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Trends in Congenital Malformations, 1974–1999: Effect of Prenatal Diagnosis and Elective Termination

Allyson J. Peller, MPH^*, Marie-Noel Westgate, MEd^* and Lewis B. Holmes, MD^*

From the *Genetics and Teratology Unit, Pediatric Service, Massachusetts General Hospital, and the Department of Newborn Medicine, Brigham and Women's Hospital, Boston, Massachusetts.

Address reprint requests to: Allyson J. Peller, MPH, Genetics and Teratology Unit, Pediatric Service, Warren 801, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114–2696; e-mail: apeller{at}partners.org.

	ABSTRACT

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OBJECTIVE: To examine trends in congenital malformations, elective terminations for malformations and correlates for the decision to terminate a pregnancy with a malformation.

METHODS: All malformed liveborn and stillborn infants and elective terminations for malformations were identified in a large urban tertiary center and general hospital for the years 1974, 1979, 1984, 1989, 1994, and 1999. Nine hundred and fifty-four women with malformed infants, who had always planned to deliver at the hospital, were identified. Prenatal screening by ultrasonography or amniocentesis before 24 weeks of gestation, severity rating of the malformation, parity, marital status, race, level of education, insurance status, and pregnancy history were determined

RESULTS: In each of these 6 years, about 2% of newborn infants had a major malformation. The rate of prenatal screening by ultrasonography and amniocentesis before 24 weeks increased from 7% in the years 1974 and 1979 to 61% in the years 1984 and 1989 to 89% in the years 1994 and 1999. Elective termination increased from less than 1% in the years 1974 and 1979 to 18% to 20% in the years 1984, 1989, 1994, and 1999. Pregnancies with fatal and severe conditions were much more likely to be terminated electively than pregnancies with moderate or mild conditions (odds ratio 53.3; 95% confidence interval 22.7–124.7)

CONCLUSION: The introduction of routine prenatal screening and the subsequent increase in elective termination for malformed fetuses means that the inclusion of terminated pregnancies in malformation surveillance programs is necessary to study prevalence and risk factors in the epidemiology of malformations.

The objectives of this study were to quantify trends in the frequency of major malformations, subdivided by severity, and their prenatal detection among affected newborn infants identified in the Active Malformations Surveillance Program of Brigham and Women's Hospital, using data from years 1974, 1979, 1984, 1989, 1994, and 1999, to examine the impact of prenatal screening and the decision to terminate the pregnancy on the number of liveborn infants with a malformation, and to examine the association between the severity of a malformation and the decision to terminate the pregnancy, while controlling for potential confounding demographic characteristics.

	SUBJECTS AND METHODS

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All infants and fetuses with major malformations were identified by the Active Malformations Surveillance Program of Brigham and Women's Hospital, a program established on February 16, 1972, at the Boston Hospital for Women, Lying-In Division. Surveillance has continued to the present, except for a period of interruption from February 15, 1975 to December 31, 1978, due to lack of office space. Staff members reviewed the medical records of all deliveries Monday through Friday, with weekend coverage beginning in the 1980s, to collect clinical findings from the pediatrician's newborn examination, reports of all consultants and diagnostic studies, and observations from surgery or autopsy, if it occurred. Only malformations detected in the first 5 postpartum days were included, because discharge from the birthing hospital occurred on day 5 in 1972. In later years, there has been a trend toward earlier discharge with typically only 2 days of observation. Birth status was classified as liveborn, stillborn, or elective termination. Spontaneous abortions (ie, pregnancy loss before 20 weeks other than elective terminations for malformations) were not included in the surveillance program, except for elective terminations of pregnancy for fetal abnormalities. A maternal interview was conducted before discharge and after delivery for each affected infant identified to collect data regarding demographic characteristics, obstetric history, prenatal testing, and family medical history. If the mother could not be interviewed, information was obtained from the medical record of the mother and her infant.

This study focused on women who had planned to deliver at Brigham and Women's Hospital, called nontransfers. They were distinguished from women who had planned originally to deliver at another hospital and transferred their care after the detection of a fetal abnormality and were considered transfers. Affected infants were subdivided by those with and without prenatal testing (ultrasonography, amniocentesis, chorionic villus sampling, or X-ray) before the end of the 24th week of pregnancy, the legal limit for termination of pregnancy in the Commonwealth of Massachusetts. Because many of these mothers had their prenatal care in private offices, the results of maternal serum screening of alpha-fetoprotein (AFP) and other analyses were not recorded in their medical record. A pregnancy history of elective termination, elective termination for malformation, spontaneous abortion, stillbirth, neonatal death, or fetal loss for any other reason was classified as a previous event, as in the analysis of Schechtman et al.⁷

A major malformation was defined as a structural abnormality of surgical, medical or cosmetic importance. The newborn examination by the pediatrician was used as the criterion standard for classifying malformations. Abnormalities only detected by prenatal screening or surgery (eg, unilateral renal anomalies), and not the examining pediatrician, were excluded. In addition, minor anomalies, birthmarks, positional deformities, and physiologic findings, such as patent ductus arteriosus in premature infants, were excluded. Chromosome abnormalities with no associated malformations, such as 47, XYY or 47, XXY, were not included.

The specific abnormality was established from a review of the infant's medical record, including the reports of all consultants and diagnostic tests, rather than using only the International Classification of Diseases, 9th Revision codes for discharge diagnoses. The malformations were subdivided by severity into 4 groups: fatal, severe handicapping, moderate fixable, and mild. Examples of malformations from these categories include: anencephaly, renal agenesis (bilateral), trisomy 18, and holoprosencephaly as fatal; Down syndrome, hydrocephalus, spina bifida, and hypoplastic left heart syndrome as severe handicapping; cleft lip and palate, omphalocele, tetralogy of Fallot, and diaphragmatic hernia as moderate fixable; and postaxial polydactyly, type B, natal teeth, conjunctival dermoid cyst, and camptodactyly as mild. These categories reflect, on average, the effect of that structural abnormality on quality of life and amenability to treatment. A fetus or infant with multiple major malformations that were not fatal was classified as having a severely handicapping abnormality. Malformations were classified as "moderate/fixable" according to medical interventions available in the 1990s, so that the rating was consistent over the entire period of this analysis.

Data from the Active Malformations Surveillance Program of Brigham and Women's Hospital for the years 1974, 1979, 1984, 1989, 1994, and 1999 were analyzed. The Cochran Mantel-Haenszel ² statistic for ordered columns was used to analyze trends over time in prenatal screening and elective abortion. Multivariable logistic regression modeling was used to assess the association between the severity of the malformation and the decision to terminate the pregnancy. Only pregnancies in the years 1984, 1989, 1994, and 1999 with prenatal screening before the end of the 24th week of pregnancy were included in the model, because prenatal screening was infrequent in 1974 and 1979. We are examining trends in the effects of prenatal screening rather than the accuracy of prenatal screening in detecting malformation. The potential confounding effects of maternal age, marital status, maternal race, parity, previous events, maternal education, religion, and insurance status were controlled by introducing these variables individually into the model. Odds ratios and 95% confidence intervals are presented to quantify significant associations. To assess the generalizability of our hospital-based sample, demographic characteristics of nontransfer mothers in the Active Malformation Surveillance Program of Brigham and Women's Hospital from the year 1999 were compared, using the ² statistic, with the demographic characteristics of mothers in 2 larger data sets recording all births in the Commonwealth of Massachusetts for the year 1999; the Commonwealth of Massachusetts Vital Records,⁸ which records all livebirths and stillbirths; and the Massachusetts Birth Defects Monitoring Program (Massachusetts Department of Public Health), which record all births with major structural birth defects but not elective terminations. The comparison was restricted to liveborns for the variables maternal age, marital status, maternal race, parity, and insurance status. We were limited in our comparison because the larger data sets did not contain the other demographic variables in our database, reported mortality statistics using a different algorithm than our data, and did not identify malformed fetuses from elective terminations. All data were analyzed using SAS 8.0 software (SAS Institute, Cary, NC). Our institutional review board approved the protocol annually.

	RESULTS

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A total of 1,662 malformed infants were identified: 954 born to nontransfer mothers and 708 to transferred mothers. The prevalence of major malformations among infants of nontransfer mothers at Brigham and Women's Hospital for the years of this study were 147 of 6,050 (2.43%) in 1974, 96 of 7,130 (1.35%) in 1979, 174 of 8,970 (1.94%) in 1984, 200 of 10,301 (1.94%) in 1989, 149 of 8,795 (1.69%) in 1994, and 188 of 9,847 (1.91%) in 1999. When transfers were included, the prevalence of major malformations increased over the study years: from 148 of 6,051 (2.45%) in 1974 to 111 of 7,145 (1.55%) in 1979, 252 of 9,048 (2.79%) in 1984, 400 of 10,501 (3.81%) in 1989, 360 of 9,006 (4.00%) in 1994, and 391 of 10,050 (3.89%) in 1999.

The sample population was predominantly white, college educated, Catholic or Protestant, privately insured, married, and parity 1 or less over this 30-year period (Table 1). Transfer patients had a higher rate of prenatal screening before 24 weeks gestation, a higher frequency of fatal and severe malformations, more elective terminations, and fewer liveborn infants than nontransfers patients (data not shown).

For pregnancies of nontransferred mothers (Table 2), the rate of prenatal screening by ultrasonography in the second or third trimester increased from 19.8% for the years 1974 and 1979 to 75.7% in the years 1984 and 1989 to 95.3% for the years 1994 and 1999 (P < .001). The rate of 19.8% for prenatal screening in the years 1974 and 1979 represented primarily ultrasonography just before delivery to identify breech position. The rate of amniocentesis increased from 3.3% for the years 1974 and 1979 to 9.9% in the years 1984 and 1989 to 30.9% for the years 1994 and 1999 (P < .001). Overall, the rate of prenatal screening with either amniocentesis or ultrasonography before 24 weeks gestation increased from 7% for the years 1974 and 1979 to 61.5% for the years 1984 and 1989 to 89.3% for the years 1994 and 1999 (P < .001). Trends for elective abortions were calculated only for those cases with prenatal screening before 24 weeks. For pregnancies of nontransferred mothers, the rate of elective abortions for any malformation increased from 0.8% for the years 1974 and 1979 to 18.1% for the years 1994 and 1999 (P < .001); for fatal malformations, the rate of elective abortions increased from 50% for the years 1974 and 1979 to 81% for the years 1994 and 1999, for severe handicapping malformations from 0% for the years 1974 and 1979 to 44.4% for the years 1994 and 1999, and for moderate fixable malformations from 0% for the years 1974 and 1979 to 3.2% for the years 1994 and 1999. It is notable that in 1974 and 1979, 2 of the 4 nontransfers with fatal malformations and prenatal screening before 24 weeks were terminated. One was a 40-year-old woman who had an amniocentesis, which showed her fetus had trisomy 18. The other was a 27-year-old woman who had placenta previa and hydramnios at 23 weeks gestation, and in whom an X-ray showed that her fetus had anencephaly. A total of 3.2% of the moderate fixable malformations with prenatal screening before 24 weeks were terminated electively. These 5 malformations included omphalocele, cleft lip (2 infants), and transposition of the great vessels (2 infants). There were no terminations for mild malformations.

Twenty-two pregnancies of nontransferred mothers with fatal malformations that had prenatal screening before 24 weeks were not terminated. The apparent reasons for not terminating their pregnancies included fatal malformation not diagnosed correctly by prenatal screening before 24 weeks (10 cases), twin pregnancies with 1 healthy twin (5 cases), parents whose religious beliefs were against elective termination of pregnancy (2 cases), and reason not specified in either the interview or the medical record (5 cases).

Trends for specific malformations were analyzed for Down syndrome, anencephaly, spina bifida, and trisomy 18 (Table 3). There was a suggestion of variability in trends among specific malformations within the same severity rating category: anencephaly and trisomy 18, both considered fatal, and Down syndrome and spina bifida, both considered severely handicapping. However, the sample sizes for these specific malformations did not have adequate statistical power to analyze trends.

The adjusted multivariable logistic regression models showed that pregnancies for nontransfers were more likely to be terminated if the malformation was fatal or severe (odds ratio 53.25; 95% confidence interval 22.74–124.71) when history of previous events, marital status, and year of current pregnancy were controlled for in the model (Table 4). This association did not change significantly when maternal age, maternal race, parity, or insurance status were added to the model. Religion and maternal education were not included in the model owing to missing values.

In comparison with the demographic characteristics of mothers recorded in the Commonwealth of Massachusetts Vital Records⁸ and the Massachusetts Birth Defects Monitoring Program (Massachusetts Department of Public Health), the Active Malformation Surveillance Program of Brigham and Women's Hospital had a more racially diverse sample with a lower percentage of white patients (P < .001) and had a higher percentage of primiparous mothers (P < .001). However, maternal age, marital status, and insurance status were not significantly different between the 3 data sets (Table 5).

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
In association with the advent of routine prenatal screening, 18–20% of all pregnancies with major malformations were terminated by choice. Statistical analyses, adjusting for multiple demographic characteristics, showed that the pregnant women were much more likely to terminate pregnancies if the malformation was either fatal or severe and handicapping. These findings show that epidemiologic studies of major malformations must include elective terminations to be complete. According to a comparison of demographic characteristics of nontransfer mothers in our sample with 2 larger data sets, the findings in the Active Malformation Surveillance Program of Brigham and Women's Hospital were generalizable to the Commonwealth of Massachusetts in terms of maternal age, marital status, and insurance status but not for race or parity in 1999, the 1 year for which both comparisons were available.

These findings are consistent with and extend those from previous smaller studies,^9–11 which reported that the severity of the malformation and the potential for neonatal or fetal therapy, as described by their physician or genetic counselor, influenced the decision to terminate. For example, both Pryde et al,⁹ in a study of 159 cases from the years 1990–1991, and Grevengood et al,¹⁰ in an analysis of 50 cases from the years 1987–1992, reported that parents whose fetuses had fatal anomalies were more likely to terminate than parents whose fetuses had abnormalities with an uncertain prognoses. Velie and Shaw¹¹ had a sample size of 538 pregnancies with neural tube defects in which the characteristics of women who terminated their pregnancies was compared with the characteristics of women who delivered liveborn or stillborn infants. White, highly educated, high-income women who had taken folic acid supplements were more likely to terminate pregnancies with neural tube defects.

Schechtman et al⁷ performed the largest previous hospital-based study (N = 2,396) and analyzed data obtained from the Division of Genetics and Ultrasound at Washington University in St. Louis for the period 1984–1997. They observed that mothers who were younger and less educated were less likely to terminate a pregnancy with a malformation than older, more educated mothers. Unfortunately, the findings reported by Schechtman et al⁷ are not comparable with those in this study because of major differences in inclusion criteria. In contrast to this study, they included nonstructural anomalies, such as cardiac arrhythmias, and malformations detected by ultrasonography, such as absence of one kidney, that are not likely to have been detected by the examining pediatrician; furthermore, the severity of all anomalies, especially heart defects, was not determined because of a lack of clinical data. Because their data were from 1984–1997, they could not analyze trends starting in the 1970s (ie, before routine prenatal screening).

The impact of prenatal screening on the number of liveborn infants was also documented by Stoll et al³ for all congenital anomalies in a registry of 11 maternity hospitals in Strasbourg, northern France 1979–1999. A declining trend in the number of liveborn infants was observed over time that varied by type of anomaly, such as Down syndrome, which decreased by 80% from 1979–1988 to 1994–1999. We have published previously the trends over the periods 1972–1990 or 1972–1994 for several common birth defects^12–16 in the Active Malformation Surveillance Program of Brigham and Women's Hospital. These studies showed, for example, that 20% of all limb reduction defects were in terminated pregnancies¹² and over 80% of the pregnancies with a fetus with Down syndrome¹⁴ were terminated by choice in the 1980s and 1990s. The number of pregnancies with a fetus with Down syndrome terminated that were tabulated in this study was different from that tabulated by Caruso et al,¹⁴ in that she analyzed all infants born in each year (1972–1994) whereas we have tabulated every fifth year.

These data have some limitations and must be interpreted in the context of the study design of the Active Malformation Surveillance Program of Brigham and Women's Hospital. The percentage of mothers interviewed is unknown because this information was not recorded prospectively. For those mothers of affected infants who could not be interviewed, the demographic information obtained was limited to that recorded in her medical record. This affected the data available on marital status, race, education, and religion with generally more data missing in the years 1974 and 1979 (Table 1). However, assessment of pregnancy outcome is uniform for all cases. If a pregnancy was terminated by a destructive procedure, such as dilatation and evacuation, there was less likelihood of identifying additional associated multiple anomalies. Another limitation is the possibility that an affected infant would be "missed" by the surveillance program. This possibility was addressed by McGuirk et al,¹² in an analysis of all infants with limb-reduction defects. She reviewed the files of the medical records of all affected infants at the adjacent Children's Hospital and in the office files of 8 hand surgeons in Boston for the study years and identified 8 infants (7.3%) that had been missed by the Surveillance Program. There is also the possibility that classification of the mother as a nontransfer was incorrectly made by this surveillance program. This is unlikely because transfer status was based on having the research assistant read the mother's medical record. In that process, the nontransfers had earlier appointments in pregnancy at the hospital. In contrast, women transferred had brief medical records, often lived outside of the Boston area, and were often transferred to physicians known to the research assistant as having many transferred patients. Additionally, there is the possibility that a pregnant woman whose fetus was diagnosed prenatally as having a major malformation and who had planned to deliver at the hospital could have chosen to deliver at or have a termination of pregnancy at another facility. There is a potential for selection bias in that follow-up time differed across periods because postpartum stay decreased from 5 days to 2 days as time progressed. There is also potential for residual confounding from data not available in the database, such as maternal serum multiple (ie, alpha-fetoprotein marker) screening results.

The increasing trend over time in elective abortions for pregnancies with malformations has important public health implications. Surveillance programs of congenital anomalies must include elective abortions to avoid biased or imprecise findings from their data. The direction and magnitude of the bias and the level of accuracy vary according to a multitude of factors that characterize the study population and the particular anomaly being studied.¹⁷ The main objectives of surveillance programs are to establish baseline frequencies of major malformations, to evaluate the efficacy of public health treatment and prevention efforts (ie, folic acid supplementation for pregnant women to reduce the occurrence of neural tube defect pregnancies), to carry out studies of associated biomarkers and etiology, and to inform policy planning of public health efforts.⁵ These objectives are precluded by the exclusion of elective abortions in surveillance programs. At this time, the majority of state malformation surveillance programs in the United States do not identify or include malformed infants from pregnancies terminated after detection by prenatal screening as part of their annual tabulations of the occurrence of major malformations in infants.⁶

	Footnotes

 
Financial support included the Centers for Disease Control and Prevention through a grant to the Massachusetts Center for Birth Defects Research and Prevention (U50/CCU1132247-03).

Presented at the 2003 Annual Meeting of the Teratology Society.

The authors thank Brent A. Coull, phd, Angela E. Lin, md, Marlene A. Anderka, scd, Martha M. Werler, scd, Cathleen Higgins, and Ruby K. Dhillon, mph, for their contributions.

Received May 17, 2004. Received in revised form July 8, 2004. Accepted July 22, 2004.

doi:10.1097/01.AOG.0000142718.53380.8f

	REFERENCES

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2. McCandless SE, Brunger JW, SB Cassidy. The burden of genetic disease on inpatient care in a children's hospital. Am J Hum Genet 2004;74:121–7.[Medline]

3. Stoll C, Alembik Y, Dott B, Roth MP. Impact of prenatal diagnosis on livebirth prevalence of children with congenital anomalies. Ann Genet 2002;45:115–21.[Medline]

4. Farmer D. Fetal surgery: several conditions are proving amenable to treatment in this nascent field. BMJ 2003;46:461–2.

5. Cordero JF. Registries of birth defects and genetic diseases. Pediatr Clin North Am 1992;39:65–76.[Medline]

6. National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention. State Birth Defects Surveillance Programs Directory. Birth Defects Research (Part A). Clin Mol Teratol 2003;67:669–728.

7. Schechtman KB, Gray DL, Bary JD, Rothman SM. Decision-making for termination of pregnancies with fetal anomalies of 53,000 pregnancies. Obstet Gynecol 2002;99:216–21.[Abstract/Free Full Text]

8. Massachusetts Community Health Information Profile (MassCHIP) [Internet database]. The Massachusetts Department of Public Health c1995–2002 [updated 2003 Feb 2]. Available at: http://masschip.state.ma.us/. Accessed September 10, 2004.

9. Pryde PG, Nelson BI, Hallak M, Johnson MP, Odgers AE, Evans MI. Determinants of parental decision to abort or continue after non-aneuploid ultrasound detected fetal abnormalities. Obstet Gynecol 1992;80:52–6.[Abstract/Free Full Text]

10. Grevengood C, Shulman LP, Dungan JS, Martens P, Phillips OP, Emerson DS, et al. Severity of abnormality influences decision to terminate pregnancies affected with fetal neural tube defects. Fetal Diagn Ther 1994;9:273–7.[Medline]

11. Velie EM, Shaw GM. Impact of prenatal diagnosis and elective termination on prevalence and risk estimates of neural tube defects in California, 1989–1991. Am J Epidemiol 1996;144:473–9.[Abstract/Free Full Text]

12. McGuirk CK, Westgate MN, Holmes LB. Limb deficiencies in newborn infants. Pediatrics 2001;108:e64–56. Available at: http://www.pediatrics.org/cgi/content/full/108/4/e64. Accessed September 10, 2004.[Abstract/Free Full Text]

13. Limb CJ, Holmes LB. Anencephaly: changes in prenatal detection and birth status, 1972 through 1990. Am J Obstet Gynecol 1994;170:1333–8.[Medline]

14. Caruso TM, Westgate MN, Holmes LB. Impact of prenatal screening on the birth status of fetuses with Down syndrome at an urban hospital, 1972–1994. Genet Med 1998;1:22–8.[Medline]

15. Lin AE, Herring AH, Amstutz KS, Westgate MN, Lacro RV, Al-Jufan M, et al. Cardiovascular malformations: changes in prevalence and birth status, 1972–1990. Am J Med Genet 1999;84:102–10.[Medline]

16. Rasmussen SA, Bieber FR, Benacerraf BR, Lachman RS, Rimoin DL, Holmes LB. Epidemiology of osteochondrodysplasias: changing trends due to advances in prenatal diagnosis. Am J Med Genet 1996;61:49–58.[Medline]

17. Cragan JD, Khoury MJ. Effect of prenatal diagnosis on epidemiologic studies of birth defects. Epidemiology 2000;11:695–9.[Medline]

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Peller, A. J. Articles by Holmes, L. B. Search for Related Content PubMed PubMed Citation Articles by Peller, A. J. Articles by Holmes, L. B. Related Collections Epidemiology/public health Genetics and teratology Prenatal Diagnosis