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,3
* Johns Hopkins University, Pune, India;
Johns Hopkins University, Bloomberg School of Public Health, Baltimore, MD;
** BJ Medical College/Sassoon Hospital, Pune, India;
Department of Medical Education and Research, Government of Maharashtra, Mumbai, India; and

Johns Hopkins University, School of Medicine, Baltimore, MD
3To whom correspondence should be addressed at Johns Hopkins University, Bloomberg School of Public Health, 615 N. Wolfe St., Rm 8132, Baltimore, MD 21205. E-mail: avshanka{at}jhsph.edu.
| ABSTRACT |
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KEY WORDS: HIV infant feeding top milk breast-feeding India
According to the Joint United Nations Programme on HIV/acquired immunodeficiency virus (AIDS) estimates, India has > 1.3 million HIV-infected women of child-bearing age (1 ) and 160,000 infected children (aged 015 y) (1 ,2 ). Transmission of HIV infection from mother to child is responsible for nearly all pediatric HIV cases and contributes to 2% of all HIV cases in India (3 ). Dunn and colleagues (4 ) estimated that the proportion of transmission attributable to breast-feeding from a mother with established infection (i.e., antibody positive before pregnancy) is 14% (95% confidence interval, 722%). With greater accessibility to antiretroviral drugs during delivery, breast-feeding is responsible for an increasingly large proportion of worldwide pediatric HIV infection.
Over the last several decades, the promotion of exclusive breast-feeding in resource-poor settings has played a critical role in improving child health by providing optimum nutrition and protection against common childhood infections (5 9 ). Unfortunately, knowledge of the risk of transmission of HIV from mother to child through breast-feeding has greatly complicated infant feeding recommendations. In areas in which adequate sanitary replacement feeding is not available, the decision to withhold breast-feeding may lead to increased rates of child morbidity and mortality from diarrhea, respiratory diseases and malnutrition. Models based on studies in developing countries suggest that infant mortality from malnutrition and other infectious causes may exceed that from HIV (10 ). In light of this difficult dilemma, the Joint United Nations Program on HIV/AIDS together with WHO and UNICEF now recommends that women with HIV-infection in developing countries are informed about the risks of breast-milk HIV transmission. Nonbreast-fed children born to HIV+ women are at less risk of illness and death only if they can be ensured uninterrupted access to nutritionally adequate breast-milk substitutes that are safely prepared (2 ). Recent studies have emphasized the importance of exclusive feeding (either breast-milk or formula) by demonstrating the detrimental effect of mixed feeding (breast-milk with other milks) (11 ). These findings call for urgent action to educate, counsel and support HIV+ women in making decisions about how to nourish their infants safely.
There is a growing body of research on HIV in India, although the data on infant feeding and HIV transmission rates are still limited. Current rates of HIV in pregnant women in India based on sentinel surveillance are
2%. In large urban areas such as Pune and Mumbai, HIV/AIDS rates are on the order of 46% (3
). A study assessing womens awareness of HIV in Pune found that nearly 70% of these women demonstrated knowledge of maternal to child transmission routes; however, a very small percentage (8%) knew of any treatments to prevent mother to infant transmission (12
).
National efforts to identify and treat pregnant women with HIV/AIDS are growing in India. Prenatal HIV screening is now being offered on a limited scale in high risk areas and there is indication that acceptability of such testing will be high. Data from Pune indicate that >80% of eligible antenatal clinic patients accepted rapid HIV testing and were tested for HIV when offered (13 ). Moreover, the National AIDS Control Organization has made zidovudine and nevirapine available to pregnant woman and infants in many urban areas in an effort to reduce mother to infant transmission.
With the availability of such antiretroviral drugs, it is now necessary to focus attention on methods of reducing HIV transmission through breast-feeding. To date, there are no published data from India that examine infant feeding choices of HIV+ mothers. This study examined feeding intention and practices of counseled HIV+ mothers attending a large urban hospital in Maharashtra. Various factors that influenced these womens decisions concerning infant feeding are presented.
| SUBJECTS AND METHODS |
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60% of women tested returned for their results. To obtain a sample that was representative of all women attending the ANC during the study period, data were collected every 3 d, thereby giving every clinic day equal coverage. We obtained data from all newly registered women who were eligible and consented to be interviewed. Women were eligible for the study if they were between 18 and 44 y old, over 28 wk gestation, identified as either HIV positive or HIV negative by ELISA (Labsystems Oy, Helsinki, Finland) and were mentally and physically healthy enough to participate in the study (as assessed by a doctor).
HIV+ pregnant women (n = 101) were recruited from December 2000 to April 2002; none of the women refused to participate in the study. All women attending the ANC on study enrollment days whose report indicated that they tested HIV+ were invited to participate and consented to three interviews as part of this study. None of the women who were approached refused to participate. Each of the women had completed HIV education and counseling, provided consent and were tested for HIV
2 wk before enrollment. On this visit, these women had already completed intensive post-test counseling. All of the counseling sessions stressed the risks and benefits of feeding choices in the context of HIV. Emphasis was placed on the dangers of mixed feeding methods.
The first short structured interview was administered in the ANC to assess the womens intended infant feeding plan. The second semistructured interview on infant feeding was conducted at the postpartum ward, within 72 h after delivery, to observe women feeding and to ask them about feeding initiation. This interview included a series of structured and open-ended questions related to their feeding decision, disclosure of their HIV serostatus and household environment. The third semistructured interview was conducted in the postnatal clinic to assess infant feeding patterns after these women had returned home, usually taking place 2 wk to 1.5 mo postpartum. The topics covered in these interviews included infant feeding plan, sociodemographic information, persons involved in deciding the feeding option, consumption of items before breast-feeding and along with breast-feeding, reasons for change in infant feeding plan and test report disclosure to husband, in-laws and parents. Postpartum changes in infant feeding choice were noted and accounts of the reason for the change were documented. All interview schedules were pretested before use. All interviews were conducted in the local language of the respondent, either Marathi or Hindi. The 101 HIV+ women in our sample represented 30% of the total HIV+ women identified by serum ELISA at this hospital during this period.
Of the sample of 101 HIV-infected mothers, the last 39 eligible women who provided consent were interviewed further (using a semistructured questionnaire) to obtain additional data on decision making including the womans level of understanding of post-test counseling content, the husbands, in-laws and parents level of understanding of risk of HIV transmission through breast-milk and factors affecting HIV status discloser.
Of the 101 total HIV-infected women, 94 delivered at the hospital. Of those delivering, 20 did not come to the postnatal clinic for follow-up and 1 infant died within 1 wk of birth. It is likely that the majority of this loss to follow-up in the PNC was due either to social pressures preventing women from leaving the house with the child before 1.5 mo had passed or that the woman left the area to visit their natal home or their husbands home soon after birth. The 20 women not appearing for the PNC visit were equally divided between breast-feeders and top feeders. A total of 73 HIV-infected women completed all scheduled interviews.
We also interviewed a cohort of HIV negative women regarding their infant feeding intentions. All of the 24 HIV negative mothers indicated that they intended to breast-feed their baby and were observed to have initiated breast-feeding and continued to do so at the PNC visit. The decision to limit our data collection to only 24 women was based on the uniformity in intention and practice to breast-feed and the fact these women were more difficult to follow-up postdelivery.
The nature of the study was explained to all women and written informed consent was obtained. The study was approved by two ethics committees in Pune, India and one ethics committee at Johns Hopkins University in the United States, the Joint Committee on Clinical Investigations.
All interviews were conducted by a trained behavioral scientist, who had a graduate-level degree in the social sciences and had undergone 2 wk of additional interviewer training. For structured interview questions, bivariate comparisons relevant to the study questions were presented using nonparametric statistics such as
2 or Fishers exact test. Data analysis was conducted using SAS, version 9 (14
). All open-ended responses were coded by thematic category. Significant response patterns were identified by counting the number of instances a view was expressed, observing thematic patterns in responses to related questions and making connections among these data, the quantitative data collected and previous research (15
).
| RESULTS |
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Women attending this antenatal clinic chose either breast-feeding or top feeding with top milk for their infants. For the 101 HIV+ women, after having gone through group education and counseling as well as the more intensive post-test counseling, an equal number stated their intention (prepartum) to breast-feed (n = 44, 44%) and top feed (n = 44, 44%), leaving 13 (12%) women undecided. The general demographic characteristics of the HIV+ women are presented in Table 1. We found no differences in demographic characteristics between women intending to breast-feed or top feed. However, mothers who preferred top feeding tended to be primiparous (P = 0.1) and more likely to disclose their test results to their in-laws and parents (P = 0.1). This lack of significant differences may be due to the small study sample size. Nearly three fourths of the women disclosed their HIV status to their husbands.
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Feeding initiation.
Actual feeding practice was evaluated for 94 women and was compared with their original feeding intention. Of those who chose to breast-feed (n = 56, 60% of total), the majority did so because it was suggested by the counselor (n = 17, 30%) or because they could not afford top milk (n = 20, 35%). A substantial percentage of women (n = 14, 25%) were concerned about the social repercussions if they did not breast-feed, whereas 8 (14%) stated they could not ensure hygienic food preparation. Of those women who chose top feeding (n = 38, 40% of total), the overwhelming majority did so to prevent passing HIV to their newborn (n = 32, 87%). Seven women (20%) relied on the doctors information in making their decision.
Changes in infant feeding from intention to practice.
Of the 94 delivered women who had decided on a specific infant feeding strategy (n = 84), 16 (19%) decided to change their infant feeding plan from their original intention. Of the undecided women, 80% (n = 10) chose to breast-feed, whereas the remaining two (20%) chose to top feed. More women changed their decision immediately after delivery (n = 10, 63%) than in the hospital postpartum (n = 6, 47%). None of the women appeared to change their decision after returning home.
The primary reason mothers intending to top feed changed their decision postpartum was because they could not afford top milk (n = 6, 60%). Family pressure was mentioned in only one case and doctors advice was important in two instances. For breast-feeding mothers, doctors were important in affecting the womans decision (n = 3, 50%). In two of the six cases (33%), the woman decided on her own not to take the risk of passing HIV to her child.
The family support in the household clearly affects the womans decision to continue with her intended feeding plan. In the case of a woman who decided to breast-feed, she noted,
"As soon as my in-laws came to know about my and my husbands report they asked us to leave the house. We are now staying separately (from my in-laws). My husband is not working. I dont know how I am going to bring up my child."
This is in contrast to a top-feeding mother who stated,
"He is a baby boy and the first child so my mother in-law came to know about my report and my husbands report. My mother-in-law takes care of my baby, the baby sleeps with her. She feeds him ... She always accompanies me to hospital."
Mixed feeding.
In this study, mixed feeding for women who primarily breast-feed is defined as giving breast-milk as well as other nonbreast-milk foods. Mixed feeding for women who primarily top feed is defined as giving breast-milk to supplement the top feeds. In our sample, 24 or 43% of breast-feeding HIV-infected mothers mix fed their infants foods such as honey, water or sugar water during their postpartum stay in the hospital. This contrasts with the 11% (n = 4) of the mothers who top fed and also gave breast-milk (
2 = 11, P < 0.001). We found two distinct types of mixed feeding in this population: 1) the giving of some liquids and foods to the child during the first 3 d after birth only, and 2) the giving of mixed feeds to the child regularly for > 3 d. In our sample, 28 (74%) of mothers were classified as mixed feeders for 3 d only, with the remaining 10 (26%) mixed fed on a more regular basis.
Mixed feeding that occurred during the first 3 d after delivery usually occurred on the advice of doctors and relatives and was related to the mothers inability to produce sufficient milk for the child, c-section discomfort and problems of feeding top milk during the night. Women who mix fed > 3 d fed their child using only one type of milk (either breast-milk or top milk) but in addition regularly gave locally available gripe water and herbal preparations thought to promote infant growth (see quotes below).
"I started breast-feeding because my husband has lost his job. Even the doctor told me to breast-feed for 4 mo. I give plain water, sugar water and herbal preparation, along with breast-milk."
"My sister-in-law forced me to breast-feed to my baby. So under her pressure I breast-fed my baby for 3 d, 3 times-every day for 15 min. Nobody at our home knows about my HIV status."
"My child used to cry during night, so my husband suggested to breast-feed during the night and top feed during the day."
Subsample study.
Of the 101 women originally interviewed, 41 HIV+ women were eligible and consented to additional interviews. Of the 41 HIV+ women, 1 child was stillborn and 1 was a home delivery, leaving 39 women who completed the antenatal, delivery and in hospital postpartum visits. Of this sample, a greater proportion of women decided to breast-feed (56%, n = 22,) as opposed to top feed (36%, n = 14). However, other demographic characteristics of this sample were similar to those of the larger sample. Infant feeding intention was most influenced by the counselor (n = 21, 54%); 31 (28%) relied on themselves and 6 (15%) on the doctors advice.
Most women disclosed their HIV status to their husbands (n = 27, 69%). However, regardless of whether they told their spouse, they were less likely to discuss their results with their in-laws or parents (n = 12, 31%). Top feeding mothers were significantly more likely to disclose their HIV status to their husbands and relatives than breast-feeding mothers [n = 12 (85%) top feeding compared with n = 12 (54%) breast-feeding mothers (P < 0.05)]. For those 12 (31%) women who did not tell their spouse, six (50%) did so out of fear. In-laws were less frequently told, either out of concern for them (n = 9, 33%) or because of fear of blame (n = 8, 30%). Parents, on the other hand, were not told so as prevent any tension or pain to them.
If the women revealed their HIV status to a family member, they were very likely to seek their advice on feeding methods. However, the most influential individual in helping them make the final feeding choice (multiple responses allowed) was the counselor (n = 29, 74%), followed by themselves (n = 21, 54%) and their husbands (n = 10, 26%). After delivery, it was mainly the counselor who spoke with the women about infant feeding practice (n = 21, 54%); 11 women (28%) received no guidance after delivery, 6 (15%) spoke with husbands and 5 (13%) spoke with a doctor.
All of the breast-feeding women knew of the risks of HIV transmission, but they chose not to top feed because they could not afford top milk (n = 9, 41%) or to prevent family suspicion that they were ill (n = 6, 27%). The majority of top feeding mothers knew about proper precautions to ensure hygienic conditions. However, only one of the mothers was aware of any health-related problems that could occur with top feeding.
Consistent with findings from the larger sample, 20% (n = 8) of these women changed their infant feeding practice from what they initially intended. Half had initially planned to breast-feed, the other planned to top feed. Reasons for change included lack of funds to buy milk (n = 3, 38%), suggestions from counselors or doctors (n = 3, 38%), or problems associated with feeding (n = 2, 25%). When asked who advised the woman to change her intended feeding plan, the majority reported that it was their own decision (n = 4, 50%) or that of a family member (n = 3, 38%). In only one case did the doctor suggest that they change their feeding plan from breast-feeding to top feeding.
| DISCUSSION |
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Unfortunately, we do not have complete data on infant feeding patterns of HIV negative women attending this clinic, a limitation of this study. However, we can glean some insights from other research. Data from the most recent Family Health Survey in India indicate that very few children are put to breast immediately after birth; only 16% of children breast-fed within 1 h of birth, and only 37% began breast-feeding within 1 d (20 ). Moreover, 55% of children < 4 mo of age are exclusively breast-fed, 23% receive breast-milk plus water, and 20% receive supplements along with breast-milk (20 ). We found very similar rates of mixed feeding (43%) in our sample of breast-feeding HIV+ mothers. However, mothers who top feed were significantly less likely to mix feed (11%). The difference in rates reflects the high rate of mixed feeding for breast-feeding mothers during the first 3 d after birth when breast-milk production may be low and usually under the guidance of a nurse or physician.
According to the WHO guidelines (21 ), the inclusion of any feeding in addition to breast-milk into the diet (with the exclusion of medicines) constitutes mixed feeding. Further investigations are warranted to document the relative effect of these distinct types of mixed feeding on HIV transmission. Because the "3-d" mixed feeding is the most common mixed feeding pattern, it is critical that the counselors and physicians be provided with the most up-to-date information on its effect so as to give the most accurate recommendations to their patients. Of those women who changed their mind, the majority were more likely to do so immediately after delivery, either due to doctors or family members advise. It is, therefore, a critical point in time for recounseling about infant feeding and providing support for the womens feeding decision to avoid any mixed feeding. Until these data are available, mixed feeding of any kind should be discouraged.
Due to the small study sample size, we should be cautious in our interpretation of the results. However, there are certain trends that are of interest. As evidenced by the high rates of HIV status disclosure in this sample, these women appear to have greater familial support for their condition than that found in other areas of the world (22 ,23 ). Moreover, our rates of HIV+ mothers choosing to feed breast-milk substitutes appeared higher than reported in other regions of South India (50 vs. 22%) (24 ). This may be due in part to the effect of the intense counseling of these patients, or the economic condition of this sample could be higher. Our qualitative data indicate that women who fed their child breast-milk substitutes had greater support from their husbands and extended family than women who chose to breast-feed. Moreover, top feeding mothers expressed far less concern about social repercussions than breast-feeding mothers.
Although the level of familial support to obtain nonbreast-milk substitutes is encouraging, access to safe infant formula feeding in India is rare. For the majority of families in India, the cost of infant formula is prohibitive. As a result, the standard replacement food advised and given to infants in this region is diluted animal milks (such as cow, buffalo or goat) plus sugar. In our review of the literature, we could not find any direct reference in medical textbooks or journals recommending top milk use for infants, nor did we find the scientific justification for such a recommendation. Only a few published studies have documented the prevalence of top milk consumption and some of its negative effects on infant health (25 ,26 ). In a recent study conducted in this hospital, there is evidence that the consumption of top milk can lead to greater morbidity, hospitalization and death for infants compared with breast-feeding (27 ).
As a result of these most recent hospitalization data, both physicians and counselors have modified their counseling to more clearly describe the benefits and risks of top feeding at this hospital. This may explain in part the greater shift to breast-feeding in the subsample of women who were interviewed later in the study [n = 44 (44%) in the earlier data compared with 22 (56%) in the substudy data (
2 = 12.5, P < 0.01]. This shift also demonstrates the effect of counselors and other hospital staff on the womens feeding choices.
Perhaps the most pressing question to be addressed is the promotion of top milk. Future research to address the nutritional value and safety of the available top milk in this region is warranted. Without proper safety data on top milk, it is not advisable to recommend this feeding option to women with HIV. Given the lack of hygienic conditions, the risk of social repercussions and in the absence of available safe infant formula, breast-feeding should be promoted for HIV+ women in this population. In the absence of available safe infant formula, interventions that reduce the risk of HIV transmission while also preserving the benefits of breast-feeding are necessary in settings such as India. An important issue that should be addressed in future research is how well HIV+ mothers in India follow the recommendation to wean within 46 mo to prevent HIV transmission to their child. With continued research to identify methods to reduce mother to infant transmission we hope that we can obtain further reductions in HIV transmission without placing the child at greater risk of morbidity and mortality from other causes.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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2 Supported by a grant from the U.S. National Institutes of Health (NIH, NIAID) (R01 AI45 462) and undertaken in collaboration with BJ Medical College (BJMC) in India. ![]()
4 Mixed feeding is defined here as the consumption of other nonbreast-milk products (e.g., infant formula, other animal milk or water) in conjunction with breastfeeding. ![]()
5 Top feeding refers to an infant feeding practice that includes top milk, the term used in India to describe diluted animal milk (either buffalo, cow or goat mixed with water and often a small amount of sugar) intended as a food for neonates and infants. ![]()
6 Gripe water is a commonly available store-bought tonic consisting of ginger, fennel, sodium bicarbonate, fructose and water. ![]()
Manuscript received 29 September 2002. Initial review completed 25 October 2002. Revision accepted 24 January 2003.
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