The success and availability of antiretroviral drug interventions that effectively reduce in utero and intrapartum transmission of HIV have shifted the focus of clinical research to identifying interventions that will reduce postnatal transmission of HIV through breast milk. One such option is to provide antiretroviral therapy to the mother who is breast-feeding or to the child for the period of breast-feeding or to both. The results of clinical trials to establish the efficacy of these interventions will not, however, be available for 2–3 years. Alternative approaches include the avoidance of all breast-feeding and the use of exclusive replacement feeds (RF) or exclusive breast-feeding for a limited duration with early and rapid cessation of breast-feeding around 4–6 months of age. The efficacy and safety of the latter approach have not been established and studies are in progress to provide further information. Finally, several approaches to inactivate HIV in breastmilk are being assessed that would allow breast-feeding to continue while reducing the risk of postnatal transmission of HIV.
The operational experience of programs focusing on the prevention of mother-to-child transmission (PMTCT) in many countries in sub-Saharan Africa highlights the complexity of delivering a critical component in the process of PMTCT, i.e., voluntary counseling and testing. More difficult again is the task of sensitively and comprehensively counseling women on realistic, sustainable infant feeding choices that will optimize their children's chances of survival. This experience needs to be borne in mind because sophisticated interventions such as those described above are proposed as public health interventions to avert MTCT.
In this review, experience is discussed from clinical trials or studies additional to their main objective of assessing rates and risk factors for MTCT. This may inform policy, programming, and training options and may be especially valuable in the absence of conclusive data on the efficacy of the interventions to be applied during the breast-feeding period. For the purpose of this review, the definitions listed in Table 1 are used.
COMPLETE AVOIDANCE OF BREAST-FEEDING
A policy of complete avoidance of breast-feeding by providing free formula is being evaluated in 5 clinical studies and 2 operational settings in Abidjan, Côte d'Ivoire; Nairobi, Kenya; Soweto and Khayelitsha, South Africa; and Bangkok, Thailand. All studies were conducted in urban populations where women of unknown HIV status usually initiate breast-feeding but thereafter commonly introduce fluids, milks, and foods within the first weeks of life and would thus be mixed breast-feeding (MBF). Determinants of choice and patterns of infant feeding are described below.
In a study in Abidjan, Côte d'Ivoire, all HIV-positive women in 6 health community centers who accepted voluntary counseling and testing were offered a peripartum intervention including zidovudine and nevirapine, multivitamins, and malaria prophylaxis. 1 They were counseled antenatally on infant feeding practices. Two infant feeding options were available: a free supply of formula with bottles and sterilizing materials for 9 months from birth of the infant, with a drug inhibiting lactation; or exclusive breast-feeding for 3 months followed by early cessation of breast-feeding. All mother–infant pairs were closely followed for 2 years, with further infant feeding advice provided at each visit. 2 Between March 2001 and May 2002, 323 HIV-positive women were enrolled in the study, of whom 256 had a live birth and had fed their child at least once. Median maternal CD4+ count at inclusion to the study was 354/mm3 (interquartile range: 239–517); nearly 20% of women had a CD4+ count <200/mm3. All but 1 woman expressed a prenatal choice of feeding practice, with a little over half planning to formula feed from birth while the rest planned to breast-feed. About 80% of the women who planned to formula feed were doing so at day 2 postpartum, and of the women who planned to EBF, half were EBF, but nearly 45% were PBF. Women who were living with their partner and those without formal education were less likely to plan to formula feed. Infant feeding intention did not appear to be association with level of schooling, personal income, or access to any source of water. Based on the limited number of children followed for more than 3 months, 75% of infants were still reportedly receiving only formula. Family pressures were reported as the main reason for changing practice.
In Nairobi, Kenya, 425 pregnant women were randomly assigned to either breast-feeding or formula feeding. 3 Formula was provided free and all women were counseled against MBF. Of 195 women randomly assigned to formula feeding and who provided information on feeding practices, three-quarters reported giving only formula, while the remaining women reported breast-feeding in addition to FF. Women who were compliant with their randomized mode of infant feeding were generally older, had fewer previous live births, and had previous experience of breast-feeding. Table 2 shows the clinical, virologic, and immune characteristics of women and their infant feeding practices. Women who reported some symptoms suggestive of advanced HIV disease or who had higher viral load tended to be more compliant with EFF; however, these women did not have lower CD4 counts or additional reports of tuberculosis infection.
As a follow-up to this study and to investigate the influence of free provision of formula on women's decisions and practices, similar data were collected from HIV-infected women who were not offered or given free formula. 4 Data were available on 128 women during pregnancy. Median age was 25 years and 74% had had a previous pregnancy; only 40% had received secondary education or higher; and as many as 72% had informed their partner of the HIV test result. Ninety-one percent of women knew that HIV could be transmitted through breast milk and 73% were aware of the risks associated with giving replacement feeds. Of the women who had declared an antenatal intention to give a replacement feed, two-thirds were exclusively replacement feeding at 1 week and about 70% at 6 weeks. Compared with women who did not exclusively replacement feed, women who exclusively replacement fed at 1 week planned not to breast-feed (odds ratio [OR] 5.1), had higher income (OR 2.0), and had spouses who were willing to have an HIV test (OR 3.1). There were 25 women who were mixed feeders at 1 week and 34 at 6 weeks; these women indicated that they had received conflicting information from health care workers and had been influenced by relatives.
In South Africa, experience has been gathered from clinical research sites in Soweto, Johannesburg and operational sites in Khayelitsha, Cape Town. In a randomized trial evaluating the effect of 2 antiretroviral (nevirapine alone vs. ZDV alone) infant regimens on peripartum transmission 83 and 86% of women in the nevirapine and ZDV arms, respectively, elected to formula feed. 5,6 Formula milk was offered free to women enrolled in the study but bottles and sterilizing materials were not otherwise provided. At 6 weeks, EFF was reported by 84% women in the nevirapine group and 86% in the ZDV group. Mixed breast-feeding was reported by 4% in both groups and breast-feeding by 13 and 11%, respectively. In a cross-sectional survey among 113 women who were part of a PMTCT program, 71% had piped water in their house and the remaining 29% had to walk a median time of 5 minutes to fetch water from public taps; 75% women had electricity in their homes. Formula milk was provided free by the PMTCT program but no support was offered to women who choose to breast-feed. One hundred eight women did not report breast-feeding at any time since their child was born, and 5 women reported breast-feeding for a few days only. Women indicated that they chose to formula feed because they were advised to do so by their nurse/counselor, because of their HIV status and health reasons, and for a few family pressures or as an interim measure until they disclosed their status. Most women (70%) did not report any diarrheal episodes in their children, while a quarter reported their child to have had an episode of diarrhea.
In Thailand, the government PMTCT program actively endorses formula feeding by all women. This policy has been generally acceptable throughout the country and uptake of formula feeding was reported to be over 80% in 2001/2002. In research sites, almost 100% of HIV-infected women are reported to be formula feeding; only 6% of women are reported to have ever breast-fed compared with >95% in the HIV-uninfected population. Among the HIV-positive women, 62% were concerned about not breast-feeding and 70% acknowledged that other family members and friends were concerned about their avoidance of breast-feeding. About half had found it hard to explain to other people in the community why they were not breast-feeding. No morbidity or mortality data were available from these sites.
In summary, formula feeding was an acceptable feeding option to many HIV-positive women in urban settings with education or intensive counseling and adequate water supply and when the formula was provided free; high compliance to EFF can be successfully achieved in both research and government PMTCT programs. Low morbidity can be achieved in some settings but to date few longitudinal data are available from operational sites to quantify the relative risks in these settings. Choice and practice were significantly influenced not only by the advice of health workers and social and family pressures but also by women's insights regarding HIV infection and the risks of replacement feeds. Innovative approaches to reducing stigma and positively involving men and fathers in infant feeding choices and practices are urgently needed.
AVOIDANCE OF MIXED FEEDING AND EARLY CESSATION OF BREAST-FEEDING
The concern around increased morbidity and mortality associated with the use of formula feeding underlies the World Health Organization (WHO)/United Nations Children's Fund (UNICEF)/United Nations Programme on HIV/AIDS (UNAIDS) recommendation that EBF should be practiced by HIV-infected women who cannot practice safe formula feeding. 7 The possibility that EBF might also be associated with a lower transmission risk than MBF 8 has prompted several clinical studies in which the feasibility of EBF at a population level is examined and to encourage women to avoid MBF. Four studies are discussed that are testing this hypothesis and the risks associated with stopping breast-feeding earlier or more abruptly than usual.
In Abidjan, Côte d'Ivoire, women taking part in the project described above who elected to breast-feed were followed-up according to the same protocol. 1,2 During follow-up the potential risks of MBF were discussed repeatedly and women were specifically counseled on how they might stop breast-feeding and when would be appropriate and possible in their circumstance. This could be any time up to 6 months postpartum. Counseling also included practical demonstrations on how to use a cup for giving replacement feeds and workshops on preparing complementary feeds. Women were offered free formula for 9 months starting from the time that they stopped breast-feeding. There was no support offered in the postnatal wards to help initiate breast-feeding or to sustain EBF in the first days, nor was there specific counseling at the antenatal clinics preparing women for initiating and sustaining EBF. One-week recall of infant feeding and morbidity data was collected at each study visit (weekly for the first 6 weeks, monthly until 12 months and 3-monthly until 2 years). Forty percent of women planned to breast-feed, and on day 2 postnatally half EBF. However, within the first 48 hours after delivery, >40% of mothers had already introduced additional fluids (other than formula). None of the mothers who had introduced fluids only in the first 48 hours (i.e., predominant BF [PBF] had reverted to EBF to 3 months. Mothers reported that stopping breast-feeding at 3 months was difficult, but counselors reported fewer difficulties from mothers who ceased breast-feeding when the child was older, about 6 months.
The only study to be performed in a rural area is in KwaZulu Natal, South Africa, where a large nonrandomized community-based intervention study has been implemented to estimate the transmission risk with EBF. 9 HIV-positive women are counseled on infant feeding options but no formula or other financial or material support is offered regardless of preferred feeding intention. Women who plan to breast-feed are intensively supported antenatally, at delivery, and postnatally to EBF. The community-based support is matched by general support for EBF in the health facilities and local district hospital, which is accredited with the Baby Friendly Hospital Initiative (BFHI). In the district, between 40–60% of households use river water, and up to a third of households in certain tribal areas have no form of toilet, even pit latrines. In the past 5 years there have been outbreaks of Shigella dysenteriae type 1 dysentery and cholera. In contrast to some other approaches for counseling on infant feeding choices, not all infant feeding options are presented by the counselor. Rather the counselor explores with the HIV-positive woman how she intends to feed her child now that she has learned her HIV status. After discussing her personal circumstances and considering the feasibility of her intention, the counselor either fully supports the intention or sensitively challenges the women if her conditions do not appear appropriate with her intention or if a better opportunity is available. This approach reflects the WHO/UNICEF/UNAIDS recommendation that HIV-infected women should be given “specific guidance in selecting the option most likely to be suitable for their situation.”
Of 189 HIV-infected women counseled, 90% planned to breast-feed and 10% intended to formula feed. There were no differences between the breast-feeding and formula feeding groups with respect to access to clean water (about 50%); access to a refrigerator (about 40%); gas, paraffin, or electricity as a fuel source (about 65%); and a regular source of income to the household (about 75%). Only if the woman herself was the main income provider was this associated with the intention to formula feed (9 vs. 28%). Access to some or all of these conditions, which reflect issues of safety, affordability, and sustainability of RF, was not associated with either feeding intention (Table 3). Most women who had immediate access to conditions that would enable making replacement feeding safer in fact chose to breast-feed, suggesting that women's choices were based on issues other than physical resources. Notably, two-thirds of women who antenatally planned to replacement feed instead initiated and sustained breast-feeding after delivery, whereas all women who planned to breast-feed managed to do so through at least the first week. HIV counselors reported that women were very receptive to information and support regarding good breast-feeding practices but commented that it was hard to counsel women knowing that they are hungry. Not unexpectedly they found that family concerns significantly influenced women's decisions and practices. Interim data suggest that breast pathologies were uncommon but oral thrush was common during the first months of life in breast-fed infants.
The Zambian exclusive breast-feeding study (ZEBS) in Lusaka, Zambia is an randomized clinical trial to test the safety and efficacy of short, exclusive breast-feeding to 4 months to reduce HIV transmission and child mortality, enrolling 1200 infected pregnant women who wished to breast-feed. 10,11 A counseling intervention was developed to support and encourage exclusive breast-feeding to at least 4 months among all women in the study. Counseling begins antenatally, breast-feeding initiation is supported by midwives after delivery, and postnatal counseling includes both a home- and clinic-based component. Women randomly allocated to abrupt cessation of all breast-feeding at 4 months receive an additional counseling intervention to prepare them for early cessation. Possible problems associated with breast-feeding cessation are discussed, including strategies to relieve breast engorgement and comfort the child without suckling. Cup feeding is introduced and nutritional guidance is offered. Women randomly allocated to the early cessation group are given infant formula and a fortified cereal for at least 3 months, as part of the study intervention. The study will monitor the risk of HIV infection and serious morbidity and mortality and aims to quantify the risk of HIV transmission through exclusive breast-feeding and the magnitude of reduction of postnatal transmission associated with early cessation at 4 months.
Among the first 400 women enrolled in the study, >90% of all women initiated EBF. Between birth and 1 week, 92% of women reported breast-feeding only in the complete absence of any other liquid or semisolid. Between 1 week and 1 month, cross-sectional recall of feeding indicated EBF was 95%; between 1 and 2 months, 96%; between 2 and 3 months, 92%; and between 3 and 4 months, 86%. Most reports of non-EBF were single instances of water or other supplements and many mothers reverted to EBF thereafter. Among the mothers randomly assigned to abrupt early cessation of breast-feeding at 4 months, 80% stopped all breast-feeding. Most women who stopped breast-feeding did so within a week (<2 days: 50%; 2–7 days: 42%), with 8% stopping within 2 weeks. There preliminary results suggest that exclusive breast-feeding may be a feasible intervention that can be achieved among the majority of HIV-infected women with appropriate counseling. Early and abrupt cessation also appears to be feasible with counseling and provision of infant formula and weaning foods. However, the efficacy and safety are still unknown. Early data suggest that compared with those who continued breast-feeding for longer, mothers and infants who stopped breast-feeding at 4 months were more likely to visit clinics and health workers, incurred a significantly greater number of diarrheal episodes, and had lower weights.
The ZVITAMBO study in Harare, Zimbabwe was a randomized trial to investigate the effect of vitamin A supplementation on maternal and infant health, recruiting 14,110 mother–infant pairs during the immediate postpartum period. At recruitment, 4496 (32%) of mothers were HIV infected. Detailed infant feeding and morbidity data were routinely collected and blood samples obtained at 6 weeks, 3 months, and then at 3-monthly intervals over a 2-year follow-up. All but 4 of the 14,110 mothers initiated breast feeding. During the course of the study, an education and counseling program on safer breast-feeding was introduced for the last 2744 women enrolled. Using the definition of. cumulative practice from birth (rather than less rigorous definitions of 24-hour or 1-week histories), EBF rates increased from 7 to 28% at 6 weeks of age and from 3 to 19% at 3 months of age, for the pre- and posteducation and counseling intervention cohorts, respectively. This illustrates that breast-feeding practices are amenable to change if an effective and committed approach is implemented and sustained. Similarly, in Zimbabwe when replacement feeds are given, cups are normally used rather bottles, which has been the government recommendation for many years. Among infants born to HIV-positive mothers, infant mortality was more than 3-fold greater (P < 0.01) among infants who were MBF by 3 months of age compared with those who were EBF to at least 3 months of age.
In summary, EBF is an acceptable and feasible feeding option for many HIV-positive women, especially where practical support is available. Early introduction of water is common in many communities and achieving EBF beyond the first months can be difficult if only limited support is offered. Avoiding the introduction of additional formula feeding rather than just other fluids, e.g., water, is more acceptable and easier to achieve. Moderate facility-based or community-based support both antenatally and around delivery can significantly increase EBF rates. Obvious determinants of practice such as physical resources at home are not always the principal basis of choice or practice. Women's status in many societies often prevents them from making and exercising choices. Counseling approaches need to effectively guide women to informed choices with support available to make these choices viable and sustainable. Further investigation is needed of methods to increase community acceptability of feeding interventions to reduce HIV transmission and increase child survival.
PREVENTING/TREATING BREAST PATHOLOGY AND INFANT THRUSH
Breast pathologies, whether clinical or subclinical, are described among the risk factors for postnatal transmission, although their effect at a population level remains to be quantified (see John-Stewart et al., p. 196 in this issue). Simple interventions to improve breast-feeding practices and thereby decrease these risks are attractive methods to make breast-feeding safer. The South African and Zambian studies described here will better quantify the transmission risks of various breast pathologies, but there are again few data that have been systematically and rigorously collected in operational settings. It is expected that improved lactation counseling, which lies at the heart of interventions to promote exclusive breast-feeding, should reduce breast pathology, but this remains to be demonstrated in the ongoing trials and studies.
In Cato Manor clinic, a government clinic serving a large urban population in an informal settlement in Durban, HIV counselors have also been trained in the WHO Breast-feeding Counseling Course and can competently describe the common breast pathologies. After HIV-positive mothers have decided how they plan to feed their child (following counseling), HIV counselors meet with them at least once more to prepare them for feeding in the first week postnatally. For mothers who have chosen to breast-feed this includes early initiation of breast-feeding, correct positioning and attachment, frequent feeding and exclusive breast-feeding, how to cope with sore nipples, and expressing breastmilk to avoid engorgement. If the opportunity presents at subsequent antenatal visits, the counselor will also discuss nutritional support for the mother and good food choices. To date, 288 women have enrolled in the PMTCT program since March 1999. Six-month follow-up data are available on 179 mother–infant pairs in which the mother has chosen to breast-feed. Cracked nipples were experienced by 12% of mothers (similar to the 11–13% rate quoted by Embree et al. 12). This was usually in the first month of life and was rarely associated with bleeding. Breast-feeding counselors, either the HIV counselor or another dedicated breast-feeding counselor, would recommend applying pure lanolin ointment or breastmilk to the affected nipple. In addition, the counselor advises the mother to expose the breast to sunlight whenever she can. If the infant has oral thrush or if nipple candida is suspected then nystatin ointment is also recommended. The mother is advised to continue feeding from the breast unless there is obvious bleeding. Mastitis was diagnosed in only 2% of mothers (compared with 7–11% in Nairobi 12). Management of mastitis included using warm cloths to ease engorgement, expressing and discarding breastmilk from the affected breast while continuing feeding from the unaffected breast, and giving the mother antibiotics. Infant thrush was seen commonly; 39% infants were diagnosed with oral thrush on at least one occasion in the first 6 months. They were treated with oral nystatin drops. No data are yet available on the HIV status of these infants.
BREAST MILK TREATMENT
HIV is heat sensitive and is inactivated by pasteurization at temperatures between 56 and 62°C. 13 Breastmilk banks in developed countries use expensive, thermostatically controlled, pasteurizing equipment that is not available in resource-poor settings. A low-cost, low-tech method, the Pretoria pasteurization method, makes use of passive heat transfer from water that has been heated to boiling point, to milk that is contained in a glass jar standing in the water. The woman expresses her milk into a clean glass peanut butter jar, which is then placed into a 1-L aluminium cooking pot. Water is boiled by any methods and when boiling vigorously, the hot water is poured into the cooking pot in which the jar of milk is standing. The jar and milk are left to stand in the hot water until the water is a comfortable temperature, approximately 25 minutes. The final temperature reached by the milk and the duration for which it remains at that temperature are dependent on the volume of boiling water and the sizes and materials of the milk and water containers. Using water at boiling point has the advantage that it can be achieved every time without the need for a thermometer or thermostat. Several sets of apparatus were investigated and the glass jar and aluminium pot were found to provide the best results. The desired temperature range is between 56 and 62°C as this will maintain a large proportion of the secretory IgA within the milk. 14 The method was tested and found to be reliable under a wide range of conditions. 15
The Pretoria pasteurization method has been shown to reliably inactivate HIV in the milk of HIV-infected women, as well as in high-titer cell-free and cell-associated virus inoculated into human milk. 16 The method was implemented at Kalafong Hospital, South Africa, at the end 2001 for feeding preterm infants born to HIV-infected mothers, who found the method acceptable and easy to perform. By August 2002, 38 infants had been followed to ≥3 months of age. The mean birth weight in this group was 1488 g (± 490 g). Two infants died, the first of whom was discharged at 6 weeks of age in a satisfactory condition, but at this time the mother elected to change to formula feeding and the infant died of diarrhea 6 weeks later; the second infant had a birth weight of 1100 g and died on day 5 from complications of severe prematurity. All 36 other infants had satisfactory weight gain and were discharged from hospital. After leaving hospital, 20 mothers claimed to have continued with the Pretoria pasteurization. Others indicated that they had stopped using the method because of the fear of disclosing their HIV status to family or community members. Others were influenced by family members to use more traditionally acceptable feeding methods. The introduction of Pretoria pasteurization into the neonatal unit obviated placing at least 25% of the infants onto formula feeds and was associated with a reduction in the number of cases of necrotizing enterocolitis from 11 in the preceding year to 3 in the 11 months following the introduction of the Pretoria method.
Heat-treated expressed breastmilk (HTEBM) has also been recommended and supported at the Cato Manor site in Durban. It was poorly accepted by mothers; only 6% ever gave HTEBM in the first 6 months, who commented that it was only a viable option from 6 months of age. Counselors were surprised at the low uptake of HTEBM and discussed reasons for this with the mothers. Some of the reasons put forward for low uptake were that there had been no official endorsement or media coverage of the method and that they felt that a reduced amount of milk would be expressed and therefore the baby would not be satisfied. Other mothers, who did not have the opportunity to see a demonstration or try it out under supervision, stated that they lacked confidence in the procedure. Some mothers were concerned about the possibility of stigmatization or associations being made in the community regarding of heat treatment and witchcraft; finally, and perhaps most practically, mothers found it too time consuming especially when formula is readily available as an alternative. In an effort to promote HTEBM, the Cato Manor team has produced a video on breast-feeding with a section on heat treatment. A separate room for nutrition counseling and demonstrating heat treatment has been set up. Finally, the counselors are encouraging mothers to express and heat treat breastmilk from early on so that it becomes a normal practice.
In summary, correctly applied HTEBM can reliably inactivate HIV within the milk. It is easy to implement for motivated women but avoidance of suckling the infant and contending with family and community pressures are serious considerations for success. Pretoria pasteurization is a useful method for feeding preterm infants born to HIV-infected mothers in an institutional setting but its use in a domestic setting and for term infants requires further investigation. It may have a valuable role as an alternative to exclusive breast-feeding during times of increased risk, such as mastitis and cracked or bleeding nipples.
The experience from these studies suggests that both EFF and EBF are acceptable and feasible options to HIV-positive women to reduce MTCT of HIV. The decision-making process and the ability to achieve these depend on the personal motivation of HIV-infected women, the support of partners and close family, and the practical support of health care staff. Programs that promote EBF in populations where HIV is not a major problem clearly demonstrate the feasibility of achieving high EBF rates especially for the first months of life; the BFHI has been able to mobilize the enthusiasm and commitment of all sectors of communities to support EBF. In Nigeria, communities have been designated “Baby Friendly” by national BFHI committees because of the practical support they offer to enable women to EBF. This experience should be exploited in communities where EBF is likely to be widely adopted by HIV-positive women. Similarly the widespread use of cups to feed small babies in Zimbabwe illustrates how community practices can be changed when the political commitment is given to such health initiatives. Greater understanding is needed of the support that is needed by women who choose EFF to avoid mixed feeding.
It is not clear at present whether there are differential risks associated with different types of non-EBF, i.e., predominant vs. partial vs. mixed breast-feeding. The mortality data from the Zvitambo study suggest that this may be the case but the HIV transmission data for these children are not yet available. Operational experience suggests that it is possible to avoid mixing of BF with other nonhuman milk but that social pressures often result in mothers adding at least other fluids or foods. It is unlikely that, if EBF is protective, it will be an all-or-nothing phenomenon, and the addition of water may carry a different risk from the addition of more complex proteins and foods such as formula or other nonhuman milk. Even if antiretroviral prophylaxis to mother or infant in the breast-feeding period (see Gaillard et al., p. 178 in this issue) is shown to significantly reduce the risk of transmission through breast-feeding, this is unlikely to become widely available quickly. Reliable knowledge about other approaches on how to make breast-feeding safer for HIV-infected women is thus not only of scientific interest but also of public health importance.
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