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Intestinal Amebiasis: A Diagnosis not to be Missed
PATHOLOGY
Teaching Case
RESEARCH AND PRACTICE © Urban & Fischer Verlag http://www.urbanfischer.de/journals/prp
Intestinal Amebiasis: A Diagnosis not to be Missed Victoria A. Marcus1, Brian J. Ward2 and Philippe Jutras3 1
Departments of Pathology and 2Tropical Medicine, McGill University Health Centre, Montreal General Hospital, Montreal, Canada; 3Department of Microbiology, Rimouski Regional Hospital, Rimouski, Canada
Summary Entamoeba histolytica is a well-recognized cause of infectious colitis and disseminated amebic abscesses. Most prevalent in the tropics and subtropics, E. histolytica infections may also occur in the developed world. We describe a case of a North American traveler with intestinal amebiasis, a diagnosis first made by colonic biopsy. We review the available diagnostic tools and the role of the surgical pathologist in the detection of this infection. Key words: Entamoeba histolytica – Amebiasis – Colonoscopy
Introduction Entamoeba histolytica is a well-known cause of infectious colitis, typically producing diarrhea and occasionally frank dysentery. This organism may also spread to involve extraintestinal sites such as the liver, lung, central nervous system, and other organs, usually in the form of amebic abscesses [1, 5, 6]. E. histolytica has a worldwide distribution, but is most prevalent in the developing world, with broad regions of elevated risk in the tropics and subtropics. E. histolytica infections are also seen with regularity in the developed world, most commonly in immigrants, travelers, refugees, aboriginals, residents of penal and mental institutions, and in male homosexuals [1, 5, 6]. We report a case of a North American traveler with chronic abdominal pain who was first diagnosed with Pathol. Res. Pract. 197: 271–274 (2001)
intestinal amebiasis by colonic biopsy. We discuss the available diagnostic tools and the role of the surgical pathologist in the detection of this infection.
Case History The patient was a 41-year-old French-Canadian male who presented with a 5-month history of waxing and waning abdominal complaints, beginning during a 3month family vacation in Mexico. His principal complaint was intermittent abdominal cramping with occasional loose stools. He denied any episodes of fever, hematochezia, mucous, or profuse diarrhea. A slight worsening of his chronic symptoms prompted him to seek medical advice. At that time, stool examinations for ova and parasites were negative and no biochemical or hematologic abnormality was noted. His personal and family histories were negative for gastrointestinal diseases and he had no other relevant medical history. Gastroscopy was normal, but a full-length colonoscopy revealed multiple ulcers in the cecum with involvement of the terminal ileum. A working diagnosis of Crohn’s disease was made. However, before steroids were initiated, histopathologic examination revealed many amebic trophozoites in the cecal ulcers (pathology described below). The patient was treated with metronidazole
Address for correspondence: Victoria A. Marcus, Montreal General Hospital, 1650 Cedar Ave, Montreal, Quebec, Canada H3G 1A4. Phone: ++1(514) 937-6011, ext. 3860, Fax: ++1(514) 934-8296. E-mail: [email protected] 0344-0338/01/197/4-271 $15.00/0
272 · V. A. Marcus et al.
(750 mg t.i.d. for 10 days) and diodoquinol (650 mg b.i.d. for 20 days) with good response. However, within one month of completing diodoquinol therapy, his symptoms returned. Two repeat stool examinations for ova and parasites were still negative. A repeat colonoscopy demonstrated ulcers in the cecum and the presence of amebae was confirmed by histopathology. Serology, carried out at this time, was positive for anti-amebic antibodies. A second course of metronidazole and diodoquinol resulted in the resolution of his symptoms. Two subsequent colonoscopies with biopsy were normal, and he remains asymptomatic after 1.5 years of follow-up.
(Fig. 1). These trophozoites were round to oval in shape and were the size of large histiocytes. The organisms contained single, small round nuclei and had eosinophilic vacuolated cytoplasm that was periodic acid-Schiff (PAS) positive, diastase sensitive. The cytoplasm also contained characteristic phagocytosed red blood cells. At the time of the second colonoscopy, endoscopic biopsies were obtained only from the cecum. They showed less inflammation and no significant architectural abnormality, but ulceration and obvious amebae were still present.
Discussion Pathology At the time of the first colonoscopy, endoscopic biopsies were taken from the terminal ileum and the cecum. The ileal biopsies showed only patchy neutrophilic infiltration of the surface epithelium, as well as an overlying fibrinopurulent exudate. There was no evidence of an ulcer bed and no amebic organisms were found in the terminal ileum. The cecum showed mild architectural changes, with focal crypt branching and deep lymphoplasmacytic inflammation. There was patchy acute cryptitis and the lamina propria contained a moderate amount of chronic inflammation. In addition, ulceration was identified, consisting of active granulation tissue with a denuded surface epithelium and overlying necrotic fibrinopurulent material. Numerous typical amebic trophozoites were noted within the exudate
Amebiasis is a major cause of morbidity by parasites worldwide. It is the third most common parasitic cause of death after malaria and schistosomiasis [12]. While endemic in large regions of the tropics, amebiasis also occurs sporadically in the temperate climates of developed countries. Transmission of E. histolytica is by the fecal-oral route. Infection is typically acquired from ingestion of food or water contaminated by amebic cysts. Upon ingestion, cysts release vegetative motile trophozoites in the ileocecal valve region, which then multiply by binary fission. Symptoms occur only when the trophozoites invade the intestinal mucosa. The life cycle of E. histolytica is complete when trophozoites encyst and these infectious cysts are excreted in the feces. There is no intermediate animal host [1, 5, 6].
Fig. 1. Typical Entamoeba histolytica trophozoites found in fibrinopurulent exudate above ulceration. Note the pathgnomonic red blood cells within the cytoplasm (H&E, original magnification ×400).
Intestinal Amebiasis · 273
The clinical consequences of E. histolytica are highly variable. Some individuals appear to be colonized without obvious ill effects, while others present with a wide range of acute or chronic symptoms. Acute presentations include moderate diarrhea, frank dysentery and, rarely, fulminant toxic megacolon. Subacute or chronic presentations are also quite common and may be endoscopically indistinguishable from other forms of colitis, including idiopathic inflammatory bowel disease, ischemic colitis, pseudomembranous colitis, or other types of infectious colitis [1, 11, 13]. Rarely, a mass of granulation tissue caused by localized amebic infection (an “ameboma”) may be the presenting lesion and may be confused with malignancy. Amebic strictures can also occur, usually forming around the anus and the rectosigmoid [1, 5]. Pathologic examination of colonic biopsies may be vital in the diagnosis of intestinal amebiasis [7, 9, 10]. Early infection may show only non-specific neutrophilic infiltration and erosions of the intestinal mucosa. In more advanced cases, the classic picture of undermined, flask-shaped ulcers up to 3 cm in diameter may be seen in the cecum or ascending colon and, less commonly, in the rectosigmoid, terminal ileum, and elsewhere in the colon. Between ulcers, the intestinal mucosa may have only minor alterations or may show acute cryptitis or crypt abscesses. Diagnostic trophozoites are usually detected in the necrotic debris above the ulcers. Trophozoites typically measure ~25 µm in diameter and contain a single, round nucleus (~5 µm), as well as vacuolated PAS-positive cytoplasm. The presence of ingested red blood cells is considered to be pathognomonic for E. histolytica [1, 5, 6]. The diagnosis of dysenteric amebiasis is often relatively straightforward in the developed world. Most patients have a recent history of travel to an endemic area or have a known risk factor for infection, such as residence in institutions for the mentally handicapped, residence in aboriginal communities, or male homosexuals [1, 5, 6]. Characteristic trophozoites can often be seen by wet mount or by stained stool preparations made from the dysenteric stools. However, the diagnosis of the less common manifestations of amebiasis (e.g., amebic abscess, ameboma, or chronic colitis) is more complicated, and a high degree of suspicion must be maintained. A “routine” stool examination will often be negative in these patients due to the intermittent nature of cyst passage and the usual absence of trophozoites. Although repeated stool sampling and permanent stains can increase the yield by at least 10–15% [14], the precise number of specimens and their optimal handling remain controversial [4]. Microscopic diagnosis is further complicated by the recent recognition that cysts from the closely related and non-pathogenic species, Entamoeba dispar, are morphologically indistinguishable from E. histolytica cysts [2]. Since stool mi-
croscopy has often been used as a “gold standard” assay, this recent discovery has made suspect many of the sensitivity estimates for amebic diagnostic testing reported in the literature to date. Although zymodeme analysis and antigen detection assays can distinguish between these two species [2], the former is technically complex and the latter works poorly at low parasite densities (JD MacLean – personal communication). However, unlike E. dispar, trophozoites of E. histolytica may contain ingested red blood cells in their cytoplasm. A variety of serological assays for E. histolytica have also been described (e.g., indirect hemagglutination assay, ELISA) [8]. Serological detection of antibodies to amebae appears to be highly sensitive for patients with amebic liver abscesses, but is considerably less sensitive for those with disease limited to the colon (~90% sensitivity versus ~70% sensitivity) [6]. Furthermore, anti-amebic antibodies are typically detectable only 2–4 weeks after infection and can persist for years, leading to potential confusion between recent and past exposures [6, 8]. E. histolytica can also be cultured and nucleic acid-based tests (e.g., PCR) have been described[2]. However, these tests remain primarily as research tools and are only carried out in highly specialized laboratories. Although Entamoeba histolytica is a relatively uncommon intestinal protozoan in the developed world, in recent stool surveys, it is consistently among the most common intestinal parasite with major pathologic potential in North America [6]. Increasing numbers of North Americans either originate from or travel to areas of the world endemic for E. histolytica. Furthermore, recent outbreaks of Cyclospora cayetanensis imported to North America on berries clearly demonstrate that ‘traveling food’ has become another important risk factor for socalled ‘tropical’ parasitoses [3]. E. histolytica should be included in the differential diagnosis of patients with ordinary as well as unusual gastrointestinal presentations. It is crucial to differentiate amebic colitis from the more common causes of colitis. Great care must be exercised in the application and interpretation of the currently available diagnostic tests. As is demonstrated by this case, the alert surgical pathologist has the potential to be the first to suspect and establish the diagnosis. Acknowledgement: We are grateful to Drs. Marcel Bélanger, Georges Touma, Valère Allard, Réal Lagacé, and Claude Delage, who were involved in the patient’s care. In addition, we thank Matthew Litwiller and Robert Derval for their expert technical support.
References 1. Fenoglio-Preiser CM, Noffinsinger AE, Stemmermann GN, Lantz PE, Listrom MB, Rilke FO (1999) Nonneo-
274 · V. A. Marcus et al. plastic lesions of the colon. In: Fenoglio-Preiser CM, Noffinsinger AE, Stemmermann GN, Lantz PE, Listrom MB, Rilke FO (Eds) Gastrointestinal Pathology: an Atlas and Text, 2nd ed., pp 845–849. Lippincott-Raven Publishers, Philadelphia 2. Haque R, Ali IK, Akther S, Petri WA, Jr. (1998) Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of Entamoeba histolytica infection. J Clin Microbiol 36: 449–52 3. Herwaldt BL, Beach MJ (1999) The return of Cyclospora in 1997: another outbreak of cyclosporiasis in North America associated with imported raspberries. Cyclospora Working Group. Ann Intern Med 130: 210–20 4. Hiatt RA, Markell EK, Ng E (1995) How many stool examinations are necessary to detect pathogenic intestinal protozoa? Am J Trop Med Hyg 53: 36–9 5. Li E, Stanley SL, Jr. (1996) Protozoa. Amebiasis. Gastroenterol Clin North Am 25: 471–92 6. Petri WA, Jr., Singh U (1999) Diagnosis and management of amebiasis. Clin Infect Dis 29: 1117–25 7. Pittman FE, Hennigar GR (1974) Sigmoidoscopic and colonic mucosal biopsy findings in amebic colitis. Arch Pathol 97: 155–8 8. Proctor EM (1991) Laboratory diagnosis of amebiasis. Clin Lab Med 11: 829–59
9. Radhakrishnan S, Al Nakib B, Shaikh H, Menon NK (1986) The value of colonoscopy in schistosomal, tuberculous, and amebic colitis. Two-year experience. Dis Colon Rectum 29: 891–5 10. Rozen P, Baratz M, Rattan J (1981) Rectal bleeding due to amebic colitis diagnosed by multiple endoscopic biopsies: report of two cases. Dis Colon Rectum 24: 127–9 11. Tedesco FJ, Hardin RD, Harper RN, Edwards BH (1983) Infectious colitis endoscopically simulating inflammatory bowel disease: a prospective evaluation. Gastrointest Endosc 29: 195–7 12. Walsh JA (1986) Problems in recognition and diagnosis of amebiasis: estimation of the global magnitude of morbidity and mortality. Rev Infect Dis 8: 228–38 13. Wolloch Y, Chaimoff C, Zer M, Dintsman M (1973) Pitfalls in the diagnosis of amebic colitis. Dis Colon Rectum 16: 42–5 14. Yang J, Scholten T (1977) A fixative for intestinal parasites permitting the use of concentration and permanent staining procedures. Am J Clin Pathol 67: 300–4
Received: June 28, 2000 Accepted in revised version: January 20, 2001
Teaching Case
RESEARCH AND PRACTICE © Urban & Fischer Verlag http://www.urbanfischer.de/journals/prp
Intestinal Amebiasis: A Diagnosis not to be Missed Victoria A. Marcus1, Brian J. Ward2 and Philippe Jutras3 1
Departments of Pathology and 2Tropical Medicine, McGill University Health Centre, Montreal General Hospital, Montreal, Canada; 3Department of Microbiology, Rimouski Regional Hospital, Rimouski, Canada
Summary Entamoeba histolytica is a well-recognized cause of infectious colitis and disseminated amebic abscesses. Most prevalent in the tropics and subtropics, E. histolytica infections may also occur in the developed world. We describe a case of a North American traveler with intestinal amebiasis, a diagnosis first made by colonic biopsy. We review the available diagnostic tools and the role of the surgical pathologist in the detection of this infection. Key words: Entamoeba histolytica – Amebiasis – Colonoscopy
Introduction Entamoeba histolytica is a well-known cause of infectious colitis, typically producing diarrhea and occasionally frank dysentery. This organism may also spread to involve extraintestinal sites such as the liver, lung, central nervous system, and other organs, usually in the form of amebic abscesses [1, 5, 6]. E. histolytica has a worldwide distribution, but is most prevalent in the developing world, with broad regions of elevated risk in the tropics and subtropics. E. histolytica infections are also seen with regularity in the developed world, most commonly in immigrants, travelers, refugees, aboriginals, residents of penal and mental institutions, and in male homosexuals [1, 5, 6]. We report a case of a North American traveler with chronic abdominal pain who was first diagnosed with Pathol. Res. Pract. 197: 271–274 (2001)
intestinal amebiasis by colonic biopsy. We discuss the available diagnostic tools and the role of the surgical pathologist in the detection of this infection.
Case History The patient was a 41-year-old French-Canadian male who presented with a 5-month history of waxing and waning abdominal complaints, beginning during a 3month family vacation in Mexico. His principal complaint was intermittent abdominal cramping with occasional loose stools. He denied any episodes of fever, hematochezia, mucous, or profuse diarrhea. A slight worsening of his chronic symptoms prompted him to seek medical advice. At that time, stool examinations for ova and parasites were negative and no biochemical or hematologic abnormality was noted. His personal and family histories were negative for gastrointestinal diseases and he had no other relevant medical history. Gastroscopy was normal, but a full-length colonoscopy revealed multiple ulcers in the cecum with involvement of the terminal ileum. A working diagnosis of Crohn’s disease was made. However, before steroids were initiated, histopathologic examination revealed many amebic trophozoites in the cecal ulcers (pathology described below). The patient was treated with metronidazole
Address for correspondence: Victoria A. Marcus, Montreal General Hospital, 1650 Cedar Ave, Montreal, Quebec, Canada H3G 1A4. Phone: ++1(514) 937-6011, ext. 3860, Fax: ++1(514) 934-8296. E-mail: [email protected] 0344-0338/01/197/4-271 $15.00/0
272 · V. A. Marcus et al.
(750 mg t.i.d. for 10 days) and diodoquinol (650 mg b.i.d. for 20 days) with good response. However, within one month of completing diodoquinol therapy, his symptoms returned. Two repeat stool examinations for ova and parasites were still negative. A repeat colonoscopy demonstrated ulcers in the cecum and the presence of amebae was confirmed by histopathology. Serology, carried out at this time, was positive for anti-amebic antibodies. A second course of metronidazole and diodoquinol resulted in the resolution of his symptoms. Two subsequent colonoscopies with biopsy were normal, and he remains asymptomatic after 1.5 years of follow-up.
(Fig. 1). These trophozoites were round to oval in shape and were the size of large histiocytes. The organisms contained single, small round nuclei and had eosinophilic vacuolated cytoplasm that was periodic acid-Schiff (PAS) positive, diastase sensitive. The cytoplasm also contained characteristic phagocytosed red blood cells. At the time of the second colonoscopy, endoscopic biopsies were obtained only from the cecum. They showed less inflammation and no significant architectural abnormality, but ulceration and obvious amebae were still present.
Discussion Pathology At the time of the first colonoscopy, endoscopic biopsies were taken from the terminal ileum and the cecum. The ileal biopsies showed only patchy neutrophilic infiltration of the surface epithelium, as well as an overlying fibrinopurulent exudate. There was no evidence of an ulcer bed and no amebic organisms were found in the terminal ileum. The cecum showed mild architectural changes, with focal crypt branching and deep lymphoplasmacytic inflammation. There was patchy acute cryptitis and the lamina propria contained a moderate amount of chronic inflammation. In addition, ulceration was identified, consisting of active granulation tissue with a denuded surface epithelium and overlying necrotic fibrinopurulent material. Numerous typical amebic trophozoites were noted within the exudate
Amebiasis is a major cause of morbidity by parasites worldwide. It is the third most common parasitic cause of death after malaria and schistosomiasis [12]. While endemic in large regions of the tropics, amebiasis also occurs sporadically in the temperate climates of developed countries. Transmission of E. histolytica is by the fecal-oral route. Infection is typically acquired from ingestion of food or water contaminated by amebic cysts. Upon ingestion, cysts release vegetative motile trophozoites in the ileocecal valve region, which then multiply by binary fission. Symptoms occur only when the trophozoites invade the intestinal mucosa. The life cycle of E. histolytica is complete when trophozoites encyst and these infectious cysts are excreted in the feces. There is no intermediate animal host [1, 5, 6].
Fig. 1. Typical Entamoeba histolytica trophozoites found in fibrinopurulent exudate above ulceration. Note the pathgnomonic red blood cells within the cytoplasm (H&E, original magnification ×400).
Intestinal Amebiasis · 273
The clinical consequences of E. histolytica are highly variable. Some individuals appear to be colonized without obvious ill effects, while others present with a wide range of acute or chronic symptoms. Acute presentations include moderate diarrhea, frank dysentery and, rarely, fulminant toxic megacolon. Subacute or chronic presentations are also quite common and may be endoscopically indistinguishable from other forms of colitis, including idiopathic inflammatory bowel disease, ischemic colitis, pseudomembranous colitis, or other types of infectious colitis [1, 11, 13]. Rarely, a mass of granulation tissue caused by localized amebic infection (an “ameboma”) may be the presenting lesion and may be confused with malignancy. Amebic strictures can also occur, usually forming around the anus and the rectosigmoid [1, 5]. Pathologic examination of colonic biopsies may be vital in the diagnosis of intestinal amebiasis [7, 9, 10]. Early infection may show only non-specific neutrophilic infiltration and erosions of the intestinal mucosa. In more advanced cases, the classic picture of undermined, flask-shaped ulcers up to 3 cm in diameter may be seen in the cecum or ascending colon and, less commonly, in the rectosigmoid, terminal ileum, and elsewhere in the colon. Between ulcers, the intestinal mucosa may have only minor alterations or may show acute cryptitis or crypt abscesses. Diagnostic trophozoites are usually detected in the necrotic debris above the ulcers. Trophozoites typically measure ~25 µm in diameter and contain a single, round nucleus (~5 µm), as well as vacuolated PAS-positive cytoplasm. The presence of ingested red blood cells is considered to be pathognomonic for E. histolytica [1, 5, 6]. The diagnosis of dysenteric amebiasis is often relatively straightforward in the developed world. Most patients have a recent history of travel to an endemic area or have a known risk factor for infection, such as residence in institutions for the mentally handicapped, residence in aboriginal communities, or male homosexuals [1, 5, 6]. Characteristic trophozoites can often be seen by wet mount or by stained stool preparations made from the dysenteric stools. However, the diagnosis of the less common manifestations of amebiasis (e.g., amebic abscess, ameboma, or chronic colitis) is more complicated, and a high degree of suspicion must be maintained. A “routine” stool examination will often be negative in these patients due to the intermittent nature of cyst passage and the usual absence of trophozoites. Although repeated stool sampling and permanent stains can increase the yield by at least 10–15% [14], the precise number of specimens and their optimal handling remain controversial [4]. Microscopic diagnosis is further complicated by the recent recognition that cysts from the closely related and non-pathogenic species, Entamoeba dispar, are morphologically indistinguishable from E. histolytica cysts [2]. Since stool mi-
croscopy has often been used as a “gold standard” assay, this recent discovery has made suspect many of the sensitivity estimates for amebic diagnostic testing reported in the literature to date. Although zymodeme analysis and antigen detection assays can distinguish between these two species [2], the former is technically complex and the latter works poorly at low parasite densities (JD MacLean – personal communication). However, unlike E. dispar, trophozoites of E. histolytica may contain ingested red blood cells in their cytoplasm. A variety of serological assays for E. histolytica have also been described (e.g., indirect hemagglutination assay, ELISA) [8]. Serological detection of antibodies to amebae appears to be highly sensitive for patients with amebic liver abscesses, but is considerably less sensitive for those with disease limited to the colon (~90% sensitivity versus ~70% sensitivity) [6]. Furthermore, anti-amebic antibodies are typically detectable only 2–4 weeks after infection and can persist for years, leading to potential confusion between recent and past exposures [6, 8]. E. histolytica can also be cultured and nucleic acid-based tests (e.g., PCR) have been described[2]. However, these tests remain primarily as research tools and are only carried out in highly specialized laboratories. Although Entamoeba histolytica is a relatively uncommon intestinal protozoan in the developed world, in recent stool surveys, it is consistently among the most common intestinal parasite with major pathologic potential in North America [6]. Increasing numbers of North Americans either originate from or travel to areas of the world endemic for E. histolytica. Furthermore, recent outbreaks of Cyclospora cayetanensis imported to North America on berries clearly demonstrate that ‘traveling food’ has become another important risk factor for socalled ‘tropical’ parasitoses [3]. E. histolytica should be included in the differential diagnosis of patients with ordinary as well as unusual gastrointestinal presentations. It is crucial to differentiate amebic colitis from the more common causes of colitis. Great care must be exercised in the application and interpretation of the currently available diagnostic tests. As is demonstrated by this case, the alert surgical pathologist has the potential to be the first to suspect and establish the diagnosis. Acknowledgement: We are grateful to Drs. Marcel Bélanger, Georges Touma, Valère Allard, Réal Lagacé, and Claude Delage, who were involved in the patient’s care. In addition, we thank Matthew Litwiller and Robert Derval for their expert technical support.
References 1. Fenoglio-Preiser CM, Noffinsinger AE, Stemmermann GN, Lantz PE, Listrom MB, Rilke FO (1999) Nonneo-
274 · V. A. Marcus et al. plastic lesions of the colon. In: Fenoglio-Preiser CM, Noffinsinger AE, Stemmermann GN, Lantz PE, Listrom MB, Rilke FO (Eds) Gastrointestinal Pathology: an Atlas and Text, 2nd ed., pp 845–849. Lippincott-Raven Publishers, Philadelphia 2. Haque R, Ali IK, Akther S, Petri WA, Jr. (1998) Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of Entamoeba histolytica infection. J Clin Microbiol 36: 449–52 3. Herwaldt BL, Beach MJ (1999) The return of Cyclospora in 1997: another outbreak of cyclosporiasis in North America associated with imported raspberries. Cyclospora Working Group. Ann Intern Med 130: 210–20 4. Hiatt RA, Markell EK, Ng E (1995) How many stool examinations are necessary to detect pathogenic intestinal protozoa? Am J Trop Med Hyg 53: 36–9 5. Li E, Stanley SL, Jr. (1996) Protozoa. Amebiasis. Gastroenterol Clin North Am 25: 471–92 6. Petri WA, Jr., Singh U (1999) Diagnosis and management of amebiasis. Clin Infect Dis 29: 1117–25 7. Pittman FE, Hennigar GR (1974) Sigmoidoscopic and colonic mucosal biopsy findings in amebic colitis. Arch Pathol 97: 155–8 8. Proctor EM (1991) Laboratory diagnosis of amebiasis. Clin Lab Med 11: 829–59
9. Radhakrishnan S, Al Nakib B, Shaikh H, Menon NK (1986) The value of colonoscopy in schistosomal, tuberculous, and amebic colitis. Two-year experience. Dis Colon Rectum 29: 891–5 10. Rozen P, Baratz M, Rattan J (1981) Rectal bleeding due to amebic colitis diagnosed by multiple endoscopic biopsies: report of two cases. Dis Colon Rectum 24: 127–9 11. Tedesco FJ, Hardin RD, Harper RN, Edwards BH (1983) Infectious colitis endoscopically simulating inflammatory bowel disease: a prospective evaluation. Gastrointest Endosc 29: 195–7 12. Walsh JA (1986) Problems in recognition and diagnosis of amebiasis: estimation of the global magnitude of morbidity and mortality. Rev Infect Dis 8: 228–38 13. Wolloch Y, Chaimoff C, Zer M, Dintsman M (1973) Pitfalls in the diagnosis of amebic colitis. Dis Colon Rectum 16: 42–5 14. Yang J, Scholten T (1977) A fixative for intestinal parasites permitting the use of concentration and permanent staining procedures. Am J Clin Pathol 67: 300–4
Received: June 28, 2000 Accepted in revised version: January 20, 2001