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Clinical and biological landscape of constitutional mismatch-repair deficiency syndrome: an International Replication Repair Deficiency Consortium cohort study
AB. Ercan, M. Aronson, NR. Fernandez, Y. Chang, A. Levine, ZA. Liu, L. Negm, M. Edwards, V. Bianchi, L. Stengs, J. Chung, A. Al-Battashi, A. Reschke, A. Lion, A. Ahmad, A. Lassaletta, AT. Reddy, AF. Al-Darraji, AC. Shah, A. Van Damme, A. Bendel,...
Language English Country England, Great Britain
Document type Journal Article, Research Support, Non-U.S. Gov't, Multicenter Study
NLK
ProQuest Central
from 2000-09-01 to 2 months ago
Nursing & Allied Health Database (ProQuest)
from 2000-09-01 to 2 months ago
Health & Medicine (ProQuest)
from 2000-09-01 to 2 months ago
Public Health Database (ProQuest)
from 2000-09-01 to 2 months ago
- MeSH
- Neoplastic Syndromes, Hereditary * genetics therapy MeSH
- Child MeSH
- DNA-Binding Proteins * MeSH
- Adult MeSH
- MutS Homolog 2 Protein genetics MeSH
- Incidence MeSH
- Colorectal Neoplasms genetics pathology mortality MeSH
- Humans MeSH
- Longitudinal Studies MeSH
- Adolescent MeSH
- Young Adult MeSH
- Mutation MeSH
- MutL Protein Homolog 1 genetics MeSH
- Brain Neoplasms genetics therapy mortality pathology epidemiology MeSH
- DNA Mismatch Repair MeSH
- Child, Preschool MeSH
- Cross-Sectional Studies MeSH
- Check Tag
- Child MeSH
- Adult MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Male MeSH
- Child, Preschool MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Multicenter Study MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Constitutional mismatch repair deficiency (CMMRD) syndrome is a rare and aggressive cancer predisposition syndrome. Because a scarcity of data on this condition contributes to management challenges and poor outcomes, we aimed to describe the clinical spectrum, cancer biology, and impact of genetics on patient survival in CMMRD. METHODS: In this cohort study, we collected cross-sectional and longitudinal data on all patients with CMMRD, with no age limits, registered with the International Replication Repair Deficiency Consortium (IRRDC) across more than 50 countries. Clinical data were extracted from the IRRDC database, medical records, and physician-completed case record forms. The primary objective was to describe the clinical features, cancer spectrum, and biology of the condition. Secondary objectives included estimations of cancer incidence and of the impact of the specific mismatch-repair gene and genotype on cancer onset and survival, including after cancer surveillance and immunotherapy interventions. FINDINGS: We analysed data from 201 patients (103 males, 98 females) enrolled between June 5, 2007 and Sept 9, 2022. Median age at diagnosis of CMMRD or a related cancer was 8·9 years (IQR 5·9-12·6), and median follow-up from diagnosis was 7·2 years (3·6-14·8). Endogamy among minorities and closed communities contributed to high homozygosity within countries with low consanguinity. Frequent dermatological manifestations (117 [93%] of 126 patients with complete data) led to a clinical overlap with neurofibromatosis type 1 (35 [28%] of 126). 339 cancers were reported in 194 (97%) of 201 patients. The cumulative cancer incidence by age 18 years was 90% (95% CI 80-99). Median time between cancer diagnoses for patients with more than one cancer was 1·9 years (IQR 0·8-3·9). Neoplasms developed in 15 organs and included early-onset adult cancers. CNS tumours were the most frequent (173 [51%] cancers), followed by gastrointestinal (75 [22%]), haematological (61 [18%]), and other cancer types (30 [9%]). Patients with CNS tumours had the poorest overall survival rates (39% [95% CI 30-52] at 10 years from diagnosis; log-rank p<0·0001 across four cancer types), followed by those with haematological cancers (67% [55-82]), gastrointestinal cancers (89% [81-97]), and other solid tumours (96% [88-100]). All cancers showed high mutation and microsatellite indel burdens, and pathognomonic mutational signatures. MLH1 or MSH2 variants caused earlier cancer onset than PMS2 or MSH6 variants, and inferior survival (overall survival at age 15 years 63% [95% CI 55-73] for PMS2, 49% [35-68] for MSH6, 19% [6-66] for MLH1, and 0% for MSH2; p<0·0001). Frameshift or truncating variants within the same gene caused earlier cancers and inferior outcomes compared with missense variants (p<0·0001). The greater deleterious effects of MLH1 and MSH2 variants as compared with PMS2 and MSH6 variants persisted despite overall improvements in survival after surveillance or immune checkpoint inhibitor interventions. INTERPRETATION: The very high cancer burden and unique genomic landscape of CMMRD highlight the benefit of comprehensive assays in timely diagnosis and precision approaches toward surveillance and immunotherapy. These data will guide the clinical management of children and patients who survive into adulthood with CMMRD. FUNDING: The Canadian Institutes for Health Research, Stand Up to Cancer, Children's Oncology Group National Cancer Institute Community Oncology Research Program, Canadian Cancer Society, Brain Canada, The V Foundation for Cancer Research, BioCanRx, Harry and Agnieszka Hall, Meagan's Walk, BRAINchild Canada, The LivWise Foundation, St Baldrick Foundation, Hold'em for Life, and Garron Family Cancer Center.
Aga Khan University Hospital Karachi Pakistan
Alfac Cancer and Blood Disorders Center Children's Healthcare of Atlanta Atlanta GA USA
Arthur and Sonia Labatt Brain Tumor Research Centre Toronto ON Canada
Associate Professor of Human Genetics Emory University Atlanta GA USA
Cancer Axis Lady Davis Institute Jewish General Hospital Montreal QC Canada
Center for Personalized Genetic Healthcare Cleveland Clinic Cleveland OH USA
Central Michigan University Mount Pleasant MI USA
CHI Saint Joseph Health Cancer Care Lexington KY USA
Children and Young People's Unit Royal Marsden NHS Foundation Trust London UK
Children's Cancer Centre The Royal Children's Hospital Melbourne VIC Australia
Children's Clinic St Olavs University Hospital Trondheim Norway
Children's Hospital of Eastern Ontario Genetics Ottawa ON Canada
Children's Minnesota Minneapolis MN USA
Clinic of Pediatric Oncology and Hematology University Children's Hospital Banská Bystrica Slovakia
College of Medicine University of Baghdad Paediatric Oncology Unit Baghdad Iraq
Crown Princess Victoria Children's Hospital Linköping University Hospital Linköping Sweden
De La Salle Medical and Health Sciences Institute Dasmariñas Philippines
Department of Clinical Genomics Mayo Clinic Rochester MN USA
Department of Diagnostic Imaging The Hospital for Sick Children Toronto ON Canada
Department of Health Medicine and Caring Sciences Linköping University Linköping Sweden
Department of Hematology Oncology CHU de Quebec Universite Laval Quebec QC Canada
Department of Medical Imaging University of Toronto Toronto ON Canada
Department of Neurosurgery Taipei Veterans General Hospital Taipei Taiwan
Department of Oncology St Jude Children's Research Hospital Memphis TN USA
Department of Pathology Tata Medical Center Rajarhat Kolkata India
Department of Pathology University of Cambridge Cambridge UK
Department of Pediatric Hemato oncology Tata Medical Center Kolkata India
Department of Pediatric Hemato Oncology Tel Aviv Medical Center Tel Aviv Israel
Department of Pediatric Hemato Oncology Tel Aviv Sourasky Medical Center Tel Aviv Israel
Department of Pediatric Hematology and Oncology Atrium Health Charlotte NC USA
Department of Pediatric Hematology and Oncology The Royal Hospital Muscat Oman
Department of Pediatric Hematology Oncology CancerCare Manitoba Winnipeg MB Canada
Department of Pediatric Hematology Oncology Hospital Infantil Universitario Nino Jesus Madrid Spain
Department of Pediatric Hematology Oncology Istanbul University Oncology Institute Istanbul Türkiye
Department of Pediatric Hematology Oncology King Fahad Specialist Hospital Dammam Saudi Arabia
Department of Pediatric Hematology Oncology Prisma Health Columbia SC USA
Department of Pediatric Hematology Oncology Schneider Children's Medical Center Petah Tikva Israel
Department of Pediatric Hematology Oncology University of Michigan Medical School Ann Arbor MI USA
Department of Pediatric Laboratory Medicine The Hospital for Sick Children Toronto ON Canada
Department of Pediatric Neurosurgery Tel Aviv Sourasky Medical Center Tel Aviv Israel
Department of Pediatrics Federal University of Parana Curitiba Parana
Department of Pediatrics Medical College of Wisconsin Milwaukee WI USA
Department of Pediatrics Sahlgrenska Academy University of Gothenburg Gothenburg Sweden
Department of Pediatrics Stanford University School of Medicine Stanford CA USA
Division of Clinical Studies The Institute of Cancer Research London UK
Division of Hematology and Oncology Oregon Health and Science University Portland OR USA
Division of Hematology and Oncology The Hospital for Sick Children Toronto ON Canada
Division of Hematology Oncology IWK Health Halifax NS Canada
Division of Medical Genetics Department of Pediatrics IWK Health Centre Halifax NS Canada
Division of Oncology Children's Hospital of Philadelphia Philadelphia PA USA
Division of Pathology The Hospital for Sick Children Toronto ON Canada
Division of Pediatric Hematology Oncology American University of Beirut Beirut Lebanon
Division of Pediatric Hematology Oncology Stanford Medicine Stanford CA USA
Division of Pediatric Hematology Oncology University of California San Diego CA USA
Division of Rehabilitation Neuropsychology Emory University School of Medicine Atlanta GA USA
Faculty of Medicine Tel Aviv University Tel Aviv Israel
Golisano Children's Hospital SUNY Upstate Syracuse NY USA
Hopp Children's Cancer Center King Fahad Specialist Hospital Dammam Saudi Arabia
Indus Hospital and Health Network Karachi Pakistan
Kid's Cancer Centre Sydney Children's Hospital Sydney NSW Australia
King Hussein Cancer Center Amman Jordan
MAHAK Pediatric Cancer Treatment and Research Tehran Iran
Maine Children's Cancer Program Portland ME USA
Neuro Oncology Division Tel Aviv Medical Center Tel Aviv University Tel Aviv Israel
Ottawa Hospital Research Institute Ottawa ON Canada
Pediatric Oncology Department National Institute of Child Health Karachi Pakistan
Pediatric Oncology Department University Hospital de São João Porto Portugal
Pediatric Unit Fondazione IRCCS Istituto Nazionale dei Tumori Milan Italy
Program in Genetics and Genome Biology The Hospital for Sick Children Toronto ON Canada
Shaukat Khanum Memorial Cancer Hospital and Research Centre Lahore Pakistan
Sheba Medical Center Cancer Research Center Tel Hashomer Israel
South Australia Health and Medical Research Institute Adelaide SA Australia
South Australia Immunogenomics Cancer Institute University of Adelaide Adelaide SA Australia
St Jude Children's Research Hospital Memphis TN USA
Sutter Health Cancer Risk Program Sacramento CA USA
The Genetics Institute and Genomics Center Tel Aviv Sourasky Medical Center Tel Aviv Israel
UCSF Benioff Children's Hospital Oakland Oakland CA USA
University of California San Francisco CA USA
University of Child Health Sciences Children's Hospital Lahore Lahore Pakistan
Valley Children's Hospital Madera CA USA
Wayne State University and Karmanos Cancer Institute Detroit MI USA
Winship Cancer Institute Emory University Hospital Atlanta GA USA
Zane Cohen Centre for Digestive Diseases Sinai Health System Toronto ON Canada
References provided by Crossref.org
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- $a Clinical and biological landscape of constitutional mismatch-repair deficiency syndrome: an International Replication Repair Deficiency Consortium cohort study / $c AB. Ercan, M. Aronson, NR. Fernandez, Y. Chang, A. Levine, ZA. Liu, L. Negm, M. Edwards, V. Bianchi, L. Stengs, J. Chung, A. Al-Battashi, A. Reschke, A. Lion, A. Ahmad, A. Lassaletta, AT. Reddy, AF. Al-Darraji, AC. Shah, A. Van Damme, A. Bendel, A. Rashid, AS. Margol, BL. Kelly, B. Pencheva, B. Heald, B. Lemieux-Anglin, B. Crooks, C. Koschmann, C. Gilpin, CC. Porter, D. Gass, D. Samuel, DS. Ziegler, DT. Blumenthal, DJ. Kuo, D. Hamideh, D. Basel, DA. Khuong-Quang, D. Stearns, E. Opocher, F. Carceller, H. Baris Feldman, H. Toledano, I. Winer, I. Scheers, I. Fedorakova, JM. Su, J. Vengoechea, J. Sterba, J. Knipstein, JR. Hansford, JR. Gonzales-Santos, K. Bhatia, KJ. Bielamowicz, K. Minhas, KE. Nichols, KA. Cole, L. Penney, MA. Hjort, M. Sabel, MJ. Gil-da-Costa, MJ. Murray, M. Miller, ML. Blundell, M. Massimino, M. Al-Hussaini, MF. Al-Jadiry, MA. Comito, M. Osborn, MP. Link, M. Zapotocky, M. Ghalibafian, N. Shaheen, N. Mushtaq, N. Waespe, N. Hijiya, N. Fuentes-Bolanos, O. Ahmad, O. Chamdine, P. Roy, PN. Pichurin, P. Nyman, R. Pearlman, RC. Auer, RK. Sukumaran, R. Kebudi, R. Dvir, R. Raphael, R. Elhasid, RB. McGee, R. Chami, R. Noss, R. Tanaka, S. Raskin, S. Sen, S. Lindhorst, S. Perreault, S. Caspi, S. Riaz, S. Constantini, S. Albert, S. Chaleff, S. Bielack, S. Chiaravalli, SL. Cramer, S. Roy, S. Cahn, S. Penna, SA. Hamid, T. Ghafoor, U. Imam, V. Larouche, V. Magimairajan Issai, WD. Foulkes, YY. Lee, PC. Nathan, YE. Maruvka, MC. Greer, C. Durno, A. Shlien, B. Ertl-Wagner, A. Villani, D. Malkin, C. Hawkins, E. Bouffet, A. Das, U. Tabori
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- $a Ahmad, Olfat $u Hopp Children's Cancer Center, King Fahad Specialist Hospital, Dammam, Saudi Arabia
- 700 1_
- $a Chamdine, Omar $u Department of Pediatric Hematology Oncology, King Fahad Specialist Hospital, Dammam, Saudi Arabia
- 700 1_
- $a Roy, Paromita $u Department of Pathology, Tata Medical Center, Rajarhat, Kolkata, India
- 700 1_
- $a Pichurin, Pavel N $u Department of Clinical Genomics, Mayo Clinic, Rochester, MN, USA
- 700 1_
- $a Nyman, Per $u Crown Princess Victoria Children's Hospital, Linköping University Hospital, Linköping, Sweden; Department of Health, Medicine and Caring Sciences, Linköping University, Linköping, Sweden
- 700 1_
- $a Pearlman, Rachel $u Department of Internal Medicine, The Ohio State University Comprehensive Cancer Center, Columbus, OH, USA
- 700 1_
- $a Auer, Rebecca C $u Ottawa Hospital Research Institute, Ottawa, ON, Canada
- 700 1_
- $a Sukumaran, Reghu K $u Department of Pediatric Hemato-oncology, Tata Medical Center, Kolkata, India
- 700 1_
- $a Kebudi, Rejin $u Department of Pediatric Hematology-Oncology, Istanbul University, Oncology Institute, Istanbul, Türkiye
- 700 1_
- $a Dvir, Rina $u Department of Pediatric Hemato-Oncology, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
- 700 1_
- $a Raphael, Robert $u UCSF Benioff Children's Hospital Oakland, Oakland, CA, USA
- 700 1_
- $a Elhasid, Ronit $u Department of Pediatric Hemato-Oncology, Tel Aviv Medical Center, Tel Aviv, Israel
- 700 1_
- $a McGee, Rose B $u St Jude Children's Research Hospital, Memphis, TN, USA
- 700 1_
- $a Chami, Rose $u Division of Pathology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Noss, Ryan $u Center for Personalized Genetic Healthcare, Cleveland Clinic, Cleveland, OH, USA
- 700 1_
- $a Tanaka, Ryuma $u Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI, USA
- 700 1_
- $a Raskin, Salmo $u Department of Pediatrics, Federal University of Parana, Curitiba, Parana
- 700 1_
- $a Sen, Santanu $u Department of Pediatric Hematology, Oncology, and Bone Marrow Transplant, Kokilaben Dhirubhai Ambani Hospital and Medical Research Institute, Mumbai, India
- 700 1_
- $a Lindhorst, Scott $u Department of Neurosurgery, Division of Neuro-Oncology, Medical University of South Carolina, Charleston, SC, USA
- 700 1_
- $a Perreault, Sebastien $u Division of Child Neurology, Department of Pediatrics, CHU Sainte-Justine, Université de Montréal, Montreal, QC, Canada
- 700 1_
- $a Caspi, Shani $u Sheba Medical Center, Cancer Research Center, Tel Hashomer, Israel
- 700 1_
- $a Riaz, Shazia $u Department of Hematology and Oncology, The Children's Hospital and University of Child Health Sciences, Lahore, Pakistan
- 700 1_
- $a Constantini, Shlomi $u Department of Pediatric Neurosurgery, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
- 700 1_
- $a Albert, Sophie $u Cancer Axis, Lady Davis Institute, Jewish General Hospital, Montreal, QC Canada
- 700 1_
- $a Chaleff, Stanley $u Maine Children's Cancer Program, Portland, ME, USA
- 700 1_
- $a Bielack, Stefan $u Padiatrie 5 (Onkologie, Hamatologie, Immunologie), Zentrum fur Kinder-, Jugend- und Frauenmedizin, Stuttgart Cancer Center, Klinikum Stuttgart-Olgahospital, Stuttgart, Germany
- 700 1_
- $a Chiaravalli, Stefano $u Pediatric Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
- 700 1_
- $a Cramer, Stuart Louis $u Department of Pediatric Hematology/Oncology, Prisma Health, Columbia, SC, USA
- 700 1_
- $a Roy, Sumita $u Central Michigan University, Mount Pleasant, MI, USA; Division of Genetics, Genomic & Metabolic Disorders, Pediatric Cancer Genetics Clinic, Children's Hospital of Michigan, Detroit, MI, USA
- 700 1_
- $a Cahn, Suzanne $u Winship Cancer Institute, Emory University Hospital, Atlanta, GA, USA
- 700 1_
- $a Penna, Suzanne $u Division of Rehabilitation Neuropsychology, Emory University School of Medicine, Atlanta, GA, USA
- 700 1_
- $a Hamid, Syed Ahmer $u Indus Hospital and Health Network, Karachi, Pakistan
- 700 1_
- $a Ghafoor, Tariq $u Department of Hematology and Stem Cell Transplant, Armed Forces Bone Marrow Transplant Center, National Institute of Blood and Marrow Transplant, Rawalpindi, Pakistan
- 700 1_
- $a Imam, Uzma $u Pediatric Oncology Department, National Institute of Child Health, Karachi, Pakistan
- 700 1_
- $a Larouche, Valerie $u Department of Hematology-Oncology, CHU de Quebec-Universite Laval, Quebec, QC, Canada
- 700 1_
- $a Magimairajan Issai, Vanan $u Department of Pediatric Hematology-Oncology, CancerCare Manitoba, Winnipeg, MB, Canada
- 700 1_
- $a Foulkes, William D $u Departments of Oncology and Human Genetics, McGill University Health Centre, Cancer Genetics Program, Montreal, QC, Canada
- 700 1_
- $a Lee, Yi Yen $u Department of Neurosurgery, Taipei Veterans General Hospital, Taipei, Taiwan
- 700 1_
- $a Nathan, Paul C $u Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Maruvka, Yosef E $u Faculty of Biotechnology and Food Engineering, The Lokey Center for Life Science and Engineering, TECHNION-Israel Institute of Technology, Haifa, Israel
- 700 1_
- $a Greer, Mary-Louise C $u Department of Diagnostic and Interventional Radiology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Durno, Carol $u Division of Gastroenterology, Hepatology, and Nutrition, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Shlien, Adam $u Program in Genetics and Genome Biology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Ertl-Wagner, Birgit $u Department of Diagnostic Imaging, The Hospital for Sick Children, Toronto, ON, Canada; Department of Medical Imaging, University of Toronto, Toronto, ON, Canada
- 700 1_
- $a Villani, Anita $u Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Malkin, David $u Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Hawkins, Cynthia $u Department of Pediatric Laboratory Medicine, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Bouffet, Eric $u Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Das, Anirban $u Arthur and Sonia Labatt Brain Tumor Research Centre, Toronto, ON, Canada; Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada
- 700 1_
- $a Tabori, Uri $u Arthur and Sonia Labatt Brain Tumor Research Centre, Toronto, ON, Canada; Division of Hematology and Oncology, The Hospital for Sick Children, Toronto, ON, Canada. Electronic address: uri.tabori@sickkids.ca
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