Enteric Opportunistic Infection and the Impact of Antiretroviral Therapy among HIV/AIDS Patients from Tehran, Iran
-
Hossein MASOUMI-ASL
,
Khadijeh KHANALIHA
,
Farah BOKHARAEI-SALIM
,
Abdoulreza ESTEGHAMATI
,
Saeed KALANTARI
,
Maryam HOSSEINYRAD
Abstract
Background: Opportunistic parasites have been identified as human pathogens, especially in immunodeficient patients. Microsporidian and coccidian infections cause chronic diarrhea as common clinical manifestation in HIV positive patients. In this study, the frequency of opportunistic infections, including microsporidian and coccidian infections, was evaluated in HIV/AIDS patients from Tehran and phylogenic analysis was performed for E. bieneusi isolates from these patients.
Methods: One hundred and two stool samples were collected from confirmed HIV/AIDS patients, referred to Consult Center of Behavior Diseases, West Health Center, Iran University of Medical Sciences in Tehran, Iran. The samples were transferred to Research Center of Pediatric Infectious Diseases, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences from Jan 2016 to Dec 2016. After conventional formalin-ether concentration, aniline blue staining method and acid-fast staining technique were used for detection of microsporidian spores and Cyclospora oocysts. DNA was extracted and nested PCR was performed.
Results: Two (1.96%) cases were found to be positive for intestinal microsporidia infection using aniline blue staining method and were confirmed as E. bieneusi by nested PCR. One patient was found with Cyclospora cayetanensis infection by acid-fast staining method and PCR. Giardia lamblia and Blastocystis hominis were detected as non-opportunistic parasites in 1/102 (0.98%) and 2/102 (1.96%) of the HIV positive patients, respectively.
Conclusion: With respect to the use of antiretroviral therapy (ART) in HIV positive patients, we found a low frequency of infection.
1. Agholi M, Hatam GR, Motazedian MH (2013). HIV/AIDS-associated opportunistic protozoal diarrhea. AIDS Res Hum Retroviruses, 29:35-41.
2. Agholi M, Hatam GR, Motazedian MH (2013). Microsporidia and coccidia as causes of persistence diarrhea among liver transplant children: incidence rate and species/genotypes. Pediatr Infect Dis J, 32(2):185-187.
3. Anane S, Attouchi H (2010). Microsporidiosis: epidemiology, clinical data and therapy. Gastroenterol Clin Biol, 34(8-9):450-464.
4. Bachur TPR, Vale JM, Coêlho ICB et al (2008). Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis, 12(2):115-122.
5. Cegielski JP, Ortega YR, McKee S, Madden JF et al (1999). Cryptosporidium, Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis, 28(2):314-321.
6. Chawla R, Ichhpujani R (2011). Enteric spore-forming opportunistic parasites in HIV/AIDS. Trop Parasitol, 1(1):15-19.
7. Conteas CN, Berlin O, LaRiviere MJ et al (1998). Examination of the prevalence and seasonal variation of intestinal microsporidiosis in the stools of persons with chronic diarrhea and human immunodeficiency virus infection. Am J Trop Med Hyg, 58:559-561.
8. Coyle CM, Wittner M, Kotler DP et al (1996). Prevalence of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon (Septata) intestinalis among patients with AIDS-related diarrhea: determination by polymerase chain reaction to the microsporidian small-subunit rRNA gene. Clin Infect Dis, 23:1002-1006.
9. Daryani A, Sharif M, Meigouni M et al (2009). Prevalence of intestinal parasites and profile of CD4+ counts in HIV+/AIDS people in north of Iran, 2007-2008. Pak J Biol Sci, 12(18):1277-1281.
10. Dengjel B, Zahler M, Hermanns W et al (2001). Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol, 39(12):4495-4499.
11. Escobedo AA, Núñez FA (1999). Prevalence of intestinal parasites in Cuban acquired immunodeficiency syndrome (AIDS) patients. Acta Trop, 72(1):125-130.
12. Espern A, Morio F, Miegeville M et al (2007). Molecular study of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among human immunodeficiency virus-infected patients from two geographical areas: Niamey, Niger, and Hanoi, Vietnam. J Clin Microbiol, 45(9):2999-3002.
13. Field A, Hing M, Milliken S, Marriott D (1993). Microsporidia in the small intestine of HIV-infected patients. A new diagnostic technique and a new species. Med J Aust, 158(6):390-394.
14. Garcia LS, Bruckner DA (1993). Diagnostic medical parasitology. Washington, DC:131-135.
15. Ghaderipour M, Khanaliha K, Mohebali M et al (2017). Emerging Intestinal Microsporidia Infection in General Population in Jiroft District, Southeastern Iran: A Cross-sectional Study in 2013–2014. Iran J Public Health, 46(12):1697-1703.
16. Ghoyounchi R, Ahmadpour E, Spotin A et al (2017). Microsporidiosis in Iran: A systematic review and meta-analysis. Asian Pac J Trop Med, 10(4):341-350.
17. Khanaliha K, Masoumi-Asl H, Bokharaei-Salim F et al (2017). Double-stranded RNA viral infection of Trichomonas vaginalis (TVV1) in Iranian isolates. Microb Pathog, 109:56-60.
18. Khanaliha K, Mirjalali H, Mohebali M, Tarighi F, Rezaeian M (2014). Comparison of three staining methods for the detection of intestinal Microspora spp. Iran J Parasitol, 9(4): 445–451.
19. Khanaliha K, Mohebali M, Davoudi S et al (2015). Detection of emergence Cyclospora cayetanensis in A HIV+/AIDS patient with diarrhea from Tehran: a case report. Iran J Public Health, 44(6): 865–868.
20. Kulkarni SV, Kairon R, Sane SS et al (2009). Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunesuppression. Indian J Med Res, 130(1):63-6.
21. Lono AR, Kumar S, Chye TT (2008). Incidence of microsporidia in cancer patients. J Gastrointest Cancer, 39(1-4):124-129.
22. Maggi P, Larocca AM, Quarto M et al (2000). Effect of antiretroviral therapy on cryptosporidiosis and microsporidiosis in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis, 19(3):213-217.
23. Manatsathit S, Tansupasawasdikul S, Wanachiwanawin D et al (1996). Causes of chronic diarrhea in patients with AIDS in Thailand: a prospective clinical and microbiological study. J Gastroenterol, 31(4):533-537.
24. Matos O, Lobo ML, Xiao L (2012). Epidemiology of Enterocytozoon bieneusi infection in humans. J Parasitol Res, 2012:981424.
25. Missaye A, Dagnew M, Alemu A, Alemu A (2013). Prevalence of intestinal parasites and associated risk factors among HIV/AIDS patients with pre-ART and on-ART attending dessie hospital ART clinic, Northeast Ethiopia. AIDS Res Ther, 10(1):7.
26. Mohandas K, Sehgal R, Sud A, Malla N (2002). Prevalence of intestinal parasitic pathogens in HIV-seropositive individuals in Northern India. Jpn J Infect Dis, 55(3):83-84.
27. Nsagha DS, Njunda AL, Assob NJC et al (2016). Intestinal parasitic infections in relation to CD4+ T cell counts and diarrhea in HIV/AIDS patients with or without antiretroviral therapy in Cameroon. BMC Infect Dis, 11;16:9.
28. Ojuromi OT, Izquierdo F, Fenoy S et al (2012). Identification and characterization of microsporidia from fecal samples of HIV-positive patients from Lagos, Nigeria. PLoS One, 7(4):e35239.
29. Orlandi PA, Lampel KA (2000). Extraction-free, filter-based template preparation for rapid and sensitive PCR detection of pathogenic parasitic protozoa. J Clin Microbiol, 38(6):2271-2277.
30. Pape JW, Verdier R-I, Boncy M et al (1994). Cyclospora infection in adults infected with HIV: clinical manifestations, treatment, and prophylaxis. Ann Intern Med, 121(9):654-657.
31. Polley SD, Boadi S, Watson J, Curry A, Chiodini PL (2011). Detection and species identification of microsporidial infections using SYBR Green real-time PCR. J Med Microbiol, 60(Pt 4):459-466.
32. Rinder H, Thomschke A, Dengjel B et al (2000). Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J Parasitol, 86(1):185-188.
33. Ryan NJ, Sutherland G, Coughlan K et al B (1993). A new trichrome-blue stain for detection of microsporidial species in urine, stool, and nasopharyngeal specimens. J Clin Microbiol, 31(12):3264-3269.
34. Sak B, Brady D, Pelikánová M et al (2011). Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. J Clin Microbiol, 49(3):1064-1070.
35. Saksirisampant W, Prownebon J, Saksirisampant P et al S (2009). Intestinal parasitic infections: prevalences in HIV/AIDS patients in a Thai AIDS-care centre. Ann Trop Med Parasitol, 103(7):573-581.
36. Samie A, Obi C, Tzipori S, Weiss L, Guerrant R (2007). Microsporidiosis in South Africa: PCR detection in stool samples of HIV-positive and HIV-negative individuals and school children in Vhembe district, Limpopo Province. Trans R Soc Trop Med Hyg, 101(6):547-554.
37. Santín M, Trout JM, Vecino JAC, Dubey J, Fayer R (2006). Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol, 141(3-4):334-339.
38. Sarfati C, Bourgeois A, Menotti J et al (2006). Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus–infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg, 74(1):162-164.
39. Sobottka I, Schwartz DA, Schottelius J et al (1998). Prevalence and clinical significance of intestinal microsporidiosis in human immunodeficiency virus-infected patients with and without diarrhea in Germany: a prospective coprodiagnostic study. Clin Infect Dis, 26(2):475-480.
40. Sokolova OI, Demyanov AV, Bowers LC et al (2011). Emerging microsporidian infections in Russian HIV-infected patients. J Clin Microbiol, 49:2102-2108.
41. Sulaiman Im, Bern C, Gilman R et al (2003). A Molecular Biologic Study of Enterocytozoon bieneusi in HIV‐Infected Patients in Lima, Peru. J Eukaryot Microbiol, 50:591-596.
42. Van Gool T, Snijders F, Reiss P et al (1993). Diagnosis of intestinal and disseminated microsporidial infections in patients with HIV by a new rapid fluorescence technique. J Clin Pathol, 46(8):694-699.
43. Van Hal S, Muthiah K, Matthews G et al (2007). Declining incidence of intestinal microsporidiosis and reduction in AIDS-related mortality following introduction of HAART in Sydney, Australia. Trans R Soc Trop Med Hyg, 101(11):1096-100.
44. Velasquez J, Carnevale S, Cabrera M et al (2004). [Cyclospora cayetanensis in patients with AIDS and chronic diarrhea]. Acta Gastroenterol Latinoam, 34(3):133-137.
45. Weber R, Ledergerber B, Zbinden R et al (1999). Enteric infections and diarrhea in human immunodeficiency virus–infected persons: prospective community-based cohort study. Arch Intern Med, 159(13):1473-1480.
46. Yazar S, Yalcln S, Sahin Í (2004). Human cyclosporiosis in Turkey. World J Gastroenterol, 10:1844.
47. Zali MR, Mehr AJ, Rezaian M et al (2004). Prevalence of intestinal parasitic pathogens among HIV-positive individuals in Iran. Jpn J Infect Dis, 57(6):268-70.
2. Agholi M, Hatam GR, Motazedian MH (2013). Microsporidia and coccidia as causes of persistence diarrhea among liver transplant children: incidence rate and species/genotypes. Pediatr Infect Dis J, 32(2):185-187.
3. Anane S, Attouchi H (2010). Microsporidiosis: epidemiology, clinical data and therapy. Gastroenterol Clin Biol, 34(8-9):450-464.
4. Bachur TPR, Vale JM, Coêlho ICB et al (2008). Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis, 12(2):115-122.
5. Cegielski JP, Ortega YR, McKee S, Madden JF et al (1999). Cryptosporidium, Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis, 28(2):314-321.
6. Chawla R, Ichhpujani R (2011). Enteric spore-forming opportunistic parasites in HIV/AIDS. Trop Parasitol, 1(1):15-19.
7. Conteas CN, Berlin O, LaRiviere MJ et al (1998). Examination of the prevalence and seasonal variation of intestinal microsporidiosis in the stools of persons with chronic diarrhea and human immunodeficiency virus infection. Am J Trop Med Hyg, 58:559-561.
8. Coyle CM, Wittner M, Kotler DP et al (1996). Prevalence of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon (Septata) intestinalis among patients with AIDS-related diarrhea: determination by polymerase chain reaction to the microsporidian small-subunit rRNA gene. Clin Infect Dis, 23:1002-1006.
9. Daryani A, Sharif M, Meigouni M et al (2009). Prevalence of intestinal parasites and profile of CD4+ counts in HIV+/AIDS people in north of Iran, 2007-2008. Pak J Biol Sci, 12(18):1277-1281.
10. Dengjel B, Zahler M, Hermanns W et al (2001). Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol, 39(12):4495-4499.
11. Escobedo AA, Núñez FA (1999). Prevalence of intestinal parasites in Cuban acquired immunodeficiency syndrome (AIDS) patients. Acta Trop, 72(1):125-130.
12. Espern A, Morio F, Miegeville M et al (2007). Molecular study of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among human immunodeficiency virus-infected patients from two geographical areas: Niamey, Niger, and Hanoi, Vietnam. J Clin Microbiol, 45(9):2999-3002.
13. Field A, Hing M, Milliken S, Marriott D (1993). Microsporidia in the small intestine of HIV-infected patients. A new diagnostic technique and a new species. Med J Aust, 158(6):390-394.
14. Garcia LS, Bruckner DA (1993). Diagnostic medical parasitology. Washington, DC:131-135.
15. Ghaderipour M, Khanaliha K, Mohebali M et al (2017). Emerging Intestinal Microsporidia Infection in General Population in Jiroft District, Southeastern Iran: A Cross-sectional Study in 2013–2014. Iran J Public Health, 46(12):1697-1703.
16. Ghoyounchi R, Ahmadpour E, Spotin A et al (2017). Microsporidiosis in Iran: A systematic review and meta-analysis. Asian Pac J Trop Med, 10(4):341-350.
17. Khanaliha K, Masoumi-Asl H, Bokharaei-Salim F et al (2017). Double-stranded RNA viral infection of Trichomonas vaginalis (TVV1) in Iranian isolates. Microb Pathog, 109:56-60.
18. Khanaliha K, Mirjalali H, Mohebali M, Tarighi F, Rezaeian M (2014). Comparison of three staining methods for the detection of intestinal Microspora spp. Iran J Parasitol, 9(4): 445–451.
19. Khanaliha K, Mohebali M, Davoudi S et al (2015). Detection of emergence Cyclospora cayetanensis in A HIV+/AIDS patient with diarrhea from Tehran: a case report. Iran J Public Health, 44(6): 865–868.
20. Kulkarni SV, Kairon R, Sane SS et al (2009). Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunesuppression. Indian J Med Res, 130(1):63-6.
21. Lono AR, Kumar S, Chye TT (2008). Incidence of microsporidia in cancer patients. J Gastrointest Cancer, 39(1-4):124-129.
22. Maggi P, Larocca AM, Quarto M et al (2000). Effect of antiretroviral therapy on cryptosporidiosis and microsporidiosis in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis, 19(3):213-217.
23. Manatsathit S, Tansupasawasdikul S, Wanachiwanawin D et al (1996). Causes of chronic diarrhea in patients with AIDS in Thailand: a prospective clinical and microbiological study. J Gastroenterol, 31(4):533-537.
24. Matos O, Lobo ML, Xiao L (2012). Epidemiology of Enterocytozoon bieneusi infection in humans. J Parasitol Res, 2012:981424.
25. Missaye A, Dagnew M, Alemu A, Alemu A (2013). Prevalence of intestinal parasites and associated risk factors among HIV/AIDS patients with pre-ART and on-ART attending dessie hospital ART clinic, Northeast Ethiopia. AIDS Res Ther, 10(1):7.
26. Mohandas K, Sehgal R, Sud A, Malla N (2002). Prevalence of intestinal parasitic pathogens in HIV-seropositive individuals in Northern India. Jpn J Infect Dis, 55(3):83-84.
27. Nsagha DS, Njunda AL, Assob NJC et al (2016). Intestinal parasitic infections in relation to CD4+ T cell counts and diarrhea in HIV/AIDS patients with or without antiretroviral therapy in Cameroon. BMC Infect Dis, 11;16:9.
28. Ojuromi OT, Izquierdo F, Fenoy S et al (2012). Identification and characterization of microsporidia from fecal samples of HIV-positive patients from Lagos, Nigeria. PLoS One, 7(4):e35239.
29. Orlandi PA, Lampel KA (2000). Extraction-free, filter-based template preparation for rapid and sensitive PCR detection of pathogenic parasitic protozoa. J Clin Microbiol, 38(6):2271-2277.
30. Pape JW, Verdier R-I, Boncy M et al (1994). Cyclospora infection in adults infected with HIV: clinical manifestations, treatment, and prophylaxis. Ann Intern Med, 121(9):654-657.
31. Polley SD, Boadi S, Watson J, Curry A, Chiodini PL (2011). Detection and species identification of microsporidial infections using SYBR Green real-time PCR. J Med Microbiol, 60(Pt 4):459-466.
32. Rinder H, Thomschke A, Dengjel B et al (2000). Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J Parasitol, 86(1):185-188.
33. Ryan NJ, Sutherland G, Coughlan K et al B (1993). A new trichrome-blue stain for detection of microsporidial species in urine, stool, and nasopharyngeal specimens. J Clin Microbiol, 31(12):3264-3269.
34. Sak B, Brady D, Pelikánová M et al (2011). Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. J Clin Microbiol, 49(3):1064-1070.
35. Saksirisampant W, Prownebon J, Saksirisampant P et al S (2009). Intestinal parasitic infections: prevalences in HIV/AIDS patients in a Thai AIDS-care centre. Ann Trop Med Parasitol, 103(7):573-581.
36. Samie A, Obi C, Tzipori S, Weiss L, Guerrant R (2007). Microsporidiosis in South Africa: PCR detection in stool samples of HIV-positive and HIV-negative individuals and school children in Vhembe district, Limpopo Province. Trans R Soc Trop Med Hyg, 101(6):547-554.
37. Santín M, Trout JM, Vecino JAC, Dubey J, Fayer R (2006). Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol, 141(3-4):334-339.
38. Sarfati C, Bourgeois A, Menotti J et al (2006). Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus–infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg, 74(1):162-164.
39. Sobottka I, Schwartz DA, Schottelius J et al (1998). Prevalence and clinical significance of intestinal microsporidiosis in human immunodeficiency virus-infected patients with and without diarrhea in Germany: a prospective coprodiagnostic study. Clin Infect Dis, 26(2):475-480.
40. Sokolova OI, Demyanov AV, Bowers LC et al (2011). Emerging microsporidian infections in Russian HIV-infected patients. J Clin Microbiol, 49:2102-2108.
41. Sulaiman Im, Bern C, Gilman R et al (2003). A Molecular Biologic Study of Enterocytozoon bieneusi in HIV‐Infected Patients in Lima, Peru. J Eukaryot Microbiol, 50:591-596.
42. Van Gool T, Snijders F, Reiss P et al (1993). Diagnosis of intestinal and disseminated microsporidial infections in patients with HIV by a new rapid fluorescence technique. J Clin Pathol, 46(8):694-699.
43. Van Hal S, Muthiah K, Matthews G et al (2007). Declining incidence of intestinal microsporidiosis and reduction in AIDS-related mortality following introduction of HAART in Sydney, Australia. Trans R Soc Trop Med Hyg, 101(11):1096-100.
44. Velasquez J, Carnevale S, Cabrera M et al (2004). [Cyclospora cayetanensis in patients with AIDS and chronic diarrhea]. Acta Gastroenterol Latinoam, 34(3):133-137.
45. Weber R, Ledergerber B, Zbinden R et al (1999). Enteric infections and diarrhea in human immunodeficiency virus–infected persons: prospective community-based cohort study. Arch Intern Med, 159(13):1473-1480.
46. Yazar S, Yalcln S, Sahin Í (2004). Human cyclosporiosis in Turkey. World J Gastroenterol, 10:1844.
47. Zali MR, Mehr AJ, Rezaian M et al (2004). Prevalence of intestinal parasitic pathogens among HIV-positive individuals in Iran. Jpn J Infect Dis, 57(6):268-70.
| Files | ||
| Issue | Vol 48 No 4 (2019) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v48i4.1007 | |
| Keywords | ||
| Opportunistic infection HIV Coccidian Microsporidian | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
MASOUMI-ASL H, KHANALIHA K, BOKHARAEI-SALIM F, ESTEGHAMATI A, KALANTARI S, HOSSEINYRAD M. Enteric Opportunistic Infection and the Impact of Antiretroviral Therapy among HIV/AIDS Patients from Tehran, Iran. Iran J Public Health. 2019;48(4):730-739.
