Prevalence of intestinal parasites in rural Southern Indians

Introduction

Intestinal parasites are widely prevalent in developing countries, probably due to poor sanitation and inadequate personal hygiene. It is estimated that as much as 60% of the world's population is infected with gut parasites, which may play a role in morbidity due to intestinal infections. The commonest parasitic infections reported globally are Ascaris (20%), hookworm (18%), Trichuris trichuira (10%), and Entamoeba histolytica (10%) (World Health Organization 1987). In India overall prevalence rates range from 12.5% to 66%, with varying prevalence rates for individual parasites (Amin et al. 1979; Ramesh et al. 1991; Singh et al. 1991, 1993). However, most reports are based on single samples from a variety of patient groups and controls, and the community prevalence has not been documented in detail. We now report a detailed analysis of the prevalence of potentially pathogenic intestinal parasites in a Southern Indian rural community and estimate the optimum number of stool samples which should be examined to give reliable and reproducible results. Evidence for differences in host response among asymptomatic individuals is also presented.

Materials and methods

Results

One or more potentially pathogenic parasites were found in 451 of the 993 stool samples. Nine potentially pathogenic parasites, 3 protozoan (E. histolytica, Giardia and Cryptosporidium) and 6 helminths (hookworm, Strongyloides, Ascaris, Hymenolepis nana, Trichuris and Enterobius vermicularis) were identified (Table 1). Parasites were present in the stool samples from 76 of 78 individuals and only 2 were apparently not colonized with potentially pathogenic parasites. A 4-month-old, exclusively breastfed child was found to excrete Giardia oocysts and hookworm ova; both parents had hookworm ova and Strongyloides larvae in their stool, but Giardia oocysts were not detected in any of their samples. The frequency of parasite detection increased with increasing number of stool samples that were examined (Figure 1). The examination of 3 samples gave 80% identification and a further 3 samples (giving a total of 6) identified 90%.

Table 1. Excretion of potentially pathogenic parasites by study subjectsf

The commonest parasites identified were hookworm in 48 (61.5%) subjects, Giardia in 42 (53.8%) and Cryptosporidium in 31 (39.7%). Of these, hookworm infestation was commoner in the older children (65%) and adults (71%) than in preschool children (22%) (Figure 2). Giardia and Cryptosporidium infections were more common in the children below 15 than in adults. Strongyloides and Enterobius were seen in less than 20% of the population and Ascaris and Trichuris were only occasional parasites being found in less than 5% of the population. Ascaris infection did not affect the two younger age groups and the highest prevalence was in the oldest age group (Figure 2). Hookworm and Giardia were found to be present in all 15 families, with Cryptosporidium in 14 and E. histolytica and H. nana in 10 families.

An average of 5.1 different parasites were found per family. The minimum number of parasites identified in any family was 3 and the maximum was 7 parasites. The maximum number of parasites in a single stool was 4, and that subject had 5 different parasites (Giardia, E. histolytica, Cryptosporidium, hookworm and Ascaris). Parasite excretion by all subjects was intermittent with no parasite found in all samples obtained from a single subject. On analysis of the excretion patterns for the commonest parasites, Giardia, Cryptosporidium, H. nana and hookworm, the infected subjects could be broadly divided into two groups: those who excreted parasites frequently or only occasionally (Figure 3). There was no significant correlation between frequency of parasite excretion and age or sex of the subjects.

Discussion

This study shows a much higher prevalence of intestinal parasites than previously reported from the Indian subcontinent (Table 2). However, the number of stool samples examined is also much higher than in any other study. Most of these reports were based on 3 samples per subject at the most, and while this may be appropriate when there are manifest gastrointestinal symptoms, it may be inadequate when intensity of infection is low and no symptoms are present. The data shown in Figure 1 show that by the 3rd sample, nearly 80% of the potential carriers are identified and 90% identification occurs by the 6th sample. In this asymptomatic population, 95% confidence of detection is achieved by examining 8 stool samples. The cost of such detailed studies have to be balanced against the potential gain in sensitivity and is likely to be acceptable in research situations only. The intermittent nature of parasite detection probably reflects the low density of parasite load in this asymptomatic group. In clinical practice, 3 stools should give a sensitivity of more than 75%.

Table 2. Prevalence of potentially pathogenic parasites reported between 1965 and 1996 from India

When the excretion of parasites by individual subjects is considered as in Figure 3, it is interesting to note that for 4 of the 5 most commonly encountered parasites, subjects fall into 2 groups. One group excretes the parasite in less than a third of their samples (infrequent excretors), whereas the other excretes parasites in over half their samples (frequent excretors). This is seen with both protozoan parasites, as in Giardia, as well as with helminths such as hookworm and H.nana. However, the asymptomatic subjects with Cryptosporidium all showed very infrequent excretion of oocysts. Based on these findings, it is possible that excretion of parasites by an individual is a host characteristic determined by the response of the host's immunological defence mechanisms to the parasite. Infrequent excretors may be those subjects with a high level of resistance to the parasite, in whom replication of the parasite is prevented to some extent. The lack of frequent excretors of Cryptosporidium could then be because replication of this parasite above a critical level would result in diarrhoea.

Striking differences in the prevalence of intestinal pathogens are seen when available reports from the Indian subcontinent were examined (Table 2). In several of these studies only a single stool sample was examined and in the 16 studies reviewed, parasite prevalence rates ranged from 12.5% to 67%, with prevalence rates for individual parasites varying widely between studies. E. histolytica appears to have the highest prevalence in large metropolitan cities, especially in coastal areas. The prevalence of Giardia appears to parallel this except in the present study. Unfortunately, similar techniques of sampling and laboratory methodology have not been used in these studies and we cannot draw meaningful conclusions about geographical differences.

When the results of our study are analysed as a percentage of the total number of samples examined, as in the studies in Table 2, the total percentage prevalence of parasites appears to be 45.4% rather than the actual prevalence in the population of 97.4% of individuals excreting parasites. This highlights the need for repeated sampling in order to determine accurate prevalence rates in any population.

The extremely high prevalence rates in this study may be a function of the unprotected water supply and the defaecation practices of the villagers. Defaecation occurs in the surrounding fields and the stools are exposed to scavenging animals and the drying effects of the sun and wind. Animals and wind have been proposed as sources of water supply contamination, and of direct infection (Bidinger et al. 1981).

The age-specific prevalence rates of Giardia, Cryptosporidium and hookworm reflect their modes of transmission (Figure 2). Giardia and Cryptosporidium are transmitted by the faecal-oral route and are commoner in children, the lower prevalence in adults also suggesting acquired immunity after repeated infections. Hookworm infestation results from penetration of the skin by filariform larvae and is mainly seen in older age groups who are more likely to be exposed to the larvae while walking barefoot in the fields.

The high prevalence of potentially pathogenic intestinal parasites in this rural population is the consequence of the large number of samples examined from each individual and the actual parasite load in each person could be low. None of the individuals had any apparent ill effects because of the parasites. We have also reported a high prevalence of asymptomatic colonization of the intestinal tract by pathogenic enteric bacteria and enteroviruses in this population (Patel et al. 1984; Mathan & Rajan 1986). This would appear to be the norm for gut ecology in many preindustrialized countries. The bacteria, parasites and viruses colonizing the gastrointestinal tract are in apparent symbiotic balance with the host. It is likely that a combination of host-related factors such as nutritional status, local and systemic immunity also play a major role in determining whether presence of a potential pathogen results in clinical disease and morbidity. In this study, although there was no demonstrable effect on the health of the subjects in the form of symptomatic disease, the observation that subjects in the same environment can excrete parasites with high or low frequency indicates that host-related factors probably determine parasite excretion rates. Acute infectious diarrhoea is likely to be the result of an alteration of the environment of the gut associated with presence of a pathogenic organism and a better understanding of gut ecology may help in devising optimum methods of control.