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Systematic Review

Red and processed meat intakes and cardiovascular disease and type 2 diabetes mellitus: An umbrella systematic review and assessment of causal relations using Bradford Hill’s criteria

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References

  • Abete, I., D. Romaguera, A. R. Vieira, A. Lopez de Munain, and T. Norat. 2014. Association between total, processed, red and white meat consumption and all-cause, CVD and IHD mortality: a meta-analysis of cohort studies. The British Journal of Nutrition 112 (5):762–75. doi: 10.1017/S000711451400124X.
  • Akesson, A., L. F. Andersen, A. G. Kristjánsdóttir, E. Roos, E. Trolle, E. Voutilainen, and E. Wirfält. 2013. Health effects associated with foods characteristic of the Nordic diet: a systematic literature review. Food Nutr Res 57:1–21.
  • An, R., J. Liu, and R. Liu. 2020. Pork consumption in relation to body weight and composition: a systematic review and meta-analysis. American Journal of Health Behavior 44 (4):513–25. doi: 10.5993/AJHB.44.4.12.
  • Arnett, D. K., R. S. Blumenthal, M. A. Albert, A. B. Buroker, Z. D. Goldberger, E. J. Hahn, C. D. Himmelfarb, A. Khera, D. Lloyd-Jones, J. W. McEvoy, Jr., Sr., et al. 2019. 2019 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 140 (11):e596–e646.
  • Aromataris, E., R. Fernandez, C. M. Godfrey, C. Holly, H. Khalil, and P. Tungpunkom. 2015. Summarizing systematic reviews: methodological development, conduct and reporting of an umbrella review approach. International Journal of Evidence-Based Healthcare 13 (3):132–40. doi: 10.1097/XEB.0000000000000055.
  • Aslam, S, and P. Emmanuel. 2010. Formulating a researchable question: a critical step for facilitating good clinical research. Indian Journal of Sexually Transmitted Diseases and AIDS 31 (1):47–50. doi: 10.4103/0253-7184.69003.
  • Aune, D., G. Ursin, and M. B. Veierød. 2009. Meat consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies. Diabetologia 52 (11):2277–87. doi: 10.1007/s00125-009-1481-x.
  • Bechthold, A., H. Boeing, C. Schwedhelm, G. Hoffmann, S. Knüppel, K. Iqbal, S. De Henauw, N. Michels, B. Devleesschauwer, S. Schlesinger, et al. 2019. Food groups and risk of coronary heart disease, stroke and heart failure: a systematic review and dose-response meta-analysis of prospective studies. Critical Reviews in Food Science and Nutrition 59 (7):1071–90. doi: 10.1080/10408398.2017.1392288.
  • Bendinelli, B., D. Palli, G. Masala, S. J. Sharp, M. B. Schulze, M. Guevara, A. D. van der, F. Sera, P. Amiano, B. Balkau, et al. 2013. Association between dietary meat consumption and incident type 2 diabetes: the EPIC-InterAct study. Diabetologia 56 (1):47–59.
  • Bergeron, N., S. Chiu, P. T. Williams, S. M. King, and R. M. Krauss. 2019. Effects of red meat, white meat, and nonmeat protein sources on atherogenic lipoprotein measures in the context of low compared with high saturated fat intake: a randomized controlled trial. The American Journal of Clinical Nutrition 110 (1):24–33. doi: 10.1093/ajcn/nqz035.
  • Beyerbach, J., J. Stadelmaier, G. Hoffmann, S. Balduzzi, N. Bröckelmann, and L. Schwingshackl. 2022. Evaluating concordance of bodies of evidence from randomized controlled trials, dietary intake, and biomarkers of intake in cohort studies: a meta-epidemiological study. Advances in Nutrition (Bethesda, Md.) 13 (1):48–65. doi: 10.1093/advances/nmab095.
  • Brown, A. W., S. Aslibekyan, D. Bier, R. Ferreira da Silva, A. Hoover, D. M. Klurfeld, E. Loken, E. Mayo-Wilson, N. Menachemi, G. Pavela, et al. 2021. Toward more rigorous and informative nutritional epidemiology: the rational space between dismissal and defense of the status quo. Critical Reviews in Food Science and Nutrition 1–18. doi: 10.1080/10408398.2021.1985427.
  • Brown, A. W., M. M. Bohan Brown, and D. B. Allison. 2013. Belief beyond the evidence: using the proposed effect of breakfast on obesity to show 2 practices that distort scientific evidence. The American Journal of Clinical Nutrition 98 (5):1298–308. doi: 10.3945/ajcn.113.064410.
  • Byers, T, and B. Lyle. 1999. The role of epidemiology in determining when evidence is sufficient to support nutrition recommendations. Summary statement. The American Journal of Clinical Nutrition 69 (6):1365s–7s. doi: 10.1093/ajcn/69.6.1365S.
  • Chan, D. S., R. Lau, D. Aune, R. Vieira, D. C. Greenwood, E. Kampman, and T. Norat. 2011. Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One 6 (6):e20456. doi: 10.1371/journal.pone.0020456.
  • Chen, G. C., D. B. Lv, Z. Pang, and Q. F. Liu. 2013. Red and processed meat consumption and risk of stroke: a meta-analysis of prospective cohort studies. European Journal of Clinical Nutrition 67 (1):91–5. doi: 10.1038/ejcn.2012.180.
  • Chudasama, Y. V., K. Khunti, C. L. Gillies, N. N. Dhalwani, M. J. Davies, T. Yates, and F. Zaccardi. 2020. Healthy lifestyle and life expectancy in people with multimorbidity in the UK Biobank: a longitudinal cohort study. PLoS Medicine 17 (9):e1003332. doi: 10.1371/journal.pmed.1003332.
  • Cross, A. J., J. R. Pollock, and S. A. Bingham. 2003. Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Research 63 (10):2358–60.
  • DGA 2015. U.S. Department of Health and Human Services and U.S. Department of Agriculture. 2015 – 2020 Dietary Guidelines for Americans. 8th ed. https://health.gov/our-work/food-nutrition/previous-dietary-guidelines/2015.
  • DGA 2020. U.S. Department of Agriculture and U.S. Department of Health and Human Services. Dietary guidelines for Americans, 2020–2025. 9th ed. DietaryGuidelines.gov.
  • Dyda, A., S. Stelzer-Braid, D. Adam, A. A. Chughtai, and C. R. MacIntyre. 2018. The association between acute flaccid myelitis (AFM) and Enterovirus D68 (EV-D68) - what is the evidence for causation? Eurosurveillance 23 (3):17–00310. doi: 10.2807/1560-7917.ES.2018.23.3.17-00310
  • Evert, A. B., M. Dennison, C. D. Gardner, W. T. Garvey, K. H. K. Lau, J. MacLeod, J. Mitri, R. F. Pereira, K. Rawlings, S. Robinson, Jr, et al. 2019. Nutrition therapy for adults with diabetes or prediabetes: a consensus report. Diabetes Care 42 (5):731–54. doi: 10.2337/dci19-0014.
  • Einarson, T. R., A. Acs, C. Ludwig, and U. H. Panton. 2018. Prevalence of cardiovascular disease in type 2 diabetes: A systematic literature review of scientific evidence from across the world in 2007-2017. Cardiovasc Diabetol 17 (1):83.
  • Fan, M., Y. Li, C. Wang, Z. Mao, W. Zhou, L. Zhang, X. Yang, S. Cui, and L. Li. 2019. Dietary protein consumption and the risk of type 2 diabetes: a dose-response meta-analysis of prospective studies. Nutrients 11 (11):2783. doi: 10.3390/nu11112783.
  • Farvid, M. S., M. C. Stern, T. Norat, S. Sasazuki, P. Vineis, M. P. Weijenberg, A. Wolk, K. Wu, B. W. Stewart, and E. Cho. 2018. Consumption of red and processed meat and breast cancer incidence: a systematic review and meta-analysis of prospective studies. International Journal of Cancer 143 (11):2787–99. doi: 10.1002/ijc.31848.
  • Feiveson, A. 2017. Explanation of the delta method. https://www.stata.com/support/faqs/statistics/delta-method/#.
  • Fundora, J. B., P. Guha, D. R. Shores, M. Pammi, and A. Maheshwari. 2020. Intestinal dysbiosis and necrotizing enterocolitis: assessment for causality using Bradford Hill criteria. Pediatric Research 87 (2):235–48. doi: 10.1038/s41390-019-0482-9.
  • Förstermann, U. 2008. Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nature Clinical Practice. Cardiovascular Medicine 5 (6):338–49. doi: 10.1038/ncpcardio1211.
  • Gascon, A., H. Jacques, S. Moorjani, Y. Deshaies, L. D. Brun, and P. Julien. 1996. Plasma lipoprotein profile and lipolytic activities in response to the substitution of lean white fish for other animal protein sources in premenopausal women. The American Journal of Clinical Nutrition 63 (3):315–21. doi: 10.1093/ajcn/63.3.315.
  • Gifford, C., L. O’Connor, W. Campbell, D. Woerner, and K. Belk. 2017. Broad and inconsistent muscle food classification is problematic for dietary guidance in the U.S. Nutrients 9 (9):1027. doi: 10.3390/nu9091027.
  • Guasch-Ferré, M., A. Satija, S. A. Blondin, M. Janiszewski, E. Emlen, L. E. O’Connor, W. W. Campbell, F. B. Hu, W. C. Willett, and M. J. Stampfer. 2019. Meta-analysis of randomized controlled trials of red meat consumption in comparison with various comparison diets on cardiovascular risk factors. Circulation 139 (15):1828–45. doi: 10.1161/CIRCULATIONAHA.118.035225.
  • He, F. J, and G. A. MacGregor. 2002. Effect of modest salt reduction on blood pressure: a meta-analysis of randomized trials. Implications for public health. Journal of Human Hypertension 16 (11):761–70. doi: 10.1038/sj.jhh.1001459.
  • Higgins, J., and S. Green 2011. Cochrane handbook for systematic reviews of intervention Version 5.1.0. Table 5.6a: Some advantages and disadvantages of broad versus narrow review questions. [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.handbook.cochrane.org.
  • Hill, A. B. 1965. The environment and disease: association or causation? Proceedings of the Royal Society of Medicine 58 (5):295–300. doi: 10.1177/003591576505800503.
  • Hodson, L., C. M. Skeaff, and W. A. Chisholm. 2001. The effect of replacing dietary saturated fat with polyunsaturated or monounsaturated fat on plasma lipids in free-living young adults. European Journal of Clinical Nutrition 55 (10):908–15. doi: 10.1038/sj.ejcn.1601234.
  • Iqbal, R., M. Dehghan, A. Mente, S. Rangarajan, A. Wielgosz, A. Avezum, P. Seron, K. F. AlHabib, P. Lopez-Jaramillo, S. Swaminathan, et al. 2021. Associations of unprocessed and processed meat intake with mortality and cardiovascular disease in 21 countries [Prospective Urban Rural Epidemiology (PURE) Study]: a prospective cohort study. The American Journal of Clinical Nutrition 114 (3):1049–58. doi: 10.1093/ajcn/nqaa448.
  • Johnston, B. C., P. Alonso-Coello, M. M. Bala, D. Zeraatkar, M. Rabassa, C. Valli, C. Marshall, R. E. Dib, R. W. M. Vernooij, P. O. Vandvik, et al. 2018. Methods for trustworthy nutritional recommendations NutriRECS (Nutritional Recommendations and accessible Evidence summaries Composed of Systematic reviews): a protocol. BMC Medical Research Methodology 18 (1):162. doi: 10.1186/s12874-018-0621-8.
  • Johnston, B. C., D. Zeraatkar, M. A. Han, R. W. M. Vernooij, C. Valli, R. E. Dib, C. Marshall, P. J. Stover, S. Fairweather-Taitt, G. Wójcik, et al. 2019. Unprocessed red meat and processed meat consumption: dietary guideline recommendations from the nutritional recommendations (NutriRECS) consortium. Annals of Internal Medicine 171 (10):756–64. doi: 10.7326/M19-1621.
  • Kaluza, J., A. Wolk, and S. C. Larsson. 2012. Red meat consumption and risk of stroke: a meta-analysis of prospective studies. Stroke 43 (10):2556–60. doi: 10.1161/STROKEAHA.112.663286.
  • Kaluza, J., A. Wolk, and S. C. Larsson. 2013. Heme iron intake and risk of stroke: a prospective study of men. Stroke 44 (2):334–9. doi: 10.1161/STROKEAHA.112.679662.
  • Kim, K., J. Hyeon, S. A. Lee, S. O. Kwon, H. Lee, N. Keum, J. K. Lee, and S. M. Park. 2017. Role of total, red, processed, and white meat consumption in stroke incidence and mortality: a systematic review and meta-analysis of prospective cohort studies. Journal of the American Heart Association. 6 (9):1–16.
  • Kim, S. R., K. Kim, S. A. Lee, S. O. Kwon, J. K. Lee, N. Keum, and S. M. Park. 2019. Effect of red, processed, and white meat consumption on the risk of gastric cancer: an overall and dose-response meta-analysis. Nutrients 11 (4):826. doi: 10.3390/nu11040826.
  • Kim, Y, and Y. Je. 2018. Meat consumption and risk of metabolic syndrome: results from the korean population and a meta-analysis of observational studies. Nutrients 10 (4):390. doi: 10.3390/nu10040390.
  • Kleinbongard, P., A. Dejam, T. Lauer, T. Jax, S. Kerber, P. Gharini, J. Balzer, R. B. Zotz, R. E. Scharf, R. Willers, et al. 2006. Plasma nitrite concentrations reflect the degree of endothelial dysfunction in humans. Free Radical Biology and Medicine 40 (2):295–302. doi: 10.1016/j.freeradbiomed.2005.08.025.
  • Klurfeld, D. M. 2015. Research gaps in evaluating the relationship of meat and health. Meat Science 109:86–95. doi: 10.1016/j.meatsci.2015.05.022.
  • Krishnan, S., L. E. O’Connor, Y. Wang, E. R. Gertz, W. W. Campbell, and B. J. Bennett. 2021. Adopting a Mediterranean-style eating pattern with low, but not moderate, unprocessed, lean red meat intake reduces fasting serum trimethylamine N-oxide (TMAO) in adults who are overweight or obese. British Journal of Nutrition 1–9. doi: 10.1017/S0007114521004694.
  • Lew, Q. J., T. H. Jafar, H. W. Koh, A. Jin, K. Y. Chow, J. M. Yuan, and W. P. Koh. 2017. Red meat intake and risk of ESRD. Journal of the American Society of Nephrology 28 (1):304–12. doi: 10.1681/ASN.2016030248.
  • Lichtenstein, A. H., L. J. Appel, M. Vadiveloo, F. B. Hu, P. M. Kris-Etherton, C. M. Rebholz, F. M. Sacks, A. N. Thorndike, L. Van Horn, and J. Wylie-Rosett. 2021. 2021 dietary guidance to improve cardiovascular health: a scientific statement from the American Heart Association. Circulation 144 (23):472–487. doi: 10.1161/CIR.0000000000001031.
  • Lippi, G., C. Mattiuzzi, and F. Sanchis-Gomar. 2015. Red meat consumption and ischemic heart disease. A systematic literature review. Meat Science 108:32–6. doi: 10.1016/j.meatsci.2015.05.019.
  • Liu, G., G. Zong, K. Wu, Y. Hu, Y. Li, W. C. Willett, D. M. Eisenberg, F. B. Hu, and Q. Sun. 2018. Meat cooking methods and risk of type 2 diabetes: results from three prospective cohort studies. Diabetes Care 41 (5):1049–60. doi: 10.2337/dc17-1992.
  • Livesey, G, and H. Livesey. 2019. Coronary heart disease and dietary carbohydrate, glycemic index, and glycemic load: dose-response meta-analyses of prospective cohort studies. Mayo Clinic Proceedings. Innovations, Quality & Outcomes 3 (1):52–69. doi: 10.1016/j.mayocpiqo.2018.12.007.
  • Livesey, G., R. Taylor, H. F. Livesey, A. E. Buyken, D. J. A. Jenkins, L. S. A. Augustin, J. L. Sievenpiper, A. W. Barclay, S. Liu, T. M. S. Wolever, et al. 2019. Dietary glycemic index and load and the risk of type 2 diabetes: assessment of causal relations. Nutrients 11 (6):1436. doi: 10.3390/nu11061436.
  • Maki, K. C., M. E. Van Elswyk, D. D. Alexander, T. M. Rains, E. L. Sohn, and S. McNeill. 2012. A meta-analysis of randomized controlled trials that compare the lipid effects of beef versus poultry and/or fish consumption. Journal of Clinical Lipidology 6 (4):352–61. doi: 10.1016/j.jacl.2012.01.001.
  • McGrowder, D., D. Ragoobirsingh, and T. Dasgupta. 2001. Effects of S-nitroso-N-acetyl-penicillamine administration on glucose tolerance and plasma levels of insulin and glucagon in the dog. Nitric Oxide. 5 (4):402–12. doi: 10.1006/niox.2001.0360.
  • Mente, A., L. de Koning, H. S. Shannon, and S. S. Anand. 2009. A systematic review of the evidence supporting a causal link between dietary factors and coronary heart disease. Archives of Internal Medicine 169 (7):659–69. doi: 10.1001/archinternmed.2009.38.
  • Micha, R., M. L. Shulkin, J. L. Peñalvo, S. Khatibzadeh, G. M. Singh, M. Rao, S. Fahimi, J. Powles, and D. Mozaffarian. 2017. Etiologic effects and optimal intakes of foods and nutrients for risk of ­cardiovascular diseases and diabetes: systematic reviews and meta-analyses from the Nutrition and Chronic Diseases Expert Group (NutriCoDE). PLoS One 12 (4):e0175149. doi: 10.1371/journal.pone.0175149.
  • Micha, R., S. K. Wallace, and D. Mozaffarian. 2010. Red and processed meat consumption and risk of incident coronary heart disease, stroke, and diabetes mellitus: a systematic review and meta-analysis. Circulation 121 (21):2271–83. doi: 10.1161/CIRCULATIONAHA.109.924977.
  • Moher, D., A. Liberati, J. Tetzlaff, and D. G. Altman. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ (Clinical Research ed.) 339:b2535. doi: 10.1136/bmj.b2535.
  • Naghipour, S., A. J. Cox, J. N. Peart, E. F. Du Toit, and J. P. Headrick. 2021. Trimethylamine N-oxide: heart of the microbiota-CVD nexus? Nutrition Research Reviews 34 (1):125–46. doi: 10.1017/S0954422420000177.
  • NCEP 2001. Executive Summary of the third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285 (19):2486–97. doi: 10.1001/jama.285.19.2486.
  • Neuhouser, M. L. 2020. Red and processed meat: more with less? The American Journal of Clinical Nutrition 111 (2):252–5. doi: 10.1093/ajcn/nqz294.
  • O'Connor, L. E., K. A. Herrick, R. Parsons, and J. Reedy. 2021. Heterogeneity in Meat Food Groups Can Meaningfully Alter Population-Level Intake Estimates of Red Meat and Poultry. Frontier in Nutrition 8:778369. doi: 10.3389/fnut.2021.778369. PMC: 34977122
  • O'Connor, L. E., C. L. Gifford, D. R. Woerner, J. L. Sharp, K. E. Belk, and W. W. Campbell. 2020. Dietary meat categories and descriptions in chronic disease research are substantively different within and between experimental and observational studies: a systematic review and landscape analysis. Advances in Nutrition. 11 (1):41–51.
  • O’Connor, L. E., J. E. Kim, and W. W. Campbell. 2017. Total red meat intake of ≥0.5 servings/d does not negatively influence cardiovascular disease risk factors: a systemically searched meta-analysis of randomized controlled trials. The American Journal of Clinical Nutrition 105 (1):57–69. doi: 10.3945/ajcn.116.142521.
  • O'Connor, L. E., J. E. Kim, C. M. Clark, W. Zhu, and W. W. Campbell. 2021. Effects of Total red meat intake on glycemic control and inflammatory biomarkers: a meta-analysis of randomized controlled trials. Advances in Nutrition 12 (1):115–27. doi: 10.1093/advances/nmaa096.
  • O'Connor, L. E., E. A. Wambogo, K. A. Herrick, R. Parsons, and J. Reedy. 2021. A Standardized Assessment of Processed Red Meat and Processed Poultry Intake in the US Population Aged ≥2 Years Using NHANES. The Journal of Nutrition 152 (1):190–9. doi: 10.1093/jn/nxab316.
  • O'Sullivan, T. A., K. Hafekost, F. Mitrou, and D. Lawrence. 2013. Food sources of saturated fat and the association with mortality: a meta-analysis. American Journal of Public Health 103 (9):e31–e42. doi: 10.2105/AJPH.2013.301492.
  • O’Connor, L. E, and W. W. Campbell. 2017. Red meat and health: getting to the heart of the matter. Nutrition Today 52 (4):167–73. doi: 10.1097/NT.0000000000000225.
  • Papier, K., A. Knuppel, N. Syam, S. A. Jebb, and T. J. Key. 2021. Meat consumption and risk of ischemic heart disease: a systematic review and meta-analysis. Critical Reviews in Food Science and Nutrition 1–12. doi: 10.1080/10408398.2021.1949575.
  • Portha, B., M. H. Giroix, J. C. Cros, and L. Picon. 1980. Diabetogenic effect of N-nitrosomethylurea and N-nitrosomethylurethane in the adult rat. Annales de la Nutrition et de L'alimentation 34 (5-6):1143–51.
  • Potischman, N, and D. L. Weed. 1999. Causal criteria in nutritional epidemiology. The American Journal of Clinical Nutrition 69 (6):1309s–14s. doi: 10.1093/ajcn/69.6.1309S.
  • PROSPERO 2011. International prospective register of systematic reviews. National Institute of Health Research. https://www.crd.york.ac.uk/prospero/.
  • Pérez-Martínez, P., D. P. Mikhailidis, V. G. Athyros, M. Bullo, P. Couture, M. I. Covas, L. de Koning, J. Delgado-Lista, A. Díaz-López, C. A. Drevon, et al. 2017. Lifestyle recommendations for the prevention and management of metabolic syndrome: an international panel recommendation. Nutrition Reviews 75 (5):307–26. doi: 10.1093/nutrit/nux014.
  • Rothman, K. J, and S. Greenland. 2005. Causation and causal inference in epidemiology. American Journal of Public Health 95 (Suppl 1):S144–S150. doi: 10.2105/AJPH.2004.059204.
  • Rouhani, M. H., A. Salehi-Abargouei, P. J. Surkan, and L. Azadbakht. 2014. Is there a relationship between red or processed meat intake and obesity? A systematic review and meta-analysis of observational studies. Obesity Reviews: An Official Journal of the International Association for the Study of Obesity 15 (9):740–8. doi: 10.1111/obr.12172.
  • Sacks, F. M., L. P. Svetkey, W. M. Vollmer, L. J. Appel, G. A. Bray, D. Harsha, E. Obarzanek, P. R. Conlin, E. R. Miller, D. G. Simons-Morton, et al. 2001. Effects on blood pressure of reduced dietary sodium and the Dietary Approaches to Stop Hypertension (DASH) diet. DASH-Sodium Collaborative Research Group. New England Journal of Medicine 344 (1):3–10. doi: 10.1056/NEJM200101043440101.
  • Sanders, P. W. 2009. Vascular consequences of dietary salt intake. American Journal of Physiology. Renal Physiology 297 (2):F237–243. doi: 10.1152/ajprenal.00027.2009.
  • Satija, A., E. Yu, W. C. Willett, and F. B. Hu. 2015. Understanding nutritional epidemiology and its role in policy. Advances in Nutrition (Bethesda, Md.) 6 (1):5–18. doi: 10.3945/an.114.007492.
  • Schlesinger, S., M. Neuenschwander, C. Schwedhelm, G. Hoffmann, A. Bechthold, H. Boeing, and L. Schwingshackl. 2019. Food groups and risk of overweight, obesity, and weight gain: a systematic review and dose-response meta-analysis of prospective studies. Advances in Nutrition (Bethesda, Md.) 10 (2):205–18. doi: 10.1093/advances/nmy092.
  • Schwingshackl, L., G. Hoffmann, K. Iqbal, C. Schwedhelm, and H. Boeing. 2018. Food groups and intermediate disease markers: a systematic review and network meta-analysis of randomized trials. The American Journal of Clinical Nutrition 108 (3):576–86. doi: 10.1093/ajcn/nqy151.
  • Schwingshackl, L., G. Hoffmann, A. M. Lampousi, S. Knüppel, K. Iqbal, C. Schwedhelm, A. Bechthold, S. Schlesinger, and H. Boeing. 2017. Food groups and risk of type 2 diabetes mellitus: a systematic review and meta-analysis of prospective studies. European Journal of Epidemiology 32 (5):363–75. doi: 10.1007/s10654-017-0246-y.
  • Schwingshackl, L., C. Schwedhelm, G. Hoffmann, S. Knüppel, K. Iqbal, V. Andriolo, A. Bechthold, S. Schlesinger, and H. Boeing. 2017. Food groups and risk of hypertension: a systematic review and dose-response meta-analysis of prospective studies. Advances in Nutrition (Bethesda, Md.) 8 (6):793–803. doi: 10.3945/an.117.017178.
  • Seman, D. L., D. D. Boler, C. C. Carr, M. E. Dikeman, C. M. Owens, J. T. Keeton, T. D. Pringle, J. J. Sindelar, D. R. Woerner, A. S. de Mello, et al. 2018. Meat science lexicon. Meat and Muscle Biology 2 (3). doi: 10.22175/mmb2017.12.0059.
  • Shan, Z., C. D. Rehm, G. Rogers, M. Ruan, D. D. Wang, F. B. Hu, D. Mozaffarian, F. F. Zhang, and S. N. Bhupathiraju. 2019. Trends in dietary carbohydrate, protein, and fat intake and diet quality among US adults, 1999-2016. JAMA 322 (12):1178–87. doi: 10.1001/jama.2019.13771.
  • Shea, B. J., J. M. Grimshaw, G. A. Wells, M. Boers, N. Andersson, C. Hamel, A. C. Porter, P. Tugwell, D. Moher, and L. M. Bouter. 2007. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Medical Research Methodology 7:10. doi: 10.1186/1471-2288-7-10.
  • Shea, B. J., B. C. Reeves, G. Wells, M. Thuku, C. Hamel, J. Moran, D. Moher, P. Tugwell, V. Welch, E. Kristjansson, et al. 2017. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ (Clinical Research ed.) 358:j4008. doi: 10.1136/bmj.j4008.
  • Shim, J. S., K. Oh, and H. C. Kim. 2014. Dietary assessment methods in epidemiologic studies. Epidemiol Health 36:e2014009.
  • Sinha, R., A. J. Cross, B. I. Graubard, M. F. Leitzmann, and A. Schatzkin. 2009. Meat intake and mortality: a prospective study of over half a million people. Archives of Internal Medicine 169 (6):562–71. doi: 10.1001/archinternmed.2009.6.
  • Sorkin, J. D., M. Manary, P. A. M. Smeets, A. J. MacFarlane, A. Astrup, R. L. Prigeon, B. B. Hogans, J. Odle, T. A. Davis, K. L. Tucker, et al. 2021. A guide for authors and readers of the American Society for Nutrition Journals on the proper use of P values and strategies that promote transparency and improve research reproducibility. The American Journal of Clinical Nutrition 114 (4):1280–5. doi: 10.1093/ajcn/nqab223.
  • Stern, C, and J. Kleijnen. 2020. Language bias in systematic reviews: you only get out what you put in. JBI Evidence Synthesis 18 (9):1818–9. doi: 10.11124/JBIES-20-00361.
  • Sterne, J., M. Egger, and D. Moher. 2011. Cochrane Handbook for Systematic Reviews of Intervention. Chapter 10: addressing reporting biases. In: Higgins J., and Green S. (editors). Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from www.handbook.cochrane.org.
  • Strazzullo, P., L. D'Elia, N. B. Kandala, and F. P. Cappuccio. 2009. Salt intake, stroke, and cardiovascular disease: meta-analysis of prospective studies. BMJ (Clinical Research ed.) 339:b4567. doi: 10.1136/bmj.b4567.
  • Subar, A. F., L. S. Freedman, J. A. Tooze, S. I. Kirkpatrick, C. Boushey, M. L. Neuhouser, F. E. Thompson, N. Potischman, P. M. Guenther, V. Tarasuk, et al. 2015. Addressing current criticism regarding the value of self-report dietary data. The Journal of Nutrition 145 (12):2639–45. doi: 10.3945/jn.115.219634.
  • Terrin, N., C. H. Schmid, and J. Lau. 2005. In an empirical evaluation of the funnel plot, researchers could not visually identify publication bias. Journal of Clinical Epidemiology 58 (9):894–901. doi: 10.1016/j.jclinepi.2005.01.006.
  • Thiese, M. S. 2014. Observational and interventional study design types; an overview. Biochemia Medica 24 (2):199–210. doi: 10.11613/BM.2014.022.
  • Tian, S., Q. Xu, R. Jiang, T. Han, C. Sun, and L. Na. 2017. Dietary protein consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies. Nutrients 9 (9):982. doi: 10.3390/nu9090982.
  • Todt, O, and J. L. Luján. 2017. Health claims and methodological controversy in nutrition science. Risk Analysis: An Official Publication of the Society for Risk Analysis 37 (5):958–68. doi: 10.1111/risa.12665.
  • University, B 2017. Boston University School of Public Health. Confidence Intervals for the Risk Ratio (Relative Risk). https://sphweb.bumc.bu.edu/otlt/MPH-Modules/BS/BS704_Confidence_Intervals/BS704_Confidence_Intervals8.html.
  • USDA 2015. Dietary Guidelines Advisory Committee. 2015. Scientific Report of the 2015 Dietary Guidelines Advisory Committee: Advisory Report to the Secretary of Health and Human Services and the Secretary of Agriculture. U.S. Department of Agriculture, Agricultural Research Service, Washington, DC.
  • USDA 2020. Dietary Guidelines Advisory Committee. 2020. Scientific Report of the 2020 Dietary Guidelines Advisory Committee: Advisory Report to the Secretary of Agriculture and the Secretary of Health and Human Services. U.S. Department of Agriculture, Agricultural Research Service, Washington, DC.
  • Valli, C., M. Rabassa, B. C. Johnston, R. Kuijpers, A. Prokop-Dorner, J. Zajac, D. Storman, M. Storman, M. M. Bala, I. Solà et al. 2019. Health-related values and preferences regarding meat consumption: a mixed-methods systematic review. Annals of Internal Medicine 171 (10):742–55. doi: 10.7326/M19-1326.
  • Vernooij, R. W., M. D. Zeraatkar, M. A. Han, R. E. Dib, M. Zworth, K. Milio, D. Sit, Y. Lee, H. Gomaa, C. Valli, et al. 2019. Patterns of red and processed meat consumption and risk for cardiometabolic and cancer outcomes: a systematic review and meta-analysis of cohort studies. Annals of Internal Medicine 171 (10):732–41. doi: 10.7326/M19-1583.
  • Wang, X., X. Lin, Y. Y. Ouyang, J. Liu, G. Zhao, A. Pan, and F. B. Hu. 2016. Red and processed meat consumption and mortality: dose-response meta-analysis of prospective cohort studies. Public Health Nutrition 19 (5):893–905. doi: 10.1017/S1368980015002062.
  • World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Judging the Evidence. Available at https://www.dietandcancerreport.org.
  • WCRF 2018. American Institute for Cancer Research Continuous Update Project. Meat, fish and dairy products and the risk of cancer. World Cancer Research Fund. www.wcrf.org/wp-content/uploads/2021/02/Meat-fish-and-dairy-products.pdf.
  • Weaver, C. M, and J. W. Miller. 2017. Challenges in conducting clinical nutrition research. Nutrition Reviews 75 (7):491–9. doi: 10.1093/nutrit/nux026.
  • Willett, W. 2012. Nutritional Epidemiology. Chapter 1: overview of nutritional epidemiology. Oxford University. doi: 10.1093/acprof:oso/9780199754038.003.0001.
  • Wolmarans, P., A. J. Benadé, T. J. Kotze, A. K. Daubitzer, M. P. Marais, and R. Laubscher. 1991. Plasma lipoprotein response to substituting fish for red meat in the diet. The American Journal of Clinical Nutrition 53 (5):1171–6. doi: 10.1093/ajcn/53.5.1171.
  • Yang, C., L. Pan, C. Sun, Y. Xi, L. Wang, and D. Li. 2016. Red meat consumption and the risk of stroke: a dose-response meta-analysis of prospective cohort studies. Journal of Stroke and Cerebrovascular Diseases: The Official Journal of National Stroke Association 25 (5):1177–86. doi: 10.1016/j.jstrokecerebrovasdis.2016.01.040.
  • Yang, X., Y. Li, C. Wang, Z. Mao, W. Zhou, L. Zhang, M. Fan, S. Cui, and L. Li. 2020. Meat and fish intake and type 2 diabetes: dose-response meta-analysis of prospective cohort studies. Diabetes & Metabolism 46 (5):345–52. doi: 10.1016/j.diabet.2020.03.004.
  • Zeraatkar, D., M. A. Han, G. H. Guyatt, R. W. M. Vernooij, R. E. Dib, K. Cheung, K. Milio, M. Zworth, J. J. Bartoszko, C. Valli, et al. 2019. Red and processed meat consumption and risk for all-cause mortality and cardiometabolic outcomes: a systematic review and meta-analysis of cohort studies. Annals of Internal Medicine 171 (10):703–10. doi: 10.7326/M19-0655.
  • Zeraatkar, D., B. C. Johnston, J. Bartoszko, K. Cheung, M. M. Bala, C. Valli, M. Rabassa, D. Sit, K. Milio, B. Sadeghirad, et al. 2019. Effect of lower versus higher red meat intake on cardiometabolic and cancer outcomes: a systematic review of randomized trials. Annals of Internal Medicine 171 (10):721–31. doi: 10.7326/M19-0622.
  • Zhao, Z., S. Li, G. Liu, F. Yan, X. Ma, Z. Huang, and H. Tian. 2012. Body iron stores and heme-iron intake in relation to risk of type 2 diabetes: a systematic review and meta-analysis. PLoS One 7 (7):e41641. doi: 10.1371/journal.pone.0041641.