Abstract
Background and aims
The association between prognosis of variceal bleeding and portal vein thrombosis (PVT) is unclear. In this multicentre study, we determined the effect of PVT on rebleeding and mortality in patients with acute variceal bleeding (AVB) after oesophageal variceal band ligation (EVL).
Methods
Cirrhotic patients with AVB who had undergone EVL were included. The patients were allocated to either the PVT group or the control cirrhotic group (CCG) based on the presence or absence of PVT. One-year rebleeding episodes and mortality after EVL were recorded.
Results
A total of 218 cirrhotic patients with AVB from 3 centres were included. Patients with PVT had a higher rate of 14-day and 6-week rebleeding than those without PVT (14-day: 8.26% vs. 1.83%, p = 0.03; 6-week: 11.92% vs. 1.83%, p = 0.003). The rates of 5-day failure (3.67% vs. 0.92%, p = 0.175), 1-year rebleeding (21.10% vs. 20.18%, p = 0.867), and 14-day, 6-week, and 1-year mortality were similar between the groups (14-day: 3.67% vs. 0.92%, p = 0.175; 6-week: 3.67% vs. 0.92%, p = 0.175; 1-year: 3.67% vs. 1.83%, p = 0.408). The Child–Pugh class [p = 0.022, hazard ratio (HR): 1.453; 95% confidence interval (CI) 1.056–1.998], PVT (p = 0.050, HR: 4.622, 95% CI 0.999–21.395), albumin < 30 g/L (p = 0.023, HR: 5.886, 95% CI 1.272–27.245), and number of bands (p = 0.010, HR: 1.207, 95% CI 1.046–1.393) were identified as the predictors for 14-day rebleeding; the multivariate analysis revealed only the number of bands (p = 0.009, HR: 1.247, 95% CI 1.056–1.473) as the independent factor. PVT (p = 0.012, HR: 6.732, 95% CI 1.519–29.835) and albumin < 30 g/L (p = 0.027, HR: 3.643, 95% CI 1.160–11.441) were identified as predictors for 6-week rebleeding; however, only PVT (p = 0.015, HR: 6.380, 95% CI 1.427–28.515) was found to be the independent factor in the multivariate analysis. Further analysis showed that superior mesenteric vein (SMV) thrombosis is the only risk factor predicting 6-week rebleeding in patients with PVT (p = 0.032, HR: 3.405, 95% CI 1.112–10.429).
Conclusions
PVT was associated with high 14-day and 6-week rebleeding in patients after EVL. SMV thrombosis was the only risk factor for 6-week rebleeding in patients with PVT. High albumin levels may serve as a protective factor for the 14-day and 6-week rebleeding risk. PVT was not responsible for mortality after EVL during 1-year follow-up.
Similar content being viewed by others
Data availability
All date generated or analyzed during this study are included in this published article.
References
Tantai X, Liu N, Yang L, Wei Z, Xiao C, Song Y, et al. Prognostic value of risk scoring systems for cirrhotic patients with variceal bleeding. World J Gastroenterol 2019;25(45):6668–6680
de Franchis R. Expanding consensus in portal hypertension: report of the Baveno VI Consensus Workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol 2015;63(3):743–752
Lv Y, Qi X, He C, Wang Z, Yin Z, Niu J, et al. Covered TIPS versus endoscopic band ligation plus propranolol for the prevention of variceal rebleeding in cirrhotic patients with portal vein thrombosis: a randomised controlled trial. Gut 2018;67(12):2156–2168
Kovacs TOG, Jensen DM. Varices. Clin Liver Dis 2019;23(4):625–642
Turon F, Hernández-Gea V, García-Pagán JC. Portal vein thrombosis. Curr Opin Organ Transplant 2018;23(2):250–256
Nery F, Chevret S, Condat B, de Raucourt E, Boudaoud L, Rautou PE, et al. Causes and consequences of portal vein thrombosis in 1,243 patients with cirrhosis: results of a longitudinal study. Hepatology 2015;61(2):660–667
Yan Z, Bao-yan X, Xian-bo W, Xin Z, Yan H, Jinjun C, et al. Prevalence and clinical significance of portal vein thrombosis in patients with cirrhosis and acute decompensation. Clin Gastroenterol Hepatol 2020;18:2564–2572
Intagliata NM, Caldwell SH, Tripodi A. Diagnosis, development, and treatment of portal vein thrombosis in patients with and without cirrhosis. Gastroenterology 2019;156(6):1582–1599
Razek AA, Massoud SM, Azziz MR, El-Bendary MM, Zalata K, Motawea EM. Prediction of esophageal varices in cirrhotic patients with apparent diffusion coefficient of the spleen. Abdom Imaging 2015;40(6):1465–1469
Bochnakova T. Hepatic venous pressure gradient. Clin Liver Dis (Hoboken) 2021;17(3):144–148
Vorobioff JD, Groszmann RJ. Hepatic venous pressure gradient measurement in pre-primary and primary prophylaxis of variceal hemorrhage. Ann Hepatol 2013;12(1):22–29
Lee S, Lee S, Lee T, Lee T, Chang C, Chang C. Independent factors associated with recurrent bleeding in cirrhotic patients with esophageal variceal hemorrhage. Digest Dis Sci 2009;54(5):1128–1134
Amitrano L, Guardascione MA, Scaglione M, Menchise A, Martino R, Manguso F, et al. Splanchnic vein thrombosis and variceal rebleeding in patients with cirrhosis. Eur J Gastroenterol Hepatol 2012;24(12):1381–1385
Chen PH, Chen WC, Hou MC, Liu TT, Chang CJ, Liao WC, et al. Delayed endoscopy increases re-bleeding and mortality in patients with hematemesis and active esophageal variceal bleeding: a cohort study. J Hepatol 2012;57(6):1207–1213
Yang M, Chen H, Lee H, Lin C. Risk factors and survival of early bleeding after esophageal variceal ligation. Hepatogastroenterology 2007;54(78):1705
Amitrano L, Guardascione MA, Manguso F, Bennato R, Bove A, Denucci C, et al. The effectiveness of current acute variceal bleed treatments in unselected cirrhotic patients: refining short-term prognosis and risk factors. Am J Gastroenterol 2012;107(12):1872–1878
Trebicka J, Gu W, Ibanez-Samaniego L, Hernandez-Gea V, Pitarch C, Garcia E, et al. Rebleeding and mortality risk are increased by ACLF but reduced by pre-emptive TIPS. J Hepatol 2020;73(5):1082–1091
Razek AAKA, Khashaba M, Abdalla A, Bayomy M, Barakat T. Apparent diffusion coefficient value of hepatic fibrosis and inflammation in children with chronic hepatitis. Radiol Med (Torino) 2014;119(12):903–909
de Franchis R. Revising consensus in portal hypertension: report of the Baveno V consensus workshop on methodology of diagnosis and therapy in portal hypertension. J Hepatol 2010;53(4):762–768
Wiesner R. MELD and PELD: application of survival models to liver allocation. Liver Transplant 2001;7(7):567–580
Tajiri T, Yoshida H, Obara K, Onji M, Kage M, Kitano S, et al. General rules for recording endoscopic findings of esophagogastric varices (2nd edition). Digest Endosc 2010;22(1):1–9
Sarin SK, Lahoti D, Saxena SP, Murthy NS, Makwana UK. Prevalence, classification and natural history of gastric varices: a long-term follow-up study in 568 portal hypertension patients. Hepatology (Baltimore, MD) 1992;16(6):1343–1349
Sarin SK, Philips CA, Kamath PS, Choudhury A, Maruyama H, Nery FG et al. Towards a comprehensive new classification of portal vein thrombosis in patients with cirrhosis. Gastroenterology 2016;151(4):574–577
D’Amico G. Upper digestive bleeding in cirrhosis. Post-therapeutic outcome and prognostic indicators. Hepatology 2003;38(3):599–612
Tierney A. Interventions and outcomes of treatment of postbanding ulcer hemorrhage after endoscopic band ligation: a single-center case series. Gastrointest Endosc 2013;77:136–140
Dueñas E, Cachero A, Amador A, Rota R, Salord S, Gornals J, et al. Ulcer bleeding after band ligation of esophageal varices: risk factors and prognosis. Digest Liver Dis 2020;52(1):79–83
Drolz A, Schramm C, Seiz O, Groth S, Vettorazzi E, Horvatits T, et al. Risk factors associated with bleeding after prophylactic endoscopic variceal ligation in cirrhosis. Endoscopy 2021;53(3):226–234
EASL Clinical Practical Guidelines. Vascular diseases of the liverq. J Hepatol 2016;64:179–202
Mercado MA. Surgical treatment for portal hypertension. Br J Surg 2015;102(7):717–718
Leung JC, Loong TC, Pang J, Wei JL, Wong VW. Invasive and non-invasive assessment of portal hypertension. Hepatol Int 2018;12(S1):44–55
Carvalho JR, Verdelho Machado M. New insights about albumin and liver disease. Ann Hepatol 2018;17(4):547–560
Wang Z, Xie Y, Lu Q, Yan H, Liu X, Long Y, et al. The impact of albumin infusion on the risk of rebleeding and in-hospital mortality in cirrhotic patients admitted for acute gastrointestinal bleeding: a retrospective study of a single institute. Bmc Gastroenterol 2020;20(1):198–206
Xingshun Qi CH, Wengang G, Zhanxin Y, Jianhong W, Zhengyu W, Jing N, et al. Transjugular intrahepatic portosystemic shunt for portal vein thrombosis with variceal bleeding in liver cirrhosis: outcomes and predictors in a prospective cohort study. Liver Int 2016;36:667–676
Leonardi F, Maria ND, Villa E. Anticoagulation in cirrhosis: a new paradigm? Clin Mol Hepatol 2017;23(1):13–21
Zhou T, Sun X, Zhou T, Li Y, Chen X, Cheng B, et al. Efficacy and safety of nadroparin calcium-warfarin sequential anticoagulation in portal vein thrombosis in cirrhotic patients: a randomized controlled trial. Clin Transl Gastroenterol 2020;11(9):e228
Artaza T, Lopes M, Romero M, Gómez A, de la Cruz G, Sánchez JJ, et al. Efficacy and safety of anticoagulation in non-malignant portal vein thrombosis in patients with liver cirrhosis. Gastroenterol Hepatol 2018;41(10):611–617
Hayashi T, Takatori H, Horii R, Nio K, Terashima T, Iida N, et al. Danaparoid sodium-based anticoagulation therapy for portal vein thrombosis in cirrhosis patients. Bmc Gastroenterol 2019;19(1):217–227
Noronha Ferreira C, Reis D, Cortez-Pinto H, TatoMarinho R, Gonçalves A, Palma S, et al. Anticoagulation in cirrhosis and portal vein thrombosis is safe and improves prognosis in advanced cirrhosis. Digest Dis Sci 2019;64(9):2671–2683
Berry K, Taylor J, Liou IW, Ioannou GN. Portal vein thrombosis is not associated with increased mortality among patients with cirrhosis. Clin Gastroenterol Hepatol 2015;13(3):585–593
Luca A, Caruso S, Milazzo M, Marrone G, Mamone G, Crinò F, et al. Natural course of extrahepatic nonmalignant partial portal vein thrombosis in patients with cirrhosis. Radiology 2012;265(1):124–132
Qi X, Dai J, Yang M, Ren W, Jia J, Guo X. Association between portal vein thrombosis and survival in non-liver-transplant patients with liver cirrhosis: a systematic review of the literature. Gastroenterol Res Pract 2015;2015:1–7
Zhao Y, Ren M, Lu G, Lu X, Yin Y, Zhang D, et al. The prognosis analysis of liver cirrhosis with acute variceal bleeding and validation of current prognostic models: a large scale retrospective cohort study. Biomed Res Int 2020;2020:1–7
Thomopoulos K, Theocharis G, Mimidis K, Lampropouloukaratza C, Alexandridis E, Nikolopoulou V. Improved survival of patients presenting with acute variceal bleeding prognostic indicators of short- and long-term mortality. Digest Liver Dis 2006;38(12):899–904
Abdel Razek AAK, El-Serougy LG, Saleh GA, Shabana W, Abd E-W. Liver imaging reporting and data system version 2018: what radiologists need to know. J Comput Assist Tomogr 2020;44(2):168–177
Xu X, Guo X, De Stefano V, Silva-Junior G, Goyal H, Bai Z, et al. Nonselective beta-blockers and development of portal vein thrombosis in liver cirrhosis: a systematic review and meta-analysis. Hepatol Int 2019;13(4):468–481
Mehta G, Gustot T, Mookerjee RP, Garcia-Pagan JC, Fallon MB, Shah VH, et al. Inflammation and portal hypertension—the undiscovered country. J Hepatol. 2014;61(1):155–63
Acknowledgements
We are sincerely grateful to the physicians and all co-medical staff.
Funding
There is no financial support of this study.
Author information
Authors and Affiliations
Contributions
Professor YG designed and administrated the study. ZG conducted the study, collected and interpreted the data, drafted the manuscript. J-RZ interpreted the result and supervised the study. XL and SL administrated the study. MW collected the date. All authors had access to the study data and had reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Zhanjuan Gao, Jingrun Zhao, Xiaofeng Liu, Senlin Li, Minghui Wang,Yanjing Gao declare that there is no conflict of interest.
Ethical approval
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation and with the Helsinki Declaration of 1975. Each institution approved the protocol, and the data of all patients were recorded in a standard form. Because of retrospective, we did not have consent to participate, but all the patients information will be kept strictly confidential.
Animal research
This article does not contain any studies with animal subjects.
Informed consent
Informed consent for publication was obtained from all participants (Zhanjuan Gao, Jingrun Zhao, Xiaofeng Liu, Senlin Li, Minghui Wang, Yanjing Gao).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gao, Z., Zhao, J., Liu, X. et al. Portal vein thrombosis associated with high 14-day and 6-week rebleeding in patients after oesophageal variceal band ligation: a retrospective, multicentre, nested case–control study. Hepatol Int 15, 1183–1195 (2021). https://doi.org/10.1007/s12072-021-10224-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12072-021-10224-4