Obstetrics & Gynecology:
Reconciling the High Rates of Preterm and Postterm Birth in the United States
Joseph, K S. MD, PhD; Huang, Ling MD, MSc; Liu, Shiliang MB, PhD; Ananth, Cande V. PhD, MPH; Allen, Alexander C. MD; Sauve, Reg MD, MPH; Kramer, Michael S. MD; for the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System
From the Perinatal Epidemiology Research Unit, Department of Obstetrics & Gynaecology and Pediatrics, Dalhousie University and the IWK Health Centre, Halifax, Nova Scotia, Canada; the Maternal and Infant Health Section, Division of Health Surveillance and Epidemiology, Public Health Agency of Canada, Ottawa, Ontario, Canada; the Division of Epidemiology and Biostatistics, Department of Obstetrics, Gynecology, and Reproductive Sciences, Robert Wood Johnson Medical School, University of Medicine and Dentistry of New Jersey, New Brunswick, New Jersey; the Department of Paediatrics and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada; and the Departments of Pediatrics and Epidemiology and Biostatistics, McGill University, Montreal, Quebec, Canada.
See related editorial on page 798.
Dr. Joseph is supported by a Peter Lougheed New Investigator award from the Canadian Institutes of Health Research. Dr. Ananth is partially supported through a grant (HD038902) from the National Institutes of Health. Dr. Kramer is a Senior Investigator of the Canadian Institutes of Health Research.
The authors thank the National Center for Heath Statistics for access to the U.S. data and the Vital Statistics Registrars of Canada for access to the Canadian data. Contributing members of the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System include Dr. Jane Evans and Russell Wilkins.
Presented at a meeting of the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System, April 20, 2006, Ottawa, Ontario, and at a meeting of the Society for Pediatric and Perinatal Epidemiologic Research, June 20–21, 2006, Seattle, Washington.
Corresponding author: Dr. K. S. Joseph, Division of Neonatal Pediatrics, IWK Health Centre, 5980 University Avenue, Halifax, Nova Scotia, Canada B3K 6R8; email: firstname.lastname@example.org.
OBJECTIVE: Preterm and postterm birth rates are substantially higher in the United States than in Canada and other industrialized countries, although relative mortality at preterm compared with term gestation is considerably lower. We attempted to explain these differences based on differences in the method of gestational age estimation.
METHODS: We used information on all live births in the United States and Canada for 1995–2002 and on singleton births and perinatal deaths for 1996–1999. Gestational age in Canada was based on the clinical estimate, whereas in the United States both menstrual-based and clinical estimates were used.
RESULTS: In 2002, preterm (12.3%) and postterm birth (6.6%) rates in the United States were far higher than in Canada (7.6% and 1.0%, respectively) when U.S. rates were based on menstrual dates. Differences were reduced or abolished when U.S. rates were based on the clinical estimate of gestation (10.1% and 1.0%, respectively). In Canada, the rate ratio for perinatal death at preterm compared with term gestation was 27.8 (95% confidence interval [CI] 26.3–29.3), similar to that in the United States when gestation was based on the clinical estimate (rate ratio 26.5, 95% CI 26.1–26.9, P value for difference in rate ratios=.06) but not when based on menstrual dates (rate ratio 18.9, 95% CI 18.7–19.2, P<.001).
CONCLUSION: Menstrual dates in U.S. data misclassify gestational duration and overestimate both preterm and postterm birth rates. For international comparisons, gestational age in the United States should be based on the clinical estimate.
Level of Evidence: II
Prevention of preterm birth (less than 37 completed weeks) is widely acknowledged as the most serious perinatal challenge facing industrialized countries.1,2 Despite a longstanding focus on preterm birth, several fundamental aspects of preterm birth remain poorly explained. One feature that has received little attention is the wide variation in rates of preterm birth among industrialized countries. Most notably, the rate of preterm birth in the United States far exceeds the rate in other industrialized countries: 12.3% in 20033 compared with 7.7% in 2003 in Canada,4 7.9% in 2003 in Australia,5 6.2% in France in 1998,6 7.4% in the Netherlands in 1999,6 6–7% in 2001 in New Zealand,7 7.3% in 2000 in Scotland,6 and 6.4% in 2000 in Sweden.6 Even larger differences are evident with regard to postterm birth (42 or more completed weeks): in 2003, 6.4% of live births in the United States were postterm,3 compared with 0.8% in Canada4 and 1.5% in Australia.5
Another puzzling comparison concerns mortality among preterm compared with term births. Previous studies have documented substantially lower mortality rate ratios in preterm compared with term births in the United States than in Canada.8 For instance, infant mortality rates among singleton live births at 32–33 weeks of gestation in the United States were 6.6 (95% confidence interval [CI] 6.1–7.0) times higher than infant mortality rates at term gestation but 15.2 (95% CI 13.2–17.5) times higher in Canada.8
In this study, we tested the hypothesis that differences in the method of gestational age estimation between the United States and Canada may contribute to differences in preterm birth rates, postterm birth rates, and relative mortality at preterm compared with term gestation.
MATERIALS AND METHODS
Data on all live births in the United States for the years 1995–2002 were obtained from the National Center for Health Statistics perinatal mortality data files. The data contained two estimates of gestational age: the menstrual-based estimate and the clinical estimate of gestational age. The former, typically used in routine national reports,3 is based primarily on the interval between the first day of the mother's last normal menstrual period and the date of birth (National Center for Health Statistics algorithm for gestational age based on last normal menstrual period). Gestational age is imputed by the National Center for Health Statistics for births with valid month and year but missing day of the last normal menstrual period.9,10 The clinical estimate of gestation is used if the last normal menstrual period is missing or if the last normal menstrual period–based gestational age is inconsistent with birth weight (used in 5.1% of births in 1995 and in 4.6% of births in 20029,10). The second estimate of gestational age is provided by the clinical estimate of gestational age, with the exact source of the estimate unspecified (ie, as to whether it is based on the obstetrician's physical examination of the mother, ultrasound-based estimate, or the pediatric examination of the newborn).
We used data on all live births in Canada from Statistics Canada's live births database for the years 1995–2002. Information in this database was obtained from birth registrations forwarded to Statistics Canada by provincial and territorial vital statistics registries.11 A single estimate of gestational age is provided in the live birth registration. This is supplied by the physician responsible for the delivery or by the mother and represents the best clinical estimate of gestational duration. Data for Canada excluded births from the province of Ontario because of documented problems with data quality.12,13
Rates of preterm birth (less than 37 completed weeks) and postterm birth (42 or more completed weeks) were computed for the United States and Canada. For the United States, preterm birth rates were calculated using both the menstrual and the clinical estimate of gestation after restricting the data to those records which 1) had a menstrual estimate of gestational age, 2) had a clinical estimate of gestational age, 3) were 20–50 weeks of gestation according to both the menstrual and clinical estimates of gestation, and 4) were 500 g or more in birth weight (to reduce potential bias due to differences in birth registration practices, especially at the borderline of viability14). The exclusion of records without a clinical estimate of gestation meant that births from California were not included in the study (because California does not provide the clinical estimate of gestation to National Center for Health Statistics). Separate rates of preterm and postterm birth in the United States were also calculated for non-Hispanic whites and non-Hispanic blacks.
Gestational age–specific rates of stillbirth, neonatal mortality, and extended perinatal mortality (stillbirth plus neonatal deaths) were calculated for the United States and Canada based on singleton births for the years 1996–1999 (the most recent years for which linked file data were available for both countries at the time of the study). Stillbirth files and linked live birth and infant death files from the National Center for Health Statistics and Statistics Canada were used for this purpose. We estimated mortality (stillbirth, neonatal death, and perinatal death) rates within standard gestational age categories (less than 37 weeks, 37 or more weeks; less than 28 weeks, 28–31 weeks, 32–33 weeks, 34–36 weeks, and 37 or more weeks). Mortality rate ratios (95% CIs) contrasting the mortality at preterm gestation (less than 37 weeks) to that at term (37 or more weeks) gestation were also estimated. The significance of observed differences between mortality rate ratios for Canada and the United States was assessed with the χ2 test for heterogeneity of the odds ratio.15 We also compared mortality using the fetuses-at-risk approach.16–19 Under this alternative framework, the denominator for the stillbirth or perinatal mortality rate at any gestation is the number of fetuses at that gestational age.18,19
Preterm birth rates in Canada increased from 7.0% in 1995 to 7.6% in 2002. This contrasted with preterm birth rates in the United States of 11.5% in 1995 and 12.3% in 2002 when gestational age was based on menstrual dates (Fig. 1). When preterm birth in the United States was based on the clinical estimate of gestation, the overall rate dropped to 9.1% in 1995 and 10.1% in 2002. The rate in 2002 was 9.5% among non-Hispanic whites and 14.2% among non-Hispanic blacks. Both menstrual and clinical estimates showed that preterm birth rates among non-Hispanic whites increased between 1995 and 2002, whereas rates among non-Hispanic blacks decreased in the later years of the study (Fig. 1).
Rates of postterm birth (42 or more weeks) in Canada declined from 2.5% in 1995 to 1.0% in 2002. The magnitude and pattern of decline in postterm birth in the United States (2.5% in 1995 and 1.0% in 2002) were identical to those in Canada when gestation was based on the clinical estimate (Fig. 2A). On the other hand, when postterm birth in the United States was based on menstrual dates, rates were several-fold higher than rates in Canada (8.6% in 1995 and 6.6% in 2002). Rates of postterm birth among non-Hispanic whites and non-Hispanic blacks were approximately similar and showed temporal declines, with rates based on menstrual dates being substantially higher than rates based on the clinical estimate.
Characteristics of the singleton population born between 1996 and 1999 in Canada and the United States are shown in Table 1. The proportion of births at more than 44 weeks of gestation (ie, implausibly high gestational ages) was less than 0.01% in Canada, 1.0% in the United States based on menstrual dates, and less than 0.01% in the United States according to the clinical estimate of gestation. The stillbirth rate in Canada was 45.5 per 1,000 total births at preterm gestation and 1.5 per 1,000 total births at term gestation (rate ratio 29.7, 95% CI 27.7–31.9, Table 2). The magnitude of this Canadian rate ratio was similar to the same rate ratio in the United States when gestational age was based on the clinical estimate (rate ratio 27.9, 95% CI 27.4–28.4, P value for difference in rate ratios=.06) but not when the U.S. rate ratio was estimated with menstrual-based gestational age (rate ratio 19.5, 95% CI 19.1–19.8, P value for difference in rate ratios<.001).
The same phenomenon was evident for neonatal death (Table 3). In Canada, the rate ratio for neonatal death at preterm relative to term gestation was 26.0 (95% CI 23.8–28.4), whereas in the United States it was 18.6 (95% CI 18.2–19.0, P value for difference in rate ratios<.001) for the menstrual-based gestational age estimate and 25.5 (95% CI 25.0–26.1) for the clinical estimate (P value for difference in ratio ratios=.68). Similarly, the rate ratio for perinatal death at preterm relative to term gestation was 27.8 (95% CI 26.3–29.3) in Canada, similar to that in the United States when based on the clinical estimate (rate ratio 26.5, 95% CI 26.1–26.9, P value for difference in rate ratios=.06) but not when based on menstrual dates (rate ratio 18.9, 95% CI 18.7–19.2, P value for difference in rate ratios<.001).
Stillbirth, neonatal mortality, and perinatal mortality rate ratios at mild (34–36 weeks) and moderate (32–33 weeks) preterm gestation were not significantly different between Canada and the United States when gestational age was based on the clinical estimate but significantly lower in the United States when based on menstrual dates (Table 4). Thus, the perinatal mortality rate ratio was 25.8 (95% CI 23.1–28.7) at 32–33 weeks compared with that at term in Canada and 24.8 (95% CI 24.2–25.5) in the United States when gestational age was based on the clinical estimate (P value for difference in rate ratios=.44). The rate ratio for perinatal mortality at 32–33 weeks compared with that at term gestation in the United States, with gestation based on menstrual dates, was 16.2 (95% CI 15.8–16.6), which was significantly different from that observed in Canada (P value for difference in rate ratios<.001). At very preterm gestation, however, this pattern did not hold; rate ratios for perinatal death at less than 28 weeks and at 28–31 weeks (compared with term gestation) were substantially and significantly higher in Canada compared with the United States, irrespective of how gestational age was estimated (Table 4). Thus, rate ratios for perinatal death at 28–31 weeks of gestation were 56.0 (95% CI 51.5–61.0) in Canada, 47.9 (95% CI 46.9–48.9) in the United States when based on the clinical estimate of gestation, and 34.3 (95% CI 33.6–35.0) in the United States when based on menstrual dates (P value for difference between the Canadian and the two U.S. rate ratios<.001 and <.001). This was true of stillbirth rate ratios and neonatal mortality rate ratios at very preterm gestation as well. Nevertheless, stillbirth, neonatal mortality, and perinatal mortality rate ratios at very preterm gestation were significantly higher in the United States (and closer to the Canadian estimates) when preterm birth was based on clinical estimates rather than on menstrual dates (Table 4).
Figure 3 shows incidence rates of birth and perinatal death in Canada and the United States based on the fetuses-at-risk approach. Birth rate patterns were more alike between Canada and the United States when gestational age for the latter was based on the clinical estimate of gestation. At the extremes of gestation, U.S. mortality rates based on the clinical estimate of gestation were closer to the Canadian rates.
Births from California constituted a majority of the live births excluded from the U.S. study population due to missing information on the clinical estimate of gestation (95.7% of live births excluded in 1995 and 98.6% of live births excluded in 2002 were from California). Menstrual dates showed that the rate of preterm birth among excluded live births was lower than in the remaining study population (10.8% and 10.3% in 1995 and 2002, respectively, among those with missing information on the clinical estimate of gestation compared with 11.5% and 12.3%, respectively, in the remaining population). The rate of postterm birth (based on menstrual dates) among those with missing information on the clinical estimate of gestation was 8.7% in 1995 and 7.5% in 2002, compared with 8.6% in 1995 and 6.6% in 2002 in the remaining population.
Our study shows that preterm and postterm birth rates in the United States are closer in magnitude to those in Canada (and other industrialized countries) than routine reports suggest. To a large extent, the observed variation in rates of preterm birth is a consequence of differences in the method of gestational age estimation. Preterm and postterm birth rates in Canada in 2002 were 7.6% and 1.0%, respectively, whereas those in the United States in 2002 were 10.1% and 1.0%, respectively, when the clinical estimate of gestation was used to define gestational age. Non-Hispanic whites had preterm and postterm birth rates of 9.5% and 1.0%, respectively, and non-Hispanic blacks had rates of 14.2 and 1.0%, respectively, based on the clinical estimate. The U.S. rates excluded a substantial fraction of live births with missing information on the clinical estimate of gestation (primarily those from California). Because California has a relatively lower rate of preterm birth based on menstrual dates, we speculate that the inclusion of these live births would have further lowered the rate of preterm birth in the United States
Menstrual dates are prone to error for several reasons, including irregularity of menstrual cycles, delayed ovulation, bleeding in early pregnancy, unrecognized miscarriage, and poor recollection or related errors.20,21 These problems, along with data collection and transcription errors, inflate the rates of preterm and postterm birth in large perinatal datasets (eg, the postterm birth rate in the United States in 2003 was 6.4% based on menstrual dates3 compared with 1.5% in Australia5 and 0.8% in Canada,4 where gestational age is based on the clinical estimate).
Misclassification of term births as preterm births is also responsible for the well-known bimodality observed in the birth weight distribution at preterm gestation (Ananth CV. Menstrual versus clinical estimate of gestational age: temporal trends and variability in indices of perinatal outcomes in the United States, in press),22,23 besides contributing to the inflated preterm birth rate. The clinical estimate of gestation, on the other hand, is typically based on information from early ultrasonography or examination of the newborn infant, as well as menstrual dates. It thus represents the clinician's best estimate of gestational age and reduces the potential for misclassification. The bimodality of birth weight is not evident at preterm gestation when gestational age is based on the clinical estimate (Ananth, in press).23 The most serious drawback of the clinical estimate of gestation appears to be the absence of specification and standardization with regard to the mode of ascertainment (ie, whether from menstrual dates or early ultrasonography or neonatal examination). Also, the accuracy of the clinical estimate of gestation is limited by the availability of an early ultrasound measurement and various measurement errors.
One feature of gestational age estimation using menstrual dates is worthy of note. Errors in menstrual dates in large perinatal databases lead to an artifactually higher rate of preterm birth relative to preterm birth rates based on a clinical estimate of gestation. This is in contradistinction to menstrual estimates of preterm birth rates in hospital-based studies, which are lower than preterm birth rates based on early ultrasound estimates of gestational age.24,25 Menstrual dates in hospital-based studies contain errors due to delayed ovulation (more than 14 days after the last normal menstrual period), which is more frequent than early ovulation.26,27 Menstrual dates in vital statistics data sets, on the other hand, appear to be more seriously compromised because of additional errors in recall, data collection, and transcription, which misclassify a larger fraction of term births as preterm births.
Relative mortality rates also confirm that the clinical estimate of gestation is preferable for international comparisons of preterm birth and other gestational age–based outcomes. The rate ratio for perinatal mortality at preterm compared with term gestation is comparable between the United States and Canada when preterm birth in the United States is based on the clinical estimate of gestation but not when based on menstrual dates. The lower mortality among preterm births (relative to term births) in the United States when preterm birth is based on menstrual dates suggests that menstrual dating is responsible for the misclassification of some term births as preterm births. A somewhat different mortality pattern was observed at very preterm gestation (Table 4), which could indicate differences in the clinical estimates in Canada compared with the United States or true differences in perinatal mortality at early gestation, perhaps due to more aggressive clinical management in the United States
We had expected that relative mortality comparisons between Canada and the United States would be more informative when based on the fetuses-at-risk approach, given the causal nature of this latter model.18,19 In hindsight, it is apparent that this expectation was misplaced; the large denominator that characterizes this calculation at preterm gestation (ie, all fetuses at risk at that gestation) is insensitive to the relatively small amount of misclassification that occurs. On the other hand, the traditional calculation of gestational age–specific perinatal mortality, which uses births at a particular gestation as the denominator, is very sensitive to misclassified births since there are relatively few births occurring at preterm gestation.
Perinatal reports from Canada and other industrialized countries have embraced changes in the method of gestational age estimation. This initially led to demonstrated changes in the gestational age distribution (less even digit preference for weeks of gestation, eg, 37 weeks versus 36 weeks) and a decline in rates of preterm birth.28 The United States, on the other hand, has continued to report preterm birth rates using menstrual dates (while simultaneously collecting information on the clinical estimate of gestation). Aside from international comparisons, the continued use of menstrual-based gestational age in surveillance and research reports may have important implications for the United States even within its own borders. For instance, recent declines in preterm birth rates among non-Hispanic blacks in North Carolina (based on menstrual dates) have been interpreted as an artifact of improvements in data quality.29 However, the decline in preterm birth among non-Hispanic blacks in the United States based on the clinical estimate of gestation (14.8% in 2000 and 14.2% in 2002, Fig. 1) and other evidence related to trends in preterm birth subtypes (Joseph KS, Ananth CV. Re: “Preterm delivery rates in North Carolina: are they really declining among non-Hispanic African Americans?” [letter]. Am J Epidemiol 2005;161:1181)30 suggests that the decline may not be an artifact. The National Center for Health Statistics, cognizant of the advantages and shortcomings of the clinical and menstrual-based estimates of gestation, has recently proposed a new algorithm31 that further edits menstrual-based estimates of gestational age using the clinical estimate of gestation. Whereas the merits of alternative estimates of gestational age deserve scrutiny and debate, the purpose of international comparisons appears best served by the clinical estimate of gestation, because that is the only estimate collected in many countries (including Canada). Nevertheless, the absence of a clinical estimate of gestation for births from California means that national temporal trends of preterm birth, postterm birth, and related indices in the United States have to be based on menstrual estimates of gestational age.
Although differences between menstrual-based and clinical estimates of gestation are well recognized, the discrepancy between the high rates of preterm and postterm birth in the United States and the more modest rates in other industrialized countries, such as Canada, has never before been explained on the basis of differences in the method of gestational age ascertainment. Any change in the method of gestational age estimation in the United States would also require a reevaluation of the Healthy People 2010 goal for the preterm birth rate (currently set at 7.6%32), given the artificial nature of the reduction in preterm birth that would follow a change in definition of gestational age. Another issue of relevance to clinicians is the issue of fetal growth standards. Whereas clinicians typically work with the clinical estimate of gestation, the U.S. national fetal growth standard33 was created using the menstrual-based estimate of gestational age. If the U.S. fetal growth standard is recreated based on the clinical estimate of gestation, this will impact the identification and consequent management of small-for gestational-age and large-for-gestational-age fetuses and infants.
In summary, our study shows substantial differences in rates of preterm and postterm birth in Canada and the United States when gestational age in the United States is based on menstrual dates. The differences in preterm birth rates are reduced and those in postterm birth are eliminated when U.S. rates are based on the clinical estimate of gestation. More importantly, the rate ratio for perinatal death at preterm gestation compared with term gestation in the United States is very similar to that in Canada when gestational age is based on the clinical estimate. Our findings suggest that U.S. data on gestational age and its derivative indicators should be based on the clinical estimate, especially for all international comparisons.
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