Provision of antiretroviral prophylaxis to HIV-infected women and their HIV-exposed infants is a cornerstone of pediatric HIV prevention. Routine counseling and HIV testing during pregnancy is a critical entry point for access to these services. Despite its theoretical simplicity, programs for the prevention of mother-to-child HIV transmission (PMTCT) in low-income and middle-income countries face considerable challenges in successfully identifying and treating all at-risk women and their infants [1–8].
In 2003, we used cord blood specimens to conduct city-wide surveillance in Zambia and found that only 30% of the HIV-infected/exposed women/infant pairs who received antenatal care within the Lusaka Urban District public antenatal care centers had received a full course of both maternal/intrapartum and newborn nevirapine (NVP), that is NVP coverage was 30% . The predominant reasons for failed coverage were: undiagnosed HIV infection among pregnant women despite availability of antenatal HIV testing and; NVP nonadherence among women diagnosed with HIV during antenatal care. We conducted a cluster-randomized trial designed to determine whether the addition of targeted PMTCT services in the labor ward would improve NVP coverage.
At the time of our study (October 2005 to January 2006), the PMTCT program in Lusaka offered voluntary, opt-in HIV counseling and testing to nearly all women attending antenatal care in its 27 public-sector antenatal clinics. Women/infant pairs found to be HIV-infected/exposed were provided with single dose NVP . Back-up doses were provided in the labor ward for women who reported that they did not take the intended NVP dose. At the time of the study, more complex PMTCT regimens and maternal antiretroviral therapy were not a routine component of antenatal care in Lusaka (although this has since changed).
The study was conducted in 12 public-sector delivery centers in Lusaka, Zambia. The intervention was enhanced labor ward-based PMTCT services, involving distinct interventions based upon a woman's HIV serostatus upon presentation. Those of unknown status were offered labor ward-based HIV testing, and, if seropositive and in active labor, immediate single-dose NVP administration. Women were considered to be unaware of their HIV status if they were not tested for HIV during their current pregnancy and there was no documentation of earlier seropositive results. Those presenting with known HIV infection were administered a rapid, structured assessment of NVP adherence in the labor ward.
NVP coverage was our primary outcome. Maternal coverage was defined as the proportion of HIV-infected women with confirmed NVP ingestion measured by HIV and NVP testing of umbilical cord blood specimens from all deliveries that occurred in the 12 Lusaka District labor wards during the study periods. Infant coverage was determined by chart reviews to assess whether NVP had been administered by clinic personnel prior to discharge. Both the HIV-infected women and her HIV-exposed infant must have received NVP to be considered ‘covered’. The trial consisted of two study periods: a baseline surveillance period (preintervention) in which NVP coverage was measured in both the treatment and control arms; and an intervention surveillance period during which the labor ward PMTCT services were offered in the treatment arm only and NVP coverage was again measured in both arms.
Cord blood surveillance
In October and November 2005, we conducted the baseline surveillance phase of the trial to determine the background NVP coverage in all 12 public-sector labor and delivery centers in Lusaka District. During this phase, midwives in each labor ward collected anonymous umbilical cord blood specimens from all discarded placentas and extracted nonidentifying information from the woman's medical record onto the anonymous surveillance form which was linked to the cord blood specimen by a mutual identification number. The surveillance form recorded the following antenatal and delivery care information: mother's age, gravidity, number of antenatal care visits, shift of admission, length of time between admission and delivery, whether or not the woman had been offered (and accepted, if offered) HIV counseling and testing and maternal HIV status. The form further recorded whether or not infected mothers were given a dose of NVP and whether a baby was given NVP prior to discharge. Maternal HIV status was obtained from the mother's antenatal care card . If cord blood was not collected, the midwife noted the reason on the surveillance form.
Following completion of the baseline surveillance, the 12 labor wards were stratified according to size (based on the number of deliveries per month) and their historical NVP coverage level (based on the 2003 surveillance data)  and randomized to the treatment or control arms. The use of stratification was intended to create balance between arms (Fig. 1). Between December 2005 and January 2006, we conducted the intervention phase of the trial. During the intervention phase, the midwifery staff continued to collect cord blood and to complete the linked, anonymous surveillance form on all women. Enhanced labor ward services were provided in the six treatment arm clinics which included rapid HIV testing and; a rapid NVP adherence assessment. The six control clinics received the standard of PMTCT care that did not include labor ward HIV testing or rapid assessment of NVP adherence.
Rapid HIV testing
Women unaware of their HIV status were offered opt-in HIV counseling and testing if they were in the first stage of labor and the midwife deemed there was sufficient time before delivery. All women who chose to be tested for HIV provided written consent (standard procedure at that time) and indicated whether they wanted to learn their test result before or after delivery. Those who chose to learn their results after delivery could nonetheless consent to NVP, if infected, and have NVP administered to their babies prior to receiving their results by so indicating. The consent form explained that they would be offered a tablet (NVP or similarly appearing calcium tablet) regardless of the results of their HIV test. Women who tested seropositive were given a NVP tablet (200 mg) and their exposed infants received NVP syrup (2 mg/kg) in the postpartum ward prior to discharge. We offered the calcium tablet to HIV seronegative women so as not to inadvertently disclose a woman's status during labor or to stigmatize HIV-infected women.
We used a point-of-care rapid HIV testing strategy in the labor wards. Women were screened for HIV using the DETERMINE HIV-1/2 rapid test (Abbott Laboratories, Abbott Park, Illinois, USA) and positive results were confirmed with the GENIE II HIV 1/2 rapid test (BioRad Laboratories, Hercules, California, USA). NVP was administered to all women who tested positive on the DETERMINE test. Confirmatory HIV testing was done on positive specimens either before or after delivery as time permitted.
Rapid nevirapine adherence assessment
The rapid NVP adherence assessment was conducted on known HIV-infected women who presented to the labor ward. It was designed to help ensure that they ingested NVP during labor. The assessment consisted of asking these women the following structured question.
‘Nevirapine is a medication that may help prevent your baby from getting HIV.’ Which statement best describes your interest in taking nevirapine?
- I did not take nevirapine before coming here and do not want to take nevirapine.
- I haven't taken nevirapine yet but would like to take it now.
- I already took my nevirapine tablet.'
Women who reported not having ingested NVP were given a back-up dose. This approach replaced the informal practice of asking women if they ingested NVP prior to admission in a more direct manner (e.g. ‘Did you take your nevirapine tablet?’).
Umbilical cord blood collection and processing
The umbilical cord blood specimens were collected in 10 ml EDTA vacuum tubes and stored in the labor wards at 2–8°C until pick-up by the study team. The study team reviewed all surveillance forms and corrected errors or discrepancies when possible in consultation with the delivering midwife or midwife in-charge. Forms and specimens were picked up daily and transported to a central laboratory where the plasma analyzed for HIV antibodies using the DETERMINE rapid HIV test only . In the rare event that the cord blood and antenatal care results were discordant, we considered the cord blood results to be definitive. After rapid HIV testing, all plasma specimens were aliquoted and frozen at −70°C. HIV seropositive plasma specimens were shipped on dry ice to the University of Alabama at Birmingham pharmacology laboratory for NVP assay via high performance liquid chromatography (HPLC) with a detection threshold of 25 ng/ml of NVP . In a previous study in Lusaka, we detected NVP in the cord blood of 178 of 179 women (>99%) of women in whom NVP ingestion had been observed directly .
We used Microsoft Excel 2003 (Microsoft Corp, Redmond, Washington, USA) to randomize labor wards to the intervention and control arms of the trial. All other statistical analyses were performed using SAS 9.1 software (SAS Institute Inc., Cary, North Carolina, USA). We used generalized estimating equations (GEE) to determine the odds of coverage associated with the intervention, adjusting for the nonindependence of individuals within clinics. Given the known tendency of GEE to underestimate standard errors when the number of clusters is small, we used permutation tests to validate any significant results from the GEE models. Due to the prospective nature of the study, the parameters for the estimated GEE model were used to estimate probability of coverage. To estimate relative risk, the ratio of the probability of coverage in treatment clinics to the probability of coverage in control clinics was calculated. Variables significant in the bivariate GEE model at P < 0.10 were included in the multivariable model. To provide 95% confidence intervals for point estimates produced by the GEE models, 1000 bootstrap samples were drawn based upon the stratified randomization design of the study. The 2.5th and 97.5th bootstrap percentiles defined our reported 95% confidence intervals. The study was approved by the Research Ethics Committee at the University of Zambia and the Institutional Review Board at the University of Alabama at Birmingham.
During the baseline and intervention study periods, 7664 women gave birth in the 12 Lusaka District labor wards. We collected cord blood specimens from 7592 (99%) deliveries and obtained HIV results on 7438 (97%). Cord blood testing indicated that 1618 of 7438 (22%) women were HIV seropositive. Seroprevalence was higher among women presenting to the labor ward unaware of their HIV status (26%) as compared to women who learned their status during antenatal care (21%; P < 0.0001). We tested 1279 of the 1618 (79%) seropositive specimens for NVP by HPLC and detected NVP in 816 (64%) of the specimens (indicating maternal coverage). A total of 769 (60%) of the infants born to this group of 1279 HIV-infected mothers received NVP according to chart documentation (indicating infant coverage). Only 608 of 1279 (48%) cord blood seropositive mother–infant pairs received both a maternal and infant doses of NVP.
The remaining 339 (21%) specimens were not tested for NVP due to inadequate fiscal resources. Seropositive cord blood specimens that were not analyzed were distributed similarly between the control (145 of 760, 19.1%) and treatment arms (194 of 858, 22.6%). The probability of a sample being unanalyzed was not related to any covariates that were associated with coverage in the GEE model (number of antenatal care visits or place of first antenatal care visit).
During the 4-week baseline surveillance period, 3123 women gave birth to infants in the control (1491 of 3123, 48%) and treatment arm (1632 of 3123, 52%) labor wards (Table 1, Fig. 1). HIV prevalence among cord blood samples obtained from both arms was 20%. NVP coverage among HIV-infected/exposed woman/infant pairs was 53% and 42% in the control and treatment arms, respectively. [Note: Although allocation of clinics to either control or treatment arms occurred after completion of the baseline surveillance period, intervention arm assignment was retrospectively applied to the baseline period for the analysis.]
During the 6-week intervention surveillance period, 4541 women gave birth to infants in the control (2106 of 4541, 46%) and treatment arm (2435 of 4541, 54%) labor wards (Table 1, Fig. 1). Cord blood seroprevalence was 23% in both arms. NVP coverage among HIV-infected/exposed woman/infant pairs in the control arm was 43%, representing an absolute decline of 10% from 53% during the baseline period. In the treatment arm, NVP coverage was 52% when labor ward PMTCT services were available, representing an absolute increase of 10% from 42% coverage during the baseline period.
Five of the six treatment arm labor wards experienced improvements in NVP coverage when the labor ward PMTCT services were offered (range 3 to 33%) although one labor ward experienced a 10% decline in coverage (Table 2). During the baseline surveillance period (preintervention) the probability of a given mother–infant pair being ‘covered’ in the treatment clinics was 0.89 times the probability of being covered in the control clinics, whereas during the intervention period, the probability of being covered in the treatment clinics was 1.22 times the probability of being covered in the control clinics. This change represents a multiplicative effect of 1.37 upon the relative risks ratio at baseline (ratio of relative risks 1.37, bootstrapped 95% CI, 1.04–1.77).
In bivariate GEE analysis, two variables were positively associated with NVP coverage and therefore included in the full model: number of antenatal care visits (P-value from permutation test = 0.015) and place of first antenatal care visit (P-value from permutation test = <0.001). The probability of coverage among women who received at least three antenatal care visits were greater than for those who received two or fewer visits (RR 1.15, 95% bootstrap CI, 1.01–1.27). Women who received their first antenatal care visit in Lusaka had probability of coverage 2.5 times (RR 2.5, 95% bootstrap Interval 1.78–5.51) that of women who did not receive their first antenatal care visit in Lusaka. In a multivariable model adjusted for these two variables, the estimated effect of the intervention remained significant (adjusted relative risk, 1.35, 95% bootstrap CI 1.02–1.72) with the relative risk of a given mother–infant pair being ‘covered’ in the treatment clinics as compared with the control clinics being 0.86 during the baseline period and 1.17 during the intervention period.
In a planned subset analysis of women presenting in labor unaware of their serostatus, rapid HIV testing was associated with an absolute increase in coverage of 16% (range 4–25%) in the treatment clinics (from 0% at baseline, data not shown). Coverage among women in the control clinics was zero. Due to the extreme sparseness of the outcome at baseline, the statistical model did not converge.
During the intervention period, midwives in the treatment clinics reported using the rapid assessment of NVP adherence on 89% of women presenting with known seropositive status. This rapid assessment was associated with a 4% increase in coverage in the treatment clinics (from 63% at baseline to 67% during the intervention) compared with a 9% drop in coverage in the control clinics (from 74% at baseline to 65% during the intervention period, Table 3). On the basis of statistical models, the relative risk of coverage among women in the treatment arm as compared with women in the control arm was 0.92 at baseline and 1.02 during the intervention period. This change represents a ratio of relative risks of 1.15 (RR 1.15, 95% CI 1.04–1.22) (Table 3).
We demonstrate that implementation of a labor ward-based PMTCT package can have a significant, positive effect on NVP coverage. One of the strengths of this intervention was that it targeted two distinct groups of women depending on their HIV status: women of unknown HIV status were offered HIV counseling and testing and NVP as needed; and women with known HIV-infection were offered a rapid screening assessment regarding NVP adherence and were given NVP as per their responses and willingness. The studied labor ward-based package was associated with a 10% absolute increase in NVP coverage and this increase occurred in the presence of falling coverage in the control clinics. Although the decline in coverage in the control clinics was surprising to us, we suspect this may in part be attributable to staffing shortages which are often most severe in Lusaka during the Christmas and New Years holidays.
Owing to the limited number of labor wards available for participation, this study was not powered a priori to look at the individual effects of rapid HIV testing or the rapid NVP adherence assessment. Nonetheless, coverage among women unaware of their serostatus improved significantly when rapid HIV testing was offered (0–16%). The reasons for failed coverage are discussed in a separate manuscript . We believe that the impact of labor ward testing would have been greater if opt-out testing had been employed rather than the opt-in approach used in this study [14,15].
We observed modest improvements in coverage among known HIV-infected women associated with use of the rapid NVP adherence assessment. We have previously reported that as many as one-third of women in the Lusaka PMTCT program were not adherent to their NVP dose  and in a clinical trial setting we found that 28% of women who were queried about NVP ingestion, falsely reporting ingesting it . This rapid assessment was specifically designed to improve NVP adherence among women by allowing them to express their interest in taking NVP rather than simply answering ‘yes’ or ‘no’ to whether or not they had ingested NVP an approach found to be effective in other clinical settings .
Only one labor ward in the treatment arm experienced a decline in coverage (−10%) associated with the rapid NVP adherence assessment and uniquely this same labor ward experienced the smallest improvement in coverage attributable to rapid HIV testing (4%). We have qualitative feedback suggesting that staff morale and staffing shortages may have contributed to the poor results at this site. Low staff morale can adversely affect uptake of services in clinical trial settings  and others have reported staffing shortages to be an impediment to labor ward counseling and testing [18,19]. Although we were not able to account for potential confounders such as current coverage level, staffing levels, staff morale, staff knowledge of HIV and experience level, we believe that a randomized controlled trial using a placebo calcium tablet for seronegative women (to avoid stigmatizing HIV-infected women) is a superior research design than typical program evaluations.
Given the cluster-randomized design of this study, it is inherently subject to recruitment bias. In order to adjust for this potential imbalance, we stratified the labor wards, based on their historical NVP coverage level  and by their size, prior to randomization. We did not find any statistical evidence that the proportion of women eligible for either of the labor ward interventions differed by study period (baseline or intervention) or treatment group (control or treatment). Furthermore, the short duration of the intervention period and the distance between clinics made it unlikely that women migrated from control clinics to treatment clinics seeking PMTCT services.
One limitation of this study is that infant HIV outcomes were not assessed. Rather, we relied upon NVP coverage as a proxy for infant outcomes. The efficacy of single dose NVP has been demonstrated in several clinical trials including, two trials which have shown that NVP is effective even when used late in labor [20,21]. Although single dose NVP is no longer the standard of care for PMTCT in much of sub-Saharan Africa, NVP remains an important component of prophylactic regimens prescribed during antenatal care and to women who test positive in the labor ward.
Our study shows that labor ward-based PMTCT programs are feasible and can have significant, positive impact on NVP coverage. Four out of six labor wards offering these services experienced substantial increases in coverage (between 18 and 33%) and two clinics experienced insignificant effects. The latter suggests the need to address staffing issues and minimize testing complexity, such as removing the ‘written informed consent’ step to HIV testing and moving to an opt-out testing strategy (this has been done subsequently by Zambian health officials). In settings where women commonly present to the labor ward unaware of their HIV status [4,19–25] intrapartum testing could have a substantial impact on NVP coverage [14,18,19,26,27] The labor ward is a realistic venue for continuing efforts to prevent infant HIV infections by offering rapid testing and treatment to women who are unaware of their HIV status [28,29] and enhancing antiretroviral adherence among those women who know that they are HIV-infected.
K.M., M.S., S.V., D.R., R.G. and J.S. contributed to the conception and design of the study. K.M., S.V., D.R., M.B. and J.S. were involved in the analysis of the data and all authors were involved in the interpretation of the data. K.M., S.V., D.R., J.S. drafted the manuscript and all co-authors critically revised the manuscript contributing important intellectual content. The final version of the manuscript was approved by all authors. K.M. is the guarantor accepting full responsibility for the conduct of the study and the data.
Support for the programmatic work reported herein was supported by a multi-country grant to the Elizabeth Glaser Pediatric AIDS Foundation from the United States Centers for Disease Control and Prevention (U62/CCU12354) through the President's Emergency Plan for AIDS Relief (PEPFAR). Support for the intervention and evaluation components was provided by the University of Alabama at Birmingham and the Elizabeth Glaser Pediatric AIDS Foundation (EGSA 19-02).
Role of the funding source: Neither the Elizabeth Glaser Pediatric AIDS Foundation nor the CDC was involved in data collection or management, nor were they engaged in direct contact with patients or identifiable patient data.
Data presented and published as an abstract at the XVII International AIDS Conference in Mexico City (August 2008).
There are no conflicts of interest.
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