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Homero Martínez and Andrew M. Tomkins
Diarrhoeal disease may cause, precipitate, or exacerbate protein-energy and micronutrient malnutrition through five possible mechanisms: 1) reduced food intake-reduction of food intake during diarrhoea may be due to the child's anorexia, maternal food-withholding behaviour, or both; 2) decreased absorption of nutrients-structural damage to the intestine, as well as the physical action of increased intestinal movement and reduced fluid transit time, interact to produce decreased absorption of nutrients; 3) increased catabolic losses-under the influence of the inflammatory process, diarrhoea of infectious origin induces an average daily negative nitrogen balance of 0.9 g/kg/day, as muscle protein is converted to glucose through gluconeogenesis by the liver; this glucose is used as a fuel by tissues to sustain the hypermetabolism associated with fever; 4) nutrient loss from the intestine-in diarrhoea nutrients are lost directly from the intestinal tract; 5) metabolic inefficiency due to micronutrient deficiency-the increased rate of tissue synthesis displayed by children recovering from protein-energy malnutrition may be hampered by a limited supply of nutrients from the body pool, which in turn may not be replenished fast enough by dietary intake. The two main driving forces that determine nutritional care of the sick child in the home are advice from healthcare providers (mainly physicians) and the mothers' own beliefs; a third determinant of care is the social support network available to mothers or social pressure to act in a determined way. Therefore, health providers should be knowledgeable about appropriate feeding management of illness, and should provide sound advice to mothers.
The likelihood that mothers will follow the recommendations given by the health-care system (whether formal or informal) will be greater if these conform to mothers' cultural norms and their explanatory model of disease. Feeding practices followed in health facilities should be consistent with those advised for the mothers at home. In order to make a successful change in a given practice, culture-sensitive interventions should be used.
Effects of diarrhoea on nutrition status, food intake, and food utilization in children
Several landmarks in understanding the relationship between infection and nutrition have emerged from the study of nutrition in diarrhoea! disease. Moreover, through an examination of feeding children with diarrhoea, we have come to a better understanding of approaches to feeding children with infectious diseases in general. Therefore, although the discussion in this article will focus on diarrhoea! disease, in light of the other considerations presented here, one might extend it to other conditions.
Diarrhoeal diseases may cause, precipitate, or exacerbate protein-energy and micronutrient malnutrition through five possible mechanisms: reduced food intake, decreased absorption of nutrients, increased catabolic losses, nutrient loss from the intestine, and metabolic inefficiency due to micronutrient deficiency (table 1).
Reduced food intake
Reduction of food intake during diarrhoea may be due to a child's anorexia, maternal food-withholding behaviour, or both [1, 2]. Evidence of children's reduced food intake during illness has been explored by several authors. During episodes of diarrhoea or fever in 131 Peruvian infants, a significant decrease in total energy intake was found, representing up to20% to 30% of energy intake. This decrease was due to reduced consumption of non-breastmilk foods . Structured observations in the homes of 40 Peruvian children aged 4 to 36 months revealed that anorexia reduced a child's acceptance of food, despite the mother's encouragement to eat . In Guatemalan children aged 15 to 60 months, diarrhoea was found to be associated with an average reduction in daily food intake of nearly 20%, equivalent to 175 kcal and 4.8 g of protein . Children's anorexia is a consequence of clinical disturbances, including dehydration, electrolyte imbalance, fever, and vomiting or abdominal discomfort . Mothers may withhold food as a result of medical advice or on their own, either in response to their child's anorexia or as a practice for managing diarrhoea. Whatever the reason, the result may be the cessation of breastfeeding, compromises in the quality and quantity of weaning foods, and, in some cases, reduction of food intake by lactating mothers themselves .
TABLE 1. Main by which disease may cause, accelerate, or exacerbate protein-energy and/or micronutrient malnutrition
increased catabolic losses
nutrient loss from the intestine
decreased absorption of nutrients
metabolic inefficiency due to rnicronutrient deficiency
Cultural beliefs affecting (restricting/modifying) the foods offered by the caregiver
Limitation of caregiver's knowledge/time/skills in feeding the
Decreased absorption of nutrients
Structural damage to the intestine, as well as the physical action of increased intestinal movement and reduced fluid transit time, interact to decrease absorption of nutrients during an episode of diarrhoea. In 1982, the effects of diarrhoea on nutrient intake of 19 hospitalized children with cholera and 13 with rotavirus infections were studied. Not only was the intake of nitrogen, fat, and calories reduced in the acute stage (by 44%, 32%, and 36%, respectively, in cholera, and 22%, 10%, and 27%, respectively, in rotavirus patients), but the coefficient of nitrogen absorption was reduced to an average of 45% for all children [6-8].
During the inflammatory process, muscle protein is converted into glucose through gluconeogenesis by the liver. This glucose is used as a fuel by the diseased tissues, immune system, liver, kidneys, brain, and tissues generally to sustain the hypermetabolism associated with the development of fever. Experimental studies in rabbits suggest that glucose may also be used by the intestine itself, in response to the diarrhoea, to sustain the secretory process that accompanies infectious diarrhoeas .
Although gluconeogenesis may seem to destroy muscle mass in acute diarrhoea! illness, it nevertheless appears to serve a critical purpose. In a study of patients aged 15 years or less admitted to a diarrhoea treatment center in Dhaka, Bangladesh, the investigators found that children who fail to mount a proper gluconeogenetic response are more likely to die .
Further, the liver takes the amino acids usually used for forming albumin, transferrin, and other proteins to form the acute-phase proteins designed to protect the host against the infection.
Powanda has reviewed the metabolic changes present in patients with acute infections, noting that diarrhoea of infectious origin induced an average daily negative nitrogen balance of 0.9 g/kg/day . However, measurement of increased protein catabolism in childhood diarrhoea has been complicated by the fact that the usual measure of protein catabolism, nitrogen balance, is affected by often very large intestinal protein losses.
Nutrient loss from the intestine
In diarrhoea nutrients are lost directly from the intestinal tract. An increased stool clearance of alfaxx1-antitrypsin, a serum protein marker present in the stools, has been observed in about half of all rotavirus diarrhoeas and even more frequently in shigellosis infection, in which tissue destruction is accompanied by losses of plasma, epithelia, and blood cells. Nearly two-thirds of patients with enterotoxigenic Escherichia coli also show an excessive loss of protein in the faeces . Structural alterations in the mucosal epithelium due to Shigella sip., rotavirus, and Campylobacter sp. infections also result in a "protein-losing enteropathy," similar to the measles-induced abrupt fall in plasma albumin through faecal losses . Losses of zinc and copper during early stages of acute diarrhoea in Chilean children have been documented. These losses were greater when stool losses were larger .
Metabolic Inefficiency due to micronutrient deficiency
Children recovering from protein-energy malnutrition show, on a magnified scale, several metabolic changes that take place during normal growth, as they gain weight at over 20 times the normal rate . In these cases, the increased rate of tissue synthesis may be hampered by a limited supply of nutrients from the body pool that may not be replenished fast enough by dietary intake. Limited growth associated with diets marginal in zinc has been found in North American children [15, 16]. An acute depletion of plasma zinc has been shown in marasmic children recovering from malnutrition when they were fed an energy-dense diet meant to promote growth . These children were in zinc balance before their energy intake was increased. Based on these observations, it is likely that zinc deficiency may be a limiting factor for children to recover the weight lost during an acute infection.
Nutritional support during illness
There is general agreement about the need for adequate nutritional support of the sick child; however, how to do this has been a subject of considerable debate. Health-care providers' (mainly physicians') advice and mothers' own beliefs are the two driving forces that determine the nutritional care of the sick child in the home. The social support network available to mothers or, conversely, social pressure to act in a specific way, is a third determinant of this care (fig. 1).
It is more likely that mothers will follow the recommendations given by the health care system (whether formal or informal) if these conform to cultural norms and the explanatory model of disease. However, these norms, like other aspects of human culture, are constantly evolving, being shaped by external forces. Therefore, mothers may eventually incorporate consistent advice from health workers in relation to a given aspect of care into their practices . This is, in fact, what has happened in relation to the restriction of food to the diarrhoea-affected child.
FIG. 1. Main influences on the nutritional care provided to the young child during illness
Dietary management of acute diarrhoea by health providers
For centuries, the dietary approach for treating diarrhoea recommended by physicians and other health workers consisted of a variable period of food reduction or, more likely, fasting, and then a gradual reintroduction of foods and nutrients during the recovery period. This practice was meant to avoid the clinical consequences of diarrhoea-induced malabsorption, based on the assumption that withholding food will reduce stool volume and duration of diarrhoea. The practice was transmitted by physicians to mothers as a need to "keep the bowel at rest" during the bout of diarrhoea, and was incorporated into traditional home-based treatments of the illness.
At present, WHO, UNICEF, and several other international agencies recommend sustained feeding of the child with diarrhoea . This recommendation is based on the rationale that an important proportion of nutrients offered during the diarrhoea episode is actually absorbed; therefore, it is more important to emphasize absorption during diarrhoea, disregarding the degree of malabsorption that does occur when nutrients are offered, thus shortening the period during which nutritional requirements remain unsatisfied .
This approach is supported by evidence from several studies from clinical and field settings in developing and developed countries. As early as 1924, it was suggested that a child's net balance of nutrients, rather than the number of stools, should be the primary clinical concern in the treatment of a child with diarrhoea . In the late 1940s, a series of clinical studies revealed that the continued feeding approach for children with diarrhoea had better outcomes than the one- or two-day fasting routine treatment [21, 22].
More recently, the effects of early versus delayed feeding on 128 non-malnourished children up to 36 months of age were compared . The children were randomly assigned to receive one of four dietary treatments: 1) full-strength formula (110 kcal/ kg/day) from the onset of the treatment regimen; 2) half-strength formula for two days and full-strength formula from then on; 3) oral glucose-electrolyte solution for two days, followed by half-strength formula for another two days, and finally full-strength formula; 4) intravenous rehydration with total fasting for two days, continuing thereafter with two days of glucose-electrolyte solution, two days of half-strength formula, and full-strength formula. Although the stool volume was higher in the first group and lower in the others, the duration of illness was not significantly different among the four treatment groups, and therapeutic success rates were comparable.
On the other hand, net absorption of nitrogen, fat, and carbohydrate, as well as total energy intake, was higher in the first group, reflecting better nitrogen retention and larger increments in body weight, arm circumference, and skinfold thicknesses, from the onset of treatment and throughout the observation period.
The sustained feeding recommendation gives particular attention to foods eaten by the child before the onset of diarrhoea . This is particularly sound when dealing with diarrhoea at home (as opposed to the hospitalized child). Several studies have shown better acceptability  and clinical outcomes using diets based on traditional foods than using more conventional therapeutic diets . For example, a shorter duration of diarrhoea was reported in children fed a diet based on local Peruvian staples than in children fed a potato and milk diet or those fed a soy-protein formula (1.5 vs. 2.7 and 4.9 days, respectively) .
Similarly, a median duration of diarrhoea of 1.8 days was reported in children fed a pap of corn, cottonseed flour, lysine, sugar, and a vitamin-mineral mix, developed by the Institute of Nutrition for Central America and Panama (INCAP) and locally known as Incaparina, complemented with a mixture of rice, corn, beans, oil, and sugar. This was significantly shorter than the 5.3 days median duration of diarrhoea in children fed a lactose-hydrolysed milk and a mixture of rice, egg, oatmeal, oil, and sugar [27, 28]. Similar successful experiences were reported using fermented milks and yoghurts in an area where these foods are culturally acceptable .
The use of milk feedings during acute diarrhoea episodes is of particular concern in infants and toddlers. There is evidence from different clinical trials that reintroducing normal feedings (including full strength milk) immediately after rehydration results in less weight loss and earlier hospital discharge [30, 31]. Current recommendations, based on clinical trials, are that breastfed infants should continue breastfeeding during acute diarrhoea [28, 32, 33]. Non breastfed infants who receive cow's milk should continue to receive it with no dilution . Other authors suggest that children less than nine months old, or who have moderate to severe dehydration associated with the episode, should be individually evaluated to prevent possible recurrence of diarrhoea due to lactose intolerance [34, 35].
Malnourished children with acute diarrhoea may develop carbohydrate intolerance, including intolerance to monosaccharides, as well as protein hypersensitivity. These complications may lead to protracted diarrhoea or to more acute complications such as necrotizing enterocolitis, so nutrition should be managed according to the clinical needs of each patient [25, 36].
Dietary management of acute diarrhoea by mothers
Ethnographic studies of maternal behaviour when confronting diarrhoea (and other diseases) show that mothers have an ample repertoire of treatments that usually include a combination of Western medicine (either self-prescribed or prescribed by a physician or other member of the health team), home remedies, and indigenous practices [17, 37]. More often than not, a combination of treatments is used to manage an episode of illness [17, 38-41]. Mothers' infant-feeding practices are shaped by cultural aspects, including advice from elders (their own mothers, their mothers-in-law, or other women with ascendance) and home-based practices passed from generation to generation. A particular choice will also be influenced by the availability of the remedy, its cost, and the social value of that particular mode of therapy [37-39, 42]. Mothers may also adopt new practices or change old ones depending on experience obtained in treating previous episodes of illness.
Therefore, there are multiple opportunities for influencing mothers' choices. However, successful changes must be culture-sensitive. Thus, it is essential to understand maternal beliefs and practices regarding diet during acute diarrhoea in children.
Several studies have consistently shown, across different cultures, that although some mothers tend to withhold food completely from the child during diarrhoea, most recognize the need to feed, although they tend to modify the usual diet [9, 40, 43-45]. Reasons to withhold specific foods vary, as do reasons to offer particular foods during diarrhoea. Mothers usually recognize several different causes for diarrhoea, not all of which have an equivalent in Western medical culture.
In some cultures, for example, diarrhoea is seen under a "hot-cold" system of classification. Some types of diarrhoea are "hot" ("bloody" diarrhoea), whereas others are "cold" ("mucus" diarrhoea) [46, 47]. Some forms of diarrhoea are associated with fright (susto in Hispanic America) or anger . Other forms of diarrhoea are associated with ingesting particular foods within a definite category (a "strong" food). Some forms of diarrhoea are thought to be due to malevolent supernatural causes ("evil eye") [37, 39], whereas others, like those associated with teething, are considered to be part of the child's normal development [43, 50].
Although these classifications may not make much sense to the health worker, the putative causes recognized by the community are closely linked to mothers' management of the disease at home. For example, giving or withholding a certain food may be related to its hot or cold quality [51, 52].
It is encouraging that several field studies have found that mothers often consider it important to continue giving breast milk the sick child . This practice is fully supported by epidemiological and intervention studies, which show that an infant's appetite for breastmilk does not seem to be diminished during uncomplicated diarrhoea episodes , and that breastfeeding practiced at adequate levels provides significant protection against diarrhoea [53-56].
Care practices during acute diarrhoea
Mothers and other close caregivers should provide emotional support, love, and comfort to the sick child. They should actively encourage the child to drink more fluids than usual, to eat small, frequent meals, and to eat more during convalescence. To do this, a mother requires sufficient time to devote to the child and access to good social support. Consider, for example, that she may have to change the diapers many times per day; take greater care of the child if the child has fever, cough, or vomiting; spend more time and energy trying to feed the child; calm her restless child; and hold the child in her arms. Preparing home remedies also takes time. She may take the child to a doctor, leaving her home chores undone or leaving the rest of the family unattended.
Yet the role of the social support structure goes beyond that of supporting a mother's time. It is important for the mother of a sick child that her husband, parents, in-laws, neighbours, and friends encourage her to practice good habits and discourage potentially harmful ones. She also needs appropriate advice from health workers, as well as access to adequate medical care services.
Health-care providers' practices should take into account the points covered in this review. They should be knowledgeable about appropriate feeding management of illness, and should provide sound advice to mothers. Feeding practices followed in health facilities should be consistent with those advised for mothers at home. In particular cases, it may be necessary to supplement specific nutrients (such as zinc or vitamin A) that may have been depleted during the illness [57, 58]. If a child needs to be hospitalized, care should not be limited to treating and managing the underlying disease and associated complications; the staff should also offer understanding and comfort to the child.
Even at home, caregivers should realize that illness is not a pleasant experience for the child. Consider even a mild diarrhoea in a toddler. The child has to be cleaned many times a day, or go around with dirty diapers or pants, smelly, and uncomfortable; he may suffer vomiting, cough, or fever; he may not be hungry, or may not have a taste for the food offered, or may even be unable to eat at all; he will be in a bad mood; he will be tired or weak, unable to play with siblings; he may be actually suffering pain.
An assessment and analysis framework has been laid for the nutritional management of illness in the young child. The appropriate action that should follow involves different levels. Members of the international community, representing both the health and the nutrition areas, should promote appropriate recommendations, to be taken by specific programmes (at national, regional, and district levels). Investigators should undertake operations research designed to test the feasibility of proposed approaches.
There are several challenges to be met by research, including understanding local beliefs and practices, designing purposeful interventions that take those beliefs into account, evaluating the impact of those interventions, and refining these actions through reflective feedback from field staff to programme managers and to decision makers.
Health practitioners need to be updated in proper care practices, including managing illness, providing sound information to mothers for effective management at home, and offering care and understanding to the sick child. Mothers require proper information on adequate health and nutrition practices, to be used not only during illness, but equally importantly, during convalescence and wellness . We expect that this interactive process, involving different actors, will help to fine-tune the interventions that will eventually improve care and nutrition practices for children at need throughout the world.
We wish to acknowledge the useful comments provided by Dr. Kenneth H. Brown on an earlier draft of this paper.
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