Jennifer Erickson, RD *; Behnam Sadeghirad, PharmD, MPH *; Lyubov Lytvyn, MSc; Joanne Slavin, PhD, RD; Bradley C. Johnston, PhD
Note: As the guarantors of the study, Drs. Johnston and Slavin take full responsibility for the work as a whole, including the study design, access to data, and the decision to submit and publish the manuscript.
Acknowledgment: The authors thank Tamsin Adams-Webber, clinical librarian, for helping to develop our search strategy and Gordon Guyatt, GRADE Working Group Co-Chair, for advice on applying the GRADE methods and for reviewing the manuscript.
Financial Support: This project was funded by the Technical Committee on Dietary Carbohydrates of ILSI North America. The authors wrote the protocol, the scope of which was reviewed and approved by ILSI; and conducted the study independently from ILSI.
Disclosures: Dr. Slavin served on the 2010 Dietary Guidelines for Americans Advisory Committee (DGAC) where she chaired the carbohydrate committee that reviewed the relationships between added sugar intake and health outcomes. The results of that review were published in the 2010 DGACs, in Nutrition Reviews (Slavin J. Beverages and body weight: challenges in the evidence-based review process of the Carbohydrate Subcommittee from the 2010 Dietary Guidelines Advisory Committee. Nutr Rev. 2012;70 Suppl 2:S111-20.). She has presented widely on her work as chair of the carbohydrate and protein committees for the 2010 DGAC. Most of her research is in the areas of dietary fiber and gut health. As a dietitian, she is interested in dietary patterns and whole foods. Her research funding in the area of dietary sugars is summarized below. She received a grant from ILSI-NA Carbohydrate Committee in 2010 to examine sugar recommendations. That work was published in 2012 (Hess J, Latulippe ME, Ayoob K, Slavin J. The confusing world of dietary sugars: definitions, intakes, food sources and international dietary recommendations. Food Funct. 2012;3:477-86.). One of the co-authors of that paper was an employee of ILSI-NA at the time. That information is disclosed in the paper. Dr. Slavin and the University of Minnesota received the grant from ILSI-NA to support the current project. Besides ILSI-NA, Dr. Slavin thanks the following organizations for providing research funds for her laboratory the past 3 years: Minnesota Beef Council (satiety), Minnesota Cultivated Wild Rice Council (literature review), Barilla (snacking), Novartis Consumer Health (GSK) (fiber), American Pulse Association (satiety), MNDrive Global Food Ventures (nutrients in spinach), United States Department of Agriculture (fiber), The Mushroom Council (gut health), Pepsico (oatmeal), Welch’s (FODMAPs), Nestle Health Sciences (FODMAPs), and DSM (fiber). Her laboratory also has received contracts for services for analytical services in the areas of dietary fiber, whole grains, legumes, FODMAPS, digestive health, protein needs, carbohydrate needs, and snacking: Besides the companies listed, the laboratory has received funds in the past 3 years from Danone (snacking) and Coca-Cola (fiber). When the work is published, the funding source for all work in the laboratory will be disclosed as outlined by the journal. Dr. Slavin speaks widely on a range of human nutrition topics. Some talks on the topic of interest in this paper: "Fluid Consumption: Caloric Contribution to Weight Gain/Loss and Health: Factors That Influence Satiety" (Second International Conference on hydration and Health, sponsored by the ILSI North America Committee on Hydration, November 2011); "The Confusing World of Dietary Sugars: Views From the 2010 Dietary Guidelines Scientific Advisory Committee" (2012 Nutrition News Forecast, Academy of Nutrition and Dietetics, April 2012); "Food Is Not a Talisman: Reflections on the Science and Practice of Nutrition" (WO Atwater Lecture at Experimental Biology, April 2015). For full financial disclosure: ILSI meetings do not pay speakers; other scientific meetings also typically do not pay speakers if you are a member of that society. Dr. Slavin serves on the scientific advisory board for Tate and Lyle, Kerry Ingredients, Atkins Nutritionals, and Midwest Dairy Association. She also owns one-third share of the Slavin Sisters Farm LLC, a 119-acre farm in Walworth, Wisconsin, that is currently rented. Crops in 2016 included corn, soybeans, and pumpkins. Dr. Johnston is a member of GRADE, a working group that has developed a common, sensible, and transparent approach to grading quality of evidence and strength of recommendations. In addition to being a methods consultant to ILSI for this project, over the last 5 years, he has held investigator-initiated grants unrelated to the topic of sugar from BioK+ (a probiotic manufacturer), Genzyme (a manufacturer of enzyme replacement therapy for patients with rare lysosomal storage diseases), and a joint grant funded by Nestle and MITACS Accelerate (a provincially and federally supported not-for-profit organization that works with Canadian universities and companies to build partnerships that support industrial and social innovation in Canada) to assess probiotics for preventing necrotizing enterocolitis. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M16-2020.
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 and Johnson & Johnson.
Reproducible Research Statement:Study protocol: Available at www.crd.york.ac.uk/PROSPERO/display_record.asp?ID=CRD42015029182. Statistical code: Not applicable. Data set: See tables and appendices for all relevant data.
Requests for Single Reprints: Bradley C. Johnston, PhD, Prevention Lab, Child Health Evaluative Sciences, The Hospital for Sick Children Research Institute, Peter Gilgan Centre for Research and Learning, 686 Bay Street, Room 11.9859 West, Toronto, Ontario M5G 0A4, Canada; e-mail, email@example.com.
Current Author Addresses: Ms. Erickson and Dr. Slavin: Department of Food Science and Nutrition, University of Minnesota, 1334 Eckles Avenue, St. Paul, MN 55108.
Dr. Sadeghirad: Department of Clinical Epidemiology & Biostatistics, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada.
Ms. Lytvyn and Dr. Johnston: Child Health Evaluative Sciences, The Hospital for Sick Children Research Institute, Peter Gilgan Centre for Research and Learning, 686 Bay Street, Room 11.9859 West, Toronto, Ontario M5G 0A4, Canada.
Author Contributions: Conception and design: L. Lytvyn, J. Slavin, B.C. Johnston.
Analysis and interpretation of the data: J. Erickson, B. Sadeghirad, L. Lytvyn, J. Slavin, B.C. Johnston.
Drafting of the article: J. Erickson, B. Sadeghirad, L. Lytvyn, B.C. Johnston.
Critical revision of the article for important intellectual content: J. Erickson, B. Sadeghirad, L. Lytvyn, J. Slavin, B.C. Johnston.
Final approval of the article: J. Erickson, B. Sadeghirad, L. Lytvyn, J. Slavin, B.C. Johnston.
Provision of study materials or patients: J. Slavin, B.C. Johnston.
Statistical expertise: B. Sadeghirad.
Obtaining of funding: J. Slavin, B.C. Johnston.
Administrative, technical, or logistic support: L. Lytvyn, J. Slavin, B.C. Johnston.
Collection and assembly of data: J. Erickson, B. Sadeghirad, L. Lytvyn, B.C. Johnston.
The relationship between sugar and health is affected by energy balance, macronutrient substitutions, and diet and lifestyle patterns. Several authoritative organizations have issued public health guidelines addressing dietary sugars.
To systematically review guidelines on sugar intake and assess consistency of recommendations, methodological quality of guidelines, and the quality of evidence supporting each recommendation.
MEDLINE, EMBASE, and Web of Science (1995 to September 2016); guideline registries; and gray literature (bibliographies, Google, and experts).
Guidelines addressing sugar intake that reported their methods of development and were published in English between 1995 and 2016.
Three reviewers independently assessed guideline quality using the Appraisal of Guidelines for Research and Evaluation, 2nd edition (AGREE II), instrument. To assess evidence quality, articles supporting recommendations were independently reviewed and their quality was determined by using GRADE (Grading of Recommendations Assessment, Development and Evaluation) methods.
The search identified 9 guidelines that offered 12 recommendations. Each of the reviewed guidelines indicated a suggested decrease in the consumption of foods containing nonintrinsic sugars. The guidelines scored poorly on AGREE II criteria, specifically in rigor of development, applicability, and editorial independence. Seven recommendations provided nonquantitative guidance; 5 recommended less than 25% to less than 5% of total calories from nonintrinsic sugars. The recommendations were based on various health concerns, including nutrient displacement, dental caries, and weight gain. Quality of evidence supporting recommendations was low to very low.
The authors conducted the study independent of the funding source, which is primarily supported by the food and agriculture industry.
Guidelines on dietary sugar do not meet criteria for trustworthy recommendations and are based on low-quality evidence. Public health officials (when promulgating these recommendations) and their public audience (when considering dietary behavior) should be aware of these limitations.
Technical Committee on Dietary Carbohydrates of the North American branch of the International Life Sciences Institute. (PROSPERO: CRD42015029182)
Appendix Table 1. Additional Data Sources
Appendix Table 2. AGREE II Instrument
Summary of evidence search and selection.
Table 1. Identified Guidelines and Corresponding Sugar Recommendations
Table 2. Public Health Guideline Domain Scores on the AGREE II Instrument
Appendix Table 3. COI Reporting Across Guidelines
Appendix Table 4. Assessment of the Supporting Evidence for Each Recommendation (GRADE)
Appendix Table 5. Assessment of Individual Studies Supporting Recommendations (GRADE)
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Stephen Strum, MD
American Board of Internal Medicine
December 20, 2016
"Scientific Basis" Re Guidelines on Sugar Intake.
Reading the entire article Erickson et al was certainly frustrating if the goal in reading any article is to apply the findings to one's clinical practice. It's obvious to anyone's observations that in the USA & increasingly abroad, the population is growing in girth. Individuals with a BMI of ≤ 25 have become rarities. We are amidst an epidemic of over-consumption of calories with excessive high-glycemic carbohydrate consumption a major part of this problem coupled with more sedentary lifestyles. Taking a dietary history of my overweight-obese patients routinely indicates that for a majority, breakfast alone, involves the consumption of over 100 grams of high glycemic carbs. If one were to take a "one size fits all" approach and assume that the typical American eats 3,000 calories a day, then the guideline of < 10% of calories as "added sugars" would amount to 75 grams for the entire day. This amount is frequently exceeded with the typical American breakfast when high-glycemic sugars are considered. It's these carbs that result in prolonged blood glucose levels with glycosylation of protein and lipids over time and the resultant damage to all major systems. What is the value of this review by Ericsson et al when the harsh reality the physician sees with such patients is that they do not assess their caloric intake per meal nor their ingestion of high-glycemic carbohydrates (be they "added" or "intrinsic"). Frankly, I do not care about guidelines when they miss the mark insofar as informing either the patient or the physician how I can assess a situation and derive a strategy to alter a particular medical reality. Furthermore, when such guidelines are supported by the food & beverage industry, I wonder why bother to accept such a publication that simply adds another article to the peer-reviewed literature that contributes little to nothing about guiding the "consumer" and physician to improved health. Major parts of the global community over consume, work their bodies less, eat unhealthy "food" while other societies are starving. These are the issues I wish we would focus on and not the pseudoscience or junk science that is the "pablum" being increasingly fed to physicians and patients.
Alain Braillon MD, PhD
University Hospital. 80000 Amiens, France
December 28, 2016
My network emailed me the devastating NYT article (http://www.nytimes.com/2016/12/19/well/eat/a-food-industry-study-tries-to-discredit-advice-about-sugar.html) shaming the Journal for its publication about recommendations on sugar intake.(1) At first glance I hardly understood how the Journal published a piece funded by the food and agriculture industry because as a tobacco control advocate I was very happy when several journals banned studies funded by the tobacco industry. However, if industry funded research should be banned, the first should be the pharmaceutical industry, considering its top ranking among the False Claim Act defrauders.(2) However, banning is anti-science, debate is a prerequisite for science and restricting free speech is a very slippery slope.Erickson et al concluded: “Guidelines on dietary sugar do not meet criteria for trustworthy recommendations and are based on low-quality evidence.”(1) Despite I cannot (time and expertise) review their work, I’ll trust them. First, considering studies such as the huge European Prospective Investigation into Cancer and Nutrition (519,978 men and women in 10 European countries between 1992-2000) the robustness is not obvious. Tortures of the data by statistical analyses seem worse that in Guantanamo and the clinical relevance of findings remains to be assessed: investigators refused to indicate the number needed to treat (ie, diet with the highest quartile of consumption of leafy vegetables) during 8 y to avoid one death from myocardial infarction.(3)Second, the production of guidelines has reached epidemic proportions and too many seems unnecessary or conflicted. Eg. WHO clinical practice guidelines have been characterized by strong recommendations based on low or very low confidence estimates for evidence.(4) Last, readers who are experts in the field can send comments. The International Committee of Medical Journal Editors (ICMJE) recommends “Responsible debate, critique and disagreement are important features of science, and journal editors should encourage such discourse ….”(http://www.icmje.org/recommendations/browse/publishing-and-editorial-issues/correspondence.html) The Journal implements this recommendation, whether critical or favourable. The editorial board even accepts to be seriously tackled.(5) I am only uncomfortable with the paragraph about limitations: " The authors conducted the study independent of the funding source, which is primarily supported by the food and agriculture industry."(1) “Believed having conducted” or “tried to conduct” would be more correct. However, no shame. The limitation is on the abstract and cannot be missed. This is so rare. Abstracts should mention conflicts of interest. The Journal is a beacon for highlighting the potential conflict of interest in the abstract. ICMJE could consider this as a new recommendation.1 Erickson J, Sadeghirad B, Lytvyn L, Slavin J, Johnston BC. The scientific basis of guideline recommendations on sugar intake: A systematic review. Ann Intern Med 2016 Dec 20. doi: 10.7326/M16-2020. 2 Braillon A. Drug industry is now biggest defrauder of US government. BMJ 2012;344:d8219. 3 Braillon A. European Prospective Investigation into Cancer and Nutrition (EPIC): methods and clinical relevance. Am J Clin Nutr 2011;93:1386-7;4 Alexander PE, Brito JP, Neumann I et al. World Health Organization strong recommendations based on low-quality evidence (study quality) are frequent and often inconsistent with GRADE guidance. J Clin Epidemiol 2016;72:98-106.5 Braillon A. Moderate alcohol intake and cardiometabolic risk in adults with type 2 diabetes. Ann Intern Med 2016 ;165:68.
C. Albert Yeung, MPhil, MPH, MMedSci
National Health Service Lanarkshire, Bothwell, Scotland
January 3, 2017
Sugar Guidelines: Who to believe? What to believe?
The systematic review by Erickson et al. (1) challenged recommendations by public health officials for people to cut sugar consumption; saying there was no clear link between consumption of added sugars and health effects.The researchers said that the 2015-2020 Dietary Guidelines for Americans (2) did not cite any previously published studies as evidence for its recommendations. However, an extensive appendix (3) has been posted on the U.S. Department of Health and Human Services website. A 500-page supplementary report (4) was also published.While the methodology of the review is sound, the authors failed to point out when it comes to diet and the impact on health that high-quality evidence has been difficult to find. The gold standard of evidence-based medicine, i.e. randomized controlled trials, are impractical to carry out on large population groups for long periods of time. Public health officials have to work with the available evidence.It is important to consider the validity of the process for developing guidelines separately from the validity of the science linking increased sugar intake with health outcomes. Sometimes decisions for public health need to be based on the available evidence.The argument that various guidelines were based on evidence judged to be of low to very low quality may be an entirely valid point. However, it should not be taken as an implication that there is a body of high-quality evidence that contradicts the guidelines.References1. Erickson J, Sadeghirad B, Lytvyn L, Slavin J, Johnston BC. The scientific basis of guideline recommendations on sugar intake. A systematic review. Ann Intern Med.2016 Dec 20. [Epub ahead of print] [PMID: 27992898] doi:10.7236/M16-20202. U.S. Department of Health and Human Services, U.S. Department of Agriculture. 2015-2020 Dietary Guidelines for Americans. 8th Edition. December 2015. Accessed at http://health.gov/dietaryguidelines/2015/guidelines on 3 January 2017.3. U.S. Department of Health and Human Services. 2015 Dietary Guidelines Advisory Report. Accessed at https://health.gov/dietaryguidelines/2015-scientific-report on 3 January 2017.4. U.S. Department of Agriculture. A series of systematic reviews on the relationship between dietary patterns and health outcomes. March 2014. Accessed at http://www.nel.gov/vault/2440/web/files/DietaryPatterns/DPRptFullFinal.pdf on 3 January 2017.
Clinical Asst. Prof. Harvard Medical School
January 28, 2017
And so another once trusted journal stoops to publishing industry-sponsored faddle. ILSI is widely recognized as a corrupt front for the sugared beverage and other less-than-health-promoting industries. Enough!
Charles Norman Scholfield
February 3, 2017
Should promote the sugar interests
Since the study is based mainly on government reports, the AGREE II tool is not an appropriate metric to assess quality of the studies. Although many of the problems with this paper are given in the Editorial, this is not a free download while the offending article is free. Since the article is likely to interest many non-experts, they have no access to a balanced judgement. This is irresponsible publishing
Behnam Sadeghirad, PharmD, MPH, PhD, Bradley C. Johnston, PhD
May 9, 2017
We would like to thank Dr. Strum and Mr. Yeung for their comments and to clarify a number of items based on our study findings (1).
Our study was a systematic review of available public health guidelines on sugar intake aimed to assess the methodological quality of the guidelines, and the quality (certainty) of the evidence provided for their recommendations.
There is no disagreement that the overconsumption of calories, unhealthy eating habits, and the rise in sedentary lifestyles are the main drivers of the obesity epidemic in children and adults worldwide. However, this issue is quite separate from the quality and trustworthiness of public health guidelines on sugar intake. Our findings did not imply that increased sugar consumption is a good idea. Instead, the message, which seemed to be largely dismissed, was that dietary guidelines need to be developed with a higher degree of rigor, including transparency with respect to the certainty of evidence for chosen sugar thresholds and health outcomes that are important to the public. Dietary guidelines use large swaths of money from the public purse and guideline panels should be encouraged to follow the 2011 Institute of Medicine standards for trustworthy guidelines. For example, Institute of Medicine standards state that guideline recommendations should be based on systematic reviews of the literature and guidelines should closely manage intellectual and financial conflicts of interest.
We agree that it is often difficult to conduct randomized trials to address public health nutrition questions (2, 3). We also agree that public health officials may have limited quality evidence (e.g. observational studies, diet modeling) to make recommendations. By adopting the GRADE methodology as intended, including overall risk of bias, imprecision, inconsistency among primary studies, indirectness to the research question, and likelihood of publication bias, it is possible to overcome the problems with existing guidelines that rely largely on low quality evidence and discordantly produce strong recommendations (4).
As for the 2015 – 2020 Dietary Guidelines for Americans (5), although an extensive scientific report (6) was published, the guideline cited food pattern modeling and U.S. national caloric intake data from added sugars to inform their recommendations. As we previously indicated in our publication, we intended to evaluate the certainty of the evidence used in the model components as well as the accuracy of the modeling procedure; however, these details were not publicly available.
1. Erickson J, Sadeghirad B, Lytvyn L, Slavin J, Johnston BC. The Scientific Basis of Guideline Recommendations on Sugar Intake: A Systematic Review. Ann Intern Med. 2017;166(4):257-67.
2. Moher D, Tricco AC. Issues related to the conduct of systematic reviews: a focus on the nutrition field. Am J Clin Nutr. 2008;88.
3. Salam RA, Welch V, Bhutta ZA. Systematic reviews on selected nutrition interventions: descriptive assessment of conduct and methodological challenges. BMC Nutrition. 2015;1:9.
4. Alexander PE, Brito JP, Neumann I, Gionfriddo MR, Bero L, Djulbegovic B, et al. World Health Organization strong recommendations based on low-quality evidence (study quality) are frequent and often inconsistent with GRADE guidance. J Clin Epidemiol. 2016;72:98-106.
5. U.S. Department of Agriculture. Dietary Guidelines for Americans, 2015-2020. 8th ed. Washington, DC: US Gov Pr Off: U.S. Department of Health and Human Services; 2015.
6. U.S. Department of Agriculture. Scientific Report of the 2015 Dietary Guidelines Advisory Committee. U.S. Department of Health and Human Services; 2015.
Erickson J, Sadeghirad B, Lytvyn L, et al. The Scientific Basis of Guideline Recommendations on Sugar Intake: A Systematic Review. Ann Intern Med. 2017;166:257–267. [Epub ahead of print 20 December 2016]. doi: 10.7326/M16-2020
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Published: Ann Intern Med. 2017;166(4):257-267.
Published at www.annals.org on 20 December 2016
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