Skip to main content

Advertisement

Log in

Multimethodological Approach to Gastrointestinal Microsporidiosis in HIV-Infected Patients

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Microsporidiosis is an opportunistic infection that produces chronic diarrhoea and cholangiopathy in patients with AIDS, mainly caused by two species of microsporidia, Enterocytozoon bieneusi and Encephalitozon intestinalis. The aim of this work was to develop an integral system for the diagnosis of microsporidiosis of the intestine and biliary tract in HIV-infected patients, comprising microscopic and molecular techniques.

Methods

The study population comprised 143 adult patients of both sexes with diagnosis of HIV infection, with chronic diarrhoea, and with or without HIV-associated cholangiopathy. Stool studies for microsporidia identification of spores were performed on each patient. A video esofagogastroduodenoscopy with biopsy collection was also carried out for routine histology and semi-thin sections stained with Azure II. Species identification was carried out by transmission electron microscopy and/or polymerase chain reaction for the species E. bieneusi and E. intestinalis.

Results

Out of the 143 patients a total of 12.6% (n = 18) were infected with microsporidia. Microsporidia species identified in most cases was E. bieneusi (16/18 cases), followed by E. intestinalis (4/18), all of these last ones in coinfection with E. bieneusi.

Conclusions

Clinical, imaging, microscopic and molecular analyses, when applied in a systematic and integrated approach, allow diagnosis and identification of microsporidia at species level in AIDS patients with chronic diarrhoea, and with or without HIV-associated cholangiopathy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Abdalian R, Heathcote EJ (2006) Sclerosing cholangitis: a focus on secondary causes. Hepatology 44:1063–1074

    PubMed  Google Scholar 

  2. Aissa S, Chabchoub N, Abdelmalek R, Kanoun F, Goubantini A, Ammari L, Kilani B, Bouratbine A, Tiouiri-Ben Aissa H, Aoun K (2017) Asymptomatic intestinal carriage of microsporidia in HIV-positive patients in Tunisia: prevalence, species, and pathogenesis. Med Sante Trop 27:281–285. https://doi.org/10.1684/mst.2017.0697

    Article  CAS  PubMed  Google Scholar 

  3. Anastasi JK, Capili B (2000) HIV and diarrhea in the era of HAART: 1998 New York state hospitalizations. Am J Infect Control 28:262–266

    CAS  PubMed  Google Scholar 

  4. Asmuth DM, DeGirolami PC, Federman M, Ezratty CR, Pleskow DK, Desai G, Wanke CA (1994) Clinical features of microsporidosis in patients with AIDS. Clin Infect Dis 18:819–825

    CAS  PubMed  Google Scholar 

  5. Bartholomew JW (1981) Stains for microorganisms in sections. In: Clark G (ed) Staining procedures, 4th edn. Williams & Wilkins, Baltimore, pp 441–473

    Google Scholar 

  6. Bednarska M, Jankowska I, Pawelas A, Piwczyńska K, Bajer A, Wolska-Kuśnierz B, Wielopolska M, Welc-Falęciak R (2018) Prevalence of Cryptosporidium, Blastocystis, and other opportunistic infections in patients with primary and acquired immunodeficiency. Parasitol Res 117:2869–2879. https://doi.org/10.1007/s00436-018-5976-6

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bini EJ, Cohen J (1998) Diagnostic yield and cost-effectiveness of endoscopy in chronic human immunodeficiency virus-related diarrhea. Gastrointest Endosc 48:354

    CAS  PubMed  Google Scholar 

  8. Blanshard C, Ellis DS, Tovey DG, Dowell S, Gazzard BG (1992) Treatment of intestinal microsporidiosis with albendazole in patients with AIDS. AIDS 6:311–313

    CAS  PubMed  Google Scholar 

  9. Blanshard C, Francis N, Gazzard BG (1996) Investigation of chronic diarrhoea in acquired immunodeficiency syndrome. A prospective study of 155 patients. Gut 39:824–832

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Boldorini R, Tosoni A, Mazzucco G, Cernuschi M, Caramello P, Maran E, Costanzi G, Monga G (1996) Intracellular protozoan infection in small intestinal biopsies of patients with AIDS. Pathol Res Pract 192:249–259

    CAS  PubMed  Google Scholar 

  11. Bouche H, Housset C, Dumont JL, Carnot F, Menu Y, Aveline B, Belghiti J, Boboc B, Erlinger S, Berthelot P (1993) AIDS-related cholangitis: diagnostic features and course in 15 patients. J Hepatol 17:34–39

    CAS  PubMed  Google Scholar 

  12. Bozzola J, Russel LD (1999) Specimens preparation for transmission electron microscopy. In: Bozzola J, Russel LD (eds) Electron microscopy: principles and techniques for biologist, 2nd edn. Jones and Bartlett Publishers, Sudbury, pp 16–47

    Google Scholar 

  13. Brasil P, de Lima DB, de Paiva DD, Lobo MS, Sodre FC, da Silva SP, Verissimo-Villela E, da Silva EJ, Peralta JM, Morgado M, Moura H (1999) Emerging and opportunistic intestinal parasites in HIV-infected patients with chronic diarrhea in Rio de Janeiro, Brazil. J Eukaryot Microbiol 46:40S–41S

    CAS  PubMed  Google Scholar 

  14. Brasil P, de Lima DB, de Paiva DD, Lobo MS, Sodré FC, Silva SP, Villela EV, Silva EJ, Peralta JM, Morgado M, Moura H (2000) Clinical and diagnostic aspects of intestinal microsporidiosis in HIV-infected patients with chronic diarrhea in Rio de Janeiro, Brazil. Rev Inst Med Trop Sao Paulo 42:299–304

    CAS  PubMed  Google Scholar 

  15. Bryan RT, Schwartz DA (1999) Epidemiology of microsporidiosis. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. A.M.S. Press, Washington DC, pp 502–516

    Google Scholar 

  16. Cali A, Becnel JJ, Takvorian PM (2017) Microsporidia. In: Archibald JM, Simpson AGB, Slamovits CH (eds) Handbook of the protists. Publisher Springer International Publishing AG, Cham, pp 1559–1618

    Google Scholar 

  17. Cali A, Kotler DP, Orenstein JM (1993) Septata intestinalis n.g., n. sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients. J Eukaryot Microbiol 40:101–112

    CAS  PubMed  Google Scholar 

  18. Canning EU (1993) Microsporidia. In: Kreier JP, Baker JR (eds) Parasitic protozoa. Academic Press, New York, pp 299–385

    Google Scholar 

  19. Canning EU, Lom J (1986) The microsporidia of vertebrates. Academic, London

    Google Scholar 

  20. Carnevale S, Velásquez JN, Labbé JH, Chertcoff A, Cabrera MG, Rodríguez MI (2000) Diagnosis of Enterocytozoon bieneusi by PCR in stool samples eluted from filter paper disks. Clin Diagn Lab Immunol 7:504–506

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Carville A, Mansfield K, Widmer G, Lackner A, Kotler D, Wiest P, Gumbo T, Sarbah S, Tzipori S (1997) Development and application of genetic probes for detection of Enterocytozoon bieneusi in formalin-fixed stools and in intestinal biopsy specimens from infected patients. Clin Diagn Lab Immunol 4:405–408

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Cello JP (1989) Acquired immunodeficiency syndrome cholangiopathy: spectrum of disease. Am J Med 86:539–546

    CAS  PubMed  Google Scholar 

  23. Cello JP, Day LW (2009) Idiopathic AIDS enteropathy and treatment of gastrointestinal opportunistic pathogens. Gastroenterology 136:1952–1965. https://doi.org/10.1053/j.gastro.2008.12.073

    Article  CAS  PubMed  Google Scholar 

  24. Cello JP (1997) Hepatobiliary manifestations in AIDS. In: Podolsky DK, Friedman LS (eds) Gastroenterology in the centennial year and beyond. AGA, Washington DC, pp 399–403

    Google Scholar 

  25. Chacin-Bonilla L, Panunzio AP, Monsalve-Castillo FM, Parra-Cepeda IE, Martinez R (2006) 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 74:482–486

    PubMed  Google Scholar 

  26. Choudhary MM, Metcalfe MG, Arrambide K, Bern C, Visvesvara GS, Pieniazek NJ, Bandea RD, Deleon-Carnes M, Adem P, Choudhary MM, Zaki SR, Saeed MU (2011) Tubulinosema sp. microsporidian myositis in immunosuppressed patient. Emerg Infect Dis 17:1727–1730. https://doi.org/10.3201/eid1709.101926

    Article  PubMed  PubMed Central  Google Scholar 

  27. Cohen J, West AB, Bini EJ (2001) Infectious diarrhea in human immunodeficiency virus. Gastroenterol Clin N Am 30:637–664

    CAS  Google Scholar 

  28. Conteas CN, Berlin OG, Lariviere MJ, Pandhumas SS, Speck CE, Porschen R, Nakaya T (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

    CAS  PubMed  Google Scholar 

  29. Coyle CM, Wittner M, Kotler DP, Noyer C, Orenstein JM, Tanowitz HB, Weiss M (1996) Prevalence of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon (Septata) intestinalis among patients with AIDS-related diarrhea: determination by the polymerase chain reaction to the microsporidian small subunit-rRNA gene. Clin Infect Dis 23:1002–1006

    CAS  PubMed  Google Scholar 

  30. Curgy JJ, Vavra J, Vivares C (1980) Presence of ribosomal RNAs with prokaryotic properties in microsporidia, eukaryotic organisms. Biol Cell 38:49–51

    CAS  Google Scholar 

  31. da Silva AJ, Schwartz DA, Visvesvara GS, de Moura H, Slemenda SB, Pieniazek NJ (1997) Detection of Septata intestinalis (Microsporidia) Cali et al. 1993 using polymerase chain reaction primers targeting the small submit subunit ribosomal RNA coding region. Mol Diagn 2:47–52

    PubMed  Google Scholar 

  32. da Silva AJ, Schwartz DA, Visvesvara GS et al (1996) Sensitive PCR diagnosis of infections by Enterocytozoon bieneusi (microsporidia) using primers based on the region coding for small-subunit rRNA. J Clin Microbiol 34(4):986–987

    PubMed  PubMed Central  Google Scholar 

  33. David F, Schuitema AR, Sarfati C, Liguory O, Hartskeerl RA, Derouin F, Molina JM (1996) Detection and species identification of intestinal microsporidia by polymerase chain reaction in duodenal biopsies from human immunodeficiency virus-infected patients. J Infect Dis 174:874–877

    CAS  PubMed  Google Scholar 

  34. del Aguila C, Lopez-Velez R, Fenoy S, Turrientes C, Cobo J, Navajas R, Visvesvara GS, Croppo GP, da Silva AJ, Pieniazek NJ (1997) Identification of Enterocytozoon bieneusi spores in respiratory samples from an AIDS patient with 2-year history of intestinal microsporidiosis. J Clin Microbiol 35:1862–1866

    PubMed  PubMed Central  Google Scholar 

  35. Devarbhavi H, Sebastian T, Seetharamu SM, Karanth D (2010) HIV/AIDS cholangiopathy: clinical spectrum, cholangiographic features and outcome in 30 patients. J Gastroenterol Hepatol 25:1656–1660. https://doi.org/10.1111/j.1440-1746.2010.06336.x

    Article  PubMed  Google Scholar 

  36. Dickson BC, Streutker CJ, Chetty R (2006) Coeliac disease: an update for pathologists. J Clin Pathol 59:1009–1016

    Google Scholar 

  37. Eeftinck Schattenkerk JK, van Gool T, van Ketel RJ, Bartelsman JF, Kuiken CL, Terpstra WJ, Reiss P (1991) Clinical significance of small-intestinal microsporidiosis in HIV-1-infected individuals. Lancet 337:895–898

    CAS  PubMed  Google Scholar 

  38. Espern A, Morio F, Miegeville M, Illa H, Abdoulaye M, Meyssonnier V, Adehossi E, Lejeune A, Cam PD, Besse B, Gay-Andrieu F (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 45:2999–3002

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Fayer R, Santin-Duran M (2014) Epidemiology of micro-sporidia in human infections. In: Weiss L, Becnel JJ (eds) Microsporidia: pathogens of opportunity. Wiley, New Yersey, pp 135–164

    Google Scholar 

  40. Fletcher SM, Stark D, Harkness J, Ellis J (2012) Enteric protozoa in the developed world: a public health perspective. Clin Microbiol Rev 25:420–449. https://doi.org/10.1128/CMR.05038-11

    Article  PubMed  PubMed Central  Google Scholar 

  41. Flórez AC, García DA, Moncada L, Beltrán M (2003) Prevalence of microsporidia and other intestinal parasites in patients with HIV infection, Bogota, 2001. Biomedica 23:274–282

    PubMed  Google Scholar 

  42. Franzen C, Kuppers R, Müller A et al (1996) Genetic evidence for latent Septata intestinalis infection in human immunodeficiency virus-infected patients with intestinal microsporidiosis. J Infect Dis 173(4):1038–1040

    CAS  PubMed  Google Scholar 

  43. Franzen C, Müller A (1999) Cryptosporidia and Microsporidia-waterborne diseases in the immunocompromised host. Diagn Microbiol Infect Dis 34:245–262

    CAS  PubMed  Google Scholar 

  44. Franzen C, Müller A, Hartmann P, Kochanek M, Diehl V, Fätkenheuer G (1996) Disseminated Encephalitozoon (Sepatata) intestinalis infection in a patient with AIDS. N Engl J Med 335:1610–1611

    CAS  PubMed  Google Scholar 

  45. Franzen C, Müller A, Hegener P, Salzberger B, Hartmann P, Fätkenheuer G, Diehl V, Schrappe M (1995) Detection of microsporidia (Enterocytozoon bieneusi) in intestinal biopsy specimens from human immunodeficiency virus-infected patients by PCR. J Clin Microbiol 33:2294–2296

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Garcia LS (2002) Laboratory identification of the microsporidia. J Clin Microbiol 40:1892–1901

    PubMed  PubMed Central  Google Scholar 

  47. Gazzard B, Blanshard C (1993) Diarrhoea in AIDS and other immunodeficiency states. Baillieres Clin Gastroenterol 7:387–419

    CAS  PubMed  Google Scholar 

  48. Ghoyounchi R, Mahami-Oskouei M, Rezamand A, Spotin A, Aminisani N, Nami S, Pirestani M, Berahmat R, Madadi S (2019) Molecular phylodiagnosis of Enterocytozoon bieneusi and Encephalitozoon intestinalis in children with cancer: microsporidia in malignancies as an emerging opportunistic infection. Acta Parasitol. https://doi.org/10.2478/s11686-018-00012-w (epub ahead of print)

    Article  PubMed  Google Scholar 

  49. Graczyk TK, Johansson MA, Tamang L, Visvesvara GS, Moura LS, DaSilva AJ, Girouard AS, Matos O (2007) Retrospective species identification of microsporidian spores in diarrheic fecal samples from human immunodeficiency virus/AIDS patients by multiplexed fluorescence in situ hybridization. J Clin Microbiol 45:1255–1260

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Greigert V, Pfaff AW, Abou-Bacar A, Candolfi E, Brunet J (2018) Intestinal microsporidiosis in Strasbourg from 2014 to 2016: emergence of an Enterocytozoon bieneusi genotype of Asian origin. Emerg Microbes Infect 7:97. https://doi.org/10.1038/s41426-018-0099-9

    Article  PubMed  PubMed Central  Google Scholar 

  51. Hassan NA, Lim YAL, Mahmud R, Mohd-Shaharuddin N, Wan Sulaiman WY, Ngui R (2018) Molecular diagnosis of microsporidia among immunocompromised patients in Kuala Lumpur, Malaysia. Am J Trop Med Hyg 99:1562–1566. https://doi.org/10.4269/ajtmh.17-0901

    Article  CAS  PubMed  Google Scholar 

  52. Hutin YJ, Sombardier MN, Liguory O, Sarfati C, Derouin F, Modaï J, Molina JM (1998) Risks factors for intestinal microsporidiosis in patients infected with human immunodeficiency virus. J Infect Dis 178:904–907

    CAS  PubMed  Google Scholar 

  53. Ishihara R, Hayashi Y (1968) Some properties of ribosomes from the sporoplasm of Nosema bombysis. J Invertebr Pathol 11:377–385

    CAS  Google Scholar 

  54. Kearney DJ, Steuerwald M, Koch J (1999) A prospective study of endoscopy in HIV associated diarrhea. Am J Gastroenterol 94:596–602

    CAS  PubMed  Google Scholar 

  55. Kim LS, Hadley WK, Stansell J, Cello JP, Koch J (1998) Declining prevalence of cryptosporidiosis in San Francisco. Clin Infect Dis 27:655–656

    CAS  PubMed  Google Scholar 

  56. Kotler DP, Orenstein JM (1995) Microsporidia. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL (eds) Infections of the gastrointestinal tract. Raven Press, New York, pp 1129–1140

    Google Scholar 

  57. Kotler DP, Orenstein JM (1997) Clinical syndromes associated with microsporidiosis. In: Chandler FW, Schwartz DA, Manz HJ, Lack EE (eds) Pathology of infectious diseases. Appleton & Lange, Stamford, pp 258–292

    Google Scholar 

  58. Kotler DP, Orenstein JM (1998) Clinical syndromes associated with microsporidiosis. Adv Parasitol 40:321–349

    CAS  PubMed  Google Scholar 

  59. Kotler DP, Orenstein JM (1999) Clinical syndromes associated with microsporidiosis. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. A.M.S. Press, Washington DC, pp 258–292

    Google Scholar 

  60. Li W, Feng Y, Santin M (2019) Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol 35:436–451. https://doi.org/10.1016/j.pt.2019.04.004

    Article  PubMed  Google Scholar 

  61. Liguory O, David F, Sarfati C, Schuitema AR, Hartskeerl RA, Derouin F, Modaï J, Molina JM (1997) Diagnosis of infections caused by Enterocytozoon bieneusi and Encephalitozoon intestinalis using polymerase chain reaction in stool specimens. AIDS 11:723–726

    CAS  PubMed  Google Scholar 

  62. Mansfield KG, Carville A, Shvetz D, MacKey J, Tzipori S, Lackner AA (1997) Identification of an Enterocytozoon bieneusi-like microsporidian parasite in simian-immunodeficiency-virus-inoculated macaques with hepatobiliary disease. Am J Pathol 150:1395–1405

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Maratka Z (1984) Terminology, definitions and diagnostic criteria in digestive endoscopy. With the collaboration of the members of the Terminology Committee of the World Society of Digestive Endoscopy/OMED. Scand J Gastroenterol Suppl 103:1–74

    CAS  PubMed  Google Scholar 

  64. McWilliam LJ, Curry A (1990) Intestinal microsporidiosis in AIDS. J Clin Pathol 43:173–174

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Michiels JF, Hofman P, Saint Paul MC, Loubière R, Bernard E, LeFichoux Y (1993) Pathological features of intestinal microsporidiosis in HIV positive patients: a report of 13 new cases. Pathol Res Pract 189:377–383

    CAS  PubMed  Google Scholar 

  66. Mönkemüller KE, Call SA, Lazenby AJ, Wilcox CM (2000) Declining prevalence of opportunistic gastrointestinal disease in the era of combination antiretroviral therapy. Am J Gastroenterol 95:457–462

    PubMed  Google Scholar 

  67. Morio F, Poirier P, Le Govic Y, Laude A, Valot S, Desoubeaux G, Argy N, Nourrisson C, Pomares C, Machouart M, Dalle F, Botterel F, Bourgeois N, Cateau E, Leterrier M, Beser J, Lavergne RA, Le Pape P (2019) Assessment of the first commercial multiplex PCR kit (ParaGENIE Crypto-Micro Real-Time PCR) for the detection of Cryptosporidium spp., Enterocytozoon bieneusi, and Encephalitozoon intestinalis from fecal samples. Diagn Microbiol Infect Dis. https://doi.org/10.1016/j.diagmicrobio.2019.04.004

    Article  PubMed  Google Scholar 

  68. Moura H, Da Silva JL, Sodré FC, Brasil P, Wallmo K, Wahlquist S, Wallace S, Croppo GP, Visvesvara GS (1996) Gram-chromotrope: a new technique that enhaces detection of microsporidial spores in clinical samples. J Eukaryot Microbiol 43:94S–95S

    CAS  PubMed  Google Scholar 

  69. Nasarudin SN, Zainudin NS, Bernadus M, Nawi AM, Hanafiah A, Osman E (2015) Loop-mediated isothermal amplification for rapid molecular detection of Enterocytozoon bieneusi in faecal specimens. J Med Microbiol 64:1329–1334

    CAS  PubMed  Google Scholar 

  70. Nooshadokht M, Sharifi I, Mohammadi MA, Pirestani M, Afgar A, Mahootchi A, Salari S (2017) Intestinal microsporidiosis in Iran: infection in immune-compromised and immunocompetent patients. Curr Med Mycol 3:30–36. https://doi.org/10.18869/acadpub.cmm.3.1.30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ombrouck C, Ciceron L, Biligui S, Brown S, Marechal P, van Gool T, Datry A, Danis M, Desportes-Livage I (1997) Specific PCR assay for direct detection of intestinal microsporidia Enterocytozoon bieneusi and Encephalitozoon intestinalis in fecal specimens from human immunodeficiency virus-infected patients. J Clin Microbiol 35:652–655

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Ombrouck C, Ciceron L, Desportes-Livage I (1996) Specific and rapid detection of Microsporidia in stool specimens from AIDS patients by PCR. Parasite 3:85–86

    CAS  PubMed  Google Scholar 

  73. Ombrouck C, Desportes-Livage I, Achbarou A, Gentilini M (1996) Specific detection of microsporidia Encephalitozoon intestinalis in AIDS patients. C R Acad Sci III 319:39–43

    CAS  PubMed  Google Scholar 

  74. Orenstein JM (1991) Microsporidiosis in the acquired immunodeficiency syndrome. J Parasitol 77:843–864

    CAS  PubMed  Google Scholar 

  75. Orenstein JM (1997) Microsporidiosis. In: Chandler FW, Schwartz DA, Manz HJ, Lack EE (eds) Pathology of infectious diseases. Appleton & Lange, Stamford, pp 1223–1239

    Google Scholar 

  76. Orenstein JM, Chiang J, Steinberg W, Smith PD, Rotterdam H, Kotler DP (1990) Intestinal microsporidiosis as cause of diarrhea in human immunodeficiency virus-infected patients: a report of 20 cases. Hum Pathol 21:475–481

    CAS  PubMed  Google Scholar 

  77. Orenstein JM, Tenner M, Kotler DP (1992) Localization of infection by microsporidian Enterocytozoon bieneusi in the gastrointestinal tract of AIDS patients with diarrhea. AIDS 6:195–197

    CAS  PubMed  Google Scholar 

  78. Pariyakanok L, Satitpitakul V, Putaporntip C, Jongwutiwes S (2015) Femtosecond laser-assisted anterior lamellar keratoplasty in stromal keratitis caused by an Endoreticulatus-like microsporidia. Cornea 34:588–591. https://doi.org/10.1097/ICO.0000000000000392

    Article  PubMed  Google Scholar 

  79. Peacock CS, Blanshard C, Tovey DG, Ellis DS, Gazzard BG (1991) Histological diagnosis of intestinal microsporidiosis in patients with AIDS. J Clin Pathol 44:558–563

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Pol S, Romana CA, Richard S, Amouyal P, Desportes-Livage I, Carnot F, Pays JF, Berthelot P (1993) Microsporidia infection in patients with the human immunodeficiency virus and unexplained cholangitis. N Engl J Med 328:95–99

    CAS  PubMed  Google Scholar 

  81. Rabeneck L, Genta RM, Gyorkey F, Clarridge JE, Gyorkey P, Foote LW (1995) Observations on the pathological spectrum and clinical course of microsporidiosis in men infected with the human immunodeficiency virus: follow-up study. Clin Infect Dis 20:1229–1235

    CAS  PubMed  Google Scholar 

  82. Rijpstra AC, Canning EU, Van Ketel RJ, Eeftinck Schattenkerk JK, Laarman JJ (1988) Use of light microscopy to diagnose small-intestinal microsporidiosis in patients with AIDS. J Infect Dis 157:827–831

    CAS  PubMed  Google Scholar 

  83. Rinder H, Janitschke K, Aspöck H, Da Silva AJ, Deplazes P, Fedorko DP, Franzen C, Futh U, Hünger F, Lehmacher A, Meyer CG, Molina JM, Sandfort J, Weber R, Löscher T (1998) Blinded, externally controlled multicenter evaluation of light microscopy and PCR for detection of microsporidia in stool specimens. The Diagnostic Multicenter Study Group on Microsporidia. J Clin Microbiol 36:1814–1818

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Sabrá A, Madi K (1994) Correlação clínica e estudo estereomicroscópico e histológico da mucosa intestinal. In: Sabrá A (ed) Diarréia Aguda e Crônica em Pediatria. Quarta edição. Editora Cultura medica, Rio de Janeiro, pp 82–92

    Google Scholar 

  85. Shibata D (1994) Extraction of DNA from paraffin-embedded tissue for analysis by polymerase chain reaction: new tricks from an old friend. Hum Pathol 25:561–563

    CAS  PubMed  Google Scholar 

  86. Sodré FC (1996) Microsporidioses humanas: desenvolvimento de métodos para o diagnóstico morfológico das microsporidioses intestinais em pacientes HIV-positivos no município do Rio de Janeiro (Master’s thesis). Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro

    Google Scholar 

  87. Sokolova OI, Demyanov AV, Bowers LC, Didier ES, Yakovlev AV, Skarlato SO, Sokolova YY (2011) Emerging microsporidian infections in Russian HIV-infected patients. J Clin Microbiol 49:2102–2108. https://doi.org/10.1128/JCM.02624-10

    Article  PubMed  PubMed Central  Google Scholar 

  88. Sprague V, Becnel JJ, Hazard EI (1992) Taxonomy of the phylum microspora. Crit Rev Microbiol Rev 18:285–395

    CAS  Google Scholar 

  89. Stentiford GD, Becnel -J, Weiss LM, Keeling PJ, Didier ES, Williams BP, Bjornson S, Kent ML, Freeman MA, Brown MJF, Troemel ER, Roesel K, Sokolova Y, Snowden KF, Solter L (2016) Microsporidia—emergent pathogens in the global food chain. Trends Parasitol 32:336–348. https://doi.org/10.1016/j.pt.2015.12.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Sulaiman IM, Bern C, Gilman R, Cama V, Kawai V, Vargas D, Ticona E, Vivar A, Xiao L (2003) A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. J Eukaryot Microbiol 50(Suppl):591–596

    CAS  PubMed  Google Scholar 

  91. Talal AH, Kotler DP, Orenstein JM, Weiss LM (1998) Detection of Enterocytozoon bieneusi in fecal specimens by polymerase chain reaction analysis with primers to the small-subunit rRNA. Clin Infect Dis 26:673–675

    CAS  PubMed  Google Scholar 

  92. Taniuchi M, Verweij JJ, Sethabutr O, Bodhidatta L, Garcia L, Maro A, Kumburu H, Gratz J, Kibiki G, Houpt ER (2011) Multiplex polymerase chain reaction method to detect Cyclospora, Cystoisospora, and Microsporidia in stool samples. Diagn Microbiol Infect Dis 71:386–390. https://doi.org/10.1016/j.diagmicrobio.2011.08.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Telemann W (1908) Eine methode zur erleichterung der auffindung von parasiteneiern in den faeces. Dtsch Med Wochenschr 35:1510–1511

    Google Scholar 

  94. Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, Akiyoshi DE, Tzipori S (2005) Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg 73:921–925

    PubMed  Google Scholar 

  95. van Gool T, Vetter JC, Weinmayr B, Van Dam A, Derouin F, Dankert J (1997) High seroprevalence of Encephalitozoon species in immunocompetent subjects. J Infect Dis 175:1020–1024

    PubMed  Google Scholar 

  96. Velásquez JN, Carnevale S, Guarnera EA, Labbé JH, Chertcoff A, Cabrera MG, Rodríguez MI (1996) Detection of the microsporidian parasite Enterocytozoon bieneusi in specimens from patients with AIDS by PCR. J Clin Microbiol 34:3230–3232

    PubMed  PubMed Central  Google Scholar 

  97. Velásquez JN, Carnevale S, Oelemann WM, Etchart C, Peralta JM (2005) Diagnosis of Enterocytozoon bieneusi by the polymerase chain reaction in archival fixed duodenal tissue. Enferm Infecc Microbiol Clin 23:218–220

    PubMed  Google Scholar 

  98. Velásquez JN, Chertcoff AV, Etchart C, di Risio C, Sodré FC, Cucher MA, Carnevale S (2012) First case report of infection caused by Encephalitozoon intestinalis in a domestic cat and a patient with AIDS. Vet Parasitol 190:583–586. https://doi.org/10.1016/j.vetpar.2012.06.034

    Article  PubMed  Google Scholar 

  99. Verweij JJ, Ten Hove R, Brienen EA, van Lieshout L (2007) Multiplex detection of Enterocytozoon bieneusi and Encephalitozoon spp. in fecal samples using real-time PCR. Diagn Microbiol Infect Dis 57:163–167

    CAS  PubMed  Google Scholar 

  100. Wanachiwanawin D, Manatsathit S, Lertlaituan P, Thakerngpol K, Suwanagool P (1998) Intestinal microsporidiosis in HIV infected patients with chronic diarrhea in Thailand. Southeast Asian J Trop Med Public Health 29:767–771

    CAS  PubMed  Google Scholar 

  101. Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, Zhu XQ (2018) Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasit Vectors 11:28. https://doi.org/10.1186/s13071-017-2558-x

    Article  PubMed  PubMed Central  Google Scholar 

  102. Watts MR, Chan RC, Cheong EY, Brammah S, Clezy KR, Tong C, Marriott D, Webb CE, Chacko B, Tobias V, Outhred AC, Field AS, Prowse MV, Bertouch JV, Stark D, Reddel SW (2014) Anncaliia algerae microsporidial myositis. Emerg Infect Dis 20:185–191. https://doi.org/10.3201/eid2002.131126

    Article  PubMed  PubMed Central  Google Scholar 

  103. Weber R, Bryan RT, Owen RL, Wilcox CM, Gorelkin L, Visvesvara GS (1992) Improved light-microscopical detection of microsporidia spores in stool and duodenal aspirates. N Engl J Med 326:161–166

    CAS  PubMed  Google Scholar 

  104. Weber R, Bryan RT, Schwartz DA, Owen RL (1994) Human microsporidial infections. Clin Microbiol Rev 7:426–461

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Weber R, Sauer B, Spycher MA, Deplazes P, Keller R, Ammann R, Briner J, Lüthy R (1994) Detection of Septata intestinalis in stool specimens and coprodiagnostic monitoring of successful treatment with albendazole. Clin Infect Dis 19:342–345

    CAS  PubMed  Google Scholar 

  106. Weiss LM, Vossbrinck CR (1998) Microsporidiosis: molecular and diagnostic aspects. Adv Parasitol 40:351–395

    CAS  PubMed  Google Scholar 

  107. Wilcox CM, Rabeneck L, Friedman S (1996) AGA technical review: malnutrition and cachexia, chronic diarrhea and hepatobiliary disease in patients with human immunodeficiency virus infection. Gastroenterology 111:1724–1736

    CAS  PubMed  Google Scholar 

  108. Willson R, Harrington R, Stewart B, Fritsche T (1995) Human immunodeficiency virus 1- associated necrotizing cholangitis caused by infection with Septata intestinalis. Gastroenterology 108:247–251

    CAS  PubMed  Google Scholar 

  109. Wittner M (1999) Historic perspective on the microsporidia: expanding horizons. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. A.M.S. Press, Washington DC, pp 1–6

    Google Scholar 

  110. Zhu X, Wittner M, Tanowitz HB, Kotler D, Cali A, Weiss LM (1993) Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. J Infect Dis 168:1570–1575

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jorge Néstor Velásquez.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Velásquez, J.N., di Risio, C., Etchart, C. et al. Multimethodological Approach to Gastrointestinal Microsporidiosis in HIV-Infected Patients. Acta Parasit. 64, 658–669 (2019). https://doi.org/10.2478/s11686-019-00095-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-019-00095-z

Keywords

Navigation