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Margaret E. Bentley, Maureen M. Black, and Elena Hurtado
Feeding is an ideal context in which to examine the interaction between biological development and cultural variability in international efforts to promote children's survival and health. The transition from liquid to semi-solid and solid feeding is a major developmental milestone that occurs in the first year of life. Appetite is a central component in the decision making process used by caregivers to determine when and how much to feed their infants. Anecdotal, qualitative, and dietary consumption data provide evidence that both illness-related and chronic anorexia is an important problem among infants and young children in developing countries. For example, nutrition programme personnel have noted that children simply do not appear to be hungry or to eat all that is offered to them, even if they are clearly undernourished. Following the UNICEF triple-A framework, this paper describes programme strategies to improve child-feeding and appetite.
Feeding is an ideal context in which to examine the interaction between biological development and cultural variability in international efforts to promote children's survival and health. The transition from liquid to semi-solid and solid feeding is a major developmental milestone that occurs in the first year of life. Infants are faced with maturational, social, and cultural challenges as they learn to chew, swallow, and digest a wide array of culture-specific foods necessary to promote their growth and development. Disruptions in growth, illness, or disruptions in the acquisition of feeding skills are serious problems that undermine children's survival and are the focus of concern by parents and healthcare providers. Strategies to facilitate adopting positive feeding practices must accommodate the multiple factors ranging from biological requirements to cultural practices that influence feeding.
Public health importance of anorexia
Appetite is a central component in the decision making process used by caregivers to determine when and how much to feed their infants. Castonguay and Stern  define appetite as "mild hunger usually directed at a choice of food items and often with expectations of reward." Hunger differs from appetite in that hunger is often regarded as a physiological concept, whereas appetite is usually culturally defined . In this article, anorexia is defined as a loss of appetite, often as observed or perceived by caretakers attempting to feed an infant.
Anecdotal, qualitative, and dietary consumption data provide evidence that both illness-related and chronic anorexia is an important problem among infants and young children in developing countries. For example, nutrition programme personnel have noted that children simply do not appear to be hungry or to eat all that is offered to them, even if they are clearly undernourished. A monotonous diet may be an important factor in chronic anorexia .
Food may be limited and monotonous in flavour and texture. The monotony of the diet may act synergistically with the consequences of repeated infectious morbidity, and result in chronically depressed appetite and limited acceptance of additional food in quantity and variety at the time when this becomes critical for meeting the nutritional needs of the growing infants.
Historical and experimental literature supports this hypothesis. In a series of experiments among college men, it was found that food acceptance and caloric intake were related to a monotonous diet and presentation of food . Similarly, other investigators [5, 6] reported that dietary variety (including variety in the number of foods and alternative shapes, tastes, and presentations) resulted in higher satiety and food intake, compared with a less diverse diet.
Diets lacking variety are common in developing countries, particularly among weanlings. For example, in rural Guatemala , an average of eight foods accounted for almost 80% of children's energy intake. However, the relationships among low dietary diversity, nutrient intake, and nutrition status in infants of developing countries have not been examined systematically.
A longitudinal study of urban Peruvian infants  has shown an incidence of anorexia during 15% of all days, with a parallel reduction in total energy intake. Fever, diarrhoea, and respiratory infection were also associated with reduced appetite. However, anorexia was not related to changes in maternal feeding behaviour . Perhaps this was because mothers rarely reported infant anorexia before solid foods were consumed regularly. Reports of reduced appetite were positively associated with children's age and usually followed, rather than preceded, changes in infant-feeding behaviour. Thus, maternal feeding practice decisions may be influenced by poor growth rather than by infant-feeding behaviour.
In rural Mexico, 45 children between the ages of 33 and 60 months were observed for one 12-hour day to assess their dietary intakes and growth [10, 11]. Children had access to more than 2,000 kcal/ day, but mean dietary intakes averaged only slightly more than 1,500 kcal/day. Children requested foods frequently and received positive responses 76% of the time, suggesting that food availability did not restrict intake. Many of the children were growth stunted, suggesting that factors such as anorexia should be included in analyses of dietary intake and growth.
In every setting, there are cultural norms for when and how infants should receive foods and drinks in addition to breastmilk. Cross-cultural studies of infant-feeding document wide variation in the timing, type, and amount of supplemental feeds and in beliefs about the appropriate styles of feeding . Although substantial variation can occur within a culture or a group, each culture has a set of generalized rules for feeding infants and for meeting their developmental milestones. Although these cultural norms are dynamic and undergo periodic changes, they are passed down through subsequent generations and retain at least some traditional features.
Cultural patterns of weaning often do not conform to paediatric recommendations to add semi-solid foods as a complement to breastmilk when the child is four to six months of age [21, 22]. For example, in many settings, weaning foods and drinks are offered very early, even during the first month of life, whereas in other settings, infants are not given any substantial supplemental foods until they are at least one year old. In addition, styles of infant-feeding also vary based on cultural norms. In some settings, infants are fed out of their own bowl with a spoon, whereas in others caretakers use their hands to feed infants, or infants eat out of a shared family pot. Likewise, the desired consistency of first foods usually has a strong cultural basis, in general being more liquid or semi-solid and soft [23-25].
In many settings, caretakers are relatively passive during the feeding process, following cues given by the child and often allowing the child to feed himself or herself [13-16, 2326]. In other settings, caretakers have been socialized to be extremely proactive in their feeding mode, ranging from verbal encouragement, e.g., "Open the hatch for your vegetables, Jaime," to the use of rewards or bribery to achieve a clean plate .
Embedded within each culture or group's beliefs and norms of infant-feeding are caretakers' perceptions of children's appetite, including how appetite can change because of the infant's developmental stage or health status and what, if anything, caretakers should do in response to short- or long-term changes in appetite.
Investigators observing children with poor growth and their mothers during mealtime have reported parent-child interaction patterns characterized by unclear messages, premature termination of feeding, inconsistent mealtimes, and limited food availability [28-35]. Evidence also suggests that there is a high rate of insecure attachment between children with poor growth and their parents [36-38].
When parents do not structure mealtimes, children do not learn to anticipate when they will eat, and may feel anxious and irritable . In contrast, children who "fill up" on liquids, such as fruit juice, and do not eat regularly structured meals do not get adequate nutrients and are at risk for growth failure, even when they come from middle- and upper-income American families . Therefore, so that children will develop an expectation and an appetite around mealtime, mealtimes should be structured and children should not "graze" or feed ad lib.
Caretaker responses to anorexia
In many developing countries, caretakers are generally passive in their feeding mode, allowing children to set the pace. Food is offered on the basis of specific signals children send, such as crying or grabbing for food. When a child sends a "food reject" signal, a common response is to give in to the child's will. In developing countries, a child is rarely forced to eat when he or she resists, with the Yoruba of Nigeria as a notable exception [25, 41]. In Guatemala, mothers report that "the child's stomach knows how much food it needs," and believe that forcing a child to eat could make the child sick or vomit or could worsen the illness of one who is already sick.
Most parents have a mental construct of what a "normal" child's appetite should be and recognize that anorexia-a child's refusal to eat-is not normal . However, parents may not have ideas about how to cope with anorexia, and may be convinced that the primary solution is to administer vitamins or tonics to improve the child's appetite. They place the burden of eating on the child, often taking cues from their infants about when and what foods should be offered. This scenario has been described among Bangladeshi infants:
One of the most common reasons reported for not giving more complementary food was because "the child refused." Although normal interactive feeding behaviours have been observed between Bangladeshi infants and mothers ... the reasons why the children do not demand and consume food sufficient to sustain normal growth, as healthy children are expected to do, remain unclear. Caretaker inattentiveness to feeding, as well as frequent acute infections, chronic illnesses, and malnutrition in the child, may account for a portion of the energy deficit .
A framework adapted from one by Dettwyler (fig. 1) represents two interacting continuums: the caretaker's feeding behaviour and the child's acceptance of food, or appetite [13,14]. The range of caretaker behaviours is shown horizontally, with passive feeding behaviours on the left and active feeding behaviours on the right. In developing countries it is common for caretakers to be relatively passive, offering little physical or verbal encouragement to eat- unless a child is perceived to be ill or is exhibiting frank rejection of food. When this happens, caretakers often respond to the child's lack of interest in or rejection of food through more active feeding behaviour. When children recover from illness, however, caretakers resume their passive feeding behaviours once again, shifting back along the continuum. Moreover, although research evidence is sparse, it appears that when children experience chronic anorexia, caretaker behaviour may remain relatively passive until children's growth falters.
On the vertical axis, the child's acceptance of food, or appetite, is also represented on a continuum, so that the child's behaviour moves from positive appetite to negative appetite. This continuum is likely to be dynamic, so that when children experience repeated infections or illness symptoms, their behaviour will reflect reduced appetite during the illness and a return of appetite during recovery or convalescence. Anorexia associated with illness, particularly fever, may be an adaptive physiological response related to immune function , and emphasis for encouraging feeding should perhaps focus more on the convalescent period when appetite returns [23, 24].
When chronic anorexia occurs, the appetite may remain below normal for extended periods. The child's cues that reflect a lack of interest in food or a rejection of food may not be as pronounced as when children are ill, and caretakers may assume such behaviours are normal.
In the centre of the diagram and where interaction between the caretaker's and the child's behaviours occur, there are several important factors influencing the interaction, including the age of the child; the quality, quantity, and characteristics of the weaning diet; breastfeeding status; health and nutrition status of the child; caretaker time; and the ability to recognize and respond to the child's feeding cues. These factors represent the transactional nature of feeding whereby both the child and the caregiver are influenced by each other and the overall quality of their interaction. For example, a diet that is monotonous, non-nutritious, or of an inappropriate consistency may have a negative impact on a child's acceptance of food or appetite. An older child who receives primarily breastmilk rather than the more energy-dense weaning foods may not be receiving adequate nutrient intake even if the child appears to prefer breastmilk. The poor nutrition status or high morbidity of a child may influence the caretaker's behaviour. The ability of caretakers to respond to children's cues may be influenced by their resources, time, or knowledge and by other demands.
The likelihood of malnutrition increases when a child has anorexia and the caretaker's style of feeding is passive [13,14, 42]. Although more research is needed to clarify the relationships among the caretaker's feeding style, the child's acceptance of food, and nutrient intake, programmes can use the diagram to promote healthy feeding behaviours. For caretakers, programmes should emphasize a shift from passive to more active feeding behaviours-regardless of the child's health status. For infants and children, programmes should promote foods, feeding styles, and contexts that are associated with positive appetite. Although children may experience transitory anorexia, usually during an infectious disease episode (particularly fever), programmes that are culturally based and incorporate the caretaker-child interaction into their recommendations are likely to have most success in promoting positive appetite and reducing the occurrence of chronically negative appetite. For example, programmes that promote breastfeeding or improve overall hygiene to reduce morbidity and subsequent illness-related anorexia could be important for both caregivers and children. As important as these recommendations are, programmes that address the caregiver-child relationship are extremely important. Programmes should be designed to understand the caretaker's and the child's behaviours and feeding cues, and develop behavioural change programmes and messages to facilitate more active feeding.
FIG. 1. Interaction of the caretaker's child-feeding behaviour and the child's appetite
UNICEF triple-A framework
Although the long-term solution to the problem of poor growth in children may be to eliminate the underlying causes of poverty and malnutrition, programme activities focusing on improving infant feeding practices, feeding environment, infant diet, and other factors can make a difference. Following the UNICEF triple-A framework, programme alternatives to improve feeding and appetite can be organized into four activities: assessment, analysis, trial, and action.
Assessment: Collection of basic information
Following the framework presented in figure 1, the first step of assessment should focus on understanding the environmental, cultural, and behavioural factors that influence child-feeding and acceptance of food, and children's nutrition and health status. This step should be able to draw heavily on secondary data analysis, although it is likely that some primary data collection will need to be done. Information on infant-feeding practices and determinants, cultural norms regarding child-feeding behaviour, children's health and nutrition status, characteristics of the weaning diet (quantity, quality, taste), and morbidity patterns should be investigated. A detailed list of such factors is presented in appendix 1.
Particular attention should be paid to understanding the interactions between the caretaker's feeding behaviour and the child's feeding cues, within a specific cultural context. As discussed above, programmes need to identify where caretakers' normal feeding behaviours are on the passive-active continuum, what specific children's feeding cues trigger a response, how caretakers recognize children's cues, and how they respond to children's cues.
The analysis of the problem requires knowledge of the cultural context; available food resources; the family's beliefs regarding meals, feeding, and growth; and the interaction between the child and the caretaker.
Analysis: Ethnographic, communications, and behavioural
Analysis focuses on the search for solutions. There are at least three kinds of analysis necessary for health-care providers to develop intervention strategies.
Descriptive analysis (including ethnographic analysis) provides information on the caretakers" and children's feeding practices, the context in which they take place, and the factors that influence them (resources, time, beliefs).
Communication and organization analysis indicates what information mothers are currently receiving on child-feeding, from whom, what is the mode, the tone, the language, the terminology used in the communication, and so on. Also, it indicates the organizations that are likely to participate in the intervention, and where to look for effective change agents (for example, midwives, health promoters, mother leaders).
Behavioural analysis, social marketing, and social communication  separate behavioural patterns into discrete sequential steps that become the focus of intervention. Several criteria (such as cost and compatibility with existing beliefs and practices) are used to evaluate behaviours that are critical in improving nutrition and health outcomes in a specific cultural setting, and behaviours that are feasible to be changed.
Once the analysis and a solution or a set of solutions are defined, a testing and adapting activity should take place. Typically, behavioural trials at the household level [23, 24, 45-47] begin with a pilot trial by asking a group of community mothers to try out the specific set of behaviours recommended for a limited period of time, usually one week. Their reactions, learning difficulties, resource constraints, and changes made are examined. The product is a more refined list of feasible recommendations that can be systematically implemented and evaluated.
Once the problem analysis is completed, programmes can evaluate how specific actions can be integrated into ongoing programmes and where new programmes could be initiated. This process should sort the assessment information into programmatic categories. For example, if mothers' lack of time is identified as a constraint to promoting more active feeding behaviours, then ongoing programmes that address time allocation should be listed as possible entry points. If children's illness appears to be a major problem, then programmes to improve case management or reduce morbidity burden should be identified as points to strengthen.
Support to shift caretakers' feeding behaviours from passive to active might incorporate some of the following:
Teach caretakers to monitor the food consumption of young children, making sure that small children get as much nutritious food as they want to eat.
- Encourage caretakers to be on the lookout for any changes in the infant's normal eating habits, whether or not there are other obvious signs of illness.
- Support caretakers in encouraging the child to eat more, through culturally appropriate games, messages, or phrases, as well as active feeding of the child with fingers or a spoon, at the first signs of anorexia (if not as a general rule for infant feeding interactions on a daily basis).
- Encourage caretakers to be prepared to offer special foods to sick children, including foods they particularly like, foods that may be soothing for their illness (e.g., liquids), and foods high in nutritional value.
- Support caretakers to provide extra encouragement and food to children following an infectious episode, during the "catch-up" convalescent period.
- Encourage caretakers of anorexia children to seek assistance from health-care providers.
- Encourage caretakers to establish a routine feeding environment with the focus on more proactive feeding.
- Implement weaning interventions to improve the overall weaning diet so it consists of more energy- and nutrient-dense foods.
- Provide caretakers with a variety of responses to children's anorexia, and teach them that they can be effective in overcoming this common symptom of disease.
By incorporating participatory and rapid ethnographic assessment methods that include caretakers in defining the problem and in the intervention process [48, 52-56], programmes can implement and evaluate innovative strategies to encourage more active feeding behaviours and to overcome the impact of anorexia on children's dietary intake and growth. These strategies should be incorporated into systematic implementation and evaluation designs as developed for the Weaning Project [45, 46], the Dietary Management of Diarrhoea Programme [23, 24, 47-49], the Nutrition Communication Project [50, 51], and others .
Parts of this paper have drawn heavily on a manuscript by Bentley, Caulfield, and Dettwyler currently in press and an unpublished manuscript by M. Bentley and M. Black that was presented at the Experimental Biology Meeting on 2428 April 1994 in Anaheim, California, USA.
Appendix 1. Study of child-feeding with emphasis on child's acceptance of food (appetite)
Specific feeding behaviours are related to the child feeding process that begins at birth and ends when the child is eating the adult diet. Stages in this process are: pre-lacteal feeds and intake of colostrum breastfeeding complementary feeding and weaning complete introduction to adult diet
The most important stages to focus on to assess the child's appetite and acceptance of food are complementary feeding and weaning, and complete introduction to adult diet.
Various dimensions of the study of behaviours can include:
A. Features of the behaviour
1. Food handling and preparation
Optimal complementary feeding practices Who prepares the child's food?
Personal and food-hygiene behaviours, which are especially important for infants and children, as they are more susceptible to diarrhoeal diseases; illness influences acceptance of food.
How food is prepared, such as cutting, mashing, straining, putting in a bottle; consistency of foods.
Re-heating of previously prepared foods.
Storage of infant foods.
2. Feeding and eating
What? Both mother's or caregiver's and child's behaviours; the feeding episode.
How? Breast, bottle, feeding semi-solid and solid food by hand, with spoon, on own or shared plate.
Where? Environment and specific place where child is fed or eats; bodily position.
Who? Mothers or other caretakers feed child; do other people eat with child, and are other people normally present?
When? Meal patterns, scheduled or on demand.
Sequence? Crying or asking for food and other behaviours indicative of child's appetite, or mother or caregiver initiating episode.
How often? How many times a day is child fed?
How much? Amount of food given; is child given seconds?
Interaction? Mutual interactions of the mother or caregiver and the child, such as child's eating or refusing food, maternal responses, etc.
How long? Duration of feeding episode.
How well? Acceptance of food by the child.
How strong? Intensity of child's refusing or accepting foods.
Mother's awareness or responses to good appetite: ignore, encourage to eat, compliment for eating, physically help child to eat, give more food.
Mother's responses to anorexia: ignore, verbally encourage child to eat, physically help child to eat or to finish all food, give special or preferred foods, force feed; under what circumstances, which foods?
Other strategies: seating child next to caregiver, seating child on lap.
Care-seeking behaviours to get treatment for an anorexic child.
B. Determinants of child-feeding behaviours
1. Physical environment: particularly availability of foods, variety of foods available.
2. Economic conditions: particularly accessibility of foods.
3. Material and other resources: material re sources (bottle, spoon, plate, mat, high chair); maternal time to prepare foods, feed child; change in patterns when mother is away.
4. Household, maternal, and child characteristics:
Social support; husband's role in child feeding.
Health status of child, of mother; what changes in child-feeding practice occur when mother is sick; foods withheld, foods given; differences for different illness.
Nutrition status of child and mother.
Breastfeeding status of child.
Age of child.
Emotional health of child and mother; temperament.
Previous experience of child and mother.
5. Cultural beliefs
About complementary feeding; appropriate foods; appropriate age of the child; child cues.
About weaning; appropriate age.
About child developmental stages, names; perceptions about the meaning of particular infant behaviours.
About illness and feeding.
About causes of anorexia; what is normal, what is not?
Why? Purposes of, reasons given for child-feeding practices.
Perceived costs and benefits of current child-feeding practices; of new practices.
Antecedents and consequences of child-feeding practices.
7. Influence of health sectors
Health provider practices.
Health provider advice on child-feeding; appetite.
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