Advertisement

Impact of different dietary approaches on blood lipid control in patients with type 2 diabetes mellitus: a systematic review and network meta-analysis

  • Manuela Neuenschwander
  • Georg Hoffmann
  • Lukas SchwingshacklEmail author
  • Sabrina Schlesinger
META-ANALYSIS

Abstract

The aim of this study was to assess the effects of different dietary approaches on low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, and triglyceride (TG) levels in patients with type 2 diabetes (T2D) by applying network meta-analysis (NMA). Systematic electronic and hand searches were conducted until January 2018. Randomized controlled trials (RCTs) with an intervention period of ≥ 12 weeks, focussing on adults with T2D, and comparing dietary approaches regarding LDL, HDL or TGs, were included. For each outcome measure, random effects NMA was performed in order to determine the effect of each dietary approach compared to every other dietary intervention. Mean differences (MDs) and 95% confidence intervals (95% CIs) were calculated, and for the ranking, the surface under the cumulative ranking curves (SUCRA) was determined. Additionally, the credibility of evidence was evaluated. 52 RCTs (44 for LDL, 48 for HDL and 52 for TGs) comparing nine dietary approaches (low fat, vegetarian, Mediterranean, high protein, moderate carbohydrate, low carbohydrate, control, low glycaemic index/glycaemic load and Palaeolithic diet) enrolling 5360 T2D patients were included. The vegetarian diet most effectively reduced LDL levels [MD (95% CI): − 0.33 (− 0.55, − 0.12) mmol/L; compared to the control diet]. The Mediterranean diet beneficially raised HDL [MD (95% CI): 0.09 (0.04, 0.15) mmol/L] and decreased TG levels [MD (95% CI): − 0.41 (− 0.72, − 0.10) mmol/L] compared to the control diet. The Mediterranean diet was the most effective dietary approach to manage diabetic dyslipidaemia altogether (SUCRA: 79%). The overall findings are mainly limited by low credibility of evidence.

Keywords

Type 2 diabetes Diet Blood lipids Systematic review Network meta-analysis 

Notes

Acknowledgements

We thank Pamela Dyson, Ph.D. RD and Robyn Larsen, Ph.D. for sending additional data for the corresponding meta-analysis.

Author’s contribution

LS, SS contributed to the conception and design of the systematic review and meta-analysis. LS, MN, GH were involved in the acquisition and analysis of the data. LS, SS, MN interpreted the results. LS, SS, MN drafted this manuscript. All authors provided critical revisions of the protocol and approved submission of the final manuscript.

Funding

The German Diabetes Center (DDZ) is funded by the German Federal Ministry of Health and the Ministry of Innovation, Science, Research and Technology of the State North Rhine-Westphalia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10654_2019_534_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1176 kb)

References

  1. 1.
    International Diabetes Federation. IDF Diabetes Atlas, 8th Edition2017 2017.Google Scholar
  2. 2.
    Jacobs E, Hoyer A, Brinks R, Icks A, Kuss O, Rathmann W. Healthcare costs of type 2 diabetes in Germany. Diabet Med. 2017;34(6):855–61.  https://doi.org/10.1111/dme.13336.CrossRefPubMedGoogle Scholar
  3. 3.
    WHO. Global report on diabetes. Geneva: World Health Organization 2016.Google Scholar
  4. 4.
    Jaiswal M, Schinske A, Pop-Busui R. Lipids and lipid management in diabetes. Best Pract Res Clin Endocrinol Metab. 2014;28(3):325–38.  https://doi.org/10.1016/j.beem.2013.12.001.CrossRefPubMedGoogle Scholar
  5. 5.
    Chahil TJ, Ginsberg HN. Diabetic dyslipidemia. Endocrinol Metab Clin North Am. 2006;35(3):491–510.  https://doi.org/10.1016/j.ecl.2006.06.002 vii–viii.CrossRefPubMedGoogle Scholar
  6. 6.
    Erion DM, Park HJ, Lee HY. The role of lipids in the pathogenesis and treatment of type 2 diabetes and associated co-morbidities. BMB Rep. 2016;49(3):139–48.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bardini G, Rotella CM, Giannini S. Dyslipidemia and diabetes: reciprocal impact of impaired lipid metabolism and beta-cell dysfunction on micro- and macrovascular complications. Rev Diabet Stud. 2012;9(2–3):82–93.  https://doi.org/10.1900/RDS.2012.9.82.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Wang Y, Lammi-Keefe CJ, Hou L, Hu G. Impact of low-density lipoprotein cholesterol on cardiovascular outcomes in people with type 2 diabetes: a meta-analysis of prospective cohort studies. Diabetes Res Clin Pract. 2013;102(1):65–75.  https://doi.org/10.1016/j.diabres.2013.07.009.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Vazquez-Benitez G, Desai JR, Xu S, Goodrich GK, Schroeder EB, Nichols GA, et al. Preventable major cardiovascular events associated with uncontrolled glucose, blood pressure, and lipids and active smoking in adults with diabetes with and without cardiovascular disease: a contemporary analysis. Diabetes Care. 2015;38(5):905–12.  https://doi.org/10.2337/dc14-1877.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Toth PP, Simko RJ, Palli SR, Koselleck D, Quimbo RA, Cziraky MJ. The impact of serum lipids on risk for microangiopathy in patients with type 2 diabetes mellitus. Cardiovasc Diabetol. 2012;11:109.  https://doi.org/10.1186/1475-2840-11-109.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Russo GT, De Cosmo S, Viazzi F, Pacilli A, Ceriello A, Genovese S, et al. Plasma triglycerides and HDL-C levels predict the development of diabetic kidney disease in subjects with type 2 diabetes: the AMD annals initiative. Diabetes Care. 2016;39(12):2278–87.  https://doi.org/10.2337/dc16-1246.CrossRefPubMedGoogle Scholar
  12. 12.
    Zoppini G, Targher G, Chonchol M, Perrone F, Lippi G, Muggeo M. Higher HDL cholesterol levels are associated with a lower incidence of chronic kidney disease in patients with type 2 diabetes. Nutr Metab Cardiovasc Dis. 2009;19(8):580–6.  https://doi.org/10.1016/j.numecd.2008.11.003.CrossRefPubMedGoogle Scholar
  13. 13.
    Evert AB, Boucher JL, Cypress M, Dunbar SA, Franz MJ, Mayer-Davis EJ, et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care. 2014;37(Suppl 1):S120–43.  https://doi.org/10.2337/dc14-S120.CrossRefPubMedGoogle Scholar
  14. 14.
    Dyson PA, Twenefour D, Breen C, Duncan A, Elvin E, Goff L, et al. Diabetes UK evidence-based nutrition guidelines for the prevention and management of diabetes. Diabet Med. 2018;35(5):541–7.  https://doi.org/10.1111/dme.13603.CrossRefPubMedGoogle Scholar
  15. 15.
    American Diabetes A. 5. Lifestyle management: standards of medical care in diabetes—2019. Diabetes Care. 2019;42(Suppl 1):S46–60.  https://doi.org/10.2337/dc19-s005.CrossRefGoogle Scholar
  16. 16.
    Ajala O, English P, Pinkney J. Systematic review and meta-analysis of different dietary approaches to the management of type 2 diabetes. Am J Clin Nutr. 2013;97(3):505–16.  https://doi.org/10.3945/ajcn.112.042457.CrossRefPubMedGoogle Scholar
  17. 17.
    Meng Y, Bai H, Wang S, Li Z, Wang Q, Chen L. Efficacy of low carbohydrate diet for type 2 diabetes mellitus management: a systematic review and meta-analysis of randomized controlled trials. Diabetes Res Clin Pract. 2017;131:124–31.  https://doi.org/10.1016/j.diabres.2017.07.006.CrossRefPubMedGoogle Scholar
  18. 18.
    Schwingshackl L, Hoffmann G. Comparison of the long-term effects of high-fat v. low-fat diet consumption on cardiometabolic risk factors in subjects with abnormal glucose metabolism: a systematic review and meta-analysis. Br J Nutr. 2014;111(12):2047–58.  https://doi.org/10.1017/s0007114514000464.CrossRefPubMedGoogle Scholar
  19. 19.
    Huo R, Du T, Xu Y, Xu W, Chen X, Sun K, et al. Effects of mediterranean-style diet on glycemic control, weight loss and cardiovascular risk factors among type 2 diabetes individuals: a meta-analysis. Eur J Clin Nutr. 2015;69(11):1200–8.  https://doi.org/10.1038/ejcn.2014.243.CrossRefPubMedGoogle Scholar
  20. 20.
    Viguiliouk E, Kendall CW, Kahleova H, Rahelic D, Salas-Salvado J, Choo VL, et al. Effect of vegetarian dietary patterns on cardiometabolic risk factors in diabetes: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr. 2018.  https://doi.org/10.1016/j.clnu.2018.05.032.CrossRefPubMedGoogle Scholar
  21. 21.
    Ludwig DS, Willett WC, Volek JS, Neuhouser ML. Dietary fat: From foe to friend? Science. 2018;362(6416):764–70.  https://doi.org/10.1126/science.aau2096.CrossRefPubMedGoogle Scholar
  22. 22.
    Schwingshackl L, Buyken A, Chaimani A. Network meta-analysis reaches nutrition research. Eur J Nutr. 2018.  https://doi.org/10.1007/s00394-018-1849-0.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Schwingshackl L, Schwarzer G, Rucker G, Meerpohl JJ. Perspective: network meta-analysis reaches nutrition research: current status, scientific concepts, and future directions. Adv Nutr. 2019.  https://doi.org/10.1093/advances/nmz036.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Pan B, Wu Y, Yang Q, Ge L, Gao C, Xun Y, et al. The impact of major dietary patterns on glycemic control, cardiovascular risk factors, and weight loss in patients with type 2 diabetes: a network meta-analysis. J Evid Based Med. 2018.  https://doi.org/10.1111/jebm.12312.CrossRefPubMedGoogle Scholar
  25. 25.
    Schwingshackl L, Chaimani A, Hoffmann G, Schwedhelm C, Boeing H. A network meta-analysis on the comparative efficacy of different dietary approaches on glycaemic control in patients with type 2 diabetes mellitus. Eur J Epidemiol. 2018;33(2):157–70.  https://doi.org/10.1007/s10654-017-0352-x.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Schwingshackl L, Chaimani A, Hoffmann G, Schwedhelm C, Boeing H. Impact of different dietary approaches on glycemic control and cardiovascular risk factors in patients with type 2 diabetes: a protocol for a systematic review and network meta-analysis. Syst Rev. 2017;6(1):57.  https://doi.org/10.1186/s13643-017-0455-1.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Hutton B, Salanti G, Caldwell DM, Chaimani A, Schmid CH, Cameron C, et al. The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med. 2015;162(11):777–84.  https://doi.org/10.7326/M14-2385.CrossRefPubMedGoogle Scholar
  28. 28.
    Chaimani A, Caldwell DM, Li T, Higgins JPT, Salanti G. Additional considerations are required when preparing a protocol for a systematic review with multiple interventions. J Clin Epidemiol. 2017;83:65–74.  https://doi.org/10.1016/j.jclinepi.2016.11.015.CrossRefPubMedGoogle Scholar
  29. 29.
    Schwingshackl L, Hoffmann G. Comparison of effects of long-term low-fat versus high-fat diets on blood lipid levels in overweight or obese patients: a systematic review and meta-analysis. J Acad Nutr Diet. 2013;113(12):1640–61.  https://doi.org/10.1016/j.jand.2013.07.010.CrossRefPubMedGoogle Scholar
  30. 30.
    Schwingshackl L, Hoffmann G. Long-term effects of low-fat diets either low or high in protein on cardiovascular and metabolic risk factors: a systematic review and meta-analysis. Nutr J. 2013;12:48.  https://doi.org/10.1186/1475-2891-12-48.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Schwingshackl L, Hoffmann G. Long-term effects of low glycemic index/load versus high glycemic index/load diets on parameters of obesity and obesity-associated risks: a systematic review and meta-analysis. Nutr Metab Cardiovasc Dis. 2013;23(8):699–706.  https://doi.org/10.1016/j.numecd.2013.04.008.CrossRefPubMedGoogle Scholar
  32. 32.
    Haider LM, Schwingshackl L, Hoffmann G, Ekmekcioglu C. The effect of vegetarian diets on iron status in adults: a systematic review and meta-analysis. Crit Rev Food Sci Nutr. 2018;58(8):1359–74.  https://doi.org/10.1080/10408398.2016.1259210.CrossRefPubMedGoogle Scholar
  33. 33.
    Trichopoulou A, Costacou T, Bamia C, Trichopoulos D. Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med. 2003;348(26):2599–608.  https://doi.org/10.1056/NEJMoa025039.CrossRefGoogle Scholar
  34. 34.
    Jonsson T, Granfeldt Y, Ahren B, Branell UC, Palsson G, Hansson A, et al. Beneficial effects of a Paleolithic diet on cardiovascular risk factors in type 2 diabetes: a randomized cross-over pilot study. Cardiovasc Diabetol. 2009;8:35.  https://doi.org/10.1186/1475-2840-8-35.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Brehm BJ, Lattin BL, Summer SS, Boback JA, Gilchrist GM, Jandacek RJ, et al. One-year comparison of a high-monounsaturated fat diet with a high-carbohydrate diet in type 2 diabetes. Diabetes Care. 2009;32(2):215–20.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Heilbronn LK, Noakes M, Clifton PM. Effect of energy restriction, weight loss, and diet composition on plasma lipids and glucose in patients with type 2 diabetes. Diabetes Care. 1999;22(6):889–95.CrossRefPubMedGoogle Scholar
  37. 37.
    Krebs JD, Elley CR, Parry-Strong A, Lunt H, Drury PL, Bell DA, et al. The diabetes excess weight loss (DEWL) trial: a randomised controlled trial of high-protein versus high-carbohydrate diets over 2 years in type 2 diabetes. Diabetologia. 2012;55(4):905–14.CrossRefPubMedGoogle Scholar
  38. 38.
    Larsen RN, Mann NJ, Maclean E, Shaw JE. The effect of high-protein, low-carbohydrate diets in the treatment of type 2 diabetes: a 12 month randomised controlled trial. Diabetologia. 2011;54(4):731–40.CrossRefPubMedGoogle Scholar
  39. 39.
    Milne RM, Mann JI, Chisholm AW, Williams SM. Long-term comparison of three dietary prescriptions in the treatment of NIDDM. Diabetes Care. 1994;17(1):74–80.CrossRefPubMedGoogle Scholar
  40. 40.
    Shige H, Nestel P, Sviridov D, Noakes M, Clifton P. Effect of weight reduction on the distribution of apolipoprotein AI in high-density lipoprotein subfractions in obese non-insulin-dependent diabetic subjects. Metabolism. 2000;49(11):1453–9.CrossRefPubMedGoogle Scholar
  41. 41.
    Tay J, Luscombe-Marsh ND, Thompson CH, Noakes M, Buckley JD, Wittert GA, et al. Comparison of low- and high-carbohydrate diets for type 2 diabetes management: a randomized trial. Am J Clin Nutr. 2015;102(4):780–90.CrossRefPubMedGoogle Scholar
  42. 42.
    Watson N, Dyer K, Buckley J, Brinkworth G, Coates A, Parfitt G, et al. Effects of low-fat diets differing in protein and carbohydrate content on cardiometabolic risk factors during weight loss and weight maintenance in obese adults with type 2 diabetes. Nutrients. 2016;8(5):289.CrossRefPubMedCentralGoogle Scholar
  43. 43.
    Brinkworth GD, Noakes M, Parker B, Foster P, Clifton PM. Long-term effects of advice to consume a high-protein, low-fat diet, rather than a conventional weight-loss diet, in obese adults with type 2 diabetes: one-year follow-up of a randomised trial. Diabetologia. 2004;47(10):1677–86.CrossRefPubMedGoogle Scholar
  44. 44.
    Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, high-monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care. 2002;25(3):425–30.CrossRefPubMedGoogle Scholar
  45. 45.
    Ceriello A, Esposito K, La SL, Pujadas G, De NV, Testa R, et al. The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report. Cardiovasc Diabetol. 2014;13:140.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Daly ME, Paisey R, Paisey R, Millward BA, Eccles C, Williams K, et al. Short-term effects of severe dietary carbohydrate-restriction advice in type 2 diabetes—a randomized controlled trial. Diabet Med. 2006;23(1):15–20.CrossRefPubMedGoogle Scholar
  47. 47.
    Davis NJ, Tomuta N, Schechter C, Isasi CR, Segal-Isaacson CJ, Stein D, et al. Comparative study of the effects of a 1-year dietary intervention of a low-carbohydrate diet versus a low-fat diet on weight and glycemic control in type 2 diabetes. Diabetes Care. 2009;32(7):1147–52.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    de Bont AJ, Baker IA, St Leger AS, Sweetnam PM, Wragg KG, Stephens SM, et al. A randomised controlled trial of the effect of low fat diet advice on dietary response in insulin independent diabetic women. Diabetologia. 1981;21(6):529–33.CrossRefPubMedGoogle Scholar
  49. 49.
    Esposito K, Maiorino MI, Ciotola M, Di PC, Scognamiglio P, Gicchino M, et al. Effects of a Mediterranean-style diet on the need for antihyperglycemic drug therapy in patients with newly diagnosed type 2 diabetes: a randomized trial. Ann Intern Med. 2009;151(5):306–14.CrossRefPubMedGoogle Scholar
  50. 50.
    Fabricatore AN, Wadden TA, Ebbeling CB, Thomas JG, Stallings VA, Schwartz S, et al. Targeting dietary fat or glycemic load in the treatment of obesity and type 2 diabetes: a randomized controlled trial. Diabetes Res Clin Pract. 2011;92(1):37–45.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Guldbrand H, Dizdar B, Bunjaku B, Lindstrom T, Bachrach-Lindstrom M, Fredrikson M, et al. In type 2 diabetes, randomisation to advice to follow a low-carbohydrate diet transiently improves glycaemic control compared with advice to follow a low-fat diet producing a similar weight loss. Diabetologia. 2012;55(8):2118–27.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Li X, Cai X, Ma X, Jing L, Gu J, Bao L, et al. Short- and long-term effects of wholegrain oat intake on weight management and glucolipid metabolism in overweight type-2 diabetics: a randomized control trial. Nutrients. 2016;8(9):549.CrossRefPubMedCentralGoogle Scholar
  53. 53.
    Iqbal N, Vetter ML, Moore RH, Chittams JL, Dalton-Bakes CV, Dowd M, et al. Effects of a low-intensity intervention that prescribed a low-carbohydrate versus a low-fat diet in obese, diabetic participants. Obesity. 2010;18(9):1733–8.CrossRefPubMedGoogle Scholar
  54. 54.
    McLaughlin T, Carter S, Lamendola C, Abbasi F, Schaaf P, Basina M, et al. Clinical efficacy of two hypocaloric diets that vary in overweight patients with type 2 diabetes: comparison of moderate fat versus carbohydrate reductions. Diabetes Care. 2007;30(7):1877–9.CrossRefPubMedGoogle Scholar
  55. 55.
    Nicholson AS, Sklar M, Barnard ND, Gore S, Sullivan R, Browning S. Toward improved management of NIDDM: a randomized, controlled, pilot intervention using a lowfat, vegetarian diet. Prev Med. 1999;29(2):87–91.CrossRefPubMedGoogle Scholar
  56. 56.
    Rock CL, Flatt SW, Pakiz B, Taylor KS, Leone AF, Brelje K, et al. Weight loss, glycemic control, and cardiovascular disease risk factors in response to differential diet composition in a weight loss program in type 2 diabetes: a randomized controlled trial. Diabetes Care. 2014;37(6):1573–80.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Walker KZ, O’Dea K, Nicholson GC, Muir JG. Dietary composition, body weight, and NIDDM. Comparison of high-fiber, high-carbohydrate, and modified-fat diets. Diabetes Care. 1995;18(3):401–3.CrossRefPubMedGoogle Scholar
  58. 58.
    Kahleova H, Matoulek M, Malinska H, Oliyarnik O, Kazdova L, Neskudla T, et al. Vegetarian diet improves insulin resistance and oxidative stress markers more than conventional diet in subjects with type 2 diabetes. Diabet Med. 2011;28(5):549–59.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    American Diabetes A. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S13–27.  https://doi.org/10.2337/dc18-s002.CrossRefGoogle Scholar
  60. 60.
    Canadian Diabetes Association Clinical Practice Guidelines Expert C, Wharton S, Sharma AM, Lau DC. Weight management in diabetes. Can J Diabetes. 2013;37(Suppl 1):S82–6.  https://doi.org/10.1016/j.jcjd.2013.01.025.CrossRefGoogle Scholar
  61. 61.
    American Diabetes A. 7. Obesity management for the treatment of type 2 diabetes: standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S65–72.  https://doi.org/10.2337/dc18-s007.CrossRefGoogle Scholar
  62. 62.
    Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.  https://doi.org/10.1136/bmj.d5928.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Dyson PA, Beatty S, Matthews DR. A low-carbohydrate diet is more effective in reducing body weight than healthy eating in both diabetic and non-diabetic subjects. Diabet Med. 2007;24(12):1430–5.CrossRefPubMedGoogle Scholar
  64. 64.
    Higgins JPT, Green S. Cochrane handbook for systematic reviewsof interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. www.cochrane-handbook.org. Accessed 20 Aug 2016.
  65. 65.
    Chaimani A, Higgins JP, Mavridis D, Spyridonos P, Salanti G. Graphical tools for network meta-analysis in STATA. PLoS ONE. 2013;8(10):e76654.  https://doi.org/10.1371/journal.pone.0076654.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Jansen JP, Naci H. Is network meta-analysis as valid as standard pairwise meta-analysis? It all depends on the distribution of effect modifiers. BMC Med. 2013;11:159.  https://doi.org/10.1186/1741-7015-11-159.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Salanti G, Ades AE, Ioannidis JP. Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial. J Clin Epidemiol. 2011;64(2):163–71.  https://doi.org/10.1016/j.jclinepi.2010.03.016.CrossRefPubMedGoogle Scholar
  68. 68.
    Schwarzer G, Carpenter J, Ruecker G. Meta-analysis with R. 2015. http://meta-analysis-with-r.org. https://github.com/guido-s/netmeta. Accessed 20 May 2019.
  69. 69.
    Schwarzer G. netmeta: network meta-analysis using frequentist methods. 2019. https://github.com/guido-s/netmeta. Accessed 20 May 2019.
  70. 70.
    Salanti G, Del Giovane C, Chaimani A, Caldwell DM, Higgins JP. Evaluating the quality of evidence from a network meta-analysis. PLoS ONE. 2014;9(7):e99682.  https://doi.org/10.1371/journal.pone.0099682.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Bucher HC, Guyatt GH, Griffith LE, Walter SD. The results of direct and indirect treatment comparisons in meta-analysis of randomized controlled trials. J Clin Epidemiol. 1997;50(6):683–91.CrossRefPubMedGoogle Scholar
  72. 72.
    Dias S, Welton NJ, Caldwell DM, Ades AE. Checking consistency in mixed treatment comparison meta-analysis. Stat Med. 2010;29(7–8):932–44.  https://doi.org/10.1002/sim.3767.CrossRefGoogle Scholar
  73. 73.
    Higgins JP, Jackson D, Barrett JK, Lu G, Ades AE, White IR. Consistency and inconsistency in network meta-analysis: concepts and models for multi-arm studies. Res Synth Methods. 2012;3(2):98–110.  https://doi.org/10.1002/jrsm.1044.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Jackson D, Barrett JK, Rice S, White IR, Higgins JP. A design-by-treatment interaction model for network meta-analysis with random inconsistency effects. Stat Med. 2014;33(21):3639–54.  https://doi.org/10.1002/sim.6188.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Harbord RM, Higgins J. Meta-regression in Stata. Stata J. 2008;8(4):493–519.CrossRefGoogle Scholar
  76. 76.
    Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol. 2008;61(10):991–6.  https://doi.org/10.1016/j.jclinepi.2007.11.010.CrossRefPubMedGoogle Scholar
  77. 77.
    Andrews RC, Cooper AR, Montgomery AA, Norcross AJ, Peters TJ, Sharp DJ, et al. Diet or diet plus physical activity versus usual care in patients with newly diagnosed type 2 diabetes: the Early ACTID randomised controlled trial. Lancet. 2011;378(9786):129–39.  https://doi.org/10.1016/S0140-6736(11)60442-X.CrossRefPubMedGoogle Scholar
  78. 78.
    Barnard ND, Cohen J, Jenkins DJ, Turner-McGrievy G, Gloede L, Green A, et al. A low-fat vegan diet and a conventional diabetes diet in the treatment of type 2 diabetes: a randomized, controlled, 74-wk clinical trial. Am J Clin Nutr. 2009;89(5):1588S–96S.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Brand JC, Colagiuri S, Crossman S, Allen A, Roberts DC, Truswell AS. Low-glycemic index foods improve long-term glycemic control in NIDDM. Diabetes Care. 1991;14(2):95–101.CrossRefPubMedGoogle Scholar
  80. 80.
    Brunerova L, Smejkalova V, Potockova J, Andel M. A comparison of the influence of a high-fat diet enriched in monounsaturated fatty acids and conventional diet on weight loss and metabolic parameters in obese non-diabetic and type 2 diabetic patients. Diabet Med. 2007;24(5):533–40.CrossRefPubMedGoogle Scholar
  81. 81.
    Coppell KJ, Kataoka M, Williams SM, Chisholm AW, Vorgers SM, Mann JI. Nutritional intervention in patients with type 2 diabetes who are hyperglycaemic despite optimised drug treatment–Lifestyle Over and Above Drugs in Diabetes (LOADD) study: randomised controlled trial. BMJ. 2010;341:c3337.  https://doi.org/10.1136/bmj.c3337.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Elhayany A, Lustman A, Abel R, Attal-Singer J, Vinker S. A low carbohydrate Mediterranean diet improves cardiovascular risk factors and diabetes control among overweight patients with type 2 diabetes mellitus: a 1-year prospective randomized intervention study. Diabetes Obes Metab. 2010;12(3):204–9.CrossRefPubMedGoogle Scholar
  83. 83.
    Hockaday TD, Hockaday JM, Mann JI, Turner RC. Prospective comparison of modified fat-high-carbohydrate with standard low-carbohydrate dietary advice in the treatment of diabetes: one year follow-up study. Br J Nutr. 1978;39(2):357–62.CrossRefPubMedGoogle Scholar
  84. 84.
    Huang MC, Hsu CC, Wang HS, Shin SJ. Prospective randomized controlled trial to evaluate effectiveness of registered dietitian-led diabetes management on glycemic and diet control in a primary care setting in Taiwan. Diabetes Care. 2010;33(2):233–9.CrossRefPubMedGoogle Scholar
  85. 85.
    Itsiopoulos C, Brazionis L, Kaimakamis M, Cameron M, Best JD, O’Dea K, et al. Can the Mediterranean diet lower HbA1c in type 2 diabetes? Results from a randomized cross-over study. Nutr Metab Cardiovasc Dis. 2011;21(9):740–7.CrossRefPubMedGoogle Scholar
  86. 86.
    Jenkins DJ, Kendall CW, McKeown-Eyssen G, Josse RG, Silverberg J, Booth GL, et al. Effect of a low-glycemic index or a high-cereal fiber diet on type 2 diabetes: a randomized trial. JAMA. 2008;300(23):2742–53.CrossRefPubMedGoogle Scholar
  87. 87.
    Jenkins DJ, Kendall CW, Augustin LS, Mitchell S, Sahye-Pudaruth S, Blanco MS, et al. Effect of legumes as part of a low glycemic index diet on glycemic control and cardiovascular risk factors in type 2 diabetes mellitus: a randomized controlled trial. Arch Intern Med. 2012;172(21):1653–60.CrossRefPubMedGoogle Scholar
  88. 88.
    Jenkins DJ, Kendall CW, Vuksan V, Faulkner D, Augustin LS, Mitchell S, et al. Effect of lowering the glycemic load with canola oil on glycemic control and cardiovascular risk factors: a randomized controlled trial. Diabetes Care. 2014;37(7):1806–14.CrossRefPubMedGoogle Scholar
  89. 89.
    Lee YM, Kim SA, Lee IK, Kim JG, Park KG, Jeong JY, et al. Effect of a brown rice based vegan diet and conventional diabetic diet on glycemic control of patients with type 2 diabetes: a 12-week randomized clinical trial. PLoS ONE. 2016;11(6):e0155918.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Liu H, Zhang M, Wu X, Wang C, Li Z. Effectiveness of a public dietitian-led diabetes nutrition intervention on glycemic control in a community setting in China. Asia Pac J Clin Nutr. 2015;24(3):525–32.PubMedGoogle Scholar
  91. 91.
    Luger M, Holstein B, Schindler K, Kruschitz R, Ludvik B. Feasibility and efficacy of an isocaloric high-protein versus standard diet on insulin requirement, body weight and metabolic parameters in patients with type 2 diabetes on insulin therapy. Exp Clin Endocrinol Diabetes. 2013;121(5):286–94.CrossRefPubMedGoogle Scholar
  92. 92.
    Ma Y, Olendzki BC, Merriam PA, Chiriboga DE, Culver AL, Li W, et al. A randomized clinical trial comparing low-glycemic index versus ADA dietary education among individuals with type 2 diabetes. Nutrition. 2008;24(1):45–56.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Mishra S, Xu J, Agarwal U, Gonzales J, Levin S, Barnard ND. A multicenter randomized controlled trial of a plant-based nutrition program to reduce body weight and cardiovascular risk in the corporate setting: the GEICO study. Eur J Clin Nutr. 2013;67(7):718–24.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Pedersen E, Jesudason DR, Clifton PM. High protein weight loss diets in obese subjects with type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis. 2014;24(5):554–62.CrossRefPubMedGoogle Scholar
  95. 95.
    Saslow LR, Kim S, Daubenmier JJ, Moskowitz JT, Phinney SD, Goldman V, et al. A randomized pilot trial of a moderate carbohydrate diet compared to a very low carbohydrate diet in overweight or obese individuals with type 2 diabetes mellitus or prediabetes. PLoS ONE. 2014;9(4):e91027.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Sato J, Kanazawa A, Makita S, Hatae C, Komiya K, Shimizu T, et al. A randomized controlled trial of 130 g/day low-carbohydrate diet in type 2 diabetes with poor glycemic control. Clin Nutr. 2017;36(4):992–1000.CrossRefPubMedGoogle Scholar
  97. 97.
    Uusitupa M, Laitinen J, Siitonen O, Vanninen E, Pyorala K. The maintenance of improved metabolic control after intensified diet therapy in recent type 2 diabetes. Diabetes Res Clin Pract. 1993;19(3):227–38.CrossRefPubMedGoogle Scholar
  98. 98.
    Westman EC, Yancy WS Jr, Mavropoulos JC, Marquart M, McDuffie JR. The effect of a low-carbohydrate, ketogenic diet versus a low-glycemic index diet on glycemic control in type 2 diabetes mellitus. Nutr Metab (Lond). 2008;5:36.CrossRefGoogle Scholar
  99. 99.
    Wolever TM, Gibbs AL, Mehling C, Chiasson JL, Connelly PW, Josse RG, et al. The Canadian trial of carbohydrates in diabetes (CCD), a 1-y controlled trial of low-glycemic-index dietary carbohydrate in type 2 diabetes: no effect on glycated hemoglobin but reduction in C-reactive protein. Am J Clin Nutr. 2008;87(1):114–25.CrossRefPubMedGoogle Scholar
  100. 100.
    Wycherley TP, Noakes M, Clifton PM, Cleanthous X, Keogh JB, Brinkworth GD. A high-protein diet with resistance exercise training improves weight loss and body composition in overweight and obese patients with type 2 diabetes. Diabetes Care. 2010;33(5):969–76.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Yamada Y, Uchida J, Izumi H, Tsukamoto Y, Inoue G, Watanabe Y, et al. A non-calorie-restricted low-carbohydrate diet is effective as an alternative therapy for patients with type 2 diabetes. Intern Med. 2014;53(1):13–9.CrossRefPubMedGoogle Scholar
  102. 102.
    Yusof BN, Talib RA, Kamaruddin NA, Karim NA, Chinna K, Gilbertson H. A low-GI diet is associated with a short-term improvement of glycaemic control in Asian patients with type 2 diabetes. Diabetes Obes Metab. 2009;11(4):387–96.CrossRefPubMedGoogle Scholar
  103. 103.
    Yokoyama Y, Levin SM, Barnard ND. Association between plant-based diets and plasma lipids: a systematic review and meta-analysis. Nutr Rev. 2017;75(9):683–98.  https://doi.org/10.1093/nutrit/nux030.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Wang F, Zheng J, Yang B, Jiang J, Fu Y, Li D. Effects of vegetarian diets on blood lipids: a systematic review and meta-analysis of randomized controlled trials. J Am Heart Assoc. 2015;4(10):e002408.  https://doi.org/10.1161/JAHA.115.002408.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Archundia Herrera MC, Subhan FB, Chan CB. Dietary patterns and cardiovascular disease risk in people with type 2 diabetes. Curr Obes Rep. 2017;6(4):405–13.  https://doi.org/10.1007/s13679-017-0284-5.CrossRefPubMedGoogle Scholar
  106. 106.
    Goff LM, Cowland DE, Hooper L, Frost GS. Low glycaemic index diets and blood lipids: a systematic review and meta-analysis of randomised controlled trials. Nutr Metab Cardiovasc Dis. 2013;23(1):1–10.  https://doi.org/10.1016/j.numecd.2012.06.002.CrossRefPubMedGoogle Scholar
  107. 107.
    Fleming P, Godwin M. Low-glycaemic index diets in the management of blood lipids: a systematic review and meta-analysis. Fam Pract. 2013;30(5):485–91.  https://doi.org/10.1093/fampra/cmt029.CrossRefPubMedGoogle Scholar
  108. 108.
    Garcia M, Bihuniak JD, Shook J, Kenny A, Kerstetter J, Huedo-Medina TB. The Effect of the traditional mediterranean-style diet on metabolic risk factors: a meta-analysis. Nutrients. 2016;8(3):168.  https://doi.org/10.3390/nu8030168.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Kodama S, Saito K, Tanaka S, Maki M, Yachi Y, Sato M, et al. Influence of fat and carbohydrate proportions on the metabolic profile in patients with type 2 diabetes: a meta-analysis. Diabetes Care. 2009;32(5):959–65.  https://doi.org/10.2337/dc08-1716.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Mansoor N, Vinknes KJ, Veierod MB, Retterstol K. Effects of low-carbohydrate diets v. low-fat diets on body weight and cardiovascular risk factors: a meta-analysis of randomised controlled trials. Br J Nutr. 2016;115(3):466–79.  https://doi.org/10.1017/s0007114515004699.CrossRefPubMedGoogle Scholar
  111. 111.
    Bonaccio M, Di Castelnuovo A, Costanzo S, Persichillo M, De Curtis A, Donati MB, et al. Adherence to the traditional Mediterranean diet and mortality in subjects with diabetes. Prospective results from the MOLI-SANI study. Eur J Prev Cardiol. 2016;23(4):400–7.  https://doi.org/10.1177/2047487315569409.CrossRefPubMedGoogle Scholar
  112. 112.
    Grosso G, Marventano S, Yang J, Micek A, Pajak A, Scalfi L, et al. A comprehensive meta-analysis on evidence of Mediterranean diet and cardiovascular disease: are individual components equal? Crit Rev Food Sci Nutr. 2017;57(15):3218–32.  https://doi.org/10.1080/10408398.2015.1107021.CrossRefPubMedGoogle Scholar
  113. 113.
    Nordmann AJ, Nordmann A, Briel M, Keller U, Yancy WS Jr, Brehm BJ, et al. Effects of low-carbohydrate versus low-fat diets on weight loss and cardiovascular risk factors: a meta-analysis of randomized controlled trials. Arch Intern Med. 2006;166(3):285–93.  https://doi.org/10.1001/archinte.166.3.285.CrossRefPubMedGoogle Scholar
  114. 114.
    Goulet J, Lamarche B, Nadeau G, Lemieux S. Effect of a nutritional intervention promoting the Mediterranean food pattern on plasma lipids, lipoproteins and body weight in healthy French–Canadian women. Atherosclerosis. 2003;170(1):115–24.CrossRefPubMedGoogle Scholar
  115. 115.
    Barnard ND, Scialli AR, Bertron P, Hurlock D, Edmonds K, Talev L. Effectiveness of a low-fat vegetarian diet in altering serum lipids in healthy premenopausal women. Am J Cardiol. 2000;85(8):969–72.CrossRefPubMedGoogle Scholar
  116. 116.
    Ling WH, Laitinen M, Hänninen O. Shifting from conventional diet to an uncooked vegan diet reversibly alters serum lipid and apolipoprotein levels. Nutr Res. 1992;12:1431–40.CrossRefGoogle Scholar
  117. 117.
    Kastorini CM, Milionis HJ, Esposito K, Giugliano D, Goudevenos JA, Panagiotakos DB. The effect of Mediterranean diet on metabolic syndrome and its components: a meta-analysis of 50 studies and 534,906 individuals. J Am Coll Cardiol. 2011;57(11):1299–313.  https://doi.org/10.1016/j.jacc.2010.09.073.CrossRefPubMedGoogle Scholar
  118. 118.
    Busetto L, Marangon M, De Stefano F. High-protein low-carbohydrate diets: What is the rationale? Diabetes Metab Res Rev. 2011;27(3):230–2.  https://doi.org/10.1002/dmrr.1171.CrossRefPubMedGoogle Scholar
  119. 119.
    Ebbeling CB, Feldman HA, Klein GL, Wong JMW, Bielak L, Steltz SK, et al. Effects of a low carbohydrate diet on energy expenditure during weight loss maintenance: randomized trial. BMJ. 2018;363:k4583.  https://doi.org/10.1136/bmj.k4583.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Jonsson T, Granfeldt Y, Lindeberg S, Hallberg AC. Subjective satiety and other experiences of a Paleolithic diet compared to a diabetes diet in patients with type 2 diabetes. Nutr J. 2013;12:105.  https://doi.org/10.1186/1475-2891-12-105.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Huntriss R, Campbell M, Bedwell C. The interpretation and effect of a low-carbohydrate diet in the management of type 2 diabetes: a systematic review and meta-analysis of randomised controlled trials. Eur J Clin Nutr. 2018;72(3):311–25.  https://doi.org/10.1038/s41430-017-0019-4.CrossRefPubMedGoogle Scholar
  122. 122.
    Ros E. Dietary cis-monounsaturated fatty acids and metabolic control in type 2 diabetes. Am J Clin Nutr. 2003;78(3 Suppl):617S–25S.  https://doi.org/10.1093/ajcn/78.3.617S.CrossRefPubMedGoogle Scholar
  123. 123.
    Qian F, Korat AA, Malik V, Hu FB. Metabolic effects of monounsaturated fatty acid-enriched diets compared with carbohydrate or polyunsaturated fatty acid-enriched diets in patients with type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Diabetes Care. 2016;39(8):1448–57.  https://doi.org/10.2337/dc16-0513.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Mensink RP, Zock PL, Kester AD, Katan MB. Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr. 2003;77(5):1146–55.  https://doi.org/10.1093/ajcn/77.5.1146.CrossRefPubMedGoogle Scholar
  125. 125.
    O’Mahoney LL, Matu J, Price OJ, Birch KM, Ajjan RA, Farrar D, et al. Omega-3 polyunsaturated fatty acids favourably modulate cardiometabolic biomarkers in type 2 diabetes: a meta-analysis and meta-regression of randomized controlled trials. Cardiovasc Diabetol. 2018;17(1):98.  https://doi.org/10.1186/s12933-018-0740-x.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Chehade JM, Gladysz M, Mooradian AD. Dyslipidemia in type 2 diabetes: prevalence, pathophysiology, and management. Drugs. 2013;73(4):327–39.  https://doi.org/10.1007/s40265-013-0023-5.CrossRefPubMedGoogle Scholar
  127. 127.
    Femlak M, Gluba-Brzozka A, Cialkowska-Rysz A, Rysz J. The role and function of HDL in patients with diabetes mellitus and the related cardiovascular risk. Lipids Health Dis. 2017;16(1):207.  https://doi.org/10.1186/s12944-017-0594-3.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Holmes MV, Asselbergs FW, Palmer TM, Drenos F, Lanktree MB, Nelson CP, et al. Mendelian randomization of blood lipids for coronary heart disease. Eur Heart J. 2015;36(9):539–50.  https://doi.org/10.1093/eurheartj/eht571.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Manuela Neuenschwander
    • 1
  • Georg Hoffmann
    • 2
  • Lukas Schwingshackl
    • 3
    Email author
  • Sabrina Schlesinger
    • 1
  1. 1.Institute for Biometrics and Epidemiology, German Diabetes CenterLeibniz Center for Diabetes Research at Heinrich Heine University DüsseldorfDüsseldorfGermany
  2. 2.Department of Nutritional SciencesUniversity of ViennaViennaAustria
  3. 3.Institute for Evidence in Medicine, Faculty of Medicine and Medical CenterUniversity of FreiburgFreiburgGermany

Personalised recommendations