DOI QR코드

DOI QR Code

The Carcinogenic Liver Fluke Opisthorchis viverrini is a Reservoir for Species of Helicobacter

  • Deenonpoe, Raksawan (WHO Collaborating Centre for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Laboratory) ;
  • Chomvarin, Chariya (Department of Microbiology, Faculty of Medicine, Khon Kaen University) ;
  • Pairojkul, Chawalit (Department of Pathology, Faculty of Medicine, Khon Kaen University) ;
  • Chamgramol, Yaowalux (Department of Pathology, Faculty of Medicine, Khon Kaen University) ;
  • Loukas, Alex (Australian Institute of Tropical Health & Medicine, James Cook University) ;
  • Brindley, Paul J (Department of Microbiology, Immunology & Tropical Medicine, and Research Center for Neglected Diseases of Poverty, School of Medicine & Health Sciences, The George Washington University) ;
  • Sripa, Banchob (WHO Collaborating Centre for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Laboratory)
  • Published : 2015.03.18

Abstract

There has been a strong, positive correlation between opisthorchiasis-associated cholangiocarcinoma and infection with Helicobacter. Here a rodent model of human infection with Opisthorchis viverrini was utilized to further investigate relationships of apparent co-infections with O. viverrini and H. pylori. A total of 150 hamsters were assigned to five groups: i) Control hamsters not infected with O. viverrini; ii) O. viverrini-infected hamsters; iii) non-O. viverrini infected hamsters treated with antibiotics (ABx); iv) O. viverrini-infected hamsters treated with ABx; and v) O. viverrini-infected hamsters treated both with ABx and praziquantel (PZQ). Stomach, gallbladder, liver, colonic tissue, colorectal feces and O. viverrini worms were collected and the presence of species of Helicobacter determined by PCR-based approaches. In addition, O. viverrini worms were cultured in vitro with and without ABx for four weeks, after which the presence of Helicobacter spp. was determined. In situ localization of H. pylori and Helicobacter-like species was performed using a combination of histochemistry and immunohistochemistry. The prevalence of H. pylori infection in O. viverrini-infected hamsters was significantly higher than that of O. viverrini-uninfected hamsters ($p{\leq}0.001$). Interestingly, O. viverrini-infected hamsters treated with ABx and PZQ (to remove the flukes) had a significantly lower frequency of H. pylori than either O. viverr-iniinfected hamsters treated only with ABx or O. viverrini-infected hamsters, respectively ($p{\leq}0.001$). Quantitative RT-PCR strongly confirmed the correlation between intensity H. pylori infection and the presence of liver fluke infection. In vitro, H. pylori could be detected in the O. viverrini worms cultured with ABx over four weeks. In situ localization revealed H. pylori and other Helicobacter-like bacteria in worm gut. The findings indicate that the liver fluke O. viverrini in the biliary tree of the hamsters harbors H. pylori and Helicobacter-like bacteria. Accordingly, the association between O. viverrini and H. pylori may be an obligatory mutualism.

Keywords

Opisthorchis viverrini;Helicobacter;H. pylori;reservoir host;hamster

Acknowledgement

Supported by : Khon Kaen University

References

  1. Boonyanugomol W, Chomvarin C, Baik SC, et al (2011). Role of cagA-positive Helicobacter pylori on cell proliferation, apoptosis, and inflammation in biliary cells. Dig Dis Sci, 56, 1682-92. https://doi.org/10.1007/s10620-010-1512-y
  2. Boonyanugomol W, Chomvarin C, Song JY, et al (2012a). Effects of Helicobacter pylori gamma-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci, 57, 2615-24. https://doi.org/10.1007/s10620-012-2216-2
  3. Boonyanugomol W, Chomvarin C, Sripa B, et al (2012b). Helicobacter pylori in Thai patients with cholangiocarcinoma and its association with biliary inflammation and proliferation. HPB (Oxford), 14, 177-84. https://doi.org/10.1111/j.1477-2574.2011.00423.x
  4. Boonyanugomol W, Chomvarin C, Sripa B, et al (2012c). Molecular analysis of Helicobacter pylori virulentassociated genes in hepatobiliary patients. HPB (Oxford), 14, 754-63. https://doi.org/10.1111/j.1477-2574.2012.00533.x
  5. Bouvard V, Baan R, Straif K, et al (2009). A review of human carcinogens--Part B: biological agents. Lancet Oncol, 10, 321-2. https://doi.org/10.1016/S1470-2045(09)70096-8
  6. Carpenter, HA (1998). Bacterial and parasitic cholangitis. Mayo Clin Proc, 73, 473-8. https://doi.org/10.1016/S0025-6196(11)63734-8
  7. Cid TP, Fernandez MC, Benito Martinez S, et al (2013). Pathogenesis of Helicobacter pylori infection. Helicobacter, 18, 12-7. https://doi.org/10.1111/hel.12076
  8. Dunne C, Dolan B, Clyne M (2014). Factors that mediate colonization of the human stomach by Helicobacter pylori. World J Gastroenterol, 20, 5610-24. https://doi.org/10.3748/wjg.v20.i19.5610
  9. Foster, JR (1984). Bacterial infection of the common bile duct in chronic fascioliasis in the rat. J Comp Pathol, 94, 175-81. https://doi.org/10.1016/0021-9975(84)90038-0
  10. Fox JG, Shen Z, Muthupalani S (2009). Chronic hepatitis, hepatic dysplasia, fibrosis, and biliary hyperplasia in hamsters naturally infected with a novel Helicobacter classified in the H. bilis cluster. J Clin Microbiol, 47, 3673-81. https://doi.org/10.1128/JCM.00879-09
  11. Fox JG, Yan LL, Dewhirst FE, et al (1995). Helicobacter bilis sp. nov, a novel Helicobacter isolated from bile, livers, and intestines of aged, inbred mouse strains. J Clin Microbiol, 33, 445-54.
  12. Goldman CG, Mitchell HM (2010). Helicobacter spp. other than Helicobacter pylori. Helicobacter, 15, 69-75. https://doi.org/10.1111/j.1523-5378.2010.00780.x
  13. Hartman DJ, Owens SR (2012). Are routine ancillary stains required to diagnose Helicobacter infection in gastric biopsy specimens? An institutional quality assurance review. Am J Clin Pathol, 137, 255-60. https://doi.org/10.1309/AJCPD8FFBJ5LSLTE
  14. Hatakeyama M (2014). Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe, 15, 306-16. https://doi.org/10.1016/j.chom.2014.02.008
  15. Huai JP, Ding J, Ye XH, et al (2014). Inflammatory bowel disease and risk of cholangiocarcinoma: evidence from a meta-analysis of population-based studies. Asian Pac J Cancer Prev, 15, 3477-82. https://doi.org/10.7314/APJCP.2014.15.8.3477
  16. Hynes SO, McGuire J, Falt T, et al (2003). The rapid detection of low molecular mass proteins differentially expressed under biological stress for four Helicobacter spp. using ProteinChip technology. Proteomics, 3, 273-8. https://doi.org/10.1002/pmic.200390040
  17. IARC (2012). Biological agents. Vo. 100 B. a review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum, 100, 1-441.
  18. Khoshnegah J, Jamshidi S, Mohammadi M, et al (2011). The efficacy and safety of long-term Helicobacter species quadruple therapy in asymptomatic cats with naturally acquired infection. J Feline Med Surg, 13, 88-93. https://doi.org/10.1016/j.jfms.2010.10.003
  19. Linke S, Lenz J, Gemein S, et al (2010). Detection of Helicobacter pylori in biofilms by real-time PCR. Int J Hyg Environ Health, 213, 176-82. https://doi.org/10.1016/j.ijheh.2010.03.006
  20. Lvova MN, Tangkawattana S, Balthaisong S, et al (2012). Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitol Int, 61, 167-72. https://doi.org/10.1016/j.parint.2011.08.005
  21. Mairiang E, Laha T, Bethony JM, et al (2012). Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitol Int, 61, 208-11. https://doi.org/10.1016/j.parint.2011.07.009
  22. Malhi H, Gores GJ (2006). Cholangiocarcinoma: modern advances in understanding a deadly old disease. J Hepatol, 45, 856-67. https://doi.org/10.1016/j.jhep.2006.09.001
  23. Mateos-Munoz B, Perez-de-la-Serna J, Ruiz-de-Leon A, et al (2013). Enterohepatic Helicobacter other than Helicobacter pylori. Rev Esp Enferm Dig, 105, 477-84. https://doi.org/10.4321/S1130-01082013000800006
  24. Matsukura N, YokomuroS, Yamada S, et al (2002). Association between Helicobacter bilis in bile and biliary tract malignancies: H. bilis in bile from Japanese and Thai patients with benign and malignant diseases in the biliary tract. Jpn J Cancer Res, 93, 842-7. https://doi.org/10.1111/j.1349-7006.2002.tb01327.x
  25. Matsumoto K, Onoyama T, Kawata S, et al (2014). Hepatitis B and C virus infection is a risk factor for the development of cholangiocarcinoma. Intern Med, 53, 651-4. https://doi.org/10.2169/internalmedicine.53.1410
  26. McDaniels AE, Wymer L, Rankin C, et al (2005). Evaluation of quantitative real time PCR for the measurement of Helicobacter pylori at low concentrations in drinking water. Water Res, 39, 4808-16. https://doi.org/10.1016/j.watres.2005.09.030
  27. Murphy G, Michel A, Taylor PR, et al (2014). Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study. Hepatology, 60, 1963-71. https://doi.org/10.1002/hep.27193
  28. Pellicano R, Mazzaferro V, Grigioni WF, et al (2004). Helicobacter species sequences in liver samples from patients with and without hepatocellular carcinoma. World J Gastroenterol, 10, 598-601. https://doi.org/10.3748/wjg.v10.i4.598
  29. Pellicano R, Menard A, Rizzetto M, et al (2008). Helicobacter species and liver diseases: association or causation? Lancet Infect Dis, 8, 254-60. https://doi.org/10.1016/S1473-3099(08)70066-5
  30. Petney TN, Andrews RH, Saijuntha W, et al (2013). The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini. Int J Parasitol, 43, 1031-46. https://doi.org/10.1016/j.ijpara.2013.07.007
  31. Pisani P, Whary MT, Nilsson I, et al (2008). Cross-reactivity between immune responses to Helicobacter bilis and Helicobacter pylori in a population in Thailand at high risk of developing cholangiocarcinoma. Clin Vaccine Immunol, 15, 1363-8. https://doi.org/10.1128/CVI.00132-08
  32. Plieskatt JL, Deenonpoe R, Mulvenna JP, et al (2013). Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. FASEB J, 27, 4572-84. https://doi.org/10.1096/fj.13-232751
  33. Rizvi S, Gores GJ (2013). Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology, 145, 1215-29. https://doi.org/10.1053/j.gastro.2013.10.013
  34. Sachs G, Scott DR, Wen Y, (2011). Gastric infection by Helicobacter pylori. Curr Gastroenterol Rep, 13, 540-6. https://doi.org/10.1007/s11894-011-0226-4
  35. Shao C, Zhang Q, Sun Y, et al (2008). Helicobacter pylori protein response to human bile stress. J Med Microbiol, 57, 151-8. https://doi.org/10.1099/jmm.0.47616-0
  36. Shin HR, Oh JK, Masuyer E, et al (2010). Comparison of incidence of intrahepatic and extrahepatic cholangiocarcinoma-focus on East and South-Eastern Asia. Asian Pac J Cancer Prev, 11, 1159-66.
  37. Sithithaworn P, Yongvanit P, Duenngai K, et al (2014). Roles of liver fluke infection as risk factor for cholangiocarcinoma. J Hepatobiliary Pancreat Sci, 21, 301-8. https://doi.org/10.1002/jhbp.62
  38. Sripa B (2003). Pathobiology of opisthorchiasis: an update. Acta Trop, 88, 209-20. https://doi.org/10.1016/j.actatropica.2003.08.002
  39. Sripa B, Brindley PJ, Mulvenna J, et al (2012). The tumorigenic liver fluke Opisthorchis viverrini-multiple pathways to cancer. Trends Parasitol, 28, 395-407. https://doi.org/10.1016/j.pt.2012.07.006
  40. Sripa B, Kaewkes S, Sithithaworn P, et al (2007). Liver fluke induces cholangiocarcinoma. PLoS Med, 4, 201. https://doi.org/10.1371/journal.pmed.0040201
  41. Sripa B, Pairojkul C (2008). Cholangiocarcinoma: lessons from Thailand. Cur Opin Gastroenterol, 24, 349-56. https://doi.org/10.1097/MOG.0b013e3282fbf9b3
  42. Strazzabosco M, Spirli C, Okolicsanyi L, (2010). Pathophysiology of the intrahepatic biliary epithelium. J Gastroenterol Hepatol, 15, 244-53.
  43. Wongpaitoon V, Thuvasethakul P, Kurathong S, et al (1988). Biliary bile acids and lipids composition in Opisthorchiasis viverrini. J Med Assoc Thai, 71, 394-9.
  44. Wonkchalee O, Boonmars T, Kaewkes S, et al (2012). Comparative studies on animal models for Opisthorchis viverrini infection: host interaction through susceptibility and pathology. Parasitol Res, 110, 1213-23. https://doi.org/10.1007/s00436-011-2616-9
  45. Wu Q, He XD, Yu L, et al (2012). The metabolic syndrome and risk factors for biliary tract cancer: a case-control study in China. Asian Pac J Cancer Prev, 13, 1963-9. https://doi.org/10.7314/APJCP.2012.13.5.1963
  46. Zhou D, Wang JD, Weng MZ, et al (2013). Infections of Helicobacter spp. in the biliary system are associated with biliary tract cancer: a meta-analysis. Eur J Gastroenterol Hepatol, 25, 447-54.

Cited by

  1. The role of H. pylori infection in gall bladder cancer: clinicopathological study vol.36, pp.9, 2015, https://doi.org/10.1007/s13277-015-3444-9
  2. Chronic Opisthorchis viverrini Infection Changes the Liver Microbiome and Promotes Helicobacter Growth vol.11, pp.11, 2016, https://doi.org/10.1371/journal.pone.0165798
  3. High Prevalence of Helicobacter pylori Resistance to Clarithromycin: a Hospital-Based Cross-Sectional Study in Nakhon Ratchasima Province, Northeast of Thailand vol.16, pp.18, 2016, https://doi.org/10.7314/APJCP.2015.16.18.8281
  4. Helicobacter Species are Possible Risk Factors of Cholangiocarcinoma vol.17, pp.1, 2016, https://doi.org/10.7314/APJCP.2016.17.1.37
  5. Liver fluke infection and cholangiocarcinoma: a review vol.116, pp.1, 2017, https://doi.org/10.1007/s00436-016-5276-y
  6. Biliary Microbiota, Gallstone Disease and Infection with Opisthorchis felineus vol.10, pp.7, 2016, https://doi.org/10.1371/journal.pntd.0004809
  7. Coinfection with Helicobacter pylori and Opisthorchis viverrini Enhances the Severity of Hepatobiliary Abnormalities in Hamsters vol.85, pp.4, 2017, https://doi.org/10.1128/IAI.00009-17
  8. Elevated prevalence of Helicobacter species and virulence factors in opisthorchiasis and associated hepatobiliary disease vol.7, pp.1, 2017, https://doi.org/10.1038/srep42744
  9. Elevated Levels of Urinary 8-oxodG Correlate with Persistent Periductal Fibrosis after Praziquantel Treatment in Chronic Opisthorchiasis vol.98, pp.6, 2018, https://doi.org/10.4269/ajtmh.17-0971
  10. Liver Fluke-Associated Biliary Tract Cancer vol.12, pp.3, 2018, https://doi.org/10.5009/gnl17102
  11. Chinese liver fluke Clonorchis sinensis infection changes the gut microbiome and increases probiotic Lactobacillus in mice vol.118, pp.2, 2019, https://doi.org/10.1007/s00436-018-6179-x