Epidemiologic Factors in Relation to Colorectal Cancer Risk and Survival by Genotoxic Colibactin Mutational Signature-Reference-Cited by-同舟云学术

Epidemiologic Factors in Relation to Colorectal Cancer Risk and Survival by Genotoxic Colibactin Mutational Signature

Published:2024-01-22 Issue:4 Volume:33 Page:534-546
ISSN:1055-9965
Container-title:Cancer Epidemiology, Biomarkers & Prevention
language:en
Short-container-title:

Author:

Thomas Claire E.¹^ORCID,Georgeson Peter²³^ORCID,Qu Conghui¹^ORCID,Steinfelder Robert S.¹^ORCID,Buchanan Daniel D.²³⁴^ORCID,Song Mingyang⁵⁶⁷^ORCID,Harrison Tabitha A.¹^ORCID,Um Caroline Y.⁸^ORCID,Hullar Meredith A.¹^ORCID,Jenkins Mark A.⁹^ORCID,Van Guelpen Bethany¹⁰¹¹^ORCID,Lynch Brigid M.⁹¹²^ORCID,Melaku Yohannes Adama¹²¹³^ORCID,Huyghe Jeroen R.¹^ORCID,Aglago Elom K.¹⁴^ORCID,Berndt Sonja I.¹⁵^ORCID,Boardman Lisa A.¹⁶^ORCID,Campbell Peter T.¹⁷^ORCID,Cao Yin¹⁸¹⁹²⁰^ORCID,Chan Andrew T.⁷²¹²²²³²⁴²⁵^ORCID,Drew David A.²⁶^ORCID,Figueiredo Jane C.²⁷^ORCID,French Amy J.²⁸^ORCID,Giannakis Marios²⁹³⁰³¹^ORCID,Goode Ellen L.³²^ORCID,Gruber Stephen B.³³^ORCID,Gsur Andrea³⁴^ORCID,Gunter Marc J.³⁵³⁶^ORCID,Hoffmeister Michael³⁷^ORCID,Hsu Li¹³⁸^ORCID,Huang Wen-Yi¹⁵^ORCID,Moreno Victor³⁹⁴⁰⁴¹⁴²^ORCID,Murphy Neil⁴³^ORCID,Newcomb Polly A.¹⁴⁴^ORCID,Newton Christina C.⁸^ORCID,Nowak Jonathan A.⁴⁵⁴⁶^ORCID,Obón-Santacana Mireia³⁹⁴⁰⁴¹^ORCID,Ogino Shuji⁴⁵⁴⁷⁴⁸⁴⁹^ORCID,Sun Wei¹^ORCID,Toland Amanda E.⁵⁰^ORCID,Trinh Quang M.⁵¹^ORCID,Ugai Tomotaka⁷^ORCID,Zaidi Syed H.⁵¹^ORCID,Peters Ulrike¹⁴⁴^ORCID,Phipps Amanda I.¹⁴⁴^ORCID

Affiliation:

1. 1Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, Washington.

2. 2Colorectal Oncogenomics Group, Department of Clinical Pathology, Melbourne Medical School, The University of Melbourne, Parkville, Australia.

3. 3University of Melbourne Centre for Cancer Research, The University of Melbourne, Parkville, Australia.

4. 4Genomic Medicine and Family Cancer Clinic, The Royal Melbourne Hospital, Parkville, Victoria, Australia.

5. 5Department of Nutrition, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.

6. 6Clinical and Translational Epidemiology Unit and Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

7. 7Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.

8. 8Department of Population Science, American Cancer Society, Atlanta, Georgia.

9. 9Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Victoria, Australia.

10. 10Department of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.

11. 11Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden.

12. 12Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.

13. 13FHMRI Sleep, College of Medicine and Public Health, Flinders University, Adelaide, South Australia, Australia.

14. 14Department of Epidemiology and Biostatistics, Imperial College London, School of Public Health, London, UK.

15. 15Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.

16. 16Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota.

17. 17Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, New York.

18. 18Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St Louis, Missouri.

19. 19Alvin J. Siteman Cancer Center at Barnes-Jewish Hospital and Washington University School of Medicine, St. Louis, Missouri.

20. 20Division of Gastroenterology, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri.

21. 21Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

22. 22Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.

23. 23Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

24. 24Broad Institute of Harvard and MIT, Cambridge, Massachusetts.

25. 25Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.

26. 26Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

27. 27Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California.

28. 28Division of Laboratory Genetics, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota.

29. 29Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.

30. 30Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

31. 31Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.

32. 32Department of Quantitative Health Sciences, Division of Epidemiology, Mayo Clinic, Rochester, Minnesota.

33. 33Department of Medical Oncology and Therapeutics Research and Center for Precision Medicine, City of Hope National Medical Center, Duarte, California.

34. 34Center for Cancer Research, Medical University of Vienna, Vienna, Austria.

35. 35Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.

36. 36Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, Norfolk Place, London, UK.

37. 37Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.

38. 38Department of Biostatistics, University of Washington, Seattle, Washington.

39. 39Unit of Biomarkers and Susceptibility (UBS), Oncology Data Analytics Program (ODAP), Catalan Institute of Oncology (ICO), L'Hospitalet del Llobregat, Barcelona, Spain.

40. 40ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

41. 41Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain.

42. 42Department of Clinical Sciences, Faculty of Medicine and health Sciences and Universitat de Barcelona Institute of Complex Systems (UBICS), University of Barcelona (UB), L'Hospitalet de Llobregat, Barcelona, Spain.

43. 43Nutrition and Metabolism Section, International Agency for Research on Cancer, World Health Organization, Lyon, France.

44. 44Department of Epidemiology, University of Washington, Seattle, Washington.

45. 45Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.

46. 46Department of Pathology, Dana-Farber Cancer Institute, Boston, Massachusetts.

47. 47Department of Oncologic Pathology, Dana-Farber Cancer Institute, Boston, Massachusetts.

48. 48Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

49. 49Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

50. 50Departments of Cancer Biology and Genetics and Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio.

51. 51Ontario Institute for Cancer Research, Toronto, Ontario, Canada.

Abstract

Abstract Background: The genotoxin colibactin causes a tumor single-base substitution (SBS) mutational signature, SBS88. It is unknown whether epidemiologic factors’ association with colorectal cancer risk and survival differs by SBS88. Methods: Within the Genetic Epidemiology of Colorectal Cancer Consortium and Colon Cancer Family Registry, we measured SBS88 in 4,308 microsatellite stable/microsatellite instability low tumors. Associations of epidemiologic factors with colorectal cancer risk by SBS88 were assessed using multinomial regression (N = 4,308 cases, 14,192 controls; cohort-only cases N = 1,911), and with colorectal cancer–specific survival using Cox proportional hazards regression (N = 3,465 cases). Results: 392 (9%) tumors were SBS88 positive. Among all cases, the highest quartile of fruit intake was associated with lower risk of SBS88-positive colorectal cancer than SBS88-negative colorectal cancer [odds ratio (OR) = 0.53, 95% confidence interval (CI) 0.37-0.76; OR = 0.75, 95% CI 0.66–0.85, respectively, Pheterogeneity = 0.047]. Among cohort studies, associations of body mass index (BMI), alcohol, and fruit intake with colorectal cancer risk differed by SBS88. BMI ≥30 kg/m2 was associated with worse colorectal cancer–specific survival among those SBS88-positive [hazard ratio (HR) = 3.40, 95% CI 1.47–7.84], but not among those SBS88-negative (HR = 0.97, 95% CI 0.78–1.21, Pheterogeneity = 0.066). Conclusions: Most epidemiologic factors did not differ by SBS88 for colorectal cancer risk or survival. Higher BMI may be associated with worse colorectal cancer–specific survival among those SBS88-positive; however, validation is needed in samples with whole-genome or whole-exome sequencing available. Impact: This study highlights the importance of identification of tumor phenotypes related to colorectal cancer and understanding potential heterogeneity for risk and survival.

Funder

National Institutes of Health

Herzfelder'sche Familienstiftung

Austrian Research Funding Agency

American Cancer Society

Instituto de Salud Carlos III

Junta de Castilla y León

Spanish Association Against Cancer

German Research Council

German Federal Ministry of Education and Research

International Agency for Research on Cancer

Australian NHMRC