Advertisement
Review Article| Volume 191, 110071, September 2022

Consumption of different animal-based foods and risk of type 2 diabetes: An umbrella review of meta-analyses of prospective studies

Published:September 02, 2022DOI:https://doi.org/10.1016/j.diabres.2022.110071

      Abstract

      We performed an umbrella review of dose–response meta-analyses of prospective studies reporting the incidence of type 2 diabetes associated with the consumption of animal-based foods. A systematic search was conducted in PubMed, Web of Science, Scopus, and Embase according to PRISMA. Thirteen meta-analyses are included in the study providing 175 summary risk ratio estimates. The consumption of 100 g/day of total or red meat, or 50 g/day of processed meat, were associated with an increased risk; RR and 95 % CI were respectively 1.20, 1.13–1.27; 1.22, 1.14–1.30 and 1.30, 1.22–1.39. White meat (50 g/day) was associated with an increased risk, but of lesser magnitude (RR 1.04, 95 % CI 1.00–1.08). A risk reduction was reported for 200 g/day of total dairy (RR 0.95, 95 % CI 0.92–0.98) or low-fat dairy (RR 0.96, 95 % CI 0.92–1.00) or milk (RR 0.90, 95 % CI 0.83–0.98), or 100 g/day of yogurt (RR 0.94, 95 % CI 0.90–0.98). No association with diabetes risk was reported for fish or eggs. In conclusions animal-based foods have a different association with diabetes risk. To reduce diabetes risk the consumption of red and processed meat should be restricted; a moderate consumption of dairy foods, milk and yogurt, can be encouraged; moderate amounts of fish and eggs are allowed.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Diabetes Research and Clinical Practice
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. Chung WK, Erion K, Florez JC, Hattersley AT, Hivert MF, Lee CG, et al. Precision medicine in diabetes: a consensus report from the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetes Care 2020;43. doi: 10.2337/dci20-0022.

        • Afshin A.
        • Sur P.J.
        • Fay K.A.
        • Cornaby L.
        • Ferrara G.
        • Salama J.S.
        • et al.
        Health effects of dietary risks in 195 countries, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017.
        The Lancet. 2019; 393: 1958-1972https://doi.org/10.1016/S0140-6736(19)30041-8
      2. Erratum: Department of Error (The Lancet (2019) 393(10184) (1958–1972), (S0140673619300418), (10.1016/S0140-6736(19)30041-8)). The Lancet 2021;397. doi: 10.1016/S0140-6736(21)01342-8.

        • Schwingshackl L.
        • Missbach B.
        • König J.
        • Hoffmann G.
        Adherence to a Mediterranean diet and risk of diabetes: a systematic review and meta-analysis.
        Public Health Nutr. 2015; 18: 1292-1299https://doi.org/10.1017/S1368980014001542
        • Schwingshackl L.
        • Hoffmann G.
        Diet quality as assessed by the healthy eating index, the alternate healthy eating index, the dietary approaches to stop hypertension score, and health outcomes: a systematic review and meta-analysis of cohort studies.
        J Acad Nutr Diet. 2015; 115: 780-800.e5https://doi.org/10.1016/j.jand.2014.12.009
        • Lindström J.
        • Ilanne-Parikka P.
        • Peltonen M.
        • Aunola S.
        • Eriksson J.G.
        • Hemiö K.
        • et al.
        Sustained reduction in the incidence of type 2 diabetes by lifestyle intervention: follow-up of the Finnish Diabetes Prevention Study.
        Lancet. 2006; 368: 1673-1679https://doi.org/10.1016/S0140-6736(06)69701-8
      3. American Diabetes Association Professional Practice Committee, Draznin B, Aroda VR, Bakris G, Benson G, Brown FM, et al. 8. Obesity and weight management for the prevention and treatment of type 2 diabetes: standards of medical care in diabetes-2022. Diabetes Care 2022;45:S113–24. doi: 10.2337/dc22-S008.

        • Paulweber B.
        • Valensi P.
        • Lindström J.
        • Lalic N.
        • Greaves C.
        • McKee M.
        • et al.
        A European evidence-based guideline for the prevention of type 2 diabetes.
        Hormone Metabolic Res = Hormon- Und Stoffwechselforschung = Hormones et Metabolisme. 2010; 42: S3-S36https://doi.org/10.1055/s-0029-1240928
        • Ley S.H.
        • Hamdy O.
        • Mohan V.
        • Hu F.B.
        Prevention and management of type 2 diabetes: dietary components and nutritional strategies.
        Lancet. 2014; 383: 1999-2007https://doi.org/10.1016/S0140-6736(14)60613-9
        • Halkjær J.
        • Olsen A.
        • Bjerregaard L.J.
        • Deharveng G.
        • Tjønneland A.
        • Welch A.A.
        • et al.
        Intake of total, animal and plant proteins, and their food sources in 10 countries in the European Prospective Investigation into Cancer and Nutrition.
        Eur J Clin Nutr. 2009; 63: S16-S36https://doi.org/10.1038/ejcn.2009.73
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        • Altman D.
        • Antes G.
        • et al.
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        Ann Intern Med. 2009; https://doi.org/10.7326/0003-4819-151-4-200908180-00135
        • Shea B.J.
        • Hamel C.
        • Wells G.A.
        • Bouter L.M.
        • Kristjansson E.
        • Grimshaw J.
        • et al.
        AMSTAR is a reliable and valid measurement tool to assess the methodological quality of systematic reviews.
        J Clin Epidemiol. 2009; 62: 1013-1020https://doi.org/10.1016/j.jclinepi.2008.10.009
        • Shea B.J.
        • Bouter L.M.
        • Peterson J.
        • Boers M.
        • Andersson N.
        • Ortiz Z.
        • et al.
        External validation of a measurement tool to assess systematic reviews (AMSTAR).
        PLoS ONE. 2007; 2: e1350https://doi.org/10.1371/journal.pone.0001350
      4. Sharif MO, Sharif FNJ, Ali H, Ahmed F. Systematic reviews explained: AMSTAR-how to tell the good from the bad and the ugly. Oral Health Dent Manag 2013;12.

        • Schwingshackl L.
        • Knüppel S.
        • Schwedhelm C.
        • Hoffmann G.
        • Missbach B.
        • Stelmach-Mardas M.
        • 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: 994-1004https://doi.org/10.3945/an.116.013052
        • DerSimonian R.
        • Laird N.
        Meta-analysis in clinical trials revisited.
        Contemp Clin Trials. 2015; 45: 139-145https://doi.org/10.1016/j.cct.2015.09.002
        • Higgins J.P.
        • Thompson S.G.
        • Deeks J.J.
        • Altman D.G.
        Measuring inconsistency in meta-analyses.
        BMJ. 2003; 327: 557-560https://doi.org/10.1136/bmj.327.7414.557
        • Riley R.D.
        • Higgins J.P.T.
        • Deeks J.J.
        Interpretation of random effects meta-analyses.
        BMJ. 2011; 342: d549https://doi.org/10.1136/bmj.d549
        • Egger M.
        • Smith G.D.
        • Schneider M.
        • Minder C.
        Bias in meta-analysis detected by a simple, graphical test.
        BMJ. 1997; 315: 629-634https://doi.org/10.1136/bmj.315.7109.629
        • Micha R.
        • Wallace S.K.
        • Mozaffarian D.
        Red and processed meat consumption and risk of incident coronary heart disease, stroke, and diabetes mellitus: a systematic review and meta-analysis.
        Circulation. 2010; 121: 2271-2283https://doi.org/10.1161/CIRCULATIONAHA.109.924977
        • Feskens E.J.M.
        • Sluik D.
        • van Woudenbergh G.J.
        Meat consumption, diabetes, and its complications.
        Curr DiabRep. 2013; 13: 298-306https://doi.org/10.1007/s11892-013-0365-0
        • Yang X.
        • Li Y.
        • Wang C.
        • Mao Z.
        • Zhou W.
        • Zhang L.
        • et al.
        Meat and fish intake and type 2 diabetes: dose–response meta-analysis of prospective cohort studies.
        Diabetes Metabolism. 2020; 46: 345-352https://doi.org/10.1016/j.diabet.2020.03.004
        • Aune D.
        • Ursin G.
        • Veierød M.B.
        Meat consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies.
        Diabetologia. 2009; 52: 2277-2287https://doi.org/10.1007/s00125-009-1481-x
        • Schwingshackl L.
        • Hoffmann G.
        • Lampousi A.-M.
        • Knüppel S.
        • Iqbal K.
        • Schwedhelm C.
        • et al.
        Food groups and risk of type 2 diabetes mellitus: a systematic review and meta-analysis of prospective studies.
        Eur J Epidemiol. 2017; 32: 363-375https://doi.org/10.1007/s10654-017-0246-y
        • Fan M.
        • Li Y.
        • Wang C.
        • Mao Z.
        • Zhou W.
        • Zhang L.
        • et al.
        Dietary protein consumption and the risk of type 2 diabetes: a dose-response meta-analysis of prospective studies.
        Nutrients. 2019; 11: 2783https://doi.org/10.3390/nu11112783
        • Wu J.H.Y.
        • Micha R.
        • Imamura F.
        • Pan A.n.
        • Biggs M.L.
        • Ajaz O.
        • et al.
        Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis.
        Br J Nutr. 2012; 107: S214-S227https://doi.org/10.1017/S0007114512001602
        • Pastorino S.
        • Bishop T.
        • Sharp S.J.
        • Pearce M.
        • Akbaraly T.
        • Barbieri N.B.
        • et al.
        Heterogeneity of associations between total and types of fish intake and the incidence of type 2 diabetes: federated meta-analysis of 28 prospective studies including 956,122 participants.
        Nutrients. 2021; 13: 1223https://doi.org/10.3390/nu13041223
        • Gao D.
        • Ning N.
        • Wang C.
        • Wang Y.
        • Li Q.
        • Meng Z.
        • et al.
        Dairy products consumption and risk of type 2 diabetes: systematic review and dose-response meta-analysis.
        PLoS ONE. 2013; 8: e73965https://doi.org/10.1371/journal.pone.0073965
        • Soedamah-Muthu S.S.
        • de Goede J.
        Dairy consumption and cardiometabolic diseases: systematic review and updated meta-analyses of prospective cohort studies.
        Curr Nutr Rep. 2018; 7: 171-182https://doi.org/10.1007/s13668-018-0253-y
        • Aune D.
        • Norat T.
        • Romundstad P.
        • Vatten L.J.
        Dairy products and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies.
        Am J Clin Nutr. 2013; 98: 1066-1083https://doi.org/10.3945/ajcn.113.059030
        • Gijsbers L.
        • Ding E.L.
        • Malik V.S.
        • de Goede J.
        • Geleijnse J.M.
        • Soedamah-Muthu S.S.
        Consumption of dairy foods and diabetes incidence: a dose-response meta-analysis of observational studies.
        Am J Clin Nutr. 2016; 103: 1111-1124https://doi.org/10.3945/ajcn.115.123216
        • Drouin-Chartier J.-P.
        • Schwab A.L.
        • Chen S.
        • Li Y.
        • Sacks F.M.
        • Rosner B.
        • et al.
        Egg consumption and risk of type 2 diabetes: findings from 3 large US cohort studies of men and women and a systematic review and meta-analysis of prospective cohort studies.
        Am J Clin Nutr. 2020; 112: 619-630https://doi.org/10.1093/ajcn/nqaa115
        • Neuenschwander M.
        • Ballon A.
        • Weber K.S.
        • Norat T.
        • Aune D.
        • Schwingshackl L.
        • et al.
        Role of diet in type 2 diabetes incidence: umbrella review of meta-analyses of prospective observational studies.
        BMJ. 2019; 366l2368https://doi.org/10.1136/bmj.l2368
        • Vessby B.
        Dietary fat and insulin action in humans.
        Br J Nutr. 2000; 83: S91-S96
        • Cavicchia P.P.
        • Steck S.E.
        • Hurley T.G.
        • Hussey J.R.
        • Ma Y.
        • Ockene I.S.
        • et al.
        A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein.
        J Nutr. 2009; 139: 2365-2372https://doi.org/10.3945/jn.109.114025
        • Förstermann U.
        Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies.
        Nat. Clin. Pract. Cardiovasc. Med. 2008; 5: 338-349https://doi.org/10.1038/ncpcardio1211
        • Lundberg J.O.
        • Carlström M.
        • Weitzberg E.
        Metabolic effects of dietary nitrate in health and disease.
        Cell Metab. 2018; 28: 9-22https://doi.org/10.1016/j.cmet.2018.06.007
        • Mitri J.
        • Muraru M.D.
        • Pittas A.G.
        Vitamin D and type 2 diabetes: a systematic review.
        Eur J Clin Nutr. 2011; 65: 1005-1015https://doi.org/10.1038/ejcn.2011.118
        • Dong J.-Y.
        • Xun P.
        • He K.
        • Qin L.-Q.
        Magnesium intake and risk of type 2 diabetes: meta-analysis of prospective cohort studies.
        Diabetes Care. 2011; 34: 2116-2122https://doi.org/10.2337/dc11-0518
        • Funaki M.
        Saturated fatty acids and insulin resistance.
        J Med Invest. 2009; 56: 88-92https://doi.org/10.2152/jmi.56.88
        • Jahan-Mihan A.
        • Luhovyy B.L.
        • el Khoury D.
        • Anderson G.H.
        Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract.
        Nutrients. 2011; 3: 574-603https://doi.org/10.3390/nu3050574
        • Anderson G.H.
        • Moore S.E.
        Dietary proteins in the regulation of food intake and body weight in humans.
        J Nutr. 2004; 134: 974Shttps://doi.org/10.1093/jn/134.4.974S
        • Zemel M.B.
        • Shi H.
        • Greer B.
        • Dirienzo D.
        • Zemel P.C.
        Regulation of adiposity by dietary calcium.
        FASEB J. 2000; 14: 1132-1138
        • El Khoury D.
        • Vien S.
        • Sanchez-Hernandez D.
        • Kung B.
        • Wright A.
        • Goff H.D.
        • et al.
        Increased milk protein content and whey-to-casein ratio in milk served with breakfast cereal reduce postprandial glycemia in healthy adults: an examination of mechanisms of action.
        J Dairy Sci. 2019; 102: 6766-6780https://doi.org/10.3168/jds.2019-16358
        • Hidayat K.
        • Du X.
        • Shi B.-M.
        Milk in the prevention and management of type 2 diabetes: the potential role of milk proteins.
        Diabetes Metab Res Rev. 2019; 35https://doi.org/10.1002/dmrr.3187
        • Giosuè A.
        • Calabrese I.
        • Vitale M.
        • Riccardi G.
        • Vaccaro O.
        Consumption of dairy foods and cardiovascular disease: a systematic review.
        Nutrients. 2022; 14: 831https://doi.org/10.3390/nu14040831
        • Kim Y.A.
        • Keogh J.B.
        • Clifton P.M.
        Probiotics, prebiotics, synbiotics and insulin sensitivity.
        Nutr Res Rev. 2018; 31: 35-51https://doi.org/10.1017/S095442241700018X
        • Mozaffarian D.
        • Wu J.H.Y.
        Flavonoids, dairy foods, and cardiovascular and metabolic health: a review of emerging biologic pathways.
        Circ Res. 2018; 122: 369-384https://doi.org/10.1161/CIRCRESAHA.117.309008
        • Astrup A.
        • Geiker N.R.W.
        • Magkos F.
        Effects of full-fat and fermented dairy products on cardiometabolic disease: food is more than the sum of its parts.
        Adv Nutr. 2019; 10: 924S-930Shttps://doi.org/10.1093/advances/nmz069
        • Echarte M.
        • Zulet M.A.
        • Astiasaran I.
        Oxidation process affecting fatty acids and cholesterol in fried and roasted salmon.
        J Agric Food Chem. 2001; 49: 5662-5667https://doi.org/10.1021/jf010199e
        • Salmerón J.
        • Hu F.B.
        • Manson J.E.
        • Stampfer M.J.
        • Colditz G.A.
        • Rimm E.B.
        • et al.
        Dietary fat intake and risk of type 2 diabetes in women.
        Am J Clin Nutr. 2001; 73: 1019-1026https://doi.org/10.1093/ajcn/73.6.1019
        • Lopez-Garcia E.
        • Schulze M.B.
        • Meigs J.B.
        • Manson J.E.
        • Rifai N.
        • Stampfer M.J.
        • et al.
        Consumption of trans fatty acids is related to plasma biomarkers of inflammation and endothelial dysfunction.
        J Nutr. 2005; 135: 562-566https://doi.org/10.1093/jn/135.3.562
        • Tomey K.M.
        • Sowers M.R.
        • Li X.
        • McConnell D.S.
        • Crawford S.
        • Gold E.B.
        • et al.
        Dietary fat subgroups, zinc, and vegetable components are related to urine F2a-isoprostane concentration, a measure of oxidative stress, in midlife women.
        J Nutr. 2007; 137: 2412-2419https://doi.org/10.1093/jn/137.11.2412