Mi Ah Han, MD, PhD; Dena Zeraatkar, MSc; Gordon H. Guyatt, MD; Robin W.M. Vernooij, PhD; Regina El Dib, PhD; Ying Zhang, PhD; Abdullah Algarni, MBBS; Gareth Leung, BHSc; Dawid Storman, MD; Claudia Valli, MSc; Montserrat Rabassa, PhD; Nadia Rehman, BDS; Michael K. Parvizian, BHSc; Max Zworth, BA⪼ Jessica J. Bartoszko, HBSc; Luciane Cruz Lopes, PhD; Daegan Sit, MD; Malgorzata M. Bala, MD, PhD; Pablo Alonso-Coello, MD, PhD; Bradley C. Johnston, PhD
Note: Drs. Han, Guyatt, and Johnston and Ms. Zeraatkar act as the guarantors of this article.
Acknowledgment: The authors thank Thomasin Adams-Webber (Hospital for Sick Children) for her help designing the search strategy.
Disclosures: Dr. El Dib received a São Paulo Research Foundation (FAPESP) (2018/11205-6) scholarship and funding from the National Council for Scientific and Technological Development (CNPq) (CNPq 310953/2015-4) and the Faculty of Medicine, Dalhousie University. Dr. Johnston received a grant from Texas A&M AgriLife Research to fund investigator-driven research related to saturated and polyunsaturated fats within the 36-month reporting period required by the International Committee of Medical Journal Editors, as well as funding received from the International Life Science Institute (North America) that ended before the 36-month reporting period. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M19-0699.
Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that her spouse has stock options/holdings with Targeted Diagnostics and Therapeutics. Darren B. Taichman, MD, PhD, Executive 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. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Catharine B. Stack, PhD, MS, Deputy Editor, Statistics, reports that she has stock holdings in Pfizer, Johnson & Johnson, and Colgate-Palmolive. Christina C. Wee, MD, MPH, Deputy Editor, reports employment with Beth Israel Deaconess Medical Center. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Yu-Xiao Yang, MD, MSCE, Deputy Editor, reports that he has no financial relationships or interest to disclose.
>Reproducible Research Statement: Study protocol: Registered in PROSPERO (CRD42017074074). Statistical code: See Methods and Appendix. Code is available on request. Data set: See the tables and Appendix. Data are available on request from Dr. Han (e-mail, firstname.lastname@example.org).
Corresponding Author: Gordon H. Guyatt, MD, Department of Health Research Methods, Evidence and Impact, McMaster University, 1280 Main Street West, Hamilton, Ontario L8N 3Z5, Canada; e-mail, email@example.com.
Current Author Addresses: Dr. Han: Department of Preventive Medicine, College of Medicine, Chosun University, 309 Pilmun-daero, Dong-gu, Gwangju 61452, Korea.
Ms. Zeraatkar, Drs. Guyatt and Rehman, Mr. Leung, Mr. Parvizian, Mr. Zworth, and Ms. Bartoszko: McMaster University Health Sciences Center, 1280 Main Street West, Hamilton, Ontario L8S 4L8, Canada.
Dr. Vernooij: Department of Research, Netherlands Comprehensive Cancer Organisationn, Godebaldkwartier 419, Utrecht 3511DT, the Netherlands.
Dr. El Dib: Institute of Science and Technology, Universidade Estadual Paulista, Avenida Engenheiro Francisco José Longo, 777, Jardim São Dimas, São José dos Campos, Sao Paolo 12245-000, Brazil.
Dr. Zhang: Center for Evidence-based Chinese Medicine, Beijing University, 11 Beisanhuan Dong Lu, Chaoyang District, Beijing 100029, China.
Dr. Algarni: Department of Internal Medicine, Aseer Central Hospital, 4076 Al Muruj, Unit 3, Al Rabwah, Abha 62523, Saudi Arabia.
Drs. Storman and Bala: Department of Hygiene and Dietetics, Jagiellonian University Medical College, 7 Kopernika Street, Kraków 31-034, Poland.
Ms. Valli and Drs. Rabassa and Alonso-Coello: Iberoamerican Cochrane Centre, Instituto de Investigación Biomédica de Sant Pau (IIB Sant Pau-CIBERESP), Carrer de Sant Antoni Maria Claret, 167, Barcelona 08025, Spain.
Dr. Lopes: University of Sorocaba (UNISO), Rodovia Raposo Tavares, Km 92,5, Sorocaba, Sao Paulo 180230-000, Brazil.
Dr. Sit: University of British Columbia, 107-1165 West 13th Avenue, Vancouver, British Columbia V6H 1N4, Canada.
Dr. Johnston: Department of Community Health and Epidemiology, Centre for Clinical Research, Dalhousie University, 5790 University Avenue, Room 404, Halifax, Nova Scotia B3J 0E4, Canada.
Author Contributions: Conception and design: M.A. Han, D. Zeraatkar, G.H. Guyatt, M.M. Bala, P. Alonso-Coello, B.C. Johnston.
Analysis and interpretation of the data: M.A. Han, D. Zeraatkar, R. El Dib, M. Rabassa, N. Rehman, D. Sit, M.M. Bala, P. Alonso-Coello, B.C. Johnston.
Drafting of the article: M.A. Han, R. El Dib, D. Sit, B.C. Johnston.
Critical revision of the article for important intellectual content: M.A. Han, D. Zeraatkar, G.H. Guyatt, R.W.M. Vernooij, D. Sit, M.M. Bala, P. Alonso-Coello, B.C. Johnston.
Final approval of the article: M.A. Han, D. Zeraatkar, G.H. Guyatt, R.W.M. Vernooij, R. El Dib, Y. Zhang, A. Algarni, G. Leung, D. Storman, C. Valli, M. Rabassa, N. Rehman, M.K. Parvizian, M. Zworth, J.J. Bartoszko, L.C. Lopes, D. Sit, M.M. Bala, P. Alonso-Coello, B.C. Johnston.
Statistical expertise: M.A. Han, D. Zeraatkar.
Administrative, technical, or logistic support: M.A. Han, D. Zeraatkar.
Collection and assembly of data: M.A. Han, D. Zeraatkar, R.W.M. Vernooij, Y. Zhang, A. Algarni, G. Leung, D. Storman, C. Valli, M. Rabassa, M.K. Parvizian, M. Zworth, J.J. Bartoszko, L.C. Lopes, D. Sit, B.C. Johnston.
This article has been corrected. The original version (PDF) is appended to this article as a Supplement.
Cancer incidence has continuously increased over the past few centuries and represents a major health burden worldwide.
To evaluate the possible causal relationship between intake of red and processed meat and cancer mortality and incidence.
Embase, Cochrane Central Register of Controlled Trials, Web of Science, CINAHL, and ProQuest from inception until July 2018 and MEDLINE from inception until April 2019 without language restrictions.
Cohort studies that included more than 1000 adults and reported the association between consumption of unprocessed red and processed meat and cancer mortality and incidence.
Teams of 2 reviewers independently extracted data and assessed risk of bias; 1 reviewer evaluated the certainty of evidence, which was confirmed or revised by the senior reviewer.
Of 118 articles (56 cohorts) with more than 6 million participants, 73 articles were eligible for the dose–response meta-analyses, 30 addressed cancer mortality, and 80 reported cancer incidence. Low-certainty evidence suggested that an intake reduction of 3 servings of unprocessed meat per week was associated with a very small reduction in overall cancer mortality over a lifetime. Evidence of low to very low certainty suggested that each intake reduction of 3 servings of processed meat per week was associated with very small decreases in overall cancer mortality over a lifetime; prostate cancer mortality; and incidence of esophageal, colorectal, and breast cancer.
Limited causal inferences due to residual confounding in observational studies, risk of bias due to limitations in diet assessment and adjustment for confounders, recall bias in dietary assessment, and insufficient data for planned subgroup analyses.
The possible absolute effects of red and processed meat consumption on cancer mortality and incidence are very small, and the certainty of evidence is low to very low.
None. (PROSPERO: CRD42017074074)
Evidence search and selection.
Table 1. Summary of Findings for Reduction of Unprocessed Red Meat Intake (3 Servings per Week) and Cancer Mortality and Incidence
Nonlinear association between processed meat intake and breast cancer incidence.
The solid black line represents the point estimate, the shaded region represents the 95% CIs, and the tick marks represent the positions of the study-specific estimates.
Table 2. Summary of Findings for Reduction of Processed Meat Intake (3 Servings per Week) and Cancer Mortality and Incidence
Nonlinear association between intake of mixed unprocessed red and processed meat and breast cancer incidence.
Richard M Fleming, PhD, MD, JD (FHHI-OI-Camelot); Matthew R. Fleming, BS, NRP (FHHI-OI-Camelot); William C. Dooley, MD (OUHSC); Tapan K Chaudhuri, MD (Eastern Virginia Medical School)
FHHI-OI-Camelot; Oklahoma University Health Science Center; Eastern Virginia Medical School
February 23, 2020
Conflict of Interest:
FMTVDM issued to first author.
Using Qualitative Observational Studies with a Relative GRADED Scale to declare that there is only a small risk of cancer from Red and Processed Meat Consumption - is a Very Premature Statement.
The paper in Annals – as with the other papers included in this series discussing Red and Processed Meats – with its comment made by Mi Ah Han, et al  that “red meat’s effect on cancer over a lifetime of exposure was, however, very small, and the overall certainty of evidence was low or very low” represents a premature statement. The observational methods used by the authors, looking at a collection of studies, which looked for the qualitative presence or absence of disease – in this instance CANCER - and a “graded” system of comparisons, severely limits the conclusions the authors can scientifically make regarding the impact of Red and Processed meat consumption. As already established, the use of qualitative and semi-quantitative information – while acceptable in horseshoes – is woefully inadequate in medicine [2-4] and even more inadequate when making generalized statements regarding the effect of any treatment including dietary. We would encourage the authors and readers of Annals to cautiously consider such statements and the need to quantitatively measure  tissue changes associated with any treatment group including considerations of specific foods. References:1. Han MA, Zeraatkar D, Guyatt GH, et al. Reduction of Red and Processed Meat Intake and Cancer Mortality and Incidence: A Systematic Review and Meta-analysis of Cohort Studies. Ann Intern Med. 2019;171:711–720. [Epub ahead of print 1 October 2019]. doi: https://doi.org/10.7326/M19-06992. Fleming RM, Fleming MR, Chaudhuri TK. Evidence Based Medicine – Accurately Diagnosing Cancer. Austin J Women’s Health 2019;6(1):1036. 3. Fleming RM, Fleming MR, Chaudhuri TK, Dooley WC. Independent Study Validating FMTVDM Measurements of Breast Cancer and Transitional Tissue Changes with Confirmation of Gompertz Function & Laird Model. Inter J Res Studies Med & Health Sci. 2019;4(10):21-26. ISSN:2456-6373. 4. Fleming RM, Fleming MR, Dooley WC, Chaudhuri TK. Invited Editorial. The Importance of Differentiating Between Qualitative, Semi-Quantitative and Quantitative Imaging – Close Only Counts in Horseshoes. Eur J Nucl Med Mol Imaging. DOI:10.1007/s00259-019-04668-y. Published online 17 January 2020 https://link.springer.com/article/10.1007/s00259-019-04668-y
Han MA, Zeraatkar D, Guyatt GH, et al. Reduction of Red and Processed Meat Intake and Cancer Mortality and Incidence: A Systematic Review and Meta-analysis of Cohort Studies. Ann Intern Med. 2019;171:711–720. [Epub ahead of print 1 October 2019]. doi: https://doi.org/10.7326/M19-0699
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Published: Ann Intern Med. 2019;171(10):711-720.
Published at www.annals.org on 1 October 2019
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