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PROTOCOL FOR LIVER TRANSPLANTATION IN UNRESECTABLE COLORECTAL METASTASIS

ABSTRACT - BACKGROUND:

Colorectal cancer (CRC) is the third most common neoplasm, and half of the patients with CRC develop liver metastasis. The best prognostic factor for colorectal liver metastasis (CRLM) is the possibility of performing a resection with free margins; however, most of them remain unresectable. The justification for performing liver transplantation (LT) in patients with CRLM regards an increase in the number of resectable patients by performing total hepatectomy.

AIM:

The aim of this study was to provide a Brazilian protocol for LT in patients with unresectable CRLM.

METHOD:

The protocol was carried out by two Brazilian institutions, which perform a large volume of resections and LTs, based on the study carried out at the University of Oslo. The elaboration of the protocol was conducted in four stages.

RESULT:

A protocol proposal for this disease is presented, which needs to be validated for clinical use.

CONCLUSION:

The development of an LT protocol for unresectable CRLM aims to standardize the treatment and to enable a better evaluation of surgical results.

HEADINGS:
Transplantation; Liver Transplantation; Colorectal Neoplasms; Neoplasm Metastasis

RESUMO - RACIONAL:

O câncer colorretal é a terceira neoplasia mais frequente e metade dos pacientes desenvolvem metástase hepática. O melhor fator prognóstico na metástase hepática de câncer colorretal (MHCCR) é a possibilidade de ressecção com margens livres, porém a maioria permanece irressecável. O racional em realizar transplante hepático (TH) em pacientes portadores de MHCCR está na ampliação do número de pacientes ressecáveis através de uma hepatectomia total.

OBJETIVO:

Apresentar protocolo brasileiro para realização de transplante hepático em pacientes com MHCCR irressecável.

MÉTODO:

O protocolo foi realizado por duas instituições com grande volume de ressecções e transplantes hepáticos no Brasil, baseado no trabalho realizado pela Universidade de Oslo. A elaboração foi dividida em 4 etapas.

RESULTADO:

É apresentada proposta de protocolo para esta doença a ser validada na aplicação clínica.

CONCLUSÃO:

Foi possível elaborar protocolo de transplante hepático para MHCCR irressecável a fim de uniformizar o tratamento e melhor avaliar os resultados cirúrgicos.

DESCRITORES:
Transplante; Transplante de Fígado; Neoplasias Colorretais; Metástase.

INTRODUCTION

Colorectal cancer (CRC) is the third most common type of cancer in both genders. At the time of diagnosis, nearly 25% of patients have metastasis and the liver is the most affected organ (present in 80% of cases); it is estimated that half of the patients with CRC will develop liver metastasis at some point in the course of the disease1313. Krüger JAP, Fonseca GM, Makdissi FF, Jeismann VB, Coelho FF, Herman P. Evolution in the surgical management of colorectal liver metastases: Propensity score matching analysis (PSM) on the impact of specialized multidisciplinary care across two institutional eras. J Surg Oncol. 2018; 118(1):50-60; doi: 10.1002/jso.25098.
https://doi.org/10.1002/jso.25098...
,1414. Lee RM, Cardona K, Russell MC. Historical perspective: Two decades of progress in treating metastatic colorectal cancer. J Surg Oncol. 2019;119(5):549-563; doi: 10.1002/jso.25431.
https://doi.org/10.1002/jso.25431...
.

Currently, the treatment of metastatic CRC (stage IV) is based on a multidisciplinary and multimodal approach1313. Krüger JAP, Fonseca GM, Makdissi FF, Jeismann VB, Coelho FF, Herman P. Evolution in the surgical management of colorectal liver metastases: Propensity score matching analysis (PSM) on the impact of specialized multidisciplinary care across two institutional eras. J Surg Oncol. 2018; 118(1):50-60; doi: 10.1002/jso.25098.
https://doi.org/10.1002/jso.25098...
,1818. Raoof M, Haye S, Ituarte PHG, Fong Y. Liver Resection Improves Survival in Colorectal Cancer Patients: Causal-effects From Population-level Instrumental Variable Analysis. Ann Surg. 2019; 270(4):692-700. doi: 10.1097/SLA.0000000000003485.
https://doi.org/10.1097/SLA.000000000000...
. The possibility of performing a resection with free margins is the best prognostic factor for colorectal liver metastasis (CRLM)1414. Lee RM, Cardona K, Russell MC. Historical perspective: Two decades of progress in treating metastatic colorectal cancer. J Surg Oncol. 2019;119(5):549-563; doi: 10.1002/jso.25431.
https://doi.org/10.1002/jso.25431...
. In this scenario, hepatectomy has become the main treatment of CRLM, having an overall survival rate of 30-55% in 5 years and 20-25% in 10 years11. Adams RB, Aloia TA, Loyer E, Pawlik TM, Taouli B, Vauthey JN; Americas Hepato-Pancreato-Biliary Association; Society of Surgical Oncology; Society for Surgery of the Alimentary Tract. Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB (Oxford). 2013;15(2):91-103. doi: 10.1111/j.1477-2574.2012.00557.x.
https://doi.org/10.1111/j.1477-2574.2012...
,77. Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999; 230(3):309-18; discussion 318-21. doi: 10.1097/00000658-199909000-00004.
https://doi.org/10.1097/00000658-1999090...
,1414. Lee RM, Cardona K, Russell MC. Historical perspective: Two decades of progress in treating metastatic colorectal cancer. J Surg Oncol. 2019;119(5):549-563; doi: 10.1002/jso.25431.
https://doi.org/10.1002/jso.25431...
,1818. Raoof M, Haye S, Ituarte PHG, Fong Y. Liver Resection Improves Survival in Colorectal Cancer Patients: Causal-effects From Population-level Instrumental Variable Analysis. Ann Surg. 2019; 270(4):692-700. doi: 10.1097/SLA.0000000000003485.
https://doi.org/10.1097/SLA.000000000000...
. Several strategies have been used to expand the possibility of resection and to ensure adequate liver remnants, such as parenchyma-preserving techniques, portal vein embolization, two-stage liver resection (LR), and ALLPS (Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy). Even with the use of these strategies, most patients with CRLM remain functionally or anatomically unresectable2020. Schadde E, Grunhagen DJ, Verhoef C, Krzywon L, Metrakos P. Limitations in resectability of colorectal liver metastases 2020 - A systematic approach for clinicians and patients. Semin Cancer Biol. 2021;71:10-20. doi: 10.1016/j.semcancer.2020.09.008.
https://doi.org/10.1016/j.semcancer.2020...
.

The justification for performing liver transplantation (LT) in patients with CRLM regards the increase in the number of resectable patients by performing a total hepatectomy. However, LT in patients with CRLM was considered an absolute contraindication before 1995, due to unacceptable results obtained at the time. The first experience was reported by the European Liver Transplant Registry (ELTR), presenting survival rate of 62% in 1 year and 18% in 5 years55. European Liver Transplant Registy (ELTR). Data Analysis Booklet. Paris. 2007.. It is worth mentioning that both the perioperative results of LT and the chemotherapy drugs available for the treatment of CRC in the late 1980s and early 1990s justify these aforementioned negative results. The poor results associated with organ scarcity resulted in the discontinuation of LT for CRLM88. Foss A, Adam R, Dueland S. Liver transplantation for colorectal liver metastases: revisiting the concept. Transpl Int. 2010; 23(7):679-85. doi: 10.1111/j.1432-2277.2010.01097.x.
https://doi.org/10.1111/j.1432-2277.2010...
,1212. Hoti E, Adam R. Liver transplantation for primary and metastatic liver cancers. Transpl Int. 2008; 21(12):1107-17; doi: 10.1111/j.1432-2277.2008.00735.x
https://doi.org/10.1111/j.1432-2277.2008...
. Based on the data currently available, the International Liver Transplant Society (ILTS) is recommended to perform LT with a specific protocol for CLRM1111. Hibi T, Rela M, Eason JD, Line PD, Fung J, Sakamoto S, Selzner N, Man K, Ghobrial RM, Sapisochin G. Liver Transplantation for Colorectal and Neuroendocrine Liver Metastases and Hepatoblastoma. Working Group Report From the ILTS Transplant Oncology Consensus Conference. Transplantation. 2020; 104(6):1131-1135. doi: 10.1097/TP.0000000000003118.
https://doi.org/10.1097/TP.0000000000003...
.

Therefore, the aim of this study was to present a protocol proposal to guide the clinical use of LT in CRLM. This protocol needs to be validated in future studies.

METHODS

This protocol was performed by two high-volume centers of LT and LR in Brazil: University Hospital of the Medical School of the University of São Paulo (HCFMUSP) and Hospital Adventista Silvestre/Hospital São Lucas. The elaboration of the protocol was conducted in four stages.

In the first stage, a search in the literature was performed in order to obtain the main published studies regarding LT for CRLM to date. In the second stage, an outline of the protocol was designed by the first two authors and the last author, based on the SECA trials from the University of Oslo44. Dueland S, Syversveen T, Solheim JM, Solberg S, Grut H, Bjørnbeth BA, Hagness M, Line PD. Survival Following Liver Transplantation for Patients With Nonresectable Liver-only Colorectal Metastases. Ann Surg. 2020; 271(2):212-218. doi: 10.1097/SLA.0000000000003404.
https://doi.org/10.1097/SLA.000000000000...
,99. Hagness M, Foss A, Line PD, Scholz T, Jørgensen PF, Fosby B, Boberg KM, Mathisen O, Gladhaug IP, Egge TS, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013; 257(5):800-6. doi: 10.1097/SLA.0b013e3182823957.
https://doi.org/10.1097/SLA.0b013e318282...
. In the third stage, 10 experts elaborated the last version of the protocol, adapted to the Brazilian reality. The fourth stage consisted of the protocol submitted for approval in the National Transplant System (SNT-Sistema Nacional de Transplantes) of the Brazilian Ministry of Health.

Brazilian centers were selected for inclusion in the multicentric research project, and a total of 30 patients underwent transplantation according to the criteria of this protocol and were referred to these centers by the SNT. Preoperative, intraoperative, and postoperative data were prospectively recorded on the REDCap platform1010. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009 Apr;42(2):377-81. doi: 10.1016/j.jbi.2008.08.010.
https://doi.org/10.1016/j.jbi.2008.08.01...
. The following pretransplantation data were analyzed: age, gender, body mass index (BMI), clinical performance, comorbidities, laboratory examinations, staging examinations, size and number of tumors, previous chemotherapy, response to chemotherapy, anatomopathological analysis of the primary tumor, time between diagnosis of CRC and LT, and type of LT (deceased donor or living donor). The number of patients referred for the LT evaluation, as well as the number of patients who effectively met the criteria and were included for undergoing LT and those who were excluded before the LT (due to not meeting the criteria) were also assessed. After the LT, disease-free survival and overall survival rate in 1, 3, and 5 years, immunosuppression protocol, rejection episodes, and need for retransplantation were analyzed.

RESULTS

Figure 1 shows the LT protocol for CRLM proposed in this study by the authors. Figure 2 shows the document of SNT to be filled in to request a special situation for CRLM.

Figure 1 -
Protocol created by the authors for liver transplantation in unresectable colorectal metastasis.

Figure 2 -
Document of SNT to be filled in to request a special situation for unresectable CRLM.

DISCUSSION

In the past two decades, there has been improvement in the survival rates after LT by 20-30% and improvement in the imaging examinations; there was also the introduction of immunosuppressants with antineoplastic action (mTOR inhibitors)1515. Lima AS, Pereira BB, Jungmann S, Machado CJ, Correia MITD. Risk factors for post-liver transplant biliary complications in the absence of arterial complications. Arq Bras Cir Dig. 2020;33(3):e1541. doi: 10.1590/0102-672020200003e1541.
https://doi.org/10.1590/0102-67202020000...
,1717. Pinto LEV, Coelho GR, Coutinho MMS, Torres OJM, Leal PC, Vieira CB, Garcia JHP. Risk factors associated with hepatic artery thrombosis: analysis of 1050 liver transplants. Arq Bras Cir Dig. 2021;33(4):e1556. doi: 10.1590/0102-672020200004e1556.
https://doi.org/10.1590/0102-67202020000...
. This technical progress combined with the peculiar transplantation scenario in Norway, which has more organ donors than recipients on the list, provided the ideal scenario for performing LT in CRLM. In the SECA I study, conducted from 2006 to 2011 at the University of Oslo, 21 patients underwent LT for CRLM, whose main inclusion criteria at the time consisted of good clinical performance (ECOG 0 or 1), complete resection of the primary tumor, and a minimum of 6 weeks of chemotherapy. The authors obtained an overall survival rate of 60% in 5 years and identified four clinical variables associated with a worse prognosis (Oslo criteria): tumor diameter >5.5 cm, CEA > 80 ng/ml, interval between resection and LT <2 years, and progression of the disease during chemotherapy99. Hagness M, Foss A, Line PD, Scholz T, Jørgensen PF, Fosby B, Boberg KM, Mathisen O, Gladhaug IP, Egge TS, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013; 257(5):800-6. doi: 10.1097/SLA.0b013e3182823957.
https://doi.org/10.1097/SLA.0b013e318282...
.

The same group from Oslo continued the investigation of LT for CRLM through the SECA II study. From 2012 to 2016, 15 patients were transplanted with restrictive criteria in order to obtain a result similar to other causes of LT. Several criteria were included for the performance of LT, such as the Oslo criteria, the nonresectability due to partial hepatectomy, and the radiological tumor response after chemotherapy. The authors obtained an overall survival rate of 100% in 1 year, 83% in 3 years, and 83% in 5 years. Disease-free survival rate obtained was 53% in 1 year, 44% in 3 years, and 35% in 3 years. The main site of recurrence was pulmonary and most of them were fit for resection; therefore, the high rates of recurrence had less influence on the survival rate of patients44. Dueland S, Syversveen T, Solheim JM, Solberg S, Grut H, Bjørnbeth BA, Hagness M, Line PD. Survival Following Liver Transplantation for Patients With Nonresectable Liver-only Colorectal Metastases. Ann Surg. 2020; 271(2):212-218. doi: 10.1097/SLA.0000000000003404.
https://doi.org/10.1097/SLA.000000000000...
.

Both the aforementioned Norwegian studies have major importance in the “Transplant Oncology,” a term used to describe LT as a treatment option for hepatobiliopancreatic neoplasms. Recently, multiple centers in Europe and in the United States have started to perform LT for CRLM1111. Hibi T, Rela M, Eason JD, Line PD, Fung J, Sakamoto S, Selzner N, Man K, Ghobrial RM, Sapisochin G. Liver Transplantation for Colorectal and Neuroendocrine Liver Metastases and Hepatoblastoma. Working Group Report From the ILTS Transplant Oncology Consensus Conference. Transplantation. 2020; 104(6):1131-1135. doi: 10.1097/TP.0000000000003118.
https://doi.org/10.1097/TP.0000000000003...
,1919. Sapisochin G, Hibi T, Ghobrial M, Man K. The ILTS Consensus Conference on Transplant Oncology: Setting the Stage. Transplantation. 2020; 104(6):1119-1120. doi: 10.1097/TP.0000000000003175.
https://doi.org/10.1097/TP.0000000000003...
. Fernandes et al. were pioneers in performing the first LT with a living donor in Latin America in a patient with CRLM, in agreement with the Oslo criteria66. Fernandes ESM, Line PD, Mello FP, Andrade RO, Girão CL, Pimentel LS, César C, Suleiman TS, Waechter FL, Oliveira ATT, Torres OJM. Living donor liver transplant for colorectal liver metastasis: the first case in Latin America. Arq Bras Cir Dig. 2019; 32(4):e1468. doi: 10.1590/0102-672020180001e1468.
https://doi.org/10.1590/0102-67202018000...
.

The exclusion of transplantation in cases of right colon tumor and/or the presence of positive BRAF is a topic to be discussed. Mutation-positive BRAF is considered a risk factor and is associated with worse outcomes after transplantation. Tumors of the right colon also have a worse prognosis, precisely due to their higher frequency of positive BRAF1616. Line PD, Dueland S. Liver transplantation for secondary liver tumours: The difficult balance between survival and recurrence. J Hepatol. 2020; 73(6):1557-1562. doi: 10.1016/j.jhep.2020.08.015.
https://doi.org/10.1016/j.jhep.2020.08.0...
. Clinical studies that are still in progress present heterogeneity regarding these items and, therefore, we chose to maintain them in our protocol until further studies. In Norway (NCT01479608, NCT02215889, and NCT03494946) and Germany (NCT03488953), the studies do not adopt these exclusion criteria, while in France (NCT02597348), Canada (NCT02864485), and Italy (NCT03803436), positive BRAF is the exclusion criteria33. ClinicalTrials.gov [Internet]. Bethesda (MD): U.S. National Library of Medicine; 2002. Available from: https://clinicaltrials.gov/ct2/home;
https://clinicaltrials.gov/ct2/home...
,1111. Hibi T, Rela M, Eason JD, Line PD, Fung J, Sakamoto S, Selzner N, Man K, Ghobrial RM, Sapisochin G. Liver Transplantation for Colorectal and Neuroendocrine Liver Metastases and Hepatoblastoma. Working Group Report From the ILTS Transplant Oncology Consensus Conference. Transplantation. 2020; 104(6):1131-1135. doi: 10.1097/TP.0000000000003118.
https://doi.org/10.1097/TP.0000000000003...
.

The regulation of this protocol is in progress in the SNT for validation in the Brazilian national territory22. Brasil. Decreto n. 2.268, de 30 de junho de 1997. Regulamenta a Lei n. 9.434, de 4 de fevereiro de 1997, que dispõe sobre a remoção de órgãos, tecidos e partes do corpo humano para fins de transplante e dá outras providências. Brasília: Diário Oficial da União 1 jul 1997; (1):13739..

CONCLUSION

An LT protocol for colorectal unresectable metastasis was created to standardize the treatment and to enable a better evaluation of not only surgical results but also disease-free survival and overall survival of patients with CRLM.

ACKNOWLEDGMENT

The authors thank Eduardo Fernandes and Pål-Dag Line, whose expertise was essential for carrying out this study.

REFERÊNCIAS

  • 1
    Adams RB, Aloia TA, Loyer E, Pawlik TM, Taouli B, Vauthey JN; Americas Hepato-Pancreato-Biliary Association; Society of Surgical Oncology; Society for Surgery of the Alimentary Tract. Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB (Oxford). 2013;15(2):91-103. doi: 10.1111/j.1477-2574.2012.00557.x.
    » https://doi.org/10.1111/j.1477-2574.2012.00557.x
  • 2
    Brasil. Decreto n. 2.268, de 30 de junho de 1997. Regulamenta a Lei n. 9.434, de 4 de fevereiro de 1997, que dispõe sobre a remoção de órgãos, tecidos e partes do corpo humano para fins de transplante e dá outras providências. Brasília: Diário Oficial da União 1 jul 1997; (1):13739.
  • 3
    ClinicalTrials.gov [Internet]. Bethesda (MD): U.S. National Library of Medicine; 2002. Available from: https://clinicaltrials.gov/ct2/home;
    » https://clinicaltrials.gov/ct2/home
  • 4
    Dueland S, Syversveen T, Solheim JM, Solberg S, Grut H, Bjørnbeth BA, Hagness M, Line PD. Survival Following Liver Transplantation for Patients With Nonresectable Liver-only Colorectal Metastases. Ann Surg. 2020; 271(2):212-218. doi: 10.1097/SLA.0000000000003404.
    » https://doi.org/10.1097/SLA.0000000000003404
  • 5
    European Liver Transplant Registy (ELTR). Data Analysis Booklet. Paris. 2007.
  • 6
    Fernandes ESM, Line PD, Mello FP, Andrade RO, Girão CL, Pimentel LS, César C, Suleiman TS, Waechter FL, Oliveira ATT, Torres OJM. Living donor liver transplant for colorectal liver metastasis: the first case in Latin America. Arq Bras Cir Dig. 2019; 32(4):e1468. doi: 10.1590/0102-672020180001e1468.
    » https://doi.org/10.1590/0102-672020180001e1468
  • 7
    Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999; 230(3):309-18; discussion 318-21. doi: 10.1097/00000658-199909000-00004.
    » https://doi.org/10.1097/00000658-199909000-00004
  • 8
    Foss A, Adam R, Dueland S. Liver transplantation for colorectal liver metastases: revisiting the concept. Transpl Int. 2010; 23(7):679-85. doi: 10.1111/j.1432-2277.2010.01097.x.
    » https://doi.org/10.1111/j.1432-2277.2010.01097.x
  • 9
    Hagness M, Foss A, Line PD, Scholz T, Jørgensen PF, Fosby B, Boberg KM, Mathisen O, Gladhaug IP, Egge TS, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013; 257(5):800-6. doi: 10.1097/SLA.0b013e3182823957.
    » https://doi.org/10.1097/SLA.0b013e3182823957
  • 10
    Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009 Apr;42(2):377-81. doi: 10.1016/j.jbi.2008.08.010.
    » https://doi.org/10.1016/j.jbi.2008.08.010
  • 11
    Hibi T, Rela M, Eason JD, Line PD, Fung J, Sakamoto S, Selzner N, Man K, Ghobrial RM, Sapisochin G. Liver Transplantation for Colorectal and Neuroendocrine Liver Metastases and Hepatoblastoma. Working Group Report From the ILTS Transplant Oncology Consensus Conference. Transplantation. 2020; 104(6):1131-1135. doi: 10.1097/TP.0000000000003118.
    » https://doi.org/10.1097/TP.0000000000003118
  • 12
    Hoti E, Adam R. Liver transplantation for primary and metastatic liver cancers. Transpl Int. 2008; 21(12):1107-17; doi: 10.1111/j.1432-2277.2008.00735.x
    » https://doi.org/10.1111/j.1432-2277.2008.00735.x
  • 13
    Krüger JAP, Fonseca GM, Makdissi FF, Jeismann VB, Coelho FF, Herman P. Evolution in the surgical management of colorectal liver metastases: Propensity score matching analysis (PSM) on the impact of specialized multidisciplinary care across two institutional eras. J Surg Oncol. 2018; 118(1):50-60; doi: 10.1002/jso.25098.
    » https://doi.org/10.1002/jso.25098
  • 14
    Lee RM, Cardona K, Russell MC. Historical perspective: Two decades of progress in treating metastatic colorectal cancer. J Surg Oncol. 2019;119(5):549-563; doi: 10.1002/jso.25431.
    » https://doi.org/10.1002/jso.25431
  • 15
    Lima AS, Pereira BB, Jungmann S, Machado CJ, Correia MITD. Risk factors for post-liver transplant biliary complications in the absence of arterial complications. Arq Bras Cir Dig. 2020;33(3):e1541. doi: 10.1590/0102-672020200003e1541.
    » https://doi.org/10.1590/0102-672020200003e1541
  • 16
    Line PD, Dueland S. Liver transplantation for secondary liver tumours: The difficult balance between survival and recurrence. J Hepatol. 2020; 73(6):1557-1562. doi: 10.1016/j.jhep.2020.08.015.
    » https://doi.org/10.1016/j.jhep.2020.08.015
  • 17
    Pinto LEV, Coelho GR, Coutinho MMS, Torres OJM, Leal PC, Vieira CB, Garcia JHP. Risk factors associated with hepatic artery thrombosis: analysis of 1050 liver transplants. Arq Bras Cir Dig. 2021;33(4):e1556. doi: 10.1590/0102-672020200004e1556.
    » https://doi.org/10.1590/0102-672020200004e1556
  • 18
    Raoof M, Haye S, Ituarte PHG, Fong Y. Liver Resection Improves Survival in Colorectal Cancer Patients: Causal-effects From Population-level Instrumental Variable Analysis. Ann Surg. 2019; 270(4):692-700. doi: 10.1097/SLA.0000000000003485.
    » https://doi.org/10.1097/SLA.0000000000003485
  • 19
    Sapisochin G, Hibi T, Ghobrial M, Man K. The ILTS Consensus Conference on Transplant Oncology: Setting the Stage. Transplantation. 2020; 104(6):1119-1120. doi: 10.1097/TP.0000000000003175.
    » https://doi.org/10.1097/TP.0000000000003175
  • 20
    Schadde E, Grunhagen DJ, Verhoef C, Krzywon L, Metrakos P. Limitations in resectability of colorectal liver metastases 2020 - A systematic approach for clinicians and patients. Semin Cancer Biol. 2021;71:10-20. doi: 10.1016/j.semcancer.2020.09.008.
    » https://doi.org/10.1016/j.semcancer.2020.09.008
  • 4
    How to cite this article: Ernani L, Fernandes ESM, Martino RB, Coelho FF, Mello FPT, Andrade R, Pimentel LS, Haddad LBP, Herman P, Andraus W, D’Albuquerque LAC. Protocol for liver transplantation in unresectable colorectal metastasis. ABCD Arq Bras Cir Dig. 2021;34(4):e1625. https://doi.org//10.1590/0102-672020210002e1625
  • Financial source: none

Publication Dates

  • Publication in this collection
    31 Jan 2022
  • Date of issue
    2021

History

  • Received
    20 Dec 2020
  • Accepted
    25 Apr 2021
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