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Can Schistosoma japonicum infection cause liver cancer?

Published online by Cambridge University Press:  10 February 2025

S. Jain Open the ORCID record for S. Jain [Opens in a new window]
S. Jain*
Affiliation:
Independent Researcher, Institute for Globally Distributed Open Research and Education (IGDORE), Rewari, Haryana, India
*
Corresponding author: S. Jain; Email: [email protected]
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Abstract

A co-relation between Schistosoma japonicum (Sj) and liver cancer (LC) in humans has been reported in the literature; however, this association is circumstantial. Due to the inconclusive nature of this association, the International Agency for Research on Cancer has placed Sj in Group 2B for LC, signifying it to be a ‘possible carcinogen’. Many epidemiological, pathological and clinical studies have identified multiple factors, linked with Sj infection, which can lead to liver carcinogenesis. These factors include chronic inflammation in response to deposited eggs (which leads to fibrosis, cirrhosis and chromosomal instability at cellular level), hepatotoxic effects of egg-antigens, co-infection with hepatitis viruses, and up-regulation of glycolysis linked genes among others which predisposes hepatic tissue towards malignant transformation. The objective of this work is to present the current understanding on the association of Sj infection with LC. Mechanisms and factors linked with Sj infection that can lead to LC are emphasized, along with measures to diagnose and treat it. A comparison of liver carcinogenesis is also provided for cases linked with and independent of Sj infection. It appears that Sj, alone or with another carcinogen, is an important factor in liver carcinogenesis, but further studies are warranted to conclusively label ‘infection with Sj alone’ as a liver carcinogen.

Keywords

Schistosoma japonicumliver cancerinflammationcirrhosisgranuloma
Type
Review Article
Information
Journal of Helminthology , Volume 99 , 2025 , e11
Copyright
© The Author(s), 2025. Published by Cambridge University Press

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References

Abruzzi, A, Fried, B and Alikhan, SB (2016) Coinfection of Schistosoma species with hepatitis B or hepatitis C viruses. Advances in Parasitology 91, 111–231. https://doi.org/10.1016/bs.apar.2015.12.003CrossRefGoogle ScholarPubMed
Ahmed, K, Safdar, K, Kemmer, N, Atiq, M, Wang, J and Neff, GW (2007) Intestinal schistosomiasis following orthotopic liver transplantation: a case report. Transplantation Proceedings 39(10), 3502–3504. https://doi.org/10.1016/j.transproceed.2007.07.093CrossRefGoogle ScholarPubMed
Andrade, ZA and Santana, TS (2010) Angiogenesis and schistosomiasis. Memorias do Instituto Oswaldo Cruz 105(4), 436–439. https://doi.org/10.1590/s0074-02762010000400013CrossRefGoogle ScholarPubMed
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), 11–15. https://doi.org/10.5009/gnl18081CrossRefGoogle Scholar
Bataller, R and Brenne, DA (2005) Liver fibrosis. The Journal of Clinical Investigation 115(2), 209–218. https://doi.org/10.1172/JCI24282CrossRefGoogle ScholarPubMed
Bialecki, ES and Di Bisceglie, AM (2005) Diagnosis of hepatocellular carcinoma. HPB 7(1), 26–34. https://doi.org/10.1080/13651820410024049CrossRefGoogle 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 73(2), 252–258.Google ScholarPubMed
Butrous, G (2019) Schistosome infection and its effect on pulmonary circulation. Glob Cardiol Sci Pract 2019(1), 5. doi: 10.21542/gcsp.2019.5.Google ScholarPubMed
Campbell, SJ, Biritwum, NK, Woods, G, Velleman, Y, Fleming, F and Stothard, JR (2018) Tailoring water, sanitation, and hygiene (WASH) targets for soil-transmitted helminthiasis and schistosomiasis control. Trends in Parasitology 34(1), 53–63. https://doi.org/10.1016/j.pt.2017.09.004CrossRefGoogle ScholarPubMed
CDC (2024) Schistosomiasis. https://www.cdc.gov/dpdx/schistosomiasis/index.html. Accessed November 21, 2024.Google Scholar
Chami, P, Jarnagin, W, Abou-Alfa, GK, Harding, J, Kim, N, Lin, H, El Homsi, M, Crane, C and Hajj, C (2023) Non-surgical locoregional therapies alone or in combination with systemic therapy in patients with hepatocellular carcinoma. Cancers 15(6), 1748. https://doi.org/10.3390/cancers15061748CrossRefGoogle ScholarPubMed
Chang, YC, Chan, MH, Yang, YF, Li, CH and Hsiao, M (2023) Glucose transporter 4: insulin response mastermind, glycolysis catalyst and treatment direction for cancer progression. Cancer Letters 563, 216179. https://doi.org/10.1016/j.canlet.2023.216179CrossRefGoogle ScholarPubMed
Chen, HZ, Chuang, SC, Hsieh, FC, Lin, LJ, Hung, RM and Lee, KT (2007) Diagnosis of Schistosomiasis japonica infection coincident with hepatocellular carcinoma by fine-needle aspiration. Diagnostic Cytopathology 35(11), 722–724. https://doi.org/10.1002/dc.20725CrossRefGoogle ScholarPubMed
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):141–150. doi: 10.1016/j.pt.2013.12.009CrossRefGoogle ScholarPubMed
Chuah, C, Jones, MK, Burke, ML, Owen, HC, Anthony, BJ, McManus, DP, Ramm, GA and Gobert, GN (2013) Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils. Journal of Leukocyte Biology 94(2), 353–365. https://doi.org/10.1189/jlb.1212653CrossRefGoogle ScholarPubMed
Colley, DG, Bustinduy, AL, Secor, WE and King, CH (2014) Human schistosomiasis. Lancet 383(9936), 2253–2264. https://doi.org/10.1016/S0140-6736(13)61949-2CrossRefGoogle ScholarPubMed
Cooper, GM and Hausman, RE (2007) The cell-a molecular approach. Sinauer Associates, USA: SunderlandGoogle Scholar
Coutinho, HM, McGarvey, 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. The Journal of Infectious Diseases 192(3), 528–536. https://doi.org/10.1086/430929CrossRefGoogle Scholar
Culver, EL, Watkins, J and Westbrook, RH (2016) Granulomas of the liver. Clinical Liver Disease 7(4), 92–96. 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), 9–17. https://doi.org/10.4103/ijmr.IJMR_1456_17CrossRefGoogle ScholarPubMed
Dhar, D, Baglieri, J, Kisseleva, T and Brenner, DA (2020) Mechanisms of liver fibrosis and its role in liver cancer. Experimental Biology and Medicine (Maywood, N.J.) 245(2), 96–108. https://doi.org/10.1177/1535370219898141CrossRefGoogle 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
Dou, Q, Grant, AK, Callahan, C, de Souza, P, Mwin, D, Booth, AL, Nasser, I, Moussa, M, Ahmed, M and Tsai, LL (2023) PFKFB3-mediated pro-glycolytic shift in hepatocellular carcinoma proliferation. Cellular and Molecular Gastroenterology and Hepatology 15(1), 61–75. https://doi.org/10.1016/j.jcmgh.2022.09.009CrossRefGoogle ScholarPubMed
Elbaz, T and Esmat, G (2013) Hepatic and intestinal schistosomiasis: review. Journal of Advanced Research 4(5), 445–452. https://doi.org/10.1016/j.jare.2012.12.001CrossRefGoogle 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), 1733–1741. https://doi.org/10.1053/j.gastro.2003.09.035CrossRefGoogle ScholarPubMed
Feng, Y, Xiong, Y, Qiao, T, Li, X, Jia, L and Han, Y (2018) Lactate dehydrogenase A: a key player in carcinogenesis and potential target in cancer therapy. Cancer Medicine, 7(12), 6124–6136. https://doi.org/10.1002/cam4.1820CrossRefGoogle 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
Gui, QF, Jin, HL, Zhu, F, Lu, HF, Zhang, Q, Xu, J, Yang, YM and Xiao, C (2021) Gut microbiota signatures in Schistosoma japonicum infection-induced liver cirrhosis patients: a case-control study. Infectious Diseases of Poverty, 10(1), 43. https://doi.org/10.1186/s40249-021-00821-8CrossRefGoogle ScholarPubMed
Hamid, AS, Tesfamariam, IG, Zhang, Y and Zhang, ZG (2013) Aflatoxin B1-induced hepatocellular carcinoma in developing countries: geographical distribution, mechanism of action and prevention. Oncology Letters 5(4), 1087–1092. https://doi.org/10.3892/ol.2013.1169CrossRefGoogle 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), 284–303. https://doi.org/10.1002/em.20122CrossRefGoogle ScholarPubMed
Hirata, M, Hara, T, Kage, M, Fukuma, T and Sendo, F (2002). Neutropenia augments experimentally induced Schistosoma japonicum egg granuloma formation in CBA mice, but not in C57BL/6 mice. Parasite Immunology 24(9-10), 479–488. https://doi.org/10.1046/j.1365-3024.2002.00491.xCrossRefGoogle 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 (Baltimore, Md. : 1950) 164(12), 6406–6416. https://doi.org/10.4049/jimmunol.164.12.6406CrossRefGoogle ScholarPubMed
Hu, C, Zhu, S, Wang, J, Lin, Y, Ma, L, Zhu, L, Jiang, P, Li, Z and Pan, W (2019) Schistosoma japonicum MiRNA-7-5p inhibits the growth and migration of hepatoma cells via cross-species regulation of S-phase kinase-associated protein 2. Frontiers in Oncology 9, 175. https://doi.org/10.3389/fonc.2019.00175CrossRefGoogle ScholarPubMed
Huang, JQ, Tao, R, Li, L, Ma, K, Xu, L, Ai, G, Fan, XX, Jiao, YT and Ning, Q (2014) Involvement of heat shock protein 47 in Schistosoma japonicum-induced hepatic fibrosis in mice. International Journal for Parasitology 44(1), 23–35. https://doi.org/10.1016/j.ijpara.2013.08.009CrossRefGoogle ScholarPubMed
Huang, P, Ma, H, Cao, Y, Zhan, T, Zhang, T, Wang, X, Zhang, Y, Xu, J and Xia, C (2022a) Activation of primary hepatic stellate cells and liver fibrosis induced by targeting TGF-β1/Smad signaling in schistosomiasis in mice. Parasites & Vectors 15(1), 456. https://doi.org/10.1186/s13071-022-05584-1CrossRefGoogle ScholarPubMed
Huang, Y, Xian, L, Liu, Z, We, L, Qin, L, Xiong, Y, H, L, Zho, S, Fu, Q, Li, B and Qin, Y (2022b) AMPKα2/HNF4A/BORIS/GLUT4 pathway promotes hepatocellular carcinoma cell invasion and metastasis in low glucose microenviroment. Biochemical Pharmacology, 203, 115198. https://doi.org/10.1016/j.bcp.2022.115198CrossRefGoogle ScholarPubMed
IARC (1994) Infection with schistosomes (Schistosoma haematobium, Schistosoma mansoni and Schistosoma japonicum). IARC Monogr Eval Carcinog Risks Hum 61, 45–119.Google Scholar
Iida, F, Iida, R, Kamijo, H, Takaso, K, Miyazaki, Y, Funabashi, W, Tsuchiya, K and Matsumoto, Y (1999) Chronic Japanese schistosomiasis and hepatocellular carcinoma: ten years of follow-up in Yamanashi Prefecture, Japan. Bulletin of the World Health Organization 77(7), 573–581.Google ScholarPubMed
Inaba, Y (1984) A cohort study on the causes of death in an endemic area of schistosomiasis japonica in Japan. Annals of the Academy of Medicine, Singapore 13(2), 142–148.Google Scholar
Inaba, Y (1987) Liver cancer in an endemic area of schistosomiasis japonica in Yamanashi Prefecture, Japan. Princess Takamatsu Symposia 18, 211–218.Google Scholar
Inaba, Y, Maruchi, N, Matsuda, M, Yoshihara, N and Yamamoto, S (1984) A case-control study on liver cancer with special emphasis on the possible aetiological role of schistosomiasis. International Journal of Epidemiology 13(4), 408–412. https://doi.org/10.1093/ije/13.4.408CrossRefGoogle ScholarPubMed
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/10.1155/2021/5905357CrossRefGoogle Scholar
Jain, S (2024) Is Schistosoma mansoni playing a part in liver carcinogenesis? Journal of Helminthology 98, e61. https://doi.org/10.1017/S0022149X24000506CrossRefGoogle ScholarPubMed
Jain, S and Kumar, S (2020) Cancer immunotherapy: dawn of the death of cancer?. International Reviews of Immunology 1–18. 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), 723–734. 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), 453–462. https://doi.org/10.1080/07357907.2019.1662918CrossRefGoogle ScholarPubMed
Jiang, P, Wang, J, Zhu, S, Hu, C, Lin, Y and Pan, W (2022) Identification of a Schistosoma japonicum microRNA that suppresses hepatoma cell growth and migration by targeting host FZD4 gene. Frontiers in Cellular and Infection Microbiology 12, 786543. https://doi.org/10.3389/fcimb.2022.786543CrossRefGoogle ScholarPubMed
Johnson, PJ (2005) Non-surgical treatment of hepatocellular carcinoma. HPB 7(1), 50–55. https://doi.org/10.1080/13651820410024076CrossRefGoogle ScholarPubMed
Kamal, SM, Rasenack, JW, Bianchi, L, Al Tawil, A, El Sayed Khalifa, K, Peter, T, Mansour, H, Ezzat, W and Koziel, M (2001) Acute hepatitis C without and with schistosomiasis: correlation with hepatitis C-specific CD4(+) T-cell and cytokine response. Gastroenterology 121(3), 646–656. https://doi.org/10.1053/gast.2001.27024CrossRefGoogle 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
Kojiro, M, Kakizoe, S, Yano, H, Tsumagari, J, Kenmochi, K and Nakashima, T (1986) Hepatocellular carcinoma and schistosomiasis japonica. A clinicopathologic study of 59 autopsy cases of hepatocellular carcinoma associated with chronic schistosomiasis japonica. Acta Pathologica Japonica 36(4), 525–532. https://doi.org/10.1111/j.1440-1827.1986.tb01041.xCrossRefGoogle ScholarPubMed
Koyama, Y, Xu, J, Liu, X and Brenner, DA (2016) New developments on the treatment of liver fibrosis. Digestive Diseases (Basel, Switzerland) 34(5), 589–596. https://doi.org/10.1159/000445269CrossRefGoogle ScholarPubMed
Larouzé, B, Dazza, MC, Gaudebout, C, Habib, M, Elamy, M and Cline, B (1987) Absence of relationship between Schistosoma mansoni and hepatitis B virus infection in the Qalyub Governate, Egypt. Annals of Tropical Medicine and Parasitology 81(4), 373–375. https://doi.org/10.1080/00034983.1987.11812134CrossRefGoogle ScholarPubMed
Levrero, M and Zucman-Rossi, J (2016). Mechanisms of HBV-induced hepatocellular carcinoma. Journal of hepatology 64(1 Suppl), S84–S101. https://doi.org/10.1016/j.jhep.2016.02.021CrossRefGoogle 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
Li, QF, Li, YX, Yang, YY, Dong, PP, Mei, CJ, Lu, JL, … Yang, K (2023) The egg ribonuclease SjCP1412 accelerates liver fibrosis caused by Schistosoma japonicum infection involving damage associated molecular patterns (DAMPs). Parasitology 1–36. doi:10.1017/S0031182023001361CrossRefGoogle Scholar
Li, TE, Wang, S, Shen, XT, Zhang, Z, Chen, M, Wang, H, Zhu, Y, Xu, D, Hu, BY, Wei, R, Zheng, Y, Dong, QZ and Qin, LX (2020) PKM2 drives hepatocellular carcinoma progression by inducing immunosuppressive microenvironment. Frontiers in Immunology 11, 589997. https://doi.org/10.3389/fimmu.2020.589997CrossRefGoogle ScholarPubMed
Li, Y, Yu, Y, Yang, L and Wang, R (2023) Insights into the role of oxidative stress in hepatocellular carcinoma development. Frontiers in Bioscience (Landmark edition) 28(11), 286. https://doi.org/10.31083/j.fbl2811286CrossRefGoogle ScholarPubMed
Liu, XF, Ju, S, Wang, KY, Li, Y and Qiang, JW (2023). The prevalence rate, mortality, and 5-year overall survival of Schistosoma japonicum patients with human malignancy. Frontiers in Oncology 13, 1288197. https://doi.org/10.3389/fonc.2023.1288197CrossRefGoogle 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
Llanwarne, F and Helmby, H (2021). Granuloma formation and tissue pathology in Schistosoma japonicum versus Schistosoma mansoni infections. Parasite Immunology 43(2), e12778. https://doi.org/10.1111/pim.12778CrossRefGoogle ScholarPubMed
Lodish, H, Berk, A, Zipursky, SL, Matsudira, P, Baltimore, D and Darnell, JE (2003) Molecular cell biology, 5th edn. W. H. Freeman, New York.Google Scholar
Marchese, V, Beltrame, A, Angheben, A, Marocco, S, Gaeta, GB and Bisoffi, Z (2020) The impact of schistosomiasis co-infection in the presentation of viral hepatitis B in migrants: an observational study in non-endemic area. Travel Medicine and Infectious Disease 35, 101467. https://doi.org/10.1016/j.tmaid.2019.101467CrossRefGoogle ScholarPubMed
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
McManus, DP, Dunne, DW, Sacko, M, Utzinger, J, Vennervald, BJ and Zhou, XN (2018) Schistosomiasis. Nature Reviews 4(1), 13. https://doi.org/10.1038/s41572-018-0013-8Google ScholarPubMed
Mejias, M, Gallego, J, Naranjo-Suarez, S, Ramirez, M, Pell, N, Manzano, A, Suñer, C, Bartrons, R, Mendez, R and Fernandez, M (2020) CPEB4 increases expression of PFKFB3 to induce glycolysis and activate mouse and human hepatic stellate cells, promoting liver fibrosis. Gastroenterology 159(1), 273–288. https://doi.org/10.1053/j.gastro.2020.03.008CrossRefGoogle ScholarPubMed
Molehin, AJ (2020) Schistosomiasis vaccine development: update on human clinical trials. Journal of Biomedical Science 27(1), 28. https://doi.org/10.1186/s12929-020-0621-yCrossRefGoogle ScholarPubMed
Molehin, AJ, McManus, DP and You, H (2022) Vaccines for human schistosomiasis: recent progress, new developments and future prospects. International Journal of Molecular Sciences 23(4), 2255. https://doi.org/10.3390/ijms23042255CrossRefGoogle ScholarPubMed
Morais, CN, Souza, JR, Melo, WG, Aroucha, ML, Miranda, P, Domingues, AL, Abath, FG and Montenegro, SM (2008). Cytokine profile associated with chronic and acute human schistosomiasis mansoni. Memorias do Instituto Oswaldo Cruz 103(6), 561–568. 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), S87–S96. https://doi.org/10.1053/j.gastro.2004.09.020CrossRefGoogle ScholarPubMed
Nakashima, T, Okuda, K, Kojiro, M, Sakamoto, K and Kubo, Y (1975) Primary liver cancer coincident with Schistosomiasis japonica. A study of 24 necropsies. Cancer 36(4), 1483–1489. https://doi.org/10.1002/1097-0142(197510)36:4%3C1483::AID-CNCR2820360441%3E3.0.CO;2-93.0.CO;2-9>CrossRefGoogle 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. (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.)Google Scholar
Ningarhari, M, Caruso, S, Hirsch, TZ, Bayard, Q, Franconi, A, Védie, AL, Noblet, B, Blanc, JF, Amaddeo, G, Ganne, N, Ziol, M, Paradis, V, Guettier, C, Calderaro, J, Morcrette, G, Kim, Y, MacLeod, AR, Nault, JC, Rebouissou, S and Zucman-Rossi, J (2021) Telomere length is key to hepatocellular carcinoma diversity and telomerase addiction is an actionable therapeutic target. Journal of Hepatology 74(5), 1155–1166. https://doi.org/10.1016/j.jhep.2020.11.052CrossRefGoogle Scholar
Oliphant, CJ, Barlow, JL and McKenzie, AN (2011) Insights into the initiation of type 2 immune responses. Immunology 134(4), 378–385. https://doi.org/10.1111/j.1365-2567.2011.03499.xCrossRefGoogle ScholarPubMed
Omar, HH (2019) Impact of chronic schistosomiasis and HBV/HCV co-infection on the liver: current perspectives. Hepat Med 11, 131–136. https://doi.org/10.2147/HMER.S155962CrossRefGoogle ScholarPubMed
Peng, C, Stewart, AG, Woodman, OL, Ritchie, RH and Qin, CX (2020) Non-alcoholic steatohepatitis: a review of its mechanism, models and medical treatments. Frontiers in Pharmacology 11, 603926. https://doi.org/10.3389/fphar.2020.603926CrossRefGoogle ScholarPubMed
Pierce, RJ, Dubois-Abdesselem, F, Caby, S, Trolet, J, Lancelot, J, Oger, F, Bertheaume, N and Roger, E (2011) Chromatin regulation in schistosomes and histone modifying enzymes as drug targets. Memorias do Instituto Oswaldo Cruz 106(7), 794–801. https://doi.org/10.1590/s0074-02762011000700003CrossRefGoogle ScholarPubMed
Pierce, RJ, Dubois-Abdesselem, F, Lancelot, J, Andrade, L and Oliveira, G (2012) Targeting schistosome histone modifying enzymes for drug development. Current Pharmaceutical Design 18(24), 3567–3578.Google ScholarPubMed
Pinter, M, Trauner, M, Peck-Radosavljevic, M and Sieghart, 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 (Baltimore, Md.) 40(1), 80–86. 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), 1473–1492. https://doi.org/10.1002/cphy.c120035CrossRefGoogle ScholarPubMed
Qiu, DC, Hubbard, AE, Zhong, B, Zhang, Y and Spear, RC (2005) A matched, case-control study of the association between Schistosoma japonicum and liver and colon cancers, in rural China. Annals of Tropical Medicine and Parasitology 99(1), 47–52. https://doi.org/10.1179/136485905X19883CrossRefGoogle ScholarPubMed
Raza, A and Sood, GK (2014) Hepatocellular carcinoma review: current treatment, and evidence-based medicine. World Journal of Gastroenterology 20(15), 4115–4127. https://doi.org/10.3748/wjg.v20.i15.4115CrossRefGoogle ScholarPubMed
Rho, H, Terry, AR, Chronis, C and Hay, N (2023) Hexokinase 2-mediated gene expression via histone lactylation is required for hepatic stellate cell activation and liver fibrosis. Cell Metabolism 35(8), 1406–1423. e8. https://doi.org/10.1016/j.cmet.2023.06.013CrossRefGoogle ScholarPubMed
Roberts, L, Janovy, J and Nadler, S (2012) Foundations of parasitology. McGraw-Hill Education, USAGoogle Scholar
Rudge, JW, Carabin, H, Balolong, E, Tallo, V, Shrivastava, J, Lu, DB, Basáñez, MG, Olveda, R, McGarvey, ST and Webster, JP (2008) Population genetics of Schistosoma japonicum within the Philippines suggest high levels of transmission between humans and dogs. PLoS Neglected Tropical Diseases 2(11), e340. https://doi.org/10.1371/journal.pntd.0000340CrossRefGoogle ScholarPubMed
Saharti, S, Ding, X, Massarani-Wafai, R and Pambuccian, SE (2018) Fine-needle aspirate of the liver showing coexistence of Schistosoma japonicum ova and hepatocellular carcinoma. Diagnostic Cytopathology 46(8), 716–720. https://doi.org/10.1002/dc.23969CrossRefGoogle ScholarPubMed
Santos, LL, Santos, J, Gouveia, MJ, Bernardo, C, Lopes, C, Rinaldi, G, Brindley, PJ and Costa, JMCD (2021) Urogenital schistosomiasis-history, pathogenesis, and bladder cancer. Journal of Clinical Medicine 10(2), 205. https://doi.org/10.3390/jcm10020205CrossRefGoogle ScholarPubMed
Serra, M, Di Matteo, M, Serneels, J, Pal, R, Cafarello, ST, Lanza, M, Sanchez-Martin, C, Evert, M, Castegna, A, Calvisi, DF, Mazzone, M and Columbano, A (2022) Deletion of lactate dehydrogenase-a impairs oncogene-induced mouse hepatocellular carcinoma development. Cellular and Molecular Gastroenterology and Hepatology 14(3), 609–624. https://doi.org/10.1016/j.jcmgh.2022.06.003CrossRefGoogle ScholarPubMed
Shang, B, Lu, F, Jiang, S, Xing, M, Mao, X, Yang, G and Zhang, H (2023) ALDOC promotes non-small cell lung cancer through affecting MYC-mediated UBE2N transcription and regulating Wnt/β-catenin pathway. Aging 15(18), 9614–9632. https://doi.org/10.18632/aging.205038CrossRefGoogle ScholarPubMed
Sheng, S, Chen, B, Xu, R, Han, Y, Mao, D, Chen, Y, Li, C, Su, W, Hu, X, Zhao, Q, Lowe, S, Huang, Y, Shao, W and Yao, Y (2024) A prognostic model for Schistosoma japonicum infection-associated liver hepatocellular carcinoma: strengthening the connection through initial biological experiments. Infectious Agents and Cancer 19(1), 10. https://doi.org/10.1186/s13027-024-00569-4CrossRefGoogle 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
Stadecker, MJ, Asahi, H, Finger, E, Hernandez, HJ, Rutitzky, LI and Sun, J (2004) The immunobiology of Th1 polarization in high-pathology schistosomiasis. Immunological Reviews 201, 168–179. https://doi.org/10.1111/j.0105-2896.2004.00197.xCrossRefGoogle 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), 209–249. https://doi.org/10.3322/caac.21660Google ScholarPubMed
Szklaruk, J, Silverman, PM and Charnsangavej, C (2003) Imaging in the diagnosis, staging, treatment, and surveillance of hepatocellular carcinoma. AJR American Journal of Roentgenology 180(2), 441–454. https://doi.org/10.2214/ajr.180.2.1800441CrossRefGoogle ScholarPubMed
Takemura, Y, Kikuchi, S and Inaba, Y (1998) Epidemiologic study of the relationship between schistosomiasis due to Schistosoma japonicum and liver cancer/cirrhosis. The American journal of tropical medicine and hygiene 59(4), 551–556. https://doi.org/10.4269/ajtmh.1998.59.551CrossRefGoogle ScholarPubMed
Tamarozzi, F, Fittipaldo, VA, Orth, HM, Richter, J, Buonfrate, D, Riccardi, N and Gobbi, FG (2021) Diagnosis and clinical management of hepatosplenic schistosomiasis: a scoping review of the literature. PLoS Neglected Tropical Diseases 15(3), e0009191. https://doi.org/10.1371/journal.pntd.0009191CrossRefGoogle ScholarPubMed
Trottein, F, Nutten, S, Angeli, V, Delerive, P, Teissier, E, Capron, A, Staels, B and Capron, M (1999) Schistosoma mansoni schistosomula reduce E-selectin and VCAM-1 expression in TNF-alpha-stimulated lung microvascular endothelial cells by interfering with the NF-kappaB pathway. European Journal of Immunology 29(11), 3691–3701. https://doi.org/10.1002/(SICI)1521-4141(199911)29:11<3691::AID-IMMU3691>3.0.CO;2-L3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Voizard, N, Cerny, M, Assad, A., Billiard, JS, Olivié, D, Perreault, P, Kielar, A, Do, RKG, Yokoo, T, Sirlin, CB and Tang, A (2019) Assessment of hepatocellular carcinoma treatment response with LI-RADS: a pictorial review. Insights Into Imaging 10(1), 121. https://doi.org/10.1186/s13244-019-0801-zCrossRefGoogle 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. doi: 10.3390/cells10081982.CrossRefGoogle ScholarPubMed
Wang, Q, Chou, X, Guan, F, Fang, Z, Lu, S, Lei, J, Li, Y and Liu, W (2017) Enhanced Wnt signalling in hepatocytes is associated with Schistosoma japonicum infection and contributes to liver fibrosis. Scientific Reports 7(1), 230. https://doi.org/10.1038/s41598-017-00377-4CrossRefGoogle ScholarPubMed
Wang, X, Tang, Q, Bergquist, R, Zhou, X and Qin, Z (2023) The cytokine profile in different stages of Schistosomiasis Japonica. Pathogens (Basel, Switzerland) 12(10), 1201. https://doi.org/10.3390/pathogens12101201Google ScholarPubMed
Wang, Y, Fan, X, Lei, N, He, X, Wang, X, Luo, X, Zhang, D and Pan, W (2020) A microRNA derived from Schistosoma japonicum promotes schistosomiasis hepatic fibrosis by targeting host secreted frizzled-related protein 1. Frontiers in Cellular and Infection Microbiology 10, 101. https://doi.org/10.3389/fcimb.2020.00101CrossRefGoogle 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, G R (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), 290–294. https://doi.org/10.1016/0035-9203(93)90133-bCrossRefGoogle ScholarPubMed
Wynn, TA (2008) Cellular and molecular mechanisms of fibrosis. The Journal of Pathology 214(2), 199–210. https://doi.org/10.1002/path.2277CrossRefGoogle ScholarPubMed
Wynn, TA and Cheever, AW (1995) Cytokine regulation of granuloma formation in schistosomiasis. Current Opinions in Immunology 7, 505.CrossRefGoogle ScholarPubMed
Xu, R and Hajdu, CH (2008) Wilson disease and hepatocellular carcinoma. Gastroenterology & Hepatology 4(6), 438–439.Google ScholarPubMed
Xu, ZP, Chang, H, Ni, YY, Li, C, Chen, L, Hou, M and Ji, MJ (2019) Schistosoma japonicum infection causes a reprogramming of glycolipid metabolism in the liver. Parasites & Vectors 12(1), 388. https://doi.org/10.1186/s13071-019-3621-6CrossRefGoogle ScholarPubMed
Ye, XP, Fu, YL, Anderson, RM and Nokes, DJ (1998) Absence of relationship between Schistosoma japonicum and hepatitis B virus infection in the Dongting lake region, China. Epidemiology and Infection 121(1), 193–195. https://doi.org/10.1017/s0950268898008917CrossRefGoogle ScholarPubMed
Yu, DC, Chen, J and Ding, YT (2010).Hypoxic and highly angiogenic non-tumor tissues surrounding hepatocellular carcinoma: the ‘niche’ of endothelial progenitor cells. International Journal of Molecular Sciences 11(8), 2901–2909. https://doi.org/10.3390/ijms11082901CrossRefGoogle ScholarPubMed
Yu, Y, Wang, J, Wang, X, Gu, P, Lei, Z, Tang, R, Wei, C, Xu, L, Wang, C, Chen, Y, Pu, Y, Qi, X, Yu, B, Chen, X, Zhu, J, Li, Y, Zhang, Z, Zhou, S and Su, C (2021) Schistosome eggs stimulate reactive oxygen species production to enhance M2 macrophage differentiation and promote hepatic pathology in schistosomiasis. PLoS Neglected Tropical Diseases 15(8), e0009696. https://doi.org/10.1371/journal.pntd.0009696CrossRefGoogle ScholarPubMed
Yunna, C, Mengru, H, Lei, W and Weidong, C (2020) Macrophage M1/M2 polarization. European Journal of Pharmacology 877, 173090. https://doi.org/10.1016/j.ejphar.2020.173090CrossRefGoogle 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), 10512–10522. https://doi.org/10.3748/wjg.v22.i48.10512CrossRefGoogle ScholarPubMed
Zhang, Y, Xie, Y, Chen, Q, Chen, X, Dong, Z and Tan, X (2020) Prevalence and co-infection of schistosomiasis/hepatitis B among rural populations in endemic areas in Hubei, China. Transactions of the Royal Society of Tropical Medicine and Hygiene 114(3), 155–161. https://doi.org/10.1093/trstmh/trz086CrossRefGoogle ScholarPubMed
Zhao, R, Li, L, Yang, J, Niu, Q, Wang, H, Qin, X, Zhu, N and Shi, A (2020) Overexpression of pyruvate kinase M2 in tumor tissues is associated with poor prognosis in patients with hepatocellular carcinoma. Pathology Oncology Research 26(2), 853–860. https://doi.org/10.1007/s12253-019-00630-3CrossRefGoogle 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
Zhu, D, Yang, C, Shen, P, Chen, L, Chen, J, Sun, X, Duan, L, Zhang, L, Zhu, J and Duan, Y (2018) rSjP40 suppresses hepatic stellate cell activation by promoting microRNA-155 expression and inhibiting STAT5 and FOXO3a expression. Journal of Cellular and Molecular Medicine 22(11), 5486–5493. https://doi.org/10.1111/jcmm.13819CrossRefGoogle ScholarPubMed