Jpn. J. Infect. Dis., 55, 83-84, 2002

Short Communication

Prevalence of Intestinal Parasitic Pathogens in HIV-Seropositive
Individuals in Northern India
Kava Mohandas, Rakesh Sehgal*, Archana Sud1 and Nancy Malla
Department of Parasitology and 1Department of Internal Medicine,
Post Graduate Institute of Medical Education and Research,
Chandigarh, India(Received April 10, 2002. Accepted July 26, 2002)
SUMMARY: To assess the prevalence of intestinal parasitic infections in human immunodeficiency virus (HIV)seropositive subjects, fecal samples were collected from 120 HIV-seropositive patients and were analyzed forvarious intestinal parasites. Thirty-six patients (30%) were found to harbor an intestinal parasite. Cryptosporidium
parvum was the most common (10.8%), followed by Giardia lamblia (8.3%). Cyclospora cayetanensis andBlastocystis hominis each were detected in 3.3% of the patients, while Isospora belli and Enterocytozoon bieneusi
were each detected in 2.5% of the patients. The other parasites observed were Entamoeba histolytica/E. dispar in
two cases and hookworm ova in one patient. Of the 36 patients who tested positive for intestinal parasites, 27(75%) had diarrhea. The most common parasite, which was associated with diarrhea, was C. parvum. The present
study highlights the importance of testing for intestinal parasites in patients who are HIV-positive, and emphasizes
the necessity of increasing awareness among clinicians regarding the occurrence of these parasites in this population.
collected in 10% buffered formalin in clean wide-mouthedplastic containers and were subjected to concentration by aformalin-ethyl acetate sedimentation concentration technique(3). Specimens were examined as wet saline mounts and iniodine preparation for the detection of protozoan ova, cysts,and helminthic eggs and larvae (3). A modified version of theZiehl-Neelsen technique was used for staining for coccidia(4). Modified trichrome and Gram chromotrope stains wereused for detecting microsporidia (3).
A total of 186 fecal samples were collected from 120 HIVpositive patients. Among these, majority (113; 94.2%) wasfrom adults, with a male preponderance (64%).
Fifty-three (44.2%) patients had a history of diarrhea, which
was the presenting complaint in 26 (49.05%) subjects. Theremaining 27 patients (50.94%) had a history of episodic
diarrhea in the recent past. Thirty-six (30%) patients withdiarrhea were found positive for parasitic pathogens (Table1). These findings are similar to those from previous reports(1).
Among the 120 patients studied, 13 had C. parvum, 10 had
G. lamblia, 4 had C. cayetanensis, 4 had B. hominis; 3 had
I. belli, and 3 had Enterocytozoon bieneusi, while 2 had E.
histolytica/E. dispar, 1 had hookworm, and 1 had E. coli

Intestinal opportunistic parasitic infections in humanimmunodeficiency virus (HIV)-infected subjects present
commonly as diarrhea. Reports indicate that diarrhea occurs
in 30-60% of AIDS patients in developed countries and in
about 90% of AIDS patients in Haiti and Africa (1). Moreover,
HIV/AIDS is fast becoming a major threat in the Indian
subcontinent. As of June 2000, 98,451 HIV-seropositive cases
had been detected, with 12,389 cases of AIDS, and an estimated
3.7 million persons were infected with HIV (2). Chronic
diarrhea is responsible for considerable morbidity and mortality
in such patients. Protozoan parasites, namely Cryptosporidium
parvum, Isospora belli, Cyclospora cayetanensis, Microsporidia,
Entamoeba histolytica/Entamoeba dispar, and Giardia
lamblia account for a significant number of cases of diarrhea
in this population.
The Nehru Hospital attached to the Postgraduate Instituteof Medical Education and Research, Chandigarh, India, isa tertiary care hospital catering to a large population from
Northern India. The present study reports the prevalence ofintestinal parasites in HIV-seropositive patients coming to thehospital, and investigates the correlation of these infections
with diarrhea.
One hundred and twenty HIV-seropositive patients chosenrandomly from the Inpatient and Outpatient Departments ofInternal Medicine and allied specialties of the hospital wereincluded in the present study. Written consent was obtained
from all participants. HIV-seropositive patients were definedas those who had tested positive for HIV-1 and -2 infection
by two sequential ELISA tests (UBI: United Biochem Inc.,
Hauppage, N.Y., USA and Detect: Biochem Immunosystem,Montreal, Canada) and one rapid test (Immunocomb: Organics,Yavne, Isreal) (2). Fifty persons, employees of the Departmentof Parasitology at the Institute or their relatives, all apparently
healthy, were included as controls. Fecal samples wereTable 1. Intestinal parasites detected in HIV-positive individuals andtheir correlation with diarrhea*Corresponding author: Fax: +91-172-744401, E-mail: sehgalr@satyam.net.in
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Parasite detected

Number (%)

Diarrhea (%)

Cryptosporidium parvum
Giardia lamblia
Cyclospora cayetanensis
Blastocystis hominis
Isospora belliEnterocytozoon bieneusi
Entamoeba histolytica/E. dispar
Hookworm
Entamoeba coli13 (10.8)
10 (8.3)
4 (3.3)4 (3.3)3 (2.5)3 (2.5)2 (1.7)1 (0.8)1 (0.8)12 (92.3)
4 (40)
3 (75)
3 (75)
3 (100)3 (100)2 (100)00

conventional staining techniques.
Of the 50 control samples tested, G. lamblia was detected
in 4 subjects (8%), and E. hitolytica and C. parvum were
foundin 1 person each (2%).
In conclusion, the present study highlights the presence ofvarious intestinal parasites, especially E. bieneusi, which isreported in this area for the first time. Symptomatic parasitic
infections in patients infected with HIV were analyzed in thisstudy as well. Knowledge of the pattern of infection can often
guide therapy when resource limitations hamper the exact
diagnosis of the etiological agent in HIV-associated diarrhea.
ACKNOWLEDGMENTS

Fig. 1. Spores of E. bieneusi. Gram-chromotrope staining.
( ×1000 = Opti. mag. 10 × Subj. mag. 100)

We are grateful to Dr. Elizabeth Didier, Tulane Primate
Research Center, Covington, La, U.S., and we also wish tothank researchers at the London School of Hygiene andTropical Medicine, London, U.K., for their assistance inconfirming the isolates of E. bieneusi.

(Table 1). Diarrhea was present in 92.3% of the patients withC. parvum, 75% of the patients with B. hominis and C.
cayetanensis, 40% of the patients with G. lamblia, and in allof the patients with I. belli, E. histolytica/E. dispar, and E.
bieneusi (Table 1). Of the 53 patients with a history of diarrhea,
27 patients showed a presence of a parasitic etiology (50.9%).
CD4+ cell counts were available for 14 of 36 patients inwhom parasites were detected. A majority of the HIV/AIDSpositive patients did have diarrhea, irrespective of the CD4+
cell counts. The only exception was the patients with G.
lamblia infection, in whom diarrhea appears to be associatedwith counts of lower than 30 cells/mm3. C. parvum was themost common parasite isolated (10.8%) in HIV-seropositivepatients, whereas earlier reported rates ranged from 6-37%(1). G. lamblia was the second most common parasite
detected (8.3%). Earlier studies have reported rates of infection with G. lamblia between 1-11% (5). However, in 8% of
the normal controls, G. lamblia was detected. This findingshows that giardiasis does not occur in greater frequencies in
HIV-positive patients than in HIV-negative individuals. C.
cayetanensis was present in 3.3% of the patients, a rate thatis slightly lower than the 11% incidence reported by anotherstudy (6). Studies from Southern India have reported a higher
prevalence of I. belli than that of Cryptosporidium (7). E.
bieneusi was identified in three cases (2.5%) in the presentstudy (Fig. 1). This result appears to be the first report of thismicrosporidial species from this country. The relatively low
number of microsporidia identified may be due to thedifficulty of detecting these organisms in fecal specimens byREFERENCES
1. Framm, S. R. and Soave, R. (1997): Agents of diarrhea.
Med. Clin. North. Am., 81, 427-447.
2. Government of India (1999): Epidemiology of HIV/AIDS.
p. 1-11. In B.B. Rewari (ed.), Specialists Training andReference Module. National AIDS Control Organization,New Delhi.
3. Garcia, L. S. and Bruckner, D. A. (1993): Macroscopic andmicroscopic examination of fecal specimens. p. 508-512.
In L. S. Garcia (ed.), Diagnostic Medical Parasitology.
2nd ed. American Society for Microbiology, Washington,D.C.
4. Sehgal, R., Mahajan, R. C., Thapa, B. R. and Ganguly,
N. K.(1989): Cryptosporidiosis causing chronic diarrhea
in a child. Indian J. Pediatr., 56, 145-147.
5. Janoff, E. N., Smith, P. D. and Blaser, M. J. (1988): Acuteantibody responses to Giardia lamblia are depressed inpatients with AIDS. J. Infect. Dis., 157, 798-804.
6. Soave, R. (1996): Cyclosporiasis. Clin. Infect. Dis., 23,429-437.
7. Mukhopadhya, A., Ramakrishna, B. S., Kang, G.,Pulimood, A. B., Mathan, M. M., Zacharian, A. andMathai, D. C. (1999): Enteric pathogens in southern
Indian NIH-infected patients with and without diarrhoea.
Indian J. Med. Res., 109, 85-89.

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