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AIDS:
doi: 10.1097/QAD.0b013e3282f163b5
Clinical Science

Prevention of mother-to-child transmission: program changes and the effect on uptake of the HIVNET 012 regimen in Malawi

Moses, Agnesa; Zimba, Chifundoa; Kamanga, Esmiea; Nkhoma, Jacquelinea; Maida, Aliceb; Martinson, Francisa; Mofolo, Innocenta; Joaki, Georgea,✠; Muita, Janec; Spensley, Allisond; Hoffman, Irvinge; van der Horst, Charles Me; for the UNC Project Call to Action Program

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Author Information

From the aUNC Project, USA

bMalawi Ministry of Health and Population, USA

cUNICEF, Lilongwe, Malawi, USA

dElizabeth Glaser Pediatric AIDS Foundation, Washington, DC, USA

eUniversity of North Carolina, Chapel Hill, North Carolina, USA.

Deceased.

Received 22 February, 2007

Revised 14 August, 2007

Accepted 20 August, 2007

Correspondence to Dr C. van der Horst, University of North Carolina, CB 3368, Chapel Hill, North Carolina, 27599-3368, USA. E-mail: cvdh@med.unc.edu

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Abstract

Objective(s): To evaluate uptake of HIV testing in a prevention of mother-to-child transmission program (PMTCT) in Lilongwe, Malawi from April 2002 until December 2006.

Design: Retrospective analysis of monthly reports from the beginning of the program.

Setting: Four antenatal clinics in Lilongwe, Malawi.

Methods: Pregnant women attending urban antenatal clinics in Lilongwe were invited to participate in a PMTCT program. Women were given information and education on antenatal care and PMTCT in groups of 8 to 12. Written informed consent for HIV testing was obtained privately. Women returned for the test result 1–2 weeks later. Mothers and infants were given the HIVNET 012 regimen. Rapid HIV testing and ‘opt-out’ testing were instituted in July 2003 and April 2005, respectively. Infants were tested using HIV DNA PCR and, if HIV positive, a CD4 cell percentage was obtained and the infants were referred for further medical evaluation and treatment.

Results: The program reached 20 000 pregnant women in the first 12 months. Acceptance of HIV testing increased from 45% to 73% (P < 0.001) when rapid, same day testing was instituted. When opt-out testing was instituted, 99% of the mothers agreed to testing. Of the infants tested, 15.5% were HIV positive.

Conclusion: Rapid HIV testing using the opt-out method increased acceptance of HIV testing in the PMTCT program to 99% in urban Lilongwe, Malawi.

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Introduction

In Malawi, a country of 13 million, more than 90 000 children aged 0–14 years were HIV infected in 2006 [1]. Approximately 90% of the infected children acquired the virus through vertical transmission from their mother. With a dose of nevirapine given at onset of labor to the mothers and newborn infants, the rate of infection has been reduced from 27% to 11.9% at 6 weeks and 16% at 8 weeks after delivery in a breast-feeding population [2–4]. This report describes a program for prevention of mother-to-child transmission (PMTCT) using this regimen in Lilongwe, Malawi and adjustments that increased uptake of HIV testing.

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Methods

In 2001, the University of North Carolina (UNC) Project in in Lilongwe, Malawi received a planning grant from the Elizabeth Glaser Pediatric AIDS Foundation. Partners included UNICEF Malawi for supplies, Baxa Corporation for pediatric feeding syringes, and Global Strategies for HIV Prevention for nevirapine. PMTCT services at the antenatal clinic at Bottom Maternity Hospital were introduced in April 2002 and expanded in late 2002 to the District Health Centers in Kawale and Areas 18 and 25. Eleven full-time staff provided counselling services in addition to the existing government staff. Collaboration with existing AIDS support agencies, National Association of People with HIV and AIDS Malawi and Kanengo AIDS Support Organization, was fostered to help with information, education, and communication for the community.

All pregnant women were given education on prenatal care, nutrition, HIV, sexually transmitted infections, family planning and the PMTCT program in the waiting area. Detailed information on PMTCT was given in groups of 8 to 12. Pretest counselling, written consent and a physical examination were done privately. Counselling time was 1 h. A 5 ml whole blood sample was obtained for HIV enzyme-linked immunosorbent assay (ELISA) (BioRad Genetic Systems HIV-1/2 EIA; Hercules, California, USA), syphilis testing (Determine Syphilis TP; Abbott, Abbott Park, Illinois, USA), and hemoglobin. Urine protein and glucose were also obtained. The women returned for the test result 1–2 weeks later and for individual post-test counselling. HIV-positive mothers were given a single dose of nevirapine 200 mg at week 32 to be take at the onset of labor. All women also received routine antenatal care according to national guidelines, including tetanus vaccination and malaria prophylaxis with sulfadoxine–pyrimethamine once during the second and third trimesters. All exposed infants were given nevirapine 2 mg/kg within 72 h of birth. If the mother delivered before receiving nevirapine or before 32 weeks, the baby was given nevirapine immediately after birth and a second dose within 48–72 h.

In July 2003, two parallel rapid HIV tests [Abbott Determine HIV-1/2 and Uni-Gold HIV (Trinity Biotech plc, Bray, Eire)] replaced the use of ELISA. The Bioline HIV-1/2 3.0 (Standard Diagnostics, Kyonggi-do, South Korea) was used as a tie-breaker. Ten percent of all the samples were sent to the UNC Project laboratory for quality assurance. Confidentiality was ensured by use of identification numbers.

In April 2005, ‘opt-out’ testing was instituted in collaboration with the Malawi Ministry of Health. All women received health education in the waiting area where opt-out was explained, then moved into smaller groups of eight for pretest counselling and then to a private room for routine antenatal care. If the woman verbally consented, blood was obtained for the rapid test at the laboratory. Post-test counselling for all women was done individually. With this change, women were provided with nevirapine during the same day visit. There was no retesting of women prior to delivery. A yellow card for identification by the nurse on duty in the labor ward was given to each woman so the infant was not missed during delivery.

Infants who returned with their mothers at 6 weeks postpartum for well-baby care were offered an HIV DNA PCR test (Amplicor HIV-1 DNA test version 1.5; Roche Molecular Systems, Branchburg, New Jersey, USA) and hemoglobin estimation. An ELISA was done at 18 months. Beginning in May 2006, all infants received cotrimoxizole from 6 weeks, and if they were HIV positive their CD4 cell percentage was measured with referral for evaluation and treatment. Since July 2006, all women with a CD4 lymphocyte count < 500 cells/μl received cotrimoxizole.

Ratios were compared by the two-tailed χ2 and 95% confidence intervals (CI) were calculated using the exact binomial method.

This analysis constituted an evaluation of a government public service program and information for data analysis was recorded so that subjects could not be identified and was exempted upon review by the UNC and Malawi Institutional Review Boards.

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Results

Figure 1 illustrates the increasing number of pregnant women approached to participate in the PMTCT program as the program was rolled out over a period of a year and increasing acceptance of voluntary counselling and testing (VCT) as changes were implemented to improve the program. As the program was simplified and education improved in the waiting areas, in the community education visits to surrounding villages, and through marketplace theater, the percentage of women agreeing to HIV testing steadily increased. In the early days of the program, uptake increased from 45% (95%, CI, 43.62–46.25) (second quarter 2003) to 73% (95% CI, 71.53–73.98) (second quarter 2004) (P < 0.001) when the introduction of rapid testing allowed women to obtain results without having to return to the clinic for an additional visit. The women who refused to participate usually cited a need to speak to their husbands before agreeing to a test. By switching to an opt-out procedure, uptake of HIV testing increased to over 99% (95% CI, 99.68–99.93; P < 0.001). In many cases, those few women refusing to have the HIV test returned the next week requesting that they be tested. Formative research of clients did not reveal any evidence of coercion with introduction of opt-out, nor has there been a diminution in the number of clients.

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Fig. 1
Fig. 1
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Although women do not always deliver at one of the four sites, the percentage of pregnant women delivering in facilities has steadily increased from 23.5% (95% CI, 21.65–25.50) in 2003 to 54.6% (95% CI, 52.88–56.38) in 2006 (P < 0.001; Fig. 2). However, 45.4% of infants did not receive nevirapine in 2006 as the baby was delivered by a traditional birth attendant at their home. From October to December 2006, information was collected from three of the four maternity wards to determine the number of women who were delivering at the health centers but had not been through the PMTCT program. Only in 54 out of 1286 (4%) deliveries did the woman have an unknown HIV status.

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Early diagnoses through HIV DNA PCR at 6 weeks has been offered through the program since 2004. During the first year, only 459 (19.4%; 95% CI, 17.82–21.05) of the babies born to HIV-infected mothers were tested and 26.6% were infected. Testing increased in 2005 to 734 infants (16.5% positive) and in 2006, 1090 (34.5%; 95% CI, 32.85–36.19) of the infants were tested (15.5% positive; P < 0.001).

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Discussion

The implementation of any PMTCT program requires effective monitoring and evaluation to guide the services provided. Continuously monitoring the various steps of the process from community education, client education, informed consent, HIV testing, adherence to the regimen, delivery at a health center, and early diagnosis of infected infants allowed early realization and correction of program weaknesses. Staff were trained not only to provide the service but also to conduct the monitoring and evaluation themselves, generating weekly reports on each step of the process, which were then reviewed by the senior staff. Through partnership with a variety of governmental and nongovernmental agencies, we were able to reach 20 000 pregnant women annually for VCT within 18 months of receipt of the planning grant.

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Fig. 2
Fig. 2
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Initially we limited our program to the VCT aspect and the HIVNET 012. regimen, leaving the responsibility of providing antenatal care to the government. Uptake was poor and women were not receiving full antenatal care largely because of ‘stock-outs’ of essential medications and staff shortages. Uptake of the program improved dramatically with joint training of government staff, hiring of additional staff, implementation of rapid testing, and provision of supplies directly from UNICEF to the project. The goal is for the eventual complete integration of services: that is, existing personnel provide PMTC and antenatal care within the government system.

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Our rate of acceptance of testing is higher than many previous reports. At the Médecins Sans Frontières PMTCT site in Thyolo, Malawi, there was an uptake of 95% for HIV testing (2996 mothers) but only 45% of the mothers and 34% of the infants received nevirapine [5]. In Mombasa, Kenya, of the 3564 first-visit pregnant women receiving health education, 2484 (69.7%) were tested; 348 (14%) were HIV positive, and 106 women took nevirapine in labor [6]. In Burkina Faso, only 18.3% of pregnant women accepted VCT, with a seroprevalence of 10.6% (95% CI, 8.8–12.5) [7]. An evaluation routine of HIV test acceptance at four antenatal clinics in Francistown, Botswana was conducted in 2004; this compared the last 4 months of the traditional opt-in testing method to the first 3 months of opt-out testing [8]. Uptake increased from 75.3% to 90.5% when opt-out was introduced (P < 0.001).

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In some countries, the PMTCT programs have begun routine testing during labor and delivery to reach women who have not had antenatal care [9,10]. In Lilongwe, > 90% of pregnant women access antenatal care, and uptake of HIV testing is now 100% among those who access antenatal care. Our survey of maternities show that it would not be cost effective to implement testing in the labor ward in Lilongwe.

The major weakness in our program is that 45% of women still do not deliver at one of the four maternity wards, and, consequently, infants miss their nevirapine dose. We now provide the mothers with a syringe containing the infant's nevirapine dose, as is done in the Kenya program, and are incorporating the traditional birth attendant to facilitate and record this procedure. One constant problem is the maternity wards are chronically understaffed and the poor nurse to client ratio makes delivering at a healthcare facility less attractive.

Another weakness of the program is that we do not have a measure of the compliance of the mothers with their nevirapine dose. Since this is not a cohort study and few infants return for testing, the transmission rate data are biased owing to self-selection. Nonetheless our rate of 15.5–16.5% compares with that of a similar population enrolled in a multisite randomized study from Malawi, Tanzania, and Zambia, where follow-up was excellent and the rate of transmission after single-dose nevirapine was 15.8–16.2% at 6 weeks [4].

Diagnosis for data collection purposes is valuable, but we believe it is crucial to link testing with treatment for both mothers and infants, including the provision of cotrimoxizole and antiretroviral drugs. Although improving over time, only 35% of the infected mothers returned with their babies for early diagnosis of HIV at 6 weeks, despite linking early infant diagnosis with routine vaccination dates and provision of antiretroviral drugs. Integration of PMTCT services into routine antenatal care has proven crucial for the success not only of uptake of the PMTCT services but also of VCT. This successful integration is a result of strong and focused collaboration with many stakeholders. Although there are clearly PMTCT regimens that are more effective, currently the cost of these and the necessary staffing levels to implement them are not available in Malawi. Given the successes of our program, expansion to other centers in Malawi should be undertaken in a similar model.

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Acknowledgements

We thank Pius Tih and Thomas Welty from Cameroon for advice on begining the program; Nina Pagadala and Cathy Wilfert from the Elizabeth Glaser Pediatric AIDS Foundation; Alisa Cameron from USAID; Miriam Chipimo and Joyce Meme from UNICEF; Emily Sickbert-Bennett for the statistical analysis; Topia Banda, David Chilongozi, and Topia Banda from UNC Project; Peter Kazembe from Kamuzu Central Hospital; and David Jones, without whose help none of this would be possible.

Sponsorship: This study was supported by the Elizabeth Glaser Pediatric AIDS Foundation (planning and implementation grants), Global Strategies for HIV Prevention (the initial nevirapine shipment), Baxa Corp. (syringes), UNICEF (supplies), Axios (nevirapine from Boehringer Ingelheim Gmbt and the Abbott HIV Determine Tests from Abbott Laboratories), World Food Program (food baskets for mothers), and USAID (support for the last year). Dr van der Horst is supported by the UNC Center for AIDS Research (P30-AI50410), the NIH South Africa CIPRA (5U19AI053217) and the US Centers for Disease Control and Prevention BAN Study (SIP 26-04 U48/DP000059-01); Irving Hoffman, Innocent Mofolo, and Francis Martinson by the Johns Hopkins–UNC–Malawi College of Medicine HPTN Award (PO 8011-39050-0) and Agnes Moses and George Joaki by the UNC Fogarty Award (5-D43 TW01039-07).

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References

1. UNAIDS. Report on the Global AIDS Epidemic 2006, Annex 2: HIV and AIDS Estimates and Data, 2005 and 2003. Geneva: UNAIDS, 2006.

2. Biggar RJ, Miotti PG, Taha TE, Mtimavalve L, Broadhead R, Justesen A, et al. Perinatal intervention trial in Africa: effect of birth canal cleansing intervention to prevent HIV transmission. Lancet 1996; 347:1647–1650.

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4. Taha TE, Brown ER, Hoffman IF, Fawzi W, Read JS, Sinkala M, et al. A phase III clinical trial of antibiotics to reduce chorioamnionitis-related perinatal HIV-1 transmission. AIDS 2006; 20:1313–1321.

5. Manzi M, Zachariah R, Teck R, Buhendwa L, Kazima J, Bakali E, et al. High acceptability of voluntary counselling and HIV-testing but unacceptable loss to follow up in a prevention of mother-to-child HIV transmission programme in rural Malawi: scaling-up requires a different way of acting. Trop Med Int Health 2005; 10:1242–1250.

6. Temmerman M, Quaghebeur A, Mwanyumba F, Mandaliya K. Mother-to-child HIV transmission in resource poor settings: how to improve coverage. AIDS 2003; 17:1239–1242.

7. Pignatelli S, Simpore J, Pietra V, Ouedraogo L, Conombo G, Saleri N, et al. Factors predicting uptake of voluntary counselling and testing in a real-life setting in a mother-and-child center in Ouagadougou, Burkina Faso. Trop Med Int Health 2006; 11:350–357.

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Keywords:

Africa; prevention of perinatal transmission; vertical transmission; women

© 2008 Lippincott Williams & Wilkins, Inc.

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