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,3
ZVITAMBO Project, Harare, Zimbabwe;
* SARA Project, Academy for Educational Development, Washington, DC;
University of Zimbabwe, Department of Paediatrics and Child Health, Harare, Zimbabwe;
** Formerly of the ZVITAMBO Project, Harare, Zimbabwe;
Harare City Health Department, Harare, Zimbabwe; and

The Johns Hopkins Bloomberg School of Public Health, Department of International Health, Baltimore, MD
3To whom correspondence should be addressed. E-mail: jhumphrey{at}zvitambo.co.zw.
| ABSTRACT |
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KEY WORDS: breast-feeding HIV exclusive breast-feeding mother to child transmission Zimbabwe
An estimated 630,000 infants and young children are infected with HIV each year through mother-to-child transmission, and the vast majority of cases occur in sub-Saharan Africa (1). Breast-feeding is an important route of transmission, causing about 280,000 to 300,000 infections annually, or about 42% of pediatric infections (2). This has created one of the most poignant dilemmas of the HIV pandemic, because breast-feeding also protects infants from diarrhea and other infections, and is an important birth-spacing method for millions of families. A recent review noted that breast-feeding promotion programs could directly prevent 1.3 million child deaths each year and that breast-feeding promotion and support is one of the most feasible child survival interventions to implement (3).
Although it has been known since the mid-1980s that HIV can be transmitted through breast milk, the public health community remains divided about how to address this issue in developing countries. Initially, in statements issued in 1987 and 1992, the United Nations agencies continued to recommend breast-feeding for all infants of HIV-positive mothers living in resource-poor countries, believing that the benefits of breast-feeding outweighed the risk of HIV transmission in all areas where infectious disease was the leading cause of infant death (4,5).
In June 1998, growing evidence about the risk of HIV transmission through breast-feeding culminated in revised recommendations urging countries to make counseling and HIV-testing accessible to antenatal women and stating that women should be "empowered to make fully informed decisions about infant feeding" and "suitably supported in carrying them out" (6). Later, in 2001, international guidelines were further modified to state that "when replacement feeding is acceptable, feasible, affordable, sustainable, and safe, avoidance of all breastfeeding by HIV-infected mothers is recommended" (7).
Programmatically, these recommendations challenge health care services to move from a general message that can be delivered to all women unequivocally promoting exclusive breast-feeding (EBF)5 to the need for individualized counseling, wherein HIV test results and infant feeding options are discussed, and an array of risks, benefits, costs, and psychological factors are weighed with each HIV-positive mother.
In addition to helping HIV-positive mothers decide whether to breast-feed at all, counseling must also address ways in which the risk of breast-feedingassociated transmission can be reduced. Two reports published in 1999 suggested that the HIV-risk imposed by breast-feeding might be modifiable. In South Africa, Coutsoudis and colleagues (8) observed a 48% reduction in HIV transmission by 3 mo among mothers who breast-fed exclusively (feeding breast milk only and no other milks, liquids, or solid foods) when compared with transmission risks by mothers who practiced early mixed feeding (feeding breast milk plus other solids, milks, or liquid foods). In Malawi, subclinical mastitis was associated with higher breast milk viral loads and transmission (9), suggesting that good lactation management to minimize engorgement, mastitis, and nipple disease may reduce transmission. This concept, that breast-feeding could be made safer, is particularly promising for women and infants living in settings where clean water is unavailable, where replacement feeding is unaffordable, and where many HIV-positive women are choosing to breast-feed even knowing the risks.
We developed an education and counseling program to inform and to support new mothers about infant feeding in the context of HIV. We evaluated the programs impact on maternal knowledge, feeding practices, and postnatal HIV transmission. The work was done within the ZVITAMBO trial, a randomized clinical trial testing the impact of postpartum vitamin A supplementation on several health outcomes. ZVITAMBO enrolled 14,110 motherinfant pairs from November 1997 through January 2000, covering the time period when the 1998 HIV and infant-feeding guidance was issued, but before the introduction of antenatal HIV counseling and testing in Harare.
This paper describes the steps taken to develop the intervention and its impact on maternal knowledge, timely receipt of HIV test results, and infant-feeding practices. The impact of the program on postnatal HIV transmission and HIV-free survival will be reported elsewhere.
| METHODS |
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The ZVITAMBO trial has been described previously (10). Briefly, motherbaby pairs were enrolled, following written consent, within 96 h of delivery at one of 14 maternity clinics in greater Harare, being eligible if neither had an acutely life-threatening condition, the baby was a singleton with birth weight > 1500 g, and the mother planned to stay in Harare after delivery. Written informed consent included permission to test mothers for HIV. Mothers could learn their results at any time during the study with appropriate pre- and post-test counseling, but they were not required to do so. This feature makes ZVITAMBO unique. All other studies of infant feeding and HIV have been conducted among mothers who knew their HIV status.
Socioeconomic, demographic, breast-feeding initiation, and prelacteal feeding data were collected by interview at enrollment. Details of the pregnancy and the delivery were transcribed from hospital records. At delivery, 32% of the mothers were HIV positive (10). Follow-up visits at 6 wk, 3 mo, and at 3-mo intervals for up to 24 mo included maternal and infant blood collection. Detailed infant feeding information, including breast-feeding status and whether or not any of 22 nonmilk liquids, nonhuman milks (animal milks and commercial formula), medicines (traditional fluids, oral rehydration salts, other prescribed), or solid foods had ever been given to the infant were collected at enrollment, 6 wk, 3 mo, and 6 mo after delivery.
Infants who provided infant-feeding information at enrollment, 6 wk, and 3 mo were classified into 1 of 3 early breast-feeding patterns: 1) EBFonly breast milk, vitamins, or prescribed medicines at all 3 time points, or at 2 of 3 time points. One lapse in exclusivity of EBF at 1 of the 3 time points was allowed only if the nonbreast milk item consumed was a nonmilk liquid; 2) predominant breast-feedingbreast milk plus nonmilk liquids; 3) mixed breast-feedingbreast milk plus nonhuman milks and/or solid foods at one or more time points. Classification was limited to the first 3 mo, because 93% of study infants were mixed breast-feeding by 6 mo.
Psychosocial counseling was available throughout the study. The date and reason for each individual counseling session, and whether HIV test results were obtained, was documented.
Formative research to design the education and counseling program
The first public-sector HIV-testing facility in Zimbabwe opened in March 1999. Before this, very few antenatal women or any other Zimbabweans had the opportunity to know their HIV status, other than women participating in our trial. Hence, there was little experience to inform us about how to implement new HIV infant-feeding guidance, or how mothers and their families would respond. To address this gap, we carried out a formative research study from April to July 1999 to help us to design a locally appropriate education and counseling intervention.
Focus groups were used to assess knowledge, beliefs, and attitudes in the community about mother-to-child transmission (MTCT) of HIV, breast-feeding and replacement feeding, and HIV testing and status disclosure. A purposeful sample of 48 fathers, 53 lactating women, and 47 pregnant women participated in one of 24 discussions (8 for each type of person). In-depth interviews were conducted with postpartum women participating in the ZVITAMBO trial to learn how they had made the decisions of whether to receive and to disclose their HIV results and how to feed their baby. Eleven women who knew they were HIV positive and 7 women who knew they were HIV negative were enrolled on a rolling basis as they came for post-test counseling; an additional 19 women who chose not to know their HIV status were selected, matched to the HIV status-known women on infant age and family income.
All discussions and interviews were conducted in Shona by 1 of 4 trained interviewers using field guides, and were tape recorded, transcribed, and translated. Participants provided written informed consent.
Formative research analysis
Textual data were read to identify recurrent patterns, and summaries were written about each case. Codes were created and assigned to text so that it could be systematically searched (11). Data were computerized and analyzed using the software NUDIST (12).
Formative research: key findings
The majority of respondents believed that all babies of HIV-positive mothers would become HIV infected and that there was nothing that could be done to prevent transmission. Few Zimbabweans can afford replacement feeding, and it was felt that mothers who do not breast-feed may face negative social consequences. People may believe that she is a witch, stole the child, has a bad omen or spirit, has been promiscuous so that this child is not her husbands, or that she is HIV positive. Some people held the misconception that mixed feeding is a good way to reduce the risk of HIV transmission, because smaller volumes of infected milk are consumed. Both wives and husbands agreed that husbands have the final say in whether and how long their babies are breast-fed.
Learning ones HIV test results was perceived as an extremely negative and fearful experience. Mothers who tested for HIV before their husbands were tested were worried that they would be accused of bringing HIV into the home. Understanding that maternal HIV seroconversion during breast-feeding places babies at especially high risk of breast-feedingassociated transmission was the key point that helped married men to understand their role in MTCT and to accept responsibility to be tested and to take preventive measures. Married men wanted to be informed about MTCT issues directly rather than through their wives so they could assume a leadership role in the discussion. Wives wanted to be relieved of the responsibility of informing their husbands.
Development of the education and counseling program
The education and counseling program ("the intervention") was developed from June to August, 1999 and included the following components.
Antenatal education. Basic information about infant feeding in the context of HIV was incorporated into education sessions held for women receiving antenatal care at ZVITAMBO recruitment sites. Key messages included these facts: only some (not all) babies of HIV-positive mothers become infected themselves, breast-feeding is a major mode of HIV transmission and the risk is particularly high for mothers who seroconvert during breast-feeding, and making an informed choice about infant feeding is one reason to learn ones HIV status.
Male outreach and education. Information on MTCT, including infant feeding, was incorporated into ongoing male education programs in Harare, including work-place outreach.
Infant feeding options for HIV-positive mothers. Infant feeding was integrated into HIV counseling for ZVITAMBO women who chose to learn their HIV status. Post-test counseling of HIV-positive women included a full discussion of the risks, benefits, and costs of 4 feeding options: 1)"safer breastfeeding," consisting of 4 practices (EBF to 6 mo; proper infant positioning and attachment to the breast to minimize breast pathology; seeking medical care quickly for breast problems; and practicing safe sex, especially during the breast-feeding period); 2) heat-treated expressed breast milk; 3) replacement feeding with commercial formula; 4) replacement feeding with homemade formula. HIV-positive mothers were counseled to stop breast-feeding rapidly at 6 mo and to then feed their infants using locally available foods.
Infant feeding options for other mothers. HIV-negative mothers and mothers who chose not to learn their HIV status were educated in "safer breast-feeding." Educational materials were developed, including 2 videos, 3 pamphlets, counseling tools describing the costs, advantages and disadvantages of each feeding option for HIV-positive women, and take-home fact sheets providing step-by-step instructions for implementing each feeding option safely.
Implementation of the intervention
Over a 2-mo period, beginning September 1, 1999, 12 HIV counselors and >50 health educators, all employed by the study, were trained on MTCT and infant feeding, and on how to use the education and counseling materials. The program was considered to be partially operational during the 2-mo period when training was taking place. By November 1, all staff had been trained, and educational materials were available for individual counseling and group education sessions. Thus, women enrolled in ZVITAMBO before September 1, 1999, September 1, 1999 to October 31, 1999, and November 1, 1999 to January 31, 2000, were classified as the "pre-," "partial-," and "full-" enrollment cohorts with respect to the intervention.
Evaluation of the intervention
A questionnaire was administered to 1996 women in the "partial" and "full" cohorts to ascertain sources of information and knowledge about 16 issues regarding HIV, MTCT, risk factors, and ways to reduce breast-feedingassociated transmission. Recall of exposure to any of the 7 educational materials used in the program (3 brochures, 2 videos, group education, individual counseling) at any of 4 time points (antenatal, delivery, 6 wk postpartum, and other times) was also measured. The impact of the intervention on maternal knowledge was compared according to the number of reported exposures to the program, timing of exposure, and whether or not individualized counseling and/or group education was received. The impact of the intervention on early infant-feeding practices and the decision to learn ones HIV status was evaluated by comparing these behaviors between enrollment cohorts (pre, partial, and full) for the total study population and then, among mothers completing the knowledge/exposure (KE) questionnaire, according to the timing, type, and number of reported exposures to the program.
Analysis methods
Statistical analysis was conducted using SAS Version 8.1 (13). Baseline characteristics were compared for mothers in the pre, partial, and full cohorts using ANOVA and chi-square tests for continuous and categorical variables, respectively. Mothers exposure to the intervention was quantified by summing the total number of reported contacts with the 7 ZVITAMBO educational materials at the 4 time points, for a total of 28 possible exposures. Logistic regression models were used to investigate the effect of exposure to the intervention on knowledge of HIV/AIDS and infant feeding, decisions about HIV testing, and on EBF for at least 3 mo. Models were constructed with and without adjusting for other explanatory variables. Independent factors were retained in the multivariate logistic regression models at the
= 0.05 level.
| RESULTS |
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Impact of the intervention on knowledge
Among women who reported no exposure to the intervention, about half were able to distinguish between HIV and AIDS, and most knew that a healthy-looking person can be HIV positive, but few could name risk factors for postnatal transmission or could cite ways to reduce this risk (Table 2). Exposure to the intervention was a significant determinant of knowledge for 13 of the 16 HIV facts that were measured. The likelihood of knowing these 13 facts rose significantly, by 10% to 39%, with each additional exposure to the intervention, after adjusting for maternal education, parity, timing of the interview, and knowledge of HIV status at the time of the interview. Most of this impact was due to receiving group education (data not shown). Exposure at antenatal care, delivery, and 6-wk postpartum were significantly associated with knowing 11, 10, and 9 of the 16 HIV facts, respectively, after adjusting for maternal characteristics and exposure at the other time points, indicating that all time points were effective teaching times (data not shown).
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Among all the women enrolled in ZVITAMBO, only 2182 mothers (15.5%) chose to learn their HIV status at any time during the study. Thus, the educational intervention on safer breast-feeding for women of unknown HIV status was one of the most important aspects of the program. Of those who learned their status, 1022 (46.8%) learned in the first 3 mo (13 wk) after delivery. Early acquisition of test results is important, because it allows mothers the opportunity to make informed decisions about breast-feeding and HIV prevention practices. In final logistic regression models, mothers in the full-intervention cohort were 70% more likely to learn their HIV status in the first 3 mo than mothers in the preintervention cohort, after adjusting for other significant covariates (Table 3).
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Complete data on early feeding patterns were available for 8591 infants. The EBF rate increased and the mixed breast-feeding rate decreased among women enrolled in the full intervention compared with the preintervention cohorts (Fig. 1). Predominant breast-feeding rates were similar across enrollment cohorts. The adjusted odds ratio for EBF was 8.43 among women exposed to the full intervention (Table 3). Learning ones HIV status before 3 mo was associated with a relatively small (28%) increase in the likelihood of EBF and was not retained in the final model.
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| DISCUSSION |
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The education and counseling program was effective in improving knowledge about MTCT of HIV, risk factors for HIV transmission during breast-feeding, and ways to prevent breast-feedingassociated HIV transmission. The intervention also increased the likelihood that a mother would learn her HIV status early in the postnatal period and that she would breast-feed exclusively for at least 3 mo, a practice that was associated with a 50% reduction in postnatal HIV transmission in this study population (14). The decision to breast-feed exclusively was independent of knowledge of HIV status in this study. The impact of our program on HIV transmission by mothers of known and unknown HIV status is now being analyzed.
In spite of the significant positive impact of exposure to the program, the proportion of mothers in the full-intervention cohort who followed our recommendations was still disappointingly low, leaving much room for improvement: only 7.1% learned their HIV status before 3 mo and only 24.6% breast-fed exclusively for at least 3 mo. In the future, to achieve greater compliance, efforts to sensitize communities about HIV and infant feeding should combine group education with individualized counseling, reaching women (and their partners) frequently during the antenatal and postnatal periods. Group education should cover basic facts about HIV and infant feeding, including safer breast-feeding practices. Individualized counseling is needed to help all mothers safely implement feeding decisions.
| FOOTNOTES |
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2 The ZVITAMBO project was supported by the Canadian International Development Agency (CIDA) (R/C Project 690/M3688), United States Agency for International Development (USAID) (cooperative agreement number HRN-A-0097-0001500 between Johns Hopkins University and USAIDs Office of Health and Nutrition), and a grant from the Bill and Melinda Gates Foundation, Seattle, WA, with supplemental funding from the Rockefeller Foundation (New York City, NY) and BASF (Ludwigshafen, Germany). Additional funding for the infant feeding work was provided by the Support for Analysis and Research in Africa (SARA) and LINKAGES Projects, operated by the Academy for Educational Development, Washington, DC. The SARA Project is funded by USAIDs Bureau for Africa, Office of Sustainable Development under the terms of Contract AOT-C-0099-0023700. The LINKAGES Project is funded by USAIDs Bureau for Global Health, GH/HIDN, under Cooperative Agreement No. HRN-A-0097-00000700. ![]()
4 Members of the ZVITAMBO Study Group, in addition to the named authors are: Henry Chidawanyika, Agnes Mahomva, Florence Majo, Michael Mbizvo, Lawrence Moulton, Kuda Mutasa, Mary Ndhlovu, Lidia Propper, Philipa Rambanepasi, Andrea Ruff, Lynn Zijenah, and Partson Zvandasara. ![]()
5 Abbreviations used: EBF, exclusive breast-feeding; KE, knowledge/exposure; MTCT, mother-to-child transmission of HIV. ![]()
| LITERATURE CITED |
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1. Joint United Nations Programme on HIV/AIDS (UNAIDS) (2004) 2004 report on the global HIV/AIDS epidemic: 4th global report 2004 UNAIDS Geneva, Switzerland .
2. The Breastfeeding and HIV International Transmission Study Group (2004) Late postnatal transmission of HIV-1 in breast-fed children: an individual patient data meta-analysis. J. Infect. Dis. 189:2154-2166.[Medline]
3. Jones, G., Steketee, R. W., Black, R. E., Bhutta, Z. A. & Morris, S. S., the Bellagio Child Survival Study Group (2003) How many child deaths can we prevent this year?. Lancet 362:65-71.[Medline]
4. WHO Special Program on AIDS (1987) Special Programme on AIDS Statement: Breast-Feeding/Breast Milk and Human Immunodeficiency Virus [Online]. WHO/SPA/INF/87.8. WHO, Geneva, Switzerland. http://whqlibdoc.who.int/hq/1987/WHO_SPA_INF_87.8.pdf [accessed July 15, 2004].
5. WHO Global Programme on AIDS (1992) Consensus Statement from the WHO/UNICEF Consultation on HIV Transmission and Breast-Feeding. Geneva, April 30 to May 1, 1992 [Online]. Report No. WHO/GPA/INF/92.1. WHO, Geneva, Switzerland. http://whqlibdoc.who.int/hq/1992/WHO_GPA_INF_92.1.pdf [accessed July 15, 2004].
6. UNAIDS/UNICEF/WHO (1998) HIV and Infant Feeding: Guidelines for Decision-Makers. WHO/FRH/NUT/CHD/98.1.WHO/UNAIDS 1998 WHO Geneva, Switzerland.
7. WHO (2001) New Data on the Prevention of Mother-to-Child Transmission of HIV and Their Policy Implications: Conclusions, and Implications. WHO Technical Consultation on Behalf of the UNFPA/UNICEF/WHO/UNAIDS Inter-Agency Task Team on Mother-to-Child Transmission of HIV, Geneva, October 1113, 2000 [Online]. Report No. WHO/RHR/01.28. Geneva, Switzerland. http://www.unaids.org/NetTools/Misc/DocInfo.aspx?LANG=en&href=http%3a%2f%2fgva-doc-owl%2fWEBcontent%2fDocuments%2fpub%2fPublications%2fIRC-pub05%2fMTCT_Consultation_Report_en%26%2346%3bdoc [accessed July 15, 2004].
8. Coutsoudis, A., Pillay, K, Spooner, E., Kuhn, L. & Coovadia, H. M., the South African Vitamin A Study Group (1999) Influence of infant-feeding patterns on early mother-to-child transmission of HIV-1 in Durban, South Africa: a prospective cohort study. Lancet 354:471-476.[Medline]
9. Semba, R. D., Kumwenda, N., Hoover, D. R., Taha, T. E., Quinn, T. C., Mtimavalye, L., Biggar, R. J., Broadhead, R. & Miotti, P. G., et al (1999) Human immunodeficiency virus load in breast milk, mastitis, and mother-to-child transmission of human immunodeficiency virus type 1. J. Infect. Dis. 180:93-98.[Medline]
10. Malaba, L. C., Iliff, P. J., Nathoo, K. J., Marinda, E., Moulton, L. H., Zijenah, L. S., Zvandasara, P., Ward, B. J., the ZVITAMBO Study Group and Humphrey & , J. H. (2005) Impact of post-partum maternal or neonatal vitamin A supplementation on infant mortality among infants born to HIV-negative mothers in Zimbabwe. Am. J. Clin. Nutr. 81:454-460.
11. Miles, M. B. & Huberman, A. M. (1994) Qualitative Data Analysis 2nd ed. 1994 Sage Publications Thousand Oaks, CA.
12. QSR (2000) QSR NUDIST4 VIVO Version 1.1 2000 QSR Melbourne, Australia.
13. SAS Institute Inc. (2002) SAS Version 8.1 2002 SAS Institute Cary, NC.
14. Iliff, P. J., Piwoz, E. G., Tavengwa, N. V., Zunguza, C. D., Marinda, E. T., Nathoo, K. J., Moulton, L. H., Ward, B. J., ZVITAMBO Study Group & Humphrey, J. H. (2004) Early exclusive breastfeeding reduces the risk of postnatal HIV-1 transmission and increases HIV-free survival. AIDS (in press).
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