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Hepatic Arterioportal Fistula Is Associated with Decreased Future Liver Remnant Regeneration after Stage-I ALPPS for Hepatocellular Carcinoma

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Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background

Hepatocellular carcinoma (HCC) patients often developed hepatic arterioportal fistula (APF). The aim of this study is to evaluate the impact of APF on future liver remnant (FLR) regeneration and surgical outcomes after the first stage of associating liver partition and portal vein ligation for staged hepatectomy (stage-I ALPPS).

Methods

Consecutive HCC patients who underwent ALPPS at our center between March 2017 and May 2019 were retrospectively studied. Data for the association between APF and clinicopathological details, liver volume, and surgical outcomes were analyzed.

Results

The enrolled 35 HCC patients were divided into three groups: 15 patients with preoperative APF were classified as the APF I group, 10 patients developed APF after stage-I ALPPS as the APF II group, whereas the other 10 patients without APF before and after stage-I ALPPS as the control group. After stage-I ALPPS, patients in the APF I and APF II groups had lower kinetic growth rate (KGR) of FLR volume (6.1±3.2%, 11.4±8.4%, 25.0±8.8% per week, respectively, P<0.001) and took longer median time to reach the sufficient FLR volume for stage-II ALPPS (17.5 days, 12 days, 6 days, respectively, P<0.001) than those in the control group. Meanwhile, the incidence of posthepatectomy liver failure (PHLF) in the APF I and APF II groups was significantly higher than that of the control group (P=0.007). There are 27 (77.1%) patients who completed stage-II ALPPS. The overall survival (OS) rates at 1 and 3 years were 59.3% and 35.1%, whereas the disease-free survival (DFS) rates at 1 and 3 years were 44.4% and 22.9%, respectively.

Conclusions

Hepatic APF is significantly associated with decreased FLR regeneration and a higher risk of PHLF after stage-I ALPPS. HCC patients who are to undergo ALPPS may benefit from the timely perioperative intervention of APF.

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References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394-424.

    Article  Google Scholar 

  2. Wong MC, Jiang JY, Goggins WB, Liang M, Fang Y, Fung FD, et al. (2017) International incidence and mortality trends of liver cancer: a global profile. Sci Rep 7:45846.

    Article  CAS  Google Scholar 

  3. Orcutt ST, Anaya DA. (2018) Liver Resection and Surgical Strategies for Management of Primary Liver Cancer. Cancer Control 25:1145179885.

    Article  Google Scholar 

  4. Chan A, Lo CM. (2020). Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS)-pushing the envelope in modulation of future liver remnant before major hepatectomy. Hepatobiliary Surg Nutr, 9:80-82.

    Article  Google Scholar 

  5. Tanaka K, Matsuo K, Murakami T, Kawaguchi D, Hiroshima Y, Koda K, et al. (2015) Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): short-term outcome, functional changes in the future liver remnant, and tumor growth activity. Eur J Surg Oncol 41:506-512.

    Article  CAS  Google Scholar 

  6. Raptis DA, Linecker M, Kambakamba P, Tschuor C, Muller PC, Hadjittofi C, et al. (2019) Defining Benchmark Outcomes for ALPPS. Ann Surg 270:835-841.

    Article  Google Scholar 

  7. Wang Z, Peng Y, Hu J, Wang X, Sun H, Sun J, et al. (2020) Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy for Unresectable Hepatitis B Virus-related Hepatocellular Carcinoma: A Single Center Study of 45 Patients. Ann Surg 271:534-541.

    Article  Google Scholar 

  8. Chan A, Zhang WY, Chok K, Dai J, Ji R, Kwan C, et al. (2019) ALPPS Versus Portal Vein Embolization for Hepatitis-related Hepatocellular Carcinoma: A Changing Paradigm in Modulation of Future Liver Remnant Before Major Hepatectomy. Ann Surg

  9. Peng C, Li C, Liu C, Wen T, Yang J, Li B, et al. (2019) The outcome of the HCC patients underwent ALPPS: Retrospective study. Medicine (Baltimore) 98:e17182.

    Article  Google Scholar 

  10. Cai X, Tong Y, Yu H, Liang X, Wang Y, Liang Y, et al. (2017) The ALPPS in the Treatment of Hepatitis B-Related Hepatocellular Carcinoma With Cirrhosis: A Single-Center Study and Literature Review. Surg Innov 24:358-364.

    Article  Google Scholar 

  11. Abshagen K, Eipel C, Vollmar B. (2012) A critical appraisal of the hemodynamic signal driving liver regeneration. Langenbeck's Arch Surg 397:579-590.

    Article  Google Scholar 

  12. Guzman EA, McCahill LE, Rogers FB. (2006) Arterioportal fistulas: introduction of a novel classification with therapeutic implications. J Gastrointest Surg 10:543-550.

    Article  Google Scholar 

  13. Kanogawa N, Chiba T, Ogasawara S, Ooka Y, Suzuki E, Motoyama T, et al. (2014) Successful interventional treatment for arterioportal fistula caused by radiofrequency ablation for hepatocellular carcinoma. Case Rep Oncol 7:833-839.

    Article  Google Scholar 

  14. Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R, et al. (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149:713-724.

    Article  Google Scholar 

  15. Dindo D, Demartines N, Clavien PA. (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205-213.

    Article  Google Scholar 

  16. Ishak K, Baptista A, Bianchi L, Callea F, De Groote J, Gudat F, et al. (1995) Histological grading and staging of chronic hepatitis. J Hepatol 22:696-699.

    Article  CAS  Google Scholar 

  17. Shi J, Lai EC, Li N, Guo WX, Xue J, Lau WY, et al. (2011) A new classification for hepatocellular carcinoma with portal vein tumor thrombus. J Hepatobiliary Pancreat Sci 18:74-80.

    Article  Google Scholar 

  18. Vauthey JN, Abdalla EK, Doherty DA, Gertsch P, Fenstermacher MJ, Loyer EM, et al. (2002) Body surface area and body weight predict total liver volume in Western adults. Liver Transpl 8:233-240.

    Article  Google Scholar 

  19. Shindoh J, Truty MJ, Aloia TA, Curley SA, Zimmitti G, Huang SY, et al. (2013) Kinetic growth rate after portal vein embolization predicts posthepatectomy outcomes: toward zero liver-related mortality in patients with colorectal liver metastases and small future liver remnant. J Am Coll Surg 216:201-209.

    Article  Google Scholar 

  20. Choi BI, Lee KH, Han JK, Lee JM. (2002) Hepatic arterioportal shunts: dynamic CT and MR features. Korean J Radiol 3:1-15.

    Article  Google Scholar 

  21. Bolognesi M, Sacerdoti D, Bombonato G, Chiesura-Corona M, Merkel C, Gatta A. (2000) Arterioportal fistulas in patients with liver cirrhosis: usefulness of color Doppler US for screening. Radiology 216:738-743.

    Article  CAS  Google Scholar 

  22. Sparrelid E, Johansson H, Gilg S, Nowak G, Ellis E, Isaksson B. (2018) Serial Assessment of Growth Factors Associated with Liver Regeneration in Patients Operated with Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy. Eur Surg Res 59:72-82.

    Article  CAS  Google Scholar 

  23. Gandhi SP, Patel K, Sutariya V, Modi P. (2016) Portal Vein Thrombosis and Arterioportal Fistula in Post Liver Transplant Recipient: A Case Report. J Clin Diagn Res 10:D13-D15.

    Google Scholar 

  24. Han P, Yang L, Huang XW, Zhu XQ, Chen L, Wang N, et al. (2018) A traumatic hepatic artery pseudoaneurysm and arterioportal fistula, with severe diarrhea as the first symptom: A case report and review of the literature. Medicine (Baltimore) 97:e9893.

    Article  Google Scholar 

  25. Vauthey JN, Tomczak RJ, Helmberger T, Gertsch P, Forsmark C, Caridi J, et al. (1997) The arterioportal fistula syndrome: clinicopathologic features, diagnosis, and therapy. Gastroenterology 113:1390-1401.

    Article  CAS  Google Scholar 

  26. Guo WP, Zhang HX, Wang ZM, Wang YQ, Ni DH, Li WX, et al. (2000) DSA analysis of hepatic arteriovenous fistula concurrent with hepatic cancer and its clinical significance. World J Gastroenterol 6:872-876.

    Article  Google Scholar 

  27. Chen JH, Huang CL, Hwang JI, Lee SK, Shen WC. (1999) Dynamic helical biphasic CT emerges as a potential tool for the diagnosis of proximal arterioportal shunting. Hepatogastroenterology 46:1791-1797.

    CAS  PubMed  Google Scholar 

  28. Teplisky D, Tincani EU, Lipsich J, Sierre S. (2012) Congenital arterioportal fistulas: radiological treatment and color Doppler US follow-up. Pediatr Radiol 42:1326-1332.

    Article  Google Scholar 

  29. Okuda K, Musha H, Yamasaki T, Jinnouchi S, Nagasaki Y, Kubo Y, et al. (1977) Angiographic demonstration of intrahepatic arterio-portal anastomoses in hepatocellular carcinoma. Radiology 122:53-58.

    Article  CAS  Google Scholar 

  30. Furuse J, Iwasaki M, Yoshino M, Konishi M, Kawano N, Kinoshita T, et al. (1997) Hepatocellular carcinoma with portal vein tumor thrombus: embolization of arterioportal shunts. Radiology 204:787-790.

    Article  CAS  Google Scholar 

  31. Dong L, Liu W, Zhao X. (2001) [Study of the route of intrahepatic metastasis of primary hepatic carcinoma]. Zhonghua Zhong Liu Za Zhi 23:142-144.

    CAS  PubMed  Google Scholar 

  32. Abshagen K, Eipel C, Kalff JC, Menger MD, Vollmar B. (2008) Kupffer cells are mandatory for adequate liver regeneration by mediating hyperperfusion via modulation of vasoactive proteins. Microcirculation 15:37-47.

    Article  CAS  Google Scholar 

  33. Diaz-Juarez J, Hernandez-Munoz R. (2011) The role of calcium and nitric oxide during liver enzyme release induced by increased physical forces as evidenced in partially hepatectomized rats. Liver Transpl 17:334-343.

    Article  Google Scholar 

  34. White CR, Frangos JA. (2007) The shear stress of it all: the cell membrane and mechanochemical transduction. Philos Trans R Soc Lond Ser B Biol Sci 362:1459-1467.

    Article  CAS  Google Scholar 

  35. Schoen SJ, Lautt WW. (2006) Nitric oxide and prostaglandins potentiate the liver regeneration cascade. Can J Gastroenterol 20:329-334.

    Article  Google Scholar 

  36. Nobuoka T, Mizuguchi T, Oshima H, Shibata T, Kimura Y, Mitaka T, et al. (2006) Portal blood flow regulates volume recovery of the rat liver after partial hepatectomy: molecular evaluation. Eur Surg Res 38:522-532.

    Article  CAS  Google Scholar 

  37. Tomassini F, D'Asseler Y, Giglio MC, Lecluyse C, Lambert B, Sainz-Barriga M, et al. (2019) Hemodynamic changes in ALPPS influence liver regeneration and function: results from a prospective study. HPB (Oxford) 21:557-565.

    Article  Google Scholar 

  38. Wen Zhang, Xu Banghao, Wang Jilong, Ye Chunhui, Lu Kaiyi, Zhang Ling, et al. (2019) Clinical efficacy of hepatic artery ringed and restriction operation-associating liver partition and portal vein ligation for staged hepatectomy in the treatment of giant hepatocellular carcinoma. Chin J Dig Surg18:489-498.

    Google Scholar 

  39. Wang Zheng, Peng Yuanfei, Sun Qiman, Qu Xudong, Tang Min, Dai Yajie, et al. (2017) Salvage transhepatic arterial embolization after failed stage I ALPPS in a patient with a huge HCC with chronic liver disease: A case report. Int J Surg Case Rep 39:131-135.

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Professor Wan Y. Lau (Faculty of Medicine, the Chinese University of Hong Kong, Prince of Wales Hospital, Sha Tin, Honk King, China) for his critical comments and help in revising the article.

Funding

This work was supported by the National Natural Science Foundation of China (No. 81560387, 81902983), the Guangxi Natural Science Foundation of China (No. 2018JJB140382), “Medical Excellence Award” funded by the creative research development grant from the first affiliated hospital of Guangxi Medical University (No. 180327), the Guangxi medical and health technology development and application project (No. S2019097, S2018100), and the project to improve the basic scientific research ability of young and middle-aged teachers of universities and colleges in Guangxi (No. 2019KY0123).

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Author notes

  1. Chunhui Ye and Ling Zhang contributed equally to this work.

Authors and Affiliations

  1. Department of Hepatobiliary Surgery and Liver transplantation, the First Affiliated Hospital of Guangxi Medical University, Shuangrong Raod 6, Nanning, 530021, China

    Chunhui Ye, Banghao Xu, Jian Li, Ya Guo, Minhao Peng, Zhang Wen & Jilong Wang

  2. Department of Radiology, the First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China

    Ling Zhang

  3. Department of Ultrasound, the First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China

    Tingting Lu

  4. Department of Pathology, the First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China

    Jingjing Zeng

  5. Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, 300000, China

    Li Bao

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  1. Chunhui Ye
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Contributions

Mr Ye: data analysis and interpretation and drafting of the manuscript

Dr Zhang: data analysis and interpretation and drafting of the manuscript

Dr Xu: data acquisition and revising of the manuscript

Mr Li: data acquisition, analysis, and interpretation

Dr Lu: data acquisition and analysis

Dr Zeng: data acquisition and analysis

Dr Guo: data acquisition and critical revision of the manuscript

Dr Peng: data acquisition and critical revision of the manuscript

Dr Bao: data analysis and critical revising of the manuscript

Dr Wen: conception and design and revising of the manuscript

Dr Wang: conception and design, data analysis, and interpretation

Corresponding authors

Correspondence to Zhang Wen or Jilong Wang.

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Ye, C., Zhang, L., Xu, B. et al. Hepatic Arterioportal Fistula Is Associated with Decreased Future Liver Remnant Regeneration after Stage-I ALPPS for Hepatocellular Carcinoma. J Gastrointest Surg 25, 2280–2288 (2021). https://doi.org/10.1007/s11605-021-05022-0

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