Email updates

Keep up to date with the latest news and content from BMC Pregnancy and Childbirth and BioMed Central.

Open Access Research article

Inadequate prenatal care and its association with adverse pregnancy outcomes: A comparison of indices

Maureen I Heaman125*, Christine V Newburn-Cook3, Chris G Green45, Lawrence J Elliott56 and Michael E Helewa2

Author Affiliations

1 Faculty of Nursing, Room 217 Helen Glass Centre for Nursing, University of Manitoba, Winnipeg, Manitoba, R3T 2N2 Canada

2 Department of Obstetrics, Gynecology, and Reproductive Sciences, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba, Canada

3 Faculty of Nursing, University of Alberta, Edmonton, Alberta, Canada

4 Manitoba Agriculture, Food and Rural Initiatives, Winnipeg, Manitoba, Canada

5 Department of Community Health Sciences, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba, Canada

6 Department of Medical Microbiology, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba, Canada

For all author emails, please log on.

BMC Pregnancy and Childbirth 2008, 8:15  doi:10.1186/1471-2393-8-15

The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2393/8/15


Received:15 June 2007
Accepted:1 May 2008
Published:1 May 2008

© 2008 Heaman et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

The objectives of this study were to determine rates of prenatal care utilization in Winnipeg, Manitoba, Canada from 1991 to 2000; to compare two indices of prenatal care utilization in identifying the proportion of the population receiving inadequate prenatal care; to determine the association between inadequate prenatal care and adverse pregnancy outcomes (preterm birth, low birth weight [LBW], and small-for-gestational age [SGA]), using each of the indices; and, to assess whether or not, and to what extent, gestational age modifies this association.

Methods

We conducted a population-based study of women having a hospital-based singleton live birth from 1991 to 2000 (N = 80,989). Data sources consisted of a linked mother-baby database and a physician claims file maintained by Manitoba Health. Rates of inadequate prenatal care were calculated using two indices, the R-GINDEX and the APNCU. Logistic regression analysis was used to determine the association between inadequate prenatal care and adverse pregnancy outcomes. Stratified analysis was then used to determine whether the association between inadequate prenatal care and LBW or SGA differed by gestational age.

Results

Rates of inadequate/no prenatal care ranged from 8.3% using APNCU to 8.9% using R-GINDEX. The association between inadequate prenatal care and preterm birth and LBW varied depending on the index used, with adjusted odds ratios (AOR) ranging from 1.0 to 1.3. In contrast, both indices revealed the same strength of association of inadequate prenatal care with SGA (AOR 1.4). Both indices demonstrated heterogeneity (non-uniformity) across gestational age strata, indicating the presence of effect modification by gestational age.

Conclusion

Selection of a prenatal care utilization index requires careful consideration of its methodological underpinnings and limitations. The two indices compared in this study revealed different patterns of utilization of prenatal care, and should not be used interchangeably. Use of these indices to study the association between utilization of prenatal care and pregnancy outcomes affected by the duration of pregnancy should be approached cautiously.

Background

Prenatal care (PNC) is a frequently used health service that has the potential to reduce the incidence of perinatal morbidity and mortality by treating medical conditions, identifying and reducing potential risks, and helping women to address behavioral factors that contribute to poor outcomes[1]. Prenatal care is more likely to be effective if women begin receiving care in the first trimester of pregnancy and continue to receive care throughout pregnancy, according to accepted standards of periodicity [1]. The Society of Obstetricians and Gynecologists of Canada (SOGC) recommends that women receive PNC visits every 4 to 6 weeks in early pregnancy, every 2 to 3 weeks after 30 weeks' gestation, and every 1 to 2 weeks after 36 weeks' gestation [2], whereas the American Academy of Pediatrics (AAP) and American College of Obstetricians and Gynecologists (ACOG) recommend that a woman with an uncomplicated pregnancy be examined every 4 weeks for the first 28 weeks of pregnancy, every 2 to 3 weeks until 36 weeks gestation, and weekly thereafter[3]. Accurate measurement of PNC utilization is critical in monitoring trends and assessing the relationship between prenatal care services and pregnancy outcomes [4]. At least four indices have been developed to measure utilization of PNC [5-8], each of which uses the month that care begins and the total number of visits adjusted relative to gestational age at delivery, to assign women to categories such as "inadequate", "intermediate", "adequate", and "intensive" PNC. However, use of the Kessner index [5] and the graduated index of PNC utilization (GINDEX)[7] have largely been abandoned because the restricted nine-visit coding limitation of these indices inaccurately classifies the PNC utilization of term and post-term pregnancies [8,9]. The Adequacy of Prenatal Care Utilization (APNCU) index [6] and the revised GINDEX (R-GINDEX) [8] are both currently used to measure utilization of PNC.

Several studies using the PNC utilization indices have demonstrated an association between inadequate PNC and preterm birth or low birth weight (LBW) [10-16]. However, some investigators have questioned the use of these indices in determining an association with outcomes that are highly influenced by gestational age, such as preterm birth and LBW [9,17]. Interestingly, the outcome of small for gestational age (SGA) infants has been explored in only a few studies [17-19], even though this outcome by definition is adjusted for gestational age [17].

Several studies in the United States have reported on rates of inadequate PNC, while other studies have compared two or more of the indices in monitoring utilization of PNC [4,6,8,20]. In Canada, there are no national data on utilization of PNC [21], and only a few studies have examined rates of inadequate PNC. One study estimated that about 8.0 to 9.0% of pregnant women in Winnipeg, Manitoba received inadequate PNC in 1987–88 [22], while rates ranged from 4.4 to 10.6% in 1987–88 in a British Columbia study [23]. No studies have compared the PNC utilization indices in a Canadian context. Therefore, the objectives of this study were:

• To determine rates of PNC utilization in Winnipeg, Manitoba from 1991 to 2000;

• To compare the two most commonly used indices of PNC utilization in identifying the proportion of the population receiving inadequate PNC;

• To determine the association between inadequate PNC and preterm birth, low birth weight (LBW), and small-for-gestational age (SGA), using each of these indices; and

• To assess whether or not, and to what extent, gestational age modifies the association between inadequate PNC and LBW or SGA.

Methods

We conducted a population-based cohort study of women having a hospital-based singleton live birth in Winnipeg, Manitoba over a ten-year period, from 1991 to 2000. Winnipeg is the capital city of the province of Manitoba, and had a population of 618,477 residents in 1996 [24]. Data sources for this study consisted of a linked mother-baby database constructed from hospital discharge abstract data and a physician claims file maintained by Manitoba Health. The project received approvals from the University of Manitoba Research Ethics Board and the Health Information and Privacy Committee of Manitoba Health.

There were 83,101 births to women residing in the city of Winnipeg from 1991 to 2000. After eliminating cases with missing or out-of-range gestational age (< 18 weeks or > 45 weeks), missing parity, maternal age less than 12 years, stillbirths or multiple births, and birth weight <400 grams but gestation >22 weeks, the final sample consisted of 80,989 births. Several mothers (37.6%) gave birth to more than one child during the ten years, and all these births were included in the analyses.

We combined two sources of data in order to estimate the number and timing of prenatal visits. We first recorded the gestational age at first visit and the total number of prenatal visits from the linked mother-baby database. These data were abstracted from the prenatal record as part of the hospital discharge abstract data system. However, several limitations of these data have been documented, including a high percent of missing information and an underestimate of timing of the first prenatal visit and total number of visits [25]. We therefore supplemented the information with data from the physician claims database. For women who received care from physicians billing on a fee-for-service basis, we determined the number of episodes of care by recording office visit tariff codes that were linked to an ICD-9-CM code indicating pregnancy (ICD-9-CM codes 640–648, 650–659, 660–669, V22, V23), and any consultation visits linked to a physician code for obstetrician/gynecologist and an ICD-9-CM code indicating pregnancy. In addition, because many physicians billed for PNC using a global tariff during the time frame of this study, direct billing of in-office or laboratory diagnostic tests was used as a surrogate measure of a PNC visit, adapted from a method previously used and validated by Mustard [25]. Finally, we determined the total number of prenatal visits by using whichever estimate of the number of visits was greater, and whichever estimate of gestational age at first visit was earlier, based on these two methods. Gestational age at delivery was determined from the newborn record. These three variables were then used to calculate the following indices of PNC utilization:

1. The Adequacy of Prenatal Care Utilization (APNCU) index, proposed by Kotelchuck[6], is comprised of two parts: the month in which PNC is initiated and the number of visits from initiation of care until delivery. Inadequate utilization is defined as either starting PNC after the 4th month of pregnancy or receiving less than 50% of expected visits based on the schedule of PNC visits recommended by ACOG [3,26]. Intermediate care is care begun by month 4 and with between 50–79% of expected visits received; adequate care is that begun by month 4 and with 80–109% of expected visits received; intensive (adequate plus) care is begun by month 4 and with 110% or more of expected visits received.

2. The revised GINDEX (R-GINDEX), proposed by Alexander and Kotelchuck [8], has six categories of care: "no care," "inadequate," "intermediate," "adequate," "intensive," and "missing." The R-GINDEX is based on the full ACOG recommendation, rather than the flawed Kessner index coding strategy of a 9-visit limit. For example, at 40 weeks gestation, a woman who began prenatal care in the first 3 months and received between 13 to 16 visits would be categorized as having adequate care, whereas a woman who began care between 1 to 6 months of pregnancy and had less than 8 visits would be categorized as having inadequate care. The intensive care category includes women who have an unexpectedly large number of PNC visits, which may indicate potential morbidity or complications. Women whose number of visits is approximately one standard deviation above the mean number of visits for each trimester of initiation and gestational age at delivery are labeled as intensive care users [4].

Algorithms for calculating both of these indices have been published [7,8]. Once the two indices were calculated, we then compared the proportion of cases assigned to each category by the indices from 1991 to 2000.

Differences in rates of inadequate/no PNC by maternal age and parity were calculated. SGA births (birth weight less than 10th percentile for gestational age) were determined using a population-based Canadian reference [27]. Logistic regression analysis with generalized estimating equation parameter estimates (GEE) was used to determine the association between inadequate/no PNC, using both indices, and birth outcomes (preterm birth, LBW, and SGA) after controlling for maternal age and parity, and adjusting for more than one birth to the same mother (i.e., within-mother dependency). Inadequate/no prenatal care was compared to the reference group of all other types of care (intermediate, adequate and intensive).

A stratified analysis was conducted to determine whether the association between inadequate/no PNC and LBW or SGA differed by gestational age. The Breslow-Day test of homogeneity was used to test the null hypothesis that the effect measure was uniform across strata [28].

Results

Table 1 compares the proportion of women assigned to various categories of PNC utilization based on the two indices. Only a small proportion of women (n = 293; 0.4%) received no care during the 10 years. The overall proportion of women assigned to the inadequate category varied slightly among the two indices, ranging from 7.9% for APNCU to 8.5% for R-GINDEX. The APNCU assigned a much higher proportion of women to the "intensive" care category (31.4%) than did the R-GINDEX (12.6%). Because of the small proportion of women receiving no care, the categories of inadequate and no care were combined for most of the remaining analyses. Table 2 summarizes the proportion of women with inadequate/no care by maternal age and parity. Women aged less than 20 years had the highest rates of inadequate/no care (ranging from 21.1% to 21.6%) while women aged 35 years and older had the lowest rates. Women with the highest level of parity (4 or more births) had the highest rates of inadequate/no PNC (ranging from 24.3% to 26.4%) while women having their first birth had the lowest rates.

Table 1. Rates of prenatal care utilization in Winnipeg, 1991–2000: A comparison of two indices

Table 2. Inadequate/no prenatal care utilization by maternal age and parity, Winnipeg, 1991–2000: A comparison of two prenatal care utilization indices

The proportion of preterm births and LBW by category of PNC varied among the two indices (Table 3), with highest rates in the no PNC group (15.0%). Using the APNCU, the rate of preterm birth in the inadequate care group (7.2%) was approximately double that of the adequate care group (3.5%). However, this was not true of the R-GINDEX, where the rate of preterm birth in the inadequate care group (6.1%) was lower than that in the adequate care group (8.8%). Using the APNCU, a high rate of preterm birth (10.8%) was also found in the intensive care category. The rate of SGA was more consistent across the indices, with the highest rate (18.8%) in the no care category and similar rates in the inadequate care category for the APNCU (13.0%) and the R-GINDEX (12.8%).

Table 3. Comparison of two prenatal care utilization indices: Percent of singleton live births assigned to each category and percent of preterm, low birth weight, and small-for-gestational age births among live births in each category, Winnipeg, 1991–2000

Table 4 reports the unadjusted and adjusted odds ratios (AOR) for the association between inadequate/no PNC care and pregnancy outcomes. Using the APNCU, the likelihood of preterm birth and LBW associated with inadequate or no PNC was significantly increased by 20% and 30% respectively (AOR 1.2 and 1.3). Using the R-GINDEX, there was no association between inadequate/no care and preterm birth (AOR 1.0) and a weak association with LBW (AOR 1.1). In contrast, both indices yielded the same result for the outcome of SGA, with the likelihood of SGA being significantly increased by 40% (AOR 1.40) among women with inadequate/no prenatal care.

Table 4. a – Odds ratios (OR) and 95% confidence intervals (CI) for association of inadequate/no prenatal care with preterm birth (< 37 completed weeks gestation)*b – Odds ratios (OR) and 95% confidence intervals (CI) for association of inadequate/no prenatal care with low birth weight (<2500 grams)*c – Odds ratios (OR) and 95% confidence intervals (CI) for association of inadequate/no prenatal care with small-for-gestational age (birth weight < 10th percentile for gestational age)*

The stratified analyses of the association between inadequate/no PNC and SGA and LBW are reported in Tables 5 and 6 respectively. The odds ratios varied widely across gestational age categories, with the association between inadequate/no PNC and both LBW and SGA increasing towards term. The Breslow-Day test of homogeneity was significant for the association between APNCU and both SGA and LBW, and between R-GINDEX and SGA, indicating the presence of heterogeneity (non-uniformity) across strata. The Breslow-Day test for the association between R-GINDEX and LBW suggested a trend towards significance (p = 0.06) and the possibility of non-uniformity across strata.

Table 5. Odds ratios (OR) for association of inadequate/no prenatal care with SGA by gestational age category: Comparison of two prenatal care utilization indices.

Table 6. Odds ratios (OR) for association of inadequate/no prenatal care with LBW (<2500 grams) by gestational age category: Comparison of two prenatal care utilization indices.

Discussion

The proportion of cases assigned to PNC utilization categories varied using the two different indices. This finding is similar to the conclusions of Alexander and Kotelchuck [8] and Kogan et al [4]. Because the indices use different algorithms to define categories of PNC utilization, they yield different patterns of PNC use in a population and should not be used interchangeably [8]. This emphasizes the need to use caution in comparing results across studies that use different indices. The proportion of women assigned to each PNC utilization category remained fairly stable over the 10 years for both indices, although it is noteworthy that the number of births steadily declined over the 10 years, from 9,093 births in 1991 to 7,124 births in 2000. This declining birth rate is consistent with that reported in a provincial surveillance report for Manitoba, 1989–1998 [29].

The rates of inadequate and no PNC utilization among women in Winnipeg are lower than those reported in the United States, likely as a result of universal health care for residents of Manitoba. About 1.5 to 2.0% of pregnant women in the United States do not receive any PNC [30], compared to 0.4% among Winnipeg women in this study. Using the APNCU index, the rate of inadequate/no PNC in the United States declined from 12.8% in 1995 to 11.7% in 1999 [31], but these rates are still considerably higher than the 8.3% of women in Winnipeg who received inadequate/no PNC from 1991 to 2000 based on the APNCU index.

The association between inadequate/no prenatal care and LBW varied using the two indices, with AOR ranging from 1.1 using the R-GINDEX to 1.3 using the APNCU. Caution needs to be used in interpreting these results because our analyses also confirmed the presence of effect modification by gestational age for both indices, with the association between inadequate/no care and LBW becoming stronger as gestational age increased. Koroukian and Rimm state, "Although adjusting the number of prenatal visits for gestational length is clearly important to assess the adequacy of prenatal care utilization, we must be mindful of the bias introduced by its use in an Index, because the gestational length is itself a birth outcome that is so strongly correlated with birth weight"[17]. Alexander and Kotelchuck suggest the use of different analytical approaches to examine the relationship between prenatal care use and birth outcomes, such as gestational age-specific, life table, survival, and two stage least squares analyses, to help control for the influence of gestational age [9]. There is growing concern that the strength of the relation between PNC and LBW and preterm birth may be far less than previously assumed [32,33]. This lack of association may result because PNC, in its present form, has limited ability to reduce the proportion of LBW and preterm births; however, some evidence suggests that PNC may make a difference in term LBW rates [32,34]. This lack of association might also explain why efforts to prevent preterm birth and LBW through increased access to PNC have shown little benefit [35,36].

Of the three adverse pregnancy outcomes selected for this study, SGA may be the preferable outcome to study because by definition it adjusts for gestational age. However, our findings still showed some degree of effect modification by gestational age when studying the association between inadequate/no PNC and SGA, so the results should be interpreted with caution. After controlling for maternal age, parity, and within-mother dependency, women receiving inadequate/no PNC were up to 40% more likely to have a SGA birth compared to women receiving other categories of care. This result is consistent with the findings of a New Zealand study that less frequent attendance at PNC was associated with SGA [18]. The reason for the observed association between inadequate PNC and SGA births is not fully understood. However, it is likely that women who do not receive adequate PNC are less likely to receive appropriate treatment or preventive care. SGA births are associated with several potentially modifiable risk factors, such as low pre-pregnancy weight, low gestational weight gain, cigarette smoking, and recreational drug use [37,38]. Several of these risk factors may be mitigated or prevented with quality PNC.

As with most research, this study has limitations. First, administrative data are prone to a certain degree of coding errors and incomplete data, which may be random or contain systematic biases. The number and timing of PNC visits was estimated from hospital discharge abstracts and physician claims files, and the accuracy of our estimates may be affected by several factors, such as missing PNC records or receipt of PNC from non-physician providers. We were unable to differentiate missing data from no care using this approach. As well, inaccurate ascertainment of gestational age may affect assignment to a PNC utilization category or determination of a preterm or SGA birth. We compared the rate of adverse birth outcomes among women with inadequate/no PNC to the remainder of the population. However, Kotelchuck suggests there is a U-shaped relationship between PNC and birth outcomes, in which women with both fewer and greater number of visits than expected are at higher risks of having poorer birth outcomes [39], so perhaps limiting the reference group to women with adequate care should be considered in future research. Our analysis was limited to singleton live births; therefore, multiple births were not represented. In addition, a limitation of both PNC utilization indices is that they only reflect the quantity of PNC; they indicate nothing about the spacing of visits or the content, clinical adequacy, or quality of PNC [8]. These indices are based on the ACOG recommendations for number of visits for low risk pregnant women; the effectiveness of this standard has not been assessed through rigorous scientific testing, nor has adequacy of care for women with high risk pregnancies been operationalized [9]. Last, selection bias is a major difficulty in assessing the impact of PNC on pregnancy outcomes, in that women who receive adequate PNC may be more likely to experience better pregnancy outcomes because of other characteristics which have independent influences on pregnancy outcomes [38,40]. We were unable to control for maternal characteristics such as socioeconomic status, race/ethnicity, intendedness of pregnancy or health behaviors because information on these variables are not recorded in the databases.

Conclusion

The rates of no PNC and inadequate PNC are lower for women giving birth in Winnipeg, Canada, compared to rates reported for women in the U.S. The two indices compared in this study revealed different utilization patterns and resulted in varying degrees of association of inadequate PNC with adverse pregnancy outcomes. Selection of a PNC utilization index for research or program evaluation requires careful consideration of the methodological underpinnings and limitations of the chosen index [8]. Although these indices remain useful for studying trends in PNC utilization or evaluating the effectiveness of programs to enhance access to care, we concur with other investigators that use of these indices to study the association between utilization of PNC and birth outcomes affected by the duration of gestation should be approached with caution due to effect modification by gestational age [8,17]. In addition, "more refined future indices should incorporate parameters that reflect the qualitative aspects of PNC in addition to measuring number of visits" [8]. Future research should go beyond simply counting the number of visits and focus on studying the relationship between quality and content of PNC and pregnancy outcomes. There is a pressing need to develop a valid and reliable instrument to measure quality of PNC.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

MIH conceived of the study and supervised all aspects of its implementation. All authors contributed to conceptualizing ideas and designing the study, provided input regarding analysis of the data, interpreted findings, and reviewed drafts of the manuscript. All authors read and approved the final manuscript.

Acknowledgements

This study was funded by an operating grant from the Manitoba Health Research Council. Dr. Heaman is supported by a New Investigator award from the Canadian Institutes of Health Research. We would like to acknowledge Dr. Greg Alexander for his helpful suggestions regarding earlier versions of this manuscript, and Ms. Mary Cheang, MMath, for her assistance with statistical analysis.

References

  1. US Department of Health and Human Services: Healthy People 2010. Maternal, Infant, and Child Health. Chapter 16. Vol. II, 2nd ed. [http://www.healthypeople.gov/document/html/volume2/16mich.htm] webcite

    2000.

  2. Society of Obstetricians and Gynaecologists of Canada: SOGC Clinical Practice Guidelines: Healthy Beginnings: Guidelines for care during pregnancy and childbirth. Volume 71. Ottawa, SOGC; 1998.

  3. American Academy of Pediatrics and American College of Obstetricians and Gynecologists: Guidelines for Perinatal Care. 3rd edition. Elk Grove Village, IL, Author; 1992:1-279. OpenURL

  4. Kogan MD, Martin JA, Alexander GR, Kotelchuck M, Ventura SJ, Frigoletto FD: The changing pattern of prenatal care utilization in the United States, 1981-1995, using different prenatal care indices.

    Jama 1998, 279:1623-1628. PubMed Abstract | Publisher Full Text OpenURL

  5. Kessner D, Singer D, Kalk C, Schlesinger E: Infant death: An analysis by maternal risk and health care. In Contrasts in Health Status. Edited by Kessner D. Washington, D.C., Institute of Medicine; 1973. OpenURL

  6. Kotelchuck M: An Evaluation of the Kessner Adequacy of Prenatal-Care Index and A Proposed Adequacy of Prenatal-Care Utilization Index.

    Am J Public Health 1994, 84:1414-1420. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  7. Alexander GR, Cornely DA: Prenatal care utilization: its measurement and relationship to pregnancy outcome.

    Am J Prev Med 1987, 3:243-253. PubMed Abstract OpenURL

  8. Alexander GR, Kotelchuck M: Quantifying the adequacy of prenatal care: A comparison of indices.

    Public Health Rep 1996, 111:408-418. PubMed Abstract | PubMed Central Full Text OpenURL

  9. Alexander GR, Kotelchuck M: Assessing the role and effectiveness of prenatal care: history, challenges, and directions for future research.

    Public Health Rep 2001, 116:306-316. PubMed Abstract | PubMed Central Full Text OpenURL

  10. Gomez-Olmedo M, Delgado-Rodriguez M, Bueno-Cavanillas A, Molina-Font JA, Galvez-Vargas R: Prenatal care and prevention of preterm birth. A case-control study in southern Spain.

    Eur J Epidemiol 1996, 12:37-44. PubMed Abstract | Publisher Full Text OpenURL

  11. Barros H, Tavares M, Rodrigues T: Role of prenatal care in preterm birth and low birthweight in Portugal.

    J Public Health Med 1996, 18:321-328. PubMed Abstract | Publisher Full Text OpenURL

  12. Krueger PM, Scholl TO: Adequacy of prenatal care and pregnancy outcome.

    J Am Osteopath Assoc 2000, 100:485-492. PubMed Abstract | Publisher Full Text OpenURL

  13. Heaman MI, Blanchard JF, Gupton AL, Moffatt ME, Currie RF: Risk factors for spontaneous preterm birth among Aboriginal and non-Aboriginal women in Manitoba.

    Paediatr Perinat Epidemiol 2005, 19:181-193. PubMed Abstract | Publisher Full Text OpenURL

  14. El-Mohandes A, Herman AA, Nabil El-Khorazaty M, Katta PS, White D, Grylack L: Prenatal care reduces the impact of illicit drug use on perinatal outcomes.

    J Perinatol 2003, 23:354-360. PubMed Abstract | Publisher Full Text OpenURL

  15. Hulsey TC, Patrick CH, Alexander GR, Ebeling M: Prenatal care and prematurity: is there an association in uncomplicated pregnancies?

    Birth 1991, 18:146-150. PubMed Abstract | Publisher Full Text OpenURL

  16. Kotelchuck M: The Adequacy of Prenatal Care Utilization Index: its US distribution and association with low birthweight.

    Am J Public Health 1994, 84:1486-1489. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  17. Koroukian SM, Rimm AA: The "Adequacy of Prenatal Care Utilization" (APNCU) index to study low birth weight: is the index biased?

    J Clin Epidemiol 2002, 55:296-305. PubMed Abstract | Publisher Full Text OpenURL

  18. Gao W, Paterson J, Carter S, Percival T: Risk factors for preterm and small-for-gestational-age babies: A cohort from the Pacific Islands Families Study.

    J Paediatr Child Health 2006, 42:785-792. PubMed Abstract | Publisher Full Text OpenURL

  19. Panaretto K, Lee H, Mitchell M, Larkins S, Manessis V, Buettner P, Watson D: Risk factors for preterm, low birth weight and small for gestational age birth in urban Aboriginal and Torres Strait Islander women in Townsville.

    Aust N Z J Public Health 2006, 30:163-170. PubMed Abstract | Publisher Full Text OpenURL

  20. Alexander GR, Kogan MD, Nabukera S: Racial differences in prenatal care use in the United States: are disparities decreasing?

    Am J Public Health 2002, 92:1970-1975. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  21. Health Canada: Canadian Perinatal Health Report, 2003. Ottawa, Minister of Public Works and Government Services Canada; 2003.

  22. Mustard CA, Roos NP: The relationship of prenatal care and pregnancy complications to birthweight in Winnipeg, Canada.

    Am J Public Health 1994, 84:1450-1457. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  23. Katz SJ, Armstrong RW, LoGerfo JP: The adequacy of prenatal care and incidence of low birthweight among the poor in Washington State and British Columbia.

    Am J Public Health 1994, 84:986-991. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  24. Statistics Canada: Canadian Statistics - Population by year, by province and territory. [http://www.statcan.ca] webcite

    2006.

  25. Mustard C: The Utilization of prenatal care and relationships to birthweight outcome in Winnipeg, 1987-88. Winnipeg, Manitoba Centre for Health Policy and Evaluation; 1993:i-79.

  26. American College of Obstetricians and Gynecologists: Standards for Obstetric-Gynecologic Services.. Chicago, American College of Obstetricians and Gynecologists; 1974. OpenURL

  27. Kramer MS, Platt RW, Wen SW, Joseph KS, Allen A, Abrahamowicz M, Blondel B, Breart G: A new and improved population-based Canadian reference for birth weight for gestational age.

    Pediatrics 2001, 108:E35. PubMed Abstract | Publisher Full Text OpenURL

  28. Rothman K, Greenland S: Modern Epidemiology. 2nd edition. Philadelphia, Lippincott-Raven Publishers; 1998. OpenURL

  29. Manitoba Health: Manitoba Perinatal Health Surveillance Report 1989-1998: Provincial and Winnipeg Geographic Breakdown. Winnipeg, Manitoba Health Public Health Branch, Epidemiology Unit.; 2000. OpenURL

  30. Taylor CR, Alexander GR, Hepworth JT: Clustering of US women receiving no prenatal care: Differences in pregnancy outcomes and implications for targeting interventions.

    Maternal and Child Health Journal 2005, 9:125-133. Publisher Full Text OpenURL

  31. Ventura SJ, Martin JA, Curtin SC, Menacker F, Hamilton BE: Births: final data for 1999.

    Natl Vital Stat Rep 2001, 49:1-100. OpenURL

  32. Alexander GR, Howell E: Preventing preterm birth and increasing access to prenatal care: two important but distinct national goals.

    Am J Prev Med 1997, 13:290-291. PubMed Abstract OpenURL

  33. Alexander GR, Korenbrot CC: The role of prenatal care in preventing low birth weight.

    Future Child 1995, 5:103-120. PubMed Abstract | Publisher Full Text OpenURL

  34. Lu MC, Tache V, Alexander GR, Kotelchuck M, Halfon N: Preventing low birth weight: is prenatal care the answer?

    J Matern Fetal Neonatal Med 2003, 13:362-380. PubMed Abstract | Publisher Full Text OpenURL

  35. Goldenberg R: Low birthweight in minority and high-risk women: Patient Outcomes Research Team (PORT) final report. Washington, DC, Agency for Health Care Policy and Research; 1998.

  36. Ray WA, Mitchel EF Jr., Piper JM: Effect of Medicaid expansions on preterm birth.

    Am J Prev Med 1997, 13:292-7. PubMed Abstract OpenURL

  37. Newburn-Cook CV, White D, Svenson LW, Demianczuk NN, Boff N, Edwards J: Where and to what extent is prevention of low birth weight possible?

    West J Nurs Res 2002, 24:887-904. PubMed Abstract | Publisher Full Text OpenURL

  38. Kramer MS, Seguin L, Lydon J, Goulet L: Socio-economic disparities in pregnancy outcome: why do the poor fare so poorly?

    Paediatr Perinat Epidemiol 2000, 14:194-210. PubMed Abstract | Publisher Full Text OpenURL

  39. Kotelchuck M: Is the APNCU Index to study LBW biased or only the article by Koroukian and Rimm?

    J Clin Epidemiol 2003, 56:286-288. PubMed Abstract | Publisher Full Text OpenURL

  40. Shoham-Vardi I, Levy E, Belmaker I, Mazor M, Goldstein D: Utilisation of prenatal services and birth outcomes: a community-based study in Israel.

    Paediatr Perinat Epidemiol 1997, 11:271-286. PubMed Abstract | Publisher Full Text OpenURL

Pre-publication history

The pre-publication history for this paper can be accessed here:

http://www.biomedcentral.com/1471-2393/8/15/prepub