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a Unité INSERM 593, Institut de Santé Publique Epidémiologie Développement, Université Victor Segalen, Bordeaux, France
b Projet ANRS 1201/1202 Ditrame Plus, Programme PAC-CI, Centre Hospitalier Universitaire de Treichville, Abidjan, Côte d'Ivoire
c Unité de Surveillance et d'Epidémiologie Nutritionnelles, Institut de Veille Sanitaire, Conservatoire National des Arts et Métiers, Paris, France
d Service de pédiatrie, Centre Hospitalier Universitaire de Yopougon, Abidjan, Côte d'Ivoire
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS. A prospective cohort study in Abidjan, Côte d'Ivoire, was conducted in HIV-infected pregnant women who were willing to breastfeed and had received a perinatal antiretroviral prophylaxis. They were requested to practice exclusive breastfeeding and initiate early cessation of breastfeeding from the fourth month to reduce breast milk HIV transmission. Nature and ages of introductory complementary feeding were described in infants up to their first birthday by longitudinal compilation of 24-hour and 7-day recall histories. These recalls were done weekly until 6 weeks of age, monthly until 9 months of age, and then quarterly. We created an index to synthesize the nutritional adequacy of infant feeding practices (in terms of quality of the source of milk, dietary diversity, food, and meal frequencies) ranging from 0 to 12. The association of this feeding index with growth outcomes in children was investigated.
RESULTS. Among the 262 breastfed children included, complete cessation of breastfeeding occurred in 77% by their first birthday, with a median duration of 4 months. Most of the complementary foods were introduced within the seventh month of life, except for infant food and infant formula that were introduced at age 4 months. The feeding index was relatively low (5 of 12) at age 6 months, mainly as a result of insufficient dietary diversity, but was improved in the next 6 months (8.5 of 12 at 12 months of age). Inadequate complementary feeding at age 6 months was associated with impaired growth during the next 12 months, with a 37% increased probability of stunting.
CONCLUSION. Adequate feeding practices around the weaning period are crucial to achieving optimal child growth. HIV-infected women should turn to early cessation of breastfeeding only when they are counseled properly to provide adequate complementary feeding to take over breast milk. Our child feeding index could contribute to the assessment of the nutritional adequacy of complementary feeding around the weaning period and therefore help to detect children who are at risk for malnutrition.
Key Words: breastfeeding • HIV • infant nutrition • nutritional status
Abbreviations: WHO—World Health Organization • ANRS—Agence Nationale de Recherches sur le Sida • CI—confidence interval • RR—relative risk
The World Health Organization (WHO) and the United Nations Children's Fund have recently advocated for increased commitment to appropriate feeding practices for all infants and young children to achieve optimal growth, development, and health.1 As a global public health recommendation, international guidelines stress that infants should be breastfed exclusively for 6 months, then frequent and on-demand breastfeeding should continue to 24 months and be coupled with the gradual introduction of complementary feeding adapted to the child's requirements and abilities.2
Nevertheless, this issue is particularly complex in high HIV prevalence resource–constrained settings where HIV-infected pregnant women face a dilemma regarding the feeding practices of their forthcoming infant.3 Indeed, in these settings where breastfeeding is widely practiced and usually prolonged 1 year after birth, the overall risk for HIV transmission through breast milk was estimated to be 8.9 new cases per 100 child-years of breastfeeding.4 Several nutritional strategies are conceivable in urban settings to reduce this risk.5 One of them is the combined promotion of exclusive breastfeeding and early cessation of breastfeeding. Indeed, the shorter the breastfeeding period, the lower the cumulative risk for HIV transmission through breast milk.6 Moreover, some observational evidence shows that exclusive breastfeeding carries a lower postnatal risk for transmission of HIV than breastfeeding with early introduction of other fluids or foods.7–9
To be assessed fully, the benefits of such a nutritional intervention in terms of reduction of postnatal HIV transmission have to be balanced with their potential risks for infant health. Indeed, this nutritional intervention could also have potential adverse effects. One of these was that complementary feeding to take over breast milk would not be nutritionally appropriate, whereas international guidelines stress that such a strategy should be coupled with the introduction of nutritionally adequate and safe complementary foods.10,11
We launched in 2001 a research study that was aimed at the prevention of mother-to-child transmission of HIV in Abidjan, Côte d'Ivoire, proposing to HIV-infected pregnant women who were willing to breastfeed to do it exclusively and to initiate early weaning.12 We had previously shown that among these breastfeeding mothers, the median duration of breastfeeding was reduced to 4 months, which was shorter than was usually practiced in this population.13–15
The purpose of our study first was to describe the nature and the ages of introduction of complementary feeding among early weaned breastfed infants up to their first birthday and second was to assess the nutritional adequacy of these complementary foods by creating a child feeding index and to investigate its association with child nutritional status.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Research Design
Within this open-labeled cohort, women received a short peripartum antiretroviral drug combination.12 Two nutritional interventions were hierarchically and systematically proposed to the women during prenatal visits.13 The first strategy was complete avoidance of breastfeeding by providing artificial milk from birth. The second option was practicing exclusive breastfeeding with the aim to obtain complete cessation of breastfeeding between 3 and 4 months of age. Breastfeeding women were encouraged to cup feed their infants when initiating weaning. In all cases, replacement feeding until 9 months of age as well as the material needed were provided free of charge, and the staff supported the choice expressed by the women and counseled them accordingly.
Follow-up Procedures
From birth up to the second birthday, 19 visits were scheduled for clinical, biological, nutritional, and psychosocial follow-up of both mothers and infants. Mother–infant pairs were seen on study sites at birth, 2 days after delivery, weekly until 6 weeks of age, monthly until 9 months of age, and every 3 months until the second birthday. Services that were 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 clinical event were supported entirely by the project.
Nutritionists counseled individually the women on study sites about infant feeding practices whenever needed. Collective sessions were organized to help mothers to position their infant correctly to the breast, to reiterate the benefits of exclusive breastfeeding, how to prepare artificial feeding safely, to initiate weaning, to use appropriate complementary feeding, or to cook the infant food. At each scheduled visit, anthropometric measurements including height and weight were taken by trained staff according to standard procedures.18
Collection of Infant Feeding Practices
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 whether 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 also documented using a 24-hour and a 7-day recall history. Social workers went over a detailed list of commonly used fluids or foods. Women were asked whether these fluids, foods, or some other items not listed had been given in the previous 7 days and, if so, how many times on the day before (24-hour recall history) and how frequently in the past 7 days.
Infants were classified at each scheduled visit as exclusively or predominantly breastfed, mixed fed, or artificial fed using these recall histories.19 Being exclusively breastfed from birth at a given time meant having been classified in this category at all of the preceding visits since birth. We used the following WHO definitions to allow a better comparability of results between studies. Exclusive breastfeeding means giving a child no other food or drink, including water, in addition to breastfeeding with the exception of medicines, vitamin drops or syrups, and mineral supplements.20 Predominant breastfeeding means breastfeeding 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.20 Artificial feeding means feeding a child on artificial feeds (including infant formula and powdered animal milk) and not breastfeeding at all.21 Mixed feeding means breastfeeding while giving nonhuman milk such as infant formula or food-based fluid or solid food.22
We defined the weaning process as the period from the introduction of the first weaning food until complete cessation of breastfeeding. We defined infant food as cereal-based infant food enriched with powdered animal milk. The term weaning food was used for all solid foods and/or any breast milk substitutes (eg, infant formula).
Child Feeding Index
To assess the nutritional adequacy of complementary feeding, we created an index to synthesize multiple dimensions of child feeding practices on the basis of both current infant feeding recommendations2,10 and previous work on the subject.23 This child feeding index was adapted to the context of the Ditrame Plus study, in which women were encouraged to breastfeed exclusively during 4 months, then replace breast milk with formula feeding until 9 months of age. From weaning initiation, women also were encouraged to provide milk sources to their infant through infant food enriched with powdered animal milk and through dairy products. The scoring system that was used to create the child feeding index at ages 6, 9, and 12 months is detailed in Table 1. The more positive the nutritional practices were, the higher scores assigned were. This index was a summation of 4 subscores that are detailed below and ranged from 0 to 12.
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A dietary diversity score was created on the basis of the number of food groups consumed by the child in the previous 24 hours. Emphasis was placed on animal products such as meat, fish, and eggs on the one hand and on products that contained animal milk (dairy products and infant food) on the other hand and constituted 2 food groups. Vegetables and fruits, which are important sources of vitamins and are rich in dietary fiber, and tubers, grain, and starchy foods, which are staples of the diet in this setting, constituted another 2 food groups. Considering that all of these food groups were essential to ensure a high dietary diversity, a score of 1 was assigned to each of them.
A food frequency score was based on the number of days the children consumed each of these food groups in the previous week. The scoring depends on the age of the child and is detailed in Table 1.
A meal frequency score was based on the number of meals (complementary foods) in the previous 24 hours. A maximum score of 2 was given to children who had received complementary feeding at least twice a day at age 6 months and at least 3 times a day at ages 9 and 12 months.
Statistical Analysis
The following analyses were conducted among women whose live-born infant initially was classified as breastfed using the recall history that was obtained at the day 2 visit. The probability of being breastfed was calculated from birth until 1 year of age, using the Kaplan-Meier method. We also detailed the proportion of children who were in each feeding category at given ages.
The proportion of children who were ever fed each food item from birth up to 12 months of age and the median ages of introduction of these food items were calculated. For each food item and for each monthly or quarterly visit from birth up to 12 months of age, we reported the proportion of children who had been given this food item at least once in the previous week.
The mean and median values of the child feeding index were calculated at ages 6, 9, and 12 months. At each of these ages, the index was grouped into tertiles to form 3 categories of child feeding practices (low, average, or high) to assess the nutritional adequacy of complementary feeding.
The relationship between these 3 nutritional categories and long-term growth outcomes in children was also investigated. For this purpose, weight-for-age, height-for-age, and weight-for-length z scores were calculated on the basis of the gender- and age-specific growth chart references that were developed by the National Center for Health Statistics and the Centers for Disease Control and Prevention and recommended for international use by WHO.24–26 The z score or SD unit is defined as the difference between the value for an individual and the median value of the reference population for the same age or height, divided by the SD of the reference population. The mean z scores were presented at ages 9, 12, and 18 months and compared between children with a low versus an average or high index at age 6 months and with a low or average versus a high index at ages 9 and 12 months.
The cumulative probability of being stunted (defined as height-for-age z scores less than –2 SD) at least once from age 7 months to 18 months was compared between children with a low versus an average or high index at 6 months, using the Kaplan-Meier technique.27,28 Multivariate analysis used Cox's proportional hazard models. This approach allowed for adjustment of this comparison on potential confounding variables: maternal education, type of housing, low birth weight (<2500 g), and pediatric HIV status (time-dependent variable). All statistical analyses were conducted with the use of SAS software (version 8.2; SAS Institute, Inc, Cary, NC).
Ethical Permissions
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 ANRS. As part of the Ditrame Plus program, the study presented here was included in the institutional review board approval.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Breastfeeding Characteristics
At 12 months of age, 77% of these mothers had completely ceased breastfeeding. Complete cessation of breastfeeding occurred a median of 4 months after delivery (interquartile range: 3–5). The probabilities of being breastfed from birth until 1 year of age are represented in Fig 1.
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Within our cohort, the cumulative probabilities of being exclusively breastfed from birth were 0.18 (95% confidence interval [CI]: 0.13–0.22), 0.10 (95% CI: 0.06–0.13), and 0.01 (95% CI: 0–0.02) at ages 1, 3, and 6 months, respectively. As detailed on Fig 2, this low prevalence of exclusive breastfeeding could be explained by early common introduction of fluids such as water (essentially tap water, but use of mineral water was also relatively common early in life). Indeed, 98% of the infants had ever been given water from a median of 8 days of age. Other fluids, such as herbal tea or fruit juice, were widely used but introduced later, ie, a median 12 weeks and 5 months after birth, respectively.
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Child Feeding Index and Its Relation to Child Growth
The values of the child feeding index scores at ages 6, 9, and 12 months are detailed in Table 2. At all ages, all of the 4 subscore values ranged from 0 to the maximum possible value, namely 2 or 4. At age 6 months, the mean values of the source of milk and meal frequency scores were satisfactory (1.63 of 2 and 1.41 of 2, respectively), whereas the dietary diversity and food frequency scores were low (<1 of 4), leading to a relatively low child feeding index score with a mean of approximately 5 of 12. At 9 and 12 months of age, the dietary diversity and food frequency were more adequate (>2.5 of 4), resulting in a considerably improved child feeding index. No statistically significant associations were found at any of the 3 ages between maternal sociodemographic characteristics and the child feeding index categories (low, average, or high).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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We had previously reported that the women who were included in the Ditrame Plus cohort were representative of the general population of Abidjan as they had been recruited among all attendees of community-run health facilities located in poor areas, with no other selection criteria than having HIV infection, being at least 18 years of age, and having accepted the study protocol.12,13 Given this resource-limited environment, breast milk substitutes (infant formula) were provided for free from the initiation of the weaning process until 9 months of age. This needs to be taken into account as it contributed to the nutritional accuracy of the source of milk provided to the infants.
This prospective study provided detailed information on infant feeding practices from birth with a reasonably high level of precision. Indeed, emphasis was made on the collection of nutritional data with the use of standardized forms to perform the recall histories, the frequent visits scheduled during the follow-up period, and interviews that were conducted by trained health care workers other than those who counseled the women on infant feeding practices. This strategy minimized the maternal recall bias that could have impaired the estimation of the complementary feeding characteristics.29,30 That the previous week of food consumption is not necessarily representative of long-term usual feeding practices might constitute another limitation. Indeed, food could have been introduced in intervals that were not covered by the interviews, which could have overestimated the age at which this food was introduced. Nevertheless, all complementary foods were introduced during the first 9 months of age, a period when interviews were conducted at least once a month, which contributed to minimization of this limitation. Moreover, the longitudinal and regular compilation of several 24-hour and 7-day recall histories tends to reflect reliably the feeding pattern during the study period.
Assessing the nutritional adequacy of complementary feeding is complex because qualitative (eg, food diversity, food frequency) as well as quantitative (eg, number of meals, exact amount of each food group, nutrient intakes, total energy intake, vitamin coverage) dimensions of infant feeding practices need to be taken into account. The child feeding index that we used essentially was qualitative and could have been improved by assessment of quantitative dimensions of child feeding practices. Nevertheless, this evaluation would have been difficult in a context in which most of the mothers were illiterate. Moreover, it would have been impractical because the recall histories already lasted 30 min in a study that had multiple judgment criteria and in which mothers also had to be interviewed by a clinician for their child and for their own health at each visit.
We believe that because of this child feeding index, our study provides a reliable longitudinal view of the evolution of both characteristics and nutritional adequacy of infant feeding practices among early weaned breastfed children. Moreover, this study highlights the critical period when such an index could be a predictor of the child's future growth outcomes.
The relationship between the different categories of the child feeding index and the nutritional status of the children was assessed using anthropometric indices. The cumulative probability of low height for age was assessed as it reflects a process of failure to reach linear growth potential as a result of suboptimal health and/or nutritional conditions.28 As stunting is a severe event in low-income countries, especially when it starts early in infancy,31 our intent was to detect the proportion of infants who were exposed at least once to this risk. This analysis was coupled with the estimations of the mean z scores. We believe that the analysis of the trajectory of height or weight for age would have been more difficult to interpret. Indeed, a relatively high standard of care was proposed within our study: close clinical and nutritional follow-up adapted to the child age and free provision of care. Children who had a z score less than –2 SD were expected consequently to be clinically and nutritionally treated, which would have positive consequences on growth velocity.
We assumed that poor growth was a consequence of the nutritional inadequacy of the complementary feeds. Poor growth also could come from illness that was associated with not receiving the immune protection from breast milk. However, the relationship between infant feeding practices and the occurrence of interim illness is difficult to interpret because of a reverse causation bias.32 In addition, poor growth could come from receiving contaminated foods. All of the women who were included in the study had access to tap water, but because two thirds of them lived in typical shared housing, the tap mainly was outside home. It was reported previously that the quality of municipal water in Abidjan was good but that household water storage was a common practice that contributed to contamination of drinking water.33 Within our study, women were encouraged to avoid water storage, but one third of them reported ever having given stored water to their child (Fig 2). Such a practice might have had adverse consequences on infant health.
Several studies that were conducted in resource-constrained countries, where breastfeeding was prolonged long term, had underlined that the protection against mortality that was provided by breast milk tended to decline with age and was probably attributable to both lower breast milk intakes and inaccurate complementary feeding.32,34 Our study provides useful knowledge on this issue in the context of a nutritional intervention aimed at the prevention of HIV through breast milk, underlying that adequate feeding practices around the weaning period seem to be crucial for achievement of optimal child growth. In resource-limited countries, HIV-infected women therefore should turn to early cessation of breastfeeding only when they are counseled to provide to their child adequate complementary feeding to take over breast milk. In this context, we strongly believe that emphasis should be placed on innovative ways to counsel women properly on infant feeding so that the public health messages could be adapted to their individual situations.
Ideally, the child feeding index presented here could be used routinely, especially around the weaning period, to contribute to the assessment of the nutritional adequacy of complementary feeding. This index therefore could help to detect children who are at risk for malnutrition and whose mothers need to receive appropriate and reinforced nutritional counseling. Nevertheless, other prospective studies are needed to assess fully the accuracy of this child feeding index to detect early children who are at risk for malnutrition in other settings and circumstances.
Composition of the ANRS 1201/1202 Ditrame Plus Study Group
Principal investigators: François Dabis, Valériane Leroy, Marguerite Timite-Konan, Christiane Welffens-Ekra; coordination in Abidjan: Laurence Bequet, Didier K. Ekouevi, Besigin Tonwe-Gold, Ida Viho; methods, biostatistics, and data management: Gérard Allou, Renaud Becquet, Katia Castetbon, Laurence Dequae-Merchadou, Charlotte Sakarovitch, Dominique Touchard; clinical team: Clarisse Amani-Bosse, Ignace Ayekoe, Gédéon Bédikou, Nacoumba Coulibaly, Christine Danel, Patricia Fassinou, Apollinaire Horo, Ruffin Likikouët, Hassan Toure; laboratory team: André Inwoley, François Rouet, Ramata Touré; psychosocial team: Héléne Agbo, Hortense Aka-Dago, Hermann Brou, Annabel Desgrées-du-Loû, Alphonse Sihé, Annick Tijou-Traoré, Benjamin Zanou; Scientific Committee: Stéphane Blanche, Jean-François Delfraissy, Philippe Lepage, Laurent Mandelbrot, Christine Rouzioux, Roger Salamon.
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ACKNOWLEDGMENTS |
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We gratefully acknowledge the women and children who participated in the 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.
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FOOTNOTES |
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Address correspondence to Renaud Becquet, PhD, Unité INSERM 593, Institut de Santé Publique Epidémiologie et Développement (ISPED), Université Victor Segalen Bordeaux 2, 146 rue Léo Saignat, 33076 Bordeaux Cedex, France. E-mail: Renaud.Becquet{at}isped.u-bordeaux2.fr
The authors have indicated they have no financial relationships relevant to this article to disclose.
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REFERENCES |
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This article has been cited by other articles:
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  M. M Moursi, Y. Martin-Prevel, S. Eymard-Duvernay, G. Capon, S. Treche, B. Maire, and F. Delpeuch Assessment of child feeding practices using a summary index: stability over time and association with child growth in urban Madagascar Am. J. Clinical Nutrition, May 1, 2008; 87(5): 1472 - 1479. [Abstract] [Full Text] [PDF]
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