analysis. We entered variables using the manual stepwise (forward backward) method. To reduce the over reliance in the estimates and the selection mechanism that may arise due to rarity of stillbirths, we used the bootstrapping approach to calculate standard errors. In the multivariable analysis all variables reaching a 0.05 significance level were retained in the model. We also considered van cleef and arpels earrings fake all two factor interactions between the explanatory variables and used empirical probability plots to check the final model to assess whether the modelling assumptions were met. We carried out sensitivity analyses to assess the influence of factors excluded because of P>0.05, potential clustering by maternity unit, and the effect of repeat pregnancies from the same mother.To assess the proportion of stillbirths that could be potentially prevented if risk factors were removed, we calculated adjusted population attributable risk estimates using standard methods25: population attributable risk=expected number of cases in the populationexpected number of cases if nobody in the population has the risk factor of interest/expected number of cases in the population 100The analyses were done using statistical package STATA version 11.ResultsA total of 105476 cases were entered during the two year collection period. Of these, 13258 were excluded because of congenital anomaly or multiple pregnancy, which left 92218 normally formed singleton pregnancies leading to 91829 live births and 389 stillbirths. This represented a stillbirth rate of 4.2/1000 births and compares with nationally reported stillbirth rates of normally formed singletons of 3.9 4.1/1000 over the same period.26 The analysis included 841 (0.9%) repeat pregnancies during the two year period of the 92218 mothers in the cohort.Univariate analysisTable 1 lists the variables, grouped according to maternal and fetal characteristics, social factors, medical history, and complications during pregnancy. Analysis was for complete cases only. The stillbirth rate is presented for subgroups, together with relative risks and 95% confidence intervals in relation to the respective reference values.Table 1 Univariate analysis of risk factors associated with stillbirths compared with live birthsView this table:View popupView inlineFor maternal characteristics, stillbirth rates were increased in first as well as third and subsequent pregnancies compared with second pregnancies, and in mothers of African, African Caribbean, and South Asian ethnic origin compared with their European counterparts. First generation migrants had an overall higher risk of stillbirth. Maternal age indicated a slight increase in younger (Social factors with significant associations included deprivation and unemployment of the mother or her partner. Pregnancies in which the parents were blood relations were not at significantly increased risk. Obesity (body mass index 30), active as well as passive smoking, lack of antenatal folic acid, and booking after 13 weeks were all associated with an increased risk of stillbirth. A history of mental health problems, diabetes, and stillbirth increased the risk. In the current pregnancy, pre eclampsia and antepartum haemorrhage were strongly associated, whereas gestational diabetes was not.The strongest factor was fetal growth restriction, with a relative risk of 4.0 (95% confidence interval 2.8 to 5.7) when fetal growth restriction was detected antenatally, doubling to 8.0 (6.5 to 9.9) when it was not detected. The overall stillbirth rate (per 1000 births) was 4.2, which was a composite of a rate of 2.4 (185/76356) in pregnancies without fetal growth restriction and 16.7 (195/11697) in pregnancies with fetal growth restriction (table 1). Of pregnancies with fetal growth restriction, the stillbirth rate for cases detected antenatally was 9.7 (35/3601), whereas the rate increased to 19.8 (160/8096) when cases were not detected (fig 1).
AbstractObjective To assess the main risk factors associated with stillbirth in a multiethnic English maternity population.Results Multivariable analysis identified a significant risk of stillbirth for parity (para 0 and para 3), ethnicity (African, African Caribbean, Indian, and Pakistani), maternal obesity (body mass index 30), smoking, pre existing diabetes, and history of mental health problems, antepartum haemorrhage, and fetal growth restriction (birth weight below 10th customised birthweight centile). As potentially modifiable risk factors, maternal obesity, smoking in pregnancy, and fetal growth restriction together accounted for 56.1% of the stillbirths. Presence of fetal growth restriction constituted the highest risk, and this applied to pregnancies where mothers did not smoke (adjusted relative risk 7.8, 95% confidence interval 6.6 to 10.9), did smoke (5.7, 3.6 to 10.9), and were exposed to passive smoke only (10.0, 6.6 to 15.8). Fetal growth restriction also had the largest population attributable risk for stillbirth and was fivefold greater if it was not detected antenatally than when it was (32.0% v 6.2%). In total, 195 of the 389 stillbirths in this cohort had fetal growth restriction, but in 160 (82%) it had not been detected antenatally. Antenatal recognition of fetal growth restriction resulted in delivery 10 days earlier than when it was not detected: median 270 (interquartile range 261 279) days v 280 (interquartile range 273 287) days. Stillbirth rates in the United Kingdom are among the highest in high income countries2 and have shown little improvement since the early 1990s.3Despite free availability of postmortem investigations in the English National Health Service as many as 50 70% of stillbirths have until recently been categorised as unclassified or unexplained4 and are, by implication, often considered unavoidable.5 Further investigation found that many stillborn fetuses had failed to reach their growth potential,6 7 8 and inclusion of fetal growth restriction as a category in stillbirth classifications resulted in imitation van cleef gold necklace a substantial drop to around 15% in the proportion of cases considered unexplained.8 9 This encouraged a renewed focus on understanding the underlying, mostly placental disease related, causes of fetal growth restriction. Recent reports of laboratory investigations10 and postmortem studies11 have confirmed the large contribution of placental failure in the cause of stillbirth.The clinical relevance of such findings van cleef alhambra necklace imitation is that although there are limited means by which to treat fetal growth restriction in utero, recognition that the fetus is at risk after appropriate maternal fetal investigations can lead to well timed delivery and improved perinatal outcome.12 13 However, there are currently no established and routinely used means to predict stillbirth, and risk factors known at the beginning of pregnancy are considered weak predictors of outcome.14We investigated the role of demographic, social, and medical risk factors that can be ascertained at the beginning of pregnancy together with those that become apparent as pregnancy progresses, and their respective contributions to the incidence of stillbirths in an NHS region in England with a multiethnic population.15 To focus on potentially avoidable factors we excluded congenital anomalies, as their contribution to stillbirth is contingent on incidence as well as cultural choices on antenatal screening, prenatal diagnosis, and decisions in response to positive results. We therefore explored the risk factors in pregnancies with normally formed singletons and estimated the respective contribution of these factors to the overall burden of stillbirth in our population.MethodsMaternity dataThe database was derived from the regional, NHSnet based perinatal episode electronic record (PEER) hosted and managed by the West Midlands Perinatal Institute.16 This electronic record was first implemented in April 2009 in the 19 maternity units in the West Midlands. For this study we used the data collected over a two year period, representing births between June 2009 and May 2011.The data originated from prospective records created in the standardised hand held maternity notes during pregnancy by the midwives and doctors.17 Trained data clerks in the respective hospitals transfer information from the notes on to the perinatal episode electronic record at the end of pregnancy. Quality was assured by central project staff through training workshops and regular on site data quality audits. The dataset contained 87 regionally agreed and defined data items,18 with information about maternal characteristics, including age, parity, ethnic origin, and maternal height and weight (expressed as body mass index); social factors, including employment status of the mother and her partner, consanguinity with the partner, and index of multiple deprivation; history of mental health problems, pre existing diabetes or hypertensive disease, or previous stillbirth; smoking status, alcohol consumption, non prescription drugs, folic acid intake, and time of first visit in pregnancy (the information for all these previous variables was usually recorded at the early pregnancy booking visit); complications in pregnancy, including gestational diabetes, antepartum haemorrhage, pregnancy induced hypertension, and pre eclampsia (defined as pregnancy induced hypertension with proteinuria); and fetal or neonatal characteristics, including sex, gestational age and weight at birth, and estimated weight during pregnancy. Gestational age was determined on the basis of routinely offered dating scans, which were carried out in the first or second trimester (The presence of intrauterine growth restriction was established on the basis of a birth weight below the 10th weight for gestational age centile, using the gestation related optimal weight standard (GROW),19 with coefficients derived from the West Midlands population. This method defines the fetal growth potential by excluding pathological factors such as smoking and diabetes, and individual adjustment or "customisation" for the baby's sex and the mother's height, weight, ethnic origin, and parity.20 21 A weight that is small for gestational age after such adjustment by growth potential has been shown to represent pathological smallness22 and is referred to as fetal growth restriction. We applied the 10th centile as the cut off, as it is in standard clinical use and has been validated through receiver operator curves as being close to optimal for predicting pathology by customised centiles.23The case notes were also examined for any recording of fetal growth problems. Fetal growth surveillance is usually done by a protocol of measuring fundal height at each antenatal visit in the third trimester, with referral for ultrasound assessment of estimated fetal weight when the serially plotted fundal height measurements do not follow the predicted curve. In pregnancies where assessment of fundal height is difficult (for example, maternal obesity) or where the risk of fetal growth restriction is considered increased (for example, due to obstetric history) serial estimated fetal weight measurements are done according to local protocols of varying scan frequency. Antenatal recognition of fetal growth restriction in pregnancies with birth weights below the 10th customised centile was defined as at least one antenatal entry with this diagnosis, usually based on one or more estimated fetal weights below the 10th customised centile, or an abnormal umbilical artery Doppler, or both. This assessment of the maternity record is part of routine ascertainment, as the proportion of pregnancies with antenatally detected fetal growth restriction is a regionally agreed key performance indicator.Linkage to mortality dataData on fetal, neonatal, and infant deaths and congenital anomalies were notified to the Perinatal Institute by a network of coordinators, and had a consistently high level of ascertainment. The information is held on secure NHS servers and is pseudonymised before any further analysis. Data linkage was established with the electronic maternity database, using the NHS number as unique identifier.Stillbirth was defined as a child born after the 24th week of pregnancy who did not, at any time after delivery, breathe or show any other signs of life. Along the lines of previously applied methods,6 we adjusted the gestational age of each stillborn fetus by deducting two days from the length of pregnancy at delivery, to correct for the estimated 48 hour average delay between intrauterine death and delivery.24Confidentiality and consentMaternal consent was obtained by provision of information and opt out. Mothers are informed at their first antenatal visit about the intention of collection and analysis of secondary data, and this is also explained in text printed in their standardised, hand held pregnancy notes. That this information has been given and explained is recorded in the notes and signed by the midwife. A mother can opt out at any time from her data being used, in which case her NHS number is added to an "opt out register" and further analysis is blocked. The Perinatal Institute's confidentiality and consent protocol has been reviewed and passed as appropriate by UK Connecting for Health, the NHS, and the Information Commissioner.Statistical analysesAfter initial exploratory analysis, we assessed the independent and multiple variable effects of explanatory variables on stillbirths in Poisson regression models. Variables entered in the multivariable analysis are those of known clinical relevance and from previous publications2 14 and included maternal age, parity, ethnic origin, place of birth, body mass index, history of mental health problems, pre existing hypertension, pre existing diabetes, cardiac disease, previous stillbirths, smoking in pregnancy, alcohol consumption, antenatal folic acid intake, late booking (13 weeks), gestational diabetes, pregnancy induced hypertension, pre eclampsia, antepartum haemorrhage, and fetal growth restriction. In addition to the index of multiple deprivation, we included maternal and paternal employment status as social factors in the multivariable analysis. We entered variables using the manual stepwise (forward backward) method. To reduce the over reliance in the estimates and the selection mechanism that may arise due to rarity of stillbirths, we used the bootstrapping approach to calculate standard errors. In the multivariable analysis all variables reaching a 0.05 significance level were retained in the model. We also considered van cleef and arpels earrings fake all two factor interactions between the explanatory variables and used empirical probability plots to check the final model to assess whether the modelling assumptions were met. We carried out sensitivity analyses to assess the influence of factors excluded because of P>0.05, potential clustering by maternity unit, and the effect of repeat pregnancies from the same mother.To assess the proportion of stillbirths that could be potentially prevented if risk factors were removed, we calculated adjusted population attributable risk estimates using standard methods25: population attributable risk=expected number of cases in the populationexpected number of cases if nobody in the population has the risk factor of interest/expected number of cases in the population 100The analyses were done using statistical package STATA version 11.ResultsA total of 105476 cases were entered during the two year collection period. Of these, 13258 were excluded because of congenital anomaly or multiple pregnancy, which left 92218 normally formed singleton pregnancies leading to 91829 live births and 389 stillbirths. This represented a stillbirth rate of 4.2/1000 births and compares with nationally reported stillbirth rates of normally formed singletons of 3.9 4.1/1000 over the same period.26 The analysis included 841 (0.9%) repeat pregnancies during the two year period of the 92218 mothers in the cohort.Univariate analysisTable 1 lists the variables, grouped according to maternal and fetal characteristics, social factors, medical history, and complications during pregnancy. Analysis was for complete cases only. The stillbirth rate is presented for subgroups, together with relative risks and 95% confidence intervals in relation to the respective reference values.Table 1 Univariate analysis of risk factors associated with stillbirths compared with live birthsView this table:View popupView inlineFor maternal characteristics, stillbirth rates were increased in first as well as third and subsequent pregnancies compared with second pregnancies, and in mothers of African, African Caribbean, and South Asian ethnic origin compared with their European counterparts. First generation migrants had an overall higher risk of stillbirth. Maternal age indicated a slight increase in younger (Social factors with significant associations included deprivation and unemployment of the mother or her partner. Pregnancies in which the parents were blood relations were not at significantly increased risk. Obesity (body mass index 30), active as well as passive smoking, lack of antenatal folic acid, and booking after 13 weeks were all associated with an increased risk of stillbirth. A history of mental health problems, diabetes, and stillbirth increased the risk. In the current pregnancy, pre eclampsia and antepartum haemorrhage were strongly associated, whereas gestational diabetes was not.The strongest factor was fetal growth restriction, with a relative risk of 4.0 (95% confidence interval 2.8 to 5.7) when fetal growth restriction was detected antenatally, doubling to 8.0 (6.5 to 9.9) when it was not detected. The overall stillbirth rate (per 1000 births) was 4.2, which was a composite of a rate of 2.4 (185/76356) in pregnancies without fetal growth restriction and 16.7 (195/11697) in pregnancies with fetal growth restriction (table 1). Of pregnancies with fetal growth restriction, the stillbirth rate for cases detected antenatally was 9.7 (35/3601), whereas the rate increased to 19.8 (160/8096) when cases were not detected (fig 1).
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