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Organ Transplantation Related Cancer ORGAN TRANSPLANTATION RELATED CANCER by Rajeev Ramarao Desai A thesis submitted to The University of Birmingham for the degree of Doctor of Philosophy October 2015 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Abstract Cancer is an important cause of morbidity and mortality among the recipients of solid organ transplantation. Cancer transmitted from the donors often has a poor outcome and the fear of such transmission results in organs from certain donors not being accepted. A study of the transplant recipients in the UK over a period of 10 years identified 15 cases of transmitted cancers. The rate of cancer transmission was 0.05%. The risk of cancer transmission was 9 times higher from donors older than 45 years. Cancer transmission occurred from donors without a history of cancer. A comparison of the organ donor data with the guidelines classifying the donor’s risk of cancer transmission showed that a carefully selected cohort of donors, who are classed as a high risk of cancer transmission by the guidelines, could safely donate their organs resulting in valuable additional survival for the recipients, with low risk of cancer transmission. These results provide evidence, based on which the donor classification guidelines can be modified resulting in increased availability of safe organs for transplantation. The risk of recurrence after transplantation of cancers treated before transplantation was low in carefully selected recipients undergoing transplantation after a waiting period of 2 years following the diagnosis of cancer. No association was found between the donor-recipient CMV status and the risk of post transplant cancer. No chronological changes were noted in the incidence of PTLD or in the survival rates after the diagnosis of PTLD. This research estimated the risk of cancer transmission to the organ transplant recipients enabling improved risk assessment in transplantation. This research also explored the ways of increasing the number of safe organs for transplantation whilst reducing inappropriate wastage of donor organs. 1 Disclaimer This is to certify that I have, as first author, already published some of the text and the data presented in Chapters 3, 4, 6, and 8 of this thesis. These publications have been used to facilitate the development of evidence-based national guidelines for improving the selection of organ donors. Such content is referenced with their respective publications as follows: Chapter 3; pages 117 to 143 (paragraphs 3.1 to 3.5) published in: DESAI, R., COLLETT, D., WATSON, C. J., JOHNSON, P., EVANS, T. & NEUBERGER, J. 2012. Cancer transmission from organ donors-unavoidable but low risk. Transplantation, 94, 1200-7 Chapter 4; pages 145 to 171 (paragraphs 4.1 to 4.5) published in: DESAI, R., COLLETT, D., WATSON, C. J., JOHNSON, P., EVANS, T. & NEUBERGER, J. 2014. Estimated risk of cancer transmission from organ donor to graft recipient in a national transplantation registry. Br J Surg, 101, 768-74 Chapter 6; pages 192 to 217 (paragraphs 6.1 to 6.5) published in: DESAI, R., COLLETT, D., WATSON, C. J., JOHNSON, P. J., MOSS, P. & NEUBERGER, J. 2015. Impact of Cytomegalovirus on Long-term Mortality and Cancer Risk After Organ Transplantation. Transplantation, 99, 1989-94 Chapter 8; pages 265 to272 (paragraphs 8.1.2, 8.1.3 and 8.1.5) published in three publications mentioned above 2 Dedication I wish to dedicate this thesis to my family, particularly to my wife Seema and children Rahul and Tanya, for their support, patience and encouragement. 3 Acknowledgements There are many people and organisations to thank, without whose help this work would not have been possible. I would like to thank: Professor James Neuberger for offering me the privilege of working with him and learn from him, the support, guidance, supervision and encouragement provided throughout the period of this research Professor Philip Johnson for his supervision and guidance in completing this work and Mrs Johnson for the secretarial support Professor Dave Collett for helping me in learning the statistical methods and enabling me to perform independently, all the statistical analyses needed to complete this research The team of statisticians, clinical governance team, information governance team, the duty office and the secretaries at Organ Donation and Transplantation, NHS Blood and Transplant, Bristol The NHS Blood and Transplant for funding this study Professor Chris Watson for the support and advice offered during the data collection and analysis Professor Paul Moss for his advice in writing chapter 6 Dr Ian Rowe for his advice in writing chapter 1 4 The transplant doctors, specialist nurses and data management teams in all the transplant centres in the UK for helping me with the database search to identify cases of donor- transmitted cancer The team of specialist nurses in organ donation at NHS Blood and Transplant, Birmingham for their help with the potential donors project Dr Tim Evans, Cancer Registration Information manager at Public Health England, Birmingham and Dr David Greenberg, Senior Analyst at the Eastern Cancer Registration and Information centre, Cambridge for their help in providing the data from the Cancer registries The IT departments at NHSBT Birmingham and Bristol for their support in IT related issues All the patients included in the study and their families for exhibiting their generosity particularly in periods of ill health and anguish, by consenting for their data to be used in research 5 Abbreviations ARDS Adult respiratory distress syndrome AMR Antibody mediated rejection AFP Alpha-fetoprotein APC Antigen presenting cell ALG Anti-lymphocyte globulin ATG Anti-thymocyte globulin ANZDATA Australia and New Zealand Dialysis and Transplant Registry BC Before Christ BMI Body mass index CNI Calcineurin inhibitors CIS Carcinoma-in-situ CNS Central nervous system CNT Centro Nazionali di Trapianti CCL2 Chemokine (c-c motif) ligand 2 CCL5 Chemokine ligand 5 CoE Council of Europe CI Confidence interval 6 CRP C-reactive protein CT Computerised tomography CXCL10 c-x-c motif chemokine CMV Cytomegalovirus D Donor DNA De-oxy ribonucleic acid DCP Des-gamma-carboxy prothrombin DBD Donation after brain death DCD Donation after circulatory death DDC Donor derived cancer DOC Donor origin cancer DTC Donor transmitted cancer EBV Epstein-Barr virus GIST Gastrointestinal stromal tumour HR Hazard ratio HFSS Heart failure survival score HBV Hepatitis B virus HCV Hepatitis C virus 7 HL Hodgkin’s lymphoma HHV Human herpes virus HIV Human immunodeficiency virus HLA Human leukocyte antigen HPV Human papilloma virus HTLV Human T-lymphotropic virus IFN Interferon IL Interleukin iNOS Inducible nitric oxide synthetase IPITTR Israel Penn International Transplant Tumour Registry Kg Kilogram LAS Lung allocation score MRI Magnetic resonance imaging MHC Major histocompatibility complex mTOR Mammalian target of Rapamycin mTORC Mammalian target of Rapamycin complex m Metre 6MP 6-mercaptopurine 8 MELD Model for end-stage liver disease MMF Mycophenolate mofetil NCDR National Cancer Data Repository NHS National Health Service NHSBT National Health Service Blood and Transplant NOMDS National Organ Matching and Distribution Service NTTRL National Tissue Typing and Reference Laboratory NK Natural killer NHL Non-Hodgkin’s lymphoma NMSC Non-melanoma skin cancer NS Not specified NFAT Nuclear factor of activated T-cells OR Odds ratio OPTN Organ Procurement and Transplantation Network ONT Organizacion Nacional de Trasplantes PET Positron emission tomography PTLD Post-transplant lymphoproliferative disorder PCA Prostate cancer antigen 9 PSA Prostate specific antigen R Recipient SHFM Seattle heart failure model SN-OD Specialist nurses in organ donation SIR Standardised incidence ratio SAS Statistical analysis software TCR T cell receptor TTS The Transplantation Society 6TG 6-thioguanine TGF Transforming growth factor TNF Tumour necrosis factor UV Ultraviolet UK United Kingdom UKELD United Kingdom end-stage liver disease UNOS United Network for Organ Sharing USFDA United States Food and Drug Administration USA United States of America WHO World Health Organization 10 Contents Abstract……………………………………………………………………………………………………………………..…………1 Disclaimer…………………………………………………………………………………………………………………………….2 Dedication…………………………………………………………………………………………………………………………….3 Acknowledgements………………………………………………………………………………………………………………4 Abbreviations……………………………………………………………………………………………………………………….6 List of Tables……………………………………………………………………………………………………………………….20 List of Figures……………………………………………………………………………………………………………………..23 1. Introduction…………………………………………………………………………………………………………………26 1.1 Background to this research……………………………………………………………………………….27 1.2 History of transplantation…………………………………………………………………………………..28 1.2.1 Early history…………………………………………………………………………………………………28 1.2.2 Xenotransplantation…………………………………………………………………...................29 1.2.3 Early human kidney allotransplantation………………………………………………………30 1.2.4 First successful kidney
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