Introduction

In general, diarrhoea may result from poorly absorbable osmotically active solutes in the intestinal lumen (osmotic diarrhoea), active ion secretion (secretory diarrhoea), deranged intestinal motility, altered mucosal morphology or loss of absorptive surface or a combination of the above mechanisms (₁). Gastrointestinal diseases particularly diarrhoea, is the commonest presentation of Acquired Immune Deficiency Syndrome (AIDS) in Africa. Diarrhoea occurs in nearly 90% of patients with advanced Human Immunodeficiency Virus (HIV) infection in Central Africa compared with 30% to 60% in developed countries (₂). Chronic diarrhoea is a very common presentation of HIV infection in Nigeria (₃,₄,₅) with a prevalence of 61% (₃).

Diarrhoea in patients with HIV infection may be attributable to a number of conditions which include infection with conventional and opportunistic microorganisms (₆, ₇), enteropathy (₈), malignancy and even treatment with various agents. Thus, HIV related chronic diarrhoea has a multi-factorial aetiopathogenesis with enteric parasites possibly playing a prominent role. Various microorganisms have been isolated from HIV-infected patients with chronic diarrhoea either singly or in combinations. These include bacteria, viruses and parasites, notably protozoa (₇, ₉,₁₀,₁₁,₁₂,₁₃).

The objective of this study was to determine the prevalence of intestinal parasites and their association with chronic diarrhoea in HIV-infected adult patients at Jos University Teaching Hospital, Nigeria.

Patients And Methods

Study Population

Clinical Evaluation

Sample Collection and Analysis

Results

The demographic data and relative prevalence of the intestinal parasites in the patients are shown on Table I. Sixty-seven of the 101 patients were positive, giving a prevalence of 66.3%, while 13.9% had polyparasitism. In relation to gender, males recorded a prevalence of 61.4% while the females had 70.2% (χ² = 0.6260; P>0.05). The age group of 15-24 years was the most significantly infected with a prevalence of 83.3%; while 25-34, 35-44, 45-54 and ≥ 55 years recorded 71.1%, 60.0%, 33.3% and 0.0% respectively (χ² = 89.4169; P<0.05).

Figure 1

Table 1: Demographic Data and Relative Prevalence of Intestinal Parasites in HIV Adult Patients with Chronic Diarrhoea in Jos University Teaching Hospital, Nigeria.

There was no significant difference in the prevalence of intestinal parasitosis in relation to the occupational status of the patients (χ² = 2.4398; P>0.05). The artisans and students recorded the highest prevalence of 81.0%, while civil servants, housewives, unemployed, medical workers and long-distance drivers recorded 56.4%, 70.0%, 50.0%, 75.0% and 66.7% respectively.

In relation to marital status, the unmarried patients had a prevalence of 71.4%, while the married patients recorded 63.6% (χ² = 0.3703; P>0.05). There was a significant difference in the prevalence of intestinal parasites in relation to the Body Mass Index (BMI) (χ² = 4.3172; P<0.05). The patients with normal weight recorded a higher prevalence of 84.6% compared with 60.0% in underweight patients.

There was a significant difference in the prevalence of intestinal parasites in relation to the frequency of diarrhoea per day (χ² = 9.3061; P<0.05). Patients who had a prevalence of ≥ 7 times had a prevalence of 100%, while those with 1-3 times and 4-6 times recorded a prevalence of 71.4% and 64.0% respectively. With respect to the duration of diarrhoea, there was no significant difference (χ² = 4.2141; P>0.05). Patients who had been having diarrhoea for 2, 3, 4 and ≥ 5 months recorded a prevalence of 62.8%, 69.7%, 69.6% and 50.0% respectively. There was no significant difference in the prevalence of the intestinal parasites in relation to organomegaly (χ² = 0.4167; P>0.05). Those with splenomegaly recorded 53.8% as against 45.5% in those with hepatomegaly.

Table 2 shows the prevalence of the individual parasites.

Figure 2

Table 2: Prevalence of Intestinal Parasites in HIV-Infected Adult Patients (n = 101) with Chronic Diarrhoea at Jos University Teaching Hospital, Nigeria.

Cryptosporidium parvum recorded the highest prevalence of 16.83%. The other parasites and their prevalences are Enterocytozoon bieneusi/Encephalitozoon intestinalis (8.91%), Cyclospora cayetanensis (1.98%), Isospora belli (0.99%), Entamoeba histolytica (9.90%), Giardia lamblia (1.98%), Hookworm (10.89%), Trichuris trichiura (5.94%), Ascaris lumbricoides (2.97%), Strongyloides stercoralis (1.98%), Schistosoma mansoni (3.96%) and Dicrocoelium dendriticum (4.95%). Candida species (a yeast) was detected in 9.90% of the patients without any intestinal parasite.

Discussion

This study has shown a very high prevalence of intestinal parasitosis in HIV-infected adult patients with chronic diarrhoea at Jos University Teaching Hospital, Nigeria. This prevalence rate of 66.3% is similar to the 50%-80% found by Ramakrishma in Vellore, India (₁₆) and 62.6% found by Tarimo et al (₁₇) in North Eastern Tanzania. The prevalence in this study is higher than that by Merlin et al (₁₈) in Argentina that recorded a prevalence of 52.3% in HIV patients with chronic diarrhoea and the 51.9% obtained by Awole et al (₁₉) in South Western Ethiopia. It is also higher than the 48.2% obtained at the same Jos University Teaching Hospital in 2000 by Keptcheu et al (₉).

The 16.83% prevalence of Cryptosporidium parvum infection in this study is consistent with the 20% and 22% ranges recorded by Valasquez et al (₂₀) in Argentine AIDS patients with chronic diarrhoea, although a higher prevalence was obtained in studies using jejunal biopsies (₂₁). On the other hand, a few studies in Nigeria (₂₂, ₂₃) did not detect C. parvum, and this is surprising as this coccidian parasite has even been found in the faeces of apparently healthy persons by Ikeh et al (₂₄) in their study in North Central Nigeria.

Enterocytozoon bieneusi/Encephalitozoon intestinalis infection that had a prevalence of 8.91% has been shown by various authors to be associated with chronic diarrhoea in AIDS patients (₁₁, ₂₀, ₂₅). Also, C. cayetanensis infection that recorded a prevalence of 1.98% has been associated with diarrhoea in AIDS patients (₂₆). Isospora belli with a prevalence of 0.99% in this study has similarly been associated with chronic diarrhoea in AIDS patients (₂₇). The coccidian parasites (C. parvum, I. belli, C. cayetanensis, E. bieneusi/E. intestinalis) accounted for 29.0% of chronic diarrhoea in this study and thus, efforts should be made to routinely search for these parasites in this category of patients. Although, cryptosporidiosis and microsporidiosis have been reported in immunocompetent patients, diseases caused by these parasitic agents are much more common in the immunocompromised hosts (₂₄, ₂₈).

The intestinal helminths that were detected in this study are similar to those that were reported by Keptcheu et al (₉) and Nwokediuko et al (₂₃). Both studies had shown that there might not be any relationship between intestinal helminths and diarrhoea in HIV infections. Tarimo et al (₁₇) in Tanzania detected similar spectrum of helminths, but concluded that only the protozoa in that study could have accounted for the chronic diarrhoea.

The eggs of Dicrocoelium dendriticum that were detected in the faecal samples were confirmed cases of spurious parasitism due to the frequent consumption of liver diets by the AIDS patients to improve their nutritional status. The detection of large numbers of Candida species in the absence of any parasitic intestinal pathogen might be suggestive that Candida species is an aetiological agent of diarrhoea in AIDS patients. The proliferation of Candida species in the intestinal tract might be due to the frequent use of broad spectrum antibiotics to stop or reduce the recurrent diarrhoea.

The high rate of polyparasitism encountered in the study could be due to the depressed immunity in the patients, coupled with the increased habit of trying to consume vegetables and fruits which may not be adequately washed. Our study has indicated that there is no positive relationship between intestinal parasitosis and gender, occupational status, marital status, duration of diarrhoea and organomegaly (P>0.05). On the contrary, there is a significant difference in the prevalence of intestinal parasitosis in relation to the age groups, BMI, and frequency of diarrhoea per day. Patients within the age groups of 15 years to 44 years were more significantly infected. This is expected as this is the sexually active group who are more likely to acquire HIV infection.

Patients with normal BMI were more significantly infected than the underweight patients. This might be attributed to the reason that the patients with normal BMI were still stronger than the underweight patients and so they are more likely to be exposed to these parasites. On the contrary, the underweight patients may be too weak to help themselves and so the care-givers do most of the house chores for them. They are therefore, less exposed to parasitic infections compared to the normal weight patients.

In conclusion, this study has shown that the coccidial parasites, which in most cases, are not routinely searched for in the diarrhoeic faecal samples, were responsible for some of the chronic diarrhoeal cases in HIV infected patients.

Correspondence to

Professor E.I. Ikeh
Department of Medical Microbiology
Faculty of Medical Sciences
University of Jos
P.M.B. 2084
Jos, Nigeria.