Human Intestinal Spirochaetosis in Two Ulcerative Colitis Patients
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1 CSE REPORT Human Intestinal Spirochaetosis in Two Ulcerative Colitis Patients Junichi Iwamoto 1,ShoOgata 2, kira Honda 1, Yoshifumi Saito 1, Masashi Murakami 1, Tadashi Ikegami 1, Yoshikazu dachi 3 and Yasushi Matsuzaki 1 bstract histological examination of colonic biopsies of the longitudinal and irregularly-shaped ulcerative lesions of a 37-year-old man and 61-year-old man with ulcerative colitis showed so-called fringe formation, a typical finding of rachyspira infection. The antibody titer to rachyspira aalborgi showed marked elevation in both cases, and the patients were each treated with 1,000 mg of metronidazole for 14 days. Colonoscopy performed after treatment showed an improvement in the ulcerative lesions in both patients. These results indicate the possibility that intestinal spirochaetosis infection should be considered as an infectious complication in patients with ulcerative colitis receiving long-term steroid therapy. Key words: human intestinal spirochaetosis, rachyspira aalborgi and rachyspira pilosicoli, ulcerative colitis, metronidazole (Intern Med 53: , 2014) () Introduction Human intestinal spirochaetosis (HIS) was first reported by Harland and Lee in 1967 (1). HIS is a disease of the colorectum caused by the Gram-negative bacteria rachyspira aalborgi and rachyspira pilosicoli (2).. pilosicoli causes disease in humans and in various animals, whereas. aalborgi induces colonic spirochaetosis in humans only (3, 4). The definitive diagnosis of HIS requires the use of polymerase chain reaction, electron microscopy (5), imprint cytology (6) and detection of serum antibody titers to rachyspira aalborgi and rachyspira pilosicoli with agglutination titers (7). Human colonic spirochaetosis is common in developing countries, although it is relatively rare in industrialized countries, with high rates in homosexuals and HIV-infected individuals (2, 3, 8). previous study demonstrated that HIS is associated with various intestinal diseases, including colon carcinoma and colonic polyps (9, 10). Previous reports (9, 10) have also shown that HIS can be found in cases of ulcerative colitis. However, the detailed clinical features of HIS infection in ulcerative colitis patients are unclear. We herein report two cases of HIS infection in patients with ulcerative colitis who showed clinical improvements following metronidazole treatment. Case 1 Case Reports Case 1 involved a 37-year-old man with a 12-year history of pan-ulcerative (total) colitis. He experienced diarrhea two or three times per day, sometimes with bloody stools. On admission, his body temperature was 36.6, and his pulse rate was 70 beats/min. Laboratory studies showed a hemoglobin concentration of 14.7 g/dl and an erythrocyte sedimentation rate of 13 mm/h. Colonoscopy showed mild erosive mucosa in both the sigmoid colon and rectum as well as a longitudinal ulcerative lesion in the transverse colon (Fig. 1). The patient was treated with mesalazine at a dose of 2,250 mg/day and prednisolone at a dose of 5 to 10 mg/ day. His disease was responsive to therapy with predniso- Department of Gastroenterology, Tokyo Medical University Ibaraki Medical Center, Japan, Department of Pathology, National Defense Medical College, Japan and nimal Health Laboratory, School of griculture, Ibaraki University, Japan Received for publication December 26, 2013; ccepted for publication March 11, 2014 Correspondence to Dr. Junichi Iwamoto, junnki@dg.mbn.or.jp 2067
2 C Figure 1. Colonoscopy shows mild erosive mucosa in the sigmoid colon () and rectum () with an ulcerative lesion in the transverse colon (C). Figure 2. Histology of the colonic biopsy specimens revealed fringe formation reflecting collection of spirochetes on the luminal side of the colonic surface epithelium. Slightly edematous findings were seen in the background mucosa (Hematoxylin and Eosin staining) (, ). Table 1. ntibody Titers to rachyspira aalborgi and rachyspira pilosicoli in Case 1 Table 2. ntibody Titers to rachyspira aalborgi and rachyspira pilosicoli in Case 2. aalborgi (NCTC11492) Case1 Healthy control 616±33. aalborgi (NCTC11492) Case2 Healthy control 616±33. aalborgi (24-C) N.T.. aalborgi (24-C) N.T.. pilosicoli (TCC51139) ±12. pilosicoli (TCC51139) ±12 N.T.: not tested N.T.: not tested lone; however it was difficult to taper the dose of prednisolone. stool examination for conventional enteric pathogens was negative, and both cytomegalovirus antigenemia and clostridium difficile tests were negative. lthough antibody testing for amebic infection was not conducted, no endoscopic or histopathologic findings of such infections were observed. histological examination of the colonic biopsy samples of the edematous and erosive mucosa showed socalled fringe formation (Fig. 2). The agglutination titers were compared between the human serum and strains of rachyspira aalborgi and rachyspira pilosicoli. The antibody titer to rachyspira aalborgi was 616±33: 6,400, and the titer to rachyspira pilosicoli was 189±12: 400 (Table 1). diagnosis of HIS was therefore made, and the patient was treated with 1,000 mg of metronidazole for 14 days. Colonoscopy performed after the completion of treatment with metronidazole showed an improvement in the edematous mucosa of the ulcerative lesion in the transverse colon (Fig. 3), and a histological examination of colonic biopsy samples did not show any fringe formation. Furthermore, the patient s diarrhea appeared to be reduced at follow-up several weeks after treatment. Case 2 Case 2 involved a 61-year-old man with a 20-year history of distal ulcerative colitis. He experienced diarrhea four or five times a day, sometimes with bloody stools. His body temperature was 36.2, and his pulse rate was 63 beats/ 2068
3 Figure 3. Colonoscopy performed after treatment with metronidazole showed improvements in the edematous mucosa in the rectum and the ulcerative lesion in the transverse colon. Figure 4. Colonoscopy showed an irregular-shaped ulcerative lesion in the rectum (, ). min. Laboratory studies showed a hemoglobin concentration of 13.7 g/dl and an erythrocyte sedimentation rate of 15 mm/h. Colonoscopy showed an irregularly-shaped ulcerative lesion in the rectum (Fig. 4). The patient had an allergy to mesalazine, including the suppository form. He had been treated with prednisolone at a dose of 2.5 mg/day with a prednisolone (PSL) suppository. His disease was responsive to therapy with prednisolone; however, the ulcerative rectal lesion did not improve. stool examination for conventional enteric pathogens was negative, as was a cytomegalovirus antigenemia test. lthough antibody testing for amebic infection was not conducted, no endoscopic or histopathologic findings of such infections were observed. histological examination of the rectal biopsy samples obtained from the ulcerative mucosa showed so-called fringe formation (Fig. 5). The antibody titer to rachyspira aalborgi was 616±33: 6,400, and the titer to rachyspira pilosicoli was 189±12: 800 (Table 2). diagnosis of HIS was therefore made, and the patient was treated with 1,000 mg of metronidazole for 14 days. Colonoscopy performed after the completion of treatment with metronidazole showed an improvement of the ulcerative lesion in the rectum (Fig. 6), and a histological examination of colonic biopsy samples no longer demonstrated fringe formation. The patient s clinical symptoms and rectal ulceration appeared to improve for several weeks after treatment. Discussion The clinical effects of HIS infection have been studied, with various findings showing that HIS infection causes problems such as chronic diarrhea and/or abdominal pain (5, 11, 12). previous analysis of 209 HIS patients evaluated their symptoms as well as the effects of antibiotic treatment (5) and found that 51% of the patients suffered from diarrhea, while 46% suffered from abdominal pain. Furthermore, 84 of the 209 HIS patients were treated with antibiotics, such as metronidazole, 44 (52.4%) of whom showed improvements in their symptoms, indicating that the bacteria were eradicated with metronidazole (5). nother report demonstrated that 17 HIS-infected patients all suffered from either abdominal pain or gastrointestinal symptoms, 2069
4 Figure 5. Histology of the colonic biopsy specimens showed fringe formation on the luminal side of the colonic surface epithelium (Hematoxylin and Eosin staining) (, ). Figure 6. Colonoscopy performed after treatment with metronidazole showed an improvement in the ulcerative lesion in the rectum (, ). particularly long-standing diarrhea (11). In the present two cases, the patients clinical symptoms, including diarrhea, improved after treatment of HIS, indicating the possibility that the clinical symptoms were caused by the HIS infection as well as the ulcerative colitis. Furthermore, in several HIS case reports, edematous mucosa with multiple erythematous spots was detected in the ascending and proximal transverse colon, but not in the distal colon or rectum (13, 14). The colonoscopic findings in HIS patients show either non-specific ulceration of the ileocecal valve or extensive areas of ischemic ulcers (15). In the present cases, HIS was found in irregularly-shaped ulcers or extensive longitudinal ulcers. To the best of our knowledge, there are no previous reports regarding the endoscopic findings of HIS infection complicated with ulcerative colitis. Our results indicate that the presence of longitudinal or irregularly-shaped ulcers in patients with ulcerative colitis may suggest the complication of HIS infection. Previous studies have investigated the frequency of HIS in the colon and its possible correlation with various diseases. For example, Delladestima K. et al. demonstrated that 12 of 24 HIS cases were associated with carcinoma of the large intestine, three cases with adenomatous polyps, one case of hemorrhoids with metaplastic polyps and two cases with ulcerative colitis (9). Furthermore, Jensen et al. documented HIS in cases of carcinoma or polyps of the colon and ulcerative colitis (10). Recent reports have indicated that bacteria play an important role in the pathogenesis of mucosal inflammation in patients with ulcerative colitis (16, 17). In addition, previous studies have shown that Fusobacterium varium bacteria are present in a significant number of patients with active ulcerative colitis, indicating that Fusobacterium varium is an elusive pathogenic factor involved in the pathogenesis of ulcerative colitis (16). nother report suggested that the mucosa-associated microflora, especially that involving the acteroides species, plays an important role in the etiology of ulcerative colitis (17). Furthermore, several previous studies have suggested that resident enteric bacteria are necessary for the development of spontaneous colitis in animal experiments (18, 19). To the best of our knowledge, the clinical features and course of cases of ulcerative colitis involving HIS have not been well characterized. In our two HIS-positive cases, the patients endoscopic findings and clinical symptoms did not improve with mesalazine, and both patients were treated 2070
5 with long-term steroid therapy. Since the patients were classified as having an HIS infection based on histology and their antibody titers to rachyspira aalborgi and rachyspira pilosicoli, they received metronidazole and subsequently exhibited clinical and endoscopic improvements. Previous reports have demonstrated that treatment with metronidazole is effective for treating HIS infection (5, 20). Therefore, our results suggest that HIS infection may have an effect on steroid-dependent cases of ulcerative colitis. It has also been suggested that colonic spirochaetosis is transmitted via the fecal-oral route from animals, such as pigs, dogs and birds (3). In addition, homosexual and HIVinfected individuals as well as those in developing countries are at high risk for this infection (2). However, neither of our patients had these risk factors, and the route of infection in each case remains unclear. In conclusion, two ulcerative colitis patients receiving long-term steroid therapy were found to have HIS infection and exhibited a good clinical response after treatment with metronidazole. These results suggest that HIS infection should be considered as an infectious complication in patients receiving long-term steroid therapy. Further accumulation of similar cases is needed, as we cannot deny the possibility that Spirochaeta was a bystander in these cases. The authors state that they have no Conflict of Interest (COI). References 1. Harland W, Lee FD. Intestinal spirochaetosis. MJ 3: , Korner M, Gebbers JO. Clinical significance of human intestinal spirochetosis--a morphologic approach. Infection 31: , Smith JL. Colonic spirochetosis in animals and humans. J Food Prot 68: , Kraaz W, Pettersson, Thunberg U, Engstrand L, Fellstrom C. rachyspira aalborgi infection diagnosed by culture and 16S ribosomal DN sequencing using human colonic biopsy specimens. J Clin Microbio 38: , Weisheit, ethke, Stolte M. Human intestinal spirochetosis: analysis of the symptoms of 209 patients. Scand J Gastroenterol 42: , Ogata S, Higashiyama M, dachi Y, et al. Imprint cytology detects floating rachyspira in human intestinal spirochetosis. Hum Pathol 41: , be Y, Hirane, Yoshizawa, Nakajima H, dachi Y. The specific antibody to rachyspira aalborgi in serum obtained from a patient with intestinal spirochetosis. Journal of Vet Med Sci 68: , Trivett-Moore NL, Gilbert GL, Law CL, Trott DJ, Hampson DJ. Isolation of Serpulina pilosicoli from rectal biopsy specimens showing evidence of intestinal spirochetosis. J Clin Microbiol 36: , Delladestima K, Markaki S, Papadimitriou K, ntonakopoulos GN. Intestinal spirochaetosis. Light and electron microscopic study. Pathol Res Pract 182: , Jensen TK, oye M, hrens P, et al. Diagnostic examination of human intestinal spirochetosis by fluorescent in situ hybridization for rachyspira aalborgi, rachyspira pilosicoli, and other species of the genus rachyspira (Serpulina). J Clin Microbiol 39: , Calderaro, ommezzadri S, Gorrini C, et al. Infective colitis associated with human intestinal spirochetosis. J Gastroenterol Hepatol 22: , Peruzzi S, Gorrini C, Piccolo G, Calderaro, Dettori G, Chezzi C. Human intestinal spirochaetosis in Parma: a focus on a selected population during cta iomed 78: , Umeno J, Matsumoto T, Nakamura S, et al. Intestinal spirochetosis due to rachyspira pilosicoli: endoscopic and radiographic features. J Gastroenterol 42: , Nakamura S, Kuroda T, Sugai T, et al. The first reported case of intestinal spirochaetosis in Japan. Pathol Int 48: 58-62, Esteve M, Salas, Fernandez-anares F, et al. Intestinal spirochetosis and chronic watery diarrhea: clinical and histological response to treatment and long-term follow up. J Gastroenterol Hepatol 21: , Ohkusa T, Sato N. ntibacterial and antimycobacterial treatment for inflammatory bowel disease. J Gastroenterol Hepatol 20: , Matsuda H, Fujiyama Y, ndoh, Ushijima T, Kajinami T, amba T. Characterization of antibody responses against rectal mucosa-associated bacterial flora in patients with ulcerative colitis. J Gastroenterol Hepatol 15: 61-68, Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66: , Panwala CM, Jones JC, Viney JL. novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J Immunol 161: , Peghini PL, Guccion JG, Sharma. Improvement of chronic diarrhea after treatment for intestinal spirochetosis. Dig Dis Sci 45: , The Japanese Society of Internal Medicine
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