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 ~  Abstract
 ~ Introduction
 ~ Patients and Methods
 ~ Results
 ~ Discussion
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  Table of Contents  
Year : 2017  |  Volume : 35  |  Issue : 1  |  Page : 37-40

Occurrence of enteric parasitic infections among HIV-infected individuals and its relation to CD4 T-cell counts with a special emphasis on coccidian parasites at a tertiary care centre in South India

1 Infectious Diseases Laboratory, Y. R. Gaitonde Centre for AIDS Research and Education, Chennai, Tamil Nadu, India
2 Infectious Diseases Laboratory, Y. R. Gaitonde Centre for AIDS Research and Education, Chennai, Tamil Nadu, India; Laboratory-based Department, Universiti Kuala Lumpur Royal College of Medicine Perak, Ipoh, Malaysia
3 Medical Centre, Y. R. Gaitonde Centre for AIDS Research and Education, Chennai, Tamil Nadu, India
4 Medical Centre, Y. R. Gaitonde Centre for AIDS Research and Education, Chennai, Tamil Nadu, India; Department of Infectious Diseases, Johns Hopkins School of Medicine, Baltimore, USA

Date of Web Publication16-Mar-2017

Correspondence Address:
Pachamuthu Balakrishnan
YRG Care Infectious Diseases Laboratory, 2nd Floor, Admin Building, VHS Hospital Campus, Rajiv Gandhi Salai, Taramani, Chennai - 600 113, Tamil Nadu
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_16_164

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 ~ Abstract 

Context: Diarrhoea is one of the major complications occurring in over 90% of HIV-infected individuals in developing countries. Coccidian group of parasites, being opportunistic pathogens, have been implicated as the most common causative agents of diarrhoea among HIV-infected population. Aims: The aim was to study the magnitude of parasitic diarrhoea with special context to coccidian parasitic infections in HIV-infected individuals and their association with the patient's immunological status measured by CD4 T-cell counts. Settings and Design: This investigation was performed between January 2002 and December 2014 at a tertiary HIV care centre in Chennai, South India. Materials and Methods: Stool samples were collected and microscopically observed for parasites using direct, formal-ether-concentrated wet mounts and modified acid-fast staining for coccidian parasites. CD4 T-cell counts were done by FACScount. Statistical Analysis Used: All statistical analyses were performed using GraphPad Prism software, version 5.0, andP < 0.05 was considered statistically significant. Results: Coccidian parasitic infection accounted for about 23.4% of parasitic infections, and of these, Cystoisospora belli was observed to be the most common cause of diarrhoea (88.8%), followed by Cryptosporidium spp. (9.9%) and Cyclospora spp. (1.3%). Trend analysis of coccidian aetiology during the study period revealed a significant rise in the positivity of C. belli and Cryptosporidium spp. (P = 0.001). Among the HIV patients with CD4+ T-cell counts <200 cells/μL, Cryptosporidium infection was most common (90%), followed by infection with C. belli(61.4%). Conclusions: Coccidian parasites continue to be the most common aetiological agent of diarrhoea among patients with HIV. The increasing trend of positivity of both cystoisosporiasis and cryptosporidiosis over the study period and the high positivity of cryptosporidiosis in patients with lower CD4+ T-cell counts are issues of serious concern. The findings call for the need for the early diagnosis of coccidian parasites and appropriate intervention among HIV-infected patients.

Keywords: Coccidian parasitic infection, HIV, parasitic diarrhoea

How to cite this article:
Swathirajan CR, Vignesh R, Pradeep A, Solomon SS, Solomon S, Balakrishnan P. Occurrence of enteric parasitic infections among HIV-infected individuals and its relation to CD4 T-cell counts with a special emphasis on coccidian parasites at a tertiary care centre in South India. Indian J Med Microbiol 2017;35:37-40

How to cite this URL:
Swathirajan CR, Vignesh R, Pradeep A, Solomon SS, Solomon S, Balakrishnan P. Occurrence of enteric parasitic infections among HIV-infected individuals and its relation to CD4 T-cell counts with a special emphasis on coccidian parasites at a tertiary care centre in South India. Indian J Med Microbiol [serial online] 2017 [cited 2020 Dec 3];35:37-40. Available from:

 ~ Introduction Top

Opportunistic infections (OIs) and co-infections remain the hallmark of HIV infection worldwide. HIV remains the gateway of OIs since destabilising immune system makes the conditions favourable for OIs' survival, expansion and causing disease.[1],[2] OIs resulting in gastrointestinal infections are more common in HIV-infected individuals. Chronic diarrhoea occurs in almost 90% of cases in developing countries which, when untreated, results in quicker morbidity and mortality.[3]

Several groups of pathogens such as bacteria, fungi, parasites and viruses are reported as the responsible aetiologies of diarrhoea.[3],[4] Parasitic aetiology of diarrhoea includes coccidian parasites and other non-coccidian parasites. Among the coccidian parasites, Cryptosoporidium and Cystoisospora infections remain as the standout pathogens in many parts of the Indian subcontinent.[5],[6],[7]

Several reports suggest that chronic immune activation results in increased HIV disease progression.[8],[9] Parasitic infections, especially helminthic, result in chronic immune activation with immune response mechanisms skewed towards TH2 immune response pathway.[10],[11] Hence, we aimed to study the prevalence of enteric parasites in diarrhoeal cases with a special emphasis on coccidian parasites and its relation with CD4 T-cell counts in HIV-infected individuals.

 ~ Patients and Methods Top

Study design

This study was performed between January 2007 and December 2014 at a tertiary HIV care centre in Chennai, South India, which provides psycho-social and clinical care services to more than 20,000 registered HIV patients. HIV-infected individuals presented with diarrhoea were included in the study.

Stool examination

Fresh stool samples were collected from the patients in a single, clean, dry, wide-mouthed container. Direct and formal-ether-concentrated wet mount preparations using normal saline and Lugol's iodine were prepared and observed under ×100 and ×400 magnifications for intestinal parasites. Modified acid-fast bacilli staining was performed with smear prepared from concentrated stool specimen for screening coccidian parasites following methods described earlier.[12]

CD4 T-cell counts

Blood specimens were collected from the enrolled patients for CD4 T-cell counting as part of routine investigations. CD4 T-cell counts were measured using FACScount system (Becton Dickinson, CA, USA).

Statistical analysis

All statistical analyses were performed using GraphPad Prism software, version 5.0 (GraphPad software Inc, California, USA), and P < 0.05 was considered statistically significant.

 ~ Results Top

Of the 829 HIV-positive individuals screened, 625 were males and remaining were females. The median ages of male and female population were 38 and 33.5 years, respectively. Parasitic aetiology was found in 28.3% (n = 235) of the cases, of which 85.1% (n = 200) were males and 14.9% (n = 35) were females. Analysis of age-wise distribution of the study population showed higher proportion of parasitic diarrhoeal occurrence in patients between the age group of 31–40 in both sexes.

Positivity of various intestinal parasites

Coccidian parasitic infection accounted for about 23.4% of parasitic infections, in which Cystoisospora belli was found to be the most prominent cause, accounting for about 21%. Other non-coccidian parasites were diagnosed in 7.1% of cases with diarrhoeal manifestations. Individual rates of parasitic infection rates are depicted in [Figure 1]. Mixed parasitic infection (either two coccidian or one coccidian and one non-coccidian or two non-coccidian parasites) occurred in 2.17% of diarrhoeal cases.
Figure 1: Positivity rates of various intestinal parasites observed in the study group.

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Trend analysis of coccidian parasitic infection

It was observed that 88.8% of coccidian infection was caused by C. belli. Cryptosporidium spp. and Cyclospora spp. were responsible for 9.9% and 1.2% of infections, respectively. When the coccidian aetiology was analysed over the years, a statistically significant rise (P = 0.001) in the positivity of C. belli and Cryptosporidium spp. was observed from 2007 to 2012 [Figure 2].
Figure 2: Trend analysis of coccidian parasitic infections over years.

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CD4 T-cell counts and its relation with coccidian infection

The study participants were stratified into four groups based on their CD4 T-cell counts: <200, 200–350, 350–500 and >500 cells/µL.[13] It was observed that about 62% of HIV patients had presented with parasitic diarrhoea when their CD4 T-cell counts were <200 cells/µL, of which 77.7% were of coccidian origin. C. belli was observed to be the most common with 68% of infections when the CD4 T-cell count was below <200 cells/µL, while Cryptosporidium spp. caused 8.7% of infections and only one patient with Cyclospora spp. [Table 1] demonstrate the complete distribution of the coccidian parasitic infections as per the stratified CD4 counts. Among the coccidian parasites, positivity rate of cryptosporidiosis was as high as 90% when the CD4+ T-cell count was <200 cells/µL, while it was 61.4% in cystoisosporiasis. Analysing the CD4+ T-cell count-wise distribution of positivity rates of coccidian parasites by Fisher's exact test revealed that there was no statistical significance (P = 0.198). The median CD4+ T-cell count of patients with cryptosporidiosis was 22 cells/µL, whereas for cystoisosporiasis, it was 176 cells/µL, and this difference was observed to be statistically significant (P = 0.009).
Table 1: Positivity rates of coccidian parasites in HIV-infected patients stratified based on CD4+ T-cell count range

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However, it should be mentioned that, besides coccidian parasites, infection by other parasites such as Strongyloides stercoralis and Entamoeba histolytica/dispar was also present in 75% and 57.1%, respectively, of cases with CD4+ T-cell counts <200 cells/µL which decreases with increase in CD4+ T-cell counts.

 ~ Discussion Top

Diarrhoeal complications are often found in HIV-infected individuals, and parasitic involvements in those cases are very significant. In some cases, diarrhoea becomes the starting point for the diagnosis of HIV. In the present study, diarrhoea due to parasite was observed in 28.3% of cases which is slightly lower when compared to a previous study conducted in our own centre [12] and another study from North India,[14] which might be attributed to small sample size in both the studies. HIV-infected people in the age group of 21–40 and 31–40 years are most infected by intestinal parasites which is very much similar to this study where 46% of both the sexes belong to the age group of 31–40 years.[5],[15] In agreement with other studies, male preponderance was also observed in this study with 24.1% of infections in male population and 4.22% of infection in females.[6],[16] This male preponderance could be due to the finding from the same institution that HIV-infected men had lower CD4+ T-cell counts than their women counterparts during treatment initiation.[12]

In line with many studies, Entamoeba spp. (3.4%) was the most common non-coccidian and non-opportunistic pathogen found in this study followed by other pathogens such as S. stercoralis, Giardia spp., hookworm and Ascaris spp.[6],[17],[18],[19],[20] Contrasting to this observation, Giardia spp. was also reported to be the leading non-opportunistic parasite causing diarrhoea in HIV-infected individuals.[5],[15] Within the parasitic aetiology of HIV-infected individuals, coccidian parasites deserve a special mention considering the opportunistic nature of these parasites and in the involvement of chronic cryptosporidiosis and chronic cystoisosporiasis as one of the AIDS-defining illnesses. Irrespective of opportunistic and non-opportunistic categorisation, coccidian parasite, C. belli, remains the standout parasite in diarrhoeal manifestations, responsible for 60.9% of diarrhoeal events. This statement is contrasting to most of the findings across the Indian peninsula, where there is a higher prevalence of Cryptosporidium spp. with a few documenting the least diagnosis of C. belli.[5],[6],[18],[20],[21],[22] Significantly lesser cases of Cryptosporidium spp. were seen in this study, but it becomes important when combined with the fact that these infections come under one of the WHO standard HIV clinical stage 4 conditions.[23] In addition, the difference in various studies regarding the distribution of opportunistic or non-coccidian parasitic aetiology intends to prove that there is no specific pattern in causing diarrhoea in HIV-infected individuals. Moreover, it also depends on geographical location, ethnicity and the living conditions of the patients. Another alarming finding of this 11-year observation is that, from 2007, a significant increase in the incidence of cystoisosporiasis and cryptosporidiosis was noted, which is not reported elsewhere to the best of our knowledge.

Elevated rate of parasite infections was diagnosed quite often when the CD4 T-cell count is <200 cells/µL. Both coccidian and mixed parasitic infections were mostly seen when the CD4 T-cell count is <200 cells/µL. C. belli was the predominant parasite when the CD4 T-cell count is <200 cells/µL, which is conflicting with others reporting the primary pathogen in this group as Cryptosporidium spp, Assefa S et al., and Nsagha DS et al.[5],[6],[14],[17],[24] This trend is not new to our centre since we have already reported about the high rate of cystoisosporiasis in South India.[12] However, when the risk of positivity is taken into account during low CD4 T-cell counts, Cryptosporidium spp. tends to be the likely pathogen to infect with a positivity rate of 90% whereas cystoisosporiasis positivity was 61.4%, which explains the dominance of cryptosporidiosis in HIV-infected individuals with lowering CD4 T-cell counts. Besides coccidian infections, the positivity rates of S. stercoralis and E. histolytica/dispar infection were 75% and 57.1% respectively, when the CD4 T-cell is <200 cells/μL. It should be noted that positivity of coccidian and non-coccidian parasite decreases with increasing CD4 T-cell counts.

This study underlines a high rate of cystoisosporiasis, with others showing cryptosporidiosis as the primary parasite, but on a collective note, it is the coccidian parasites taking their toll in most of the situations, signifying their role as a vital partner of HIV-resulted immunosuppression. It should also be noted that there is double-fold increase in parasitic infections when the CD4 T-cell count is <200 cells/µL, which highlights its vulnerability as a co-morbidity factor. Prevention of these infections can be made by constant monitoring of the immune system and also by early detection and cure of these parasitic infections. From patients' perspective, avoiding these infections relies on adhering to proper treatment regimens and maintaining good personal hygiene such as drinking boiled water, which may help in avoiding the risk of diarrhoeal disorders.

Therefore, this study urges the need and importance of periodic monitoring of opportunistic parasitic infections, particularly for coccidian parasites during waning CD4 T-cell counts, despite HIV treatment status and during treatment failure. It is alarming to note the high incidence of cystoisosporiasis, despite trimethoprim-sulfamethoxazole (TMP-SMX) administered as a prophylactic drug for Pneumocystis jiroveci pneumonia. Hence, elucidation of drug resistance of TMP-SMX against C. belli in future gains huge importance. Since most of the HIV-infected individuals belong to low-to-moderate socioeconomic groups, improving living standards by means of periodic health and nutritional counselling definitely have an impact in lowering the incidences of parasitic infections in addition to effective HAART treatment regimens.


The authors would like to thank all the study participants without whom this study would not have been possible.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 ~ References Top

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  [Figure 1], [Figure 2]

  [Table 1]


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