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Dietary protein intake and risk of type 2 diabetes: a dose–response meta-analysis of prospective studies

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Abstract

Purpose

The association between dietary protein intake and type 2 diabetes risk has been inconsistent in the previous epidemiological studies. We aimed to quantitatively assess whether dietary total, animal, and plant protein would be associated with type 2 diabetes risk.

Methods

A comprehensive literature review was conducted to identify related articles by searching PubMed, Embase, Web of Science, and Wiley Online Library through 20th March 2018. Generalized least squares for trend estimation and restricted cubic spline regression model were applied in the dose–response analysis.

Results

Eight publications with ten prospective cohorts of 34,221 type 2 diabetes cases were included. After adjustment of potential confounders, a 5% of energy increment from dietary total and animal protein intake was related to a 9% (1.04, 1.13; I2 = 42.0%) and 12% (95% CI 1.08, 1.17; I2 = 14.0%) higher risk of type 2 diabetes respectively. However, for plant protein, a significant U-shaped curve was observed with the most risk reduction at intake of about 6% of energy intake from plant protein intake (Pnonlinearity = 0.001). The results were robust in sensitivity analysis and no publication bias was detected.

Conclusions

These findings indicate that the consumption of protein particularly animal protein may be associated with an increased risk of type 2 diabetes.

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Abbreviations

T2D:

Type 2 diabetes

RR:

Relative risks

CIs:

Confidence intervals

BMI:

Body mass index

References

  1. World Health Organization (2016) Global report on diabetes. World Health Organization, Geneva

  2. Gregg EW, Sattar N, Ali MK (2016) The changing face of diabetes complications. Lancet Diabetes Endocrinol 4:537–547. https://doi.org/10.1016/s2213-8587(16)30010-9

    Article  PubMed  Google Scholar 

  3. Promintzer M, Krebs M (2006) Effects of dietary protein on glucose homeostasis. Curr Opin Clin Nutr Metab Care 9:463–468. https://doi.org/10.1097/01.mco.0000232909.84483.a9

    Article  CAS  PubMed  Google Scholar 

  4. Rietman A, Schwarz J, Tome D, Kok FJ, Mensink M (2014) High dietary protein intake, reducing or eliciting insulin resistance? Eur J Clin Nutr 68:973–979. https://doi.org/10.1038/ejcn.2014.123

    Article  CAS  PubMed  Google Scholar 

  5. Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D, Soenen S, Westerterp KR (2009) Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr 29:21–41. https://doi.org/10.1146/annurev-nutr-080508-141056

    Article  CAS  PubMed  Google Scholar 

  6. Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Willett WC, Hu FB (2011) Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. Am J Clin Nutr 94:1088–1096. https://doi.org/10.3945/ajcn.111.018978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bendinelli B, Palli D, Masala G, Sharp SJ, Schulze MB, Guevara M, van der AD, Sera F, Amiano P, Balkau B, Barricarte A, Boeing H, Crowe FL, Dahm CC, Dalmeijer G, de Lauzon-Guillain B, Egeberg R, Fagherazzi G, Franks PW, Krogh V, Huerta JM, Jakszyn P, Khaw KT, Li K, Mattiello A, Nilsson PM, Overvad K, Ricceri F, Rolandsson O, Sanchez MJ, Slimani N, Sluijs I, Spijkerman AM, Teucher B, Tjonneland A, Tumino R, van den Berg SW, Forouhi NG, Langeberg C, Feskens EJ, Riboli E, Wareham NJ (2013) Association between dietary meat consumption and incident type 2 diabetes: the EPIC-InterAct study. Diabetologia 56:47–59. https://doi.org/10.1007/s00125-012-2718-7

    Article  CAS  PubMed  Google Scholar 

  8. Afshin A, Micha R, Khatibzadeh S, Mozaffarian D (2014) Consumption of nuts and legumes and risk of incident ischemic heart disease, stroke, and diabetes: a systematic review and meta-analysis. Am J Clin Nutr 100:278–288. https://doi.org/10.3945/ajcn.113.076901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Nanri A, Mizoue T, Takahashi Y, Kirii K, Inoue M, Noda M, Tsugane S (2010) Soy product and isoflavone intakes are associated with a lower risk of type 2 diabetes in overweight Japanese women. J Nutr 140:580–586. https://doi.org/10.3945/jn.109.116020

    Article  CAS  PubMed  Google Scholar 

  10. Sluijs I, Beulens JW, van der AD, Spijkerman AM, Grobbee DE, van der Schouw YT (2010) Dietary intake of total, animal, and vegetable protein and risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-NL study. Diabetes Care 33:43–48. https://doi.org/10.2337/dc09-1321

    Article  CAS  PubMed  Google Scholar 

  11. Wang ET, De Koning L, Kanaya AM (2010) Higher protein intake is associated with diabetes risk in South Asian Indians: the metabolic syndrome and atherosclerosis in South Asians Living in America (MASALA) study. J Am Coll Nutr 29:130–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ericson U, Sonestedt E, Gullberg B, Hellstrand S, Hindy G, Wirfalt E, Orho-Melander M (2013) High intakes of protein and processed meat associate with increased incidence of type 2 diabetes. Br J Nutr 109:1143–1153. https://doi.org/10.1017/S0007114512003017

    Article  CAS  PubMed  Google Scholar 

  13. Nielen M, Feskens EJM, Mensink M, Sluijs I, Molina E, Amiano P, Ardanaz E, Balkau B, Beulens JWJ, Boeing H, Clavel-Chapelon F, Fagherazzi G, Franks PW, Halkjaer J, Huerta JM, Katzke V, Key TJ, Khaw KT, Krogh V, Kuhn T, Menendez VVM, Nilsson P, Overvad K, Palli D, Panico S, Rolandsson O, Romieu I, Sacerdote C, Sanchez MJ, Schulze MB, Spijkerman AMW, Tjonneland A, Tumino R, A DL, Wurtz AML, Zamora-Ros R, Langenberg C, Sharp SJ, Forouhi NG, Riboli E, Wareham NJ (2014) Dietary protein intake and incidence of type 2 diabetes in Europe: the EPIC-InterAct case-cohort study. Diabetes Care 37:1854–1862. https://doi.org/10.2337/dc13-2627

    Article  CAS  PubMed  Google Scholar 

  14. Malik VS, Li Y, Tobias DK, Pan A, Hu FB (2016) Dietary protein intake and risk of type 2 diabetes in US men and women. Am J Epidemiol 183:715–728. https://doi.org/10.1093/aje/kwv268

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, Group P-P (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 349:g7647. https://doi.org/10.1136/bmj.g7647 (Clinical research ed.)

    Article  Google Scholar 

  16. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 11 Nov 2017

  17. DerSimonian R, Laird N (2015) Meta-analysis in clinical trials revisited. Contemp Clin Trials 45:139–145. https://doi.org/10.1016/j.cct.2015.09.002

    Article  PubMed  PubMed Central  Google Scholar 

  18. Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309

    Article  CAS  PubMed  Google Scholar 

  19. Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D (2012) Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 175:66–73. https://doi.org/10.1093/aje/kwr265

    Article  PubMed  Google Scholar 

  20. Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose–response data. Stata J 6:40–57

    Article  Google Scholar 

  21. Jackson D, White IR, Thompson SG (2010) Extending DerSimonian and Laird’s methodology to perform multivariate random effects meta-analyses. Stat Med 29:1282–1297. https://doi.org/10.1002/sim.3602

    Article  PubMed  Google Scholar 

  22. Desquilbet L, Mariotti F (2010) Dose-response analyses using restricted cubic spline functions in public health research. Stat Med 29:1037–1057. https://doi.org/10.1002/sim.3841

    Article  PubMed  Google Scholar 

  23. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558. https://doi.org/10.1002/sim.1186

    Article  PubMed  Google Scholar 

  24. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Song Y, Buring JE, Manson JE, Liu SM (2004) A prospective study of red meat consumption and type 2 diabetes in middle-aged and elderly women. Diabetes Care 27:2108–2115. https://doi.org/10.2337/diacare.27.9.2108

    Article  CAS  PubMed  Google Scholar 

  26. Tinker LF, Sarto GE, Howard BV, Huang Y, Neuhouser ML, Mossavar-Rahmani Y, Beasley JM, Margolis KL, Eaton CB, Phillips LS, Prentice RL (2011) Biomarker-calibrated dietary energy and protein intake associations with diabetes risk among postmenopausal women from the Women’s Health Initiative. Am J Clin Nutr 94:1600–1606. https://doi.org/10.3945/ajcn.111.018648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Alhazmi A, Stojanovski E, McEvoy M, Garg ML (2014) Macronutrient intake and type 2 diabetes risk in middle-aged Australian women. Results from the Australian Longitudinal Study on Women’s Health. Public health Nutr 17:1587–1594. https://doi.org/10.1017/s1368980013001870

    Article  PubMed  Google Scholar 

  28. Shang X, Scott D, Hodge AM, English DR, Giles GG, Ebeling PR, Sanders KM (2016) Dietary protein intake and risk of type 2 diabetes: results from the Melbourne Collaborative Cohort Study and a meta-analysis of prospective studies. Am J Clin Nutr 104:1352–1365. https://doi.org/10.3945/ajcn.116.140954

    Article  CAS  PubMed  Google Scholar 

  29. Virtanen HEK, Koskinen TT, Voutilainen S, Mursu J, Tuomainen TP, Kokko P, Virtanen JK (2017) Intake of different dietary proteins and risk of type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Br J Nutr 117:882–893. https://doi.org/10.1017/S0007114517000745

    Article  CAS  PubMed  Google Scholar 

  30. Nanri A, Mizoue T, Kurotani K, Goto A, Oba S, Noda M, Sawada N, Tsugane S (2015) Low-carbohydrate diet and type 2 diabetes risk in Japanese men and women: the Japan Public Health Center-Based Prospective Study. PLoS One 10:e0118377. https://doi.org/10.1371/journal.pone.0118377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Van Nielen M, Feskens E, Mensink M, Forouhi N, Wareham N (2013) Dietary protein intake and the incidence of type 2 diabetes in Europe: the epic-interact case-cohort study. Ann Nutr Metab 63:201

    Google Scholar 

  32. Virtanen HEK, Koskinen TT, Voutilainen S, Mursu J, Tuomainen T-P, Kokko P, Virtanen JK (2017) Intake of different dietary proteins and risk of type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Br J Nutr. https://doi.org/10.1017/s0007114517000745

    Article  PubMed  PubMed Central  Google Scholar 

  33. Koloverou E, Esposito K, Giugliano D, Panagiotakos D (2014) The effect of Mediterranean diet on the development of type 2 diabetes mellitus: a meta-analysis of 10 prospective studies and 136,846 participants. Metab Clin Exp 63:903–911. https://doi.org/10.1016/j.metabol.2014.04.010

    Article  CAS  PubMed  Google Scholar 

  34. McEvoy CT, Cardwell CR, Woodside JV, Young IS, Hunter SJ, McKinley MC (2014) A posteriori dietary patterns are related to risk of type 2 diabetes: findings from a systematic review and meta-analysis. J Acad Nutr Diet 114:1759–1775 e1754. https://doi.org/10.1016/j.jand.2014.05.001

    Article  PubMed  Google Scholar 

  35. Neu A, Behret F, Braun R, Herrlich S, Liebrich F, Loesch-Binder M, Schneider A, Schweizer R (2015) Higher glucose concentrations following protein- and fat-rich meals—the Tuebingen Grill Study: a pilot study in adolescents with type 1 diabetes. Pediatr Diabetes 16:587–591. https://doi.org/10.1111/pedi.12224

    Article  CAS  PubMed  Google Scholar 

  36. Tremblay F, Lavigne C, Jacques H, Marette A (2007) Role of dietary proteins and amino acids in the pathogenesis of insulin resistance. Annu Rev Nutr 27:293–310. https://doi.org/10.1146/annurev.nutr.25.050304.092545

    Article  CAS  PubMed  Google Scholar 

  37. Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, McCabe E, Lewis GD, Fox CS, Jacques PF, Fernandez C, O’Donnell CJ, Carr SA, Mootha VK, Florez JC, Souza A, Melander O, Clish CB, Gerszten RE (2011) Metabolite profiles and the risk of developing diabetes. Nat Med 17:448–453. https://doi.org/10.1038/nm.2307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Floegel A, Stefan N, Yu Z, Muhlenbruch K, Drogan D, Joost HG, Fritsche A, Haring HU, Hrabe de Angelis M, Peters A, Roden M, Prehn C, Wang-Sattler R, Illig T, Schulze MB, Adamski J, Boeing H, Pischon T (2013) Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes 62:639–648. https://doi.org/10.2337/db12-0495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Adeva MM, Calvino J, Souto G, Donapetry C (2012) Insulin resistance and the metabolism of branched-chain amino acids in humans. Amino Acids 43:171–181. https://doi.org/10.1007/s00726-011-1088-7

    Article  CAS  PubMed  Google Scholar 

  40. Bantle JP, Wylie-Rosett J, Albright AL, Apovian CM, Clark NG, Franz MJ, Hoogwerf BJ, Lichtenstein AH, Mayer-Davis E, Mooradian AD, Wheeler ML (2008) Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association. Diabetes Care 31(Suppl 1):S61–78. https://doi.org/10.2337/dc08-S061

    Article  CAS  PubMed  Google Scholar 

  41. Song M, Fung TT, Hu FB, Willett WC, Longo VD, Chan AT, Giovannucci EL (2016) Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med. https://doi.org/10.1001/jamainternmed.2016.4182

    Article  PubMed  PubMed Central  Google Scholar 

  42. Chen X, Wei G, Jalili T, Metos J, Giri A, Cho ME, Boucher R, Greene T, Beddhu S (2016) The associations of plant protein intake with all-cause mortality in CKD. Am J Kidney Dis Off J Natl Kidney Found 67:423–430. https://doi.org/10.1053/j.ajkd.2015.10.018

    Article  CAS  Google Scholar 

  43. Alhazmi A, Stojanovski E, McEvoy M, Garg ML (2012) Macronutrient intakes and development of type 2 diabetes: a systematic review and meta-analysis of cohort studies. J Am Coll Nutr 31:243–258

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the original studies for the contribution to conduct our meta-analysis.

Funding

This work was supported by funds from the State Key Laboratory of Oncogenes and Related Genes (#91-15-10).

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Author notes

  1. Long-Gang Zhao and Qing-Li Zhang are co-first authors and they have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Oncogene and Related Genes and Department of Epidemiology, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiaotong University School of Medicine, No. 25, Lane 2200, Xie Tu Road, Shanghai, 200032, People’s Republic of China

    Long-Gang Zhao, Qing-Li Zhang, Xiao-Li Liu, Hua Wu & Yong-Bing Xiang

  2. Division of Cancer Prevention and Population Sciences, Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, TX, 77030, USA

    Jia-Li Zheng

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  1. Long-Gang Zhao
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Contributions

Y-BX obtained the funding, conducted the research design, interpreted the results, and also had primary responsibility for the final content. L-GZ and Q-LZ analyzed the data and interpreted the results. L-GZ and Q-LZ drafted first manuscript. All authors critically reviewed and approved the manuscript. No authors have any conflicts of interest to declare.

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Correspondence to Yong-Bing Xiang.

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Zhao, LG., Zhang, QL., Liu, XL. et al. Dietary protein intake and risk of type 2 diabetes: a dose–response meta-analysis of prospective studies. Eur J Nutr 58, 1351–1367 (2019). https://doi.org/10.1007/s00394-018-1737-7

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