Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Curcumin Prevents Bile Canalicular Alterations in the Liver of Hamsters Infected with Opisthorchis viverrini

  • Received : 2013.04.30
  • Accepted : 2013.10.11
  • Published : 2013.12.31
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Abstract

Opisthorchis viverrini infection causes inflammation and liver injury leading to periductal fibrosis. Little is known about the pathological alterations in bile canaliculi in opisthorchiasis. This study aimed to investigate bile canalicular alterations in O. viverrini-infected hamsters and to examine the chemopreventive effects of curcumin on such changes. Hamsters were infected with O. viverrini and one group of animals was fed with 1% dietary curcumin supplement. Animals were examined during the acute infection phase, days 21 and 30 post-infection (PI) and chronic infection phase (day 90 PI). Scanning electron microscopy revealed that in the infected group fed with a normal diet, bile canaliculi became slightly tortuous by 30 day PI and more tortuous at day 90 PI. Transmission electron microscopy showed a reduction in microvilli density of canaliculi starting at day 30 PI, with a marked loss of microvilli at day 90 PI. These ultrastructral changes were slightly seen at day 21 PI, which was similar to that found in infected animals fed with 1% curcumin-supplemented diet. Notably, curcumin treatment prevented the reduction of microvilli density, reduced the dilation of bile canaliculi, and decreased the tortuosity of the bile canaliculi relative to non-infected animals on a normal diet at days 30 and 90 PI. These results suggest that curcumin reduces alteration of bile canaliculi and may be a promising agent to prevent the onset of bile duct abnormalities induced by O. viverrini infection.

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References

  1. The International Agency for Research on Cancer. Opisthorchis viverrini and Clonorchis sinensis. In IARC, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 100B, A Review of Human Carcinogens: Biological Agents. Lyon, France. IARC. 2012, p 341-370.
  2. Prasongwatana J, Laummaunwai P, Boonmars T, Pinlaor S. Viable metacercariae of Opisthorchis viverrini in northeastern Thai cyprinid fish dishes-as part of a rational program for control of O. viverrini-associated cholangiocarcinoma. Parasitol Res 2013; 112: 1323-1327. https://doi.org/10.1007/s00436-012-3154-9
  3. Prakobwong S, Yongvanit P, Hiraku Y, Pairojkul C, Sithithaworn P, Pinlaor P, Pinlaor S. Involvement of MMP-9 in peribiliary fibrosis and cholangiocarcinogenesis via Rac1-dependent DNA damage in a hamster model. Int J Cancer 2010; 127: 2576-2587. https://doi.org/10.1002/ijc.25266
  4. Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ. Liver fluke induces cholangiocarcinoma. PLoS Med 2007; 4: e201. https://doi.org/10.1371/journal.pmed.0040201
  5. Adam R, Hinz E, Sithithaworn P, Pipitgool V, Storch V. Ultrastructural hepatic alterations in hamsters and jirds after experimental infection with the liver fluke Opisthorchis viverrini. Parasitol Res 1993; 79: 357-364. https://doi.org/10.1007/BF00931823
  6. Motta P, Fumagalli G. Structure of rat bile canaliculi as revealed by scanning electron microscopy. Anat Rec 1975; 182: 499-513. https://doi.org/10.1002/ar.1091820408
  7. Allam G. Immunomodulatory effects of curcumin treatment on murine schistosomiasis mansoni. Immunobiology 2009; 214: 712-727. https://doi.org/10.1016/j.imbio.2008.11.017
  8. Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev 2009; 14: 141-153.
  9. Wu SJ, Tam KW, Tsai YH, Chang CC, Chao JC. Curcumin and saikosaponin a inhibit chemical-induced liver inflammation and fibrosis in rats. Am J Chin Med 2010; 38: 99-111. https://doi.org/10.1142/S0192415X10007695
  10. Shu JC, He YJ, Lv X, Ye GR, Wang LX. Curcumin prevents liver fibrosis by inducing apoptosis and suppressing activation of hepatic stellate cells. J Nat Med 2009; 63: 415-420. https://doi.org/10.1007/s11418-009-0347-3
  11. Pinlaor S, Yongvanit P, Prakobwong S, Kaewsamut B, Khoontawad J, Pinlaor P, Hiraku Y. Curcumin reduces oxidative and nitrative DNA damage through balancing of oxidant-antioxidant status in hamsters infected with Opisthorchis viverrini. Mol Nutr Food Res 2009; 53: 1316-1328. https://doi.org/10.1002/mnfr.200800567
  12. Pinlaor S, Prakobwong S, Hiraku Y, Pinlaor P, Laothong U, Yongvanit P. Reduction of periductal fibrosis in liver fluke-infect ed hamsters after long-term curcumin treatment. Eur J Pharmacol 2010; 638: 134-141. https://doi.org/10.1016/j.ejphar.2010.04.018
  13. Prakobwong S, Khoontawad J, Yongvanit P, Pairojkul C, Hiraku Y, Sithithaworn P, Pinlaor P, Aggarwal BB, Pinlaor S. Curcumin decreases cholangiocarcinogenesis in hamsters by suppressing inflammation- mediated molecular events related to multistep carcinogenesis. Int J Cancer 2011; 129: 88-100. https://doi.org/10.1002/ijc.25656
  14. Prakobwong S, Pinlaor S, Yongvanit P, Sithithaworn P, Pairojkul C, Hiraku Y. Time profiles of the expression of metalloproteinases, tissue inhibitors of metalloproteases, cytokines and collagens in hamsters infected with Opisthorchis viverrini with special reference to peribiliary fibrosis and liver injury. Int J Parasitol 2009; 39: 825-835. https://doi.org/10.1016/j.ijpara.2008.12.002
  15. Ogawa H, Itoshima T, Ukida M, Ito T, Kiyotoshi S, Kitadai M, Hattori S, Mizutani S, Kita K, Tanaka R, et al. Scanning electron microscopy of experimentally induced sequential alterations of rat liver hyperplastic nodules. Scan Electron Microsc 1984: 369-374.
  16. Tsuda N, Matsui O. Cirrhotic rat liver: reference to transporter activity and morphologic changes in bile canaliculi--gadoxetic acid-enhanced MR imaging. Radiology 2010; 256: 767-773. https://doi.org/10.1148/radiol.10092065
  17. Cullen C, Singh A, Shahidi E. Ultrastructure of liver from piglets fed Tower rapeseed oil. Histol Histopathol 1996; 11: 27-33.
  18. Phillips MJ, Fisher RL, Anderson DW, Lan SP, Lachin JM, Boyer JL. Ultrastructural evidence of intrahepatic cholestasis before and after chenodeoxycholic acid therapy in patients with cholelithiasis: the national cooperative gallstone study. Hepatology 1983; 3: 209-220.
  19. Lugo-Olivieri CH, Soyer PA, Fishman EK. Cystic fibrosis: spectrum of thoracic and abdominal CT findings in the adult patient. Clin Imaging 1998; 22: 346-354. https://doi.org/10.1016/S0899-7071(98)00031-X
  20. Pinlaor S, Sripa B, Sithithaworn P, Yongvanit P. Hepatobiliary changes, antibody response, and alteration of liver enzymes in hamsters re-infected with Opisthorchis viverrini. Exp Parasitol 2004; 108: 32-39. https://doi.org/10.1016/j.exppara.2004.07.007
  21. Pinlaor S, Hiraku Y, Ma N, Yongvanit P, Semba R, Oikawa S, Murata M, Sripa B, Sithithaworn P, Kawanishi S. Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammationmediated carcinogenesis. Nitric Oxide 2004; 11: 175-183. https://doi.org/10.1016/j.niox.2004.08.004
  22. Balázs M, Juházs J. Electron microscopic study on the injurious effects of chlorpromazine on rat liver cells. Exp Pathol (Jena) 1975; 11: 25-37.
  23. Bhamarapravati N, Thammavit W, Vajrasthira S. Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. Am J Trop Med Hyg 1978; 27: 787-794.
  24. Scoazec JY, Hassan N, Feldmann G. Bile canalicular alterations in hepatocyte nodules induced by 3'-methyl-4-dimethylaminoazobenzene in the rat: morphological clues on their pathogenesis and relevance to the neoplastic process. Carcinogenesis 1990; 11: 1119-1125. https://doi.org/10.1093/carcin/11.7.1119
  25. Lefkowitch JH, Feng-Chen KC, Sklar JA, Poh-Fitzpatrick MB. Cholic acid amelioration of light and electron microscopic hepatic lesions in experimental protoporphyria. Hepatology 1983; 3: 399-406.
  26. Li FC, Huang GT, Lin CJ, Wang SS, Sun TL, Lo SY, Lo W, Chiou LL, Dong CY, Lee HS. Apical membrane rupture and backward bile flooding in acetaminophen-induced hepatocyte necrosis. Cell Death Dis 2011; 2: e183. https://doi.org/10.1038/cddis.2011.68
  27. Esteller A. Physiology of bile secretion. World J Gastroenterol 2008; 14: 5641-5649. https://doi.org/10.3748/wjg.14.5641
  28. Deters M, Siegers C, Muhl P, Hänsel W. Choleretic effects of curcuminoids on an acute cyclosporin-induced cholestasis in the rat. Planta Med 1999; 65: 610-613. https://doi.org/10.1055/s-1999-14033
  29. Boonjaraspinyo S, Boonmars T, Aromdee C, Puapairoj A, Wu Z. Indirect effect of a turmeric diet: enhanced bile duct proliferation in Syrian hamsters with a combination of partial obstruction by Opisthorchis viverrini infection and inflammation by N-nitrosodimethylamine administration. Parasitol Res 2011; 108: 7-14. https://doi.org/10.1007/s00436-010-2031-7
  30. Ohta M, Marceau N, French SW. Pathologic changes in the cytokeratin pericanalicular sheath in experimental cholestasis and alcoholic fatty liver. Lab Invest 1988; 59: 60-74.

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