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 ~  Abstract
 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusion
 ~ Acknowledgment
 ~  References
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  Table of Contents  
Year : 2013  |  Volume : 31  |  Issue : 2  |  Page : 161-165

Prevalence of intestinal parasitic infections in HIV-infected individuals and their relationship with immune status

1 Department of Microbiology, Vardhman Mahavir Medical College and Safdarjung Hospital, New Delhi - 110 029, India
2 Department of Microbiology and Apex Regional STD Teaching, Training and Research Centre, Vardhman Mahavir Medical College and Safdarjung Hospital, New Delhi - 110 029, India
3 Department of Medicine, Vardhman Mahavir Medical College and Safdarjung Hospital, New Delhi - 110 029, India

Date of Submission09-Aug-2012
Date of Acceptance17-Feb-2013
Date of Web Publication19-Jul-2013

Correspondence Address:
M Bala
Department of Microbiology, Vardhman Mahavir Medical College and Safdarjung Hospital, New Delhi - 110 029
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0255-0857.115247

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 ~ Abstract 

Background and Objectives: Intestinal parasitic infection is a common entity in patients infected with human immunodeficiency virus (HIV). These infections may lead to fatal complications in the immuno suppressed individuals. The aim of the present study was to determine the prevalence of intestinal parasitic infections in HIV sero-positive patients and their relationship with the immune status of individuals. Materials and Method s: Fecal samples from 100 HIV sero-positive and an equal number of HIV sero-negative individuals were collected and examined for enteric parasites by direct microscopy. CD4 counts were carried out in only HIV sero-positive patients. Prevalence of intestinal parasites in patients with CD4 count <200 cells/μl, 200-499 cells/μl, and ≥500 cells/μl in HIV-infected patients were compared. Results: Enteric parasites were detected in 59.3% HIV-infected patients with CD4 count <200 cells/μl as compared with 23.5% in patients with CD4 count >200 cells/μl (P < 0.01). Prevalence of coccidian parasites was significantly (P < 0.01) higher (14%) in HIV sero-positive subjects compared with HIV sero-negative subjects (2%). Isospora belli (25%) was the most common parasite with CD4 count <200 cells/μl, followed by Cryptosporidium parvum (12.5%). Prevalence of intestinal parasitic infections was significantly higher in patients with diarrhea, 73.6% than without diarrhea, 25.9%, (P < 0.05). The mean CD4 count of HIV sero-positive patients presenting with diarrhea was significantly (P < 0.01) lower (181.26 ± 135.14) than without diarrhea (352.02 ± 204.03). Conclusion: This study emphasizes the need for routine screening of parasites especially in patients with lower CD4 count so as to decrease the morbidity by ensuring the early treatment of the cases.

Keywords: CD4 count, diarrhea, Human immunodeficiency virus, intestinal parasitic infections

How to cite this article:
Gupta K, Bala M, Deb M, Muralidhar S, Sharma D K. Prevalence of intestinal parasitic infections in HIV-infected individuals and their relationship with immune status. Indian J Med Microbiol 2013;31:161-5

How to cite this URL:
Gupta K, Bala M, Deb M, Muralidhar S, Sharma D K. Prevalence of intestinal parasitic infections in HIV-infected individuals and their relationship with immune status. Indian J Med Microbiol [serial online] 2013 [cited 2020 Nov 27];31:161-5. Available from:

 ~ Introduction Top

Human immunodeficiency virus (HIV) infections have continued to pose a serious challenge to the global health community over the past three decades. At the beginning of 1986, there were 20,000 reported acquired immune deficiency syndrome (AIDS) cases worldwide [1] and India had no reported cases of HIV/AIDS. HIV emerged later in India than it did in many other countries and infection rates soared throughout the 1990s affecting all sections of Indian society. HIV has spread beyond the "at risk" groups to the general population and from urban to rural areas (overall almost 57% cases are in rural areas). [2] Currently, there are 22.7 lakh people with HIV/AIDS in India with an estimated adult prevalence of 0.29%. [3]

The initial stage of HIV infection involves specific interaction of the virus with CD4 molecule on the T lymphocyte surface. When the CD4 cell counts falls below 200 cells/μl, there is irreversible breakdown of immune defense mechanism, and the patient becomes prey to a variety of human opportunistic pathogens like bacterial, viral, fungal, and parasitic.[4] Therefore, estimation of CD4 lymphocyte is one of the measures of ascertaining the immune competence of the HIV-infected individual throughout the broad spectrum of HIV disease. [5],[6]

The spectrum of opportunistic infections (OIs) in the HIV-infected subjects varies from one region to another. Diarrhea is a relatively common complication in symptomatic HIV infected individuals and may have multiple etiologies. [7] The infectious etiological agents for diarrhea include both opportunistic and nonopportunistic pathogens. The most commonly reported opportunistic parasites include Cryptosporidium parvum, Isospora belli, Cyclospora species, Microsporidium species, Strongyloides stercoralis, Giardia lamblia, and Entamoeba histolytica. [8]

Opportunistic agents usually cause severe, chronic or frequent gastrointestinal disease and nonopportunistic agents usually cause acute, treatable diarrheal illness. [9],[10] Chronic diarrhea defined as persistence of diarrhea beyond 4 weeks is a common symptom in HIV-infected individuals in tropics. [11] Reports indicate that diarrhea occurs in 30-60% of AIDS patients in developed countries and in about 90% of AIDS patients in developing countries. [12] These superimposed infections are one of the major health problems among HIV sero-positive patients due to defect in immunity. The progressive decline and ultimate collapse of immune system functions, which are characteristic for AIDS, usually result in morbidity and ultimately death due to OIs. [13] Because many of these infections are amenable to treatment, an early and accurate diagnosis is important. India is now facing the HIV epidemic, a good number of HIV sero-positive patients presents with diarrhea. Screening of the coccidian parasite is still not carried out as a routine test in HIV sero-positive patients in most of the laboratories and information available among clinician about the prevalence of OIs is scarce. Moreover, the published reports are lacking on data on correlations of CD4 levels with rate of opportunistic intestinal parasites. [14],[15],[16] We, therefore, planned to study the prevalence of various intestinal parasites in 100 HIV sero-positive and 100 HIV negative patients and the correlation of these intestinal parasitic infections with CD4 + count and clinical profile of HIV sero-positive patients.

 ~ Materials and Methods Top

Study design

A case-control study was conducted prospectively from January 2011 to December 2011 in the Department of Microbiology, Regional STD Center and anti retroviral Therapy (ART) clinic of a tertiary care super specialty hospital of north India. Being a tertiary care hospital, it caters to a large number of referred patients from neighboring states of Bihar, Jharkhand, UP, Haryana, and Rajasthan.

Study cases and controls

A total of 100 patients of both sexes, >12 years of age, who were HIV positive (according to National AIDS Control Organization HIV testing guidelines) with or without diarrhea were included as cases. While 100 patients of both sexes of >12 years of age, who attended various out patient departments (OPDs) with diarrhea because of malabsorption syndrome, lactose intolerance, immuno-compromised state due to cancer, malignancy, etc., and patients having diarrhea because of their unhygienic living conditions were included in this study as controls. A questionnaire was filled up for each patient to document the age, sex, geographical area, occupational status, mode of exposure, exposure to antibiotics, and complaints of diarrhea.

Stool samples were collected in sterile, screw capped, disposable plastic containers, and were immediately transported to Department of Microbiology, for parasitological study. Blood sample (2 ml) for CD4/CD3 cell count was collected aseptically in the ethylenediaminetetraacetic acid (EDTA) container.

Stool examination

All stool samples were examined for cyst, trophozoites, and larvae of parasites using direct (saline and iodine wet mount) microscopy and after formol ether concentration technique. Modified acid fast staining was done for detecting oocysts of Cryptosporidium, Isospora, and Cyclospora. Modified trichrome and Giemsa staining was done especially for detecting Microsporidial spores. [17]

CD4 cell estimation

The estimation of CD4, CD3 lymphocytes and CD4/CD3 was done by Fluorescent Activated Cell Sorter (FACS) count system (Becton Dickenson Immunocytometry system, San Jose, CA 95131-1807.) at the Regional STD Center.

Data analysis

The data were analyzed using the Chi-square test to compare the frequency data. After categorizing the CD4 counts in different categories, the statistical significance between intestinal parasitic infection and CD4 count categories was carried out by Chi-square test.

Ethical considerations

The study protocol was approved by the Ethical committee (letter no.-08-11-EC 5/18) for research projects of Safdarjang hospital. Additionally, after explaining the importance of the study briefly an informed consent was obtained from the study participants. Anyone not willing to take part in the study had full right to do so and confidentially of the study participants was also maintained. Finally patient's findings were reported to the appropriate physician at the ART center of Safdarjang hospital in order to manage and treat patients appropriately.

 ~ Results Top

The mean age of HIV-infected subjects was 33.70 ± 11.11 years, with 66 males and 34 females. Diarrhea was the presenting complaint in 19 of them while 8 patients had pulmonary tuberculosis (TB), 8 patients presented with weight loss, 8 with undiagnosed fever, 6 with pain in abdomen, 3 with skin rashes, and only 1 patient complained of vaginal discharge. In the control group, the mean age of patients was 31.54 ± 10.22 years, with 61 males and 39 females. Hence the two groups were comparable with respect to age and sex (P > 0.05). Distribution of intestinal parasites was also studied according to age, sex, geographical area, occupational status, and mode of exposure.

Intestinal parasites were seen in 35 (35%) of the 100 samples from HIV-infected individuals and in 25 (25%) of HIV negative samples. A total of 43 enteric parasites were recovered in HIV positive stool samples and 8 patients were found to be infected with more than one enteric parasites. Out of the 43 enteric parasites in HIV sero-positive individuals, Isospora belli 10 (23.2%), was found to be the predominant one among the pathogenic protozoal parasites followed by Giardia lamblia 8 (18.6%), Cryptosporidium parvum 4 (9.3%), Entamoeba histolytica 4 (9.3%). In the group of nonpathogenic parasites, Entamoeba coli 7 (16.2%) was found to be the most common followed by Endolimax nana 2 (4.3%) and Trichomonas spp. 2 (4.3%), Chilomastrix mesnili 1 (2.4%), and Blastocystis hominis 1 (2.4%) Only three helminthic parasites, Ascaris lumbricoides, Ancylostoma duodenale, and Strongyloides stercoralis were found in cases (2.3% each) [Table 1]. Dual parasitic infections were found more common 8 (22.8%) in cases as compared with controls 3 (12%).
Table 1: Distribution of enteric parasites according to CD4 count of HIV-infected patients

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Among the 25 stool samples from the control group, most common parasite was Entamoeba histolytica 9 (28.1%), followed by Entamoeba coli 7 (21.8%), Giardia lamblia 5 (15.6%), Isospora belli, Endolimax nana, Iodoamoeba buteschili, Blastocystis hominis, Trichomonas spp. each 2 in number (6.2% each). The number of helminthic parasites were only three as was observed in the cases and the parasites were Ascaris lumbricoides and Ancylostoma duodenale and Hymenolepsis nana in (3.1% each) [Table 1].

Among the HIV positive patients, 19 (19%) had presented with history of diarrhea and rest 81 (81%) had other nondiarrheal complaints. Intestinal parasites were detected more commonly (14/19, 73.7%) in patients with diarrhea than in (21/81, 25.9%) nondiarrheal patients (P < 0.01). Coccidian parasites were detected more commonly (13/19) in diarrheal than in nondiarrheal patients (1/81) (P < 0.01) [Table 2].
Table 2: Parasite recovered from diarrheal and nondiarrheal samples of HIV-infected patients

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The mean CD4 count in diarrheal patients (181 ± 135.14) was significantly lower (P < 0.05) than in patients without diarrhea (352 ± 204.03). In the present study it was observed that the prevalence of intestinal parasitic infection in HIV sero-positive patients (54.2%) was significantly higher in those having CD4 count below 200 cells/μl (P < 0.01). Most predominant parasite in individuals having CD4 count < 200 cells/μl was Isospora belli [Table 1]. Our study reflected that the prevalence of coccidian parasite was significantly more (P < 0.01) in HIV sero-positive patients (14%) than HIV sero-negative subjects (2%). The mean CD4 count in those patients harboring these coccidian parasites was found to significantly (P < 0.01) lower (119.78 ± 93.7) cells/μl than patients infected with other noncoccidian parasites (286.71 ± 169.42) cells/μl.

 ~ Discussion Top

HIV infection is a major threat to public health in India. Numerous OIs occur due to deterioration of the immune system because of HIV infection, of which intestinal parasitic infection is a universally recognized problem. This largely presents with diarrheal symptoms leading to life threatening complications. Clearly there is a need to study the magnitude of problem and develop a plan for intervention.

In the present study, overall prevalence of intestinal parasitic infection in HIV-infected individuals (35%) was found to be considerably higher than HIV negative individuals (25%). Most of the studies performed in India and other countries reported a higher prevalence of enteric parasites ranging from 30% to 60%, [14],[18],[19] leaving only few studies where the prevalence was reported lower than our study. [20],[21] However, our results were in accordance with the study of Kulkarni et al., performed in National AIDS Research Institute, Pune in 2009 [22] and the prevalence rate was 35%. A higher percent of all enteric parasites was found in controls as compared with cases because all the patients from controls were having diarrhea and most of them were from slum areas and unhygienic living conditions.

Isospora belli (23.2%) was the most common parasite seen in present study in HIV-infected individuals. Earlier studies have reported Cryptosporidium parvum as the predominant one. [23],[24],[25] A lower prevalence of Cryptosporidium parvum (9.3%) was noticed in the current study as compared with other studies done in Delhi. [23],[26],[27] The lower prevalence for Cryptosporidium in our study could be due to the methodological differences because by the use of only conventional acid fast staining for identification of Cryptosporidium parvum; there is possibility of missing the parasites because of their smaller size, 4-6 μm. Moreover, oocyst excretion is variable and single stool specimen processing might underestimate the prevalence of Cryptosporidium.

The result of the present study was in accordance with the studies done in other parts of India with prevalence ranging 3.7-11.8%. [14],[20],[28] No Cyclospora and Microsporidia were reported in the current study, because 12 patients gave history of cotrimoxazole therapy within 3 weeks of sample collection. Cotrimoxazole is only effective against Isospra and Cyclospora infections but not against Cryptosporidium, the only effective drug against Cryptosporidium infections is nitazoxanide. There were some limitations in this study, which include a limited sample size, resource constrains to perform sensitive tests like polymerase chain reaction (PCR) and immunoflourescence for confirmation of parasites like Cryptosporidium and Microsporidia. In addition, the participants were unwilling to participate in follow-up information regarding episodes of diarrhea and effectiveness of prophylactic measures.

We have found that extent of deterioration of immune system could predict the status of diarrhea and prevalence of enteric parasites especially the coccidian parasites. It has been observed that patients with Isospora, Cryptosporidium and multiple parasitic infections who presented with diarrhea had a lower CD4 count (181 ± 135.14). The presence of Isospora in one individual from the nondiarrheal group had a higher CD4 count. However, these individuals may act as carriers shedding oocysts in feces without any clinical manifestations. Therefore, treatment of these intestinal parasitic infections is of utmost importance.

 ~ Conclusion Top

This study demonstrated that there is an increased risk of symptomatic intestinal parasitic infections in HIV sero-positive patients as compared with the general population, and more so in patients with CD4 count <200 cells/μl. Pathogenic burden accelerates disease progression and contributes to early morbidity in HIV positive individuals. These enteric parasites were largely diagnosed in those practicing poor sanitation and improper personal hygiene. Prevention and control of these intestinal parasites involve proper diagnosis, adequate treatment, appropriate education, and deworming programs, provision of adequate toilet facilities, and piped water supply in all communities so that contamination of the environment with ova, cyst, and larva of parasites would be greatly reduced.

 ~ Acknowledgment Top

The authors are indebted to Mrs. Annamma MT, Regional STD Centre for her technical assistance and continuous support in carrying out this study. We are also thankful to National AIDS Control Organization for providing facilities for HIV testing and CD4 testing in this centre.

 ~ References Top

1.Ghosh T K. AIDS: A Serious Challenge to public health. J Ind Med Assoc 1986;84:29-30.  Back to cited text no. 1
2.Young people and HIV/AIDS-Situation in South East Asia (India), SEARO Publications on HIV/AIDS. 2006: 01-10 Available from: [Last accessed 17 th February, 2013]  Back to cited text no. 2
3.Chandramouli K. Current epidemiological trends of HIV/AIDS, Department of AIDS control, Ministry of Health and Family Welfare, NACO. Annual report 2009-2010. Available from: http// [Last accessed 17 th February, 2013].  Back to cited text no. 3
4.Arora DR, Arora B. Textbook of Microbiology. 2 nd ed. New Delhi: CBS Publishers and distributors; 2009.p. 605-23.  Back to cited text no. 4
5.Centers for Disease Control and Prevention. Revised surveillance case definitions for HIV infection among adults, adolescents, and children aged <18 months and for HIV infection and AIDS among children aged 18 months to <13 Years. United States, 2008. MMWR CDC Recommendations and Reports 2008;57(RR10):1-8.  Back to cited text no. 5
6.Gupta V, Gupta S. Laboratory markers associated with progression of HIV infection. Indian J Med Microbiol 2004;22:7-15.  Back to cited text no. 6
[PUBMED]  Medknow Journal  
7.Mayer HB, Wanke CA. Diagnostic strategies in HIV-infected patients with diarrhoea. AIDS 1994;8:1639-48.  Back to cited text no. 7
8.Wiwanitkit V. Intestinal parasitic infections in Thai HIV-infected patients with different immunity status. BMC Gastroenterol 2001:1-3.  Back to cited text no. 8
9.Thomas PD, Forbes A, Green J, Howdle P, Long R, Playford R, et al. Guidelines for the investigation of chronic diarrhoea. Gut 2003;52:1-15.  Back to cited text no. 9
10.Smith PD, Lane HC, Gill VG, Manilchewitz JF, Quinnan GV, Fauci As, et al. Intestinal infections in patients with AIDS: Etiology and response to therapy. Ann Intern Med 1988;108:328-33.  Back to cited text no. 10
11.WHO case definitions of HIV for surveillance and revised clinical staging and immunological classification of HIV related disease in adults aged 15 years or older. SEARO Publications on HIV/AIDS: 2006. Available from: [Last accessed on 2012 November 22].  Back to cited text no. 11
12.Framm SR, Soave R. Agents of diarrhoea. Med Clin North Am 1997;81:427-47.  Back to cited text no. 12
13.Tuli L, Gulati AK, Sundar S, Mohapatra TM. Correlation between CD4 counts of HIV patients and enteric protozoan in different seasons. BMC Gastroenterology 2008;8:36.  Back to cited text no. 13
14.Prasad KN, Nag VL, Dhole TN, Ayyagari A. Identification of enteric pathogens in HIV positive patients with diarrhoea in Northern India. J Health Popul Nutr 2000;8:23-6.  Back to cited text no. 14
15.Ramakrishnan K, Shenbagarathai R, Uma A, Kavitha K, Rajendran R, Thirumalaikolundusubramanian P. Prevalence of intestinal parasitic infections in HIV/AIDS patients with diarrhoea in Madurai City, South India. Jpn J Infect Dis 2007;60:209-10.  Back to cited text no. 15
16.Tyodugh ED, Emanghe UE, Ella AB, Onoja JU, Jombo GTA. Intestinal parasitosis among HIV/AIDS patients with diarrhoea at a missions hospital in tropical west Africa with pattern and types. Int Research J Microbiol 2012;3:55-9.  Back to cited text no. 16
17.Garcia LS. Diagnostic Medical Parasitology. 5 th ed. USA: American Society for Microbiology; 2007.p. 782-826.  Back to cited text no. 17
18.Kelly P, Todd J, Sianongo S, Mwansa J, Sinsungwe H, Katubulushi M, et al. Susceptibility to intestinal infection and diarrhoea in Zambian adults in relation to HIV status and CD4 count. BMC Gastroenterology 2009,9:7.  Back to cited text no. 18
19.Alemu A, Shiferaw Y, Getnet G, Yalew A, Addis Z. Opportunistic and other intestinal parasites among HIV/AIDS patients attending Gambi higher clinic in Bahir Dar city, North West Ethiopia. Asian Pacific J Trop Med 2011;661-5.  Back to cited text no. 19
20.Mohandas, Sehgal R, Sud A, Malla N. Prevalence of intestinal parasitic pathogens in HIV-seropositive individuals northern India. Jpn J Infect Dis 2002;55:83-4.  Back to cited text no. 20
21.Abaver DT, Nwobegahay JM, Goon DT. Prevalence of intestinal parasitic infections amon HIV/AIDS patients from two health institutions in Abuja, Nigeria. African Health Sciences. 2011;11:24-8.  Back to cited text no. 21
22.Kulkarni SV, Kairon R, Sane SS, Padmawar PS, Kale VA, Thakar MR, et al. Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunosuppression. Indian J Med Res 2009;130:63-6.  Back to cited text no. 22
23.Dwivedi KK, Prasad G, Saint S, Mahajan S, Lal S, Baveja UK. Enteric opportunistic parasites among HIV infected individuals associated with risk factors and immune status. Jpn J Infect Dis 2007;60:76-81.  Back to cited text no. 23
24.Vajpayee M, Kanswal S, Seth P, Wig N. Spectrum of Opportunistic Infections and Profile of CD4+Counts among AIDS Patients in North India. Infection 2003;31:336-40.  Back to cited text no. 24
25.Smith PD, Lane HL, Gill VG, Manilchewitz JF, Quinnan GV, Fauci AS. Intestinal infections in patients with AIDS: Etiology and response to therapy. Ann Intern Med 1988;108:328-33.  Back to cited text no. 25
26.Gupta S, Narang S, Nunavath V, Singh S. Chronic diarrhoea in HIV patients: Prevalence of coccidian parasites. Indian J Med Microbiol 2008;26:172-5.  Back to cited text no. 26
[PUBMED]  Medknow Journal  
27.Kotgire SA, Tankhiwale N. Evaluation of parasite causing gastrointestinal tract infestations in HIV/AIDS patients. Int J Basic and Applied Medical Sciences 2011;1:61-5.  Back to cited text no. 27
28.Kumar SS, Ananthan S, Saravanan P. Role of coccidian parasites in causation of diarrhoea in HIV infected patients in Chennai. Indian J Med Res 2002;116:85-9.  Back to cited text no. 28


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