Published online March 12, 2007
PEDIATRICS Vol. 119 No. 4 April 2007, pp. e900-e906 (doi:10.1542/peds.2006-1123)
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ARTICLE

Declines in Low Birth Weight and Preterm Birth Among Infants Who Were Born to HIV-Infected Women During an Era of Increased Use of Maternal Antiretroviral Drugs: Pediatric Spectrum of HIV Disease, 1989–2004

Joann Schulte, DO, MPH, Ken Dominguez, MD, MPH, Thomas Sukalac, Beverly Bohannon, MS, BSN, Mary Glenn Fowler, MD for the Pediatric Spectrum of HIV Disease Consortium

Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. Our goal was to determine trends in low birth weight and preterm birth among US infants born to HIV-infected women.

METHODS. We used data from the longitudinal Pediatric Spectrum of HIV Disease, a large HIV cohort, to assess trends in low birth weight and preterm birth from 1989 to 2004 among 11321 study infants. Among women with prenatal care, we also assessed risk factors, including maternal antiretroviral therapy during pregnancy, that were predictive of low birth weight and preterm birth using univariate and multivariate logistic regression models.

RESULTS. Overall, 11231 of 14464 infants who were enrolled in Pediatric Spectrum of HIV Disease were tested during the neonatal period. From 1989 to 2004, testing increased from 32% to 97%. The proportion of HIV-exposed infants who had low birth weight decreased from 35% to 21% and occurred in all racial/ethnic groups. Prevalence of preterm birth decreased from 35% to 22% and occurred in all groups. Any maternal antiretroviral therapy use increased from 2% to 84%. Among 8793 women who had prenatal care, low birth weight was associated with a history of illicit maternal drug use, unknown maternal HIV status before delivery, symptomatic maternal HIV disease, black race, Hispanic ethnicity, and infant HIV infection. Antiretroviral therapy or lack of it was not associated with low birth weight. Among women with prenatal care, preterm birth was associated with a history of illicit maternal drug use, symptomatic maternal HIV disease, no antiretroviral therapy, receipt of a 3-drug highly active antiretroviral therapy regimen with protease inhibitors, black race, and infant HIV infection.

CONCLUSIONS. The proportion of infants who had low birth weight or were born preterm declined during an era of increased maternal antiretroviral therapies. These Pediatric Spectrum of HIV Disease trends differ from the overall increases in both outcomes among the US population.

Key Words: low birth weight • preterm birth • HIV-infected women

Abbreviations: LBW—low birth weight • HAART—highly active antiretroviral therapy • PI—protease inhibitor • PSD—Pediatric Spectrum of HIV Disease • ARV—antiretroviral therapy

The United States has one of the highest rates of low birth weight (LBW; <2500 g) and preterm birth (<37 weeks) among industrialized countries. Infants who have LBW or are born preterm have increased rates of morbidity and mortality.1 Prevalences of LBW and preterm birth, respectively, have risen to 8.1% and 12.5% as of 2004 in the general US population.2 The proportion of LBW has increased among white infants,3 as a result of assisted reproductive technology, but black infants still have higher LBW proportions.4 LBW is higher among certain risk groups, including women who use illicit drugs and/or have sexually transmitted diseases.5 Among US HIV-infected women, LBW percentages have been reported between 12% and 48%.6–11 Among US infants of HIV-infected women, reported prevalences of preterm birth are 13% to 38.3%.11–19

It is not known whether the prevalences of LBW and preterm birth among infants who are born to HIV-infected women have changed as drug therapy have evolved into regimens of highly active antiretroviral therapy (HAART). Some studies in Europe, the United States, and Latin America have suggested that protease inhibitors (Pis) are associated with an increased risk for preterm birth, but this finding has not been reported consistently.10,16–27 Recent evidence suggests that HAART has led to increased pregnancy rates among HIV-infected women28 who are enrolled in the Adult/Adolescent Spectrum of HIV Disease. HAART availability has reduced perinatal HIV transmission,21 but HAART's impact on LBW and preterm birth is less clear. Recent recommendations for scheduled cesarean sections,29 which can reduce risks30 that are associated with vertical HIV transmission to <2%,31 could increase prevalence of preterm birth if done earlier than the recommended 38 weeks. This analysis assesses LBW and preterm birth trends among infants who were born to HIV-infected women between 1989 and 2004. All infants were enrolled in the Pediatric Spectrum of Disease (PSD) a large, longitudinal HIV study32 in the United States.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
PSD Project
Conducted from 1989 to 2004, the PSD study was 1 of the largest perinatal and pediatric HIV studies of HIV-infected and HIV-exposed children in the world.32 The PSD study reviewed newborn and pediatric medical charts of live-born, HIV-exposed/infected infants and HIV-infected children and adolescents and was performed under a protocol that was reviewed and approved by the institutional review board of the Centers for Disease Control and Prevention. PSD chart abstractions were conducted at 8 US geographic sites. PSD enrollees were identified through contact with key practitioners, review of HIV laboratory logs, and review of medical charts at the participating hospitals. Data that were collected from the pediatric medical charts included mode of delivery, birth weight, and gestational age of the infant. Additional information that was collected included maternal race/ethnicity, history of maternal prenatal care (recorded as any prenatal care, no prenatal care, or unknown prenatal care), month and year of initial infant testing, maternal antiretroviral therapy (ARV; beginning in 1995), the presence of maternal HIV symptoms at delivery, prenatal maternal HIV status, self-reported history of maternal drug use, and the child's most severe HIV status based on the 1994 Centers for Disease Control and Prevention Pediatric HIV Classification.33 Data on the maternal CD4 counts and viral loads are not included consistently in newborn/pediatric charts and were not collected in PSD.32 Data on type of delivery were collected throughout the study, but supplemental information on why cesarean sections were done was not collected until 2003,32 but such deliveries have increased.34

Definitions
The primary outcomes of this study were LBW, defined as <2500 g,1 and preterm birth, occurring at <37 weeks’ gestational age.3 Gestational age in PSD was abstracted from either pediatric or obstetric assessment in the medical charts; such assessments were not uniform throughout the PSD sites.32 Maternal HIV status was categorized by whether the mother's HIV was diagnosed before the child's birth (before pregnancy or during pregnancy) or at/after delivery.32 Symptomatic maternal HIV disease was defined as clinical HIV symptoms at delivery.32 A history of maternal drug abuse is defined as self-report any previous use of crack/cocaine or other street drugs and/or exchange of sex for drugs or money or urine drug screening.32 Prenatal care is defined only as maternal receipt of such care; PSD chart reviews did not assess the visit numbers or the trimester when care began.32 The age at first testing was calculated by subtracting the child's birthday from month and year of initial testing.32

Use of maternal ARV during pregnancy was recoded into a single categorical variable on the basis of receipt of any ARV during pregnancy and the maximum number of ARV drugs. Monotherapy was receipt of a single drug, dual therapy was use of 2 drugs, and triple therapy was HAART (receipt of 3 drugs, including either a PI or other non-PI triple ARV therapy).

Inclusion Criteria
The PSD analysis was limited to white non-Hispanic, black non-Hispanic, and Hispanic infants who were born in 1989 through 2004, for whom available data included both birth weight and gestational age, and whose HIV testing first was conducted during the first 30 days of life (neonatal period). Only infants who were tested during the neonatal period were included so that the ascertainment was consistent across birth years. Those criteria were met by 11231 infants and included both HIV-infected and -exposed infants.

Statistical Analysis
We used SAS 8.035 to characterize PSD trends in LBW and preterm birth and also assessed risk factors for both LBW and preterm birth among women who had prenatal care. Because preterm birth and LBW are highly correlated,3 we excluded preterm birth from the multivariate assessment of LBW and did not include LBW in the assessment of preterm birth. In addition, we did not include cesarean section as a variable in the models for preterm birth because no statistically significant changes in gestational age were found after HAART became routinely available to pregnant women. Performance of elective cesarean sections could have decreased the mean gestational age if performed at an earlier age (see "Results").

Results of the univariate and multivariate analyses for LBW and preterm birth are presented as odds ratios with 95% confidence intervals. All variables in the univariate analyses were entered in the logistic regression models. Risks that were significant at an {alpha} level of .10 remained in the model using a stepwise method. Perinatal exposure to 2 ARV drugs was used as the referent group10,16–27 because some European studies have suggested that PI-based HAART regimens during pregnancy can be associated with LBW and/or preterm birth.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Characteristics of Infants and Mothers
The majority of the 11231 infants were black (6916 [62%]) and male (5776 [51%]). The mean birth weight was 2890 g (range: 415–5360 g); the mean gestational age was 37.3 weeks (range: 26–42 weeks). The mean gestational age of infants who were delivered by cesarean section was 37.5 weeks in 1999, the year in which cesarean delivery was shown to reduce vertical transmission,33,34 and declined to 37.3 weeks in 2004. The change in gestational age was not statistically significant. The mean gestational age of infants who were delivered vaginally was 38 weeks in 1999 and 37.8 weeks in 2004, a change that was not statistically significant. Almost one quarter (2485 [22%]) of PSD infants were born before 1994, when the Pediatric AIDS Clinical Trial 076 results33 demonstrated that a regimen of prenatal, intrapartum, and postpartum zidovudine could reduce the risk for perinatal HIV transmission by two thirds.

The percentage of HIV-infected women who received any prenatal care increased from 48% in 1989 to 78% in 1995 (the year that HIV testing recommendations and policies were adapted for pregnant women)36 to a peak of 90% in 2001 and declined to 84% in 2004. More than half of the PSD mothers (6665 [59%]) had not received any ARV. The proportion of women who had cesarean sections increased from 19% in 1989 to 57% in 2004.

A minority of mothers (1720 [15%]) had an unknown HIV status before pregnancy or delivery, a figure that declined from 43% in 1989 to 8% in 2004. Overall, one third of mothers reported illicit drug use, but reported use declined from 67% in 1989 to 12% in 2004. A minority of mothers had symptomatic HIV disease at delivery (755 [7%]).

Changes in LBW, Preterm Birth, and HIV Infection and Antiretroviral Medication
Between 1989 and 2004, the proportion of LBW infants declined from 35% (1989) to 21% (2004) with a nadir of 19% (2003). During the same period, preterm births declined from 35% (1989) to 22% (2005) with a low of 18% (2001). During the 15-year period, given both HAART and obstetric interventions including elective cesarean section before onset of labor, the proportion of HIV-infected infants declined from 28% in 1989 to 1% in 2004.

The declining trends of LBW in PSD were observed for all 3 study groups (black non-Hispanic, white non-Hispanic, and Hispanic); proportions of LBW were highest for black infants throughout the study. Averaged across the 1989–2004 period, LBW proportions were 25% for non-Hispanic black infants, 18% for non-Hispanic white infants, and 20% for Hispanic infants. The respective LBW declines between 1989 and 2004 were 36% to 22% among black non-Hispanic infants, 21% to 0% among white non-Hispanic infants, and 38% to 21% among Hispanic infants.

In the same period, preterm birth among PSD infants declined among all 3 racial/ethnic groups. Overall, preterm birth was 23% for non-Hispanic black infants, 17% for non-Hispanic white infants, and 18% for Hispanic infants. Between 1989 and 2004, preterm birth among non-Hispanic black infants declined 39% to 22% (2004), among non-Hispanic white infants from 17% to 0%, and among Hispanic infants from 33% to 27%.

Trends in Maternal ARV Use
Documented maternal receipt of any ARV increased from 2% in 1991 to 82% in 2004 in PSD. Triple ARV therapy including either a PI or a non-PI regimen increased from 2% in 1996 to 72% in 2004. Among all women, triple ARV therapy with a PI increased from 1% in 1996 to 55% in 2004; triple therapy with a non-PI regimen increased from 1% in 1996 to 14% in 2004.

Factors Associated With LBW and Preterm Birth Among Women With Prenatal Care, 1989–2004
Factors that were associated with LBW in univariate analysis and multivariate logistic regression are shown in Table 1. In the logistic model, LBW was associated with history of maternal drug use, unknown maternal HIV status before delivery, symptomatic maternal HIV disease, black race, Hispanic ethnicity, and infant HIV infection. Male gender was predictive of normal birth weight.


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  		TABLE 1 Risk Factors for LBW Among 8793 Infants Who Were Born to HIV-Infected Mothers With Prenatal Care During an Era of Changing ARV: PSD, 1998–2004

 
Factors that were associated with preterm birth in univariate analysis and multivariate logistic regression are shown in Table 2. In the logistic model, preterm birth was associated with history of maternal drug use, symptomatic maternal HIV disease, no ARV therapy, 3-drug HAART therapy including a PI, black race, and infant HIV infection.


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  		TABLE 2 Risk Factors for Preterm Birth Among 8793 Infants Who Were Born to HIV-Infected Mothers With Prenatal Care During an Era of Changing ARV: PSD, 1998–2004

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This study presents encouraging evidence that LBW and preterm birth both have declined among PSD infants during a period (1989–2004) when therapy for maternal treatment and perinatal HIV prevention evolved into highly potent HAART regimens.17 Simultaneously, vertical HIV transmission from mother to child declined from 26% to 2% or less in the United States.34 The declines occurred during a period, beginning in 1995, of increased emphasis on routine HIV testing of all pregnant women36–38 and close follow-up and comprehensive pregnancy management.

Compared with the general US population, LBW and preterm birth still are markedly higher among infants who are born to HIV-infected women.6–10 LBW and preterm prevalences as high as 48% and 38%, respectively,11 have been reported. Although this study focuses on the PSD cohort,32 it is likely that the declines in LBW and preterm birth can be observed in other US perinatal HIV cohorts. The prevalences of LBW and preterm birth in the PSD cohort remain higher than the almost 8% and 12% reported for the general US population in 2004,2 but the declining trends of LBW and preterm births in all 3 ethnic groups represent significant health gains for infants who are born to HIV-infected mothers.

This PSD study did find consistent risks for LBW and preterm birth among infants who were born to HIV-infected women. A history of maternal drug abuse, symptomatic maternal HIV disease, black race, and infant HIV infection were associated with both LBW and preterm birth. All of these risks are well-documented associations with LBW and preterm birth in other studies3,6–14,39–43 that focused on other high-risk groups of pregnant women, including those with HIV.

Importantly, this study did not find any consistent association with HAART or lack of ARV with LBW. We did find an association between preterm birth and both no ARV and triple ARV therapy with a PI. Studies from Europe, the United States, and Latin American have found inconsistent associations between LBW and preterm birth.10,16–27 This study found such an association, but PSD data are insufficient to answer the question about associations between ARV and adverse maternal outcomes, in part because maternal CD4 counts, viral load, and details of drug therapy were not collected.

The increased emphasis on HIV testing for pregnant women36,37 opened the door to improve both access to prenatal care and pregnancy outcome. Despite the reduction of perinatal HIV transmission in the United States, ongoing surveillance is needed to monitor pregnancy outcomes as more HIV-infected women choose to bear children.27 This study found that the PSD cohort experienced better access to prenatal care, and ARV improved during the same period when vertical HIV transmission declined. However, the study cannot determine whether access to ARV and prenatal care are causal events in the declines of LBW and preterm delivery.

The PSD cohort is 1 of the largest pediatric/perinatal cohorts assembled to track the natural history of HIV and AIDS. Infants were enrolled in PSD during a span of time (1989–2004) that covered the entire spectrum of the HIV/AIDS epidemic and evolving therapy. There are certain limitations to the PSD data. First, the study is based on pediatric hospital chart review, so maternal information is limited. Second, documentation of LBW and preterm birth trends does not explain why or how these events happened. In addition, the PSD database lacks data about maternal viral load, maternal CD4 counts during pregnancy and at delivery, previous preterm delivery, reason for cesarean section, and maternal socioeconomic status. Each of these factors can influence the outcome of pregnancy, and the lack of such data limits this study's ability to assess more completely the factors that are associated with the declines in LBW and preterm birth.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Between 1989 and 2004, LBW and preterm birth both have declined among infants of HIV-infected women who were enrolled in the PSD cohort. Both declines occurred among all racial/ethnic groups in contrast to trends in the general US population. Among women who had prenatal care, preterm birth was associated with lack of ARV and HAART therapy that included a PI.


   FOOTNOTES
 
Accepted Oct 16, 2006.

Address correspondence to Joann M. Schulte, DO, MPH, Texas Department of State Health Services, Region 2/3, 1301 S Bowen Rd, Suite 200, Arlington, TX 76013. E-mail: jzs1{at}cdc.gov

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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