Role of the microbiota and antibiotics in primary sclerosing cholangitis

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Tabibian, James H ^a   Talwalkar, Jayant A ^a   Lindor, Keith D ^b  

^a MAYO CLINIC   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ANTIBIOTIC AGENT; ASPARTATE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE ISOENZYME 1; AZITHROMYCIN; CYCLOSPORIN A; METHOTREXATE; METRONIDAZOLE; MINOCYCLINE; PREDNISONE; SALAZOSULFAPYRIDINE; TETRACYCLINE; URSODEOXYCHOLIC ACID; VANCOMYCIN; ANTIINFECTIVE AGENT;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANTIBIOTIC THERAPY; BACTERIAL OVERGROWTH; DRUG MEGADOSE; ENTEROPATHY; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INNATE IMMUNITY; INTRAHEPATIC BILE DUCT; LOW DRUG DOSE; MICROFLORA; NONHUMAN; PRIMARY SCLEROSING CHOLANGITIS; RECOMMENDED DRUG DOSE; REVIEW; UNSPECIFIED SIDE EFFECT; ANIMAL; DISEASE MODEL; INFLAMMATORY BOWEL DISEASE; MICROBIOLOGY; MOUSE; PATHOLOGY; SCLEROSING CHOLANGITIS;

ANIMALS; ANTI-BACTERIAL AGENTS; CHOLANGITIS, SCLEROSING; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATORY BOWEL DISEASES; MICE; MICROBIOTA;

EID: 84887423367     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/389537     Document Type: Review

References (72)

1. Gupta A., Bowlus C. L., Primary sclerosing cholangitis: etiopathogenesis and clinical management. Frontiers in Bioscience 2012 4 1683 1705
2. Tabibian J. H., Lindor K. D., Primary sclerosing cholangitis: a review and update on therapeutic developments. Expert Review of Gastroenterology & Hepatology 2013 7 103 114
3. Bambha K., Kim W. R., Talwalkar J., Torgerson H., Benson J. T., Therneau T. M., Loftus E. V. Jr., Yawn B. P., Dickson E. R., Melton L. J. III, Incidence, clinical spectrum, and outcomes of primary sclerosing cholangitis in a United States community. Gastroenterology 2003 125 5 1364 1369 2-s2.0-0242490278 10.1016/j.gastro.2003.07.011
4. Kaplan G. G., Laupland K. B., Butzner D., Urbanski S. J., Lee S. S., The burden of large and small duct primary sclerosing cholangitis in adults and children: a population-based analysis. American Journal of Gastroenterology 2007 102 5 1042 1049 2-s2.0-34248177488 10.1111/j.1572-0241.2007.01103.x
5. Tabibian J. H., Lindor K. D., Challenges of cholangiocarcinoma detection in patients with primary sclerosing cholangitis. Journal of Analytical Oncology 2012 1 50 55
6. Wiesner R. H., Grambsch P. M., Dickson E. R., Ludwig J., MacCarty R. L., Hunter E. B., Fleming T. R., Fisher L. D., Beaver S. J., LaRusso N. F., Primary sclerosing cholangitis: natural history, prognostic factors and survival analysis. Hepatology 1989 10 4 430 436 2-s2.0-0024414279
7. Chapman R., Fevery J., Kalloo A., Nagorney D. M., Boberg K. M., Shneider B., Gores G. J., Diagnosis and management of primary sclerosing cholangitis. Hepatology 2010 51 2 660 678 2-s2.0-75449104123 10.1002/hep.23294
8. Imam M. H., Sinakos E., Gossard A. A., Kowdley K. V., Luketic V. A. C., Edwyn Harrison M., McCashland T., Befeler A. S., Harnois D., Jorgensen R., Petz J., Keach J., Decook A. C., Enders F., Lindor K. D., High-dose ursodeoxycholic acid increases risk of adverse outcomes in patients with early stage primary sclerosing cholangitis. Alimentary Pharmacology and Therapeutics 2011 34 10 1185 1192 2-s2.0-80055025463 10.1111/j.1365-2036.2011.04863.x
9. Karlsen T. H., Schrumpf E., Boberg K. M., Update on primary sclerosing cholangitis. Digestive and Liver Disease 2010 42 6 390 400 2-s2.0-77952742582 10.1016/j.dld.2010.01.011
10. Bjøro K., Brandsaerter B., Foss A., Schrumpf E., Liver transplantation in primary sclerosing cholangitis. Seminars in Liver Disease 2006 26 1 69 79 2-s2.0-33644612987
11. Alabraba E., Nightingale P., Gunson B., Hubscher S., Olliff S., Mirza D., Neuberger J., A re-evaluation of the risk factors for the recurrence of primary sclerosing cholangitis in liver allografts. Liver Transplantation 2009 15 3 330 340 2-s2.0-67649232094 10.1002/lt.21679
12. Graziadei I. W., Live donor liver transplantation for primary sclerosing cholangitis: is disease recurrence increased? Current Opinion in Gastroenterology 2011 27 3 301 305 2-s2.0-79955055249 10.1097/MOG. 0b013e3283437a8c
13. Landaverde C., Ng V., Sato A., Tabibian J., Durazo F., Busuttil R., De-novo cholangiocarcinoma in native common bile duct remnant following OLT for primary sclerosing cholangitis. Annals of Hepatology 2009 8 4 379 383 2-s2.0-77953472805
14. Tabibian J. H., O'Hara S. P., Larusso N. F., Primary sclerosing cholangitis: the Gut-Liver axis. Clinical Gastroenterology and Hepatology 2012 10 819 820 2-s2.0-84858957899 10.1016/j.cgh.2012.01.024
15. Schwartz S. I., Dale W. A., Primary sclerosing cholangitis; review and report of six cases. A.M.A. Archives of Surgery 1958 77 3 439 451 2-s2.0-70449230859
16. Thorpe M. E., Scheuer P. J., Sherlock S., Primary sclerosing cholangitis, the biliary tree, and ulcerative colitis. Gut 1967 8 5 435 448 2-s2.0-0014135147
17. Loftus E. V. Jr., Harewood G. C., Loftus C. G., Tremaine W. J., Harmsen W. S., Zinsmeister A. R., Jewell D. A., Sandborn W. J., PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis. Gut 2005 54 1 91 96 2-s2.0-10844282782 10.1136/gut.2004.046615
18. Okada H., Mizuno M., Yamamoto K., Tsuji T., Primary sclerosing cholangitis in Japanese patients: association with inflammatory bowel disease. Acta Medica Okayama 1996 50 5 227 235 2-s2.0-0030253129
19. Welcker K., Martin A., Kölle O., Siebeck M., Gross M., Increased intestinal permeability in patients with inflammatory bowel disease. European Journal of Medical Research 2004 9 10 456 460 2-s2.0-16644377769
20. Katz K. D., Hollander D., Vadheim C. M., McElree C., Delahunty T., Dadufalza V. D., Krugliak P., Rotter J. I., Intestinal permeability in patients with Crohn's disease and their healthy relatives. Gastroenterology 1989 97 4 927 931 2-s2.0-0024462586
21. Buhner S., Buning C., Genschel J., Kling K., Herrmann D., Dignass A., Kuechler I., Krueqer S., Schmidt H. H.-J., Lochs H., Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation? Gut 2006 55 3 342 347 2-s2.0-33144473772 10.1136/gut.2005. 065557
22. Tabibian J. H., Masyuk A. I., Masyuk T. V., O'Hara S. P., LaRusso N. F., Cholangiocyte physiology. Comprehensive Physiology 2013 3 541 565
23. O'Mahony C. A., Vierling J. M., Etiopathogenesis of primary sclerosing cholangitis. Seminars in Liver Disease 2006 26 1 3 21 2-s2.0-33644617718
24. O'Hara S. P., Tabibian J. H., Splinter P. L., The dynamic biliary epithelia: molecules, pathways, and disease. Journal of Hepatology 2013 58 575 582
25. Tabibian J. H., Weeding E., Jorgensen R. A., Randomised clinical trial: vancomycin or metronidazole in patients with primary sclerosing cholangitis-A Pilot Study. Alimentary Pharmacology & Therapeutics 2013 37 604 612
26. Björnsson E., Cederborg A., Åkvist A., Simren M., Stotzer P.-O., Bjarnason I., Intestinal permeability and bacterial growth of the small bowel in patients with primary sclerosing cholangitis. Scandinavian Journal of Gastroenterology 2005 40 9 1090 1094 2-s2.0-24744458143 10.1080/ 00365520510023288
27. Mistilis S. P., Skyring A. P., Goulston S. J., Effect of long-term tetracycline therapy, steroid therapy and colectomy in pericholangitis associated with ulcerative colitis. Australasian Annals of Medicine 1965 14 4 286 294 2-s2.0-0013816559
28. Pohl J., Ring A., Stremmel W., Stiehl A., The role of dominant stenoses in bacterial infections of bile ducts in primary sclerosing cholangitis. European Journal of Gastroenterology and Hepatology 2006 18 1 69 74 2-s2.0-29344470338 10.1097/00042737-200601000-00012
29. Duboc H., Rajca S., Rainteau D., Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 2013 62 4 531 539
30. DuPont A. W., DuPont H. L., The intestinal microbiota and chronic disorders of the gut. Nature Reviews Gastroenterology & Hepatology 2011 8 523 531
31. Clemente J. C., Ursell L. K., Parfrey L. W., Knight R., The impact of the gut microbiota on human health: an integrative view. Cell 2012 148 6 1258 1270 2-s2.0-84858376593 10.1016/j.cell.2012.01.035
32. Weismüller T. J., Wedemeyer J., Kubicka S., Strassburg C. P., Manns M. P., The challenges in primary sclerosing cholangitis-aetiopathogenesis, autoimmunity, management and malignancy. Journal of Hepatology 2008 48 1 S38 S57 2-s2.0-40849123925 10.1016/j.jhep.2008.01.020
33. Worthington J., Cullen S., Chapman R., Immunopathogenesis of primary sclerosing cholangitis. Clinical Reviews in Allergy and Immunology 2005 28 2 93 103 2-s2.0-24644507580
34. Färkkilä M., Karvonen A.-L., Nurmi H., Nuutinen H., Taavitsainen M., Pikkarainen P., Kärkkäinen P., Metronidazole and ursodeoxycholic acid for primary sclerosing cholangitis: a randomized placebo-controlled trial. Hepatology 2004 40 6 1379 1386 2-s2.0-10644269919 10.1002/hep.20457
35. Silveira M. G., Torok N. J., Gossard A. A., Keach J. C., Jorgensenrn R. A., Petzrn J. L., Lindor K. D., Minocycline in the treatment of patients with primary sclerosing cholangitis: results of a pilot study. American Journal of Gastroenterology 2009 104 1 83 88 2-s2.0-60749089231 10.1038/ajg.2008.14
36. Rankin J. G., Boden R. W., Goulston S. J. M., Morrow W., The liver in ulcerative colitis; treatment of pericholangitis with tetracycline. The Lancet 1959 274 7112 1110 1112 2-s2.0-0000072924
37. Mathew K. K., Metronidazole in primary cholangitis. Journal of the Indian Medical Association 1983 80 2 31 2-s2.0-0020624187
38. Kozaiwa K., Tajiri H., Sawada A., Tada K., Etani Y., Miki K., Okada S., Case report: three paediatric cases of primary sclerosing cholangitis treated with ursodeoxycholic acid and sulphasalazine. Journal of Gastroenterology and Hepatology 1998 13 8 825 829 2-s2.0-0032135138
39. Cox K. L., Cox K. M., Oral vancomycin: treatment of primary sclerosing cholangitis in children with inflammatory bowel disease. Journal of Pediatric Gastroenterology and Nutrition 1998 27 5 580 583 2-s2.0-0031782677 10.1097/00005176-199811000-00015
40. Broccoletti T., Ciccimarra E., Spaziano M., Capuano G., Petrone E., Mandato C., Migliaro F., Vajro P., Refractory primary sclerosing cholangitis becoming responsive after sulphasalazine treatment of an underlying silent colitis. Italian Journal of Pediatrics 2002 28 6 515 517 2-s2.0-0036959298
41. Tada S., Ebinuma H., Saito H., Hibi T., Therapeutic benefit of sulfasalazine for patients with primary sclerosing cholangitis. Journal of Gastroenterology 2006 41 4 388 389 2-s2.0-33744801168 10.1007/s00535-005-1758-x
42. Boner A. L., Peroni D., Bodini A., Delaini G., Piacentini G., Azithromycin may reduce cholestasis in primary sclerosing cholangitis: a case report and serendipitous observation. International Journal of Immunopathology and Pharmacology 2007 20 4 847 849 2-s2.0-37749028067
43. Davies Y. K., Cox K. M., Abdullah B. A., Safta A., Terry A. B., Cox K. L., Long-term treatment of primary sclerosing cholangitis in children with oral vancomycin: an immunomodulating antibiotic. Journal of Pediatric Gastroenterology and Nutrition 2008 47 1 61 67 2-s2.0-55549136784 10.1097/MPG.0b013e31816fee95
44. Tabibian J. H., Macura S. I., O'Hara S. P., Micro-computed tomography and nuclear magnetic resonance imaging for noninvasive, live-mouse cholangiography. Laboratory Investigation 2013 93 733 743
45. Lichtman S. N., Keku J., Clark R. L., Schwab J. H., Sartor R. B., Biliary tract disease in rats with experimental small bowel bacterial overgrowth. Hepatology 1991 13 4 766 772 2-s2.0-0025801063 10.1016/0270-9139(91)92577-U
46. Lichtman S. N., Okoruwa E. E., Keku J., Schwab J. H., Sartor R. B., Degradation of endogenous bacterial cell wall polymers by the muralytic enzyme mutanolysin prevents hepatobiliary injury in genetically susceptible rats with experimental intestinal bacterial overgrowth. Journal of Clinical Investigation 1992 90 4 1313 1322 2-s2.0-0026451945
47. Lichtman S. N., Wang J., Clark R. L., A microcholangiographic study of liver disease models in rats. Academic Radiology 1995 2 6 515 521 2-s2.0-0029311525 10.1016/S1076-6332(05)80410-6
48. Yamada S., Ishii M., Liang L. S., Yamamoto T., Toyota T., Small duct cholangitis induced by N-formyl L-methionine L-leucine L-tyrosine in rats. Journal of Gastroenterology 1994 29 5 631 636 2-s2.0-0027935792 10.1007/BF02365447
49. Haruta I., Kikuchi K., Hashimoto E., Nakamura M., Miyakawa H., Hirota K., Shibata N., Kato H., Arimura Y., Kato Y., Uchiyama T., Nagamune H., Kobayashi M., Miyake Y., Shiratori K., Yagi J., Long-term bacterial exposure can trigger nonsuppurative destructive cholangitis associated with multifocal epithelial inflammation. Laboratory Investigation 2010 90 4 577 588 2-s2.0-77950353635 10.1038/labinvest.2010.40
50. Karrar A., Broomé U., Södergren T., Jaksch M., Bergquist A., Björnstedt M., Sumitran-Holgersson S., Biliary epithelial cell antibodies link adaptive and innate immune responses in primary sclerosing cholangitis. Gastroenterology 2007 132 4 1504 1514 2-s2.0-34247196579 10.1053/j.gastro.2007. 01.039
51. Pollheimer M. J., Trauner M., Fickert P., Will we ever model PSC? 'it's hard to be a PSC model!'. Clinics and Research in Hepatology and Gastroenterology 2011 35 12 792 804 2-s2.0-82255162029
52. O'Hara S. P., Splinter P. L., Trussoni C. E., Gajdos G. B., Lineswala P. N., LaRusso N. F., Cholangiocyte N-Ras protein mediates lipopolysaccharide- induced interleukin 6 secretion and proliferation. Journal of Biological Chemistry 2011 286 35 30352 30360 2-s2.0-80052230924 10.1074/jbc.M111.269464
53. Harada K., Nakanuma Y., Cholangiopathy with respect to biliary innate immunity. International Journal of Hepatology 2012 2012 10 793569 10.1155/2012/793569
54. Chen X.-M., O'Hara S. P., Nelson J. B., Splinter P. L., Small A. J., Tietz P. S., Limper A. H., LaRusso N. F., Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NF- B. Journal of Immunology 2005 175 11 7447 7456 2-s2.0-28244478101
55. Yokoyama T., Komori A., Nakamura M., Takii Y., Kamihira T., Shimoda S., Mori T., Fujiwara S., Koyabu M., Taniguchi K., Fujioka H., Migita K., Yatsuhashi H., Ishibashi H., Human intrahepatic biliary epithelial cells function in innate immunity by producing IL-6 and IL-8 via the TLR4-NF- B and -MAPK signaling pathways. Liver International 2006 26 4 467 476 2-s2.0-33645741989 10.1111/j.1478-3231.2006.01254.x
56. Chen X.-M., O'Hara S. P., LaRusso N. F., The immunobiology of cholangiocytes. Immunology and Cell Biology 2008 86 6 497 505 2-s2.0-49649123486 10.1038/icb.2008.37
57. Katt J., Schwinge D., Schoknecht T., Increased th17 response to pathogen stimulation in patients with primary sclerosing cholangitis. Hepatology 2013 58 3 1084 1093
58. Mueller T., Beutler C., Picó A. H., Shibolet O., Pratt D. S., Pascher A., Neuhaus P., Wiedenmann B., Berg T., Podolsky D. K., Enhanced innate immune responsiveness and intolerance to intestinal endotoxins in human biliary epithelial cells contributes to chronic cholangitis. Liver International 2011 31 10 1574 1588 2-s2.0-80053991368 10.1111/j.1478-3231.2011.02635.x
59. Olsson R., Björnsson E., Bäckman L., Friman S., Höckerstedt K., Kaijser B., Olausson M., Bile duct bacterial isolates in primary sclerosing cholangitis: a study of explanted livers. Journal of Hepatology 1998 28 3 426 432 2-s2.0-0032032527 10.1016/S0168-8278(98)80316-4
60. Hiramatsu K., Harada K., Tsuneyama K., Sasaki M., Fujita S., Hashimoto T., Kaneko S., Kobayashi K., Nakanuma Y., Amplification and sequence analysis of partial bacterial 16S ribosomal RNA gene in gallbladder bile from patients with primary biliary cirrhosis. Journal of Hepatology 2000 33 1 9 18 2-s2.0-0033916878 10.1016/S0168-8278(00)80153-1
61. Sasatomi K., Noguchi K., Sakisaka S., Sata M., Tanikawa K., Abnormal accumulation of endotoxin in biliary epithelial cells in primary biliary cirrhosis and primary sclerosing cholangitis. Journal of Hepatology 1998 29 3 409 416 2-s2.0-0032171526 10.1016/S0168-8278(98)80058-5
62. Mimura Y., Sakisaka S., Harada M., Sata M., Tanikawa K., Role of hepatocytes in direct clearance of lipopolysaccharide in rats. Gastroenterology 1995 109 6 1969 1976 2-s2.0-0028804229 10.1016/0016-5085(95)90765-3
63. Osnes T., Sandstad O., Skar V., Osnes M., Lipopolysaccharides and beta-glucuronidase activity in choledochal bile in relation to choledocholithiasis. Digestion 1997 58 5 437 443 2-s2.0-0030863290
64. Liu J. Z., Hov J. R., Folseraas T., Dense genotyping of immune-related disease regions identifies nine new risk loci for primary sclerosing cholangitis. Nature Genetics 2013 45 6 670 675
65. Folseraas T., Melum E., Rausch P., Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci. Journal of Hepatology 2012 57 366 375
66. Rausch P., Rehman A., Künzel S., Häsler R., Ott S. J., Schreiber S., Rosenstiel P., Franke A., Baines J. F., Colonic mucosa-associated microbiota is influenced by an interaction of crohn disease and FUT2 (Secretor) genotype. Proceedings of the National Academy of Sciences of the United States of America 2011 108 47 19030 19035 2-s2.0-82755168804 10.1073/pnas.1106408108
67. McGovern D. P. B., Jones M. R., Taylor K. D., Marciante K., Yan X., Dubinsky M., Ippoliti A., Vasiliauskas E., Berel D., Derkowski C., Dutridge D., Fleshner P., Shih D. Q., Melmed G., Mengesha E., King L., Pressman S., Haritunians T., Guo X., Targan S. R., Rotter J. I., Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Human Molecular Genetics 2010 19 17 3468 3476 2-s2.0-77955398591 10.1093/hmg/ddq248 ddq248
68. Elfaki D. A. H., Lindor K. D., Antibiotics for the treatment of primary sclerosing cholangitis. American Journal of Therapeutics 2011 18 3 261 265 2-s2.0-79958051295 10.1097/MJT.0b013e3181b7b8c0
69. Shimizu M., Iwasaki H., Mase S., Successful treatment of primary sclerosing cholangitis with a steroid and a probiotic. Case Reports in Gastroenterology 2012 6 249 253
70. Vleggaar F. P., Monkelbaan J. F., Van Erpecum K. J., Probiotics in primary sclerosing cholangitis: a randomized placebo-controlled crossover pilot study. European Journal of Gastroenterology and Hepatology 2008 20 7 688 692 2-s2.0-62149093658 10.1097/MEG.0b013e3282f5197e
71. Davies Y. K., Tsay C. J., Caccamo D. V., Successful treatment of recurrent primary sclerosing cholangitis after orthotopic liver transplantation with oral vancomycin. Case Rep Transplant 2013 2013 5 314292 314292
72. Abarbanel D. N., Seki S. M., Davies Y., Immunomodulatory effect of vancomycin on treg in pediatric inflammatory bowel disease and primary sclerosing cholangitis. Journal of Clinical Immunology 2013 33 397 406