Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
BMC Infectious Diseases
Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region, China

Authors: Hua Liu, Zhihua Jiang, Zhongying Yuan, Jianhai Yin, Zunfu Wang, Bingxue Yu, Dongsheng Zhou, Yujuan Shen, Jianping Cao

Published in: BMC Infectious Diseases | Issue 1/2017

Login to get access

Abstract

Background

Enterocytozoon bieneusi has been increasingly reported to infect humans and various mammals. Microsporidia cause diarrhea in HIV-infected patients worldwide. PCR amplification and sequencing based on the internal transcribed spacer region have been used to describe the genotypes of E. bieneusi and transmission of microsporidiosis.

Methods

In this study, we examined E. bieneusi infection and genotypes in HIV-positive patients in Guangxi, China. Stool specimens were collected from 285 HIV-positive patients and 303 HIV-negative individuals. E. bieneusi genotypes were characterized using nested PCR and sequencing.

Results

Thirty-three (11.58%) HIV-positive patients were infected with microsporidia, and no infection was found in the 303 healthy controls. Three new genotypes were identified and named as GX25, GX456, and GX458; four known genotypes, PigEBITS7, Type IV/K, D, and Ebpc, were also identified. Our data showed that the positive rate for microsporidia was significantly higher in the rural patients than in the other occupation groups. In addition, the positive rate for microsporidia was significantly higher in the patients who drink unboiled water than in those with other drinking water sources.

Conclusions

Our results will provide baseline data for preventing and controlling E. bieneusi infection in HIV/AIDS patients. Further studies are required to clarify the epidemiology and potential sources of microsporidia. Our study showed that microsporidium infection occurs in the HIV/AIDS patients in Guangxi, China.
Appendix
Available only for authorised users
Literature
1.
Schottelius J, Da Costa SC. Microsporidia and acquired immunodeficiency syndrome. Mem Inst Oswaldo Cruz. 2000;95(Suppl 1):133–9.CrossRefPubMed
2.
Sprague V, Becnel JJ, Hazard EI. Taxonomy of phylum microspora. Crit Rev Microbiol. 1992;18:285–395.CrossRefPubMed
3.
Stentiford GD, Becnel JJ, Weiss LM, Keeling PJ, Didier ES, Williams BAP, et al. Microsporidia – Emergent Pathogens in the Global Food Chain.Trends Parasitol. 2016;32(4):336–348.
4.
Dascomb K, Frazer T, Clark RA, Kissinger P, Didier E. Microsporidiosis and HIV. J Acquir Immune Defic Syndr. 2000;24:290–2.CrossRefPubMed
5.
Desportes-Livage I. Microsporidia and other opportunistic protozoa in patients with acquired immunodeficiency syndrome (AIDS). Clin Microbiol Infect. 1996;1:152–3.CrossRefPubMed
6.
7.
Matsubayashi H, Koike T, Mikata I, Takei H, Hagiwara SA. Case of Encephalitozoon-like body infection in man. AMA Arch Pathol. 1959;67:181–7.PubMed
8.
9.
Matos O, Lobo ML, Xiao L. Epidemiology of Enterocytozoon bieneusi infection in Huamns. J Parasitol Res. 2012:981424.
10.
Ojuromi OT, Izquierdo F, Fenoy S, Fagbenro-Beyioku A, Oyibo W, Akanmu A, et al. Identification and characterization of microsporidia from fecal samples of HIV-positive patients from Lagos, Nigeria. PLoS One. 2012;7:e35239.CrossRefPubMedPubMedCentral
11.
Bern C, Kawai V, Vargas D, Rabke-Verani J, Williamson J, Chavez-Valdez R, et al. The epidemiology of intestinal microsporidiosis in patients with HIV/AIDS in lima, Peru. J Infect Dis. 2005;191:1658–64.CrossRefPubMed
12.
Sparfel JM, Sarfati C, Liguory O, Caroff B, Dumoutier N, Gueglio B, et al. Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J Eukaryot Microbiol. 1997;78S:44.
13.
Li N, Xiao LH, Wang L, Zhao SM, Zhao XK, Duan LP, et al. Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl Trop Dis. 2012;6:e18099.
14.
da Silva Fiuza VR, Lopes CW, de Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol. 2016;216:46–51.
15.
Karim MR, Wang R, Dong H, Zhang L, Li J, Zhang S, et al. Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China. Appl Environ Microbiol. 2014;80:1893–8.CrossRefPubMedPubMedCentral
16.
Galvan AL, Magnet A, Izquierdo F, Fenoy S, Rueda C, Vadillo CF, et al. Molecular characterization of human-pathogenic Microsporidia and Cyclospora cayetanensis isolated from various water sources in Spain: a year-long longitudinal study. Appl Environ Microbiol. 2013;79:449–59.CrossRefPubMedPubMedCentral
17.
Ojuromi OT, Duan L, Izquierdo F, Fenoy S, Oyibo WA, Del Aguila C, et al. Genotypes of Cryptosporidium spp. and Enterocytozoon bieneusi in human immunodeficiency virus-infected patients in Lagos, Nigeria. J Eukaryot Microbiol. 2016;64:414–8.CrossRef
18.
Aissa S, Chabchoub N, Abdelmalek R, Kanoun F, Goubantini A, Ammari L, et al. Asymptomatic intestinal carriage of microsporidia in HIV-positive patients in Tunisia: prevalence, species, and pathogenesis. Med Sante Trop. 2017;27(3):281–285.
19.
Mirjalali H, Mohebali M, Mirhendi H, Gholami R, Keshavarz H, Meamar AR, et al. Emerging intestinal Microsporidia infection in HIV(+)/AIDS patients in Iran: microscopic and molecular detection. Iran J Parasitol. 2014;9:149–54.PubMedPubMedCentral
20.
Sulaiman IM, Fayer R, Yang C, Santin M, Matos O, Xiao L. Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Parasitol Res. 2004;92:328–34.CrossRefPubMed
21.
Santin M, Fayer R. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol. 2009;56:34–8.CrossRefPubMed
22.
Karim MR, Dong H, Yu F, Jian F, Zhang L, Wang R, et al. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J Clin Microbiol. 2014;52:3297–302.CrossRefPubMedPubMedCentral
23.
Thellier M, Breton J. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite. 2008;15:349–58.CrossRefPubMed
24.
Santin M, Fayer R. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci. 2011;90:363–71.CrossRefPubMed
25.
Kotler DP, Orenstein JM. Clinical syndromes associated with microsporidiosis. Adv Parasitol. 1998;40:321–49.CrossRefPubMed
26.
Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, et al. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitol Int. 2014;63:132–7.CrossRefPubMed
27.
Tumwine JK, Kekitiinwa A, Nabukeera N, Akiyoshi DE, Buckholt MA, Tzipori S. Enterocytozoon bieneusi among children with diarrhea attending Mulago hospital in Uganda. Am J Trop Med Hyg. 2000;67:299–303.CrossRef
28.
Gumbo T, Sarbah S, Gangaidzo IT, Ortega Y, Sterling CR, Carville A, et al. Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe. AIDS. 1999;13:819–21.CrossRefPubMed
29.
Wang L, Zhang H, Zhao X, Zhang L, Zhang G, Guo M, et al. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol. 2013;51:557–63.CrossRefPubMedPubMedCentral
30.
van Hal SJ, Muthiah K, Matthews G, Harkness J, Stark D, Cooper D, et al. Declining incidence of intestinal microsporidiosis and reduction in AIDS-related mortality following introduction of HAART in Sydney, Australia. Trans R Soc Trop Med Hyg. 2007;101:1096–100.CrossRefPubMed
31.
Conteas CN, Berlin OGW, Ash LR, Pruthi JS. Therapy for human gastrointestinal microsporidiosis. Am J Trop Med Hyg. 2000;63:121–7.CrossRefPubMed
32.
Akinbo FO, Okaka CE, Omoregie R, Dearen T, Leon ET, Xiao L. Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. Am J Trop Med Hyg. 2012;86:441–5.CrossRefPubMedPubMedCentral
33.
Saksirisampant W, Prownebon J, Saksirisampant P, Mungthin M, Siripatanapipong S, Leelayoova S. Intestinal parasitic infections: prevalences in HIV/AIDS patients in a Thai AIDS-care centre[J]. Ann Trop Med Parasitol. 2009;103:573–81.CrossRefPubMed
34.
Schwartz DA, Sobottka I, Leitch GJ, Cali A, Visvesvara GS. Pathology of microsporidiosis - emerging parasitic infections in patients with acquired immunodeficiency syndrome. Arch Pathol Lab Med. 1996;120:173–88.PubMed
35.
Chukwuma C. Microsporidium in AIDS patients: a perspective. East Afr Med J. 1996;73:72–5.PubMed
36.
Canning EU, Hollister WS. Enterocytozoon bieneusi (Microspora): prevalence and pathogenicity in AIDS patients. Trans R Soc Trop Med Hyg. 1990;84:181–6.CrossRefPubMed
37.
Clarridge JE, Karkhanis S, Rabeneck L, Marino B, Foote LW. Quantitative light microscopic detection of Enterocytozoon bieneusi in stool specimens: a longitudinal study of human immunodeficiency virus-infected microsporidiosis patients. J Clin Microbiol. 1996;34:520–3.PubMedPubMedCentral
38.
Rabeneck L, Gyorkey F, Genta RM, Gyorkey P, Foote LW, Risser JM. The role of Microsporidia in the pathogenesis of HIV-related chronic diarrhea. Ann Intern Med. 1993;119:895–9.CrossRefPubMed
39.
Goetz M, Eichenlaub S, Pape GR, Hoffmann RM. Chronic diarrhea as a result of intestinal microsposidiosis in a liver transplant recipient. Transplantation. 2001;71:334–7.CrossRefPubMed
40.
Metge S, Van Nhieu JT, Dahmane D, Grimbert P, Foulet F, Sarfati C, Bretagne SA. Case of Enterocytozoon bieneusi infection in an HIV-negative renal transplant recipient. Eur J Clin Microbiol Infect Dis. 2000;19:221–3.CrossRefPubMed
41.
Rabodonirina M, Bertocchi M, Desportes-Livage I, Cotte L, Levrey H, Piens MA, Monneret G, Celard M, Mornex JF, Mojon M. Enterocytozoon bieneusi as a cause of chronic diarrhea in a heart-lung transplant recipient who was seronegative for human immunodeficiency virus. Clin Infect Dis. 1996;23:114–7.CrossRefPubMed
42.
Wanke CA, DeGirolami P, Federman M. Enterocytozoon bieneusi infection and diarrheal disease in patients who were not infected with human immunodeficiency virus: case report and review. Clin Infect Dis. 1996;23:816–8.CrossRefPubMed
43.
Liu H, Shen Y, Yin J, Yuan Z, Jiang Y, Xu Y, et al. Prevalence and genetic characterization of Cryptosporidium, Enterocytozoon, Giardia and Cyclospora in diarrheal outpatients in China. BMC Infect Dis. 2014;14:25.CrossRefPubMedPubMedCentral
44.
Breitenmoser AC, Mathis A, Burgi E, Weber R, Deplazes P. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology. 1999;118:447–53.CrossRefPubMed
45.
Deplazes P, Mathis A, Muller C, Weber R. Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J Eukaryot Microbiol. 1996;43:93S.CrossRefPubMed
46.
Breton J, Bart-Delabesse E, Biligui S, Carbone A, Seiller X, Okome-Nkoumou M, et al. New highly divergent rRNA sequence among biodiverse genotypes of Enterocytozoon bieneusi strains isolated from humans in Gabon and Cameroon. J Clin Microbiol. 2007;45:2580–9.CrossRefPubMedPubMedCentral
47.
Leelayoova S, Subrungruang I, Suputtamongkol Y, Worapong J, Petmitr PC, Mungthin M. Identification of genotypes of Enterocytozoon bieneusi from stool samples from human immunodeficiency virus-infected patients in Thailand. J Clin Microbiol. 2006;44:3001–4.CrossRefPubMedPubMedCentral
48.
Sulaiman IM, Bern C, Gilman R, Cama V, Kawai V, Vargas D, et al. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in lima, Peru. J Eukaryot Microbiol. 2003;50:591–6.CrossRefPubMed
49.
Ayinmode AB, Zhang H, Dada-Adegbola HO, Xiao L. Cryptosporidium hominis subtypes and Enterocytozoon bieneusi genotypes in HIV-infected persons in Ibadan, Nigeria. Zoonoses Public Health. 2014;61:297–303.CrossRefPubMed
50.
Mirjalali H, Mirhendi H, Meamar AR, Mohebali M, Askari Z, Mirsamadi E, et al. Genotyping and molecular analysis of Enterocytozoon bieneusi isolated from immunocompromised patients in Iran. Infect Genet Evol. 2015;36:244–9.CrossRefPubMed
51.
Chabchoub N, Abdelmalek R, Breton J, Kanoun F, Thellier M, Bouratbine A, et al. Gnotype identification of Enterocytozoon bieneusi isolates from stool samples of HIV-infected Tunisianpatients. Parasite. 2012;19:147–51.CrossRefPubMedPubMedCentral
52.
Wumba R, Longo-Mbenza B, Menotti J, Mandina M, Kintoki F, Situakibanza NH, et al. Epidemiology, clinical, immune, and molecular profiles of microsporidiosis and cryptosporidiosis among HIV/AIDS patients. Int J Gen Med. 2012;5:603–11.PubMedPubMedCentral
53.
54.
Espern A, Morio F, Miegeville M, Illa H, Abdoulaye M, Meyssonnier V, et al. 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. 2007;45:2999–3002.CrossRefPubMedPubMedCentral
55.
Buckholt MA, Lee JH, Tzipori S. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol. 2002;68:2595–9.CrossRefPubMedPubMedCentral
56.
Tavalla M, Mardani-Kateki M, Abdizadeh R, Nashibi R, Rafie A, Khademvatan S. Molecular identification of Enterocytozoon bieneusi and Encephalitozoon spp. in immunodeficient patients in Ahvaz, Southwest of Iran. Acta Trop. 2017;172:107–112.
57.
Li W, Diao R, Yang J, Xiao L, Lu Y, Li YS, et al. High diversity of human-pathogenic Enterocytozoon bieneusi genotypes in swine in northeast China. Parasitol Res. 2014;113:1147–53.CrossRefPubMed
58.
Akinbo FO, Okaka CE, Omoregie R, Adamu H, Xiao L. Unusual Enterocytozoon bieneusi genotypes and Cryptosporidium hominis subtypes in HIV-infected patients on highly active antiretroviral therapy. Am J Trop Med Hyg. 2013;89:157–61.CrossRefPubMedPubMedCentral
59.
Sarfati C, Bourgeois A, Menotti J, Liegeois F, Moyou-Somo R, Delaporte E, et al. Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg. 2006;74:162–4.PubMed
60.
Stark D, van Hal S, Barratt J, Ellis J, Marriott D, Harkness J. Limited genetic diversity among genotypes of Enterocytozoon bieneusi strains isolated from HIV-infected patients from Sydney, Australia. J Med Microbiol. 2009;58(Pt 3):355–7.CrossRefPubMed
61.
ten Hove RJ, Van Lieshout L, Beadsworth MB, Perez MA, Spee K, Claas EC, Verweij JJ. Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups. J Eukaryot Microbiol. 2009;56(4):388–93. 19602086CrossRefPubMed
62.
Khanduja S, Ghoshal U, Agarwal V, Pant P, Ghoshal UC. Identification and genotyping of Enterocytozoon bieneusi among human immunodeficiency virus infected patients. J Infect Public Health. 2017;10(1):31–40.CrossRefPubMed
Metadata
Title
Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region, China
Authors
Hua Liu
Zhihua Jiang
Zhongying Yuan
Jianhai Yin
Zunfu Wang
Bingxue Yu
Dongsheng Zhou
Yujuan Shen
Jianping Cao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2787-9

Other articles of this Issue 1/2017

BMC Infectious Diseases 1/2017 Go to the issue

Research article

Assessments of serum copper and zinc concentration, and the Cu/Zn ratio determination in patients with multidrug resistant pulmonary tuberculosis (MDR-TB) in Côte d’Ivoire

Research article

The predictors of 3- and 30-day mortality in 660 MERS-CoV patients

Case report

First case report of endocarditis caused by haematobacter massiliensis in China

Research Article

Multi-state models for the analysis of time-to-treatment modification among HIV patients under highly active antiretroviral therapy in Southwest Ethiopia

Research article

Accuracy of serum procalcitonin for the diagnosis of sepsis in neonates and children with systemic inflammatory syndrome: a meta-analysis

Research article

A comparison of the test-negative and the traditional case-control study designs for estimation of influenza vaccine effectiveness under nonrandom vaccination
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits