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Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | Immunodeficiency | Research article

Intestinal microsporidiosis among HIV/AIDS patients receiving antiretroviral therapy in Sana’a city, Yemen: first report on prevalence and predictors

Authors: Kwkab A. R. Al-Brhami, Rashad Abdul‑Ghani, Salah A. Al-Qobati

Published in: BMC Infectious Diseases | Issue 1/2022

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Abstract

Background

Intestinal microsporidiosis is an opportunistic infection associated with persistent diarrhea among HIV/AIDS patients. In Yemen, however, its epidemiology is unknown. Therefore, this study determined its prevalence and predictors among HIV/AIDS patients receiving antiretroviral therapy (ART) in Sana’a city, the capital of Yemen.

Methods

This cross-sectional study included 402 patients receiving ART at Al-Jomhori Educational Hospital in Sana’a from November 2019 to December 2020. Data about demographics, clinical characteristics and risk factors were collected using a pre-designed questionnaire. Stool samples were collected and examined for microsporidian spores using the Gram-chromotrope Kinyoun staining. Blood samples were also collected and used for CD4 cell counting by flow cytometry. Univariate analysis was used to test the association of patients’ characteristics and risk factors with intestinal microsporidiosis. Multivariable logistic regression was then used to identify the independent predictors of infection. Statistical significance was considered at P-values < 0.05.

Results

Intestinal microsporidiosis was prevalent among 14.2% (57/402) of HIV/AIDS patients and was significantly associated with diarrhea (OR 3.4, 95% CI 1.7–6.6; P = 0.001). The significant independent predictors of infection were < 200 CD4 cells/µl (AOR 3.2, 95% CI 1.5–6.9; P = 0.003), not washing hands after contacting soil (AOR 2.5, 95% CI 1.1–5.4; P = 0.026) and before eating (AOR 3.1, 95% CI 1.5–6.4; P = 0.003), eating unwashed raw produce (AOR 2.5, 95% CI 1.2–5.3; P = 0.017) and absence of indoor latrines (AOR 6.2, 95% CI 1.5–25.9; P = 0.012).

Conclusions

The prevalence of intestinal microsporidiosis among HIV/AIDS patients in Sana'a is high and comparable to that reported from several other countries, being prevalent among approximately 14.0% of patients and significantly associated with diarrhea. It could be predicted among patients who have < 200 CD4 cells/µl, have poor hand hygiene after contacting soil and before eating, usually eat unwashed raw produce, or do not possess indoor latrines. Large-scale studies on its epidemiology and predictors among HIV/AIDS patients across the country are warranted.
Literature
3.
go back to reference Weiss LM. Microsporidiosis. In: Hunter’s tropical medicine and emerging infectious diseases. 10th ed. Amsterdam: Elsevier; 2020. p. 825–31.CrossRef Weiss LM. Microsporidiosis. In: Hunter’s tropical medicine and emerging infectious diseases. 10th ed. Amsterdam: Elsevier; 2020. p. 825–31.CrossRef
8.
go back to reference Fayer R, Santin-Duran M. Epidemiology of microsporidia in humans. In: Weiss L, Becnel JJ, editors. Microsporidia: pathogens of opportunity. Hoboken: Wiley; 2014. p. 135–64. Fayer R, Santin-Duran M. Epidemiology of microsporidia in humans. In: Weiss L, Becnel JJ, editors. Microsporidia: pathogens of opportunity. Hoboken: Wiley; 2014. p. 135–64.
9.
go back to reference Zainudin NS, Nasarudin SNS, Periyasamy P, Moktar N, Noordin R, Osman E. Diagnosis of disseminated microsporidiosis: Detection of circulating Enterocytozoon bieneusi DNA in blood of HIV/AIDS patients. Trop Biomed. 2016;33(4):761–70.PubMed Zainudin NS, Nasarudin SNS, Periyasamy P, Moktar N, Noordin R, Osman E. Diagnosis of disseminated microsporidiosis: Detection of circulating Enterocytozoon bieneusi DNA in blood of HIV/AIDS patients. Trop Biomed. 2016;33(4):761–70.PubMed
11.
go back to reference Bharmal R, Tiwari R. HIV and AIDS: basic elements and priorities. Dordrecht: Springer; 2007. Bharmal R, Tiwari R. HIV and AIDS: basic elements and priorities. Dordrecht: Springer; 2007.
12.
go back to reference World Health Organization. Global health observatory (GHO) data: HIV/AIDS; 2018. World Health Organization. Global health observatory (GHO) data: HIV/AIDS; 2018.
14.
19.
go back to reference Weber R, Schwartz DA, Deplazes P. Laboratory diagnosis of microsporidiosis. In: The microsporidia and microsporidiosis. Washington: ASM Press; 1999. p. 315–62. Weber R, Schwartz DA, Deplazes P. Laboratory diagnosis of microsporidiosis. In: The microsporidia and microsporidiosis. Washington: ASM Press; 1999. p. 315–62.
22.
go back to reference Moura H, Schwartz DA, Bornay-Llinares F, Sodre FC. A new and improved" quick-hot Gram-chromotrope" technique that differentially stains microsporidian spores in clinical samples, including paraffin-embedded tissue sections. Arch Pathol Lab Med. 1997;121(8):888.PubMed Moura H, Schwartz DA, Bornay-Llinares F, Sodre FC. A new and improved" quick-hot Gram-chromotrope" technique that differentially stains microsporidian spores in clinical samples, including paraffin-embedded tissue sections. Arch Pathol Lab Med. 1997;121(8):888.PubMed
24.
go back to reference Salleh FM, Al-Mekhlafi AM, Nordin A, Yasin AM, Al-Mekhlafi HM, Moktar N. Evaluation of Gram-chromotrope Kinyoun staining technique: its effectiveness in detecting microsporidial spores in fecal specimens. Diagn Microbiol Infect Dis. 2011;69(1):82–5.CrossRef Salleh FM, Al-Mekhlafi AM, Nordin A, Yasin AM, Al-Mekhlafi HM, Moktar N. Evaluation of Gram-chromotrope Kinyoun staining technique: its effectiveness in detecting microsporidial spores in fecal specimens. Diagn Microbiol Infect Dis. 2011;69(1):82–5.CrossRef
27.
go back to reference Central Statistical Organization. Statistical Year Book: Population and Housing Census 2017 Sana'a: CSO; 2017. Central Statistical Organization. Statistical Year Book: Population and Housing Census 2017 Sana'a: CSO; 2017.
31.
go back to reference Chacin-Bonilla L, Panunzio AP, Monsalve-Castillo FM, Parra-Cepeda IE, Martinez R. Microsporidiosis in Venezuela: prevalence of intestinal microsporidiosis and its contribution to diarrhea in a group of human immunodeficiency virus–infected patients from Zulia State. Am J Trop Med Hyg. 2006;74(3):482–6.CrossRef Chacin-Bonilla L, Panunzio AP, Monsalve-Castillo FM, Parra-Cepeda IE, Martinez R. Microsporidiosis in Venezuela: prevalence of intestinal microsporidiosis and its contribution to diarrhea in a group of human immunodeficiency virus–infected patients from Zulia State. Am J Trop Med Hyg. 2006;74(3):482–6.CrossRef
32.
go back to reference Endeshaw T, Kebede A, Verweij JJ, Zewide A, Tsige K, Abraham Y, et al. Intestinal microsporidiosis in diarrheal patients infected with human immunodeficiency virus-1 in Addis Ababa, Ethiopia. Jpn J Infect Dis. 2006;59(5):306–10.PubMed Endeshaw T, Kebede A, Verweij JJ, Zewide A, Tsige K, Abraham Y, et al. Intestinal microsporidiosis in diarrheal patients infected with human immunodeficiency virus-1 in Addis Ababa, Ethiopia. Jpn J Infect Dis. 2006;59(5):306–10.PubMed
33.
go back to reference Kucerova Z, Sokolova O, Demyanov A, Kvac M, Sak B, Kvetonova D, et al. Microsporidiosis and cryptosporidiosis in HIV/AIDS patients in St. Petersburg, Russia: serological identification of microsporidia and Cryptosporidium parvum in sera samples from HIV/AIDS patients. AIDS Res Hum Retroviruses. 2011;27(1):13–5. https://doi.org/10.1089/aid.2010.0132.CrossRefPubMed Kucerova Z, Sokolova O, Demyanov A, Kvac M, Sak B, Kvetonova D, et al. Microsporidiosis and cryptosporidiosis in HIV/AIDS patients in St. Petersburg, Russia: serological identification of microsporidia and Cryptosporidium parvum in sera samples from HIV/AIDS patients. AIDS Res Hum Retroviruses. 2011;27(1):13–5. https://​doi.​org/​10.​1089/​aid.​2010.​0132.CrossRefPubMed
38.
go back to reference Yacouba A, Sawadogo MP, Diallo I, Sangare I, Bamba S, Ouattara B, et al. Opportunistic and other intestinal parasites infections among HIV-positive patients in the era of combination antiretroviral therapy and preventive treatment in Ouagadougou, Burkina Faso. J HIV Clin Sci Res. 2017;4(1):008–14. Yacouba A, Sawadogo MP, Diallo I, Sangare I, Bamba S, Ouattara B, et al. Opportunistic and other intestinal parasites infections among HIV-positive patients in the era of combination antiretroviral therapy and preventive treatment in Ouagadougou, Burkina Faso. J HIV Clin Sci Res. 2017;4(1):008–14.
45.
go back to reference Zainudin NS, Nasarudin SNSA, Moktar N, Azil AH, Osman E. Human microsporidiosis in Malaysia: review of literatures. Malays J Pub Health Med. 2017;17(2):9–18. Zainudin NS, Nasarudin SNSA, Moktar N, Azil AH, Osman E. Human microsporidiosis in Malaysia: review of literatures. Malays J Pub Health Med. 2017;17(2):9–18.
49.
go back to reference Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, et al. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg. 2005;73(5):921–5.CrossRef Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, et al. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg. 2005;73(5):921–5.CrossRef
50.
go back to reference Viriyavejakul P, Nintasen R, Punsawad C, Chaisri U, Punpoowong B, Riganti M. High prevalence of Microsporidium infection in HIV-infected patients. Southeast Asian J Trop Med Public Health. 2009;40(2):223.PubMed Viriyavejakul P, Nintasen R, Punsawad C, Chaisri U, Punpoowong B, Riganti M. High prevalence of Microsporidium infection in HIV-infected patients. Southeast Asian J Trop Med Public Health. 2009;40(2):223.PubMed
54.
go back to reference Rodríguez-Pérez EG, Arce-Mendoza AY, Montes-Zapata ÉI, Limón A, Rodríguez LÉ, Escandón-Vargas K. Opportunistic intestinal parasites in immunocompromised patients from a tertiary hospital in Monterrey. Mexico Infez Med. 2019;27:168–74.PubMed Rodríguez-Pérez EG, Arce-Mendoza AY, Montes-Zapata ÉI, Limón A, Rodríguez LÉ, Escandón-Vargas K. Opportunistic intestinal parasites in immunocompromised patients from a tertiary hospital in Monterrey. Mexico Infez Med. 2019;27:168–74.PubMed
57.
go back to reference Dwivedi KK, Prasad G, Saini S, Mahajan S, Lal S, Baveja UK. Enteric opportunistic parasites among HIV infected individuals: associated risk factors and immune status. Jpn J Infect Dis. 2007;60(2/3):76.PubMed Dwivedi KK, Prasad G, Saini S, Mahajan S, Lal S, Baveja UK. Enteric opportunistic parasites among HIV infected individuals: associated risk factors and immune status. Jpn J Infect Dis. 2007;60(2/3):76.PubMed
60.
go back to reference Meyers WM, Firpo A, Wear DJ. Topics on the pathology of protozoan and invasive arthropod diseases. Washington, DC; 2011. Meyers WM, Firpo A, Wear DJ. Topics on the pathology of protozoan and invasive arthropod diseases. Washington, DC; 2011.
63.
go back to reference Calvo M, Carazo M, Arias ML, Chaves C, Monge R, Chinchilla M. Prevalence of Cyclospora sp., Cryptosporidium sp, microsporidia and fecal coliform determination in fresh fruit and vegetables consumed in Costa Rica. Arch Latinoam Nutr. 2004;54(4):428–32.PubMed Calvo M, Carazo M, Arias ML, Chaves C, Monge R, Chinchilla M. Prevalence of Cyclospora sp., Cryptosporidium sp, microsporidia and fecal coliform determination in fresh fruit and vegetables consumed in Costa Rica. Arch Latinoam Nutr. 2004;54(4):428–32.PubMed
Metadata
Title
Intestinal microsporidiosis among HIV/AIDS patients receiving antiretroviral therapy in Sana’a city, Yemen: first report on prevalence and predictors
Authors
Kwkab A. R. Al-Brhami
Rashad Abdul‑Ghani
Salah A. Al-Qobati
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-07009-3

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