Short antiretroviral prophylaxis regimens with zidovudine or nevirapine (NVP) or with 2 drugs (zidovudine and lamivudine) reduce infant HIV infections in resource-limited settings.1-6 Extending the benefits of these recent breakthroughs in prevention of mother-to-child HIV transmission (PMTCT) to most HIV-infected women in the world remains a tremendous challenge, particularly in sub-Saharan African communities, where more than two thirds of the HIV-infected population resides.7-14
In Cameroon, from 1986 to 2000, overall HIV-1 seroprevalence increased from 5% to 11%, and approximately 62,000 newborns were at risk for mother-to-child HIV transmission in 2002.15 In 2002, the Ministry of Health established national guidelines and an implementation plan for PMTCT.15 The Cameroon Baptist Convention Health Board (CBCHB) PMTCT Program, with support from the Elizabeth Glaser Pediatric AIDS Foundation (EGPAF) began in February 2000 at 2 hospitals in Northwest Province; by December 2004, it had rapidly expanded to 115 facilities in 6 of the 10 provinces in Cameroon. This report describes how the CBCHB successfully integrated PMTCT into routine antenatal care, achieved high uptake of rapid HIV testing and posttest counseling on the same day, implemented routine use of peripartum single-dose NVP for HIV-positive mothers and their infants, continuously monitored PMTCT services, and upscaled the program in collaboration with the National AIDS Program.
The components of the CBCHB PMTCT Program in Cameroon include training staff on PMTCT and voluntary testing and counseling; providing technical assistance, HIV tests, and NVP at no charge; monitoring workload and quality of care at all facilities providing PMTCT; and establishing support groups. Before this program, CBCHB facilities did not routinely offer HIV screening to antenatal patients.
Beginning in February 2000, nurse counselors gave group talks at first antenatal clinic visits, explaining the 3 or 4 usual antenatal laboratory tests (hemoglobin, syphilis, and urinalysis, and, in some facilities, blood type) and the addition of the HIV test, which became available at no charge through the PMTCT Program. The counselors stressed the importance of the HIV test as a critical component of antenatal care and explained NVP prophylaxis. All aspects of pretest HIV counseling were included in this lecture, and the counselors facilitated dialogue among the antenatal patients about how infected and uninfected women might share the results with their spouses and encourage them to come in for testing. After this lecture, the counselors completed the pretest counseling individually and in private, answering any questions the patients had about the laboratory tests and administering a brief questionnaire on risk factors for HIV infection. All patients signed a consent form indicating which of the 4 or 5 tests, if any, they wished to decline. Because there is no legal requirement for signed consent for HIV testing in Cameroon, we began obtaining verbal consent for HIV testing in 2001 using the same methodology.
On-site laboratories performed blood type (if available), hemoglobin, syphilis, urinalysis, and 2 rapid HIV antibody tests, Determine (Abbott) and Hema Strip (Saliva Diagnostics Systems). From February through November 2000, we sent dried blood spots to the Centers for Disease Control and Prevention (CDC) for confirmatory enzyme-linked immunoassay (ELISA) and Western blot testing to assess the performance of the rapid tests.16 If the results of the Determine and Hema Strip tests were discrepant, on-site laboratories performed a third “tie-breaker” test (Capillus, Sero-Card, or HIV Chek).17
After we analyzed confirmatory ELISA and Western blot test results on the first 879 patients, we changed our rapid HIV testing protocol, because the Determine and Hema Strip tests were highly sensitive and specific.16 We now use a sequential testing algorithm with Determine as our primary test and perform a second rapid test (Hema Strip, HIV Chek, Bioline, or OraQuick) only if the Determine assay is positive.17 If the result of the second test is negative, we perform a third tie-breaker test.
While waiting for laboratory results, midwives performed routine first antenatal examinations. The same provider who counseled the patient before testing provided the posttest counseling, usually within 1 to 2 hours after phlebotomy. The counselors documented the following on the antenatal flow sheets and consultation books (medical records kept by the patients): for HIV-negative patients, “Post-test counseling done-HIV negative,” and for HIV-positive patients, “Post-test counseling done-administer NVP in labor.” They educated HIV-negative patients on prevention, the “window period” for HIV seroconversion, and the need to retest in 3 months to ensure true negative status. They educated HIV-positive patients on safe sex, disclosure methods, positive living measures to delay progression to AIDS, and the importance of taking NVP as soon as labor began and referred them to a support group. They discussed infant feeding options, reviewing the risks and benefits of artificial, mixed, and exclusive breastfeeding. The counselors scheduled follow-up visits for HIV-positive mothers, and when possible, their spouses, who were offered HIV testing at no charge.
We emphasized the importance of confidentiality to all staff and encouraged patients to share their results with their spouses and with trusted family members and friends but not to share them with other patients, even if they were negative. To maintain confidentiality, we used unique identifiers for data entry and locked up register books when not in use.
For all HIV-positive antenatal patients and their newborns, we recommended single-dose NVP (200 mg to the mother at the onset of labor and 2 mg/kg to the newborn within the first 72 hours of life), a regimen identical to the one that reduced mother-to-child transmission by 47% in Uganda.4 Initially, HIV-positive mothers signed a second consent form for NVP prophylaxis. After the World Health Organization (WHO) formally recommended the use of NVP for prevention in November 2000, we no longer obtained written consent for NVP prophylaxis.
Because a number of the HIV-positive patients did not come in until delivery was imminent or delivered elsewhere, in 2002, our staff began giving antenatal patients NVP at 34 weeks of gestation to self-administer when they went into labor. To increase even further the proportion of HIV-positive mothers treated, we began giving them NVP at their first antenatal visit in 2004, because some mothers did not return for follow-up antenatal visits and therefore never received NVP. We advised women to bring their babies for NVP prophylaxis by the third day of life, if they delivered at home or at another facility where the NVP elixir was not available.
Most infants received NVP 48 to 72 hours after birth and before discharge. If discharged less than 48 hours after delivery, the infants received it at the time of discharge. If the mother took NVP less than 2 hours before delivery or did not receive NVP, the infant was treated immediately after birth and again at discharge.
We refer all HIV-positive mothers and their spouses to support groups that meet monthly, which is the most efficient way to meet their medical, psychologic, and spiritual needs, including provision of free cotrimoxazole prophylaxis of Pneumocystis carinii pneumonia (PCP) for these mothers and their infants, treatment of latent tuberculosis infections, and HIV testing of the infant. In addition, we ask permission to make home visits to all HIV-positive women, if they do not return for their recommended antenatal and postpartum visits.
To determine the effectiveness of NVP prophylaxis, we performed DNA polymerase chain reaction (PCR) testing (Roche Amplicor HIV-1 DNA PCR test, version 1.5; Molecular Roche Systems, Alameda, CA) at Projet Retro-CI in Abidjan, Côte d'Ivoire on dried blood spots from a subset of HIV-exposed 6-week-old infants. We performed HIV antibody tests at 15 or more months of age (after maternal antibody waned), at least 3 months after weaning, to determine which children were infected through breast milk.
The CBCHB counselors gradually expanded the program to other rural and urban health facilities by one-on-one teaching of the local antenatal clinic and maternity staff on how to integrate PMTCT activities into their usual antenatal and obstetric care. This involved a planning visit and at least 2 follow-up visits, followed by monthly supervisory visits to provide program support and collect workload statistics.
In 2002, 2 nurse counselors (G. Ndikintum and G. Nkuoh) were trained and certified as counselor trainers at Mildmay International Study Center in Kampala, Uganda. Upscaling then accelerated through multiple training sessions for up to 20 antenatal, obstetric, and laboratory staff per session and the development of a training manual (available at: http://womenchildrenhiv.org) to expand the program in a more efficient and consistent manner. The manual has been translated into French, Spanish, and a regional African language (Hausa) to make it more useful. The CBCHB developed 2 videotapes in English and French designed to assist with the group pretest counseling and with the training of health care workers to implement PMTCT (available through the Johns Hopkins University Media Center, Baltimore, MD; http://www.hcpartnership.org/mmc/mmc_search.php).
Trained Birth Attendants
In 1982, the CBCHB's outreach branch, the Life Abundant Primary Health Care Program, began training birth attendants in primary health centers to provide antenatal care, assess obstetric risk, and perform low-risk deliveries in primary health centers in remote villages of Cameroon.18 Before starting the PMTCT Program in primary health centers, CBCHB staff met with each village health committee, explained the program, emphasized the importance of confidentiality, and solicited their input. In June 2002, after receiving approval from the village health committees, we began training birth attendants to provide confidential HIV counseling and testing and to integrate PMTCT into their rural practices using an oral fluid rapid HIV antibody test (OraQuick by OraSure Technologies).7,17 They are assisted by supervisory nurses, who visit their villages approximately once a month and perform a second rapid HIV test (Determine or Hema Strip) on those women whose OraQuick test result is positive. We refer women with discordant test results to a hospital or integrated (middle level) health center for a third tie-breaker assay. The birth attendants dispense NVP to HIV-positive mothers at the first visit or at 34 weeks of gestation and ensure that the mothers and their babies receive peripartum NVP prophylaxis.
We established support groups for newly identified HIV-positive mothers and encouraged spouses to participate in antenatal and obstetric care and in support groups. In June 2002, one of these support groups participated in an international conference, “PMTCT in Cameroon: Hope for the Next Generation,” sponsored by the CBCHB, EGPAF, CDC, Cameroon Ministry of Health, and United Nations Children's Fund (UNICEF).19 In April 2004, 17 members of CBCHB-sponsored support groups made multiple presentations in Yaounde, the capital city, to governmental officials, churches, national television and radio, and international radio, thereby reducing stigma and increasing awareness.
Data Management and Analysis
To facilitate data entry, each CBCHB-assisted facility maintained 2 handwritten logs of antenatal patients, HIV risk factors, counseling, test results, and NVP administration plus a tally sheet of each clinic's monthly workload. CBCHB supervisors visited each participating facility regularly, carried the first logbook and a workload tally sheet back for data entry, and left the second logbook for ongoing data collection.
We entered monthly workload data into Excel spreadsheets to track facility-specific HIV seroprevalence and other pertinent parameters, entered demographic and risk factor data from the register books into Epi Info, and exported the Epi Info data into SAS (SAS Institute, Cary, NC) for univariate and multivariate analyses. We calculated unadjusted and adjusted estimates of the prevalence odds ratios and 95% confidence intervals and performed multivariate adjustment for potential confounders using the SAS logistic procedure.
Ethical Review and Quality Improvement
The CBCHB's Institutional Review Board approved each phase of the PMTCT implementation protocol. The EGPAF contracted with Family Health International for periodic on-site program reviews to improve services further.
By December 31, 2004, the CBCHB had trained 690 health care workers to integrate PMTCT into their antenatal and obstetric care. The cumulative workload and rapid program expansion are depicted in Figures 1 and 2.
In 2004, mean HIV test acceptance and seroprevalence varied by type of facility (Table 1). Most patients who refused HIV testing said that they wanted to discuss testing with their husbands first or that they were afraid to get tested. Because of the rapid expansion to so many facilities, we do not yet know whether the change in seroprevalence (mean of 10.5% in 2000, 9.9% in 2001, 9.5% in 2002, 7.7% in 2003, and 8.9% in 2004) represents a reduction in seroprevalence or reflects the addition of more facilities in lower prevalence areas.
Since July 2002, the pilot program using trained birth attendants in 20 primary health centers has had a 96.2% acceptance rate of saliva rapid HIV testing, and 25 (4.8%) of the 520 women tested were HIV-positive. Although concerns have been raised about breaches in confidentiality resulting from birth attendants providing voluntary HIV testing and counseling in their small villages, where many people are related, we have found no evidence of such breaches. Nurse supervisors counseled some close family members of the birth attendants so as to preserve confidentiality.
Between February 2000 and June 2002, we surveyed 8452 consenting antenatal patients regarding sociodemographic and HIV risk factors. Women older than 35 years of age were at the lowest risk of infection, whereas those aged 20 to 24 years were at the highest risk (Table 2). Single women and those who were widowed, separated, or divorced were at significantly higher risk than married women. Women with positive syphilis serology (4.1% of women tested) were twice as likely to be HIV infected as those with negative syphilis serology. Anemia was strongly associated with HIV infection: women whose hemoglobin level was less than 9 g/dL (5.9% of the women tested) had 2.5 times higher HIV infection rates than those whose hemoglobin level was 13 g/dL or higher (test for trend, P < 0.001). Women with 4 or more pregnancies were less likely to be infected than women with fewer pregnancies. The median reported duration of postpartum sexual abstinence after the last pregnancy was 18 months, and the median duration of breastfeeding was 19 months (data not shown); neither was associated with prevalent HIV infection.
Initiating sexual intercourse during adolescence increased risk for HIV infection (P < 0.001). The number of sex partners reported in the past 3 years was also strongly associated with HIV-1 seropositivity (test for trend, P < 0.001). More than 40% of women who received antenatal care reported polygamous marriages; however, polygamy was not associated with HIV infection (data not shown). Ninety-nine percent of women reported that their sex partners were circumcised. Few women reported that their partners ever used condoms (18%), and those who used them did so infrequently.
Factors that remained strongly associated with HIV-1 infection in multivariate analysis included age, marital status, positive syphilis serology, low gravidity, young age at first sexual intercourse, and number of sex partners reported in the past 3 years (Table 3). Although low hemoglobin level remained strongly associated with HIV infection (P < 0.001), we did not include it in the final multivariate model, because anemia is often a manifestation of HIV/AIDS rather than a cause.20
Results of the first 5 years of the CBCHB PMTCT Program demonstrate a substantially higher HIV test acceptance rate than in most programs in sub-Saharan Africa11,21-25 and are similar to the rates described during the first year of the national PMTCT program in Thailand and in an urban South African township.12,26 We attribute our high HIV test uptake and posttest counseling rates to our strategy of offering PMTCT as a routine part of antenatal care, thus reducing stigma while educating patients about the rationale and importance of all antenatal tests. Our staff report that women who receive PMTCT services become highly effective educators to families and communities. Other factors that contribute to the high uptake of HIV testing in the CBCHB PMTCT Program are as follows:
- Interactive and enthusiastic antenatal education by trained maternity staff at the first antenatal visit, stressing the importance of HIV testing and NVP prophylaxis in increasing the likelihood of having a healthy baby.
- Provision of same-day test results and individual pre- and posttest counseling by the same counselor.
- Intensive follow-up and quality assurance provided by the supervisory staff to participating facilities.
Although some programs have advocated providing universal NVP prophylaxis to all women of unknown HIV status in communities with high HIV seroprevalence,13 we review educational and counseling techniques in facilities with below-average uptake and make recommendations to improve uptake rather than treating all women of unknown HIV status. We promote male involvement by discussing culturally appropriate ways that the mothers can present HIV test results to their spouses and by strongly encouraging spouses to attend the first antenatal visit so they can participate in the decision-making process.27
To our knowledge, this is the first PMTCT program worldwide to use trained birth attendants to provide confidential HIV counseling and testing, utilizing an oral fluid rapid test.7 The extensive discussions with and approval from each village health committee before implementation of this program likely contributed to the high acceptance rate and positive feedback from village women.18 The proximity and constant availability of a trusted birth attendant enables better patient education and follow-up than is achievable in larger health facilities to which women have to travel for care. The CBCHB is expanding PMTCT to all rural primary health centers that have birth attendants, and other organizations in Cameroon, Nigeria and Zambia are planning to start a similar program based on our model.
Risk factors for HIV infection among women of childbearing age were, for the most part, similar to those found in other African settings.28-30 Male circumcision is almost universal in Cameroon and may contribute to the lower HIV-1 seroprevalence there than in several other African nations.31-34 A history of multiple sex partners, young age at first sexual intercourse, single marital status, and positive syphilis serology remained strongly associated with HIV infection when simultaneously controlling for other covariates. The long period of postpartum sexual abstinence, which coincides with the duration of breastfeeding, is based on tribal tradition in West Africa and, contrary to a recent report,35 was not associated with prevalent HIV infection in rural Cameroon.
Although we explain the risk of breast milk transmission of HIV and offer powdered infant formula when supplies are available, artificial feeding is not an option for most rural women in Cameroon, because mixed feeding (breast milk plus water and local foods) is the cultural norm and because of the labor-intensive effort required to boil water for each feeding so as to prevent enteric illness. We promote the relatively safe alternative of exclusive breastfeeding for 3 to 6 months, followed by rapid weaning, as recommended by the WHO and in a recent review article.36 Achieving exclusive breastfeeding is difficult, however, because mothers who are subsistence farmers have to leave their young infants in the care of relatives when they are farming, and the relatives usually give them supplemental food and water. All 320 women surveyed in 4 rural villages in Cameroon in 2001 through 2002 introduced supplemental water and food by the time their infants were 6 months old, and 38% supplemented water in the first month of life.37 We are currently evaluating infant feeding practices in HIV-positive mothers.
Limitations of our program include the lack of systematic documentation of when women received NVP (usually at the first visit or 34 weeks of gestation) to self-administer at the start of labor and the lack of an infant dose that the mothers can give if they deliver at home or at a facility that does not stock NVP. We are exploring the feasibility of using prefilled leak-proof syringes of NVP syrup so that the mothers can administer the infant dose. We have improved our reporting system to document NVP prophylaxis rates more accurately.
Fifteen (13%) of the first 115 HIV-exposed infants who returned for follow-up had a positive PCR test result at 6 to 8 weeks, similar to the infection rate reported in HIVNET 0124 and to the transmission rate of 10.9% found in another study in Cameroon.38 We plan to report additional results of infant DNA PCR and antibody tests of HIV-exposed children at the age of 15 months or older elsewhere. Follow-up of all HIV-positive mothers and their babies is difficult.39 If HIV-positive mothers and their infants fail to return for follow-up as scheduled, we make home visits to those who have granted permission. We have formed 22 support groups of HIV-positive mothers and fathers with more than 650 members, thereby improving follow-up.
The PMTCT Program strives to meet the needs of the HIV-positive mothers and their babies by counseling them on nutrition, infant feeding, condom use, family planning, medical care, and spiritual strength and comfort during the monthly support group meetings. In addition, the CBCHB received a grant from the Columbia University MTCT-Plus program in 2004 to treat HIV-positive mothers, their spouses and children, and health care workers with potent combination antiretroviral therapy when indicated.40 The availability of these services and antiretroviral therapy enhanced the appeal of support groups and contributed to their rapid expansion.
Although the EGPAF is supporting 50 PMTCT programs with more than 500 participating health care facilities in 19 countries through its “Call to Action” program (available at: http://www.pedaids.org/glob_sitemap.html), few countries in sub-Saharan Africa have so far committed to nationwide implementation. Faith-based health care facilities provide a substantial proportion of health care in most sub-Saharan African nations, and the success of this program demonstrates the importance of faith-based-public sector partnerships in reaching as many pregnant women as possible with PMTCT services. The provision of donated NVP (Viramune) tablets and elixir from Boehringer Ingelheim Pharmaceutical Company and Determine rapid HIV tests from Abbott Laboratories through the Axios Foundation (available at: http://www.axios-group.com/en/Default.aspx) and the ongoing support from the EGPAF have sustained this program expansion for the past 5 years. The continuation of this support, the use of existing antenatal and obstetric staff to provide PMTCT services rather than hiring new staff, and the potential support from the National AIDS Program increase the likelihood of long-term sustainability. Funding from the EGPAF's International Leadership Award has enabled the CBCHB to expand PMTCT training nationally and internationally. Our partnership with the National PMTCT Program is an excellent example of nongovernmental organization (NGO)-government collaboration. The cost of preventing 1 HIV-infected child through this program is estimated to be $280 to $430, which is a very cost-effective intervention (Dr. Elliot Marseille, DrPH, MPP, personal communication, 2003).
The WHO recommends a 4-pronged approach to reduce the impact of HIV/AIDS on children: (1) prevention of HIV in women, especially young women; (2) prevention of unintended pregnancies in HIV-infected women; (3) PMTCT; and (4) provision of care and support to HIV-infected women as well as to their infants and families.41,42 To attain the United Nations (UN) General Assembly's goal of reducing mother-to-child transmission by 50% by the year 2010,41 it is clearly essential to improve primary prevention through behavior change. Our risk factor analysis suggests that primary HIV prevention among young women should focus especially on promotion of delay in sexual debut, fewer sexual partners, and appropriate condom use, a strategy consistent with a recent consensus statement.43 Affordable and accessible family planning and antiretroviral therapy during pregnancy and breastfeeding are also essential. After a baseline sexual survey of 4600 youth in 2004, the CBCHB started the Youth Abstinence Network in schools and young people's groups and plans to evaluate its impact. With a comprehensive 4-pronged approach, Cameroon could meet the UN goal. The success of the CBCHB PMTCT Program may encourage faith-based health care organizations and sub-Saharan African governments to form public health partnerships that use available resources most efficiently to improve clinical services and public health.
The antenatal and obstetric staff at all participating facilities worked tirelessly to implement the PMTCT Program and to document the work they did. The staff made difficult trips through mud and dust to support this program in remote health centers that have no electricity or telephone. The mothers had the courage to consent to HIV testing because of their concern for the health of their babies. Dr. Gad Fokum and Dr. Rod Zimmerman and the CBCHB medical staff provided clinical support. Dr. Derrek Massanari, Dr. Andrea Cedfeldt, Dr. Ray Shields, Forgwei Gideon, Nshom Emmanuel, Kidio Josephine, Dorothy Meyer, and Erin Petrie assisted with training, data management, and analyses. Mary Bumuh provided nutritional counseling for HIV-positive mothers. Patricia and Geoffrey Mitchell, Wanyu Benjamin, Fombe Justin, and the nurse supervisors of the Life Abundant Program provided critical training and support to birth attendants, who give high-quality antenatal and obstetric care, now including PMTCT in remote villages of Cameroon. Peter Kakute surveyed rural women on infant feeding practices. Ndosak George conducted the adolescent sexual survey and is implementing Youth Abstinence Clubs. Tancho Sam provided training and quality assurance of rapid HIV testing at all sites. Dr. Elliott Marseille performed a cost analysis of the CBCHB PMTCT Program. Dr. Mary Glenn Fowler provided expert advice on technical aspects of perinatal HIV prevention. Drs. George Alemnji, Peter Fonjungo, Marcia Kalish, and Mark Rayfield from the CDC provided technical consultation on laboratory issues and assisted with the supply of HIV tests. Dr. Bharat Parekh and Tim Granade provided confirmatory enzyme immunoassay and Western blot testing on dried blood spot specimens for our pilot study. Jeffrey Wiener assisted with data analysis and graphical presentation. Dr. Anne Nlend and Dr. Landry Tsague, National PMTCT Program Directors; Dr. Akwe Samuel, AIDS Coordinator of the Southwest Province; Dr. Mayer Magdalene, AIDS Coordinator of the Northwest Province; Dr. Nchifor Simon, Director of the Northwest Provincial Hospital; and Dr. Akam Wilfred, AIDS Coordinator of the Limbe Provincial Hospital provided enthusiastic support. The authors thank the EGPAF for financial support and the technical and administrative support provided by their staff, including Dr. Dirk Buyse, Chuck Hoblitzelle, and Trish Karlin.
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