Becquet, Renaud MPH*; Ekouevi, Didier K MD, PhD†; Viho, Ida MD†; Sakarovitch, Charlotte MSc*; Toure, Hassan MD†; Castetbon, Katia PhD‡; Coulibaly, Nacoumba MD†; Timite-Konan, Marguerite MD§; Bequet, Laurence MD†; Dabis, François MD, PhD*; Leroy, Valériane MD, PhD*
Mother-to-child transmission (MTCT) of HIV-1 (HIV) is responsible for most of the acquisition of pediatric HIV infections. Each day in the world, 2200 children become infected with HIV, 90% of them in sub-Saharan Africa, where MTCT of HIV is an increasing public health problem.1 MTCT of HIV can occur in utero, during delivery, or through breast-feeding. In settings where prolonged breast-feeding is the norm, breast milk transmission is responsible for one third to 40% of perinatally acquired HIV infections.2 The overall risk of postnatal transmission was estimated to be 8.9 new cases per 100 child-years of breast-feeding (95% confidence interval [CI]: 7.8-10.2) in a recent pooled analysis.3
The efficacy of short-course antiretroviral regimens to prevent HIV transmission around the time of delivery has been demonstrated in industrialized countries and in sub-Saharan Africa.4,5 Nevertheless, in the absence of targeted intervention, the subsequent risk of postnatal transmission of HIV considerably reduces the long-term efficacy of peripartum antiretroviral prophylaxis.6 In addition to antiretroviral-based interventions to reduce the risk of postnatal HIV transmission,7 different nutritional approaches are conceivable in modifying infant feeding practices, such as complete avoidance of breast-feeding in urban settings or shortening the breast-feeding period.8 Indeed, in areas where breast-feeding is usually prolonged until at least 12 months of age, this latter approach should reduce the cumulative risk of postnatal transmission while retaining the benefits of breast-feeding during the first months of life. Moreover, there is some observational evidence that exclusive breast-feeding carries a lower postnatal risk of transmission of HIV than breast-feeding with introduction of other fluids, feeds, or milk.9-11 Indeed, contaminants or bacteria contained in these additional feeds may damage the infant's gut, impair mucosal integrity, and thus facilitate postnatal transmission of HIV.12,13 Thus, the combined promotion of exclusivity of breast-feeding with early cessation may substantially reduce breast milk HIV transmission.
The evaluation of such postnatal nutritional interventions aimed at the prevention of mother-to-child transmission of HIV (PMTCT) must be based on several judgment criteria, beginning with the uptake of the intervention proposed, which can be itself divided into its prenatal acceptability and the long-term compliance.
The objective of this study was to assess the uptake of an infant feeding strategy in an urban West African setting based on the promotion of exclusive breast-feeding with early cessation between 3 and 4 months of age in a cohort of HIV-infected women.
SUBJECTS AND METHODS
The ANRS 1201/1202 Ditrame Plus study was granted ethical permission in Côte d'Ivoire from the Ethical Committee of the National AIDS Control Program and in France from the Institutional Review Board of the French Agence Nationale de Recherches sur le SIDA (ANRS).
The ANRS 1201/1202 Ditrame Plus study was conducted in Abidjan, the economic capital of Côte d'Ivoire (3 million inhabitants). In this setting, municipal water of good quality was widely available but household water storage was a common practice that may contribute to the contamination of drinking water.14
The study population was recruited in Abobo and Yopougon, the 2 most densely populated districts of Abidjan. HIV counseling and testing services were set up within the University Hospital of Yopougon and the antenatal clinics of 6 preexisting community-run health facilities.
From March 2001 to March 2003, any pregnant woman aged at least 18 years attending one of the selected prenatal clinics and living within the limits of Abidjan was offered pretest counseling and HIV testing.15 Those women who tested positive were offered the opportunity to enter the study from 32 weeks of gestation after having had the objectives of the study explained to them, having accepted the study protocol, and having signed an informed consent form.16
Within this open-labeled cohort, women received a short peripartum drug combination of zidovudine ± lamivudine and nevirapine in a single dose.17 Postpartum nutritional interventions were systematically proposed for women who delivered a live baby.
At inclusion, pregnant women were informed about the modalities of postnatal transmission of HIV during a 30 minute face-to-face counseling session and were told that alternatives to prolonged and predominant breast-feeding may prevent this risk. The advantages of these interventions (ie, reduction of the risk of HIV transmission through breast milk) and their disadvantages (ie, possible stigmatization and potential risks for infant health) were fully discussed with the participants.
Two nutritional interventions were then hierarchically and systematically proposed to the women and discussed again during subsequent weekly prenatal visits scheduled until delivery. The first option consisted of the complete avoidance of breast-feeding: artificial feeding from birth free of charge to 9 months of age with free provision of the material and using a single oral dose of cabergoline, whose efficacy to inhibit lactation in puerperal women has been demonstrated.18 The second option consisted of practicing exclusive breast-feeding with the aim of weaning after a short period (not exceeding 2 weeks) and obtaining complete cessation of breast-feeding between 3 and 4 months of age. Women were encouraged to cup-feed their infants when initiating weaning. Replacement feeding until 9 months of age as well as the material needed were provided free of charge. In all cases, the staff supported the choice expressed by the women and counseled them accordingly.
Two clinics were exclusively dedicated to the enrollment and follow-up of the mother-infant pairs. A total of 60 health care workers recruited from the local area were employed for this study.
From birth up to the second birthday of the child, 19 visits were scheduled for clinical, nutritional, psychosocial, and biologic follow-up of the mothers and infants. Mother-infant pairs were seen at birth, 48 hours after delivery, weekly until 6 weeks of age, monthly until 9 months of age, and every 3 months until the child's second birthday. Services dispensed by the study team were also available whenever needed between scheduled visits. All transport costs were reimbursed, and all care expenses related to any scheduled visit or clinical event were entirely supported by the project.
Four nutritionists individually counseled the women about infant feeding practices whenever needed. Collective sessions were frequently organized to help mothers correctly position their baby to the breast; reiterate the benefits of exclusive breast-feeding; and explain how to prepare artificial feeding safely, initiate weaning, use appropriate complementary feeding, or cook the baby food.
Diagnosis of Peripartum Pediatric HIV Infection
Pediatric blood samples collected at days 2 and at 4 and at 6 weeks of age were processed for plasma RNA viral load measurement by real-time polymerase chain reaction using the quantitative Taqman technology, allowing diagnosis of peripartum HIV infection.17,19
At each contact, the medical staff documented clinical events that occurred in mothers and children since the last visit. At each scheduled visit, infant feeding practices were recorded via structured questionnaires by trained social workers who were not involved in nutritional counseling. Women were asked if their child had been given breast milk, artificial milk, or both since the last visit. Fluids and foods other than breast milk or artificial milk were documented using a 24-hour and a 7-day recall history. Social workers went over a detailed list of 15 commonly used fluids or foods. Women were asked if these fluids, foods, or some other items not listed had been given in the previous 7 days, and if so, in what amount (24-hour recall history) and how frequently in the past 7 days. The first liquid given after birth was recorded at the day 2 visit.
Infants were classified at each scheduled visit as exclusively or predominantly breast-fed, mixed fed, or artificially fed using these recall histories.20 Being exclusively breast-fed from birth at a given time meant having been classified in this category at all the preceding visits since birth.
We used the following World Health Organization (WHO) definitions to allow a better comparison of results between studies. Exclusive breast-feeding means giving a child no other food or drink, including no water, in addition to breast-feeding, with the exception of medicines, vitamin drops or syrups, and mineral supplements.21 Predominant breast-feeding means breast-feeding a child but also giving small amounts of water or water-based drinks. Neither food-based fluid nor solid food is allowed under this definition.21 Artificial feeding means feeding a child artificial foods (including infant formula and powdered animal milk) and not breast-feeding at all.22 Mixed feeding means breast-feeding and also giving nonhuman milk such as infant formula, food-based fluid, or solid food.23 We defined a nutritional change as a switch from one of these categories to another and the weaning process as the period from the introduction of the first weaning food until complete cessation of breast-feeding.
Women whose live-born infants were breast-fed at least once were initially classified as breast-feeding at the day 2 visit and were included in the following analyses.
The prenatal infant feeding choice was described among women who initiated breast-feeding.
Infant feeding practices were presented in detail at 1, 3, 4, 6, and 9 months of age (M1, M3, M4, M6, and M9, respectively). For this purpose, we used a time-varying classification according to the liquids and foods consumed over the past 7 days before each of these visits, independently of what occurred before these visits.
The probability of being exclusively breast-fed from birth and the probabilities of initiating weaning and having completely ceased breast-feeding were estimated at given ages using the Kaplan-Meier technique.
We used 2 different definitions to investigate the proportion of women who successfully practiced the nutritional intervention proposed. First, we defined success as breast-feeding the infant exclusively from birth until the beginning of weaning and having completely ceased breast-feeding between M3 and M4 (definition 1). Second, we defined success as complete breast-feeding cessation occurring between M3 and M4, irrespective of the exclusivity of breast-feeding (definition 2). Because assessment of uptake was impossible among children who died or were lost to follow-up before the age of M4, although they were still being exclusively breast-fed (definition 1) or exclusively or predominantly breast-fed (definition 2) at their last contact, they were unclassified. Sensitivity analyses were performed to classify these cases as success or failure of the intervention proposed.
Baseline sociodemographic, clinical, and biologic maternal characteristics were compared between mothers who succeeded with the intervention and those who failed according to those 2 definitions of success.
Logistic regression was used to assess the determinants of complete cessation of breast-feeding occurring beyond the M3 to M4 period (failure). Multivariate analysis included maternal baseline sociodemographic, biologic, and clinical characteristics, and multivariate analysis included all variables with P < 0.25 in the univariate analysis.24
All statistical analyses were carried out with the use of SAS software (version 8.2; SAS Institute, Cary, NC).
Recruitment and Baseline Characteristics
As shown in Figure 1, 643 HIV-infected pregnant women were consecutively enrolled between March 2001 and March 2003. Sixty-three women with HIV-2 infection only or lost to follow-up before delivery were excluded from the analysis. Overall, 580 women gave birth, and after exclusion of stillbirth as well as second and third born babies of multiple birth outcomes, 569 mother-infant pairs were eligible for analysis. Among the 557 mothers whose live newborn was fed at least once, 262 (47%) initiated breast-feeding and constituted the breast-feeding group for the present analysis.
Their baseline sociodemographic, clinical, and biologic characteristics as well as the delivery circumstances and the characteristics of their newborns are detailed in Table 1. Overall, 47% of the women were illiterate and 70% were living with their partner, a quarter of whom had known their female partner's HIV status before delivery. All but 8 women had electricity at home, all had access to tap water, and 74% lived in shared housing. Three quarters of the women included were at WHO clinical stage 1 or 2, and the remaining women were at WHO clinical stage 3. Their baseline median CD4 count was 392 cells/μL (interquartile range [IQR]: 266-540 cells/μL), and their median viral load was 4.2 log (IQR: 3.6-4.7 log).
Mother-Infant Pairs Follow-Up
From birth until 9 months of age, among the 262 mother-infant pairs analyzed, 34 (13%) were lost to follow-up at a median age of 51 days (IQR: 7-133 days) and 12 (4%) infants died. Among the remaining 216 mother-infant pairs, 197 (91%) completed the 15 visits scheduled from birth until 9 months of age, with the others completing 11 visits on average.
Among the 262 women initiating breast-feeding, 255 (97%) made their choice during the prenatal period on how to feed their forthcoming infant. Of these women, 227 (89%) intended to breast-feed, of whom 84 (37%) decided that they would exclusively breast-feed. Among the 227 women wishing to breast-feed their infant, 4 (2%) considered ceasing breast-feeding before 3 months, 88 (39%) between 3 and 4 months, and 60 (26%) after 4 months; the remainder (33%) did not express an opinion antenatally.
Initial Infant Feeding Practice
In this breast-feeding group (n = 262), the first liquid given from birth was breast milk (73%), tap water (9%), boiled or mineral water (4%), sugar water (1%), infant formula (3%), or fruit juice (1%) and could not be documented for 9% of the women. Infant formula had been given by the staff of hospitals where women had been hospitalized for a cesarean section. In the first 48 hours of life, 160 (61%) children were predominantly breast-fed, 90 (34%) were exclusively breast-fed, and 12 (5%) were mixed fed.
Among the 84 mothers who had prenatally chosen to breast-feed their infant exclusively, 51% did so, and 75% of the 143 mothers who had prenatally chosen to breast-feed predominantly actually initiated this practice (P < 0.001).
Exclusivity of Breast-Feeding
As shown in Figure 2, at 1 and 3 months of age, most infants had not been exclusively but predominantly breast-fed the week before the interview (59% and 62%, respectively), because they were also given water, essentially from a tap. Use of boiled or mineral water was relatively common at 1 month of age (30%). Most of the infants (39%) were mixed fed at 4 months of age, of whom 83% were in the process of being weaned and were thus receiving infant formula. From 6 months of age, most of the infants were not breast-fed any more and received artificial feeding instead, whereas the remaining breast-fed infants were essentially mixed fed because they also received baby food and other solid or semisolid foods such as dairy products, meat, fish, or all sorts of plants.
The cumulative probabilities of being exclusively breast-fed from birth were 0.18 (95% CI: 0.13-0.22), 0.10 (95% CI: 0.06-0.13), and 0.01 (95% CI: 0-0.02) at ages M1, M3, and M6, respectively (Fig. 3).
Duration of Breast-Feeding
Overall, 167 mothers (64%) had completely ceased breast-feeding before M9; 38 infants (14%) died or were lost to follow-up before reaching that age, although they were still being breast-fed at their last contact; and 57 (22%) infants were still breast-fed at M9.
Overall, 24 women (9%) ceased breast-feeding before M3: 12 mothers were counseled by the medical and nutritional staff of the study to cease breast-feeding for maternal medical reasons (chickenpox, breast pathologic findings, and AIDS-related disease), disease of the child (candidiasis), or breast milk deficiency, and 12 mothers changed their minds and switched to feed their infant artifical foods. Altogether, 100 women (38%) completely ceased breast-feeding at M3 to M4 as recommended.
The cumulative probabilities of beginning the weaning process and having completely ceased breast-feeding are detailed in Figure 4. The median age of infants at initiation of the weaning process was 97 days (IQR: 91-125 days), and it was 106 days (IQR: 94-136 days) at complete cessation of breast-feeding. Complete cessation of breast-feeding was achieved for 94% of these infants after a single weaning endeavor. The weaning process was initiated with the introduction of infant formula to replace breast-feeding. At that time, 4% of the women preferred to be kept away from the child and 2% used bandages to cover their breasts. None of the women reported having used any repellent products to facilitate the weaning process. Women reported breast pain (33%), breast engorgement (18%), or baby tears (17%) related to the weaning process. Only 2% of the women reported partner or family disapproval of the early cessation of breast-feeding.
Success of the Intervention Proposed
Among the 262 mother-infant pairs who had initiated breast-feeding, 4 (1%) infants died or were lost to follow-up before M4, although they were still being exclusively breast-fed at their last contact. Only 14 (5%) mothers succeeded in practicing exclusive breast-feeding until weaning, having completely ceased breast-feeding between M3 and M4 as planned in the protocol on the quality of breast-feeding and its duration.
Women who failed to achieve this objective had fewer living children (median of 1 vs. 3; P = 0.01) and were at less advanced stages of HIV disease than those who succeeded (HIV-1 RNA plasma viral load of 4.2 vs. 4.6 log; P = 0.04).
We then considered the second less stringent definition of success. Among the 262 mother-infant pairs initiating breast-feeding, 33 (13%) infants died or were lost to follow-up before M3, although they were still being breast-fed at their last contact, irrespective of the exclusivity of the breast-feeding practice. Among the 229 mothers who could thus be classified, 24 (10%) ceased breast-feeding before M3, 100 (44%) between M3 and M4, and 105 (46%) after M4.
In an unadjusted analysis detailed in Table 1, being followed in the clinic based in the district of Abobo, living in typical shared housing, and having delivered at home were associated with failure of the proposed intervention. Women who failed to practice the recommended intervention also had a significantly higher CD4 count than those who succeeded.
The results of the multivariate logistic regression model investigating the determinants of complete cessation of breast-feeding occurring beyond the M3 to M4 period (n = 105 vs. n = 100) are detailed in Table 2. After adjustment, failure of the proposed intervention was significantly associated with being followed in the Abobo site, having a maternal CD4 count greater than 500 cells/μL, and living with partner's family. Similar results were obtained when investigating the determinants of complete cessation of breast-feeding after versus before M4 (ie, pooling together women who ceased breast-feeding before M3 and during the M3-M4 period).
This study investigated the uptake of a nutritional intervention aimed at preventing HIV transmission through breast milk in an urban African context. In this setting, where predominant and prolonged breast-feeding is widely practiced,6,25 HIV-infected women were given a proposal to feed their infants in an unusual way compared with common local practice, because it consisted of implementing both exclusive breast-feeding and early cessation of breast-feeding from 3 months of age. Overall, the uptake of this combined intervention was low, because only 5% of the women strictly fed their infant as planned by the study protocol in terms of exclusivity and duration of breast-feeding. Complete cessation of breast-feeding was obtained in 45% and 63% of the women at M4 and M6, respectively.
The Ditrame Plus study was conducted among all attendees of community-run health facilities located in poor areas, with no other selection criteria than being HIV infected, at least 18 years old, and having accepted the study protocol. As a result, half of the women included were illiterate and three quarters of them lived in crowded typical accommodations; thus, they were quite representative of the general population in Abidjan.25
This prospective study provided information on the evolution of infant feeding practices from birth until 9 months of age in a sub-Saharan African setting with a reasonably high level of precision. Indeed, emphasis was placed on the collection of nutritional data with the use of standardized forms to perform the recall histories, the frequent visits scheduled over the follow-up period, and interviews conducted by trained health care workers other than those who counseled the women on infant feeding practices. This minimized the maternal recall bias that could have impaired the estimation of the age of the baby at introduction of the liquids and foods and thus could have overestimated the duration of exclusive breast-feeding.26,27
Before the implementation of the Ditrame Plus study, we had performed a baseline cross-sectional study among women of unknown HIV status within the same community-run health facilities. We found that all mothers had given tap or stored water to their child a median of 1 day after delivery, underlying the finding that exclusive breast-feeding was not practiced in this population.28 Despite the efforts made during prenatal and postnatal counseling to promote exclusive breast-feeding within the Ditrame Plus study, the probability of being exclusively breast-fed from birth remained as low as 10% at M3. The same low acceptability of exclusive breast-feeding had been previously reported within another prospective study conducted in rural South Africa, where at M3, approximately 10% of children were exclusively breast-fed from birth.29 In our study, however, the proportion of mixed-fed children remained rather low in the first 3 months of life. The low uptake of exclusive breast-feeding was primarily the consequence of early introduction of liquids other than breast milk rather than early introduction of infant formula or semisolid foods. From 4 months of age, the study protocol implied a short period of mixed feeding (median of 9 days) linked to the use of both infant formula and breast milk during the weaning process, whose consequences in terms of postnatal transmission of HIV will be difficult to assess but are likely to be limited, considering the briefness of the period. Beyond 4 months of age, infants who were still exposed to breast-feeding were essentially mixed fed. These long-term breast-fed infants remained at risk for being HIV infected through breast milk, because the longer the breast-feeding continued, the higher was the postnatal risk.3
Breast-feeding women included in the Ditrame Plus study failed to practice exclusive breast-feeding, but most of them succeeded in ceasing breast-feeding early, because the median age of the babies at complete cessation of breast-feeding was 4 months (IQR: 3-5 months). Indeed, the median duration of breast-feeding was previously found to range from 8 months (IQR: 7-10 months) to 15 months (IQR: 13-18 months) within 2 different PMTCT studies conducted in Abidjan from 1995 to 2000 with no systematic counseling on infant feeding practices.30-32 Thus, our study provides useful knowledge that shortening the duration of breast-feeding would be feasible in this population.
Women who failed to cease breast-feeding before M4 were under the social pressure of the family of the partner (especially his mother) influencing the decision process about infant feeding practices. Moreover, living in crowded accommodations seemed to be linked to difficulties with early initiation of the weaning process. Prenatal sharing of HIV status with a relative tended to be associated with failure to cease breast-feeding early, but this factor never reached statistical significance, even after adjustment. These social factors must be carefully taken into account when counseling mothers on infant feeding options, however, and emphasis should be placed on issues regarding confidentiality. Women at more advanced stages of the disease were those who significantly ceased breast-feeding the earliest. They may have been too ill to be able to continue breast-feeding. Nevertheless, because these women also tended to practice more exclusive breast-feeding than the others, this is consistent with the fact that they could have decided to be more compliant to the nutritional intervention proposed. They might also have been urged by health care workers to do so, because we previously reported that the Ditrame Plus staff believed the choice of feeding practice should be guided by the value of the maternal CD4 count.33 Generally speaking, health care workers have a key role to play in encouraging the successful practice of alternatives to prolonged and predominant breast-feeding. Indeed, the fact that despite the adjustment based on the mothers' characteristics, failure to cease breast-feeding early was strongly associated with being followed at 1 of the 2 study sites could indicate differences on infant feeding counseling between the 2 sites. Indeed, this nutritional counseling remains difficult to standardize.
Acceptability of exclusive breast-feeding was extremely low in this population, where early introduction of liquids is a common practice from birth. We thus strongly believe that new tools and innovative ways of counseling women on the importance of exclusive breast-feeding for infant health are needed to make the promotion of exclusive breast-feeding feasible in this context. Shortening the duration of breast-feeding seemed to be feasible in this urban setting, given appropriate counseling on infant feeding practices, close nutritional and clinical follow-up, and the free provision of breast milk substitutes from initiation of the weaning process up to 9 months of age. To evaluate this complex nutritional intervention fully, these results will be balanced in the future with its potential benefits, such as the reduction of postnatal transmission of HIV, as well as its potential risks for infant health, especially after early weaning (eg, growth characteristics, severe morbidity, mortality) or linked to the mother (eg, incidence of new pregnancies, stigmatization).
The authors thank the women and children who participated in the ANRS 1201/1202 Ditrame Plus study. We particularly thank the Ditrame Plus staff in Abidjan for assistance in conducting the study, especially Suzanne Kouadio and Zénica Goulheon, who were in charge of infant feeding counseling, as well as Marie-Pierre Martin and Isabelle Bely (Unité INSERM 593, Bordeaux) and Philippe Lepère and Bertin Kouadio (Programme PAC-CI, Abidjan) for their administrative support.
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Composition of the ANRS 1201/1202 Ditrame Plus Study Group
Principal Investigators: François Dabis, Valériane Leroy, Marguerite Timite-Konan, and Christiane Welffens-Ekra
Coordination in Abidjan: Laurence Bequet, Didier K. Ekouévi, Besigin Tonwe-Gold, and Ida Viho
Methodology, biostatistics, and data management: Gérard Allou, Renaud Becquet, Katia Castetbon, Laurence Dequae-Merchadou, Charlotte Sakarovitch, and Dominique Touchard
Clinical team: Clarisse Amani-Bosse, Ignace Ayekoe, Gédéon Bédikou, Nacoumba Coulibaly, Christine Danel, Patricia Fassinou, Apollinaire Horo, Ruffin Likikouët, and Hassan Toure
Laboratory team: André Inwoley, François Rouet, and Ramata Touré
Psychosocial team: Hortense Aka-Dago, Hermann Brou, Annabel Desgrées-du-Loû, Alphonse hé, and Benjamin Zanou
Scientific Committee: Stéphane Blanche, Jean-François Delfraissy, Philippe Lepage, Laurent Mandelbrot, Christine Rouzioux, and Roger Salamon
© 2005 Lippincott Williams & Wilkins, Inc.