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Cumulative Incidence of Cancer Among Persons With HIV in North America: A Cohort StudyCumulative Incidence of Cancer Among Persons With HIV in North America

Michael J. Silverberg, PhD, MPH*; Bryan Lau, PhD, MHS*; Chad J. Achenbach, MD, MPH; Yuezhou Jing, MS; Keri N. Althoff, PhD, MPH; Gypsyamber D'Souza, PhD; Eric A. Engels, MD, MPH; Nancy A. Hessol, MSPH; John T. Brooks, MD; Ann N. Burchell, PhD, MSc; M. John Gill, MB ChB, MSc; James J. Goedert, MD; Robert Hogg, PhD; Michael A. Horberg, MD, MAS; Gregory D. Kirk, MD, PhD, MPH; Mari M. Kitahata, MD, MPH; Philip T. Korthuis, MD, MPH; William C. Mathews, MD, MSPH; Angel Mayor, MD, MSc; Sharada P. Modur, PhD; Sonia Napravnik, PhD; Richard M. Novak, MD; Pragna Patel, MD, MPH; Anita R. Rachlis, MD, MEd; Timothy R. Sterling, MD; James H. Willig, MD, MSPH; Amy C. Justice, MD, PhD; Richard D. Moore, MD, MHS; Robert Dubrow, MD, PhD, for the North American AIDS Cohort Collaboration on Research and Design of the International Epidemiologic Databases to Evaluate AIDS
[+] Article, Author, and Disclosure Information

* Drs. Silverberg and Lau contributed equally to this work.

† For members of the North American AIDS Cohort Collaboration on Research and Design of the International Epidemiologic Databases to Evaluate AIDS, see Appendix 1.


From Kaiser Permanente Northern California, Oakland, California; Johns Hopkins School of Medicine and Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; Northwestern University Feinberg School of Medicine, Center for Global Health, Lurie Cancer Center, and College of Medicine, University of Illinois at Chicago, Chicago, Illinois; National Cancer Institute, National Institutes of Health, Bethesda, Maryland; University of California, San Francisco, San Francisco, California; Centers for Disease Control and Prevention, Atlanta, Georgia; Ontario HIV Treatment Network, Dalla Lana School of Public Health, and Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada; University of Calgary, Calgary, Alberta, Canada; British Columbia Centre for Excellence in HIV/AIDS, Vancouver, British Columbia, Canada; Faculty of Health Sciences, Simon Fraser University, Burnaby, British Columbia, Canada; Mid-Atlantic Permanente Research Institute, Kaiser Permanente, Rockville, Maryland; University of Washington, Seattle, Washington; Oregon Health and Sciences University, Portland, Oregon; University of California, San Diego, San Diego, California; Retrovirus Research Center, Universidad Central del Caribe School of Medicine, Bayamón, Puerto Rico; School of Medicine, University of North Carolina, Chapel Hill, North Carolina; Vanderbilt University, Nashville, Tennessee; University of Alabama, Birmingham, Alabama; Veterans Affairs Connecticut Healthcare System and Yale University Schools of Medicine and Public Health, New Haven, Connecticut.

Grant Support: By the National Institutes of Health (grants U01-AI069918, U01-AA013566, U01-AA020790, U01-AI31834, U01-AI34989, U01-AI34993, U01-AI34994, U01-AI35004, U01-AI35039, U01-AI35040, U01-AI35041, U01-AI35042, UM1-AI35043, U01-AI37613, U01-AI37984, U01-AI38855, U01-AI38858, U01-AI42590, U01-AI68634, U01-AI68636, U01-AI69432, U01-AI69434, U01-DA036935, U01-HD32632, U10-EY08052, U10-EY08057, U10-EY08067, U24-AA020794, U54-MD007587, UL1-RR024131, UL1-TR000083, F31-DA037788, G12- MD007583, K01-AI071754, K01-AI093197, K23-EY013707, K24-DA00432, K24-AI065298, KL2-TR000421, MO1-RR-00052, N02-CP55504, P30-AI027763, P30-AI094189, P30-AI27757, P30-AI27767, P30-AI036219, P30-AI50410, P30-AI54999, P30-MH62246, R01-AA16893, R01-CA165937, R01-DA04334, R01-DA11602, R01-DA12568, R24-AI067039, R56-AI102622, Z01-CP010214, and Z01-CP010176); Centers for Disease Control and Prevention (contract CDC200-2006-18797); Agency for Healthcare Research and Quality (contract 90047713); Health Resources and Services Administration (contract 90051652); Canadian Institutes of Health Research (grants TGF-96118, HCP-97105, CBR-86906, and CBR-94036); Canadian Institutes of Health Research New Investigator award (Dr. Burchell); Ontario Ministry of Health and Long Term Care; and the government of Alberta, Canada. Additional support was provided by the Intramural Research Program of the National Cancer Institute and the National Institutes of Health.

Disclosures: Dr. Silverberg reports grants from Pfizer and grants from Merck outside the submitted work. Dr. Lau reports grants from National Institutes of Health during the conduct of the study. Dr. Althoff reports grants from National Institutes of Health during the conduct of the study and personal fees from Gilead Sciences outside the submitted work. Ms. Hessol reports grants from the National Institutes of Health during the conduct of the study. Dr. Horberg reports grants from the National Institute of Allergy and Infectious Diseases during the conduct of the study. Dr. Mathews reports grants from National Institutes of Health during the conduct of the study. Dr. Novak reports other from Merck, Gilead, GlaxoSmithKline, Genosea, and Nordique outside the submitted work. Dr. Rachlis reports grants from the Ontario HIV Treatment Network for the Ontario Cohort Study during the conduct of the study. Dr. Sterling reports grants from the National Institutes of Health during the conduct of the study. Dr. Moore reports grants from the National Institutes of Health during the conduct of the study. Dr. Dubrow reports grants from the National Cancer Institute during the conduct of the study. Authors not named here have disclosed no conflicts of interest. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M14-2768.

Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that she has no financial relationships or interests to disclose. Darren B. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Cynthia D. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose. Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Catharine B. Stack, PhD, MS, Deputy Editor for Statistics, reports that she has stock holdings in Pfizer.

Reproducible Research Statement:Study protocol: Available at www.naaccord.org. Statistical code and data set: Available from Dr. Lau (e-mail, blau@jhu.edu).

Requests for Single Reprints: Michael J. Silverberg, PhD, MPH, Research Scientist, Kaiser Permanente Division of Research, 2000 Broadway, 2nd Floor, Oakland, CA 94612; e-mail, Michael.J.Silverberg@kp.org.

Current Author Addresses: Dr. Silverberg: Research Scientist, Kaiser Permanente Division of Research, 2000 Broadway, 2nd Floor, Oakland, CA 94612.

Dr. Lau: Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Room E7150, Baltimore, MD 21205.

Dr. Achenbach: Division of Infectious Diseases, Center for Global Health, Northwestern University, 645 North Michigan Avenue, Suite 1058, Chicago, IL 60611.

Mr. Jing: Johns Hopkins Bloomberg School of Public Health, 111 Market Place, Suite 906, Baltimore, MD 21202.

Dr. Althoff: Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Room E7137, Baltimore, MD 21205.

Dr. D'Souza: Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Room E6132B, Baltimore, MD 21205.

Dr. Engels: Division of Cancer Epidemiology and Genetics, National Cancer Institute, 9609 Medical Center Drive, Room 6E226 MSC 9767, Bethesda, MD 20892.

Ms. Hessol: Department of Medicine, University of California, San Francisco, 3333 California Street, Suite 420, San Francisco, CA 94143.

Dr. Brooks: Division of HIV/AIDS Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Office of Infectious Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road Northeast, Mailstop E-45, Atlanta, GA 30329-4018.

Dr. Burchell: Ontario HIV Treatment Network, 1300 Yonge Street, Suite 600, Toronto, Ontario M4T 1X3, Canada.

Mr. Gill: Southern Alberta HIV Clinic, Sheldon M. Chumir Health Centre, #3223, 1213 4th Street Southwest, Calgary, Alberta T2R 0X7, Canada.

Dr. Goedert: Division of Cancer Epidemiology and Genetics, National Cancer Institute, Shady Grove, Room 6E106, Bethesda, MD 20892.

Dr. Hogg: BC Centre for Excellence in HIV/AIDS, St. Paul's Hospital, 608–1081 Burrard Street, Vancouver, British Columbia V6Z 1Y6, Canada.

Dr. Horberg: Mid-Atlantic Permanente Research Institute, 2101 East Jefferson Street, 3 East, Rockville, MD 20852.

Dr. Kirk: Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Room E6533, Baltimore, MD 21205.

Dr. Kitahata: University of Washington Center for AIDS Research, 325 Ninth Avenue, Box 359931, Seattle, WA 98104-2499.

Dr. Korthuis: Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L475, Portland, OR 97239-3098.

Dr. Mathews: University of California, San Diego Owen Clinic, University of California, San Diego Health System, University of California, San Diego Medical Center, 8681 200 West Arbor Drive, San Diego, CA 92103.

Dr. Mayor: Universidad Central del Caribe, PO Box 60327, Bayamón, PR 00960-6032.

Dr. Modur: Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Room E7014, Baltimore, MD 21205.

Dr. Napravnik: University of North Carolina School of Medicine, CB#; 7215, 130 Mason Farm Road, 2101 Bioinformatics Building, Chapel Hill, NC 27599-7215.

Dr. Novak: Department of Medicine, University of Illinois, Chicago, 808 South Wood Street, Room 888, CSN (MC 735), Chicago, IL 60612.

Dr. Patel: Centers for Disease Control and Prevention, Center of Global Health, Non-Communicable Diseases Unit, 1600 Clifton Road, MS E-93, Atlanta, GA 30333.

Dr. Rachlis: Sunnybrook Health Sciences Centre, Infectious Diseases Division, 2075 Bayview Avenue, Suite B1-03, Toronto, Ontario M4N 3M5, Canada.

Dr. Sterling: Vanderbilt University Medical Center, Section of Infectious Disease, A2200 Medical Center North, 1161 21st Avenue South, Nashville, TN 37232-0146.

Dr. Willig: University of Alabama at Birmingham, 1900 University Boulevard, THT 229, Birmingham, AL 35294.

Dr. Justice: Veterans Affairs Connecticut Healthcare System, 950 Campbell Avenue, 11-ACSLG, West Haven, CT 06516.

Dr. Moore: Johns Hopkins University, 1830 East Monument Street, Room 8059, Baltimore, MD 21287.

Dr. Dubrow: Yale School of Public Health, PO Box 208034, New Haven, CT 06520-8034.

Author Contributions: Conception and design: M.J. Silverberg, B. Lau, C.J. Achenbach, M.J. Gill, M.A. Horberg, R. Dubrow.

Analysis and interpretation of the data: M.J. Silverberg, B. Lau, C.J. Achenbach, Y. Jing, J.T. Brooks, M.J. Gill, J.J. Goedert, R. Hogg, M.A. Horberg, G.D. Kirk, A. Mayor, S. Napravnik, P. Patel, A.R. Rachlis, T.R. Sterling, J.H. Willig, A.C. Justice, R.D. Moore, R. Dubrow.

Drafting of the article: M.J. Silverberg, B. Lau, C.J. Achenbach, Y. Jing, G. D'Souza, N.A. Hessol, J.T. Brooks, M.J. Gill, A. Mayor, R.D. Moore, R. Dubrow.

Critical revision of the article for important intellectual content: M.J. Silverberg, B. Lau, K.N. Althoff, G. D'Souza, E.A. Engels, N.A. Hessol, J.T. Brooks, A.N. Burchell, M.J. Gill, J.J. Goedert, R. Hogg, M.A. Horberg, G.D. Kirk, M.M. Kitahata, P.T. Korthuis, A. Mayor, S. Napravnik, R.M. Novak, P. Patel, T.R. Sterling, J.H. Willig, A.C. Justice, R.D. Moore, R. Dubrow.

Final approval of the article: M.J. Silverberg, B. Lau, C.J. Achenbach, Y. Jing, K.N. Althoff, G. D'Souza, E.A. Engels, N.A. Hessol, J.T. Brooks, A.N. Burchell, M.J. Gill, J.J. Goedert, R. Hogg, M.A. Horberg, G.D. Kirk, M.M. Kitahata, P.T. Korthuis, W.C. Mathews, A. Mayor, S.P. Modur, S. Napravnik, R.M. Novak, P. Patel, A.R. Rachlis, T.R. Sterling, J.H. Willig, A.C. Justice, R.D. Moore, R. Dubrow.

Provision of study materials or patients: M.J. Silverberg, N.A. Hessol, J.T. Brooks, M.J. Gill, J.J. Goedert, G.D. Kirk, W.C. Mathews, S. Napravnik, R.M. Novak, A.R. Rachlis, J.H. Willig, A.C. Justice, R.D. Moore.

Statistical expertise: B. Lau, Y. Jing, K.N. Althoff, S. Napravnik.

Obtaining of funding: M.J. Silverberg, M.J. Gill, J.J. Goedert, A.C. Justice, R.D. Moore, R. Dubrow.

Administrative, technical, or logistic support: C.J. Achenbach, A.N. Burchell, M.J. Gill, S.P. Modur, A.R. Rachlis, J.H. Willig, A.C. Justice.

Collection and assembly of data: M.J. Silverberg, C.J. Achenbach, K.N. Althoff, N.A. Hessol, A.N. Burchell, M.J. Gill, R. Hogg, M.A. Horberg, G.D. Kirk, M.M. Kitahata, P.T. Korthuis, S. Napravnik, R.M. Novak, A.R. Rachlis, T.R. Sterling, J.H. Willig, A.C. Justice, R.D. Moore.


Ann Intern Med. 2015;163(7):507-518. doi:10.7326/M14-2768
Text Size: A A A

Background: Cancer is increasingly common among persons with HIV.

Objective: To examine calendar trends in cumulative cancer incidence and hazard rate by HIV status.

Design: Cohort study.

Setting: North American AIDS Cohort Collaboration on Research and Design during 1996 to 2009.

Participants: 86 620 persons with HIV and 196 987 uninfected adults.

Measurements: Cancer type–specific cumulative incidence by age 75 years and calendar trends in cumulative incidence and hazard rates, each by HIV status.

Results: Cumulative incidences of cancer by age 75 years for persons with and without HIV, respectively, were as follows: Kaposi sarcoma, 4.4% and 0.01%; non-Hodgkin lymphoma, 4.5% and 0.7%; lung cancer, 3.4% and 2.8%; anal cancer, 1.5% and 0.05%; colorectal cancer, 1.0% and 1.5%; liver cancer, 1.1% and 0.4%; Hodgkin lymphoma, 0.9% and 0.09%; melanoma, 0.5% and 0.6%; and oral cavity/pharyngeal cancer, 0.8% and 0.8%. Among persons with HIV, calendar trends in cumulative incidence and hazard rate decreased for Kaposi sarcoma and non-Hodgkin lymphoma. For anal, colorectal, and liver cancer, increasing cumulative incidence, but not hazard rate trends, were due to the decreasing mortality rate trend (−9% per year), allowing greater opportunity to be diagnosed. Despite decreasing hazard rate trends for lung cancer, Hodgkin lymphoma, and melanoma, cumulative incidence trends were not seen because of the compensating effect of the declining mortality rate.

Limitation: Secular trends in screening, smoking, and viral co-infections were not evaluated.

Conclusion: Cumulative cancer incidence by age 75 years, approximating lifetime risk in persons with HIV, may have clinical utility in this population. The high cumulative incidences by age 75 years for Kaposi sarcoma, non-Hodgkin lymphoma, and lung cancer support early and sustained antiretroviral therapy and smoking cessation.

Primary Funding Source: National Institutes of Health.

Figures

Grahic Jump Location
Figure 1.

Cumulative cancer incidence for persons with HIV, by calendar era and cancer type with age as the time scale, NA-ACCORD, 1996–2009.

Cumulative incidence (i.e., cancer risk) curves were obtained using nonparametric estimators for competing risk events. Numbers associated with curves represent cumulative incidence by age 75 y. NA-ACCORD = North American AIDS Cohort Collaboration on Research and Design.

* P < 0.05 compared with reference (1996–1999 era).

P < 0.01 compared with reference (1996–1999 era).

Grahic Jump Location
Grahic Jump Location
Figure 2.

Cumulative cancer incidence for uninfected persons, by calendar era and cancer type with age as the time scale, NA-ACCORD, 1996–2009.

Cumulative incidence (i.e., cancer risk) curves were obtained using nonparametric estimators for competing risk events. Numbers associated with curves represent cumulative incidence by age 75 y. NA-ACCORD = North American AIDS Cohort Collaboration on Research and Design.

* P < 0.05 compared with reference (1996–1999 era).

P < 0.01 compared with reference (1996–1999 era).

Grahic Jump Location

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