Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases, Part II: Diet and Activity During Pregnancy and Lactation (1992)

Enteric pathogens are transmitted by the fecal-oral route, and foods ingested by children are major vehicles of this transmission. In developed countries, the enteric pathogens most commonly associated with food-borne disease are Salmonella sp., Staphylococcus aureus, Clostridium perfringens, and Bacillus cereus (Horwitz, 1977). Salmonella also occurs in developing countries, but it is not responsible for a large fraction of episodes. S. aureus, C. perfringens, and B. cereus almost certainly cause enteric illnesses in children in developing countries, but the importance of these agents is unknown. These organisms have been implicated in outbreaks occurring in food service establishments and the home. Outbreaks are defined as two or more persons with a similar illness and an epidemiologic and laboratory investigation which confirms that a food was the source of illness. The incrimination of S. aureus or C. perfringens as the cause of an outbreak is particularly problematic since both organisms are normally found in stools of healthy people. Phage typing or serotyping of the isolates from stools of a number of ill individuals and from food is required to determine that these agents are responsible for the outbreak. The incrimination of these agents as a cause of a single case of enteric illness is almost impossible. However, if these foodborne enteric pathogens can cause outbreaks involving multiple individuals, they can certainly cause single, sporadic cases in susceptible individuals.

In developing countries, enteric pathogens can be found in at least half of the children with endemic diarrhea, with most of the agents being bacterial (Black et al., 1982b). The most commonly found bacterial pathogens in children in developing countries are enterotoxigenic and

enteropathogenic E. coli and Shigella sp. They can be transmitted by means of contaminated food, although the relative importance of this route compared with water contamination or direct person-to-person transmission is unknown. Other bacterial pathogens, such as Campylobacter jejuni or vibrios also could be transmitted by food in developing countries. It is also likely that certain viral pathogens, such as 27nm viruses like Norwalk virus, and parasitic agents, such as Entamoeba histolytica, Giardia lamblia, or Cryptosporidium sp. are often ingested with food. The offending organism may be present in raw foodstuffs or it may be introduced during food preparation or storage. It then replicates under suitable temperature and pH conditions. These conditions, which can also occur because of critical defects in food handling in developed countries, are very common in household settings in developing countries. Bacterial multiplication may be particularly important for some pathogens, such as enterotoxigenic E. coli or vibrios, that require a large ingested dose to cause disease.

Food control investigations often use enumeration of indicator organisms, rather that isolation of pathogens (Frank and Barnhart, 1986). These organisms, predominantly E. coli, are indicators of fecal contamination, since that is their usual origin. Coliform or fecal coliform indicators have been used extensively to assess water quality, and the presence of any coliforms in water is considered unacceptable for potable water (APHA, 1989). The presence of indicator bacteria in food simply suggests that there is a risk that food also is contaminated with an enteropathogen. In settings with poor sanitation and hygiene, that risk of contamination is determined in part by the frequency of enteropathogens in the stools of healthy people, and the prevalence of diarrhea during which higher numbers of enteropathogens are excreted.

In studies done in Bangladesh, El Salvador, India, Indonesia, Jamaica, Peru, and The Gambia, high levels of fecal bacteria were found in the milk or formula given to infants (Barrell and Rowland, 1979; Black et al., 1982b; Black et al., 1989). A similar hazard of fecal contamination has also been demonstrated with traditional weaning foods (Black et al., 1982a, 1989; Rowland et al., 1978). Cereal gruels and other foods specially prepared for infants were the most frequently and heavily contaminated. Pathogens, namely, enterotoxigenic E. coli and Salmonella sp. and possible pathogens, including Aaromonas hydrophila and Vibrio cholerae non-O group one, have been isolated from foods consumed by infants in studies done in The

Gambia, Bangladesh, and Peru (Black et al., 1982a, 1989; Rowland et al., 1978).

Water often is used for the preparation of liquids and other foods given to infants, and if it is fecally contaminated, it can contribute to the contamination of weaning foods. Water that has been mixed with milk or other foods often is ingested before it has been boiled adequately or given some other treatment, as indicated by the demonstrated high levels of fecal coliforms and by the isolation of specific pathogens, such as enterotoxigenic E. coli (Black et al., 1982b). In addition, the limited availability of water contributes to poor personal and domestic hygiene, which leads to food contamination.

Feeding bottles and nipples are possible sources of contamination of milk (Phillips et al., 1969). For example, in Nigeria 48 percent of feeding bottle nipples had E. coli contamination, and enteropathogenic E. coli was found on 24 percent of the nipples (Elegbe et al., 1982). In Peru, 35 percent of nipples and 23 percent of feeding bottles contained E. coli, which were also commonly found on spoons (Black et al., 1989). Cups, spoons, feeding bowls, can openers, and the hands of food preparers have also been found to be contaminated, although to a lesser degree than feeding bottles. In fact, boiled teas served in cups in Peru were rarely contaminated, but the same teas served in feeding bottles contained E. coli in 31 percent of the samples (Black et al., 1989).

Poor personal hygiene of food handlers, inadequate cooking, and storage of food at improper temperatures (Frank and Barnhart, 1986) are also important determinants of fecal coliform contamination and growth in food in households in developing countries. These households also have overcrowding, poor sanitation, and insufficient water. An important specific hygienic practice is handwashing (Feachem, 1984). Limited evidence indicates that a substantial reduction in diarrhea rates can be achieved by improved handwashing practices. The feasibility and essential components (e.g., quantity of water and/or soap) of hygiene education programs remain to be determined.

Raw foods are often contaminated with coliforms, although this is less of a problem with dry foods than with foods having a high moisture content With the application of beat, usually boiling, they are usually heated to sufficient temperatures to kill the bacteria. However, secondary contamination often occurs from the introduction of contaminated utensils or hands into the foods. The bacteria thus introduced can then multiply in the food.

A very serious hazard in food preparation is the storage of food at ambient temperature in households in developing countries. The proportion of foods with contamination and the count of indicator organisms were found to increase with the length of storage time after preparation in studies done in Bangladesh and The Gambia (Black et al., 1982a; Rowland et al., 1978). In other studies weaning foods such as gruels were found to be contaminated, and it was demonstrated that there is an even greater increase in bacterial contamination if consumption is delayed. It is likely that the seasonality of bacterial diarrheas, with a predominance in the warmer months, reflects the greater survival and multiplication of pathogens in food at higher environmental temperatures (Black et al., 1982b).

A special concern with regard to storage is that the heat-resistant spores of some pathogenic bacteria, such as C. perfringens and B. cereus, survive cooking and can germinate and multiply during subsequent storage. Inadequate reheating then permits ingestion of high numbers of the pathogens, and even subsequent boiling is not sufficient to destroy heat-stable toxins such as the emetic toxin of B. cereus. The importance of these factors is unknown since the role of organisms such as C. perfringens or B. cereus in diarrhea in people in developing countries is poorly understood.

Microbial survival or multiplication is affected by the chemical, physical, and microbiological characteristics of food (Genigeorgis, 1981). Survival or growth of enteropathogens in food can be reduced or eliminated through alteration in specific characteristics, such as the microbial flora, pH, moisture content, oxidation-reduction potential, available nutrients, natural inhibitors of microbial growth, or addition of food preservatives. Each of these has been used to inhibit bacterial growth in processed foods. Many have also been used in traditional food preparation methods because they delay food spoilage caused by microbial growth, although few have been purposefully used to inhibit enteropathogen multiplication in weaning foods in developing countries.

One of the most important factors with regard to multiplication of enteropathogens is the degree of competition from other organism in the food. Food-borne pathogens are not strong competitors and are rather easily suppressed by the nonpathogenic flora of the food. This inhibition of pathogen growth or of production of toxins can be mediated by a decrease in pH from the microbial production of certain acids, hydrogen peroxide, or other inhibitory substances (including antibiotic-like substances), or by microbial competition for essential nutrients. Milk products fermented by lactobacilli (e.g., yogurt) contain lactic acid, hydrogen peroxide, and antibiotic-like substances, which may inhibit the growth of enteropathogens.

The relationship between weaning food contamination and diarrhea can be inferred from available evidence. The high relative risk observed in infants given weaning foods (even supplementary water) compared with that observed in exclusively breastfed children in many countries suggests that food contamination may cause diarrhea in these children. The high levels of fecal contamination and the isolation of specific pathogens from some weaning foods further support the supposition that weaning foods are an important vehicle for transmission of enteric pathogens, and in one study there was a significant relationship between the degree of fecal contamination of weaning food and a child's annual incidence of diarrhea associated with enterotoxigenic E. coli (Black et al., 1982a).

The greater availability of water, improved sanitary conditions, and enhanced concern about domestic hygiene would likely reduce transmission of enteropathogens via foods, as well as by other routes. Specific hygienic behaviors such as handwashing have been shown to reduce the incidence of diarrhea, even in developing countries (Feachem, 1984).

Virtual elimination of feeding bottles has been successfully accomplished in Papua New Guinea and has been reported to reduce the rate of diarrhea. Even if their elimination cannot be achieved, improved cleansing of bottles and nipples may reduce the risk of contamination of milk or formula by (1) boiling of bottles and nipples and (2) using disinfectant solutions (commonly, 1 percent hypochlorite solution). Proper use of such procedures is often difficult because poor households may have only one feeding bottle, which is constantly in use, i.e., it contains milk or formula that is consumed by the infant ''on demand'' or the proposed methods are not applied appropriately. One study in Nigeria reported that soaking of bottle nipples in hypochlorite solution is associated with a marked reduction in bacterial contamination, even in comparison to working with detergents (Elegbe et al., 1982).

The storage of weaning foods for many hours in the home provides an opportunity for secondary contamination of foods from feeding utensils or hands, for germination of spores, for multiplication of enteropathogens, and for production of enterotoxins. Reheating to a proper temperature for sufficient time, which is not commonly done, would avert the problems that arise from storage, except for those caused by heat-resistant toxins. Without refrigeration it is difficult to achieve a sufficiently cool temperature to limit microbial multiplication in hot tropical climates. However, the safest practice would be to eat all foods at each setting and to prepare new servings, at least for infants, at the next meal. If this cannot be done, leftover foods should be reheated for a sufficient amount of time and at a sufficient temperature to kill pathogenic bacteria.

Infant feeding practices are important determinants of diarrhea in infants and children in developing countries. Since contaminated weaning foods are an important route of transmission of enteric pathogens, reduction in food contamination should reduce the incidence of diarrhea. Interventions might include improved personal and utensil hygiene, reduction of storage time of weaning foods, or improvement of storage conditions or the use of processed, e.g., fermented foods that resist contamination. Such interventions should become important components of programs to control diarrhea.

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