Original Article

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Inadequate Prenatal Care Utilization and Risks of Infant Mortality and Poor Birth Outcome: A Retrospective Analysis of 28,729,765 U.S. Deliveries over 8 Years
Sarah Partridge, M.D., B.Sc. 1 Jacques Balayla, M.D. 1 Haim A. Abenhaim, M.D., M.P.H. 1
1 Centre for Clinical Epidemiology and Community Studies, Jewish

Christina A. Holcroft, Sc.D. 1

General Hospital, Montreal, Quebec, Canada Am J Perinatol 2012;29:787 794.

Address for correspondence and reprint requests Haim A. Abenhaim, M.D., M.P.H., F.R.C.S.C., Department of Obstetrics and Gynecology, Jewish General Hospital, McGill University, Pav H, 325, 5790 CoteDes-Neiges, Montral, QC H3S 1Y9, Canada (e-mail: haim.abenhaim@gmail.com).

Abstract

Keywords

prenatal care risk factors pregnancy outcome infant mortality population characteristics

Objective To evaluate the association between adequacy of prenatal care utilization and risk of fetal and neonatal mortality and adverse outcomes. Methods We conducted a population-based cohort study using the Center for Disease Control and Preventions Linked Birth-Infant Death and Fetal Death data on all deliveries in the United States between 1995 and 2002. Inclusion criteria were singleton births 22 weeks of gestation with no known congenital malformation. Inadequate prenatal care was dened according to the Adequacy of Prenatal Care Utilization Index, and its effect on fetal and neonatal death was estimated using unconditional logistic regression analysis adjusting for maternal age, race, education, and other confounding variables. Results During our 8-year study period, 32,206,417 births occurred, 28,729,765 (89.2%) of which met inclusion criteria. Inadequate prenatal care utilization occurred in 11.2% of expectant mothers, more commonly among women 20 years, black nonHispanic and Hispanic women, and those without high school education. Relative to adequate care, inadequate care was associated with increased risk of prematurity 3.75 (3.73 to 3.77), stillbirth 1.94 (1.89 to 1.99), early neonatal dearth 2.03 (1.97 to 2.09), late neonatal death 1.67 (1.59 to 1.76), and infant death 1.79 (1.76 to 1.82). Conclusion Risk of prematurity, stillbirth, early and late neonatal death, and infant death increased linearly with decreasing care. Given the population effect of this association, public health initiatives should target program expansion to ensure timely and adequate access, particularly for women 20 years, Black non-Hispanic and Hispanic women, and those without high school education.

Adequate prenatal care (PNC) is a widely accepted determinant of maternal and child health and a focus of public health programming, despite ongoing controversy over whether PNC prevents poor birth outcomes, particularly infant mortality. PNC is considered adequate, based on the American

College of Obstetricians and Gynecologists guidelines for prenatal visits in low-risk pregnancy, if it is initiated in the rst trimester with regular visits of increasing frequency as term approaches.1 There is an absence of high-quality evidence from randomized controlled trials to establish either

received October 27, 2011 accepted after revision February 29, 2012 published online July 26, 2012

Copyright 2012 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.

DOI http://dx.doi.org/ 10.1055/s-0032-1316439. ISSN 0735-1631.

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Adequacy of Initiation of PNC and Adequacy of Received Services (a ratio of PNC visits completed relative to those expected based on gestational age and the American Congress of Gynecologists and Obstetricians recommended PNC schedule for low-risk pregnancies). Deliveries were categorized by receipt of, in increasing order of PNC utilization, inadequate care (initiated after 4 months gestation or fewer than half of predicted visits), intermediate care (initiated prior to 4 months and between 50% and 79% of expected visits), adequate care (initiated by 4 months and 80 to 109% of expected visits), or adequate-plus care (initiated by 4 months and 110% or more of expected visits). A nal group, missing care data, was created for cases where PNC adequacy could not be calculated due to the absence of essential information. The following variables were used to calculate the APNCU with a previously published SAS algorithm distributed by Dr. Milton Kotelchuck, developer of the APNCU index14,15: gestational age at initiation of PNC (2-month intervals), total number of PNC visits (excluding hospitalizations), and the gestational age in weeks. In the event of missing gestational age data, the gestational age was imputed from the sex and birth weight. Improbable birth weight (less than 250 g and more than 4999 g) was corrected for. Birth outcomes included small for gestational age (SGA) and intrauterine growth restriction (IUGR), respectively de ned as birth weight below the 10th and 3rd percentiles, and large for gestational age (LGA), de ned as birth weight above the 90th percentile, using a standard reference developed for male and female singleton births.16 Preterm birth was de ned as live birth under 37 weeks gestation. Stillbirth was de ned, based on the 1950 World Health Organization de nition, as an intrauterine demise irrespective of the duration of pregnancy and excluding all induced terminations of pregnancy. Stillbirths with missing gestational age data were proportionally distributed across gestational ages and thus were unlikely to represent a signi cant confounding factor. Early neonatal death was de ned as any infant death that occurred from birth to 7 days; late neonatal as death between 7 and 27 days; and infant death as any fatality between birth and 365 days of life. Deliveries that had incomplete records were included in the analysis, through the creation of dummy values to represent missing data. Our analysis was conducted in three steps. First, we performed descriptive statistics for the annual frequency distribution of APNCU categories from 1995 to 2002. Second, we did a sensitivity analysis to investigate the robustness of our ndings, as there was possible bias introduced by incomplete or inconsistent data collection. We examined the maternal and gestational characteristics of each APNCU class. These characteristics were the maternal age (10-year intervals), maternal race (white non-Hispanic, black non-Hispanic, Hispanic, or other non-Hispanic), maternal education (in years), marital status (married, not married), parity (zero, one, two, three or more prior births), smoking during the pregnancy (yes, no), and alcohol consumption during the pregnancy (yes, no). Finally, we performed logistic regression analysis to estimate the crude and adjusted odds ratio of eight poor birth outcomes for each APNCU category. All outcomes

Materials and Methods

We conducted a retrospective cohort study for 8 consecutive years, from 1995 to 2002, using the Birth Cohort Linked Birth-Infant Death and the Fetal Death data les from the National Center for Health Statistics (Centers for Disease Control and Prevention). The birth cohort les contain information on 3.5 million live births per year to residents and nonresidents in the United States. This information is obtained from the birth certi cate and is available for all births. The infant death le contains information on all infant deaths in the United States and can be linked to its corresponding birth record in the birth cohort through a unique identi er. The fetal death cohort le contains the record on all fetal deaths and can be readily appended to the live birth cohort le to obtain a nal cohort containing all deliveries, whether born dead or alive. We selected from these databases all records for the contiguous United States, Hawaii, and Alaska. The territories Puerto Rico, Guam, and the Virgin Islands were excluded from our cohort. Furthermore, our analysis did not include births of U.S. citizens outside of the United States. This resulted in an aggregate of 32,206,417 deliveries. We then sequentially excluded all nonsingleton gestations (1,287,495); deliveries that occurred prior to 22 weeks (317,135) or after 44 weeks of gestational age (944,273) and those with a congenital anomaly reported on the birth certi cate (1,244,884). This resulted in an 8-year cohort of 28,729,765 deliveries. The variables used in this analysis were de ned as follows. The APNCU index is a sum of two independent dimensions:
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the overall bene t of PNC or what frequency or content of care has maximal bene t. Observational and retrospective cohort studies have yielded con icting results: Some failed to establish prevention of poor outcomes,24 but others showed that minimal or no PNC is associated with low birth weight, preterm birth, or being small for gestational age.49 Trials comparing reduced to standard PNC had insuf cient power to expose associations with infant mortality.10,11 Limitations in the de nition and measurement of adequate care may underlie these con icting results. Despite dramatic declines in U.S. infant mortality rates over the past 50 years, there has been an increasing disparity in infant mortality rate by race and maternal education, which has been thought to be in part due to discrepancies in access to or utilization of adequate PNC.12 Unfortunately, given the paucity of evidence measuring associations between PNC and perinatal mortality, justication for public health initiatives promoting the implementation of programs increasing access to timely and adequate PNC may be limited given the increasing overall costs of health care in Westernized countries. The purpose of our study was thus to measure the rates of inadequate PNC as dened by the Adequacy of Prenatal Care Utilization (APNCU) index and estimate the magnitude of the relationship between inadequate care and fetal and neonatal mortality.13 We used a large administrative database of over 32 million births over 8 years to ensure sufcient power to detect differences in mortality that may exist.

Inadequate Prenatal Care Utilization

were modeled separately. We de ned adequate care as the reference group and calculated 95% con dence intervals. The eight outcomes of interest were: SGA, IUGR, LGA, preterm birth, stillbirth, early neonatal death, late neonatal death, and infant death. All outcomes were adjusted for maternal age, maternal race, maternal education, marital status, parity, maternal smoking, or alcohol consumption during pregnancy. All analyses were conducted using SAS version 9.2 (SAS Institute, Cary, NC). This protocol was approved by the Medical Research Ethics Department of the Jewish General Hospital in Montreal, Quebec.

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Results
Of the 32,206,417 births recorded during our 8-year study period, 28,729,765 (89.2%) met the study inclusion criteria. In the rst analysis, we examined the frequency distribution of deliveries from 1995 to 2002 by APNCU class. Despite annual uctuations in the relative proportions of each class, the percent annual frequency of the intermediate and adequate care groups was relatively stable over 8 years (Fig. 1). Inadequate care showed modest decreases each year, changing overall from 11.8% in 1995 to 10.74% in 2002; this was offset by an increase in adequate-plus care from 27.6% in 1995 to 30.0% in 2002. Table 1 summarizes sociodemographic and gestational characteristics by APNCU group. The proportion of mothers receiving inadequate care was greatest among those under 15 and 15 to 19 years of age, black non-Hispanic or Hispanic, not married, with less than 12 years of education, with three or more prior live births, and with smoking or drinking alcohol during the pregnancy. Among those who received adequate care, there were proportionately more mothers who were 30 to 39 years old, white non-Hispanic, married, with greater than 16 years of education, who had one or fewer prior live births. Most mothers received adequate care: 12,374,128 (43.1%).

Discussion
Adequacy of PNC utilization is an important predictor of maternal and fetal health. Over an 8-year span from 1995 to 2002, a consistent annual decrease in rates of inadequate care was offset by a rise in rates of adequate-plus care. The proportion of mothers receiving inadequate care was greatest among women under 20 years of age who were black nonHispanic or Hispanic, were not married, had less than 12 years of education, had three or more prior live births, and smoked or drank alcohol during the pregnancy. Inadequate PNC was associated with increased risk for all adverse outcomes of interest. Risk of prematurity, stillbirth, early neonatal death,

Figure 1 Percent annual frequency by Adequacy of Prenatal Care Utilization (APNCU) class 1995 2002.

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Table 2 shows the odds ratio and frequency of stillbirth, infant mortality, and adverse outcomes by APNCU category. All outcomes were modeled separately; adequate care was used as the reference, and results were signi cant with p < 0.0001. Inadequate PNC was associated with increased risk of all adverse outcomes. Stillbirth, early neonatal death, late neonatal death, and infant death showed a linear increase in risk with decreasing PNC relative to adequate care. There was a bimodal distribution according to PNC, with the greatest risks associated with the adequate-plus care and missing care data groups. The adequate-plus care group had reduced risk of IUGR and SGA and more risk of LGA; this group also had a substantially increased risk of preterm birth. Adjusting for confounding variables reduced risk estimates for all outcomes (nonadjusted data not reported). Table 3 shows a subgroup analysis of 27,900,165 births at 34 or more weeks gestation, with odds ratio and frequency of stillbirth, early neonatal death, late neonatal death, and infant death by APNCU category. All outcomes were modeled and corrected for in a fashion identical to the analysis in Table 2 and were signi cant with p < 0.0001. The linear relationship between risk of adverse outcome and decreasing PNC was preserved; however, the odds ratios were notably smaller.

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Table 1 Baseline Characteristics by APNCU Prenatal Care Category

APNCU Category Missing Care Data (n 1,063,776), % Age (y) <15 1519 2029 3039 >39 Race White non-Hispanic Black non-Hispanic Hispanic Other non-Hispanic Unknown Marital status Married Not married Maternal education (y) 08 911 12 1315 >16 Prior live births None One Two Three or more 3.5 3.3 3.7 4.7 9.8 9.6 12.2 20.2 12.8 13.2 13.5 14.0 44.1 44.7 42.2 35.9 29.8 29.2 28.4 25.1 4.8 4.6 3.7 2.9 2.6 25.1 21.2 11.8 7.2 3.6 15.5 14.0 13.1 12.5 12.4 32.4 34.5 42.0 46.0 50.9 22.1 25.6 29.3 31.3 30.5 3.1 4.9 7.1 19.6 13.0 13.4 46.7 35.6 30.0 26.5 2.7 5.7 4.8 3.9 10.2 7.3 18.4 17.4 12.6 9.9 12.6 12.4 14.7 14.6 15.1 47.3 34.0 37.3 42.5 41.3 30.1 29.5 25.8 26.5 5.6 4.5 3.7 3.4 4.0 32.1 20.3 11.7 7.0 9.4 11.8 13.5 53.0 12.7 11.6 27.1 35.8 42.8 46.5 41.2 23.4 26.0 28.5 30.4 33.7 Inadequate Care (n 3,224,001), % Intermediate Care (n 3,765,225), % Adequate Care (n 12,374,128), % Adequate-Plus Care (n 8,302,635), %

Smoking during pregnancy Yes No Alcohol during pregnancy Yes No 5.1 3.8 23.7 11.2 13.1 13.1 35.3 43.2 22.7 28.7 3.8 3.8 16.6 10.6 13.1 13.0 38.0 43.7 28.4 28.9

Table values are percentages rounded to one decimal, thus not all rows sum to 100%.

late neonatal death, and infant death increased linearly with decreasing PNC. Inadequate PNC utilization was associated with an increased risk of poor birth outcomes; however, patients with above-adequate care and missing PNC data also had substantial risk. To date the most widely used indices of PNC utilization are the Kessner and the APNCU Index. The Kessner Index was developed in 197317 and largely did not show differences in outcome between groups, possibly secondary to inadequate separation of groups.15 In the 1990s, Kotelchuck proposed the APNCU Index as a modi cation of the Kessner: Its most interesting contribution is the distinction of patients with adequate-plus care who previously had been included in the adequate care group. The adequate-plus care group has since
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been demonstrated to have poor birth outcomes, and it has been suggested that inclusion of high-risk patients in the reference group may have obscured relationships between PNC and outcome.13 The APNCU has also been shown to generate a smaller inadequate care group than the Kessner, which is likely a more precise categorization.18 For these reasons, we elected to use the APNCU Index. Our nding of a signi cant association between PNC and infant mortality is consistent with that of a random sample from the 2003 Centers for Disease Control birth cohort, where inadequate care had a twofold increase in risk of infant mortality relative to adequate care.19 Our nding of a linear relationship between decreasing PNC and increasing risk of stillbirth, early neonatal death, late neonatal death, and infant

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Table 2 OR and Frequency of Outcome by APNCU Prenatal Care Category for the 19952002 Singleton Birth Cohort (n 28,729,765)
APNCU Category Inadequate Care (n 3,224,001) % 13.3 6.3 9.7 11.6 0.7 0.2 0.1 0.7 1.79 (1.761.82) 0.3 0.3 1 1.14 (1.121.17) 1.67 (1.591.76) 0.0 0.0 1 1.08 (1.021.15) 2.03 (1.972.09) 0.1 0.1 1 1.20 (1.161.24) 1.94 (1.891.99) 0.3 0.3 1 1.21 (1.181.25) 1.20 (1.191.20) 8.7 10.7 1 0.80 (0.800.80) 1.11 (1.111.12) 9.4 7.2 1 6.1 17.4 0.6 0.3 0.1 0.6 1.26 (1.251.27) 1.30 (1.291.31) 5.7 3.7 1 3.1 1.48 (1.471.49) 3.75 (3.733.77) 3.5 3.1 1 22.5 1.05 (1.041.06) OR (95% CI) % OR (95% CI) % Reference % Intermediate Care (n 3,765,225) Adequate Care (n 12,374,128) Adequate-Plus Care (n 8,302,635) OR (95% CI) 9.10 (9.079.13) 0.78 (0.780.79) 0.80 (0.790.80) 1.80 (1.791.80) 2.24 (2.202.29) 3.07 (3.003.14) 2.52 (2.432.61) 2.22 (2.192.26)

Missing Care Data (n 1,063,776)

OR (95% CI)

Preterm birth

16.3

4.77 (4.744.81)

IUGR

5.3

1.10 (1.091.11)

SGA

8.5

1.03 (1.021.04)

LGA

12.2

1.20 (1.191.21)

Stillbirth

1.0

1.07 (1.031.10)

Early neonatal death

0.6

4.44 (4.294.59)

Late neonatal death

0.1

2.80 (2.632.98)

Infant death

1.0

2.83 (2.772.90)

Each outcome modeled separately. All p <0.0001. Adjusted for maternal race, maternal age, marital status, maternal education, prior live births, and maternal smoking and maternal alcohol in pregnancy. APNCU, Adequacy of Prenatal Care Utilization; CI, condence interval; IUGR, intrauterine growth restriction; LGA, large for gestational age; OR, odds ratio; SGA, small for gestational age.

Table 3 Births at 34 or More Weeks Gestation: OR and Frequency of Outcome by APNCU Prenatal Care Category for the 19952002 Singleton Birth Cohort (n 27,900,165)
APNCU Category Inadequate Care (n 3,224,001) % 0.24 0.06 0.05 0.42 1.72 (1.621.82) 1.45 (1.361.55) 1.56 (1.531.60) 1.76 (1.691.82) OR (95% CI) % 0.16 0.04 0.03 0.23 Intermediate Care (n 3,765,225) OR (95% CI) 1.32 (1.271.38) 1.23 (1.161.30) 1.11 (1.041.19) 1.14 (1.111.17) % 0.11 0.03 0.03 0.18 Adequate Care (n 12,374,128) Reference 1 1 1 1 % 0.16 0.05 0.04 0.25 Adequate-Plus Care (n 8,302,635) OR (95% CI) 1.46 (1.411.50) 1.63 (1.561.71) 1.42 (1.341.49) 1.34 (1.321.37)

Missing Care Data (n 1,063,776)

OR (95% CI)

Stillbirth

0.47

0.68 (0.66 0.72)

Early neonatal death

0.09

2.27 (2.112.45)

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Late neonatal death

0.05

1.60 (1.451.77)

Infant death

0.36

1.59 (1.531.65)

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Each outcome modeled separately. All p <0.0001. Adjusted for maternal race, maternal age, marital status, maternal education, prior live births, maternal smoking and maternal alcohol in pregnancy. APNCU, Adequacy of Prenatal Care Utilization; CI, con dence interval; OR, odds ratio.

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relative risk, as the bias of inclusion of missing data are toward the null. One limitation of the APNCU index is a previously described gestational age bias. Gestational age affects categorization within the index and could be expected to have a greater effect on some outcomes of interest, such as low birth weight, than adequacy of PNC. Short gestation may result in delivery before the opportunity to initiate care or misclassi cation in the adequate-plus category, as fewer visits are recommended in early pregnancy and 110% utilization could be met with one extra visit. Postdate gestations would require more visits and thus be less likely to meet criteria for inclusion in the adequate-plus group. Our nding of a ninefold increase in preterm birth for the adequate-plus group relative to the adequate group likely re ects this bias, and caution should be used in the interpretation of prematurity risks in this context. Gestational age bias can be overcome by the use of dependant variables that correct for gestational age, such as SGA in place of low birth weight,10,19,34,35 as we did in this study. A comparison of four adequacy of care indices, including the Kessner and the APNCU, showed comparable association between PNC and SGA across indices, demonstrating the robustness of this measure.19 Limitations of this study include the potential for an ecological fallacy, whereby relationships between PNC and outcome for the U.S. population as a whole may not apply to subpopulations; there is evidence that some groups are at greater risk for poor birth outcomes in the absence of PNC, and these relationships bear further investigation.36 Use of birth and death certi cate data limited our assessment to an analysis of adequacy as de ned by utilization, rather than the content of PNC. Reporting bias is also possible, as an independent assessment of the quality of national birth record data was not performed, and misclassi cation and measurement error have previously been reported with birth certi cate data: 5.1% of prenatal visits were missing in birth certi cates relative to chart review in a sample of low-risk pregnancies in Washington state from 1988 to 1989.37 In a study comparing birth certi cate data to medical records in New York for 1999, the date of initiation of care was concordant within 1 week for 76% of records; however, there was only a 38% absolute concordance for the number of prenatal visits, which increased to 70% with a two-visit range; last, the last menstrual period was correct 87% of the time and was 93% accurate with a 1-week range.38 Fortunately the large sample size this data affords was suf cient to expose signi cant associations even with this source of statistical noise. Our study is, however, unique in that it has considerable power to nd associations with relatively rare outcomes. In conclusion, this is the largest population-based cohort study to date to evaluate the association between adequacy of PNC utilization and the risk of adverse outcomes. We found a strong linear association between inadequate PNC and increased risk of prematurity, stillbirth, and neonatal and infant mortality. This increase in risk may have a small effect for individual mothers, but the population-level effect in a country with more than 3.5 million annual singleton deliveries is substantial. Mothers who disproportionately receive

death supports a direct relationship. The relative risks of adverse neonatal and infant outcomes by APNCU class were smaller in a subgroup analysis of births at 34 or more weeks gestation, suggesting that an association between inadequate PNC and prematurity is involved in some poor outcomes. The relationship between level of PNC and birth outcomes can be accounted for in a variety of ways. Some components of PNC are clearly protective, such as diagnosis and treatment of maternal genital tract infection,20 HIV infection,21 or promotion of exclusive breast-feeding.22 Another possibility is that a maternal factor, such as care-seeking behavior, could, in association with other health-promoting behaviors, account for differential risk.2,23 This possibility is reinforced by evidence that utilization of PNC is associated with increased utilization of preconception care, infant care, and infant vaccination.2426 This healthy adherer bias was recently described through a meta-analysis showing that patients who adhere to drug therapy have lower all-cause mortality, even when that therapy is a placebo, suggesting that patient adherence may itself be a surrogate for health-promoting behaviors.27 Adoption of PNC is likely multifactorial and can be predicted by factors such as having an unplanned pregnancy, late recognition of pregnancy, race, socioeconomic status, and geographic location.2831 Demographic characteristics disproportionately prevalent in the inadequate care group likely re ect underlying heterogeneity in this group, ranging from mothers under 15 years of age to multiparous women who may not appreciate the need for PNC. Our study showed that women with adequate-plus PNC have an increased risk of perinatal mortality. It has previously been suggested that this group contains disproportionately more identi ed high-risk pregnancies that required more prenatal visits and subsequent interventions.13,15 This possibility is supported by our nding that this group also had increased risk of LGA, perhaps re ecting macrosomic infants of diabetic mothers who are likely to be more closely followed both before and during the pregnancy than women who were not diabetic. There may also be an iatrogenic contribution to poor birth outcomes seen with above-adequate PNC: Maternal care providers who are categorized as more aggressive testers have a greater incidence of low birth weight, even after risk factors were controlled for.32 An element of all studies that use large administrative databases is the treatment of missing data. In their analysis of Californian births, Gould et al found that incomplete records were an independent and linearly related risk marker for infant mortality.33 For this reason, we did not exclude deliveries with incomplete records from our analysis and elected to treat those with missing PNC data as a separate subset of the population. This missing care data group had the highest relative risk for early and late neonatal and infant death. This relatively small subpopulation, with 1,063,776 deliveries over 8 years, may represent an important subset of high-risk mothers who are largely unknown to the health care system or a bias toward underdocumentation in some at risk groups. With respect to cases where PNC data were available, our results remained signi cant despite the inclusion of missing variables and likely underrepresent the true
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inadequate care were under 20 years of age, black nonHispanic and Hispanic women, and those without high school education. Given the population effect of this association, public health initiatives should target program expansion to ensure timely and adequate access to adequate PNC, particularly for women at risk.

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19 VanderWeele TJ, Lantos JD, Siddique J, Lauderdale DS. A compari-

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