Abstract
The small intestine, coming in direct contact with ingested potential pathogens, depends on active mucosal immunity to withstand invasion and damage. In patients with AIDS and severe impairment of immunoregulatory lymphocytes, proliferation of protozoal, viral, bacterial, and fungal pathogens produces diarrhea and malabsorption. When noninvasive tests of stool and blood fail to identify responsible organisms, endoscopy can reveal mucosal lesions which are suggestive if not diagnostic. Cryptosporidium, E. intestinalis, CMV, MAC, and other infections can be identified by intestinal biopsy quicker and often at lower overall cost than they can be by culture.
References
- 1.Albrecht H., Sobottka I. Enterocytozoon bieneusi infection in patients who are not infected with human immunodeficiency virus. Clin Infect Dis. 1997;25:344. doi: 10.1086/516920. [DOI] [PubMed] [Google Scholar]
- 2.Allason-Jones E., Mindel A., Sargeaunt P. Entamoeba histolytica as a commensal intestinal parasite in homosexual men. N Engl J Med. 1986;315:353. doi: 10.1056/NEJM198608073150603. [DOI] [PubMed] [Google Scholar]
- 3.Asmuth D.M., DeGirolami P.C., Federman M. Clinical features of microsporidiosis in patients with AIDS. Clin Infect Dis. 1994;18:819. doi: 10.1093/clinids/18.5.819. [DOI] [PubMed] [Google Scholar]
- 4.Asmuth D.M., Hammer S.M., Wanke C.A. Physiological effects of HIV infection on human intestinal epithelial cells: An in vitro model for HIV enteropathy. AIDS. 1994;8:205. doi: 10.1097/00002030-199402000-00008. [DOI] [PubMed] [Google Scholar]
- 5.Balthazar E.J., Gordon R., Hulnick D. Ileocecal tuberculosis: CT and radiologic evaluation. AJR Am J Roentgenol. 1990;154:499. doi: 10.2214/ajr.154.3.2106212. [DOI] [PubMed] [Google Scholar]
- 6.Balthazar E.J., Stern J. Necrotizing Candida enterocolitis in AIDS: CT features. J Comput Assist Tomogr. 1994;18:298. doi: 10.1097/00004728-199403000-00026. [DOI] [PubMed] [Google Scholar]
- 7.Bartlett J.G., Belitsos P.C., Sears C.L. AIDS enteropathy. Clin Infect Dis. 1992;15:726. doi: 10.1093/clind/15.4.726. [DOI] [PubMed] [Google Scholar]
- 8.Bashir R.M., Wilcox C.M. Symptom-specific use of upper gastrointestinal endoscopy in human immunodeficiency virus-infected patients yields high dividends. J Clin Gastroenterol. 1996;23:292. doi: 10.1097/00004836-199612000-00011. [DOI] [PubMed] [Google Scholar]
- 9.Belitsos P.C., Greenson J.K., Yardley J.H. Association of gastric hypoacidity with opportunistic enteric infections in patients with AIDS. J Infect Dis. 1992;166:277. doi: 10.1093/infdis/166.2.277. [DOI] [PubMed] [Google Scholar]
- 10.Bertoli F., Espino M., Arosemena J.R. A spectrum in the pathology of toxoplasmosis in patients with acquired immunodeficiency syndrome. Arch Pathol Lab Med. 1995;119:214. [PubMed] [Google Scholar]
- 11.Blanshard C., Benhamou Y., Dohin E. Treatment of AIDS-associated gastrointestinal cytomegalovirus infection with foscarnet and ganciclovir: A randomized comparison. J Infect Dis. 1995;172:622. doi: 10.1093/infdis/172.3.622. [DOI] [PubMed] [Google Scholar]
- 12.Blanshard C., Gazzard B.G. Natural history and prognosis of diarrhea of unknown cause in patients with acquired immunodeficiency syndrome (AIDS) Gut. 1995;36:283. doi: 10.1136/gut.36.2.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Blanshard C., Jackson A.M., Shanson D.C. Cryptosporidiosis in HIV-seropositive patients. Q J Med. 1992;85:813. [PubMed] [Google Scholar]
- 14.Blanshard C., Shanson D.C., Gazzard B.G. Pilot studies of azithromycin, letrazuril and paromomycin in the treatment of cryptosporidiosis. Int J STD AIDS. 1997;8:124. doi: 10.1258/0956462971919543. [DOI] [PubMed] [Google Scholar]
- 15.Boulard F., Cnudde F., Teron-Aboud B. Digestive histoplasmosis in a patient with AIDS from Guadeloupe. Ann Gastroenterol Hepatol. 1994;30:97. [PubMed] [Google Scholar]
- 16.Brown J.W., Savides T.J., Mathews C. Diagnostic yield of duodenal biopsy and aspirate in AIDS-associated diarrhea. Am J Gastroenterol. 1996;91:2289. [PubMed] [Google Scholar]
- Budhraja M.D., Levendoglu H., Kocka F. Duodenal musocal T cell subpopulation and bacterial cultures in acquired immunodeficiency syndrome. Am J Gastroenterol. 1987;82:427. [PubMed] [Google Scholar]
- 17.Canning E.U., Hollister W.S. Enterocytozoon bieneusi (Microspora): prevalence and pathogenicity in AIDS patients. Trans R Soc Trop Med Hyg. 1990;84:181. doi: 10.1016/0035-9203(90)90247-c. [DOI] [PubMed] [Google Scholar]
- 18.Cappell M.S. Extensive gastrointestinal aspergillosis associated with AIDS. Dig Dis Sei. 1991;36:1500. doi: 10.1007/BF01296824. [letter] [DOI] [PubMed] [Google Scholar]
- 19.Cappell M.S., Philogene C. The endoscopic appearance of severe intestinal Mycobacterium avium complex infection as a coarsely granular mucosa due to massive infiltration and expansion of intestinal villi without mucosal exudation. J Clin Gastroenterol. 1995;21:323. doi: 10.1097/00004836-199512000-00017. [DOI] [PubMed] [Google Scholar]
- 20.Carlson S., Yokoo H., Craig R.M. Small intestinal HIV-associated enteropathy: Evidence for panintestinal enterocyte dysfunction. J Lab Clin Med. 1994;124:652. [PubMed] [Google Scholar]
- 21.Chalasani N., Wilcox C.M., Hunter H.T. Endoscopic features of gastroduodenal cryptococcosis in AIDS. Gastrointest Endosc. 1997;45:315. doi: 10.1016/s0016-5107(97)70280-3. [DOI] [PubMed] [Google Scholar]
- Chalasani N., Lazenby A.J., Wilcox C.M. Unusual endoscopic features of gastric and duodenal cryptosporidiosis in AIDS. Gastrointest Endosc. 1997;45:525. doi: 10.1016/s0016-5107(97)70188-3. [DOI] [PubMed] [Google Scholar]
- 22.Collier J.A., Brandt L.J. Gastrointestinal manifestations of fungal infections in the acquired immunodeficiency syndrome. Practical Gastroenterology. 1995;19:10. [Google Scholar]
- 23.Comin C.E., Santucci M. Submicroscopic profile of Isospora belli enteritis in a patient with acquired immune deficiency syndrome. Ultrastruct Pathol. 1994;18:473. doi: 10.3109/01913129409023222. [DOI] [PubMed] [Google Scholar]
- 24.Cotte L., Rabodonirina M., Piens M.A. Prevalence of intestinal protozoans in French patients infected with HIV. J Acquir Immune Defic Syndr Hum Retrovirol. 1993;6:1024. [PubMed] [Google Scholar]
- 25.Cowley G.P., Miller R.F., Papadaki L. Disseminated microsporidiosis in a patient with acquired immunodeficiency syndrome. Histopathology. 1997;30:386. doi: 10.1046/j.1365-2559.1997.5020758.x. [DOI] [PubMed] [Google Scholar]
- 26.Dancygier H. AIDS and gastrointestinal endoscopy. Endoscopy. 1994;26:175. doi: 10.1055/s-2007-1008943. [DOI] [PubMed] [Google Scholar]
- 27.DeHovitz J.A., Pape J.W., Boncy M. Clinical manifestations and therapy of Isospora belli infection in patients with the acquired immunodeficiency syndrome. N Engl J Med. 1986;315:87. doi: 10.1056/NEJM198607103150203. [DOI] [PubMed] [Google Scholar]
- 28.Dieterich D.T., Lew E.A., Kotier D.P. Treatment with albendazole for intestinal disease due to Enterocytozoon bieneusi in patients with AIDS. J Infect Dis. 1994;169:178. doi: 10.1093/infdis/169.1.178. [DOI] [PubMed] [Google Scholar]
- 29.Dionisio D., Di Lollo S., Manneschi L.I. Morphological injury of the intestinal mucosa and infection in patients with AIDS. Ital J Gastroenterol Hepatol. 1997;29:25. [PubMed] [Google Scholar]
- 30.Dumonceau J.-M. Endoscopic appearance of Mycobacterium genavense. Gastrointest Endosc. 1997;45:334. doi: 10.1016/s0016-5107(97)70289-x. [DOI] [PubMed] [Google Scholar]
- 31.Eeftinck Schattenkerk J.K., van Gool T., van Ketel R.J. Clinical significance of small-intestinal microsporidiosis in HIV-1-infected individuals. Lancet. 1991;337:895. doi: 10.1016/0140-6736(91)90215-b. [DOI] [PubMed] [Google Scholar]
- 32.Ehrenpreis E.D. Small intestinal manifestations of HIV infection. Int J STD AIDS. 1995;6:149. doi: 10.1177/095646249500600301. [DOI] [PubMed] [Google Scholar]
- 33.Elshazly M.A., Serwadda D.M., Freers J. Endoscopic study of African AIDS patients with upper gastrointestinal symptoms. East African Med J. 1994;71:496. [PubMed] [Google Scholar]
- 34.Field A.S., Hing M.C., Milliken S.T. Microsporidia in the small intestine of HIV-infected patients: A new diagnostic technique and a new species. Med J Aust. 1993;158:390. [PubMed] [Google Scholar]
- 35.Field A.S., Marriott D.J., Hing M.C. The Warthin-Starry stain in the diagnosis of small intestinal microsporidiosis in HIV-infected patients. Folia Parasitol (Praha) 1993;40:261. [PubMed] [Google Scholar]
- 36.Flanigan T., Whalen C., Turner J. Cryptosporidium infection and CD4 counts. Ann Intern Med. 1992;116:840. doi: 10.7326/0003-4819-116-10-840. [DOI] [PubMed] [Google Scholar]
- 37.Gail M.H., Plūda J.M., Rabkin C.S. Projections of the incidence of non-Hodgkin’s lymphoma related to acquired immunodeficiency syndrome. J Natl Cancer Inst. 1991;83:695. doi: 10.1093/jnci/83.10.695. [DOI] [PubMed] [Google Scholar]
- 38.Genta R.M., Chappell C.L., White A.C., Jr. Duodenal morphology and intensity of infection in AIDS-related intestinal cryptosporidiosis. Gastroenterology. 1993;105:1769. doi: 10.1016/0016-5085(93)91075-s. [DOI] [PubMed] [Google Scholar]
- 39.Giang T.T., Kotier D.P., Garro M.L. Tissue diagnosis of intestinal microsporidiosis using the chromotrope-2R modified trichrome stain. Arch Pathol Lab Med. 1993;117:1249. [PubMed] [Google Scholar]
- 40.Gillin J.S., Urmacher C., West R. Disseminated Mycobacterium avium-intracellulare infection in acquired immunodeficiency syndrome mimicking Whipple’s disease. Gastroenterology. 1983;85:1187. [PubMed] [Google Scholar]
- 41.Goodgame R.W. Gastrointestinal cytomegalovirus disease. Ann Intern Med. 1993;119:924. doi: 10.7326/0003-4819-119-9-199311010-00010. [DOI] [PubMed] [Google Scholar]
- 42.Goodgame R.W. Understanding intestinal spore-forming protozoa: Cryptosporidia, microsporidia, isospora and cyclospora. Ann Intern Med. 1996;124:429. doi: 10.7326/0003-4819-124-4-199602150-00008. [DOI] [PubMed] [Google Scholar]
- 43.Haque A.K., Schnadig V., Rubin S.A. Pathogenesis of human strongyloidiasis: Autopsy and quantitative parasitological analysis. Mod Pathol. 1994;7:276. [PubMed] [Google Scholar]
- 44.Heneghan S.J., Li J., Petrossian E. Intestinal perforation from gastrointestinal histoplasmosis in acquired immunodeficiency syndrome: Case report and review of the literature. Arch Surg. 1993;128:464. doi: 10.1001/archsurg.1993.01420160106018. [DOI] [PubMed] [Google Scholar]
- 45.Hewan-Lowe K., Furlong B., Sims M. Coinfection with Giardia lamblia and Enterocytozoon bieneusi in a patient with acquired immunodeficiency syndrome and chronic diarrhea. Arch Pathol Lab Med. 1997;121:417. [PubMed] [Google Scholar]
- 46.Holmberg S.D., Moorman A.C., Von Bargen J.C. Possible effectiveness of clarithromycin and rifabutin for cryptosporidiosis chemoprophylaxis in HIV disease. JAMA. 1998;279:384. doi: 10.1001/jama.279.5.384. [DOI] [PubMed] [Google Scholar]
- 47.Jablonowski H., Szelenyi H., Borchard F. Visceral leishmaniasis with gastrointestinal involvement in a 30-year-old HIV infected patient. Z Gastroenterol. 1994;32:405. [PubMed] [Google Scholar]
- 48.Jacobson M.A., Hopewell P.C., Yajko D.M. Natural history of disseminated Mycobacterium avium complex infection in AIDS. J Infect Dis. 1991;164:994. doi: 10.1093/infdis/164.5.994. [DOI] [PubMed] [Google Scholar]
- 49.Johanson J.F. Diagnosis and management of AIDS-related diarrhea. Can J Gastroenterol. 1996;10:461. doi: 10.1155/1996/739845. [DOI] [PubMed] [Google Scholar]
- 50.Kaljot K.T., Ling J.P., Gold J.W.M. Prevalence of acute enteric viral pathogens in acquired immunodeficiency syndrome patients with diarrhea. Gastroenterology. 1989;97:1031. doi: 10.1016/0016-5085(89)91516-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Kaplan L.D. AIDS-associated lymphomas. Aids Clin Rev. 1991;1991:181. [PubMed] [Google Scholar]
- 52.Koehler M., Chak A., Setrakian S. Endoscopic appearance of Mycobacterium genavense: Case report and review of the literature. Gastrointest Endosc. 1996;44:331. doi: 10.1016/s0016-5107(96)70174-8. [DOI] [PubMed] [Google Scholar]
- 53.Kotier D.P., Giang T.T., Garro M.L. Light microscopic diagnosis of microsporidiosis in patients with AIDS. Am J Gastroenterol. 1994;89:540. [PubMed] [Google Scholar]
- 54.Kotier D.P., Orenstein J.M. Prevalence of intestinal microsporidiosis in HTV-infected individuals referred for gastroenterological evaluation. Am J Gastroenterol. 1994;89:1998. [PubMed] [Google Scholar]
- 55.Laguna F., Garcia-Samaniego J., Soriano V. Gastrointestinal leishmaniasis in human immunodeficiency virus-infected patients: Report of five cases and review. Clin Infect Dis. 1994;19:48. doi: 10.1093/clinids/19.1.48. [DOI] [PubMed] [Google Scholar]
- 56.Levine A.M. AIDS-associated malignant lymphoma. Med Clin North Am. 1992;76:253. doi: 10.1016/s0025-7125(16)30379-0. [DOI] [PubMed] [Google Scholar]
- 57.Ma P., Soave R. Three-step stool examination for crytosporidiosis in 10 homosexual men with protracted watery diarrhea. J Infect Dis. 1983;147:824. doi: 10.1093/infdis/147.5.824. [DOI] [PubMed] [Google Scholar]
- 58.Martin J.N., Ganem D.E., Osmond D.H. Sexual transmission and the natural history of human herpesvirus 8 infection. N Engl J Med. 1998;338:948. doi: 10.1056/NEJM199804023381403. [DOI] [PubMed] [Google Scholar]
- 59.McBride M.O., Fisher M., Skinner C.J. An unusual gastrointestinal presentation of leishmaniasis. Scand Infect Dis. 1995;27:297. doi: 10.3109/00365549509019026. [DOI] [PubMed] [Google Scholar]
- 60.Nagy-Agren S.E., Chu P., Walker Smith G.J. Zygomycosis (Mucormycosis) and HIV infection: Report of three cases and review. J Acquir Immune Defici Syndr Hum Retrovirol. 1995;10:441. doi: 10.1097/00042560-199512000-00007. [DOI] [PubMed] [Google Scholar]
- 61.Nelson M.R., Shanson D.C., Hawkins D.A. Salmonella, Campylobacter and Shigella in HIV-seropositive patients. Aids. 1992;6:1495. doi: 10.1097/00002030-199212000-00012. [DOI] [PubMed] [Google Scholar]
- 62.Orenstein J.M., Chiang J., Steinberg W. Intestinal microsporidiosis as a cause of diarrhea in human immunodeficiency virus-infected patients: A report of 20 cases. Hum Pathol. 1990;21:475. doi: 10.1016/0046-8177(90)90003-n. [DOI] [PubMed] [Google Scholar]
- 63.Pape J.W., Verdier R.I., Boncy M. Cyclospora infection in adults infected with HIV: Clinical manifestations, treatment, and prophylaxis. Ann Intern Med. 1994;121:654. doi: 10.7326/0003-4819-121-9-199411010-00004. [DOI] [PubMed] [Google Scholar]
- 64.Papp J.P., DeYoung B.R., Fromkes J.J. Endoscopic appearance of cryptosporidial duodenitis. Am J Gastroenterol. 1996;91:2235. [PubMed] [Google Scholar]
- 65.Peacock C.S., Blanshard C., Tovey D.G. Histological diagnosis of intestinal microsporidiosis in patients with AIDS. J Clin Pathol. 1991;44:558. doi: 10.1136/jcp.44.7.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Petersen C. Cryptosporidiosis in patients infected with the human immunodeficiency virus. Clin Infect Dis. 1992;15:903. doi: 10.1093/clind/15.6.903. [DOI] [PubMed] [Google Scholar]
- 67.Poorman J.C., Katon R.M. Small bowel involvement by Mycobacterium avium complex in a patient with AIDS: Endoscopic, histologic, and radiographic similarities to Whipple’s disease. Gastrointest Endosc. 1994;40:753. [PubMed] [Google Scholar]
- 68.Rabeneck L., Gyorkey F., Genta R.M. The role of microsporidia in the pathogenesis of HIV-related chronic diarrhea. Ann Intern Med. 1993;119:895. doi: 10.7326/0003-4819-119-9-199311010-00005. [DOI] [PubMed] [Google Scholar]
- 69.Ritchie D.J., Becker E.S. Update on the management of intestinal cryptosporidiosis in AIDS. Ann Pharmacother. 1994;28:767. doi: 10.1177/106002809402800615. [DOI] [PubMed] [Google Scholar]
- 70.Rodgers V.D., Kagnoff M.F. Gastrointestinal manifestations of the acquired immunodeficiency syndrome. West J Med. 1987;146:57. [PMC free article] [PubMed] [Google Scholar]
- 71.Rosenblatt J.E., Sloan L.M. Evaluation of an enzyme-linked immunosorbent assay for detection of Cryptosporidium spp. in stool specimens. J Clin Microbiol. 1993;31:1468. doi: 10.1128/jcm.31.6.1468-1471.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.Schmidt W., Schneider T., Heise W. Mucosal abnormalities in microsporidiosis. AIDS. 1997;11:1589. doi: 10.1097/00002030-199713000-00007. [DOI] [PubMed] [Google Scholar]
- 73.Schmidt W., Schneider T., Heise W. Stool viruses, coinfections, and diarrhea in HIV-infected patients. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;13:33. doi: 10.1097/00042560-199609000-00006. [DOI] [PubMed] [Google Scholar]
- 74.Sobottka I., Schwartz D.A., Schottelius J. 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. 1998;26:475. doi: 10.1086/516328. [DOI] [PubMed] [Google Scholar]
- 75.Soule J.B., Halverson A.L., Becker R.B. A patient with acquired immunodeficiency syndrome and untreated Encephalitozoon (Septata) intestinalis microsporidiosis leading to small bowel perforation. Response to albendazole. Arch Pathol Lab Med. 1997;121:880. [PubMed] [Google Scholar]
- 76.Sun T., Ilardi C.F., Asnis D. Light and electron microscopic identification of Cyclospora species in the small intestine: Evidence of the presence of asexual life cycle in human host. Am J Clin Pathol. 1996;105:216. doi: 10.1093/ajcp/105.2.216. [DOI] [PubMed] [Google Scholar]
- 77.Ullrich R., Zeitz M., Heise W. Small intestinal structure and function in patients infected with human immunodeficiency virus (HIV): Evidence for HIV-induced enteropathy. Ann Intern Med. 1989;111:15. doi: 10.7326/0003-4819-111-1-15. [DOI] [PubMed] [Google Scholar]
- 78.Wanke C.A., 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. doi: 10.1093/clinids/23.4.816. [DOI] [PubMed] [Google Scholar]
- 79.Wilcox C.M., Schwartz D.A., Cotsonis G. Chronic unexplained diarrhea in human immunodeficiency virus infection: Determination of the best diagnostic approach. Gastroenterology. 1996;110:30. doi: 10.1053/gast.1996.v110.pm8536874. [DOI] [PubMed] [Google Scholar]
- 80.Ziegler J.L., Beckstead J.A., Volberding P.A. Non-Hodgkin’s lymphoma in 90 homosexual men: Relation to generalized lymphadenopathy and the acquired immunodeficiency syndrome. N Engl J Med. 1984;311:565. doi: 10.1056/NEJM198408303110904. [DOI] [PubMed] [Google Scholar]