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The Impact of Structured Mentor Mother Programs on Presentation for Early Infant Diagnosis Testing in Rural North-Central Nigeria: A Prospective Paired Cohort Study

Sam-Agudu, Nadia A. MD*,†; Ramadhani, Habib O. MD, MPH, PhD; Isah, Christopher HND*; Erekaha, Salome MPH*; Fan-Osuala, Chinenye MPH*; Anaba, Udochisom MPH*; Adejuyigbe, Ebunoluwa A. MBChB; Charurat, Manhattan PhD

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: June 1, 2017 - Volume 75 - Issue - p S182-S189
doi: 10.1097/QAI.0000000000001345

Abstract

INTRODUCTION

Nigeria is an important target for the prevention of mother-to-child transmission (PMTCT) of HIV. In 2015, approximately 150,000 children were newly infected with HIV globally, with 41,000 in Nigeria alone.1 In the same year, only 30% of >200,000 HIV-infected pregnant women received antiretroviral therapy (ART), only 9% of HIV-exposed infants received early HIV testing, and <20% of eligible children received ART in Nigeria.2 Early infant diagnosis (EID) is a key PMTCT service recommended by the World Health Organization for all HIV-exposed infants.2,3 EID is defined as receipt of virological HIV testing among HIV-exposed infants by 2 months of age.3 Successful EID programs achieving universal or near-universal early testing for all HIV-exposed infants4 reflect effective antenatal and early postpartum programming with robust mother–infant linkage. Nigeria's low EID performance, therefore, indicates “early warning” signs of its overall PMTCT program challenges.

PMTCT programs aim to prevent infant HIV and to facilitate healthy outcomes for both HIV-exposed infants and HIV-infected mothers.2,5 PMTCT interventions are packaged in a cascade of care that includes maternal ART, antenatal, EID, and postnatal services, and linkage to long-term HIV care and support.6 Poor access, inadequate social support, and low awareness of benefits can prevent a mother–infant pair (MIP) from completing the PMTCT cascade.7,8

In Nigeria, rural areas are especially challenging for PMTCT due to low maternal health service utilization.9,10 For example, only 47% of rural women access skilled antenatal care (ANC), compared with 86% of urban-dwelling women.9 In addition, postnatal service uptake is worse in rural Nigeria: only 38% of rural vs 69% of urban women and 8% of rural vs 25% of urban infants received postnatal checkups within the first 2 days postdelivery.9 Poor PMTCT service utilization can result in HIV-exposed infants experiencing late HIV diagnoses, delays in ART initiation, and increased morbidity and mortality.11–13 Clearly, PMTCT service uptake interventions are especially needed in rural Nigeria.

Peer support (PS) interventions have been shown to improve both rural and urban HIV client outcomes in several African countries.14–18 Mentor Mothers (MMs) are HIV-positive women who have successfully completed the PMTCT cascade and are trained to support less-experienced PMTCT clients.14,19 MM support programs have proven feasible and acceptable in PMTCT,20,21 and have had positive impact on maternal HIV testing rates, drug adherence, and postnatal service uptake in several African countries.14,17,18 However, these programs have been heterogeneous, often lacking standardization in scope of work, supervision, and impact evaluations for infant-specific outcomes. Furthermore, there are little data on the impact of PS in lower-prevalence (3.1%)1 yet high HIV-burden (3.5 million)1 resource-limited settings such as in Nigeria.15,17

The MoMent (Mother Mentor) study evaluated the impact of structured MM programs on the primary outcomes of timely EID presentation and postpartum maternal retention in rural Nigeria.22 This article reports the impact of MoMent's structured PS intervention on EID presentation and secondarily on HIV-free survival among HIV-exposed infants.

METHODS

Study Design and Setting

This prospective paired cohort study was conducted at primary health care centers (PHCs) in the Federal Capital Territory and Nasarawa states in North-Central Nigeria. Because of programmatic expectations to provide trained PS among a number of potential study sites, randomization was not possible. Ultimately, after desk review and site assessments, available sites for MM intervention implementation were matched with routine care sites for comparison; details are described elsewhere.22 Based on 4 site characteristics (ANC clinic bookings per month, HIV prevalence among pregnant women, and number of staff providing EID and clinical PMTCT services), 10 routine PS sites were matched with 10 of the 16 sites available for the MM intervention. Supplemental Table 1 (see Table, Supplemental Digital Content, http://links.lww.com/QAI/A981) presents descriptions of PS programs and peer counselor roles for both study arms. Two peer counselors were assigned to each study site, aiming to maintain a counselor-to-study client cap of 1:15. PMTCT and other HIV services at all study sites were supported by the Institute of Human Virology Nigeria (IHVN).

Study Participants and Recruitment Procedures

Study participants were MIPs: HIV-positive women and their HIV-exposed infants. Women were consecutively enrolled during pregnancy: Those recruited at MM sites received structured, closely supervised MM support; women recruited at standard-of-care sites received routine PS.22 Recruitment included both ART-naive and ART-experienced women. Women of all gestational ages making at least 1 antenatal visit were eligible for recruitment; those presenting in labor were excluded. Further details on participant recruitment have been published elsewhere.22 Outcomes-specific data for both study arms were collected daily from routine health registers by research staff. Peer counselor activity/visit data were collected from structured logbooks and notebooks completed by MMs and routine PS, respectively. For infants whose mothers died, peer counselor visits to the surviving infant and family were documented. Follow-up was conducted up to 6 months postpartum for each MIP. All study participants received routine Option B PMTCT services as per national guidelines23,24 during recruitment and follow-up, including initiation of maternal ART regardless of CD4 count at booking.

Ethical Approvals

The study was approved by the Nigerian National Health Research Ethics Committee, the Ethics Review Committee of the World Health Organization, and the Institutional Review Board of the University of Maryland, Baltimore. Written informed consent was obtained from all study participants, including parental/guardian consent for infants for the nonroutine 6-month DNA polymerase chain reaction (PCR) testing.

DNA PCR Sample Collection and Processing

Whole blood samples were collected from heel or toe prick of each infant and spotted onto 5 circles on filter paper for overnight drying at ambient temperature. Dried filter papers were sealed in humidity-free bags and transported to 2 IHVN-supported referral PCR laboratories. One spot from each filter paper was tested by COBAS AmpliPrep/TaqMan HIV-1, version 2.0 real-time PCR assay (Roche Diagnostics, Indianapolis, IN), according to the manufacturer's instructions. For confirmation, all samples testing positive were retested using a second dried blood spot before issuing final results. HIV-negative samples were not retested; final negative results were issued immediately.

Sample Size Estimation

The primary outcome of interest reported in this article is presentation for EID testing as a process indicator for EID uptake. Baseline EID uptake at IHVN PHCs was calculated at 20%.22 For an intracluster correlation of 0.05, type II error (1−β) = 0.8 and type I error α = 0.05, a minimum of 21 MIPs per site would provide 80% power to detect a difference of 20% in EID uptake (20% routine PS vs 40% MM). Allowing for maternal and infant mortality, a final sample size of 480 MIPs was determined.22 Because of lower-than-projected recruitment over the first 12 months, the smallest absolute difference was increased to 25% (20% routine PS vs 45% MM). With all other assumptions unchanged while maintaining power at 80%, a revised sample size of 220 MIPs was determined.

Statistical Analysis

Variables and Definitions

Variables were defined and analyzed from an intention-to-treat approach; as such, all expected products of pregnancy were included in analysis regardless of outcome. The EID presentation outcome was defined as the number of infants presenting for DNA PCR sample collection between and including 35 and 62 days of life. Given that the primary outcome variable was timing of presentation and not collection or a result of the DNA PCR test, date of presentation, and not date of sample collection, was used to assign status for this outcome. This differed from the national program's definition of EID, which was based on DNA PCR sample collection date.25

Secondary outcomes evaluated were proportions of infants who tested positive for first and second DNA PCR tests, sampled at 2 months (35–62 days) and 6 months (169–197 days) of age, respectively. The second DNA PCR test was a nonroutine procedure implemented to evaluate for “late” MTCT (mother-to-child transmission of HIV) during the 6-month follow-up period.22 All infants identified positive for first DNA PCR were excluded from the second DNA PCR evaluation. Finally, cumulative HIV-free survival at 2 (62 days) and 6 months (197 days) postpartum were determined; this was defined as the product (1−x)(1−y), where “x” is the infant HIV DNA PCR positivity rate at 2 months and “y” is the infant HIV DNA PCR positivity rate at 6 months.

Data Analysis

Comparisons of maternal and infant characteristics between study arms were performed using χ2 test for proportions and Student t test for mean values. For nonsymmetric data, median values were compared with Wilcoxon rank-sum test. The effect of MM support on EID presentation was examined using a multivariate logistic regression model with generalized estimating equation to account for clusters. First, univariate models for associations between EID presentation, type of PS, and maternal characteristics were fit. To minimize bias on account of the nonrandomized design, biologically plausible confounders as well as those variables that changed crude estimate by ≥5% were sequentially added to the multivariate model. This was stopped when addition did not result in further change in estimate. Covariates included maternal characteristics such as age, gestational age at booking, marital status, education, religious affiliation, number of previous pregnancies, number of living children, HIV disclosure status, new or previously HIV-diagnosed, and whether new or previously on ART. Facility-level covariates were site HIV prevalence, number of PMTCT staff, and DNA-PCR sample collection staff.

All associations were presented as adjusted odds ratios (aORs) with 95% confidence intervals (CIs). Estimates whose CIs excluded 1 were considered statistically significant. For MTCT analyses, proportions of HIV-infected infants were computed. Furthermore, a composite endpoint involving HIV infections and deaths was constituted. Kaplan–Meier curves were used to assess HIV-free survival distributions among infants exposed to MMs and those exposed to routine PS. Log-rank test was used to compare the hazard functions for infants in these 2 groups. Statistical analyses were conducted using SAS version 9.3 (SAS Institute Inc., Cary, NC).

RESULTS

A total of 497 HIV-positive pregnant women were consecutively enrolled from the 20 matched sites between April 2014 and September 2015 (Fig. 1). MM intervention sites had lower ANC flow than routine PS sites during enrollment (8941 vs 14, 354). In addition, overall HIV prevalence of ANC clinics was higher at MM vs routine PS sites (5.5% vs 2.8%, P < 0.0001). Baseline characteristics of enrolled women are reported elsewhere in this supplement. Briefly, compared with the routine PS arm, MM arm recruitments were more likely to be Christian (77.7% vs 49.4%, P < 0.01) and to have secondary-level or higher education (57.7% vs 40.1%, P < 0.01). One pregnant woman in the MM arm and 51 in the routine PS arm were lost to follow-up before delivery. Delivery data were, therefore, available for 259 (99.6%) and 186 (78.5%) women in the MM and routine PS arms, respectively (Fig. 1).

FIGURE 1.
FIGURE 1.:
CONSORT flow diagram for infant outcomes analysis.

Ultimately, 408 infants were live-born, at a median of 36.4 weeks' gestation, and >95% by spontaneous vaginal delivery (Table 1). Of the all live-born infants, 263 (64.6%) were born at a health facility, and 145 (30.7%) at home. The proportion of infants born at health facilities was similar between MM (155/238, 65.4%) and routine PS arms (108/170, 63.5%) (P = 0.11). During the 2-month EID assessment period, 11 (2.7%) infants died; after 6 months (180 days), 18 (4.4%) infants had died, with no significant difference in mortality between arms. Six-month DNA PCR data for 16 infants (5 routine PS and 11 MM arm) were excluded from analysis because of failure to obtain consent for sample collection (Fig. 1).

TABLE 1.
TABLE 1.:
Delivery Characteristics and Mortality in the First 6 Months of Life Among Live-Born HIV-Exposed Infants*

Amount of maternal exposure to PS was evaluated by peer counselor-to-mother ratio and number of visits made per mother from prenatal engagement until 6 months postpartum. In this period, average MM-to-mother ratio was 1:12, compared with routine PS-to-mother ratio of 1:14, and mean number of visits (standard deviation) made per mother per 30-day month was 3.6 (±2.6) for routine PS vs 4.2 (±1.9) for MMs (P = 0.4).

EID Presentation Among HIV-Exposed Infants

Table 2 presents an analysis for factors associated with EID presentation. Timely EID presentation was achieved for 63.9% vs 35.0% of infants in the MM vs routine PS arms, respectively, an absolute difference of 28.9%. In multivariate analysis, compared with routine PS, maternal exposure to MM support was associated with increased likelihood of EID presentation among infants (aOR = 3.7, 95% CI: 2.8 to 5.0). Other factors independently associated with increased EID presentation were third trimester gestational age at booking (aOR = 2.1, 95% CI: 1.1 to 4.0) and delivery at health facility (aOR = 1.7, 95% CI: 1.1 to 2.6). Maternal education and religion were not associated with EID presentation.

TABLE 2.
TABLE 2.:
Factors Associated With Timely EID Presentation Among HIV-Exposed Infants

DNA PCR Testing and HIV Positivity Rates Among HIV-Exposed Infants

A total of 333 (81.6%) live-born infants presented for first DNA PCR regardless of promptness; of these, 228 (68.5%) presented for second DNA PCR testing. Ultimately, only 223 (67.0%) and 78 (34.2%) infants who presented for first and second DNA PCR, respectively, had results available for analysis. As per intention-to-treat analysis, 3/497 (0.6%) infants tested HIV-positive at first DNA PCR; with 1/260 (0.4%) in the MM arm vs 2/237 (0.9%) in the routine PS arm (P = 0.60) (Fig. 1 and Table 3). There were no infants identified positive at second DNA PCR testing.

TABLE 3.
TABLE 3.:
Rates of HIV Infection Among HIV-Exposed Infants at First and Second DNA PCR Testing

HIV-Free Survival Among HIV-Exposed Infants

During the 6-month postpartum follow-up, infants in the MM arm contributed 1248 person-months with median follow-up of 6.0 months (interquartile range 6.0–6.0) months. Infants in the routine PS arm contributed 693 person-months with median follow-up of 5.8 months (interquartile range 2.0–6.0 months). Among MM infants, 16 died or experienced incident HIV infection (incidence rate = 12.8 per 1000 person-months), compared with 4 routine PS infants (incidence rate = 5.8 per 1000 person-months).

Kaplan–Meier curves show MM arm infants experiencing death or incident HIV infection at a slightly higher rate than those in the routine PS arm (Fig. 2). However, this difference was not statistically significant (P = 0.12, log-rank test).

FIGURE 2.
FIGURE 2.:
HIV-free survival among HIV-exposed infants in the first 6 months of life.

DISCUSSION

Our study shows that structured, closely supervised PS is effective in increasing timely EID presentation among infants in rural settings. The structured MM intervention facilitated an absolute increase of ∼30% and a >3-fold increased likelihood of EID presentation compared with routine PS.

EID is arguably the most important infant-specific PMTCT cascade step and serves as an early “process indicator” for PMTCT program success. Some studies have evaluated the impact of social/behavioral interventions on EID uptake,17 a few have reported impact from PS. In a recent systematic review, Community health worker support, male partner involvement and phone calls/text messages improved EID uptake at different endpoints.17 However, only 2 studies reviewed demonstrated impact of PS on EID uptake by 2 months postdelivery.16,26 In Zimbabwe, Shroufi et al reported higher EID uptake with PS, compared with no support (99.2% vs 48.6%).16 Similarly, an Ethiopian study demonstrated higher EID uptake (32% vs 15%) among infants exposed to Mother Mentor support compared with infants without support.26

Despite encouraging results, these studies are not comparable with MoMent because their PS interventions were compared with no-support controls. As PS becomes routine in PMTCT care, impact evaluations will likely shift from comparisons with no support to comparisons of quality for incremental impact. In addition, study settings differed; the Zimbabwe study was conducted in an urban setting, whereas the Ethiopian study was in mixed urban and rural settings. Last, EID outcomes in these studies were measured by receipt of testing,16,26 and not presentation, as was conducted in our study.

Similar to the aforementioned studies, Nigeria's EID uptake definition is based on receipt of DNA PCR testing by age 2 months,2 which differs from MoMent's outcome measure of presentation for testing. Although timely presentation is a useful impact evaluation measure, timely receipt of results and prompt clinical decision making are the ultimate programmatic goals. Structural barriers ultimately affecting the success of PMTCT services such as EID should be considered when designing and interpreting results for interventional studies that do not directly address such barriers. MoMent's formative studies identified structural barriers such as stock-out of DNA PCR test kits and inconsistent human resources for sample collection as contributors to poor EID uptake.27 The suboptimal availability of DNA PCR results for MoMent infants who presented for testing reflects persistent programmatic challenges. In MoMent's experience, preanalytic (test kit stock-out, unavailability of sample collection staff, poorly collected samples, and transport inefficiencies), analytic (processing backlogs, sample rejection, and poor lab-to-site-communication), and postanalytic barriers (inefficient results communication and logistics) all played a part in the study's DNA PCR processing challenges. The presence of these barriers indicated the need for structural adjustments to capitalize on infants' timely presentation for EID. An analysis of MoMent-specific barriers to receipt of DNA-PCR testing and results is planned for future publication.

From our analysis, it seems that peer counselors in both study arms had comparable workload and client exposure. This suggests that the basis for the MM arm's superior EID presentation outcome was not the number of visits received per MIP but rather the quality of interactions toward client PMTCT compliance. A more in-depth analysis of peer counselor-MIP exposure and interactions is planned.

Besides MM support, late maternal gestational age at booking was also associated with increased EID presentation. This was unexpected because multiple studies have consistently associated earlier booking with uptake of EID and other postpartum services.28 It is possible that in our study setting, delayed antenatal booking and potentially late ART initiation may have motivated women to improve compliance with postpartum care, ultimately presenting their infants for timely EID.

Health facility delivery was associated with increased EID presentation; this finding is consistent with results from previous studies.28 Both outcomes are consistent manifestations of compliant health-seeking behavior.

Maternal education and religious affiliation were not associated with EID presentation. This is important to note because there were significantly more highly educated and Christian women in the MM arm, whose sites had overall lower ANC flow and higher HIV prevalence. The maternal education/religion imbalance occurred despite site-matching and may be due to better-educated women settling in economically appealing yet higher HIV-prevalence rural districts where skilled income-generating opportunities may have been better. Formative studies have also suggested that Muslim women have lower access to maternal health care partly because of economic dependence on male partners29; therefore, MoMent's health facility-based recruitment was bound to under-sample Muslim women.

In this study, rates of HIV infection among tested infants at first and second DNA PCR were extremely low; between zero and less than 1%. This is in stark contrast to the national estimate of 27.3%30 and IHVN's program result of 3.8% at PHCs.31 This may partly be explained by untested lost-to-follow-up infants, who may have high rates of infection. However, the modeled national estimate is population based, taking untested infants into account, hence the significantly high, but likely more accurate estimation. Differential breastfeeding rates may also factor: Breastfeeding rate for MoMent at 6 months postpartum was 84%, whereas the national rate at 12 months postpartum is 84%.32 Although the data are reported for different endpoints, one may infer that national breastfeeding rates at 6 months postpartum are higher than for MoMent and therefore pose higher risks for MTCT.

The MoMent study's strength lies in its generalizability, not only for the rest of Nigeria, but for similar unique and challenging high-burden, low-prevalence, low-resource settings. Optimal PMTCT service coverage and uptake in such settings may require significant adaptations to traditional interventions to reach eligible MIPs within an expansive population base. In our observation, the most important aspect of the structured intervention's success was supportive MM supervision coupled with a standard, time-bound procedure for flagging and tracking missed-appointment clients. Collaborative, knowledgeable supervisors and nonarbitrary procedures made a difference. These program elements empowered MMs to provide well-informed, objective-specific PS, which their clients positively responded to. Last, closely supervised, structured MM programs can provide the reliable maternal–infant linkages that Nigeria and similar settings need for EID and overall PMTCT program success.

Study Limitations

The nonrandomized nature of the study was a major limitation but was unavoidable because of programmatic obligations. We aimed to minimize bias through site-matching performed by an external consultant; however, ultimately there were significant differences between study-arm sites and mothers. We appropriately considered residual confounding by including site- and maternal-level covariates in the multivariate analysis model. Second, the inability to assess HIV infection among nonpresenting infants plus unavailable DNA PCR results from infants who presented for testing left potentially infected infants unaccounted for. Last, the study is limited by inability to evaluate the intervention's impact on longer-term infant outcomes, for instance survival and HIV infection rates at 12 and 24 months of life.

CONCLUSIONS

The MoMent study's demonstration of the intervention's impact on EID presentation is important because the evidence comes from a unique setting: very low-resourced (rural) communities with high PMTCT burden in a relatively low prevalence country. The large PMTCT programmatic gaps in Nigeria and in similar settings can potentially be bridged by building structure, supervision, and therefore increased quality into existing PS programs. As global efforts move from prevention to virtual elimination of MTCT, and from prophylaxis to lifetime treatment for HIV-positive pregnant women, resource-limited countries will have to increasingly engage lay workers to ease the burgeoning service-delivery burden. Peer counselor programs are proving to be appropriate resources for task-sharing and task-shifting; however, standards and structure are needed. National PMTCT programs now have ample evidence to formally adopt, support, structure, and scale-up PS interventions for desired maternal, child, and community-level outcomes.

ACKNOWLEDGMENTS

The authors thank Global Affairs Canada for financial support and the teams from WHO Geneva and Nigeria for their technical expertise.We acknowledge supportive collaboration of the Federal Ministry of Health, Nigeria, the Nasarawa State Ministry of Health, and the FCT Health and Human Services Secretariat. Our appreciation also goes to the IHVN program implementation teams for their enabling support. Finally, the authors are grateful to study site staff and pregnant women and mothers who participated in this project.

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Keywords:

PMTCT; early infant diagnosis; mentor mothers; implementation science; Nigeria

Supplemental Digital Content

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