Classification of stillbirth by relevant condition at death (ReCoDe):
http://www.100md.com
《英国医生杂志》
1 Perinatal Institute, Birmingham B6 5RQ
Correspondence to: J Gardosi gardosi@perinatal.nhs.uk
Objective To develop and test a new classification system for stillbirths to help improve understanding of the main causes and conditions associated with fetal death.
Design Population based cohort study.
Setting West Midlands region.
Subjects 2625 stillbirths from 1997 to 2003.
Main outcome measures Categories of death according to conventional classification methods and a newly developed system (ReCoDe, relevant condition at death).
Results By the conventional Wigglesworth classification, 66.2% of the stillbirths (1738 of 2625) were unexplained. The median gestational age of the unexplained group was 237 days, significantly higher than the stillbirths in the other categories (210 days; P < 0.001). The proportion of stillbirths that were unexplained was high regardless of whether a postmortem examination had been carried out or not (67% and 65%; P = 0.3). By the ReCoDe classification, the most common condition was fetal growth restriction (43.0%), and only 15.2% of stillbirths remained unexplained. ReCoDe identified 57.7% of the Wigglesworth unexplained stillbirths as growth restricted. The size of the category for intrapartum asphyxia was reduced from 11.7% (Wigglesworth) to 3.4% (ReCoDe).
Conclusion The new ReCoDe classification system reduces the predominance of stillbirths currently categorised as unexplained. Fetal growth restriction is a common antecedent of stillbirth, but its high prevalence is hidden by current classification systems. This finding has profound implications for maternity services, and raises the question whether some hitherto "unexplained" stillbirths may be avoidable.
Stillbirths are the largest contributor to perinatal mortality, but current classification systems consistently report about two thirds of stillbirths as being unexplained.1 The preponderance of fetal deaths ending up in a non-specific or unexplained category occurs despite the use of three classification methods: the pathophysiological classification by Wigglesworth,2 the fetal and neonatal classification,3 and the revised obstetric (Aberdeen) classification.4
Any classification system that results in such a high proportion of cases being defined as unexplained would seem not to be fulfilling its purpose, which is to help clinicians to understand what went wrong and to derive learning points for best clinical practice; to assist in counselling bereaved mothers and families about the loss, the underlying reasons, and prospects for the future; and to aid public health specialists and commissioners to prioritise health service resources and strategies for prevention.
We developed a classification system for defining relevant clinical categories for stillbirth and we tested the method on a dataset of stillbirths in the West Midlands over a period of seven years.
Methods
The data for our study were derived from rapid report forms submitted to the Perinatal Institute from all maternity units in the West Midlands. We analysed data on all stillbirths occurring in the West Midlands population between 1997 and 2003. Data included the date of delivery, gestational age, maternal characteristics, the baby's sex and birth weight, and pregnancy details to ascertain the cause of death, including results of any postmortem examination. The forms list the primary and sometimes secondary causes, which are used to code the relevant classifications. We obtained the denominators (all stillbirths and live births) from the Office for National Statistics.
Classification
Our new classification system (box) seeks to identify the relevant condition at the time of death in utero. (See bmj.com for the principles on which the system is based.) The system seeks to establish what went wrong, not necessarily why (as the classification does not have to rely on finding an underlying cause, more than one category can be coded if the information is available). The hierarchy starts from conditions affecting the fetus and moves outwards in simple anatomical groups, which are subdivided into pathophysiological conditions; the primary condition should be the first on the list that is applicable to a case.
Fetal growth restriction is included as the last category in group A (A7): a fetus below the 10th customised centile would be assigned this classification only if none of the other specific fetal conditions were present. Secondary coding can be used to increase descriptiveness while maintaining a hierarchy of groups A to I to reflect clinical relevance.
Birth weight for gestation centile
We calculated customised centiles along previously described principles,5 6 using the gestation related optimal weight software GROW, version 4.6 (www.gestation.net), which calculates the fetal growth potential by adjusting for the fetus's sex and constitutional characteristics known at the beginning of each pregnancy: maternal height and weight, parity, and ethnic origin. The actual birth weight is then compared with the optimal weight predicted for the corresponding gestation, and a "customised centile" is calculated. The method improves the distinction between constitutional and pathological smallness for gestational age,7 8 allowing customised smallness for gestational age to be used synonymously with fetal growth restriction. For missing data such as maternal height or weight at booking, population averages were used.
The calculation of the centile required an estimation of gestational age at the time of death. As in previous analyses of stillbirth weight,7 9 we deducted two days from the gestational age at delivery of each stillborn fetus. This is taken as the average estimated time interval in the third trimester between fetal death and delivery.10
Results
Overall, 2625 stillbirths and 451 197 births occurred during the seven year period between 1997 and 2003, representing an average stillbirth rate of 5.82 per 1000.
The table lists the causes of death according to Wigglesworth,2 which is the classification most commonly used for national statistics.1 The largest category, 66.2%, was for unexplained antepartum fetal death, and 11.7% of deaths were associated with intrapartum causes. An equivalent unexplained category was also the largest by the fetal and neonatal classification3 (66.2%) and the revised obstetric (Aberdeen) classification (52.7%).11
Classification system according to relevant condition at death (ReCoDe)
Group A: Fetus
Lethal congenital anomaly
Infection
2.1 Chronic
2.2 Acute
Non-immune hydrops
Isoimmunisation
Fetomaternal haemorrhage 6. Twin-twin transfusion 7. Fetal growth restriction*
Group B: Umbilical cord
Prolapse
Constricting loop or knot
Velamentous insertion
Other
Group C: Placenta
Abruptio
Praevia
Vasa praevia
Other "placental insufficiency"
Other
Group D: Amniotic fluid
Chorioamnionitis
Oligohydramnios
Polyhydramnios
Other
Group E: Uterus
Rupture
Uterine anomalies
Other
Group F: Mother
Diabetes
Thyroid diseases
Essential hypertension
Hypertensive diseases in pregnancy
Lupus or antiphospholipid syndrome
Cholestasis
Drug misuse
Other
Group G: Intrapartum
Asphyxia
Birth trauma
Group H: Trauma
External
Iatrogenic
Group I: Unclassified
No relevant condition identified
No information available
*<10th customised weight for gestational age centile.
If severe enough to be considered relevant.
Histological diagnosis.
The average (median) gestational age at delivery of the stillbirths denoted as unexplained by Wigglesworth was significantly higher than the gestational age of the stillbirths that fell into the other Wigglesworth categories (237 v 210 days; P < 0.001, Mann-Whitney U).
A total of 1241 of the 2625 stillbirths (47.3%) had a postmortem examination. The proportion of stillbirths that were unexplained was high regardless of whether a postmortem examination had been carried out or not (810 of 1241 (65.3%) v 928 of 1383 (67.1%); P = 0.3).
The figure shows the results using the ReCoDe classification. Only 398 (15.2%) cases remained unclassified as "no relevant condition identified" (I1). The largest category of stillbirths was A7, fetal growth restriction (43.0%). Of the 1738 unexplained stillbirths according to Wigglesworth (table), the ReCoDe system identified 1002 (57.7%) as growth restricted.
Classification of stillbirths in West Midlands, 1997-2003 using the ReCoDe (relevant condition at death) system
Classification of 2625 stillbirths according to Wigglesworth2
Information on classification of a secondary condition was available on 1146 (43.7%) of the rapid report forms (figure). A wide spread of secondary conditions was observed for several of the primary classifications. In particular, a large proportion of congenital anomalies were also growth restricted; among the primary fetal growth restriction group (A7), the most common secondary codes were placental abruption, oligohydramnios, maternal hypertensive disease, and intrapartum asphyxia; and intrapartum asphyxia was often a secondary code for stillbirth associated with abruptio.
Overall, the ReCoDe system showed a smaller proportion of deaths in the intrapartum group than did Wigglesworth (3.4% v 11.7%). As suggested from the secondary coding analysis (figure), this was because many cases of intrapartum asphyxia were assigned other primary conditions under the ReCoDe system. Fetal growth restriction and placental abruptio together accounted for 99 (63%) of the 156 cases with a secondary coding of intrapartum asphyxia.
What is already known on this topic
Stillbirths are the largest contributor to perinatal mortality
The current method of classifying perinatal deaths results in at least two thirds of stillbirths being classified as unexplained
What this study adds
A new classification system (ReCoDe) can identify relevant conditions at the time of fetal death in 85% of cases
Fetal growth restriction is the single largest category of conditions associated with stillbirth and is found in the majority of the cases previously considered unexplained
Discussion
Maternal and Child Health Consortium. CESDI 8th annual report: Confidential Enquiry of Stillbirths and Deaths in Infancy, London 2001.
Wigglesworth JS. Monitoring perinatal mortality—a pathophysiological approach. Lancet 1980;Sep 27: 684-7.
Hey EN, LLoyd DJ, Wigglesworth JS. Classifying perinatal death: fetal and neonatal factors. Br J Obstet Gynaecol 1986;93: 1213-23.
Cole SK, Hey EN, Thomson AM. Classifying perinatal death: an obstetric approach. Br J Obstet Gynaecol 1986;93: 1204-12.
Gardosi J, Chang A, Kalyan B, Sahota D, Symonds EM. Customised antenatal growth charts. Lancet 1992;339: 283-7.
Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol 1995;6: 168-74.
Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome in SGA births defined by customised versus population based birthweight standards. Br J Obstet Gynaecol 2001;108: 830-4.
McCowan L, Harding JE, Stewart AW. Customised birthweight centiles predict SGA pregnancies with perinatal morbidity. Br J Obstet Gynaecol 2005;112: 1026-33.
Gardosi J, Mul T, Mongelli M, Fagan D. Analysis of birthweight and gestational age in antepartum stillbirths. Br J Obstet Gynaecol 1998;105: 524-30.
Genest DR, Williams MA, Greene MF. Estimating the time of death in stillborn fetuses: histologic evaluation of fetal organs; an autopsy study of 150 stillborns. Obstet Gynecol 1992;80: 575-84.
Bound JP. Classification and causes of perinatal mortality. BMJ 1956;ii: 1191-6, 1260-5.
Confidential Enquiry into Maternal and Child Health. Stillbirth, neonatal and post-neonatal mortality 2000-2003, England, Wales and Northern Ireland. London: RCOG Press, 2005.
Chiswick ML. Commentary on current World Health Organisation definitions used in perinatal statistics. J Obstet Gynaecol Br Emp 1986;86: 1236-8.
Scottish programme for clinical effectiveness in reproductive health. Scottish stillbirth and infant death report 1999. Edinburgh: NHS Scotland, Information and Statistics Division, 2000.
Alessandri L, Stanley FJ, Garner JB, Newnham J, Walters BN. A case control study of unexplained antepartum stillbirths. Br J Obstet Gynaecol 1992;99: 711-8.
McIlwaine GM, Howat RCL, Dunn F, Macnaughton MC. The Scottish perinatal mortality survey. BMJ 1979;2: 1103-6.
Williams RL, Creasy RK, Cunningham GC, Hawes WE, Norris FD, Tashiro M. Fetal growth and perinatal viability in California. Obstet Gynecol 1982;59: 624-32.
Whitfield CR, Smith NC, Cockburn F, Gibson AM. Perinatally related wastage—a proposed classification of primary obstetric factors. Br J Obstet Gynaecol 1986;93: 694-703.
Huang DY Usher RH, Kramer MS, Yang H, Morin L, Fretts RC. Determinants of unexplained antepartum fetal deaths. Obstet Gynecol 2000;95: 215-21.
MacLennan A. A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement. BMJ 1999;16: 1054-9.
Hepburn M, Rosenberg K. An audit of the detection and management of small-for-gestational age babies. Br J Obstet Gynaecol 1986;93: 212-6.(Jason Gardosi, director1, Sue M Kady, pe)
Correspondence to: J Gardosi gardosi@perinatal.nhs.uk
Objective To develop and test a new classification system for stillbirths to help improve understanding of the main causes and conditions associated with fetal death.
Design Population based cohort study.
Setting West Midlands region.
Subjects 2625 stillbirths from 1997 to 2003.
Main outcome measures Categories of death according to conventional classification methods and a newly developed system (ReCoDe, relevant condition at death).
Results By the conventional Wigglesworth classification, 66.2% of the stillbirths (1738 of 2625) were unexplained. The median gestational age of the unexplained group was 237 days, significantly higher than the stillbirths in the other categories (210 days; P < 0.001). The proportion of stillbirths that were unexplained was high regardless of whether a postmortem examination had been carried out or not (67% and 65%; P = 0.3). By the ReCoDe classification, the most common condition was fetal growth restriction (43.0%), and only 15.2% of stillbirths remained unexplained. ReCoDe identified 57.7% of the Wigglesworth unexplained stillbirths as growth restricted. The size of the category for intrapartum asphyxia was reduced from 11.7% (Wigglesworth) to 3.4% (ReCoDe).
Conclusion The new ReCoDe classification system reduces the predominance of stillbirths currently categorised as unexplained. Fetal growth restriction is a common antecedent of stillbirth, but its high prevalence is hidden by current classification systems. This finding has profound implications for maternity services, and raises the question whether some hitherto "unexplained" stillbirths may be avoidable.
Stillbirths are the largest contributor to perinatal mortality, but current classification systems consistently report about two thirds of stillbirths as being unexplained.1 The preponderance of fetal deaths ending up in a non-specific or unexplained category occurs despite the use of three classification methods: the pathophysiological classification by Wigglesworth,2 the fetal and neonatal classification,3 and the revised obstetric (Aberdeen) classification.4
Any classification system that results in such a high proportion of cases being defined as unexplained would seem not to be fulfilling its purpose, which is to help clinicians to understand what went wrong and to derive learning points for best clinical practice; to assist in counselling bereaved mothers and families about the loss, the underlying reasons, and prospects for the future; and to aid public health specialists and commissioners to prioritise health service resources and strategies for prevention.
We developed a classification system for defining relevant clinical categories for stillbirth and we tested the method on a dataset of stillbirths in the West Midlands over a period of seven years.
Methods
The data for our study were derived from rapid report forms submitted to the Perinatal Institute from all maternity units in the West Midlands. We analysed data on all stillbirths occurring in the West Midlands population between 1997 and 2003. Data included the date of delivery, gestational age, maternal characteristics, the baby's sex and birth weight, and pregnancy details to ascertain the cause of death, including results of any postmortem examination. The forms list the primary and sometimes secondary causes, which are used to code the relevant classifications. We obtained the denominators (all stillbirths and live births) from the Office for National Statistics.
Classification
Our new classification system (box) seeks to identify the relevant condition at the time of death in utero. (See bmj.com for the principles on which the system is based.) The system seeks to establish what went wrong, not necessarily why (as the classification does not have to rely on finding an underlying cause, more than one category can be coded if the information is available). The hierarchy starts from conditions affecting the fetus and moves outwards in simple anatomical groups, which are subdivided into pathophysiological conditions; the primary condition should be the first on the list that is applicable to a case.
Fetal growth restriction is included as the last category in group A (A7): a fetus below the 10th customised centile would be assigned this classification only if none of the other specific fetal conditions were present. Secondary coding can be used to increase descriptiveness while maintaining a hierarchy of groups A to I to reflect clinical relevance.
Birth weight for gestation centile
We calculated customised centiles along previously described principles,5 6 using the gestation related optimal weight software GROW, version 4.6 (www.gestation.net), which calculates the fetal growth potential by adjusting for the fetus's sex and constitutional characteristics known at the beginning of each pregnancy: maternal height and weight, parity, and ethnic origin. The actual birth weight is then compared with the optimal weight predicted for the corresponding gestation, and a "customised centile" is calculated. The method improves the distinction between constitutional and pathological smallness for gestational age,7 8 allowing customised smallness for gestational age to be used synonymously with fetal growth restriction. For missing data such as maternal height or weight at booking, population averages were used.
The calculation of the centile required an estimation of gestational age at the time of death. As in previous analyses of stillbirth weight,7 9 we deducted two days from the gestational age at delivery of each stillborn fetus. This is taken as the average estimated time interval in the third trimester between fetal death and delivery.10
Results
Overall, 2625 stillbirths and 451 197 births occurred during the seven year period between 1997 and 2003, representing an average stillbirth rate of 5.82 per 1000.
The table lists the causes of death according to Wigglesworth,2 which is the classification most commonly used for national statistics.1 The largest category, 66.2%, was for unexplained antepartum fetal death, and 11.7% of deaths were associated with intrapartum causes. An equivalent unexplained category was also the largest by the fetal and neonatal classification3 (66.2%) and the revised obstetric (Aberdeen) classification (52.7%).11
Classification system according to relevant condition at death (ReCoDe)
Group A: Fetus
Lethal congenital anomaly
Infection
2.1 Chronic
2.2 Acute
Non-immune hydrops
Isoimmunisation
Fetomaternal haemorrhage 6. Twin-twin transfusion 7. Fetal growth restriction*
Group B: Umbilical cord
Prolapse
Constricting loop or knot
Velamentous insertion
Other
Group C: Placenta
Abruptio
Praevia
Vasa praevia
Other "placental insufficiency"
Other
Group D: Amniotic fluid
Chorioamnionitis
Oligohydramnios
Polyhydramnios
Other
Group E: Uterus
Rupture
Uterine anomalies
Other
Group F: Mother
Diabetes
Thyroid diseases
Essential hypertension
Hypertensive diseases in pregnancy
Lupus or antiphospholipid syndrome
Cholestasis
Drug misuse
Other
Group G: Intrapartum
Asphyxia
Birth trauma
Group H: Trauma
External
Iatrogenic
Group I: Unclassified
No relevant condition identified
No information available
*<10th customised weight for gestational age centile.
If severe enough to be considered relevant.
Histological diagnosis.
The average (median) gestational age at delivery of the stillbirths denoted as unexplained by Wigglesworth was significantly higher than the gestational age of the stillbirths that fell into the other Wigglesworth categories (237 v 210 days; P < 0.001, Mann-Whitney U).
A total of 1241 of the 2625 stillbirths (47.3%) had a postmortem examination. The proportion of stillbirths that were unexplained was high regardless of whether a postmortem examination had been carried out or not (810 of 1241 (65.3%) v 928 of 1383 (67.1%); P = 0.3).
The figure shows the results using the ReCoDe classification. Only 398 (15.2%) cases remained unclassified as "no relevant condition identified" (I1). The largest category of stillbirths was A7, fetal growth restriction (43.0%). Of the 1738 unexplained stillbirths according to Wigglesworth (table), the ReCoDe system identified 1002 (57.7%) as growth restricted.
Classification of stillbirths in West Midlands, 1997-2003 using the ReCoDe (relevant condition at death) system
Classification of 2625 stillbirths according to Wigglesworth2
Information on classification of a secondary condition was available on 1146 (43.7%) of the rapid report forms (figure). A wide spread of secondary conditions was observed for several of the primary classifications. In particular, a large proportion of congenital anomalies were also growth restricted; among the primary fetal growth restriction group (A7), the most common secondary codes were placental abruption, oligohydramnios, maternal hypertensive disease, and intrapartum asphyxia; and intrapartum asphyxia was often a secondary code for stillbirth associated with abruptio.
Overall, the ReCoDe system showed a smaller proportion of deaths in the intrapartum group than did Wigglesworth (3.4% v 11.7%). As suggested from the secondary coding analysis (figure), this was because many cases of intrapartum asphyxia were assigned other primary conditions under the ReCoDe system. Fetal growth restriction and placental abruptio together accounted for 99 (63%) of the 156 cases with a secondary coding of intrapartum asphyxia.
What is already known on this topic
Stillbirths are the largest contributor to perinatal mortality
The current method of classifying perinatal deaths results in at least two thirds of stillbirths being classified as unexplained
What this study adds
A new classification system (ReCoDe) can identify relevant conditions at the time of fetal death in 85% of cases
Fetal growth restriction is the single largest category of conditions associated with stillbirth and is found in the majority of the cases previously considered unexplained
Discussion
Maternal and Child Health Consortium. CESDI 8th annual report: Confidential Enquiry of Stillbirths and Deaths in Infancy, London 2001.
Wigglesworth JS. Monitoring perinatal mortality—a pathophysiological approach. Lancet 1980;Sep 27: 684-7.
Hey EN, LLoyd DJ, Wigglesworth JS. Classifying perinatal death: fetal and neonatal factors. Br J Obstet Gynaecol 1986;93: 1213-23.
Cole SK, Hey EN, Thomson AM. Classifying perinatal death: an obstetric approach. Br J Obstet Gynaecol 1986;93: 1204-12.
Gardosi J, Chang A, Kalyan B, Sahota D, Symonds EM. Customised antenatal growth charts. Lancet 1992;339: 283-7.
Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol 1995;6: 168-74.
Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome in SGA births defined by customised versus population based birthweight standards. Br J Obstet Gynaecol 2001;108: 830-4.
McCowan L, Harding JE, Stewart AW. Customised birthweight centiles predict SGA pregnancies with perinatal morbidity. Br J Obstet Gynaecol 2005;112: 1026-33.
Gardosi J, Mul T, Mongelli M, Fagan D. Analysis of birthweight and gestational age in antepartum stillbirths. Br J Obstet Gynaecol 1998;105: 524-30.
Genest DR, Williams MA, Greene MF. Estimating the time of death in stillborn fetuses: histologic evaluation of fetal organs; an autopsy study of 150 stillborns. Obstet Gynecol 1992;80: 575-84.
Bound JP. Classification and causes of perinatal mortality. BMJ 1956;ii: 1191-6, 1260-5.
Confidential Enquiry into Maternal and Child Health. Stillbirth, neonatal and post-neonatal mortality 2000-2003, England, Wales and Northern Ireland. London: RCOG Press, 2005.
Chiswick ML. Commentary on current World Health Organisation definitions used in perinatal statistics. J Obstet Gynaecol Br Emp 1986;86: 1236-8.
Scottish programme for clinical effectiveness in reproductive health. Scottish stillbirth and infant death report 1999. Edinburgh: NHS Scotland, Information and Statistics Division, 2000.
Alessandri L, Stanley FJ, Garner JB, Newnham J, Walters BN. A case control study of unexplained antepartum stillbirths. Br J Obstet Gynaecol 1992;99: 711-8.
McIlwaine GM, Howat RCL, Dunn F, Macnaughton MC. The Scottish perinatal mortality survey. BMJ 1979;2: 1103-6.
Williams RL, Creasy RK, Cunningham GC, Hawes WE, Norris FD, Tashiro M. Fetal growth and perinatal viability in California. Obstet Gynecol 1982;59: 624-32.
Whitfield CR, Smith NC, Cockburn F, Gibson AM. Perinatally related wastage—a proposed classification of primary obstetric factors. Br J Obstet Gynaecol 1986;93: 694-703.
Huang DY Usher RH, Kramer MS, Yang H, Morin L, Fretts RC. Determinants of unexplained antepartum fetal deaths. Obstet Gynecol 2000;95: 215-21.
MacLennan A. A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement. BMJ 1999;16: 1054-9.
Hepburn M, Rosenberg K. An audit of the detection and management of small-for-gestational age babies. Br J Obstet Gynaecol 1986;93: 212-6.(Jason Gardosi, director1, Sue M Kady, pe)