Relative Importance of Enteropathogens
A large number of bacterial, viral, and parasitic agents have been associated with diarrhea in both developing and developed countries. Because the highest rates of diarrheal diseases and the most severe consequences generally occur in young children, most studies have focused on this age group. Older children and adults may become ill from the same enteropathogens, but the relative frequencies with which these organisms are encountered varies because of immunity acquired from prior infection or from differential exposure to the various pathogens.
Community-based studies are those in which household visits are made to identify cases of diarrhea and to collect fecal specimens for identification of enteropathogens. These studies give the best measure of the overall incidence of diarrheal disease because they are not based on severity or care-seeking and are not subject to bias in the ascertainment of cases. In a review of 61 studies (published 1990-2002) with comprehensive microbiology from developing countries, enterotoxigenic
Escherichia coli (ETEC) constituted the largest proportion of episodes with a median of 14.1% (
Table 20-3). The next most commonly found organism has been
Giardia lamblia. Campylobacter species, enteropathogenic
E. coli (EPEC), and rotavirus were identified in 7-8% of these diarrheal episodes. Other organisms were less frequently observed. The relative importance of these organisms was rather variable in the different studies.
Noroviruses are emerging as an important pathogens leading to diarrhea and vomiting. Because this kind of infection is typically epidemic and seasonal, it is often not included in yearlong studies prospective studies. In the United States, norovirus causes more than 21 million gastrointestinal illnesses each year, many of which will manifest as severe acute diarrhea disease.
26
Studies in health facilities—either outpatient clinics or hospital wards—involve a more selected group of patients who have sought care because of an illness of greater severity. A review of 98 studies done in outpatient health facilities in developing countries found that rotavirus was the most frequent enteropathogen, with a median incidence of 18% (
Table 20-3). However, these studies demonstrated that bacterial pathogens predominated overall, accounting for approximately 40% of illnesses. Of these, the most common was C.
jejuni. As illustrated in the range of percentage identification in
Table 20-4, each of these bacterial pathogens can be very frequent in some settings. Among the parasites, C.
parvum and G.
lamblia were the most frequently identified. A review of 107 studies in hospitalized children found that rotavirus was the most common
pathogen, followed by EPEC and ETEC (
Table 20-5). A number of recent studies in hospitalized children with diarrhea in East Asian countries have found that 40-60% had rotavirus identified.
27,
28
In general, community-based studies identified an enteropathogen in approximately half of the episodes, and the health facility-based studies identified an enteropathogen in nearly 75% of the episodes— although these rates are difficult to estimate from the studies available, because most studies do not set out to test for all possible pathogens. The detection tests for many of the enteropathogens do not have optimal sensitivity, so these studies may have underestimated their incidence. Although it is likely that these enteropathogens individually account for only a small proportion of the episodes, collectively they may cause many of the episodes not associated with one of the more common enteropathogens. Other enteropathogens of interest are adenovirus and astrovirus,
29,
30 as well as
Bacteroides fragilis and
Clostridium difficile,31 particularly among patients taking antibiotics.
32
The identification of an enteropathogen from feces during diarrhea does not necessarily mean that that organism is causing the illness. In fact, studies that have performed comprehensive microbiology analyses have often found two or more enteropathogens simultaneously, making it difficult to assign causality. These mixed infections could occur because the individual is exposed simultaneously or sequentially, or an individual may have an asymptomatic infection with one enteropathogen at the time of exposure to another disease-causing agent.
Asymptomatic enteric infections are common in developing country populations but less so in developed country settings. In community-based studies, routine assessment of enteropathogens allows for a comparison between times when the children have diarrhea and when they are healthy. Community-based studies often find a similar rate of identification of enteropathogens in children when they have diarrhea and when they do not. For example, in nine community-based studies in developing countries, the median identification of
Campylobacter species was 8 % during diarrhea, compared to 7% when patients did not have diarrhea (
Table 20-6). Some enteropathogens, such as rotavirus, may have a higher rate of identification during diarrhea episodes. In health facility-based studies, children who came to the same facility for a reason other than diarrhea may be used as controls. Often the relative prevalence of different enteropathogens is more distinct between diarrhea cases and controls in these studies.
The pathogenicity (i.e., the number of infections with diarrhea divided by the total number of infections) varies by enteropathogen and in some cases by age (
Table 20-7). For example, the pathogenicity of rotavirus is lower in the first 6 months of life than in the second 6 months, presumably due to passive protection from maternally derived antibody in early infancy.
33 In contrast, some pathogens, such as
Shigella species, have a higher pathogenicity early in childhood. This difference may arise because the initial infection induces some immunity, which protects more effectively against subsequent illness than against infection.
The virulence (i.e., the number of severe illnesses divided by the total number of illnesses) may also vary by enteropathogen. This can be illustrated by the propensity of the organism to cause an illness that leads to dehydration. In community-based studies in Bangladesh,
34,
35 children with rotavirus diarrhea or cholera are most likely to develop dehydration (
Table 20-8). Those persons with ETEC had a modestly increased rate of dehydration compared with all other types of diarrhea.
In the United States, the relative importance of the various enteropathogens differs from that in developing countries (
Table 20-9). In studies done in health facilities, rotavirus is the most important enteropathogen associated with diarrhea, just as it is in developing countries, but this is expected to change owing to the widespread use of the rotavirus vaccine since 2006.
36 In general, the bacterial causes of diarrhea are less important in developed countries, although
Campylobacter species and
Salmonella species may be important in some settings. This pattern may be shifted closer to a developing country pattern in certain higher-risk populations. For example, residents of Indian reservations in the United States have shown higher rates of diarrhea than the general population, although good access to medical care has now reduced the diarrheal mortality to a very low level.
37,
38 In such settings (
Table 20-10), rotavirus is still the most important pathogen, but other organisms such as ETEC and
Campylobacter species may play a more prominent role than they do in the general U.S. population.
In the United States, it is estimated that each year there are 1300 deaths, 56,000 hospitalizations, and 9.4 million illnesses caused by foodborne infections, counting both outbreaks and sporadic cases caused by 31 major enteric pathogens.
39 In 2006, the CDC reported more than 1200 outbreaks of foodborne disease.
40 In the 49% of cases for which a cause was identified, norovirus was the pathogen most often identified, being responsible for 54% of the outbreaks. Traditionally,
Salmonella, Staphylococcus, and
Clostridium perfringens have been considered the main responsible organisms, and they continue to be important. A number of other organisms that are commonly spread by the foodborne route (notably
Campylobacter and
E. coli 0157:H7) have also caused substantial morbidity.
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