Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T10:47:17.022Z Has data issue: false hasContentIssue false
  • English
  • Français

Endogenous development of Cystoisospora belli in intestinal and biliary epithelium of humans

Published online by Cambridge University Press:  12 March 2019

J. P. Dubey Open the ORCID record for J. P. Dubey [Opens in a new window] ,
Kimberley J. Evason  and
Zenta Walther
J. P. Dubey*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland, 20705-2350, USA
Kimberley J. Evason
Affiliation:
Department of Pathology and Huntsman Cancer Institute, University of Utah, Salt Lake City, UT 84112, USA
Zenta Walther
Affiliation:
Department of Pathology, Yale University School of Medicine, New Haven, CT 06520-8023, USA
*
Author for correspondence: J. P. Dubey, E-mail: jitender.dubey@ars.usda.gov
Get access Rights & Permissions [Opens in a new window]

Abstract

Cystoisospora (Isospora) belli is a coccidian parasite of humans. It can cause serious digestive disorders involving infection of intestines, biliary tract and gallbladder, especially in those with depressed immunity. It has a direct fecal–oral transmission cycle. After ingestion of sporulated oocysts, the parasite multiplies asexually and sexually within host epithelial cells, resulting in unsporulated oocysts that are excreted in feces. The details of asexual and sexual stages are not known and certain inclusions in epithelial cells in biopsy samples have been erroneously identified recently as C. belli. Here, we provide details of developmental stages of C. belli in two patients, in duodenal biopsy of one and biliary epithelium of the other. Immature and mature asexual stages (schizonts/meronts) were seen in epithelial cells. The merozoites were seen singly, in pairs and in groups in single parasitophorous vacuole (pv) in host cytoplasm. Immature and mature meronts were seen together in the same pv; up to eight nuclei were seen in meronts that retained elongated crescent shape; round multinucleated schizonts, seen in other coccidians, were not found. Meronts were up to 25 µm long and contained up to ten merozoites that were 8–11 µm long. The merozoites and meronts contained PAS-positive granules. Microgamonts (male) contained up to 30 nuclei that were arranged at the periphery and had condensed chromatin; 1–3 PAS-positive, eosinophilic, residual bodies were left when microgametes were formed. The microgametes were 4 µm long and PAS-negative. All stages of macrogamonts, including oocysts were PAS-positive. The detailed description of the life cycle stages of C. belli reported here should facilitate in histopathologic diagnosis of this parasite.

Keywords

CoccidiaCystoisospora (Isospora) belligamontsmerontsmerozoitesoocystsprotozoaschizonts
Type
Research Article
Information
Parasitology , Volume 146 , Issue 7 , June 2019 , pp. 865 - 872
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agholi, M, Aliabadi, E and Hatam, GR (2016) Cystoisosporiasis-related human acalculous cholecystitis: the need for increased awareness. Polish Journal of Pathology 67, 270–276.Google Scholar
Akateh, C, Arnold, CA, Benissan-Messan, D, Michaels, A and Black, SM (2018) Cystoisospora belli gallbladder infection in a liver transplant donor. Case Reports in Infectious Diseases. Article ID 3170238.Google Scholar
Barta, JR, Schrenzel, MD, Carreno, R and Rideout, BA (2005) The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. Journal of Parasitology 91, 726–727.Google Scholar
Benator, DA, French, AL, Beaudet, LM, Levy, CS and Orenstein, JM (1994) Isospora belli infection associated with acalculous cholecystitis in a patient with AIDS. Annals of Internal Medicine 121, 663–664.Google Scholar
Bialek, R, Overkamp, D, Rettig, I and Knobloch, J (2001) Case report: Nitazoxanide treatment failure in chronic isosporiasis. American Journal of Tropical Medicine and Hygiene 65, 94–95.Google Scholar
Brandborg, LL, Goldberg, SB and Breidenbach, WC (1970) Human coccidiosis – a possible cause of malabsorption – the life cycle in small-bowel mucosal biopsies as a diagnostic feature. The New England Journal of Medicine 283, 1306–1313.Google Scholar
Comin, CE and Santucci, M (1994) Submicroscopic profile of Isospora belli enteritis in a patient with acquired immune deficiency syndrome. Ultrastructural Pathology 18, 473–482.Google Scholar
Dubey, JP (2018) A review of Cystoisospora felis and C. rivolta-induced coccidiosis in cats. Veterinary Parasitology 263, 34–48.Google Scholar
Dubey, JP and Frenkel, JK (1972) Cyst-induced toxoplasmosis in cats. Journal of Protozoology 19, 155–177.Google Scholar
Dubey, JP and Lindsay, DS (2019) Coccidiosis in dogs – 100 years of progress. Veterinary Partasitology 266, 34–55.Google Scholar
Faust, EC, Giraldo, LE, Caicedo, G and Bonfante, R (1961) Human isosporosis in the western hemisphere. American Journal of Tropical Medicine and Hygiene 10, 343–349.Google Scholar
Ferreira, LF, Coutinho, SG, Argento, CA and da Silva, JR (1962) Experimental human coccidial enteritis by Isospora belli Wenyon, 1923. A study based on the infection of 5 volunteers. El Hospital; La Revista Interamericana De Hospitales 62, 795–804.Google Scholar
Field, AS (2002) Light microscopic and electron microscopic diagnosis of gastrointestinal opportunistic infections in HIV-positive patients. Pathology 34, 21–35.Google Scholar
Frenkel, JK, de Oliveira Silva, MB, Saldanha, J, de Silva, ML, Correia Filho, VD, Barata, CH, Lages, E, Ramirez, LE and Prata, A (2003) Isospora belli infection: observation of unicellular cysts in mesenteric lymphoid tissues of a Brazilian patient with AIDS and animal inoculation. Journal of Eukaryotic Microbiology 50 (Suppl.), 682–684.Google Scholar
Hamour, A, Curry, A, Ridge, A, Baily, G, Wilson, G and Mandal, B (1997) Isospora belli in a patient with AIDS. Journal of Infection 35, 94–95.Google Scholar
Henderson, HE, Gillepsie, GW, Kaplan, P and Steber, M (1963) The human Isospora. American Journal of Tropical Medicine and Hygiene 78, 302–309.Google Scholar
Henry, K, Bird, RG and Doe, WF (1974) Intestinal coccidiosis in a patient with alpha-chain disease. British Medical Journal 1, 542–543.Google Scholar
Jarpa Gana, A (1966) Coccidiosis humana. Biologica (Santiago) 39, 3–26.Google Scholar
Jeffery, GM (1956) Human coccidiosis in South Carolina. Journal of Parasitology 42, 491–495.Google Scholar
Jongwutiwes, S, Sampatanukul, P and Putaporntip, C (2002) Recurrent isosporiasis over a decade in an immunocompetent host successfully treated with pyrimethamine. Scandinavian Journal Infectious Diseases 34, 859–862.Google Scholar
Kim, MJ, Kim, WH, Jung, HC, Chai, JW and Chai, JY (2013) Isospora belli infection with chronic diarrhea in an alcoholic patient. Korean Journal of Parasitology 51, 207–212.Google Scholar
Lagrange-Xélot, M, Porcher, R, Sarfati, C, de Castro, N, Carel, O, Magnier, JD, Delcey, V and Molina, JM (2008) Isosporiasis in patients with HIV infection in the highly active antiretroviral therapy era in France. HIV Medicine 9, 126–130.Google Scholar
Lai, KK, Goyne, HE, Hernandez-Gonzalo, D, Miller, KA, Tuohy, M, Procop, GW, Lamps, LW and Patil, DT (2016) Cystoisospora belli infection of the gallbladder in immunocompetent patients: a clinicopathologic review of 18 cases. American Journal of Surgical Pathology 40, 1070–1074.Google Scholar
Legua, P and Seas, C (2013) Cystoisospora and Cyclospora. Current Opinion in Infectious Diseases 26, 479–483.Google Scholar
Levine, ND (1973) Protozoan Parasites of Domestic Animals and of Man, 2nd edn. Minneapolis, Minnesota, USA: Burgess, pp. 1–406.Google Scholar
Liebman, WM, Thaler, MM, DeLorimier, A, Brandborg, LL and Goodman, J (1980) Intractable diarrhea of infancy due to intestinal coccidiosis. Gastroenterology 78, 579–584.Google Scholar
Lindsay, DS, Dubey, JP, Toivio-Kinnucan, MA, Michiels, JF and Blagburn, BL (1997) Examination of extraintestinal tissue cysts of Isospora belli. Journal of Parasitology 83, 620–625.Google Scholar
Martelli, MG and Lee, JY (2016) Parasitic infection of the gallbladder: Cystoisospora belli infection as a cause of chronic abdominal pain and acalculous cholecystitis. Journal of the Mississippi State Medical Association 57, 174–176.Google Scholar
Matsubayashi, H and Nozawa, T (1948) Experimental infection of Isospora hominis in man. American Journal of Tropical Medicine Hygiene 28, 633–637.Google Scholar
Meamar, AR, Rezaian, M, Zahabium, F, Faghihi, AH, Oormazdi, H and Kia, EB (2009) Severe diarrhea due to Isospora belli in a patient with thymoma. Journal of Microbiology, Immunology and Infection 42, 526–529.Google Scholar
Michiels, JF, Hofman, P, Bernard, E, Saint Paul, MC, Boissy, C, Mondain, V, Lefichoux, Y and Loubiere, R (1994) Intestinal and extraintestinal Isospora belli infection in an Aids patient. A second case report. Pathology Research and Practice 190, 1089–1093.Google Scholar
Modigliani, R, Bories, C, LeCharpentier, Y, Salmeron, M, Messing, B, Galian, A, Rambaud, JC, Lavergne, A, Cochand-Priollet, B and Desportes, I (1985) Diarrhoea and malabsorption in Acquired Immune Deficiency Syndrome: a study of four cases with special emphasis on opportunistic protozoan infestations. Gut 26, 179–187.Google Scholar
Murphy, SC, Hoogestraat, DR, Sengupta, DJ, Prentice, J, Chakrapani, A and Cookson, BT (2011) Molecular diagnosis of cystoisosporiasis using extended-range PCR screening. Journal of Molecular Diagnostics 13, 359–362.Google Scholar
Niedmann, G (1963) Elementos parasitarios en la mucosa del intestino delgado en biopsias de enfermos con isosporosis. Boletín Chileno de Parasitología 18, 22.Google Scholar
Ortega, YR, Nagle, R, Gilman, RH, Watanabe, J, Miyagui, J, Quispe, H, Kanagusuku, P, Roxas, C and Sterling, CR (1997) Pathologic and clinical findings in patients with cyclosporiasis and a description of intracellular parasite life-cycle stages. Journal of Infectious Diseases 176, 1584–1589.Google Scholar
Peng, CY and Tsai, W (1991) Isospora belli infection in a patient with Hodgkin's disease: report of a case. Journal of the Formosan Medical Association 90, 260–263.Google Scholar
Rao, ACK, Geetha, V, Ranjini, K, Vidhyalakshmi, S and Rupashree, S (2012) Histology as a diagnostic tool for intestinal isosporiasis in immunocompromised patients. Asian Pacific Journal of Tropical Disease 2012, 251–252.Google Scholar
Restrepo, C, Macher, AM and Radany, EH (1987) Disseminated extraintestinal isosporiasis in a patient with acquired immune deficiency syndrome. American Journal of Clinical Pathology 87, 536–542.Google Scholar
Sasaki, M, Tanaka, A, Nishimura, T, Tsujikawa, T, Andoh, A, Ishizuka, I, Koyama, S, Fujiyama, Y and Kushima, R (2004) A case of malabsorption syndrome caused by isosporiasis in an immunocompetent patient. Journal of Gastroenterology 39, 88–89.Google Scholar
Swanson, EA, March, JK, Clayton, F, Couturier, MR, Arcega, R, Smith, R and Evason, KJ (2018) Epithelial inclusions in gallbladder specimens mimic parasite infection: histologic and molecular examination of reported Cystoisospora belli infection in gallbladders of immunocompetent patients. American Journal of Surgical Pathology 42, 1346–1352.Google Scholar
Tatum, A (1916) The influence of bile on autolysis. Journal of Biochemistry 27, 243–248.Google Scholar
Trier, JS, Moxey, PC, Schimmel, EM and Robles, E (1974) Chronic intestinal coccidiosis in man: intestinal morphology and response to treatment. Gastroenterology 66, 923–935.Google Scholar
Velásquez, JN, Carnevale, S, Mariano, M, Kuo, LH, Caballero, A, Chertcoff, A, Ibáñez, C and Bozzini, JP (2001) Isosporosis and unizoite tissue cysts in patients with acquired immunodeficiency syndrome. Human Pathology 32, 500–505.Google Scholar
Velásquez, JN, Osvaldo, GA, Di Risio, C, Etchart, C, Chertcoff, AV, Perissé, GE and Carnevale, S (2011) Molecular characterization of Cystoisospora belli and unizoite tissue cyst in patients with acquired immunodeficiency syndrome. Parasitology 138, 279–286.Google Scholar
Velásquez, JN, di Risio, CA, Etchart, CB, Chertcoff, AV, Nigro, MG, Pantano, ML, Ledesma, BA, Vittar, N and Carnevale, S (2016) First report of Cystoisospora belli parasitemia in a patient with acquired immunodeficiency syndrome. Acta Parasitologica 61, 172–177.Google Scholar
Veldhuyzen van Zanten, SJO, Lange, JMA, Sauerwein, HP, Rijpstra, AC, Laarman, JJ, Rietra, PJGM and Danner, SA (1984) Amprolium for coccidiosis in AIDS. Lancet 2, 345–346.Google Scholar
Walther, Z and Topazian, MD (2009) Isospora cholangiopathy: case study with histologic characterization and molecular confirmation. Human Pathology 40, 1342–1346.Google Scholar
Wenyon, CM (1923) Coccidiosis of cats and dogs and the status of the Isospora of man. Annals of Tropical Medicine Parasitology 17, 231–288.Google Scholar