Epidemiology and Social
Early exclusive breastfeeding reduces the risk of postnatal HIV-1 transmission and increases HIV-free survival
Iliff, Peter Ja; Piwoz, Ellen Gb; Tavengwa, Naume Va; Zunguza, Clare Dc; Marinda, Edmore Ta; Nathoo, Kusum Jd; Moulton, Lawrence He; Ward, Brian Jf; the ZVITAMBO study group; Humphrey, Jean Ha,e
From the aZVITAMBO Project, Borrowdale, Harare, Zimbabwe
bThe SARA Project, Academy for Educational Development, Washington, DC, USA
cThe Harare City Health Department, Harare, Zimbabwe
dThe University of Zimbabwe College of Health Sciences, Harare, Zimbabwe
eThe Johns Hopkins Bloomberg School of Public Health, Department of International Health, Baltimore, MD, USA
fThe Research Institute of the McGill University Health Center, Montreal, Quebec, Canada.
Received 18 May, 2004
Revised 4 November, 2004
Accepted 18 January, 2005
Correspondence and reprint requests to Jean Humphrey, ZVITAMBO Project, 1 Borrowdale Road, Borrowdale, Harare, Zimbabwe. E-mail: firstname.lastname@example.org
Objectives: The promotion of exclusive breastfeeding (EBF) to reduce the postnatal transmission (PNT) of HIV is based on limited data. In the context of a trial of postpartum vitamin A supplementation, we provided education and counseling about infant feeding and HIV, prospectively collected information on infant feeding practices, and measured associated infant infections and deaths.
Design and methods: A total of 14 110 mother–newborn pairs were enrolled, randomly assigned to vitamin A treatment group after delivery, and followed for 2 years. At baseline, 6 weeks and 3 months, mothers were asked whether they were still breastfeeding, and whether any of 22 liquids or foods had been given to the infant. Breastfed infants were classified as exclusive, predominant, or mixed breastfed.
Results: A total of 4495 mothers tested HIV positive at baseline; 2060 of their babies were alive, polymerase chain reaction negative at 6 weeks, and provided complete feeding information. All infants initiated breastfeeding. Overall PNT (defined by a positive HIV test after the 6-week negative test) was 12.1%, 68.2% of which occurred after 6 months. Compared with EBF, early mixed breastfeeding was associated with a 4.03 (95% CI 0.98, 16.61), 3.79 (95% CI 1.40–10.29), and 2.60 (95% CI 1.21–5.55) greater risk of PNT at 6, 12, and 18 months, respectively. Predominant breastfeeding was associated with a 2.63 (95% CI 0.59–11.67), 2.69 (95% CI 0.95–7.63) and 1.61 (95% CI 0.72–3.64) trend towards greater PNT risk at 6, 12, and 18 months, compared with EBF.
Conclusion: EBF may substantially reduce breastfeeding-associated HIV transmission.
Each year, 700 000 infants acquire HIV infection from their mothers . A total of 280 000 of the infants become infected through breastfeeding, about 40% of total mother-to-child transmission.
Programmes to prevent mother-to-child transmission are expanding rapidly, particularly in southern Africa, where up to 40% of antenatal women are infected . These programmes typically provide HIV counseling and testing, antiretroviral prophylaxis, and infant feeding counseling. However, infant feeding counseling is difficult to implement for reasons that include limited data on the risks associated with different feeding practices, limited follow-up after delivery, and stigma associated with replacement feeding and exclusive breastfeeding (EBF).
International guidance currently states that when replacement feeding is acceptable, feasible, affordable, sustainable and safe, the avoidance of all breastfeeding by HIV-infected mothers is recommended . Otherwise, EBF is recommended during the first months of life. In Africa, replacement feeding that is acceptable, feasible, affordable, sustainable and safe is uncommon, and many HIV-positive women are choosing to breastfeed [4,5]. Finding ways to make breastfeeding safer for HIV-positive women living in resource-limited settings is an urgent priority [6,7].
Exclusive breastfeeding is recommended because it protects infants from morbidity and mortality whether or not HIV related [8–10]. In addition, Coutsoudis and colleagues  reported that HIV-exposed infants who were breastfed exclusively for at least 3 months had a lower risk of HIV infection than mixed-fed infants.
This report confirms the observations of Coutsoudis and colleagues , and provides additional data distinguishing the magnitude of risk of HIV transmission or death associated with different breastfeeding patterns.
Study participants and methods
The data were collected as part of the ZVITAMBO trial, designed to measure the impact of single-dose postpartum vitamin A supplementation on several maternal and neonatal health outcomes . A secondary objective was to investigate the role of infant feeding practices in breastfeeding-associated HIV transmission. From 25 November 1997 to 29 January 2000, 14 110 postpartum mothers and their neonates were randomly assigned to one of four vitamin A treatment groups within 96 h of delivery [mean (SD) = 19 (16) h post-delivery] at one of 14 maternity clinics and hospitals in the greater Harare area in Zimbabwe.
Mother–baby pairs were eligible if neither had an acutely life-threatening condition, if the baby was a singleton with a birth weight of 1500 g or greater, and if the mother planned to stay in Harare after delivery. Written informed consent, including permission for HIV testing, was obtained from the mother. Mothers could receive their HIV test results at any time during the trial. Receiving HIV test results was encouraged but not required for joining the study because women may have understandable reasons not to know their status, and we believed that this should not exclude them from participating in a trial that might benefit them and their babies.
Socioeconomic and demographic data were collected by interview. Obstetric details were transcribed from hospital records. Gestational age was estimated using the Capurro method . Infant birth weight and maternal mid-upper arm circumference (MUAC) were measured using methods described by Gibson . Whole blood was collected from mothers and babies and processed within 2 h. Maternal plasma and infant plasma and cell pellets [Amplicor whole blood polymerase chain reaction (PCR) sample preparation method; Roche Diagnostics Systems, Alameda, CA, USA] were prepared and stored at −70 °C until analysis.
UNICEF conducted a pilot mother-to-child transmission prevention programme in two Harare antenatal clinics during a period that overlapped by 8 months with ZVITAMBO recruitment. During those months, 69 HIV-positive antenatal women received zidovudine, but none of them joined ZVITAMBO after delivery. Antenatal HIV testing and antiretroviral prophylaxis was not available in any other Harare public sector facility during our recruitment.
Education and counseling about infant feeding in the context of HIV
When the trial began, information about HIV transmission through breastfeeding was scant. In June 1998, new infant feeding guidelines were published by UNAIDS/UNICEF/WHO stating that HIV-positive mothers should be fully informed about the risks and benefits of infant feeding alternatives and empowered to make their best personal choice . In response, we modified our procedures to provide a 24-h turnaround time for HIV test results. Study nurses were trained to counsel HIV-positive women about feeding options, and kitchens were established for teaching safe replacement feeding. Additional funding was obtained to conduct formative research to inform a more effective programme to educate mothers about infant feeding in the context of HIV. This programme  was fully implemented within the trial by 1 November 1999. The programme emphasized EBF for HIV-positive mothers who chose to breastfeed, optimal breastfeeding techniques to avoid cracked nipples, milk stasis, and mastitis, the prompt treatment of breast problems, and safe sex practices especially during the breastfeeding period. These four ‘safer breastfeeding’ practices were also promoted among all status-unknown and HIV-negative women. Known HIV-positive women were counseled to stop breastfeeding early.
Follow-up of subjects
Follow-up visits at 6 weeks, 3 months, and 3-monthly intervals for up to 24 months included maternal and infant blood collection following the same protocol used at recruitment. Free clinical care included the treatment of acute infections with appropriate antimicrobial drugs, referral to government treatment facilities for suspect tuberculosis, counseling and antibiotic treatment for mastitis, and oral rehydration solution education for diarrhea. HIV-related and psychosocial counseling was available throughout the study.
Maternal HIV, CD4 cell count, and hemoglobin testing
Mothers were tested for HIV at baseline by two enzyme-linked immunosorbent assays (ELISA) run in parallel (HIV 1.0.2 ICE; Murex Diagnostics, Edenvale, South Africa, and GeneScreen HIV 1/2; Sanofi Diagnostics Pasteur, Johannesburg, South Africa). Discordant ELISA results were resolved by Western Blot assay (HIV Blot 2.2; Genelabs Diagnostics SA, Geneva, Switzerland), interpreted according to the manufacturer's guidelines. Quality control was monitored by the use of kit controls, the inclusion of an internal quality control sample on every plate, and participation in the quality control programme for HIV testing of the Zimbabwe Ministry of Health.
Maternal CD4 cells were enumerated using a Facscount (Becton Dickinson International, Erembodegem, Belgium) within 48 h of phlebotomy. Quality control was monitored by the inclusion of kit controls and two additional reference samples (high and low) provided by the Research Institute of the McGill University Health Center with every batch.
Hemoglobin was measured at baseline for women enrolled after 1 October 1998 (approximately 60% of the total sample) using a hemoglobinometer (HemoCue, Mission Viejo, CA, USA) on the day of collection.
Infant HIV testing
After all patient contact was completed, the last available specimen was tested [plasma by GeneScreen ELISA for samples collected at ≥ 18 months, or cell pellets by prototype Roche Amplicor version 1.5 qualitative PCR assay (Roche Diagnostic Systems) for samples collected at < 18 months]. If the last available sample was HIV negative, the baby was classified as uninfected and no further testing was carried out. If the last sample was positive, the 3-month pellet was tested. If this sample was positive, the baseline and 6-week samples were tested. If these samples were negative, sequential samples moving forward through time were tested until two consecutive samples tested positive.
Infant feeding practices
Breastfeeding initiation and pre-lacteal feeding information was collected at baseline. At 6 weeks, 3 months, and 6 months, detailed feeding information was collected, including whether or not any of 22 liquids (water, juice, tea, cooking oil), milks (formula, fresh, tinned), medicines (traditional, oral rehydration solution, prescribed), or solid foods (porridge, sadza, fruits, vegetables, meat, eggs) had ever been given to the infant.
The analysis reported here is based on data from mothers who were HIV positive at delivery, whose babies were alive and PCR-negative for HIV at 6 weeks, and who provided infant feeding data at birth, 6 weeks, and 3 months. Infants’ breastfeeding patterns up to 3 months were classified using or adapting WHO definitions  as follows:
Exclusive breastfeeding (EBF) – the infant consumed only breast milk and no other liquids, milks or solid foods except vitamins or prescribed medicines, according to mothers’ reports at all three timepoints, or at two of three timepoints. One lapse in the exclusivity of EBF at one of the three timepoints was allowed only if the non-breast milk item consumed was a non-milk liquid. Allowing one lapse in the definition of EBF is consistent with other studies (A. Coutsoudis, N. Rollins, personal communications).
Predominant breastfeeding (PBF) – the infant's predominant source of nourishment was breast milk, but non-milk liquids (e.g. water, tea, juice, cooking oil) were also consumed according to mothers’ reports at all three timepoints, or at two of three timepoints. One lapse in PBF was allowed only if the mother reported EBF for the lapsed time period.
Mixed breastfeeding (MBF) – the infant consumed breast milk and either non-human milks, such as infant formula or cows’ milk, or solid or semisolid foods or both, according to mothers’ reports at one or more timepoints.
Statistical analysis was conducted using SAS Version 8.2 (Cary, NC, USA). Characteristics associated with early feeding practices were examined using chi-square and one-way analysis of variance for categorical and continuous variables, respectively. Turnbull methods  (using 2000 ‘bootstraps’ to calculate confidence intervals ) were used to estimate postnatal transmission (PNT) in infants who were PCR negative at their 6-week visit (42 days). This reflects HIV infection that is unequivocally attributable to breastfeeding , and is hereafter referred to as postnatal HIV transmission (PNT). Infants who never had a positive HIV test were censored at the age of their last negative test result. Infants of mothers who died or stopped breastfeeding were censored 60 days after the mother's date of death or breastfeeding cessation, respectively . PNT risks at 6, 12 and 18 months were calculated for each of the three feeding groups, and pairwise comparisons were made between the feeding groups at the same timepoints. Survival rates to 18 months were estimated using Kaplan–Meier methods.
Cox proportional hazards models were used to investigate the effect of the early breastfeeding pattern on PNT or PNT plus death, with and without adjusting for other explanatory variables, including maternal and neonatal vitamin A supplementation, household income, maternal baseline CD4 cell count, MUAC, hemoglobin, marital status, age, education, and death during the follow-up period, reported or diagnosed breast pathology (mastitis, cracked nipples), infant gestational age and birth weight, and a breastfeeding ‘propensity score’ that was developed using methods described by Joffe and Rosenbaum .
Briefly, the propensity scores were calculated using multinomial logistic regression with feeding pattern as the outcome and EBF as the reference category. Socioeconomic, obstetric, and maternal and neonatal health variables were fit in the model. The propensity score was included in models to correct for baseline imbalances between feeding groups, because infants were not randomly assigned to specific breastfeeding practices.
The CD4 cell count and hemoglobin were analysed as categorical variables (< 200, 200–349, 350–499, ≥ 500, and ‘missing’) and (< 70, ≥ 70, and ‘missing’), respectively. Cox models were also used to investigate the potential effect modification of early feeding practices by maternal baseline CD4 cell count. Independent factors were retained in the multivariate models at the α = 0.10 level; interaction terms were retained at the 0.15 level.
The Medical Research Council of Zimbabwe, the Medicines Control Authority of Zimbabwe, the Johns Hopkins Bloomberg School of Public Health Committee on Human Research, and the Montreal General Hospital Research Ethics Committee approved the study protocol.
A total of 4495 mothers (31.9%) were HIV positive at enrolment (Fig. 1). One hundred and twenty-eight infants (2.8%) born to HIV-positive mothers provided no additional follow-up data. Among the remaining infants born to HIV-positive mothers, 918 tested PCR positive at baseline or 6 weeks, including 16 infants who died before their 6-week visit. An additional 64 infants were HIV negative at birth and died before their 6-week visit, and 515 infants were alive but missing PCR status at 6 weeks. Among the remaining 2870 infants, 810 were missing feeding data at one (n = 578), two (n = 231), or all three (n = 1) timepoints. The remaining 2060 infants were included in this analysis. Compared with the 810 excluded infants, those included in the analysis had significantly higher [mean (SD)] birth weights [2960 g (45) versus 2890 g (44), P = 0.001] and MUAC [25.8 cm (2.9) versus 25.4 cm (3.0)], but were similar in all other baseline characteristics.
Breastfeeding duration was prolonged: 99.1, 94.0, and 59.1% of mothers were still breastfeeding at 6, 12, and 18 months, respectively. However, only 156 babies (7.6%) were EBF for at least 3 months, compared with 490 (23.8%) and 1414 (68.6%) infants who were PBF and MBF, respectively, to at least 3 months (Table 1). A total of 93.2% of infants were MBF by 6 months. EBF mothers were slightly older and more likely to be unemployed. EBF infants also tended to have higher absolute birth weights (P = 0.08) but were no less likely to be low birth weight (< 2500 g) than other infants. As reported previously , the single strongest prognostic factor for EBF was enrolment in the trial after the full implementation of the education and counseling programme.
Between 6 weeks and 18 months, 199 infants became HIV infected (8, 35, and 156 in the EBF, PBF, and MBF groups, respectively) and an additional 48 infants died with their last PCR test being negative (2, 13, and 33 in the EBF, PBF, and MBF groups, respectively), totaling 247 postnatal HIV infection or death events. The total number of deaths (with or without infection) was 3, 16, and 52 in the EBF, PBF, and MBF groups, respectively. Kaplan–Meier estimates of mortality at 18 months (death with or without HIV infection) were 1.96% [95% confidence interval (CI) 0.64–5.95], 3.57% (95% CI 2.19–5.81) and 4.17% (95% CI 3.18–5.47) for the EBF, PBF, and MBF groups, respectively.
Postnatal transmission at 6, 12, and 18 months was 3.9% (95% CI 3.0–4.7), 7.7% (95% CI 6.6–9.3), and 12.1% (95% CI 10.5–14.0), respectively. A total of 68.2% of all PNT occurred after 6 months. Compared with EBF babies, MBF babies had a significantly greater PNT risk, and PBF babies tended to have a higher risk (not statistically significant) (Fig. 2 and Table 2). PNT rates were 5.1, 6.7, and 10.5 per 100 child-years of breastfeeding for EBF, PBF, and MBF, respectively. The overall PNT rate was 9.2 per 100 child-years of breastfeeding, comparable to a meta-analysis rate of 8.9 per 100 child-years of breastfeeding in nine other studies in Africa .
The final Cox proportional hazard ratios for the risk of PNT at 6, 12, and 18 months are shown in Table 3, and the results for HIV infection plus death are found in Table 4. The maternal CD4 cell count was an important predictor of PNT. In mothers with CD4 cell counts less than 200 cells/μl (n = 216), PNT was 33.7% (95% CI 22.9–44.1).
Maternal nutritional status was positively associated with infant outcomes. Each additional centimetre of maternal MUAC was associated with a 6–12% reduction in PNT (Table 3). Severe maternal anemia at baseline (hemoglobin < 70 g/l) was a significant positive predictor of PNT, with the greatest risk in the first 6 months (adjusted hazards ratio 6.93; 95% CI 2.39–20.10). Findings were similar in models when HIV infection plus death was the outcome (Table 4).
In the final models, MBF was associated with a fourfold increase in PNT and a threefold increase in the risk of PNT plus death at 6 months, compared with EBF. The protective effects of early EBF declined over time, but the risks posed by early MBF were still observed at 18 months (P < 0.008). Compared with EBF, early PBF was associated with a 2.6-fold and 1.6-fold increased risk of PNT, and a 2.4-fold and 1.7-fold increased risk of PNT plus death at 6 and 18 months, respectively, but these differences were not statistically significant. When the propensity score was included in the models, it was not significant (P > 0.69) and did not substantially change the hazard ratios associated with different feeding methods (data not shown). Interactions between early breastfeeding patterns and maternal CD4 cell count were not significant. However when the analysis was restricted to mothers with baseline CD4 cell counts less than 500 cells/μl, the adjusted hazard ratio for postnatal HIV transmission at 18 months for MBF compared with EBF was 3.19 (95% CI 1.30–7.82), suggesting that the protective effects of EBF may have been even greater among the women in whom PNT risks were highest. Vitamin A supplementation was not associated with the risk of PNT or PNT plus death at any time point (Table 3 and Table 4), as reported elsewhere .
The findings of this study have three specific programmatic implications. First, the introduction before the age of 3 months of solid foods or animal milks to breastfeeding infants born to HIV-positive mothers was associated with a fourfold greater risk of PNT at 6 months compared with EBF. The protective effects of early EBF were still significant at 18 months post-delivery, with a 61% reduction in PNT compared with MBF. The risk of PBF over EBF varied from 1.6 to 2.7 over the 18-month period, reaching statistical significance at 12 months only. These findings indicate that the early introduction of non-human milks and solid foods conveys an especially high risk, but that even non-milk liquids are likely to increase the risk. Therefore, the more strictly HIV-positive mothers are able to breastfeed exclusively, the lower the risks of HIV or death will be for their infants.
Second, consistent with studies in west Africa , South Africa , and Tanzania , more than two-thirds of all PNT occurred after 6 months. Together, such studies provided strong justification for supporting early breastfeeding cessation among HIV-positive women. This can only be done, however, when women are socially supported to do so, and when safe nutritionally adequate alternatives are available.
Third, women with CD4 cell counts less than 200 cells/μl were five times more likely to transmit HIV during breastfeeding compared with women with CD4 cell counts over 500 cells/μl, confirming the findings of other studies that PNT is highly correlated with immune suppression [23, 28, 29]. Screening mothers for CD4 cell counts could help to identify infants at highest risk of PNT so that alternative feeding methods (or antiretroviral therapy for the mother) can be considered.
Three limitations of this study deserve mention. First, we did not collect data on maternal blood viral load during breastfeeding, which is an important determinant of the risk of PNT. Instead, we have used the maternal CD4 cell count, hemoglobin, MUAC, and death during the follow-up period as indicators of the severity of maternal disease. Second, we did not collect data on the frequency or quantity of non-breast milk foods and liquids consumed by infants, and therefore are unable to estimate whether there is a threshold in terms of non-exclusivity of breastfeeding that is associated with the increased risk of PNT. Third, feeding patterns were self-selected by mothers, raising the possibility of reverse causality (i.e. mothers who chose EBF might have been those already at a lower risk of transmission). The decision to breastfeed exclusively was indeed associated with some indicators of maternal and infant health (Table 1). However, adjusting for these variables, and including the propensity score in the final model, did not change the protective effect of EBF. Importantly, the strongest single predictor of EBF in this cohort and among the entire study population, including HIV-negative mothers , was enrolment in the study after implementation of the education and counseling programme, suggesting that choosing EBF was primarily the result of being better informed, not being healthier.
The practice of EBF was relatively uncommon for two probable reasons. It is the cultural norm to introduce liquids and solid foods very early in Zimbabwe . Also, the methods used to define EBF in our study were very strict. Whereas most surveys use 24-h recall methods to define EBF, we used prospectively collected data that covered the entire first 3 months of life. Following a sensitivity analysis, we decided to allow one lapse in our strict definition of EBF, which could have biased our estimates towards the null. However, the PNT risk in EBF infants with and without one lapse of non-milk liquids was similar at 6 months (1.2 versus 1.5%), suggesting that allowing this one lapse had little effect.
Our findings underscore the importance of supporting EBF, particularly in areas of high HIV prevalence, where many women do not know their HIV status, and among HIV-positive mothers who choose to breastfeed. The early introduction of non-human milks and solid foods should be strongly discouraged because it increases the risk of HIV infection for babies of HIV-positive women and the risk of diarrhea and respiratory infections for all babies [8–10]. Among breastfeeding women known to be HIV positive, early breastfeeding cessation should be considered, along with support for nutritionally adequate, safe replacement feeding. HIV-positive mothers with CD4 cell counts less than 200 cells/μl should be strongly encouraged to consider antiretroviral treatment while breastfeeding, or replacement feeding from birth because of their very high risk of PNT.
Members of the ZVITAMBO Study Team, in addition to the named authors
Henry Chidawanyika, John Hargrove, Florence Majo, Kuda Mutasa, Mary Ndhlovu, Robert Ntozini and Phillipa Rambanepasi (ZVITAMBO); Agnes Mahomva (AIDS and TB Unit, Ministry of Health and Child Welfare, Zimbabwe); Lucie Malaba (Faculty of Science, University of Zimbabwe); Michael Mbizvo, Partson Zvandasara and Lynn Zijenah (University of Zimbabwe College of Health Sciences); Lidia Propper and Andrea Ruff (The Johns Hopkins Bloomberg School of Public Health, Department of International Health).
P. Iliff participated in the conception, design, and implementation of the study, and drafting the manuscript. E. Piwoz participated in study conception and design, undertook most of the analysis and drafted the manuscript. N. Tavengwa participated in study design, implementation and interpretation. C. Zunguza contributed to study interpretation. E. Marinda and L. Moulton contributed to the statistical analysis. K. Nathoo participated in study design, implementation and interpretation. B. Ward contributed to conception, design and interpretation. J. Humphrey is the principal investigator of the ZVITAMBO trial, and participated in all aspects of the study, including conception, design, implementation, analysis and drafting of the manuscript. All primary authors reviewed the final manuscript. All members of the ZVITAMBO Team contributed to design and implementation.
Sponsorship: 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-00-97-00015-00 between Johns Hopkins University and the Office of Health and Nutrition, USAID) and a grant from the Bill and Melinda Gates Foundation, Seattle, WA, USA. Additional funding was received from the Rockefeller Foundation (NY, USA), BASF (Ludwigshafen, Germany), and from the Support for Analysis and Research in Africa (SARA) project (contract number AOT-C-00-99-00237-00 between USAID/Bureau for Africa/Office of Sustainable Development and the Academy for Educational Development).
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Hot Topics in Infection and Immunity in Children III
Prevention of transmission of HIV-1 from mothers to infants in Africa
Hot Topics in Infection and Immunity in Children III, 582():
Epidemiology and InfectionHIV-1 and HIV-2 prevalence and associated risk factors among postnatal women in Harare, ZimbabweEpidemiology and Infection
Contemporary Clinical TrialsModifications of a large HIV prevention clinical trial to fit changing realities: A case study of the Breastfeeding, Antiretroviral, and Nutrition (BAN) protocol in Lilongwe, MalawiContemporary Clinical Trials
Exclusive breastfeeding and HIV
Patient Education and CounselingInvestigating the decision-making needs of HIV-positive women in Africa using the Ottawa Decision-Support Framework: Knowledge gaps and opportunities for interventionPatient Education and Counseling
Mother-to-child transmission of HIV-1 infection during exclusive breastfeeding in the first 6 months of life: an intervention cohort study
Journal of Infectious DiseasesBreast-feeding and HIV-1 transmission - How risky for how long?Journal of Infectious Diseases
Trends in BiotechnologyHumanizing infant milk formula to decrease postnatal HIV transmissionTrends in Biotechnology
Preventive MedicineHIV and exclusive breastfeeding: Just how exclusive and when to stop?Preventive Medicine
Health PolicyBreast milk as the "water that supports and preserves life"-Socio-cultural constructions of breastfeeding and their implications for the prevention of mother to child transmission of HIV in sub-Saharan AfricaHealth Policy
Presse MedicaleThe challenges of preventing mother-to-child transmission of HIV in AfricaPresse Medicale
Social Science & Medicine"We Grandmothers Know Plenty": Breastfeeding, complementary feeding and the multifaceted role of grandmothers in MalawiSocial Science & Medicine
Journal of Human LactationPromotion of WHO feeding recommendations: A model evaluating the effects on HIV-Free survival in African childrenJournal of Human Lactation
Sexually Transmitted InfectionsThe Spectrum projection package: improvements in estimating mortality, ART needs, PMTCT impact and uncertainty boundsSexually Transmitted Infections
Plos OneThe Contribution of Family Planning towards the Prevention of Vertical HIV Transmission in UgandaPlos One
Increased risk of infant HIV infection with early mixed feeding
Maternal and child undernutrition 1 - Maternal and child undernutrition: global and regional exposures and health consequences
Maternal and Child Undernutrition 3 - What works? Interventions for maternal and child undernutrition and survival
Tropical Medicine & International HealthMaking a working clinical diagnosis of HIV infection in infants in ZimbabweTropical Medicine & International Health
Clinical Infectious DiseasesPremastication: A Possible Missing Link?Clinical Infectious Diseases
Effects of infant sex on mother-to-child transmission of HIV-1 according to timing of infection in Zimbabwe
Journal of Infectious DiseasesLaboratory indicators of mastitis are not associated with elevated HIV-1 DNA loads or predictive of HIV-1 RNA loads in breast milkJournal of Infectious Diseases
Archives of Disease in ChildhoodInfant feeding in the time of HIV: rapid assessment of infant feeding policy and programmes in four African countries scaling up prevention of mother to child transmission programmesArchives of Disease in Childhood
Jognn-Journal of Obstetric Gynecologic and Neonatal NursingAn Update on HIV and Infant Feeding Issues in Developed and Developing CountriesJognn-Journal of Obstetric Gynecologic and Neonatal Nursing
Public Health NutritionRapid assessment of infant feeding support to HIV-positive women accessing prevention of mother-to-child transmission services in Kenya, Malawi and ZambiaPublic Health Nutrition
Clinical Infectious DiseasesMilk Mysteries: Why Are Women Who Exclusively Breast-Feed Less Likely to Transmit HIV during Breast-Feeding?Clinical Infectious Diseases
Implementation ScienceTranslating global recommendations on HIV and infant feeding to the local context: the development of culturally sensitive counselling tools in the Kilimanjaro Region, TanzaniaImplementation Science
Contemporary Clinical TrialsInvolving communities in the design of clinical trial protocols: The BAN Study in Lilongwe, MalawiContemporary Clinical Trials
Nigerian Journal of Clinical Practice
Situation Analysis of the Existing Infant Feeding Pattern At the Commencement of the Prevention of Mother to Child Transmission (Pmtct) of Hiv Programme in Ibadan
Nigerian Journal of Clinical Practice, 12(4):
Maternal and Child NutritionEstablishing individual peer counselling for exclusive breastfeeding in Uganda: implications for scaling-upMaternal and Child Nutrition
Journal of Infectious DiseasesSafe Water and HIV-Exposed Infants ReplyJournal of Infectious Diseases
Clinical Infectious DiseasesAssociations between Breast Milk Viral Load, Mastitis, Exclusive Breast-Feeding, and Postnatal Transmission of HIVClinical Infectious Diseases
Journal of Infectious Diseases
Combination antiretroviral therapy in African nursing mothers and drug exposure in their infants: New pharmacokinetic and virologic findings
Journal of Infectious Diseases, 192(5):
Human Resources for HealthSupervision of community peer counsellors for infant feeding in South Africa: an exploratory qualitative studyHuman Resources for Health
Journal of Human Lactation"Peer but Not Peer": Considering the Context of Infant Feeding Peer Counseling in a High HIV Prevalence AreaJournal of Human Lactation
Bmc PediatricsNeed to optimise infant feeding counselling: A cross-sectional survey among HIV-positive mothers in Eastern UgandaBmc Pediatrics
American Journal of Public HealthThe impact of safer breastfeeding practices on postnatal HIV-1 transmission in ZimbabweAmerican Journal of Public Health
International perspectives, progress, and future challenges of paediatric HIV infection
International Journal of Gynecology & ObstetricsBreastfeeding: A woman's reproductive rightInternational Journal of Gynecology & Obstetrics
British Medical Journal
Preventing HIV infection - Needs urgent attention now that effective treatment is widely available
British Medical Journal, 331():
Journal of Parenteral and Enteral NutritionASPEN Clinical Guidelines: Nutrition Support of Children With Human Immunodeficiency Virus InfectionJournal of Parenteral and Enteral Nutrition
New England Journal of Medicine
Effects of early, abrupt weaning on HIV-free survival of children in Zambia
New England Journal of Medicine, 359(2):
Journal of Nutrition
HIV-Positive poor women may stop breast-feeding early to protect their infants from HIV infection although available replacement diets are grossly inadequate(1,2)
Journal of Nutrition, 138(2):
American Journal of Clinical Nutrition
Long-chain n-6 polyunsaturated fatty acids in breast milk decrease the risk of HIV transmission through breastfeeding
American Journal of Clinical Nutrition, 86(3):
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivPrioritising prevention strategies for patients in antiretroviral treatment programmes in resource-limited settingsAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivConsequences of HIV for children: avoidable or inevitable?AIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
International Journal of Gynecology & ObstetricsTiming and determinants of mother-to-child transmission of HIV in NigeriaInternational Journal of Gynecology & Obstetrics
Maternal and Child Nutrition
Mainstreaming nutrition into maternal and child health programmes: scaling up of exclusive breastfeeding
Maternal and Child Nutrition, 4():
Plos Clinical TrialsHigh uptake of exclusive breastfeeding and reduced early post-natal HIV transmissionPlos Clinical Trials
British Medical JournalInfant feeding and HIV - Avoiding transmission is not enoughBritish Medical Journal
Journal of Infectious Diseases
Balancing maternal and infant benefits and the consequences of breast-feeding in the developing world during the era of HIV infection
Journal of Infectious Diseases, 195(2):
Public Health NutritionCommunity-based assessment of infant feeding practices within a programme for prevention of mother-to-child HIV transmission in rural ZimbabwePublic Health Nutrition
Seminars in Fetal & Neonatal MedicineProtection, promotion and support of breastfeeding in low-income countriesSeminars in Fetal & Neonatal Medicine
Reproductive Health Matters
Exclusive breastfeeding reduces the risk of HIV transmission
Reproductive Health Matters, 13():
Reply to 'Mode of infant feeding and HIV infection in children in a program for prevention of mother-to-child transmission in Uganda' by Magoni et al
Plos OneHigh Uptake of Exclusive Breastfeeding and Reduced Early Post-Natal HIV TransmissionPlos One
Monatsschrift KinderheilkundeBreast feeding by HIV infected mothersMonatsschrift Kinderheilkunde
New England Journal of Medicine
Breast-feeding, antiretroviral prophylaxis, and HIV
New England Journal of Medicine, 359(2):
PediatricsBreastfeeding and HIV infectionPediatrics
Journal of Infectious DiseasesChallenges to pediatric HIV care and treatment in South AfricaJournal of Infectious Diseases
Effectiveness of the WHO/UNICEF guidelines on infant feeding for HIV-positive women: results from a prospective cohort study in South Africa
PediatricsTransmission of West Nile virus through human breast milk seems to be rarePediatrics
Maternal and Child NutritionAcceptability and feasibility of infant-feeding options: experiences of HIV-infected mothers in the World Health Organization Kesho Bora mother-to-child transmission prevention (PMTCT) trial in Burkina FasoMaternal and Child Nutrition
Perspectives on paediatric HIV/AIDS: Prevention of mother to child transmission of HIV
Current Science, 95(9):
Tropical Medicine & International HealthDiversity of risk of mother-to-child HIV-1 transmission according to feeding practices, CD4 cell count, and haemoglobin concentration in a South African cohortTropical Medicine & International Health
International Journal of EpidemiologyEstimating the number of vertically HIV-infected children eligible for antiretroviral treatment in resource-limited settingsInternational Journal of Epidemiology
Journal of Infectious DiseasesLate postnatal transmission of HIV-1 and associated factorsJournal of Infectious Diseases
Journal of Nutrition
A longitudinal qualitative study of infant-feeding decision making and practices among HIV-Positive women in South Africa
Journal of Nutrition, 136(9):
Food and Nutrition Bulletin
Breastfeeding and mixed feeding practices in Malawi: Timing, reasons, decision makers, and child health consequences
Food and Nutrition Bulletin, 28(1):
Plos MedicineTwo-year morbidity-mortality and alternatives to prolonged breast-feeding among children born to HIV-infected mothers in Cote d'IvoirePlos Medicine
Plos MedicineWhen is replacement feeding safe for infants of HIV-infected women?Plos Medicine
Lancet Infectious Diseases
Mother-to-child transmission of HIV-1: timing and implications for prevention
Lancet Infectious Diseases, 6():
Breast-Feeding: Early Influences on Later Health
Exclusive Breast-Feeding and Hiv Infection
Breast-Feeding: Early Influences on Later Health, 639():
Acta PaediatricaEarly cessation of breastfeeding to prevent postnatal transmission of HIV: a recommendation in need of guidanceActa Paediatrica
Preventive MedicineEarly mixed feeding and breastfeeding beyond 6 months increase the risk of postnatal HIV transmission: ANRS 1201/1202 Ditrame Plus, Abidjan, Cote d'IvoirePreventive Medicine
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivInfant feeding practices: Realities and mindsets of mothers in southern AfricaAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
Journal of Tropical PediatricsEvidence behind the WHO guidelines: Hospital care for children: What are the risks of HIV transmission through breastfeeding?Journal of Tropical Pediatrics
Human Ecology Review
The AIDS epidemic in a low-income country: Ethiopia
Human Ecology Review, 14(1):
AIDS Research and Human RetrovirusesPostpartum Plasma CD4 Change in HIV-Positive Women: Implications for Timing of HAART InitiationAIDS Research and Human Retroviruses
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivSocial determinants of mixed feeding behavior among HIV- infected mothers in Jos, NigeriaAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
American Journal of Clinical NutritionGrowth faltering due to breastfeeding cessation in uninfected children born to HIV-infected mothers in ZambiaAmerican Journal of Clinical Nutrition
American Journal of Clinical NutritionEffect of early exclusive breastfeeding on morbidity among infants born to HIV-negative mothers in ZimbabweAmerican Journal of Clinical Nutrition
Journal of Veterinary Internal Medicine
Decreased periparturient transmission of bovine leukosis virus in colostrum-fed calves
Journal of Veterinary Internal Medicine, 21(5):
Maternal and Child Nutrition
Nutrition and HIV/AIDS in infants and children in South Africa: implications for food-based dietary guidelines
Maternal and Child Nutrition, 3(4):
Post-weaning breast milk HIV-1 viral load, blood prolactin levels and breast milk volume
Bulletin of the World Health Organization
Exclusive breastfeeding and postnatal transmission of HIV
Bulletin of the World Health Organization, 83():
Journal of PerinatologyEffect of maternal HIV status on infant mortality: evidence from a 9-month follow-up of mothers and their infants in ZimbabweJournal of Perinatology
Journal of Public Health PolicyBreast feeding: A time to craft new policiesJournal of Public Health Policy
European Journal of Clinical NutritionEffect of vitamin supplementation on breast milk concentrations of retinol, carotenoids and tocopherols in HIV-infected Tanzanian womenEuropean Journal of Clinical Nutrition
Use of the Australian Milk Biscuit to combat infant malnutrition and mother-to-child transmission of HIV
Food Australia, 58():
Jama-Journal of the American Medical Association
Breastfeeding plus infant zidovudine prophylaxis for 6 months vs formula feeding plus infant zidovudine for 1 month to reduce mother-to-child HIV transmission in Botswana - A randomized trial: The Mashi study
Jama-Journal of the American Medical Association, 296(7):
American Journal of Clinical Nutrition
Effect of maternal and neonatal vitamin A supplementation and other postnatal factors on anemia in Zimbabwean infants: a prospective, randomized study
American Journal of Clinical Nutrition, 84(1):
Journal of Human LactationFactors affecting the duration of exclusive breastfeeding among HIV-infected and -uninfected women in Lusaka, ZambiaJournal of Human Lactation
Cochrane Database of Systematic ReviewsInterventions for preventing late postnatal mother-to-child transmission of HIVCochrane Database of Systematic Reviews
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivDemotivating infant feeding counselling encounters in southern Africa: Do counsellors need more or different training?AIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
American Journal of Obstetrics and GynecologyPrevention of human immunodeficiency virus-1 transmission to the infant through breastfeeding: new developmentsAmerican Journal of Obstetrics and Gynecology
American Journal of Obstetrics and GynecologySite-specific interventions to improve prevention of mother-to-child transmission of human immunodeficiency virus programs in less developed settingsAmerican Journal of Obstetrics and Gynecology
American Journal of Obstetrics and GynecologyInfant human immunodeficiency virus diagnosis in resource-limited settings: issues, technologies, and country experiencesAmerican Journal of Obstetrics and Gynecology
Plos MedicineStructural violence and clinical medicine: Free infant formula for HIV-exposed infantsPlos Medicine
Plos OneDuration, Pattern of Breastfeeding and Postnatal Transmission of HIV: Pooled Analysis of Individual Data from West and South African CohortsPlos One
Studies in Family Planning
Meeting the Family Planning Needs of Postpartum Women
Studies in Family Planning, 40(3):
Plos MedicineFurther evidence that exclusive breast-feeding reduces mother-to-child HIV transmission compared with mixed feedingPlos Medicine
HIV incidence among post-partum women in Zimbabwe: risk factors and the effect of vitamin A supplementation
Public Health NutritionMothers' infant feeding experiences: constraints and supports for optimal feeding in an HIV-impacted urban community in South AfricaPublic Health Nutrition
Clinical Microbiology ReviewsAdvances and Failures in Preventing Perinatal Human Immunodeficiency Virus InfectionClinical Microbiology Reviews
Bmc Public HealthInfant feeding among HIV-positive mothers and the general population mothers: comparison of two cross-sectional surveys in Eastern UgandaBmc Public Health
Reproductive Health MattersRights of HIV positive people to sexual and reproductive health: ParenthoodReproductive Health Matters
Tropical Medicine & International HealthAdoption of safer infant feeding and postpartum sexual practices and their relationship to maternal HIV status and risk of acquiring HIV in ZimbabweTropical Medicine & International Health
Maternal and Child Nutrition
Acceptability, feasibility and affordability of infant feeding options for HIV-infected women: a qualitative study in south-west Nigeria
Maternal and Child Nutrition, 2(3):
Bjog-An International Journal of Obstetrics and GynaecologyPreventing mother-to-child transmission of HIV: successes and challengesBjog-An International Journal of Obstetrics and Gynaecology
PediatricsComplementary feeding adequacy in relation to nutritional status among early weaned breastfed children who are born to HIV-infected mothers: ANRS 1201/1202 Ditrame Plus, Abidjan, Cote d'IvoirePediatrics
Bmc Public HealthA qualitative investigation into knowledge, beliefs, and practices surrounding mastitis in sub-Saharan Africa: what implications for vertical transmission of HIV?Bmc Public Health
Current Opinion in Clinical Nutrition & Metabolic CareFeeding of infants of HIV-positive mothersCurrent Opinion in Clinical Nutrition & Metabolic Care
Current Opinion in Obstetrics and GynecologyHIV and pregnancy: screening and management updateCurrent Opinion in Obstetrics and Gynecology
Current Opinion in PediatricsBreastfeeding and AIDS in the developing worldCurrent Opinion in Pediatrics
JAIDS Journal of Acquired Immune Deficiency SyndromesPregnancy Outcomes in HIV-Infected and Uninfected Women in Rural and Urban South AfricaJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesVitamin Content of Breast Milk From HIV-1-Infected Mothers Before and After Flash-Heat TreatmentJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesInnate Factors in Human Breast Milk Inhibit Cell-Free HIV-1 but Not Cell-Associated HIV-1 Infection of CD4+ CellsJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesFlash-Heat Inactivation of HIV-1 in Human Milk: A Potential Method to Reduce Postnatal Transmission in Developing CountriesJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesThe Risks of Not BreastfeedingJAIDS Journal of Acquired Immune Deficiency Syndromes
Journal of Pediatric Gastroenterology and NutritionBreast-feeding: A Commentary by the ESPGHAN Committee on NutritionJournal of Pediatric Gastroenterology and Nutrition
The Pediatric Infectious Disease JournalChild Mortality According to Maternal and Infant HIV Status in ZimbabweThe Pediatric Infectious Disease Journal
The Pediatric Infectious Disease JournalCare and Treatment of HIV-Infected Children in Africa: Issues and Challenges at the District Hospital LevelThe Pediatric Infectious Disease Journal
The Pediatric Infectious Disease JournalEfficacy of Pentavalent Human-Bovine (WC3) Reassortant Rotavirus Vaccine Based on Breastfeeding FrequencyThe Pediatric Infectious Disease Journal
breastfeeding; exclusive; Zimbabwe; HIV; postnatal transmission
© 2005 Lippincott Williams & Wilkins, Inc.
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