Exclusive breast-feeding  (EBF) plays a critical role in child survival and health [2,3]. An estimated 13% of under-5 deaths could be prevented by optimal breast-feeding during the infant's first year (EBF from 0 to 6 months and continued breast-feeding from 7 to 11 months ). The enormous benefits of EBF in developing countries include improved nutrition  and reductions in infant morbidity, mortality and mother-to-child transmission (MTCT) of HIV [6–10]. However, only a small number of women practice EBF [11,12]. An estimated 27% of children in sub-Saharan Africa exclusively breast-fed for the first 3 months of life, based on 24-h feeding histories .
Programs that increase breast-feeding rates do not necessarily increase exclusive breast-feeding rates [14–16]. Interventions concentrating on hospital policies and practices have shown significant impacts on early breast-feeding outcomes, but these effects are not sustained [14,15,17]. There is evidence, in low HIV prevalence communities, that EBF rates can be sustained with home visits by peer counselors [18–20] or further support through primary healthcare services .
In high HIV prevalence areas, despite guidelines to promote appropriate infant feeding choices [1,22–24], ineffective counseling and factors including the effect of mass media have resulted in widespread confusion around infant feeding. HIV-positive women do not always receive advice to practice EBF or avoid all breast-feeding (i.e., replacement feeding), resulting in mixed feeding [25–27]. Additionally, provision of free formula within Prevention of Mother-to-Child Transmission programs (PMTCT), accompanied by unclear messages about the role of breast-feeding, has resulted in spillover (avoidance of breastfeeding or mixed feeding among HIV-negative women, or women who do not know their HIV status, due to unfounded fears about HIV or of misinformation of, or the ready availability of, breast-milk substitutes) of suboptimal feeding practices to HIV-negative women .
We report on an intervention designed to improve breast-feeding practices in all HIV-negative women and HIV-positive women who opted to breast-feed in a high HIV prevalence area [29,30] with previously low rates of EBF (6% at 16 weeks) . EBF rates were assessed rigorously, both cross-sectionally and cumulatively.
Population and methods
Women attending seven rural, one semiurban and one urban antenatal clinics in KwaZulu-Natal, South Africa, between 2001 and 2004, were enrolled in a nonrandomized intervention cohort study to investigate breast-feeding and MTCT of HIV . HIV prevalence rates among pregnant women in the study area were approximately 40% [29,32].
Lay HIV (12) and breast-feeding counselors (30, and six supervisors) supported infant feeding. Counselors, with 12 completed years of schooling, were selected following assessments of literacy, numeracy and basic counseling skills. There was no age limit or requirement to have personally breast fed. All counselors participated in the WHO/UNICEF Breastfeeding Counselling Course , with subsequent on-site supervision. HIV counselors also completed the WHO/UNICEF HIV and Infant Feeding Counselling Course . Breast-feeding supervisors carried out home visits with each counselor monthly to monitor quality of counseling and also conducted problem-solving visits.
HIV counselors discussed infant feeding choices with all women, according to WHO/UNAIDS guidelines available at the time [22,24,34]. HIV-negative women received information only about EBF for the first 6 months with sustained breast-feeding thereafter . HIV-positive women were counseled on EBF, replacement feeding  and the criteria for safe replacement feeding (i.e. acceptable, feasible, affordable, sustainable and safe ). Our antenatal counseling approach has been described previously .
Breast-feeding counselors visited all women at home, after enrolment, to discuss study logistics. HIV-infected women intending to replacement feed were referred to the study infant feeding specialist for further feeding support. All women choosing to breast feed received up to three further antenatal home visits by the breast-feeding counselor to discuss issues (identified during formative research [31,36]) including exclusive breast-feeding, previous feeding practices, importance of colostrum, positioning/attaching a baby and dealing with breast-feeding difficulties. Women experiencing difficulties received additional ‘unscheduled’ visits from the breast-feeding counselor with referral to the supervisor as necessary.
Within 72 h of delivery, all women received one home visit from the breast-feeding counselor, irrespective of antenatal feeding intention. Mothers initiating breast-feeding received a further three home visits in the first 2 weeks and fortnightly thereafter for 6 months after delivery. In addition, study nurses supported mothers in feeding choices at scheduled clinic visits (6, 10, 14, 18, 22 and 26 weeks).
Breast-feeding counselors recorded information on breast health and breast-feeding technique. Mothers were also visited weekly by field monitors who documented all feeds (milk and solids) and fluids for each day of the preceding week [7,37,38]. Mothers maintained food intake diaries for use during the interview to corroborate the verbal report. If a mother was not present for a counseling or monitoring visit, the study team returned up to 2 consecutive days, and if the mother was still absent, this was classed as a missed visit and information about that week collected retrospectively at the next visit. Breast-feeding counselors and field monitors were blinded to maternal HIV status.
In the urban site, owing to concerns about staff security, separate counseling and monitoring visits were carried out at the clinic with the same frequency as home visits in the rural area. Mothers also kept diaries.
At the first antenatal home visit, maternal sociodemographic details were recorded. Antenatal CD4 counts were determined in HIV-positive women (September 2001–March 2003; FACScan; Becton, Dickinson and Company, New Jersey, USA; then Epics XL; Beckman Coulter Inc., California, USA). During the study, the Provincial policy was that all HIV-positive women and their infants received single-dose nevirapine . Highly active antiretroviral treatment was not available through the Provincial health services, but since 2004 all eligible women and infants have been referred. Free commercial infant formula became available through the KwaZulu-Natal PMTCT program from December 2002.
WHO definitions of infant feeding were used throughout the study [24,40]. EBF was defined as no other food or drink, not even water, apart from breast milk (including expressed breast milk) with the exception of drops or syrups consisting of vitamins, mineral supplements or medicines.
As there were few breast health problems, mastitis, engorgement, cracked/bleeding nipple, blocked duct, breast thrush, breast/nipple oozing pus and abscess were grouped into one ‘breast health problem’ variable. Likewise, difficulties associated with breast-feeding were grouped into one ‘feeding difficulty variable’ – maternal perception of insufficient milk, breast refusal, and baby crying, hungry or thirsty.
The analysis here presents data for 180 days, in line with the policy of promoting EBF for 6 completed months for HIV-negative women and HIV-positive women opting to breast feed.
Data were stored into a Microsoft SQL server database. Infants with more than 7 cumulative days of missing data (e.g. a missing weekly data form) were excluded from analysis from day 1 of the missing data, as an accurate feeding practice could not be ascribed to the missing days. If data for 1 day were missing, the feeding pattern on the day after the missing day was ascribed to the missed day. Analyses were performed in Stata (Version 9.1; Stata Corporation, College Station, Texas, USA). Continuous data with a normal distribution were assessed using T-test, Mann–Whitney test for nonnormal distributions, χ2 for categorical variables and Fisher's exact test if numbers were small. Cross-sectional EBF rates, at different time points, were based on feeding patterns over 24 h.
Cumulative EBF rates for all mothers and cumulative rates of feeding as per infant feeding policy  in HIV-positive women were assessed by Kaplan–Meier analysis and association with maternal and infant variables were quantified in a Cox regression analysis [41,42]. A backward stepwise regression was performed eliminating nonsignificant variables (P > 0.10) from the multivariable model and monitoring the model fit; having confirmed that the nonsignificant variables did not impact on the significant variables, all covariates were then included in the final model to allow easy comparison between HIV-positive and HIV-negative women. Feeding as per infant feeding policy, for HIV-positive women, was defined as either EBF or replacement feeding, with switching from EBF to replacement feeding allowed in the analysis, but not from replacement feeding to EBF . The proportional hazards assumption of the Cox regression was assessed using log plots and a generalized linear regression of the Schoenfeld residuals on time .
The determinants of women who returned to breast-feeding only after a period of mixed feeding were assessed in univariable and multivariable logistic regression analysis.
The effect of scheduled breast-feeding visits on EBF adherence was assessed separately in univariable and multivariable logistic regression analysis. All women were scheduled to receive a sequence of visits, but some did not, due to high mobility in this area . Scheduled visits used for analysis were four visits in the first 14 days after delivery, two visits within ±2 weeks of 1 month (30 days) of age and two visits within ±2 weeks of 3 months (90 days) of age.
The study was approved by the Biomedical Research Ethics Committee of the University of KwaZulu-Natal.
Between October 2001 and April 2005, 2781 women delivered 2831 live infants. Postnatal feeding data were available on 2436 singleton infants: 1219 (50%) infants of HIV-negative mothers and 1217 (50%) infants of HIV-positive mothers (Table 1). There were no feeding data on 313 (12.8%) liveborn infants [138 (44%) of HIV-negative, 175 (56%) of HIV-positive women]: seven (2.2%) did not fulfill the eligibility criteria (lived outside study areas; indeterminate maternal HIV status), 52 (16.6%) moved away, 102 (32.6%) withdrew consent, 66 (21.1%) were lost to follow-up, 21 (6.7%) have missing feeding data in week 1 and 65 (20.8%) died in week 1.
Forty-one sets of twins are not included in subsequent analyses. Of these, 36 of 38 infants of HIV-negative women had at least 1 day of EBF with a median of 138.5 days [interquartile range (IQR): 48.3–170.5]; and 40 of 44 infants of HIV-positive women had at least 1 day of EBF with a median of 78.5 days (IQR: 15.5–175). Six infants received no breast milk at all – two of HIV-negative and four of HIV-positive women.
Breast health and feeding problems
Eighty-four (6.9%) HIV-negative women and 88 (7.2%) HIV-positive women had a breast health problem during months 1–2, 13 (1.1%) and 34 (2.8%) during months 3–4 and 10 (0.8%) and 18 (1.5%) during months 5–6.
Breast-feeding difficulties were more common. Three hundred and eighty (31.2%) HIV-negative women and 391 (32.1%) HIV-positive women reported a difficulty during months 1–2, 255 (20.9%) and 252 (20.7%) during months 3–4, 220 (18.1%) and 199 (16.4%) during months 5–6. The most common problems reported during each period were perceived breast milk insufficiency, hungry baby and baby with blocked nose.
Overall, there were 395 415 days of follow-up, of which 309 927 (78.3%) related to days of EBF. Information was available for 1025 (84%) infants of HIV-negative mothers and 941 (77.3%) infants of HIV-positive mothers for the full 180 days of follow-up, 1012 (98.7%) and 851 (90.4%), respectively, of these infants had at least 1 day of EBF. The median duration of EBF was 177 days (R = 1–180, IQR = 150–180) for infants born to HIV-negative women and 175 (R = 1–180, IQR 137–180) for those born to HIV-positive women.
Assessed cross-sectionally, using a 24-h feeding history, over 80% of the infants were EBF at 1 month and over 60% at 5.5 months (Fig. 1). In Kaplan–Meier survival analyses, the estimated cumulative EBF rates were similar in infants of HIV-positive and HIV-negative women (Fig. 2 and Table 2). The probability of not EBF was strongly associated with socioeconomic factors (including fuel, availability of fridge, urban vs. rural setting) and reported breast health or feeding difficulties in the previous 2 weeks (Table 3). Birth weight and maternal CD4 counts, not significant univariably, were not included in the multivariable model.
Effect of breast-feeding counseling visits on adherence to cumulative exclusive breast-feeding
The impact of postnatal breast-feeding counseling visits could not be included in the overall analysis presented in Table 3, due to differential censoring, and was therefore examined separately in multivariable analysis allowing for the variables in Table 3. This was because women stopped EBF at different times and would thus have received a diminished number of visits after the initial attempts to reinstate EBF. A woman who stopped EBF at 1 month would have had fewer visits at 4 months than a woman who continued EBF to 4 months, thus confusing any causal relationship between the visits and the EBF.
At 1 month, HIV-positive women who had received the scheduled number of visits were more than twice as likely to still be EBF at that time [adjusted odds ratio (AOR): 2.29; 95% confidence interval (CI): 1.60–3.28; P < 0.0001]. At 2 and 4 months, the number of scheduled visits received was also significantly associated with the likelihood of continued EBF, especially for HIV-positive women (Table 4).
Determinants of women who return to giving breast milk only after a period of mixed feeding
Five hundred and eighty-nine HIV-negative and 561 HIV-positive women interrupted EBF before 180 days, of whom 368 (62.5%) and 316 (56.3%), respectively, returned to giving breast milk only within a median of 2 days (HIV-negative women, R = 1–157, IQR: 1–9; HIV-positive women, R = 1–129, IQR: 1–9). After adjusting for the variables detailed in Table 3, the probability of returning to giving breast milk only was strongly associated with a history of feeding difficulties in the previous 2 weeks in HIV-negative women (AOR: 1.45; 95% CI: 1.01–2.09; P 0.044) and less strongly in HIV-positive women (AOR: 1.38; 95% CI: 0.94–2.01; P 0.096).
Cumulative feeding as per infant feeding policy
In this analysis, we examined feeding as per infant feeding policy in HIV-positive women (EBF or replacement feeding, with switching from EBF to replacement feeding allowed, but not replacement feeding to EBF). In Kaplan–Meier survival analysis, an estimated 91.4% of infants were fed according to policy at 7 days, 83.3% at 1 month, 75.8% at 2 month, 70.7% at 3 months, 64.7% at 4 months, 59.7% at 5 months and 48.9% at 6 months. The probability of not feeding as per policy was strongly associated with cooking using electricity compared with wood [adjusted hazard ratio (AHR): 1.45; 95% CI: 1.09–1.92; P = 0.010], living in an urban vs. rural setting (AHR: 0.60; 95% CI: 0.41–0.88; P = 0.009), and feeding difficulties in the previous 2 weeks (AHR: 2.05; 95% CI: 1.64–2.56; P < 0.001).
After the introduction of free formula milk into the area, more women practiced replacement feeding (12.7 vs. 6.5%; P < 0.001). However, there was no significant difference in the number of mixed feeding days before and after the introduction of free formula: HIV-positive women, 7 vs. 5.5 days (P = 0.979); HIV-negative women, 5 vs. 8 days (P = 0.650). Similarly, the proportion of HIV-positive women with access to clean water, appropriate fuel and a fridge who initiated replacement feeding, as opposed to EBF, before and after the introduction of free formula was not significantly different (P = 0.558). Free formula did not have an association with the probability of women returning to breast-feeding only after a period of non-EBF.
We demonstrate high rates of EBF (cross-sectionally and cumulatively) in HIV-positive and negative women in a high HIV prevalence area. To our knowledge, this is one of the most stringent studies on community support for EBF among HIV-positive women [9,44]. The strengths of the study include a strict definition of EBF (women excluded from the ‘EBF’ category on the first occasion of giving something other than breast milk to their infant), excluding those with over 7 cumulative days of missing data, daily infant feeding patterns, cumulative lifetime EBF histories  in addition to cross-sectional rates and feeding data collected by an independent group of field workers from the breast-feeding counselors.
There was no evidence of spillover [26,28] of mixed feeding; almost all HIV-negative women breast fed with a median EBF duration of 177 days. At 5 months, more than three in four women were practicing EBF by 24-h recall, in line with research from low HIV prevalence areas [19,20], but significantly higher than reports from hospital-based interventions [15,45]. Even using the most stringent cumulative EBF data, nearly half of the HIV-negative women had given nothing else to their infants by 180 days. Women who interrupted EBF with a period of mixed feeding returned to giving breast milk only within a median of 2 days.
We demonstrate higher EBF rates in HIV-positive women than previously reported [9,46,47]. Cross-sectional EBF rates were slightly lower in HIV-positive than negative women, reflecting the use of replacement feeding in line with infant feeding policy . Cumulatively, 40% of HIV-positive women had given only breast milk to their infants for 180 days.
Prior to this intervention, we reported extremely low rates of EBF in this area that has a baby-friendly hospital . Our findings demonstrate that counseling visits were significantly associated with adherence to EBF in all women. However, further research is needed to identify how this support could be scaled up, and the intensity of counseling needed to result in changes in infant feeding that are justifiable economically.
Ninety-one percent of HIV-positive women were feeding their infants as per UN recommendations at 7 days and 64% were doing so at 4 months, in contrast to reports of suboptimal feeding practices elsewhere in the country [25,26,48]. After free formula was introduced, the proportion of infants of HIV-positive mothers receiving replacement feeding on day 7 increased significantly. However, it is encouraging that women choosing replacement feeding were as likely to have appropriate home resources after the availability of free formula as before. The finding that free formula caused no increase in days of mixed feeding is probably due to the extraordinary level of support characterizing this study.
One-third of women complained of common breast-feeding difficulties during the first 2 months. However, over 70% of all women continued EBF suggesting that, with skilled support, feeding difficulties need not be permanent barriers to EBF. Breast health problems were uncommon compared with reports in other studies [49–51], most likely due to early practical help and emphasis on demand feeding .
Carefully selected, trained and supported lay counselors offer a potentially economical alternative for promoting infant feeding, compared with reliance on an overburdened health service. The salary of one professional nurse was equivalent to that of three lay counselors. In a high HIV prevalence area, with conflicting messages around the role of breast-feeding, we integrated services for both HIV-positive and HIV-negative women, and optimized infant feeding practices in the study population. It is crucial that EBF is promoted communitywide, apart from targeting HIV-positive women, who are at risk of stigmatization if they are seen to be feeding their infants in different ways from their peers. This policy will have the advantage of improving the health of all children in communities.
Wellcome Trust supported this study (Grant #063009/Z/00/2) and the Africa Centre (Grant #050534). We are grateful to all women and children enrolled in the study and the continued dedication of the field, clinic, laboratory and data management staff at the Africa Centre, in particular Thembi Blose, Zanele Fakude, Cookie Govender, Nqobile Mkhwanazi, Londiwe Mthethwa, Samukelisiwe Mtshali and Ntombizodumo Mkwanazi. We are also grateful to Colin Newell who assisted with data management during the study and analyses, Dave Perlman and Kobus Herbst for their assistance in the design of the database, Geoff Solarsh, Shuaib Kauchali, Ameena Goga and Felicity Savage King for assistance in the initial formative pilot work and training and the World Health Organization for supplying training materials. In particular, we wish to thank the Community Liaison Office at the Africa Centre and the Community Advisory Board for their guidance and feedback throughout the study. We are also grateful to the independent members of the Study Steering Committee and the Data Monitoring and Safety Committee: Janet Darbyshire (Chair, MRC, UK), Nono Simelela (SA Department of Health), Victoria Sithole (Community Advisory Board). Data Monitoring and Safety Committee: Cathy Wilfert (Chair, Elizabeth Glaser Pediatric AIDS Foundation), Carl Lombard (Statistician, MRC, SA), Ames Dhai (Department of Obstetrics and Gynaecology and the Biomedical Ethics Unit, UKZN) and Francis Crawley (Good Clinical Practice Alliance).
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Current Opinion in Clinical Nutrition & Metabolic CareFeeding of infants of HIV-positive mothersCurrent Opinion in Clinical Nutrition & Metabolic Care
Keywords:© 2008 Lippincott Williams & Wilkins, Inc.
exclusive breast-feeding; HIV; infant feeding; rural Africa