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Is Schistosoma mansoni playing a part in liver carcinogenesis?

Published online by Cambridge University Press:  29 October 2024

S. Jain*
Affiliation:
Institute for Globally Distributed Open Research and Education (IGDORE), India
*
Corresponding author: S. Jain; Email: [email protected]

Abstract

The relationship between Schistosoma mansoni (Sm) and hepatocellular carcinoma (HCC) has been evaluated by many studies that point towards a co-relation between schistosomal infection and HCC. While many such studies demonstrated that Sm infection in the presence of another carcinogenic factors leads to HCC, none of these studies could conclusively prove the cancer-inducing ability of Sm in humans, independent of other carcinogenic factors. The aim of this work is to present the current understanding on the association of Sm with HCC. Many epidemiological, pathological, and clinical studies have shown the role of multiple events like chronic inflammation and fibrosis as well as hepato-toxic agents like soluble egg antigens (SEAs), which help in creating a micro-environment which is suitable for HCC development. The role of Sm infection and deposited eggs in causing persistent inflammation, advanced fibrosis, and the role of SEAs, especially IPSE/alpha-1, is emphasised. This work concludes that Sm infection has the potential to induce cancer independently but the same has not been reported in humans to date. Extensive research is required to establish a causal relationship between Sm infection and HCC induction, or a complete lack thereof. However, Sm infection definitely acts along with other carcinogenic factors to induce HCC at a much faster pace and also leads to an aggressive form of liver cancer, which the other carcinogenic factor could not have achieved alone.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Abdulla, MH, Lim, KC, McKerrow, JH, and Caffrey, CR (2011) Proteomic identification of IPSE/alpha-1 as a major hepatotoxin secreted by Schistosoma mansoni eggs. PLoS Neglected Tropical Diseases 5(10), e1368. https://doi.org/10.1371/journal.pntd.0001368CrossRefGoogle Scholar
Abe, K, Kagei, N, Teramura, Y, and Ejima, H (1993) Hepatocellular carcinoma associated with chronic Schistosoma mansoni infection in a chimpanzee. Journal of Medical Primatology 22(4), 237239.CrossRefGoogle Scholar
Baravelli, CM, Sandberg, S, Aarsand, AK, and Tollånes, MC (2019) Porphyria cutanea tarda increases risk of hepatocellular carcinoma and premature death: A nationwide cohort study. Orphanet Journal of Rare Diseases 14(1), 77. https://doi.org/10.1186/s13023-019-1051-3CrossRefGoogle ScholarPubMed
Barnard, A, Moch, A, and Saab, S (2018) Relationship between telomere maintenance and liver disease. Gut and Liver 13(1), 1115. https://doi.org/10.5009/gnl18081CrossRefGoogle Scholar
Bataller, R and Brenner, DA (2005) Liver fibrosis. The Journal of Clinical Investigation, 115(2), 209218. https://doi.org/10.1172/JCI24282CrossRefGoogle ScholarPubMed
Bogen, SA, Flores Villanueva, PO, McCusker, ME, Fogelman, I, Garifallou, M, el-Attar, ES, Kwan, P, and Stadecker, MJ (1995) In situ analysis of cytokine responses in experimental murine schistosomiasis. Laboratory Investigation: A Journal of Technical Methods and Pathology 73(2), 252258.Google ScholarPubMed
Calderaro, J, Rousseau, B, Amaddeo, G, Mercey, M, Charpy, C, Costentin, C, Luciani, A, Zafrani, ES, Laurent, A, Azoulay, D, Lafdil, F, and Pawlotsky, JM (2016) Programmed death ligand 1 expression in hepatocellular carcinoma: Relationship with clinical and pathological features. Hepatology, 64(6), 20382046. https://doi.org/10.1002/hep.28710CrossRefGoogle ScholarPubMed
CDC website. Schistosomiasis. Available at https://www.cdc.gov/dpdx/schistosomiasis/index.html (accessed February 17, 2024).Google Scholar
Chaudhary, B and Elkord, E (2016) Regulatory T cells in the tumor microenvironment and cancer progression: Role and therapeutic targeting. Vaccines 4(3), 28. https://doi.org/10.3390/vaccines4030028CrossRefGoogle ScholarPubMed
Chen, TTW, Cheng, PC, Chang, KC, Cao, JP, Feng, JL, Chen, CC, Lam, HYP, and Peng, SY (2019) Activation of the NLRP3 and AIM2 inflammasomes in a mouse model of Schistosoma mansoni infection. Journal of Helminthology 94, e72. https://doi.org/10.1017/S0022149X19000622CrossRefGoogle Scholar
Chuah, C, Jones, MK, Burke, ML, McManus, DP, and Gobert, GN (2014) Cellular and chemokine-mediated regulation in schistosome-induced hepatic pathology. Trends in Parasitology 30(3):141150. https://doi.org/10.1016/j.pt.2013.12.009CrossRefGoogle ScholarPubMed
Colley, DG, Bustinduy, AL, Secor, WE, and King, CH (2014) Human schistosomiasis. Lancet 383(9936), 22532264. https://doi.org/10.1016/S0140-6736(13)61949-2CrossRefGoogle ScholarPubMed
Cooper, GM and Hausman, RE (2007) The Cell-a Molecular Approach. Sunderland: Sinauer Associates.Google Scholar
Coutinho, HM, McGarve, ST, Acosta, LP, Manalo, DL, Langdon, GC, Leenstra, T, Kanzaria, HK, Solomon, J, Wu, H, Olveda, RM, Kurtis, JD, and Friedman, JF (2005) Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. Journal of Infectious Diseases 192(3), 528536. https://doi.org/10.1086/430929CrossRefGoogle Scholar
Culver, EL, Watkins, J, and Westbrook, RH (2016) Granulomas of the liver. Clinical Liver Disease 7(4), 9296. https://doi.org/10.1002/cld.544CrossRefGoogle ScholarPubMed
Deslyper, G, Doherty, DG, Carolan, JC, and Holland, CV (2019) The role of the liver in the migration of parasites of global significance. Parasites & Vectors 12(1), 531. https://doi.org/10.1186/s13071-019-3791-2CrossRefGoogle ScholarPubMed
Dhamija, E, Paul, SB, and Kedia, S (2019) Non-alcoholic fatty liver disease associated with hepatocellular carcinoma: An increasing concern. The Indian Journal of Medical Research 149(1), 917. https://doi.org/10.4103/ijmr.IJMR_1456_17Google ScholarPubMed
Donati, B and Valenti, L (2016) Telomeres, NAFLD and chronic liver disease. International Journal of Molecular Sciences 17(3), 383. https://doi.org/10.3390/ijms17030383CrossRefGoogle ScholarPubMed
Elmberg, M, Hultcrantz, R, Ekbom, A, Brandt, L, Olsson, S, Olsson, R, Lindgren, S, Lööf, L, Stål, P, Wallerstedt, S, Almer, S, Sandberg-Gertzén, H, and Askling, J (2003) Cancer risk in patients with hereditary hemochromatosis and in their first-degree relatives. Gastroenterology 125(6), 17331741. https://doi.org/10.1053/j.gastro.2003.09.035CrossRefGoogle ScholarPubMed
El-Tonsy, MM, Hussein, HM, Tel-S, Helal, Tawfik, RA, Korie, KM, and Hussein, HM (2016) Human Schistosomiasis mansoni associated with hepatocellular carcinoma in Egypt: Current perspective. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology 40(3), 976980. https://doi.org/10.1007/s12639-014-0618-0CrossRefGoogle ScholarPubMed
El-Tonsy, MM, Hussein, HM, Tel-S, Helal, Tawfik, RA, Koriem, KM, and Hussein, HM (2013) Schistosoma mansoni infection: Is it a risk factor for development of hepatocellular carcinoma? Acta Tropica 128(3), 542547. https://doi.org/10.1016/j.actatropica.2013.07.024CrossRefGoogle ScholarPubMed
Fahel, JS, Maced, GC, Pinheiro, CS, Caliari, MV, and Oliveira, SC (2010) IPSE/alpha-1 of Schistosoma mansoni egg induces enlargement of granuloma but does not alter Th2 balance after infection. Parasite Immunology 32(5), 345353. https://doi.org/10.1111/j.1365-3024.2009.01192.xCrossRefGoogle Scholar
Filgueira, NA, Saraiva CM de, A, Jucá, NT, Bezerra, MF, and Lacerda, CM (2018) Schistosomal liver fibrosis and hepatocellular carcinoma - case series of patients submitted to liver transplantation. Brazilian Journal of Infectious Diseases 22(4), 352354. https://doi.org/10.1016/j.bjid.2018.06.001CrossRefGoogle ScholarPubMed
Freedman, DO and Ottesen, EA (1988) Eggs of Schistosoma mansoni stimulate endothelial cell proliferation in vitro. Journal of Infectious Diseases 158(3), 556562. https://doi.org/10.1093/infdis/158.3.556CrossRefGoogle ScholarPubMed
Gasim, GI, Bella, A, and Adam, I (2015) Schistosomiasis, hepatitis B and hepatitis C co-infection. Virology Journal 12, 19. https://doi.org/10.1186/s12985-015-0251-2CrossRefGoogle ScholarPubMed
Haeberlein, S, Obieglo, K, Ozir-Fazalalikhan, A, Chay, MAM, Veninga, H, van der Vlugt, LEPM, Voskamp, A, Boon, L, den Haan, JMM, Westerhof, LB, Wilbers, RHP, Schots, A, Schramm, G, Hokke, CH, and Smits, HH (2017) Schistosome egg antigens, including the glycoprotein IPSE/alpha-1, trigger the development of regulatory B cells. PLoS Pathogens 13(7), e1006539. https://doi.org/10.1371/journal.ppat.1006539CrossRefGoogle ScholarPubMed
Halim, AB, Garry, RF, Dash, S, and Gerber, MA (1999) Effect of schistosomiasis and hepatitis on liver disease. American Journal of Tropical Medicine and Hygiene 60(6), 915920. https://doi.org/10.4269/ajtmh.1999.60.915CrossRefGoogle ScholarPubMed
Herrera, LA, Benítez-Bribiesca, L, Mohar, A, and Ostrosky-Wegman, P (2005) Role of infectious diseases in human carcinogenesis. Environmental and Molecular Mutagenesis 45(2–3), 284303. https://doi.org/10.1002/em.20122CrossRefGoogle ScholarPubMed
Hiatt, RA, Sotomayor, ZR, Sanchez, G, Zambrana, M, and Knight, WB (1979) Factors in the pathogenesis of acute schistosomiasis mansoni. Journal of Infectious Diseases 139(6), 659666. https://doi.org/10.1093/infdis/139.6.659CrossRefGoogle ScholarPubMed
Hoffmann, KF, Cheever, AW, and Wynn, TA (2000) IL-10 and the dangers of immune polarization: Excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. Journal of Immunology 164(12), 64066416. https://doi.org/10.4049/jimmunol.164.12.6406CrossRefGoogle ScholarPubMed
IARC (1994) Infection with schistosomes (Schistosoma haematobium, Schistosoma mansoni and Schistosoma japonicum). IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 61, 45119.Google Scholar
IARC. Revised preamble for the IARC monographs. Available at https://monographs.iarc.who.int/wp-content/uploads/2019/07/2019-SR-001-Revised_Preamble.pdf (accessed February 17, 2024).Google Scholar
Jain, D, Chaudhary, P, Varshney, N, Bin Razzak, KS, Verma, D, Khan Zahra, TR, Janmeda, P, Sharifi-Rad, J, Daştan, SD, Mahmud, S, Docea, AO, and Calina, D (2021) Tobacco smoking and liver cancer risk: Potential avenues for carcinogenesis. Journal of Oncology 2021, 5905357. https://doi.org/10.1155/2021/5905357Google ScholarPubMed
Jain, S and Kumar, S (2020) Cancer immunotherapy: Dawn of the death of cancer? International Reviews of Immunology, 118. Advance online publication. https://doi.org/10.1080/08830185.2020.1775827CrossRefGoogle Scholar
Jain, S and Rana, M (2024) From the discovery of helminths to the discovery of their carcinogenic potential. Parasitology Research 123(1), 47. https://doi.org/10.1007/s00436-023-08022-yCrossRefGoogle Scholar
Jain, S, Rana, M, Choubey, P, and Kumar, S (2023) Schistosoma japonicum associated colorectal cancer and its management. Acta Parasitologica 68(4), 723734. https://doi.org/10.1007/s11686-023-00707-9CrossRefGoogle ScholarPubMed
Jain, S, Sengupta, M, and Jain, P (2019) Non-viral parasites associated with carcinogenesis. Cancer Investigation 37(9), 453462. https://doi.org/10.1080/07357907.2019.1662918CrossRefGoogle ScholarPubMed
Kakizoe, Y (1985) The influence of Schistosoma mansoni infection on carcinogenesis of mouse livers initiated by N-2-fluorenylacetamide. Kurume Medical Journal 32(3), 169178. https://doi.org/10.2739/kurumemedj.32.169CrossRefGoogle ScholarPubMed
Kamdem, SD, Moyou-Somo, R, Brombacher, F, and Nono, JK (2018) Host regulators of liver fibrosis during human schistosomiasis. Frontiers in Immunology 9, 2781. https://doi.org/10.3389/fimmu.2018.02781CrossRefGoogle ScholarPubMed
Khatami, A, Bahadory, S, Ghorbani, S, Saadati, H, Zarei, M, Soleimani, A, and Zibaei, M (2021) Two rivals or colleagues in the liver? Hepatit B virus and Schistosoma mansoni co-infections: A systematic review and meta-analysis. Microbial Pathogenesis 154, 104828. https://doi.org/10.1016/j.micpath.2021.104828CrossRefGoogle ScholarPubMed
Li, D, He, L, Guo, H, Chen, H, and Shan, H (2015) Targeting activated hepatic stellate cells (aHSCs) for liver fibrosis imaging. EJNMMI Research 5(1), 71. https://doi.org/10.1186/s13550-015-0151-xCrossRefGoogle ScholarPubMed
Liu, T, Zhang, L, Joo, D, and Sun, SC (2017) NF-κB signaling in inflammation. Signal Transduction and Targeted Therapy 2, 19. https://doi.org/10.1038/sigtrans.2017.23CrossRefGoogle ScholarPubMed
Liu, Z, Zhang, L, Liang, Y, and Lu, L (2022) Pathology and molecular mechanisms of Schistosoma japonicum-associated liver fibrosis. Frontiers in Cellular and Infection Microbiology 12, 1035765. https://doi.org/10.3389/fcimb.2022.1035765CrossRefGoogle ScholarPubMed
Lodish, H, Berk, A, Zipursky, SL, Matsudira, P, Baltimore, D, and Darnell, JE (2003) Molecular Cell Biology, 5th edn. New York; W. H. Freeman,Google Scholar
Loeffler, DA, Lundy, SK, Singh, KP, Gerard, HC, Hudson, AP, and Boros, DL (2002) Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelial cells. Journal of Infectious Diseases 185(11), 16501656. https://doi.org/10.1086/340416CrossRefGoogle ScholarPubMed
Lurje, I, Hammerich, L, and Tacke, F (2020) Dendritic cell and T cell crosstalk in liver fibrogenesis andhHepatocarcinogenesis: Implications for prevention and therapy of liver cancer. International Journal of Molecular Sciences 21(19), 7378. https://doi.org/10.3390/ijms21197378CrossRefGoogle Scholar
Matsushita, H and Takaki, A (2019) Alcohol and hepatocellular carcinoma. BMJ Open Gastroenterology 6(1), e000260. https://doi.org/10.1136/bmjgast-2018-000260CrossRefGoogle ScholarPubMed
Michielsen, PP, Francque, SM, and van Dongen, JL (2005) Viral hepatitis and hepatocellular carcinoma. World Journal of Surgical Oncology 3, 27. https://doi.org/10.1186/1477-7819-3-27CrossRefGoogle ScholarPubMed
Morais, CNL de, Souza, JR de, Melo, WG, Aroucha, ML, Miranda, P, Domingues, ALC, Abath, FGC, and Montenegro, SML (2008) Cytokine profile associated with chronic and acute human schistosomiasis mansoni. Memórias Do Instituto Oswaldo Cruz 103(6), 561568. https://doi.org/10.1590/S0074-02762008000600009CrossRefGoogle ScholarPubMed
Morgan, TR, Mandayam, S, and Jamal, MM (2004) Alcohol and hepatocellular carcinoma. Gastroenterology 127(5 Suppl 1), S87S96. https://doi.org/10.1053/j.gastro.2004.09.020CrossRefGoogle ScholarPubMed
Mott, KE (1978) Possible relationship of Schistosoma infection and liver carcinoma. Royal Society of Tropical Medicine and Hygiene 72(5), 552553. https://doi.org/10.1016/0035-9203(78)90191-8CrossRefGoogle ScholarPubMed
Ng, J and Wu, J (2012) Hepatitis B- and hepatitis C-related hepatocellular carcinomas in the United States: Similarities and differences. Hepatitis Monthly 12(10 HCC), e7635. https://doi.org/10.5812/hepatmon.7635CrossRefGoogle ScholarPubMed
NIH (2022) National Cancer Institute- study identifies potential drug target to prevent some liver cancers. Available at https://www.cancer.gov/news-events/cancer-currents-blog/2022/spectrin-fatty-liver-disease-liver-cancer#:~:text=In%20people%20with%20NASH%2C%20a,with%20NASH%20often%20develop%20HCC (accessed July 15, 2024).Google Scholar
Nono, JK, Ndlovu, H, Aziz, NA, Mpotje, T, Hlaka, L, and Brombacher, F (2017) Host regulation of liver fibroproliferative pathology during experimental schistosomiasis via interleukin-4 receptor alpha. PLoS Neglected Tropical Diseases 11(8), e0005861. https://doi.org/10.1371/journal.pntd.0005861CrossRefGoogle ScholarPubMed
Omar, HH (2019) Impact of chronic schistosomiasis and HBV/HCV co-infection on the liver: Current perspectives. Hepatic Medicine: Evidence and Research 11, 131136. https://doi.org/10.2147/HMER.S155962CrossRefGoogle ScholarPubMed
Pearce, EJ, Caspar, P, Grzych, JM, Lewis, FA, and Sher, A (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. Journal of Experimental Medicine 173(1), 159166. https://doi.org/10.1084/jem.173.1.159CrossRefGoogle ScholarPubMed
Pereira, FEL and Goncalves, CS (1984) The association of Schistosoma mansoni infection with hepatocellular carcinoma. Revista da Sociedade Brasileira de Medicina Tropical 17, 7376.CrossRefGoogle Scholar
Pinter, M, Trauner, M, Peck-Radosavljevic, M, and Sieghar, W (2016) Cancer and liver cirrhosis: Implications on prognosis and management. ESMO Open 1(2), e000042. https://doi.org/10.1136/esmoopen-2016-000042CrossRefGoogle Scholar
Plentz, RR, Caselitz, M, Bleck, JS, Gebel, M, Flemming, P, Kubicka, S, Manns, MP, and Rudolph, KL (2004) Hepatocellular telomere shortening correlates with chromosomal instability and the development of human hepatoma. Hepatology 40(1), 8086. https://doi.org/10.1002/hep.20271CrossRefGoogle ScholarPubMed
Puche, JE, Saiman, Y, and Friedman, SL (2013) Hepatic stellate cells and liver fibrosis. Comprehensive Physiology 3(4), 14731492. https://doi.org/10.1002/cphy.c120035CrossRefGoogle ScholarPubMed
Roberts, L, Janovy, J, and Nadler, S (2012) Foundations of Parasitology. Boston, USA: McGraw-Hill.Google Scholar
Roderfeld, M, Padem, S, Lichtenberger, J, Quack, T, Weiskirchen, R, Longerich, T, Schramm, G, Churin, Y, Irungbam, K, Tschuschner, A, Windhorst, A, Grevelding, CG, and Roeb, E (2020) Schistosoma mansoni egg-secreted antigens activate hepatocellular carcinoma-associated transcription factors c-Jun and STAT3 in hamster and human hepatocytes. Hepatology 72(2), 626641. https://doi.org/10.1002/hep.30192CrossRefGoogle ScholarPubMed
Shaker, Y, Samy, N, and Ashour, E (2014) Hepatobiliary Schistosomiasis. Journal of Clinical and Translational Hepatology 2(3), 212216. https://doi.org/10.14218/JCTH.2014.00018Google ScholarPubMed
Shao, Y, Lo, CM, Ling, CC, Liu, XB, Ng, KT, Chu, AC, Ma, YY, Li, CX, Fan, ST, and Man, K (2014) Regulatory B cells accelerate hepatocellular carcinoma progression via CD40/CD154 signaling pathway. Cancer Letters 355(2), 264272. https://doi.org/10.1016/j.canlet.2014.09.026CrossRefGoogle ScholarPubMed
Shin, HK, Park, JH, Yu, JH, Jin, YJ, Suh, YJ, Lee, JW, Kim, W, and Korean Nonalcoholic Fatty Liver Study Group (KNSG) (2021) Association between telomere length and hepatic fibrosis in non-alcoholic fatty liver disease. Scientific Reports 11(1), 18004. https://doi.org/10.1038/s41598-021-97385-2CrossRefGoogle ScholarPubMed
Shousha, HI, Abdelaziz, AO, Nabeel, MM, Omran, DA, Abdelmaksoud, AH, Elbaz, TM, Salah, A, Harb, STE, Hosny, KA, Osman, A, Atef, M, Gaber, A, Zayed, NA, Yosry, AA, and Leithy, R (2022) Schistosoma mansoni infection and the occurrence, characteristics, and survival of patients with hepatocellular carcinoma: An observational study over a decade. Pathogens and Global Health 116(2), 119127. https://doi.org/10.1080/20477724.2021.1975081CrossRefGoogle ScholarPubMed
Smith, P, Walsh, CM, Mangan, NE, Fallon, RE, Sayers, JR, McKenzie, AN, and Fallon, PG (2004) Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. Journal of Immunology 173(2), 12401248. https://doi.org/10.4049/jimmunol.173.2.1240CrossRefGoogle ScholarPubMed
Stadecker, MJ (1999) The development of granulomas in schistosomiasis: Genetic backgrounds, regulatory pathways, and specific egg antigen responses that influence the magnitude of disease. Microbes and Infection 1(7), 505510. https://doi.org/10.1016/s1286-4579(99)80089-6CrossRefGoogle ScholarPubMed
Sung, H, Ferlay, J, Siegel, RL, Laversanne, M, Soerjomataram, I, Jemal, A, and Bray, F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians 71(3), 209249. https://doi.org/10.3322/caac.21660Google ScholarPubMed
Toda, KS, Kikuchi, L, Chagas, AL, Tanigawa, RY, Paranaguá-Vezozzo, DC, Pfiffer, T, MdeS, Rocha, Alves, VA, and Carrilho, FJ (2015) Hepatocellular carcinoma related to Schistosoma mansoni infection: Case series and literature review. Journal of Clinical and Translational Hepatology 3(4), 260264. https://doi.org/10.14218/JCTH.2015.00027Google ScholarPubMed
von Bülow, V, Lichtenberger, J, Grevelding, CG, Falcone, FH, Roeb, E, and Roderfeld, M (2021) Does Schistosoma Mansoni facilitate carcinogenesis? Cells 10(8), 1982. https://doi.org/10.3390/cells10081982CrossRefGoogle ScholarPubMed
von Bülow, V, Schneider, M, Dreizler, D, Russ, L, Baier, A, Buss, N, Lichtenberger, J, Härle, L, Müller, H, Tschuschner, A, Schramm, G, Pons-Kühnemann, J, Grevelding, CG, Roeb, E, and Roderfeld, M (2024) Schistosoma mansoni-induced oxidative stress triggers hepatocellular proliferation. Cellular and Molecular Gastroenterology and Hepatology 17(1), 107117. https://doi.org/10.1016/j.jcmgh.2023.08.014CrossRefGoogle ScholarPubMed
Wang, Z, Li, Z, Ye, Y, Xie, L, and Li, W (2016) Oxidative stress and liver cancer: Etiology and therapeutic targets. Oxidative Medicine and Cellular Longevity 2016, 7891574. https://doi.org/10.1155/2016/7891574CrossRefGoogle ScholarPubMed
Wiest, PM, Wu, G, Zhong, S, McGarvey, ST, Tan, E, Yuan, J, Peters, P, Olveda, RM, and Olds, GR (1993) Schistosomiasis japonica on Jishan Island, Jiangxi Province, People’s Republic of China: Persistence of hepatic fibrosis after reduction of the prevalence of infection with age. Transactions of the Royal Society of Tropical Medicine and Hygiene 87(3), 290294. https://doi.org/10.1016/0035-9203(93)90133-bCrossRefGoogle ScholarPubMed
Wynn, TA (2008) Cellular and molecular mechanisms of fibrosis. Journal of Pathology 214(2), 199210. https://doi.org/10.1002/path.2277CrossRefGoogle ScholarPubMed
Xu, R and Hajdu, CH (2008) Wilson disease and hepatocellular carcinoma. Gastroenterology & Hepatology 4(6), 438439.Google ScholarPubMed
Zhang, CY, Yuan, WG, He, P, Lei, JH, and Wang, CX (2016) Liver fibrosis and hepatic stellate cells: Etiology, pathological hallmarks and therapeutic targets. World Journal of Gastroenterology 22(48), 1051210522. https://doi.org/10.3748/wjg.v22.i48.10512CrossRefGoogle ScholarPubMed
Zheng, B, Zhang, J, Chen, H, Nie, H, Miller, H, Gong, Q, and Liu, C (2020) T lymphocyte-mediated liver immunopathology of Schistosomiasis. Frontiers in Immunology 11, 61. https://doi.org/10.3389/fimmu.2020.00061CrossRefGoogle ScholarPubMed
Zhong, H, Gui, X, Hou, L, Lv, R, and Jin, Y (2022) From inflammation to fibrosis: Novel insights into the roles of high mobility group protein box 1 in schistosome-induced liver damage. Pathogens 11(3), 289. https://doi.org/10.3390/pathogens11030289CrossRefGoogle ScholarPubMed