Bradley C. Johnston, PhD; Dena Zeraatkar, MSc; Mi Ah Han, PhD; Robin W.M. Vernooij, PhD; Claudia Valli, MSc; Regina El Dib, PhD; Catherine Marshall; Patrick J. Stover, PhD; Susan Fairweather-Taitt, PhD; Grzegorz Wójcik, PhD; Faiz Bhatia, PEng; Russell de Souza, ScD; Carlos Brotons, MD, PhD; Joerg J. Meerpohl, MD; Chirag J. Patel, PhD; Benjamin Djulbegovic, MD, PhD; Pablo Alonso-Coello, MD, PhD; Malgorzata M. Bala, MD, PhD; Gordon H. Guyatt, MD
Grant Support: 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.
Disclosures: 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. Dr. de Souza reports personal fees and nonfinancial support from the World Health Organization; personal fees from the Canadian Institutes of Health Research/Health Canada and McMaster Children's Hospital; grants from the Canadian Foundation for Dietetic Research, Canadian Institutes of Health Research, Hamilton Health Sciences Corporation, and Hamilton Health Sciences Corporation/Population Health Research Institute outside of the submitted work. He also reports other support from the College of Family Physicians of Canada, Royal College (speaking at a recent conference), and he has served on the Board of Directors of the Helderleigh Foundation. Dr. Patel reports grants from the National Institutes of Health, Sanofi, and the National Science Foundation; personal fees from XY.health, Inc, doc.ai, Janssen, and the US Centers for Disease Control and Prevention; and nonfinancial support from Microsoft, Inc, and Amazon, Inc, during the conduct of the study and equity in XY.health, Inc, outside the submitted work. A summary of disclosures is provided in the Appendix Table. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M19-1621.
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: Available at PROSPERO (www.crd.york.ac.uk/prospero/) (CRD42017074074). Statistical code and data set: Available upon request from Dr. Johnston (e-mail, firstname.lastname@example.org).
Corresponding Author: Bradley C. Johnston, PhD, Department of Community Health and Epidemiology, Dalhousie University, Centre for Clinical Research, Room 404, 5790 University Avenue, Halifax, Nova Scotia, Canada, B3H 1V7; e-mail, email@example.com.
Current Author Addresses: Dr. Johnston: Department of Community Health and Epidemiology, Dalhousie University, Centre for Clinical Research, Room 404, 5790 University Avenue, Halifax, Nova Scotia, Canada B3H 1V7.
Ms. Zeraatkar and Dr. Guyatt: Department of Health Research Methods, Evidence, and Impact, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada.
Dr. Han: Department of Preventive Medicine, College of Medicine, Chosun University, 309 Philmun-daero, Dong-gu, Gwangju 61452, Korea.
Dr. Vernooij: Department of Research, Netherlands Comprehensive Cancer Organisation, Godebaldkwartier 419, Utrecht 3511 DT, the Netherlands.
Ms. Valli and Dr. 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. El Dib: Institute of Science and Technology, São José dos Campos, Avenida Engenheiro Francisco José Longo, 777, Jardim São Dimas, São Paulo 12245-000, Brazil.
Ms. Marshall: Cochrane Consumer Group, 6 Horomona Road, Wellington 5034, New Zealand.
Dr. Stover: Texas A&M AgriLife Research, College of Agriculture and Life Sciences, Texas A&M University, Agriculture and Life Sciences Building, 600 John Kimbrough Boulevard, Suite 510, College Station, TX 77843-2142.
Dr. Fairweather-Taitt: Norwich Medical School, University of East Anglia, Norwich Research Park, Floor 2, Bob Champion Research and Education Building, James Watson Road, Norwich NR4 7UQ, United Kingdom.
Dr. Wojcik: Department of Medical Sociology, Jagiellonian University Medical College, 7 Kopernika Street, 31-034 Kraków, Poland.
Mr. Bhatia: 1503-33 Shore Breeze Drive, Etobicoke, Ontario M8V 0G1, Canada.
Dr. de Souza: Population Health Research Institute, 237 Barton Street East, Hamilton, Ontario L8L 2X2, Canada.
Dr. Brotons: Sardenya Primary Health Care Centre, Biomedical Research Institute Sant Pau (IIB Sant Pau), Sardenya 466, Barcelona 08025, Spain.
Dr. Meerpohl: Institute for Evidence in Medicine, Medical Centre, University of Freiburg, Faculty of Medicine, University of Freiburg, Breisacher Strasse 153, Freiburg 79110, Germany.
Dr. Patel: Department of Biomedical Informatics, Harvard University, 10 Shattuck Street, Room 302, Boston, MA 0211521
Dr. Djulbegovic: City of Hope, 1500 East Duarte Road, Duarte, CA 91010.
Dr. Bala: Department of Hygiene and Dietetics, Jagiellonian University Medical College, 7 Kopernika Street, 31-034 Kraków, Poland.
Author Contributions: Conception and design: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, P. Alonso-Coello, M.M. Bala, G.H. Guyatt.
Analysis and interpretation of the data: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, R. El Dib, C. Marshall, P.J. Stover, S. Fairweather-Taitt, G. Wójcik, F. Bhatia, R. de Souza, C. Brotons, J. Meerpohl, C.J. Patel, B. Djulbegovic, P. Alonso-Coello, M.M. Bala, G.H. Guyatt.
Drafting of the article: B.C. Johnston.
Critical revision of the article for important intellectual content: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, R. El Dib, C. Marshall, P.J. Stover, S. Fairweather-Taitt, G. Wójcik, F. Bhatia, R. de Souza, C. Brotons, J. Meerpohl, C.J. Patel, B. Djulbegovic, P. Alonso-Coello, M.M. Bala, G.H. Guyatt.
Final approval of the article: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, R. El Dib, C. Marshall, P.J. Stover, S. Fairweather-Taitt, G. Wójcik, F. Bhatia, R. de Souza, C. Brotons, J. Meerpohl, C.J. Patel, B. Djulbegovic, P. Alonso-Coello, M.M. Bala, G.H. Guyatt.
Provision of study materials or patients: B.C. Johnston.
Statistical expertise: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, R. El Dib, G.H. Guyatt.
Administrative, technical, or logistical support: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, R. El Dib, B. Djulbegovic, P. Alonso-Coello, M.M. Bala, G.H. Guyatt.
Collection and assembly of data: B.C. Johnston, D. Zeraatkar, M.A. Han, R.W.M. Vernooij, C. Valli, R. El Dib, B. Djulbegovic.
This article has been corrected. The original version (PDF) is appended to this article as a Supplement.
Dietary guideline recommendations require consideration of the certainty in the evidence, the magnitude of potential benefits and harms, and explicit consideration of people's values and preferences. A set of recommendations on red meat and processed meat consumption was developed on the basis of 5 de novo systematic reviews that considered all of these issues.
The recommendations were developed by using the Nutritional Recommendations (NutriRECS) guideline development process, which includes rigorous systematic review methodology, and GRADE methods to rate the certainty of evidence for each outcome and to move from evidence to recommendations. A panel of 14 members, including 3 community members, from 7 countries voted on the final recommendations. Strict criteria limited the conflicts of interest among panel members. Considerations of environmental impact or animal welfare did not bear on the recommendations. Four systematic reviews addressed the health effects associated with red meat and processed meat consumption, and 1 systematic review addressed people's health-related values and preferences regarding meat consumption.
The panel suggests that adults continue current unprocessed red meat consumption (weak recommendation, low-certainty evidence). Similarly, the panel suggests adults continue current processed meat consumption (weak recommendation, low-certainty evidence).
None. (PROSPERO 2017: CRD42017074074; PROSPERO 2018: CRD42018088854)
Appendix Table. Summary of Panelists' Potential Conflicts of Interest
Table 1. Causal Inference Assessment Based on Summary of Evidence for Statistically Significant Effects for Red Meat, Processed Meat, and Dietary Patterns
Table 2. Summary of Findings for Health-related Values and Preferences*
Henning Ansorg, MD, FACP, Public Health Officer
Public Health Department, Santa Barbara County
October 1, 2019
“Unprocessed and Processed Meat Consumption... “This is a disgrace
For the Annals to publish this article (and for the authors to even write it without concern for the environmental effects of food choices) shows, to what extent we as physicians, are out of touch with the real world. It is a disgrace! Physicians need to realize that climate deterioration poses the most immediate and grave risk to peoples’ health. In this time and age, not to take effects on global warming into consideration when reviewing “health effects” of a diet, just seems so unworthy of our calling as physicians. We can no longer afford to pretend, as if the way how we present our “scientific” findings, could be neutral. How naive are we really? Any publication will immediately be “selectively”edited and broadcasted by the media onto every phone on the planet and thus strongly influence the publics’ beliefs and behaviors.To essentially “recommend” a red meat diet for it’s non inferior health effect-and coming to this conclusion by virtue of eliminating any consideration for the profound effects of red meat production on the environment and therefore on human health- is simply unforgivable.Please let us, as physicians, wake up to the fact, that our climate crisis poses the most profound risk to individual’s and public health and that we have a responsibility in guiding the public on how to confront this threat: in part, with food choices.
October 2, 2019
Conflict of Interest:
Dietetic Student w/ plant based diet.
A Dietetic Perspective
This article looks legit, although reviewing diet does not work with the GRADE system. I'd love to see all the omitted search keys used for these systematic reviews. With all of the studies linking animal products in general to may diseases, it's ignorant for someone to spend the time to make this article unless they have undisclosed biases (meat industry). Johnston already has a study about challenging the limit of sugar, which was backed by a non-profit sponsored by large SSB companies. If your going to put all this work into a study, make sure it counts, folks. The purpose of this work seems to be confusing uneducated public populations.
Daniel A. Meyer, MD Assistant Professor of Medicine
Tufts University School of Medicine, Division Director, Division of Hospital Medicine, Department of Medicine, Maine Medical Center, Portland, ME
Missing the Forrest through the Trees
The recent article by Johnston and colleagues (1) outlining recommendations on red meat and processed meat consumption is both impressive in its approach and disappointing in that it fails to go farther. By deciding not to consider environmental impacts of red meat consumption in their recommendation that adults continue both red meat and processed consumption the group has produced a flawed report that is both an abdication of the moral responsibility physicians have to our society and also an incomplete assessment of the health impacts created by red meat consumption for individual patients.The contributions of red meat consumption to climate change are well documented. Cows are one of a number of major sources of methane gas and methane amounted to 10% of US green-house gas emissions in 2017 (2). Methane has 25 times the climate impact of a similar amount of CO2 (3) making it a major contributor to climate change. The health impacts of global warming are going to be substantial and have already started to manifest. These include rising food insecurity, water insecurity, reduced nutritional value of food, increased mosquito and vector borne diseases, and rises in diseases associated with catastrophic weather events such as heat stroke, leptospirosis and others (4). Given the significant contribution red meat consumption makes to climate change these health impacts merit consideration in societal guidelines around red meat consumption.Further, in a time when society is grappling with how to confront climate change physicians have a responsibility to support sound science, and rational decision making around policy. Recommendations from physician groups carry weight in policy assessments and have the ability to influence both governmental policy and individual decision making. That influence occurs both at the societal level through published statements such as this, and in the individual physician patient interaction where these guidelines inform the discussion. It is therefore a disappointment that these nutritional recommendations would not consider the broader health impacts of red meat consumption.The result is an article that incompletely informs the physician in how to counsel patients on the risks and benefits of red meat consumption. Johnson and colleagues would have done well to reconsider their approach. Certainly balancing all of these considerations would have increased the complexity of the task but that was the challenge they were given and they have failed to deliver recommendations that meet the needs of our time or our patients.1. Johnson BC et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations from the NutriRECS Consortium. Ann Int Med. Doi: 10.7326/M19-16212. “Greenhouse Gas Emissions”, EPA.Gov. https://www.epa.gov/ghgemissions/overview-greenhouse-gases, Accessed 2 October 2019.3. Friend, Tad. Can A Burger Help Solve Climate Change. New Yorker Magazine, September 23, 2019.4. Rossati A. Global Warming and its health impact. Int J Occup Environ Med 2017;8:7-20 doi: 10.1571/ijoem.2017.963
Annals of Internal Medicine
Conflict of Interest:
Editor in Chief, Annals of Internal Medicine
Response to Chilson
Readers can view the conflict of interest disclosures for all authors of the systematic reviews and the recommendations by clicking on the link following each article's byline on www.annals.org. None of the authors declared a financial relationship with the meat industry.
Richard M. Rosenfeld, MD, MPH, MBA
SUNY Downstate Medical Center, Brooklyn, NY, USA
October 4, 2019
Conflict of Interest:
Whole food, plant-based diet
Founder and Chair, SUNY Downstate Committee on Plant-based Health and Nutrition
Less Meat May Not Help, But It's More Plants That Really Matters
Johnston and colleagues (1) have produced a trustworthy guideline recommending that adults continue their current consumption of processed meat and unprocessed red meat. This recommendation may surprise some, but is best understood in context of the research question: how does a diet higher or lower in processed meat or unprocessed red meat (e.g., a decrease of 3 or more servings per week) impact the risk of cancer or adverse cardiometabolic outcomes? In this context, four de novo systematic reviews conducted explicitly for the guideline show small or trivial risk reductions that are deemed insufficient to recommend a change in eating patterns.A more pragmatic issue, however, is not simply reducing meat consumption but also considering what fills the void. For example, replacing meat with high-quality plant sources – soy, legumes, nuts, or high-quality carbohydrates – can lower total cholesterol, triglyceride, and LDL levels (2). Similarly, consuming more whole grains and fiber-rich carbohydrates reduces the risk of strokes (and related mortality), coronary artery disease (and related mortality), type 2 diabetes, and some cancers (breast can colorectal) (3). Adults who eat more healthy plant foods (whole grains, fruits, vegetables, nuts, and legumes) also have reduced risk of coronary heart disease compared to adults who eat less healthy foods (juices, sweetened beverages, refined grains, potatoes, fried foods, sweets) (4). Last, consuming more fruits, vegetables, and legumes can lower overall and cardiovascular mortality (5).Reducing meat consumption alone may not improve health if the replacement calories come from fried foods, refined foods, simple carbohydrates, baked goods, or sweets. Conversely, replacing meat with high quality carbohydrates and whole, unrefined plant foods could improve health. The guideline does not mention the critical issue of what replaces reduced meat intake, nor does it mention plant foods or plant-centered diets (e.g. vegan, vegetarian, flexitarian). This omission may relate to the disclosure that none of the authors are vegetarians and 14 of 15 are regular meat eaters, of whom 13 eat processed meat and 6 consume 3 or more meat servings per week. The evidence may have been interpreted differently by the guideline development group if eating patterns of participants better reflected the diversity of alternatives to an omnivore diet.References:1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed red meat and processed meat consumption: dietary guideline recommendations from the NutriRECS Consortium.Ann Int Med [Epub ahead of print 1 October 2019] doi: 10.7326/M19-1621.2. Guasch-Ferré M, Satija A, Blondin SA, et al. Meta-analysis of randomized controlled trials of red meat consumption in comparison with various comparison diets on cardiovascular risk factors. Circulation 2019; 139:1828-45.3. Reynolds A, Mann J, Cummings J, et al. Carbohydrate quality and human health: a series of systematic reviews and meta-analyses. Lancet 2019; 393:434-45.4. Satija A, Bhupathiraju SN, Spiegelman D, et al. Healthful and unhealthful plant-based diets and the risk of coronary artery heart disease in US adults. J Am Coll Cardiol 2017; 70:411-422.5. Miller M, Mente A, Dehghan M, et al. Fruit, vegetable, and legume intake, and cardiovascular disease and deaths in 18 countries (PURE): a prospective cohort study. Lancet 2017; 390:2037-49.
Richard M Fleming
October 3, 2019
Conflict of Interest:
FMTVDM issued to author.
Are We Really Prescribing the right diets for CAD, T2D, Cancer and Obesity???
One cannot read a medical journal  or participate in social media without becoming increasingly aware of the dichotomy that has taken place in the debate over what constitutes a healthy and non-healthy diet. Despite what is undoubtedly a strong concern by many over how to best address the ever-increasing incidence of “inflammatory” diseases, including coronary artery disease (CAD), adult onset diabetes mellitus (T2D), obesity and certain types of cancer, there remains considerable disagreement. This most recent publication  has done nothing to help clarify this debate – it has however, further fueled the antagonism that already exists while causing further public confusion.The clinical treatment of these diseases for hundreds of thousands to millions of people around the world depends upon when and where the patient’s physician was trained and who has influenced their training. Medicine is not a place for personal opinions or twitter biting. For many physicians the focus remains on measuring cholesterol levels and other blood tests looking for inflammation. Many of the currently published dietary studies emphasize looking for improvements in cholesterol or inflammation  to support the success of their dietary regimens or drug treatment. It is clear that many clinicians depend upon these blood tests to determine if their treatment (diet, medication, surgery, etc.) for obesity, T2D, Cancer and/or CAD is successful. These blood tests, which are commonly checked in the “fasting” state focus on looking for reductions in specific cholesterol levels, glucose, hemoglobin A1C (glycosylated hemoglobin), fibrinogen, homocysteine, c-reactive protein (CRP) and a series of other tests. The relationship of these and numerous other factors and their role of CAD are well established and are discussed in detail elsewhere [2-4].The measurement of these blood tests demonstrate an expansion in thinking from the simple, cholesterol-is-the-sole-cause-of-heart-disease, to cholesterol along with a host of other factors producing an inflammatory process , all of which are ultimately responsible to varying degrees for the impaired blood flow through the coronary arteries in any given individual. The consequential build-up of inflammatory plaques ultimately impairs the ability of the coronary arteries to relax to carry more blood flow to the heart, which in turns compromises the heart when the metabolic demands of the heart increase  producing major adverse cardiac events (MACE). What still remains up for debate, is how the various diets and medications selected for treatment of patients actually impact CAD, T2D, obesity and at least certain types of cancer. Should patients be prescribed a diet consistent with the American Heart Association recommendations? Should they be prescribed vegan or vegetarian diets? Should they be prescribed KETO genic diets? Should they be prescribed statins and PCSK9 inhibitors? Are we prescribing the right diets? Are we over prescribing medications? Are we using the right tests to know?As established in 2008 , merely measuring changes in cholesterol and inflammation do not tell us what is actually happening inside the walls of any given patients coronary arteries. The disconnect between blood tests and actual CAD raises serious questions about using these blood tests to determine the effect of diets or medications for CAD, T2D, cancer or obesity and it raises questions about the meaning of the studies presented by Johnston, et al .Quantitative measurement of changes in CAD and cancer requires a method capable of accurately, consistently and reproducibly measuring these changes . Similarly, we can also measure the true extent to which treatment of T2D and obesity is associated with changes in cancer and CAD.As we attempt to expand our knowledge and understanding into the causes and treatment of CAD, T2D, Cancer and Obesity, it becomes increasingly important that we measure the actual outcome of these treatments. If we are to truly “do no harm”, we must measure the effect of our treatments to provide the best medical care possible for our patients, making it possible to prescribe the best diet and lifestyle choices possible, while at the same time judiciously limiting the use of medications to those instances where they are truly beneficial and only for the amount of time they prove to be valuable. Acknowledgement: FMTVDM issued to author. References:1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations From the Nutritional Recommendations (NutriRECS) Consortium. Ann Intern Med 2019. DOI: 10.7326/M19-1621.2. Fleming RM. Chapter 64. The Pathogenesis of Vascular Disease. Textbook of Angiology. John C. Chang Editor, Springer-Verlag New York, NY. 1999, pp. 787-798.3. Fleming RM. Chapter 29. Atherosclerosis: Understanding the relationship between coronary artery disease and stenosis flow reserve. Textbook of Angiology. John C. Chang Editor, Springer-Verlag, New York, NY. 1999. pp. 381-387.4. Fleming RM, Harrington GM. "What is the Relationship between Myocardial Perfusion Imaging and Coronary Artery Disease Risk Factors and Markers of Inflammation?" Angiology 2008;59:16-25. 5. The Fleming Method for Tissue and Vascular Differentiation and Metabolism (FMTVDM) using same state single or sequential quantification comparisons. Patent Number 9566037. Issued 02/14/2017.
Richard M Fleming, PhD, MD
FHHI-OmnificImaging-Camelot El Segundo, CA, USA
Conflict of Interest:
FMTVDM patent was issued to primary author
Whatever Happened to Civil Scientific Discourse?
On 1 October 2019 a series of articles appeared in the Annals of Internal Medicine including the recommendations by a private group - which to the best of my understanding does not reflect the views of the Journal, the USDA, AHA or any other organization - that people need not change their intake of red or processed meats .
The process by which a paper submitted to a scientific journal is evaluated to determine if it should or will be published is one the general public and media may not be aware of, but those of us who publish research and who participate in the process of deciding what will and will not be published, should be familiar with .
While I have already addressed some of my views in comments and letters-to-the-editor, which may or may not get published - the underlying tone on both sides of this tirade- is one of disrespect and the behavior that one would expect from a second grader, not a scientist or physician.
The Annals of Internal Medicine, like any journal, is not required to publish only what its most powerful readers want published. Neither should it be limited by threats made by its readers. When we disagree with what has been published and we present an intelligent articulate message, we are listened to. When we go on social media and act like the people we disrespect, we are accordingly disrespected and doubted, adding credibility to the opposing point-of-view. If we wonder why the general public and the media are confused, we need look no further than in the mirror.
1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations From the Nutritional Recommendations (NutriRECS) Consortium. Ann Intern Med 2019. DOI: 10.7326/M19-1621.
2. Fleming RM, Fleming MR, Chaudhuri TK. Establishing Data Validity: Statistically Determining if Data is Fabricated, Falsified or Plagiarized. ACTA Scientific Med Sci 2019;3(8):169-191.
Ingvar A. Bergdahl
Department of Public Health and Clinical Medicine, Section of Sustainable Health, Umeå University, 901 87 Umeå, Sweden
October 5, 2019
The authors judge prevention of 20,000 cancer deaths per year in the U.S. as ‘very small’
The recent paper by Johnston et al. (2019) on guideline recommendations on red meat and processed meat consumption has received much attention in public discussions and newspapers. Among other things the authors point at a ‘very small and often trivial absolute risk reduction based on a realistic decrease of 3 servings of red or processed meat per week’. This ‘very small’ is often cited in the public discussions and newspapers, but what are the numbers behind? The risk reduction they refer to, given their own calculations, includes 7 saved cancer deaths per 1000 individuals. This corresponds to over 600 saved lives per year in my little country Sweden only, given the 90-100,000 annual deaths. This in turn corresponds to 3% of all cancer deaths. In the U.S. it would be 20,000 saved lives per year. It is remarkable that the authors refer to that as a ‘very small’ risk reduction, especially as this is not for total avoidance of meat, but a ‘realistic decrease of 3 servings per week’. The uncertainty of the risk is considerable and should be discussed. But as regards this particular paper, the fact that the authors name a risk reduction that corresponds to 20,000 saved lives per year in the U.S. as a ‘very small’ risk reduction gives rise to questions about the validity of the judgements made during the process of working these recommendations out.Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations From the Nutritional Recommendations (NutriRECS) Consortium. Ann Intern Med. 2019; [Epub ahead of print 1 October 2019]. doi: 10.7326/M19-1621
October 6, 2019
Conflict of Interest:
Whole food, plant-based diet Founder and Chair, SUNY Downstate Committee on Plant-based Health and Nutrition
Get your facts first, then you can distort them as you please
In the context of Mark Twain’s suggestion “Get your facts first, then distort them as you please,” one could view the meat dietary recommendations by Johnston and colleagues (1) as a potential distortion of the evidentiary facts from the supporting systematic reviews.Trustworthy systematic reviews are the foundation for guideline recommendations, offering bottom -line objective facts (e.g., pooled estimates of effect size) qualified by estimates of precision, certainty, and directness. A dirty little secret of all guideline panels, even those that follow the highly regarded GRADE process, is that consensus plays a large role in shaping the outcome (2): all evidence, including systematic reviews, must be interpreted by the panelists, who then craft recommendations reflecting the group’s values, priorities, and preferences. Ideally, the value judgments that underlie each recommendation are explicitly stated in the guideline (3).Value judgments can be shaped by conflicts of interest, which should be disclosed for all panelists as active, inactive, financial, or intellectual (4). To the credit of the 14 meat guideline panelists, they go beyond this in the Appendix Table at the end of the guideline (1) and state meat dietary preferences: 93% regularly consume red meat, 86% regularly consume processed meat, and only 1 panelist was a non-meat eater (pescatarian). Unfortunately, there are 19 authors, so the dietary patterns, and other disclosures, for the 5 authors who were not panelists is unclear.Even if conflicts are fully disclosed, not having vegetarian or vegan panelists raises serious concerns of inadequate viewpoint diversity, leading to unintentional “distortion” of facts in formulating the guideline scope, key questions, recommendation wording, and recommendation strength. Without viewpoint diversity, “problematic assumptions can go unchallenged, and it can be difficult to effectively understand or engage with others who have different backgrounds, priors, and commitments (5).” The process of reaching consensus may have progressed very differently if the panel had balanced and diverse viewpoints from meat-eaters, flexitarians, vegetarians, and whole food plant-based vegans. Hopefully future guidance from the NutriRECS Consortium will have greater respect for viewpoint diversity as a prerequisite for fair, balanced, and credible consensus.References1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed red meat and processed meat consumption: dietary guideline recommendations from the NutriRECS Consortium.Ann Int Med [Epub ahead of print 1 October 2019] doi: 10.7326/M19-1621.2. Djulbegovic B, Guyatt G. Evidence vs. consensus in clinical practice guidelines. JAMA 2019; 322:725-6.3. Rosenfeld RM, Shiffman RN, Robertson P. Clinical practice guideline development manual, third edition: a quality-drive approach for translating evidence into action. Otolaryngol Head Neck Surg 2013; 148 (Suppl 1):S1-S55.4. Qaseem A, Wilt TJ; for the Clinical Guidelines Committee of the American College of Physicians. Disclosure of interests and management of conflict of interest in clinical guidelines and guidance statements: methods from the Clinical Guidelines Committee of the American College of Physicians. Ann Intern Med 2019; 171:354-61.5. Heterodox Academy. The Problem. https://heterodoxacademy.org/the-problem/. Accessed 10/6/19.
Eric C. Westman, MD MHS
October 7, 2019
Conflict of Interest:
Past President: Obesity Medicine Association; Author: The New Atkins for a New You, Keto Clarity, Cholesterol Clarity; Owner, Adapt Your Life, Inc. (education and product company)
Epidemiology vs. Evidence-based Medicine?
Health guidelines that restrict red meat and saturated fat are based on epidemiological research.(1) However, when epidemiology has weak associations, evidence-based medicine (EBM) regards it as a method to generate hypotheses, but not to test hypotheses.(2) EBM argues that the highest level of experimental evaluations of hypotheses (randomized, controlled trials) should be used to generate guidelines, and also assesses the data for clinical relevance. If EBM principles were available years ago when red meat/saturated fat-restricting guidelines first were developed, the guidelines would not have restricted red meat or saturated fat.(3) In this paper, red meat consumption, when examined with evidence-based medicine techniques, has no clinically relevant risk.(4) A growing number of medical organizations support dietary patterns that do not restrict red meat or saturated fat.(5,6) Other guideline panels should use a modern (EBM) evaluation of data to make their recommendations too.References:1. Arnett DK, Blumenthal RS, Albert MA, et al. ACC/AHA guideline on the primary prevention of cardiovascular disease: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2019;140:e596–e646. DOI: 10.1161/2. Haynes RB, Sackett DL, Guyatt GH, Tugwell P. Clinical Epidemiology: How to do Clinical Practice Research. LWW, 2005.3. Harcombe Z, Baker JS, DiNicolantonio JJ, et al. Evidence from randomised controlled trials does not support current dietary fat guidelines: a systematic review and metaanalysis. Open Heart 2016;3: e000409. doi:10.1136/ openhrt-2016-0004094. Johnson BC et al. Unprocessed red meat and processed meat consumption: Dietary guideline recommendations from the NutriRECS Consortium. Ann Intern Med. 2019. DOI:10.7326/M19-1621.5. Obesity Medicine Association. Download algorithm guideline from www.obesityalgorithm.org6. American Diabetes Association. Evert AB, Dennison M, Gardner CD et al. Nutrition Therapy for Adults with Diabetes or Prediabetes: A Consensus Report. Diabetes Care. 2019 May;42(5):731-754.
Bradley Johnston, Dena Zeraatkar, Mi Ah Han, Robin Vernooij, Claudia Valli, Regina El Dib, Catherine Marshall, Patrick Stover, Susan Fairweather-Taitt, Grzegorz Wojcik, Faiz Bhatia, Russell de Souza, Carlos Brotons, Joerg Meerpohl, Chirag Patel, Benjamin Djulbegovic, Pablo Alonso-Coello, Malgorzata Bala, Gordon Guyatt
Response to Dr. Ansorg and Dr. Meyer re: environment concerns
We share Dr. Ansorg’s and Dr. Meyer’s environmental concerns, but have a different perspective on the role of individual autonomy in the shared decision-making process, and in the role of a guideline panel.Guideline panels should be fully informed of the best available evidence regarding all the issues that bear on their recommendations. Producing recommendations regarding meat that take into account environmental concerns would require knowledge of the relative contribution of meat consumption versus other contributors to climate change. That would require a systematic review of the relevant evidence, which was beyond the scope of our work – and indeed, of our expertise. More importantly, there are those who either do not see environmental concerns as their priority, or feel that there are many other ways to personally work to protect the environment, including the selection of foods and food products. Even an individual who has a high concern for climate change may choose not to take every possible action to protect the environment.Implicit in Dr. Ansorg and Dr. Meyer’s position is that guideline developers – and other physicians – are entitled or perhaps even obligated to base recommendations on their own particular moral stances. We, instead, followed high quality standards for the development of guidelines that require basing recommendations on the beliefs and values of the target population (1). To respect a diversity of viewpoints, we consider it useful for each person to weigh all the issues related to meat consumption – health, the environment, and animal welfare, for instance - and to consider them separately. The reason is that some of these concerns will be salient to some, and to others not at all.1. Dedios CM, Esperato A, De-Regli LM, Peña-Rosas JP, Norris SL. Improving the adaptability of WHO evidence-informed guidelines for nutrition actions: results of a mixed methods evaluation. Implement Sci. 2017; 12(1): 39.
Barbara E. Millen, DrPH, RD, FADA (Chair); Steven Abrams, MD; Lucille Adams-Campbell, PhD; Steven Clinton, MD, PhD; Raphael Perez-Escamilla, PhD; Miriam Nelson, PhD; Marian L. Neuhouser, PhD, RD; Anna Maria Siega-Riz, PhD; Mary Story, PhD, RD.
DHHS and USDA Former 2015 DGAC Members
2015-2020 Dietary Guidelines for Americans are Sound and Evidence-Based
The NutritRECS initiative presented five papers (1-5) aimed at developing “trustworthy nutritional recommendations” on red and processed meat intake. As members of the former 2015 U.S. Dietary Guidelines Advisory Committee (DGAC), which set the scientific foundation (6,7) for the 2015-2020 Dietary Guidelines for Americans (DGA)(8), we emphasize that these papers have serious methodological limitations which led to flawed data interpretation and unsound conclusions on red and processed meat consumption (9). We agree with others (10) that three of five NutriRECS meta-analyses (1-3) contradict NutriRECS’ analyses and confirm negative health effects of meat intake on total, cardiovascular and cancer mortality, and incident type 2 diabetes. The data support the 2015 DGAC and 2015-2020 DGA (6-8) which identified common features of healthy dietary patterns: higher in vegetables, fruits, whole grains, low- or non-fat dairy, seafood, legumes and nuts; lower in red and processed meats, if consumed; low in sugar-sweetened foods and drinks and refined grains; moderate in alcohol (in adults, if consumed), with saturated fat and added sugars limited to less than 10% of calories and sodium to under 2300 mg. Together with USDA scientists, the 2015 DGAC modeled alternative calorie dietary patterns to meet differing consumer preferences (including vegetarian) at 1000 to 3200 calorie levels. At 2000 calories, average daily intake includes: 2-2.5 cups of vegetable and fruits; 2-3 cups of low and non-fat dairy; if eaten, about 3 ounces of red meat and poultry and 1-2 ounces of fish; 3 ounces of eggs; 4-7 ounces of nuts and seeds; about an ounce of oil; and ½ to 8 ounces of soy protein. Healthy dietary patterns can be ‘personalized’ to include portion-controlled meats, if desired; however, current or increased average American meat consumption levels would not achieve DGA food or nutrient targets, and would be deleterious to individual, population and planetary health.
The DGA update process is overseen every five years by USDA and DHHS, but unlike NutriRECS, adheres to an open, research-driven process consistent with best practices of other expert groups (11-16) and implemented by a DGAC fully vetted for expertise, constituency representation, and to minimize conflict of interest. All DGAC conclusions are rigorously graded on research quality and confirmed by panel consensus. We should all be striving to continue improving the science that informs the DGA instead of issuing recommendations through self-appointed groups with unclear goals and whose expertise and conflict of interest have not been thoroughly evaluated.
2015 Dietary Guidelines Advisory Committee Members: Barbara E. Millen, DrPH, RD, FADA (Chair); Steven Abrams, MD; Lucille Adams-Campbell, PhD; Steven Clinton, MD, PhD; Raphael Perez-Escamilla, PhD; Miriam Nelson, PhD; Marian L. Neuhouser, PhD, RD; Anna Maria Siega-Riz, PhD; Mary Story, PhD, RD.
We are not aware of any Conflicts of Interest.
1. Vernooij RWM, Zeraatkar D, Han MA, et al. Patterns of red and processed meat consumption and risk for cardiometabolic and cancer outcomes. A systematic review and meta-analysis of cohort studies. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10 .7326/M19-1583
2. Han MA, Zeraatkar D, Guyatt G, 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. 1 October 2019 [Epub ahead of print]. doi:10.7326/M19-0699
3. Zeraatkar D, Han HA, Guyatt GH, et al. Red and processed meat consumption and risk for all-cause mortality and cardiometabolic outcomes. A systematic review and meta-analysis of cohort studies. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10.7326 /M19-0655
4. Zeraatkar D, Johnston BC, Bartoszko J, et al. Effect of lower versus higher red meat intake on cardiometabolic and cancer outcomes. A systematic review of randomized trials. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10.7326/M19-0622
5. Valli C, Rabassa M, Johnston BC, et al. Health-related values and preferences regarding meat consumption. A mixed-methods systematic review. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10.7326/M19-1326
6. Scientific Report of the 2015 Dietary Guidelines Advisory Committee. U.S. Department of Health and Human Services. U.S. Department of Agriculture. Accessed 10 4 2019 at https://health.gov/dietaryguidelines/2015-scientific-report/PDFs/Scientific-Report-of-the-2015-Dietary-Guidelines-Advisory-Committee.pdf
7. Millen BE, Abrams S, Adams-Campbell L, Anderson CAM, Brenna JT, Campbell WW, Clinton S, Hu F, Nelson M, Neuhhouser ML, Perez-Escamilla R, Siega-Riz AM, Story M, Lichtenstein AH. The 2015 Dietary Guidelines Advisory Committee Scientific Report: Development and Major Conclusions. Adv Nutr 2016; 7:438-444 doi:10.3945/an.116.012120
8. U.S. Department of Health and Human Services, U.S. Department of Agriculture. 2015–2020 Dietary Guidelines for Americans. 8th ed. Accessed 10 4 2019 at https://health.gov/dietaryguidelines/2015/resources/2015-2020_Dietary_Guidelines.pdf
9. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed red meat and processed meat consumption: dietary guideline recommendations. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10 .7326/M19-1621
11. Jensen MD, Ryan DH, Apovian CM, Ard JD, Comuzzie AG, Donato KA, Hu FB, Hubbard VS, Jakicic JM, Kushner RF, Loria CM, Millen BE, Nonas CA, Pi-Sunyer FX, Stevens J, Stevens VJ, Wadden TA, Wolfe BM, Yanovski SZ, Jordan HS, Kendall KA, Lux LJ, Mentor-Marcel R, Morgan LC, Trisolini MG, Wnek J, Anderson JL, Halperin JL, Albert NM, Bozkurt B, Brindis RG, Curtis LH, DeMets D, Hochman JS, Kovacs RJ, Ohman EM, Pressler SJ, Sellke FW, Shen WK, Smith SC Jr, Tomaselli GF; American College of Cardiology/American Heart Association Task Force on Practice Guidelines; Obesity Society. 2013 AHA/ACC/TOS Guideline for the Management of Overweight and Obesity in Adults: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society. Circulation. 2014;129(25 Suppl 2):S102-138. PMID: 24239920.
12. Eckel RH, Jakicic JM, Ard JD, de Jesus JM, Houston Miller N, Hubbard VS, Lee IM, Lichtenstein AH, Loria CM, Millen BE, Nonas CA, Sacks FM, Smith SC Jr, Svetkey LP, Wadden TA, Yanovski SZ; American College of Cardiology/American Heart Association Task Force on Practice Guidelines. 2013 AHA/ACC guideline on lifestyle management to reduce cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Am Coll Cardiol. 2014;63(25 Pt B):2960-2984. PMID: 24239922.
13. World Cancer Research Fund. American Institute for Cancer Research. Diet, Nutrition, Physical Activity and Cancer: a Global Perspective. A summary of the Third Expert Report. London: World Cancer Research Fund International; 2018.
14. American Heart Association Diet and Lifestyle Recommendations. Accessed 10 4 2019 at:
15. Health Canada. Canada's Dietary Guidelines for Health Professionals and Policy Makers. Accessed 10 4 2019 at https://food-guide.canada.ca/static/assets/pdf/CDG-EN-2018.pdf.
16. Public Health England. The Eatwell Guide. Accessed 10 4 2019 at www.gov.uk/government/publications/the-eatwell-guide.
Ari R Joffe
University of Alberta, John Dossetor Health Ethics Center
October 9, 2019
A tragic missed opportunity
I was saddened by the NutriRECS Consortium recommendations. Although the systematic reviews may be sound, the recommendations were not. They were short-sighted [i.e., prioritized personal health over only the next 10 years, and neglected concern for the environmental/atmospheric commons], and assumed the importance of individual choice to eat meat [i.e., the choice was assumed to be a morally permissible one]. Factory farming is a main contributor to [accounting for up to 50% of anthropogenic] greenhouse-gas emissions (GHG), environmental degradation [e.g., deforestation, dead-zones, biodiversity loss, etc.], and antibiotic resistance [using >70% of all antimicrobials sold on Earth].(1) Climate change due to GHG from factory farming will result in humans suffering intense heatwaves, drought, water stress, food shortages, heavy rains/storms, fires, coastal flooding, changes in vector-borne diseases, with climate refugees, and potential for ecosystems collapse as tipping points are reached.(2) The rise of ISIS can be attributed to climate change, and other climate wars are expected.(3) These effects on the morbidity and mortality of individuals now and in the future were ignored.Factory farming involves industrialized abuse of billions of sentient non-human land-animals every year [>300 killed every single second in the United States alone]. This causes unfathomable suffering from un-anesthetized mutilations [e.g., castration, tail-docking, beak-trimming, de-horning, etc.], extreme confinement, overcrowding, fear, frustration, and pain, ended in childhood by far-too-often conscious slaughter.(4) Other than assertions of bare speciesism, and as shown by the argument from species overlap, there is no morally acceptable reason to justify humans in paying for this immense suffering only to satisfy a taste for animal ‘products’.(4,5) Just as the enjoyment and tradition of human slavery cannot be considered to make owning human slaves a permissible choice, so enjoyment and tradition cannot make supporting the oppression of factory farmed non-human animals a permissible choice. These effects on the suffering and killing of sentient individuals were ignored. Physicians serve as role-models, advocates, and experts in the service of health. The missed opportunity to improve and save the lives of untold humans (of this and future generations) and sentient non-human animals is a tragedy. A dose-reduction of 3 servings/week of unprocessed red-meat or processed meat reduced all-cause, cancer, and cardiovascular mortality, stroke, myocardial infarction, and type-2 diabetes, with relative risks from 0.90-0.95. The public health effects are large, and no harms were identified. The rational recommendation is to end the support for factory farming entailed in the consumption of animals. References1. Goodland R, Anhang J. Livestock and climate change: what if the key actors in climate change are cows, pigs, and chicken? World Watch. 2009; November/December:10-19. Available online at: https://pdfs.semanticscholar.org/6704/c7a0777c82357704d82b9ae8007c1197cb07.pdf?_ga=2.65937389.2134400425.1570409950-896426943.15704099502. Hoegh-Guldberg O, Jacob D, Taylor M, Guillen Bolanos T, Bindi M, Brown S, et al. The human imperative of stabilizing global climate change at 1.5ᵒ C. Science 2019;365:eaaw6974. 3. Kelley CP, Mohtadi S, Cane MA, Seager R, Kushnir Y. Climate change in the Fertile Crescent and implications of the recent Syrian drought. Proc Nat Acad Sci 2015;112:3241-3246.4. Singer P, Mason J. The Ethics of What We Eat: why our food choices matter. Rodale Inc: USA. 2006. 5. Horta O. The scope of the argument from species overlap. J Applied Philosophy 2014; 31:142-154.
Yi Wan, Fenglei Wang
Department of Nutrition, Harvard T.H. Chan School of Public Health
October 15, 2019
Grading the Evidence in Nutrition Research
TO THE EDITOR: We read with interest the work conducted by Johnston and colleagues who performed a series of systematic reviews regarding meat consumption and made dietary guideline recommendations based on these systematic reviews (1). We appreciated the heated discussion of meat consumption brought by the authors. However, we are concerned about the evidence grading system adopted in the dietary guideline development process.The authors used GRADE (Grading of Recommendations, Assessment, Development and Evaluation) approach to rate the quality of evidence and grade strength of recommendations. The GRADE method was mainly developed for recommendations in clinical practice guidelines which provide clinicians and patients with a guide to using those recommendations in clinical practice and policymakers with a guide to their use in health policy (2). In the GRADE approach, randomized controlled trials (RCTs) start as high-quality evidence and observational studies as low-quality evidence. At least two concerns will arise when applying the GRADE method directly to nutrition research. First, not all questions in the nutrition field can be examined via RCTs due to ethical constraints. The authors conducted a systematic review of randomized trials on red meat intake as well. However, none of the trials included in this systematic review directly investigated processed meat intake. The authors also performed a meta-analysis of cohorts and found the association between processed meat consumption and adverse outcomes, although authors argued that the magnitude was small, and the evidence was downgraded to low certainty due to observational design (3). Thus, it may not be ethically feasible to conduct a trial or achieve a large gradient in processed meat consumption between intervention groups in trials. Second, for ethically feasible RCTs in nutrition research, they may have inherent methodologic constraints, including small sample size, lack of blinding, poor compliance, high dropout rates, and insufficient follow-up time (4). These methodologic constraints will lower the quality of RCTs when applying GRADE.Therefore, in the field of nutrition research, where RCTs are constrained, well-designed prospective cohort studies can provide important evidence and should be given enough weight when developing dietary guidelines. Criteria for a grading system in nutrition research should also take nutrition-specific aspects (such as dietary assessment methods and their validation, or calibration of FFQs) into account. Good examples of modified criteria for nutrition research are NutriGRADE scoring system (4), and the criteria developed by the World Cancer Research Fund (5). 1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed red meat and processed meat consumption: dietary guideline recommendations. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10 .7326/M19-16212. Guyatt G, Oxman AD, Akl EA, et al. GRADE guidelines: 1. Introduction—GRADE evidence profiles and summary of findings tables. J Clin Epidemiol. 2011;64(4):383-94.3. Zeraatkar D, Han HA, Guyatt GH, et al. Red and processed meat consumption and risk for all-cause mortality and cardiometabolic outcomes. A systematic review and meta-analysis of cohort studies. Ann Intern Med. 1 October 2019 [Epub ahead of print]. doi:10.7326 /M19-06554. Schwingshackl L, Knüppel S, Schwedhelm C, et al. Perspective: NutriGrade: a scoring system to assess and judge the meta-evidence of randomized controlled trials and cohort studies in nutrition research. Adv Nutr. 2016;7(6):994-1004.5. World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Judging the evidence. Available at dietandcancerreport.org
Cynthia L. Gong, PharmD, PhD,1,2 Nadine K. Zawadzki, MPH,3 Roy Zawadzki,4 Jeffrey Tran, MD,2 Joel W. Hay, MA, MPhil, PhD3
1, 2, 3 University of Southern California 4 California Polytechnic State University
October 14, 2019
Conflict of Interest:
The Association Between Red Meat Consumption and Adverse Outcomes is Unlikely to be Causal
The NutriRECS panel sought to clarify the relationship between meat consumption and health, noting that the 2015–2020 Dietary Guidelines for Americans recommend limiting red meat intake (including processed meat) to ~1 weekly serving.1,2 Similarly, The World Health Organization International Agency for Research on Cancer has indicated that red meat is “probably carcinogenic”, and processed meat “carcinogenic” to humans.3
These recommendations are based on observational studies at high risk for confounding, thus limiting causal inferences. NutriRECS conducted a rigorous systematic review focusing on cardiovascular and cancer outcomes, concluding that adults continue their current unprocessed red meat consumption and processed meat consumption (both weak recommendations, low-certainty evidence).1
We support the authors’ conclusions, and suggest an additional approach through which they might demonstrate observational studies’ susceptibility to unmeasured confounding. This approach is E-value analysis, which addresses the specific question: How strong would any unmeasured confounding have to be to negate the observed results?4
We calculated E-values for all studies included in the review (Supplemental Tables 1-9) to verify the validity of these recommendations. We found that of all 93 outcomes assessed, none had an E-value confidence interval bound greater than 2.5, implying that even for those outcomes with the highest E-values (i.e. gallbladder cancer, 5.0, extrahepatic cancer, 4.31, pancreatic cancer, 3.97), an unobserved confounder 2.5 times more likely to be associated with these cancers and meat intake would nullify any observed effect. These might include, for example, alcohol, smoking, and environmental pollutants. Furthermore, all cardiovascular outcomes assessed had an E-value of <2, and nearly all had a lower-bound confidence interval of <1.5, indicating that weak confounding would attenuate the results.5
These recommendations do not account for economic, environmental, humanitarian, or cultural/religious considerations, which all significantly impact the decision to eat meat, but similarly are also likely to influence the risk for cancer and cardiovascular morbidity. Nonetheless, the results suggest that the causal link between meat consumption and cancer and cardiovascular outcomes is weak.
Had the individual studies reported E-values, the results of such studies would be viewed in a different light. Publication bias of “significant” p-values results in poorly conducted scientific studies suggesting a causal link between diet and adverse outcomes, leading to erroneous conclusions about the impact of a given exposure on the outcome of interest. It would be a valuable service if, as with p-values and confidence intervals, studies assessing treatment effects with non-randomized data would routinely publish e-value statistics.
1. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations from the Nutritional Recommendations (Nutrirecs) Consortium. Annals of internal medicine. Oct 1 2019.
2. U.S. Department of Health and Human Services and U.S. Department of Agriculture. 2015 – 2020 Dietary Guidelines for Americans. 8th Edition. 2015; https://health.gov/dietaryguidelines/2015/guidelines/. Accessed October 14, 2019.
3. World Health Organization. Q&a on the Carcinogenicity of the Consumption of Red Meat and Processed Meat. 2015; https://www.who.int/features/qa/cancer-red-meat/en/. Accessed October 14, 2019.
4. Ding P, VanderWeele TJ. Sensitivity Analysis without Assumptions. Epidemiology. May 2016;27(3):368-377.
5. Gong CL, Zawadzki N, Zawadzki R, Tran J, Hay JW. The Association between Red Meat Consumption and Adverse Outcomes Is Unlikely to Be Causal. 2019; https://drive.google.com/file/d/1vNgC8odz4VBW8-SdTAcpyuI14CgIJf5D/view?usp=sharing.
Bradley C. Johnston, Dena Zeraatkar, Mi Ah Han, Robin W.M. Vernooij, Claudia Valli, Regina El Dib, Catherine Marshall, Patrick J. Stover, Susan Fairweather-Taitt, Grzegorz Wojcik, Faiz Bhatia, Russell de Souza, Carlos Brotons, Joerg J. Meerpohl, Chirag J. Patel, Benjamin Djulbegovic, Pablo Alonso-Coello, Malgorzata M. Bala, Gordon H. Guyatt
October 24, 2019
In response to Dr. Rosenfeld’s comments, we believe the issue at hand should be argued not on the basis of who was on the panel, but whether the panel judgements were appropriate. From the individual perspective we took: 1) any effects of red or processed meat on health outcomes are uncertain, 2) if there are adverse health effects, they are very small, and 3) our systematic review of peoples’ values and preference suggests that for many reasons people are attached to their red and processed meat consumptions and that, when confronted with very small and uncertain benefits of reducing meat consumption, most fully informed individuals, considering only health effects, would choose to continue their current meat consumption. Perhaps the panel was wrong in this inference, but it seems clear to us that it was not an unreasonable inference.Having said all that, our process for selecting panelists addressed many important issues including panelist representation across seven countries, and a priori screening for important and relevant financial and intellectual conflicts of interest, methods that we believe represents an advancement in the field of dietary guidelines. The focus of our recommendations was on individual health outcomes and we believe that each of the 14 panelists could be objective about health outcome data, irrespective of their personal dietary habits. Dietary habits of the five remaining guideline authors, all of whom managed the supporting systematic reviews or the survey of panelists, were not relevant as they did not vote on the red and processed meat recommendations. We acknowledge that unconscious bias or opinions that may have been uncomfortable to share could have influenced decisions, but such a phenomenon is difficult to measure, and always possible so long as humans make health care decisions.We did take measures to elicit opinions that panelists may have been uncomfortable sharing in group meetings. To move from the evidence to recommendations, we used the GRADE Evidence to Decision frameworks (1,2) to survey our panel members independently using Survey Monkey. Using the frameworks, we conducted three surveys asking panelists to consider the summary evidence, and its certainty for harms, benefits and health-related values and preferences. One survey sought to understand the panels independent recommendations prior to panel meeting #4, one survey was in real-time during panel meeting #4 to get the aggregate vote to potentially generate further discussion, a method to try and elicit opinions that individuals may have been uncomfortable sharing directly in the meeting, and one survey after panel meeting #4 to assess the process.1. Alonso-Coello P, Schünemann HJ, Moberg J, et al. GRADE Evidence to Decision (EtD) frameworks: a systematic and transparent approach to making well informed healthcare choices. 1: Introduction. BMJ. 2016 Jun 28;353:i2016. 2. Alonso-Coello P, Oxman AD, Moberg J, et al. GRADE Evidence to Decision (EtD) frameworks: a systematic and transparent approach to making well informed healthcare choices. 2: Clinicalpractice guidelines. BMJ. 2016 Jun 30;353:i2089.
A public health versus individual patient perspective for red meat recommendations
In response to Dr. Bergdahl’s comments, the fundamental issue is whether one takes a public health or individual patient perspective. A very small benefit for an individual becomes an impressive sounding benefit when one multiplies it by a few million people. Our perspective was for the individual rather than the population which we made clear repeatedly. It is an important philosophical or ethical question whether one should frame harms or benefits with respect to individual autonomy, in which case the uncertain benefit is very small, or multiply by a few million, in which case – the still uncertain benefit – looks much larger. Each perspective has its merits, but both are based on uncertain benefit to the individual (or population). The author’s point is that a very small benefit for an individual can look impressive if framed in terms of a population. Whether decisions should be left to the fully informed individual who sees a very small benefit, or to a public health official who sees a large benefit, is a fundamental matter of a philosophical approach to health care decision-making. However, given the uncertainty, we believe that if public health officials make a recommendation, the public should be aware of the degree of uncertainty. Using the internationally recognized GRADE approach, we issued a weak recommendation that most people, but not all, continue their red and processed meat consumption. A weak recommendation is typically issued when the certainty of evidence is low, suggesting that further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate, and when there is variability in values and preferences (1-4).1. Andrews JC, Schünemann HJ, Oxman AD, et al. GRADE guidelines: 15. Going from evidence to recommendation-determinants of a recommendation's direction and strength. J Clin Epidemiol. 2013 Jul;66(7):726-35.2. Hultcrantz M, Rind D, Akl EA, et al. The GRADE Working Group clarifies the construct of certainty of evidence. J Clin Epidemiol. 2017 Jul;87:4-13.3. Alper BS, Oettgen P, Kunnamo I, et al; GRADE Working Group. Defining certainty of net benefit: a GRADE concept paper. BMJ Open. 2019 Jun 4;9(6):e027445.4. Johnston BC, Alonso-Coello P, Bala MM, et al. Methods for trustworthy nutritional recommendations NutriRECS (Nutritional Recommendations and accessible Evidence summaries Composed of Systematic reviews): a protocol. BMC Med Res Methodol. 2018 Dec 5;18(1):162.
Center for Comprehensive Health Practice and VNCJ Asbury Park Community Health Center
November 25, 2019
A lot of Malarkey
That the Annals Clinical Guideline should promote that "adults continue current unprocessed red meat consumption" because of "low to very low certainty of evidence" that reduction reduces mortality, cardiovascular events and cancer mortality is a lot of malarkey! I refer the authors back to Table 1 of the guideline, where we see that 4 cardiac events per 1000 people over 10.8 years would be averted, as would 12 new onsets of diabetes. That is cumulatively 16 individuals afforded better health outcomes out of every 1000, using a lifestyle intervention. Calculated across the entire US population, this would calculate to, and indeed has been, a major public health intervention! In addition, in 2019, I challenge the authors to find individuals who can even reduce their consumption by three servings per week. I know very few people who have three servings of processed or unprocessed red meat in a week.Thank goodness with the wording of this guideline, I can continue to tell them to do what they have been doing!
Emi Okomoto, MD
December 31, 2019
I want to express my deep disappointment on reading the series of articles on red meat (11/2019). While the data was helpful to report, the interpretation feels misleading and detrimental to the population. There is a clear reduction in valuable endpoints. If Americans adopted similar reductions, we would prevent hundreds of thousands of cardiometabolic outcomes. A relatively small shift in diet likely can save as many lives as a statin; look how much praise and publicity we give statins! Please, pay more attention to the data and do not downplay significant and potentially very impactful results based on the current environment. We must stand tall behind the data and announce results that we use to benefit the population, even when it is not popular. This was extremely disappointing that we have released what I believe to be frankly harmful guidance. Actions like these by the ACP leave me questioning my membership. Carpe Diem, Emi Okamoto, MD
Barbara Hansen, PhD
University of South Florida
January 31, 2020
I am a former president of the Obesity Society, and the American Society for Nutrition, and the International Association for the Study of Obesity, and a current and longstanding member of the National Academy of Medicine. I am writing to THANK YOU for proceeding with the publication in Annals of the articles questioning the prior evidence related to "meat". Rita Rubin writing a perspective in JAMA did a great job of explaining the actual history of those articles. I can only say CHEERS to you. Those calling for the prevention of publication of those articles themselves have huge conflicts of interest and are not able to provide science based evidence for their views, only hyperbole and opinions. YOU did GREAT. THANK YOU! Barbara C Hansen, Professor of Internal Medicine and Pediatrics, University of South Florida
Richard M. Fleming, PhD, MD, JD; Matthew R. Fleming, BS, NRP; Tapan K. Chaudhuri, MD
FHHI-OI-Camelot; Eastern Virginia Medical School
February 11, 2020
Conflict of Interest:
FMTVDM Issued to First Author.
Diets, Inflammation and Heart Disease - From 20/20 to 2020.
Comparisons of recent publications by Zhong , Rubin , and Johnston  would suggest that our current understanding - surrounding the impact of diets and heart disease – has left us with little more than a food fight . It is well established that cholesterol plays an important role in the development of the inflammatory tissue process known as coronary artery disease [5,6]. It is incorrect to say that coronary artery disease is an inflammatory process and that cholesterol is unimportant – as cholesterol is defined as one of the contributing factors to the inflammatory process described in the “Inflammation and Heart Disease” theory itself [5,6]. Measurement of changes in inter alia weight, cholesterol, CRP, fibrinogen, and homocysteine, alone without measurement of the actual tissue impact – viz. coronary artery disease – provides limited information about the effect of either diet or drug treatments.While some initial investigations into the measurable impact various diets have on coronary artery disease exist, the results to date have been semi-quantitative and need further absolute quantification  to provide accurate, consistent and reproducible results. More than 20-years after the introduction of the “Inflammation and Heart Disease” Theory, we have yet to conduct the research needed to understand the changes occurring in tissue of the coronary arteries following specific dietary practices. References:1. Zhong VW, Van Horn L, Greenland P, et al. Associations of Processed Meat, Unprocessed Red Meat, Poultry, or Fish Intake With Incident Cardiovascular Disease and All-Cause Mortality. JAMA Intern Med. Published online February 03, 2020. doi:10.1001/jamainternmed.2019.69692. Rubin R. Backlash Over Meat Dietary Recommendations Raises Questions About Corporate Ties to Nutrition Scientists. JAMA. Published online January 15, 2020. doi:10.1001/jama.2019.21441.3. Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations From the Nutritional Recommendations (NutriRECS) Consortium. Ann Intern Med 2019. DOI: 10.7326/M19-1621.4. Dyer O. Food fight: controversy over red meat guidelines rumbles on. BMJ 2020;368, doi.org/10.1136/bmj.m3975. Fleming RM. Chapter 64. The Pathogenesis of Vascular Disease. Textbook of Angiology. John C. Chang Editor, Springer-Verlag New York, NY. 1999, pp. 787-798. 6. 20/20 special on Inflammation and Heart Disease. https://www.youtube.com/watch?v=Hvb_Ced7KyA&t=22s7. The Fleming Method for Tissue and Vascular Differentiation and Metabolism (FMTVDM) using same state single or sequential quantification comparisons. Patent Number 9566037. Issued 02/14/2017.
Bradley C. Johnston, Dena Zeraatkar, Robin W.M. Vernooij, Montserrat Rabassa, Claudia Valli, Mi Ah Han, Pablo Alonso-Coello, Malgorzata M. Bala, Gordon H. Guyatt
Dalhousie University, McMaster University, and Texas A&M University
February 14, 2020
Authors' Final Response
We share Dr. Meyer’s environmental concerns, but have a different perspective on the role of individual autonomy in the shared decision-making process, and in the role of a guideline panel. Guideline panels should be fully informed of the best available evidence regarding all the issues that bear on their recommendations. In our guideline, we exclusively assessed the relation between meat and health outcomes. Producing recommendations regarding meat that take into account environmental concerns would require knowledge of the relative contribution of meat consumption versus other contributors to climate change. That would require systematic reviews of the relevant evidence, which was beyond the scope of our work and resources – and indeed, of our expertise.
Implicit in Dr. Meyer’s position is that guideline developers – and other physicians – are entitled or perhaps even obligated to base recommendations on their own moral stances. We, instead, followed standards for the development of guidelines that require basing recommendations on the beliefs and values of the target population (1,2).
Composition of panel
Dr. Rosenfeld suggests that the lack of perspective from vegans on the guideline panel likely explains our (weak) recommendation to continue red and processed meat consumption. His point presupposes that panelists were unable to faithfully carry out their mandate to put aside their own views regarding meat consumption and to make their recommendation based on their view of what a group of fully informed individuals in the population of interest (those that consume meat) would choose. Indeed, if vegans were on the panel and substituted their values for that of the population for whom we made recommendations, they would have failed in carrying out their role. We believe that all panelists made an effort to carry out their mandate. In addition, our process for selecting panelists addressed many important issues including panelist representation across seven countries, and a priori screening for important and relevant financial and intellectual conflicts of interest. We believe these methods represent an advance in the field of dietary guidelines.
Food replacement analysis
Dr. Rosenfeld makes a good point regarding considering what nutrients those reducing red meat might choose as replacements. Our judgment, however, was that the available evidence, largely based on modeling data in observational studies, is insufficient to develop helpful recommendations regarding replacement nutrients. Further, replacement analysis makes assumptions (e.g., linearity between nutrients, foods and health outcomes and that all foods and nutrients are accounted for in the analyses) that are rarely justified. Replacement analysis might make for a productive issue for a future guideline to address, particularly if randomized trials exist that replace nutrients while following participants for important health outcomes (e.g. major cardiometabolic events).
Epidemiology vs evidence-based medicine
To address Dr. Westman’s comments, we put forward that clinical epidemiology is the basic science that informs evidence-based medicine (EBM). We agree that unlike the clinical epidemiology community (2-5), in general the epidemiology community, and in particular the nutritional epidemiology community, often have different views on interpreting the certainty of evidence and making causal inferences (6,7).
In 2000 a group comprised primarily of clinical epidemiologists set out to produce a systematic, transparent framework for those producing systematic reviews and practice guidelines. The group subsequently expanded to include representation from the wider scientific community, including epidemiologists, and developed and refined “GRADE” (3), a framework now in use by over 110 health care organizations worldwide (e.g. World Health Organization, Joanna Briggs Institute, Cochrane Collaboration), organizations that regularly conduct evidence synthesis work of observational studies. GRADE guidance suggests a weak recommendation when the certainty of evidence is low, which is generally the case when the evidence base comes from observational studies. Unlike strong “just do it” recommendations, weak recommendations call for shared decision-making based on the totality of evidence on potential harms, benefits, and when relevant, values and preferences, costs and burden.
E-values to address causation
We were interested to learn from Dr. Gong and colleagues about E-value calculations as a statistical method to demonstrate the susceptibility of observational studies to unmeasured confounding, and how these values can be used to estimate how strong any unmeasured confounders would have to be to nullify our pooled results from our systematic reviews of cohort studies. Although we have not explored E-values, if the estimates that Gong et al. have reported are trustworthy, then the values corroborate the GRADE approach for assessing the certainty of evidence for observational data on an outcome by outcome basis. That is, based on the identified cohort data in our systematic reviews, the certainty of evidence is low to very low across approximately 90 outcomes, indicating that a causal relationship between red and processed meat and health outcomes is unlikely. It is plausible that a host of other confounders, including known but poorly measured confounders (e.g. lifestyle) and unknown confounders (e.g. genetic), might explain the observed risk reductions among those that consume three fewer servings of meat per week.
Grading the evidence in nutrition research
Finally, regarding the issues raised by Wan and Wang on the use of GRADE in nutrition research, we refer the reader to the accompanying response by Zeraatkar et al. (8)
1. Dedios CM, Esperato A, De-Regli LM, Peña-Rosas JP, Norris SL. Improving the adaptability of WHO evidence-informed guidelines for nutrition actions: results of a mixed methods evaluation. Implement Sci. 2017; 12(1): 39.
2. Johnston BC, Seivenpiper JL, Vernooij RWM, et al. The Philosophy of Evidence-Based Principles and Practice in Nutrition. Mayo Clin Proc Innov Qual Outcomes. 2019 May 27;3(2):189-199. doi: 10.1016/j.mayocpiqo.2019.02.005.
3. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924-6.
4. Johnston BC, Alonso-Coello P, Bala MM, et al. Methods for trustworthy nutritional recommendations NutriRECS (Nutritional Recommendations and accessible Evidence summaries Composed of Systematic reviews): a protocol. BMC Med Res Methodol. 2018;18:162.
5. Zeraatkar D, Johnston BC, Guyatt G. Evidence Collection and Evaluation for the Development of Dietary Guidelines and Public Policy on Nutrition. Annu Rev Nutr. 2019 Aug 21;39:227-247.
6. Katz DL, Karlsen MC, Chung M, et al. Hierarchies of evidence applied to lifestyle medicine (HEALM): introduction of a strength-of-evidence approach based on a methodological systematic review. BMC Med Res Methodol. 2019 Dec 1;19(1):178.
7. Johnston BC, Guyatt GH. Causal inference, interpreting and communicating results on red and processed meat. Amer J Clin Nutri. 2020 (accepted).
8. Zeraatkar D, Guyatt GH, Alonso-Coello P, et al. The application of GRADE to nutritional epidemiology is appropriate. Ann Intern Med. 2020 (accepted).
Disclosures: BCJ, MM, PAC, and GG are members of the GRADE working group. The work cited in Annals for Internal Medicine on red and processed meat was unfunded. As part of his recent recruitment to Texas A&M University, BCJ receives funds from Texas A&M AgriLife Research to support investigator-initiated research related to saturated and polyunsaturated fats. Support from Texas A&M AgriLife institutional funds are from interest and investment earnings, not a sponsoring organization, industry, or company.
BCJ also received funding in 2015 (outside the 36-month ICJME reporting period) from the International Life Science Institute (North America) to assess the methodological quality of guidelines addressing sugar intake using internationally accepted GRADE and AGREE guideline standards. The authors of the study on sugar guidelines conducted the study independently without involvement of the funder.
Johnston BC, Zeraatkar D, Han MA, et al. Unprocessed Red Meat and Processed Meat Consumption: Dietary Guideline Recommendations From the Nutritional Recommendations (NutriRECS) Consortium. Ann Intern Med. 2019;171:756–764. [Epub ahead of print 1 October 2019]. doi: https://doi.org/10.7326/M19-1621
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Published: Ann Intern Med. 2019;171(10):756-764.
Published at www.annals.org on 1 October 2019
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