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Nutrition and Periodontal Health in the Patients with Diabetes Mellitus: a Review from the Viewpoint of Endothelial Function

  • Oral Disease and Nutrition (F Nishimura, Section Editor)
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A Correction to this article was published on 08 December 2021

This article has been updated

Abstract

Purpose of Review

This review aims to summarize the literature on periodontal disease and nutrition, focusing on endothelial dysfunction in diabetic patients, and their impact on oral health.

Recent Findings

Environmental factors, including smoking, obesity, and diabetes are well-known risk factors for the onset and progression of the periodontal disease. Indeed, dietary factors show an association with periodontal health through local and systemic environments. In addition, systemic factors, such as insulin resistance and diabetes, may have an important role in the periodontal health. Although molecular mechanisms underlying this are not fully understood, endothelial dysfunction mainly by hyperglycemia and/or chronic inflammation may explain the association between periodontal status and nutrition. In this paper, we reviewed recent progress in this field and propose the potential impact of nutritional intervention in the oral health from the viewpoint of endothelial function.

Summary

It is expected to become increasingly important to understand the pathology of diabetes-related periodontal disease and consider nutritional approaches with vascular dysfunction in mind for its prevention and treatment. Further accumulation of evidence is anticipated for the future.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Kruger-Genge A, Blocki A, Franke RP, Jung F. Vascular endothelial cell biology: an update. Int J Mol Sci. 2019 20.

  2. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993;329:2002–12.

    CAS  PubMed  Google Scholar 

  3. de Jager J, Dekker JM, Kooy A, Kostense PJ, Nijpels G, Heine RJ, et al. Endothelial dysfunction and low-grade inflammation explain much of the excess cardiovascular mortality in individuals with type 2 diabetes: the Hoorn Study. Arterioscler Thromb Vasc Biol. 2006;26:1086–93.

    PubMed  Google Scholar 

  4. Gui F, You Z, Fu S, Wu H, Zhang Y. Endothelial dysfunction in diabetic retinopathy. Front Endocrinol (Lausanne). 2020;11:591.

    Google Scholar 

  5. Nakagawa T, Tanabe K, Croker BP, Johnson RJ, Grant MB, Kosugi T, et al. Endothelial dysfunction as a potential contributor in diabetic nephropathy. Nat Rev Nephrol. 2011;7:36–44.

    PubMed  Google Scholar 

  6. Xu J, Zou MH. Molecular insights and therapeutic targets for diabetic endothelial dysfunction. Circulation. 2009;120:1266–86.

    PubMed  PubMed Central  Google Scholar 

  7. Zhang H, Dellsperger KC, Zhang C. The link between metabolic abnormalities and endothelial dysfunction in type 2 diabetes: an update. Basic Res Cardiol. 2012;107:237.

    PubMed  Google Scholar 

  8. Gonzalez MA, Selwyn AP. Endothelial function, inflammation, and prognosis in cardiovascular disease. Am J Med. 2003;115(Suppl 8A):99S-106S.

    CAS  PubMed  Google Scholar 

  9. Kharbanda RK, Walton B, Allen M, Klein N, Hingorani AD, MacAllister RJ, et al. Prevention of inflammation-induced endothelial dysfunction: a novel vasculo-protective action of aspirin. Circulation. 2002;105:2600–4.

    CAS  PubMed  Google Scholar 

  10. Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, et al. Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes. 2008;57:1349–54.

    CAS  PubMed  Google Scholar 

  11. Mah E, Bruno RS. Postprandial hyperglycemia on vascular endothelial function: mechanisms and consequences. Nutr Res. 2012;32:727–40.

    CAS  PubMed  Google Scholar 

  12. Torimoto K, Okada Y, Mori H, Tanaka Y. Relationship between fluctuations in glucose levels measured by continuous glucose monitoring and vascular endothelial dysfunction in type 2 diabetes mellitus. Cardiovasc Diabetol. 2013;12:1.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404:787–90.

    CAS  PubMed  Google Scholar 

  14. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54:1615–25.

    CAS  PubMed  Google Scholar 

  15. Meza CA, La Favor JD, Kim DH, Hickner RC. Endothelial dysfunction: is there a hyperglycemia-induced imbalance of NOX and NOS? Int J Mol Sci. 2019 20.

  16. Sena CM, Nunes E, Louro T, Proenca T, Fernandes R, Boarder MR, et al. Effects of alpha-lipoic acid on endothelial function in aged diabetic and high-fat fed rats. Br J Pharmacol. 2008;153:894–906.

    CAS  PubMed  Google Scholar 

  17. Suganya N, Dornadula S, Chatterjee S, Mohanram RK. Quercetin improves endothelial function in diabetic rats through inhibition of endoplasmic reticulum stress-mediated oxidative stress. Eur J Pharmacol. 2018;819:80–8.

    CAS  PubMed  Google Scholar 

  18. Pereira A, Fernandes R, Crisostomo J, Seica RM, Sena CM. The sulforaphane and pyridoxamine supplementation normalize endothelial dysfunction associated with type 2 diabetes. Sci Rep. 2017;7:14357.

    PubMed  PubMed Central  Google Scholar 

  19. Ungvari Z, Bagi Z, Feher A, Recchia FA, Sonntag WE, Pearson K, et al. Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2. Am J Physiol Heart Circ Physiol. 2010;299:H18-24.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Shinozaki K, Nishio Y, Okamura T, Yoshida Y, Maegawa H, Kojima H, et al. Oral administration of tetrahydrobiopterin prevents endothelial dysfunction and vascular oxidative stress in the aortas of insulin-resistant rats. Circ Res. 2000;87:566–73.

    CAS  PubMed  Google Scholar 

  21. Loe H. Periodontal disease The sixth complication of diabetes mellitus. Diabetes Care. 1993;16:329–34.

    CAS  PubMed  Google Scholar 

  22. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol. 1991;62:123–31.

    CAS  PubMed  Google Scholar 

  23. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad MF, Genco RJ, et al. Periodontal disease and NIDDM in Pima Indians. Diabetes Care. 1990;13:836–40.

    CAS  PubMed  Google Scholar 

  24. Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ. Periodontal status of diabetics compared with nondiabetics: a meta-analysis. J Diabetes Complications. 2006;20:59–68.

    PubMed  Google Scholar 

  25. Tsai C, Hayes C, Taylor GW. Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community Dent Oral Epidemiol. 2002;30:182–92.

    PubMed  Google Scholar 

  26. Harada K, Morino K, Ishikawa M, et al. Glycemic control and number of natural teeth: analysis of cross-sectional Japanese employment-based dental insurance claims and medical check-up data. Diabetol Int. 2021. https://doi.org/10.1007/s13340-021-00533-2.

    Article  Google Scholar 

  27. Adachi K, Miyajima SI, Nakamura N, Miyabe M, Kobayashi Y, Nishikawa T, et al. Role of poly(ADP-ribose) polymerase activation in the pathogenesis of periodontitis in diabetes. J Clin Periodontol. 2017;44:971–80.

    CAS  PubMed  Google Scholar 

  28. Nishimura F, Iwamoto Y, Mineshiba J, Shimizu A, Soga Y, Murayama Y. Periodontal disease and diabetes mellitus: the role of tumor necrosis factor-alpha in a 2-way relationship. J Periodontol. 2003;74:97–102.

    PubMed  Google Scholar 

  29. Lalla E, Lamster IB, Feit M, Huang L, Spessot A, Qu W, et al. Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest. 2000;105:1117–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu R, Bal HS, Desta T, Krothapalli N, Alyassi M, Luan Q, et al. Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res. 2006;85:510–4.

    CAS  PubMed  Google Scholar 

  31. Santos VR, Lima JA, Goncalves TE, Bastos MF, Figueiredo LC, Shibli JA, et al. Receptor activator of nuclear factor-kappa B ligand/osteoprotegerin ratio in sites of chronic periodontitis of subjects with poorly and well-controlled type 2 diabetes. J Periodontol. 2010;81:1455–65.

    CAS  PubMed  Google Scholar 

  32. Xiao E, Mattos M, Vieira GHA, Chen S, Correa JD, Wu Y, et al. Diabetes enhances IL-17 expression and alters the oral microbiome to increase its pathogenicity. Cell Host Microbe. 2017;22:120-8 e4.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Bastos AS, Graves DT, Loureiro AP, Rossa Junior C, Abdalla DS, Faulin Tdo E, et al. Lipid peroxidation is associated with the severity of periodontal disease and local inflammatory markers in patients with type 2 diabetes. J Clin Endocrinol Metab. 2012;97:E1353–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Monea A, Mezei T, Popsor S, Monea M. Oxidative stress: a link between diabetes mellitus and periodontal disease. Int J Endocrinol. 2014;2014:917631.

    PubMed  PubMed Central  Google Scholar 

  35. • Schenkein HA, Papapanou PN, Genco R, Sanz M. Mechanisms underlying the association between periodontitis and atherosclerotic disease. Periodontol. 2000;2020(83):90–106. (This is a similar review paper providing summary between periodontal and atherosclerotic diseases in general.)

    Google Scholar 

  36. Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA. Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol. 2003;23:1245–9.

    CAS  PubMed  Google Scholar 

  37. Higashi Y, Goto C, Jitsuiki D, Umemura T, Nishioka K, Hidaka T, et al. Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients. Hypertension. 2008;51:446–53.

    CAS  PubMed  Google Scholar 

  38. Punj A, Shenoy SB, Subramanyam K. Comparison of endothelial function in healthy patients and patients with chronic periodontitis and myocardial infarction. J Periodontol. 2017;88:1234–43.

    CAS  PubMed  Google Scholar 

  39. • Masi S, Orlandi M, Parkar M, Bhowruth D, Kingston I, O’Rourke C, et al. Mitochondrial oxidative stress, endothelial function and metabolic control in patients with type II diabetes and periodontitis: a randomised controlled clinical trial. Int J Cardiol. 2018;271:263–8. (This clinical trial examined the relationship between mitochondrial oxidative stress and endothelial function.)

    PubMed  PubMed Central  Google Scholar 

  40. Sugiyama S, Takahashi SS, Tokutomi FA, Yoshida A, Kobayashi K, Yoshino F, et al. Gingival vascular functions are altered in type 2 diabetes mellitus model and/or periodontitis model. J Clin Biochem Nutr. 2012;51:108–13.

    PubMed  PubMed Central  Google Scholar 

  41. Mizutani K, Park K, Mima A, Katagiri S, King GL. Obesity-associated gingival vascular inflammation and insulin resistance. J Dent Res. 2014;93:596–601.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Ohnishi T, Bandow K, Kakimoto K, Machigashira M, Matsuyama T, Matsuguchi T. Oxidative stress causes alveolar bone loss in metabolic syndrome model mice with type 2 diabetes. J Periodontal Res. 2009;44:43–51.

    CAS  PubMed  Google Scholar 

  43. Popkov VL, Fil’chukova IA, Lapina NV, Galenko-Yaroshevskii VP, Dukhanin AS. Activity of nitric oxide synthase and concentration of nitric oxide end metabolites in the gingiva under experimental pathological conditions. Bull Exp Biol Med. 2005;140:391–3.

    CAS  PubMed  Google Scholar 

  44. Sampath C, Okoro EU, Gipson MJ, Chukkapalli SS, Farmer-Dixon CM, Gangula PR. Porphyromonas gingivalis infection alters Nrf2-Phase II enzymes and nitric oxide in primary human aortic endothelial cells. J Periodontol. 2020.

  45. • Bugueno IM, Zobairi El-Ghazouani F, Batool F, El Itawi H, Angles-Cano E, Benkirane-Jessel N, et al. Porphyromonas gingivalis triggers the shedding of inflammatory endothelial microvesicles that act as autocrine effectors of endothelial dysfunction. Sci Rep. 2020;10:1778. (Endotherial cell infected with P. gingovalis cause endothelial dysfunction in vitro, providing causal effect of inflamation on endotherial function.)

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Farrugia C, Stafford GP, Potempa J, Wilkinson RN, Chen Y, Murdoch C, et al. Mechanisms of vascular damage by systemic dissemination of the oral pathogen Porphyromonas gingivalis. FEBS J. 2021;288:1479–95.

    CAS  PubMed  Google Scholar 

  47. Kato T, Inoue T, Node K. Postprandial endothelial dysfunction in subjects with new-onset type 2 diabetes: an acarbose and nateglinide comparative study. Cardiovasc Diabetol. 2010;9:12.

    PubMed  PubMed Central  Google Scholar 

  48. Shimabukuro M, Higa N, Chinen I, Yamakawa K, Takasu N. Effects of a single administration of acarbose on postprandial glucose excursion and endothelial dysfunction in type 2 diabetic patients: a randomized crossover study. J Clin Endocrinol Metab. 2006;91:837–42.

    CAS  PubMed  Google Scholar 

  49. Nystrom T, Gutniak MK, Zhang Q, Zhang F, Holst JJ, Ahren B, et al. Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am J Physiol Endocrinol Metab. 2004;287:E1209–15.

    PubMed  Google Scholar 

  50. Torimoto K, Okada Y, Mori H, Otsuka T, Kawaguchi M, Matsuda M, et al. Effects of exenatide on postprandial vascular endothelial dysfunction in type 2 diabetes mellitus. Cardiovasc Diabetol. 2015;14:25.

    PubMed  PubMed Central  Google Scholar 

  51. Maegawa H, Nishio Y, Nakao K, Ugi S, Maeda K, Uzu T, et al. Short-term low-dosage pioglitazone treatment improves vascular dysfunction in patients with type 2 diabetes. Endocr J. 2007;54:613–8.

    CAS  PubMed  Google Scholar 

  52. Baltzis D, Dushay JR, Loader J, Wu J, Greenman RL, Roustit M, et al. Effect of linagliptin on vascular function: a randomized, placebo-controlled study. J Clin Endocrinol Metab. 2016;101:4205–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Shigiyama F, Kumashiro N, Miyagi M, Iga R, Kobayashi Y, Kanda E, et al. Linagliptin improves endothelial function in patients with type 2 diabetes: a randomized study of linagliptin effectiveness on endothelial function. J Diabetes Investig. 2017;8:330–40.

    CAS  PubMed  Google Scholar 

  54. Shigiyama F, Kumashiro N, Miyagi M, Ikehara K, Kanda E, Uchino H, et al. Effectiveness of dapagliflozin on vascular endothelial function and glycemic control in patients with early-stage type 2 diabetes mellitus: DEFENCE study. Cardiovasc Diabetol. 2017;16:84.

    PubMed  PubMed Central  Google Scholar 

  55. Lavi T, Karasik A, Koren-Morag N, Kanety H, Feinberg MS, Shechter M. The acute effect of various glycemic index dietary carbohydrates on endothelial function in nondiabetic overweight and obese subjects. J Am Coll Cardiol. 2009;53:2283–7.

    CAS  PubMed  Google Scholar 

  56. Buscemi S, Cosentino L, Rosafio G, Morgana M, Mattina A, Sprini D, et al. Effects of hypocaloric diets with different glycemic indexes on endothelial function and glycemic variability in overweight and in obese adult patients at increased cardiovascular risk. Clin Nutr. 2013;32:346–52.

    CAS  PubMed  Google Scholar 

  57. Khoo J, Piantadosi C, Duncan R, Worthley SG, Jenkins A, Noakes M, et al. Comparing effects of a low-energy diet and a high-protein low-fat diet on sexual and endothelial function, urinary tract symptoms, and inflammation in obese diabetic men. J Sex Med. 2011;8:2868–75.

    CAS  PubMed  Google Scholar 

  58. Wycherley TP, Thompson CH, Buckley JD, Luscombe-Marsh ND, Noakes M, Wittert GA, et al. Long-term effects of weight loss with a very-low carbohydrate, low saturated fat diet on flow mediated dilatation in patients with type 2 diabetes: a randomised controlled trial. Atherosclerosis. 2016;252:28–31.

    CAS  PubMed  Google Scholar 

  59. Kondo K, Morino K, Nishio Y, Ishikado A, Arima H, Nakao K, et al. Fiber-rich diet with brown rice improves endothelial function in type 2 diabetes mellitus: a randomized controlled trial. PLoS ONE. 2017;12:e0179869.

    PubMed  PubMed Central  Google Scholar 

  60. Shimabukuro M, Higa M, Kinjo R, Yamakawa K, Tanaka H, Kozuka C, et al. Effects of the brown rice diet on visceral obesity and endothelial function: the BRAVO study. Br J Nutr. 2014;111:310–20.

    CAS  PubMed  Google Scholar 

  61. Cicero AFG, Caliceti C, Fogacci F, Giovannini M, Calabria D, Colletti A, et al. Effect of apple polyphenols on vascular oxidative stress and endothelium function: a translational study. Mol Nutr Food Res. 2017 61.

  62. Kwak JH, Paik JK, Kim HI, Kim OY, Shin DY, Kim HJ, et al. Dietary treatment with rice containing resistant starch improves markers of endothelial function with reduction of postprandial blood glucose and oxidative stress in patients with prediabetes or newly diagnosed type 2 diabetes. Atherosclerosis. 2012;224:457–64.

    CAS  PubMed  Google Scholar 

  63. Sedaghat A, Shahbazian H, Rezazadeh A, Haidari F, Jahanshahi A, Mahmoud Latifi S, et al. The effect of soy nut on serum total antioxidant, endothelial function and cardiovascular risk factors in patients with type 2 diabetes. Diabetes Metab Syndr. 2019;13:1387–91.

    PubMed  Google Scholar 

  64. Monti LD, Casiraghi MC, Setola E, Galluccio E, Pagani MA, Quaglia L, et al. L-arginine enriched biscuits improve endothelial function and glucose metabolism: a pilot study in healthy subjects and a cross-over study in subjects with impaired glucose tolerance and metabolic syndrome. Metabolism. 2013;62:255–64.

    CAS  PubMed  Google Scholar 

  65. Ceriello A, Esposito K, La Sala L, Pujadas G, De Nigris V, 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.

    PubMed  PubMed Central  Google Scholar 

  66. • Torres-Pena JD, Garcia-Rios A, Delgado-Casado N, Gomez-Luna P, Alcala-Diaz JF, Yubero-Serrano EM, et al. Mediterranean diet improves endothelial function in patients with diabetes and prediabetes: a report from the CORDIOPREV study. Atherosclerosis. 2018;269:50–6. (This randomized clinical study provides the efficacy of mediterial diet on endothelial function.)

    CAS  PubMed  Google Scholar 

  67. Yubero-Serrano EM, Fernandez-Gandara C, Garcia-Rios A, Rangel-Zuniga OA, Gutierrez-Mariscal FM, Torres-Pena JD, et al. Mediterranean diet and endothelial function in patients with coronary heart disease: an analysis of the CORDIOPREV randomized controlled trial. PLoS Med. 2020;17:e1003282.

    PubMed  PubMed Central  Google Scholar 

  68. Kondo K, Morino K, Nishio Y, Kondo M, Nakao K, Nakagawa F, et al. A fish-based diet intervention improves endothelial function in postmenopausal women with type 2 diabetes mellitus: a randomized crossover trial. Metabolism. 2014;63:930–40.

    CAS  PubMed  Google Scholar 

  69. Lobraico JM, DiLello LC, Butler AD, Cordisco ME, Petrini JR, Ahmadi R. Effects of krill oil on endothelial function and other cardiovascular risk factors in participants with type 2 diabetes, a randomized controlled trial. BMJ Open Diabetes Res Care. 2015;3:e000107.

    PubMed  PubMed Central  Google Scholar 

  70. Sawada T, Tsubata H, Hashimoto N, Takabe M, Miyata T, Aoki K, et al. Effects of 6-month eicosapentaenoic acid treatment on postprandial hyperglycemia, hyperlipidemia, insulin secretion ability, and concomitant endothelial dysfunction among newly-diagnosed impaired glucose metabolism patients with coronary artery disease. An open label, single blinded, prospective randomized controlled trial. Cardiovasc Diabetol. 2016;15:121.

  71. Clerici C, Nardi E, Battezzati PM, Asciutti S, Castellani D, Corazzi N, et al. Novel soy germ pasta improves endothelial function, blood pressure, and oxidative stress in patients with type 2 diabetes. Diabetes Care. 2011;34:1946–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Watts GF, Playford DA, Croft KD, Ward NC, Mori TA, Burke V. Coenzyme Q(10) improves endothelial dysfunction of the brachial artery in type II diabetes mellitus. Diabetologia. 2002;45:420–6.

    CAS  PubMed  Google Scholar 

  73. Ishikado A, Morino K, Nishio Y, Nakagawa F, Mukose A, Sono Y, et al. 4-Hydroxy hexenal derived from docosahexaenoic acid protects endothelial cells via Nrf2 activation. PLoS ONE. 2013;8:e69415.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Ishikado A, Nishio Y, Yamane K, Mukose A, Morino K, Murakami Y, et al. Soy phosphatidylcholine inhibited TLR4-mediated MCP-1 expression in vascular cells. Atherosclerosis. 2009;205:404–12.

    CAS  PubMed  Google Scholar 

  75. Amedei A, Morbidelli L. Circulating metabolites originating from gut microbiota control endothelial cell function. Molecules. 2019 24.

  76. Brunt VE, Gioscia-Ryan RA, Casso AG, VanDongen NS, Ziemba BP, Sapinsley ZJ, et al. Trimethylamine-N-oxide promotes age-related vascular oxidative stress and endothelial dysfunction in mice and healthy humans. Hypertension. 2020;76:101–12.

    CAS  PubMed  Google Scholar 

  77. Rovella V, Rodia G, Di Daniele F, Cardillo C, Campia U, Noce A, et al. Association of gut hormones and microbiota with vascular dysfunction in obesity. Nutrients. 2021 13.

  78. DeMayo F, Molinsky R, Tahir MJ, Roy S, Genkinger JM, Papapanou PN, et al. Diet quality and periodontal disease: results from the oral infections, glucose intolerance and insulin resistance study (ORIGINS). J Clin Periodontol. 2021;48:638–47.

    CAS  PubMed  Google Scholar 

  79. Merchant AT, Pitiphat W, Franz M, Joshipura KJ. Whole-grain and fiber intakes and periodontitis risk in men. Am J Clin Nutr. 2006;83:1395–400.

    CAS  PubMed  Google Scholar 

  80. Salazar CR, Laniado N, Mossavar-Rahmani Y, Borrell LN, Qi Q, Sotres-Alvarez D, et al. Better-quality diet is associated with lower odds of severe periodontitis in US Hispanics/Latinos. J Clin Periodontol. 2018;45:780–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. • Wright DM, McKenna G, Nugent A, Winning L, Linden GJ, Woodside JV. Association between diet and periodontitis: a cross-sectional study of 10,000 NHANES participants. Am J Clin Nutr. 2020;112:1485–91. (This large cohort cross-sectional study investigates association between diet and periodontal disease.)

    PubMed  Google Scholar 

  82. Jenzsch A, Eick S, Rassoul F, Purschwitz R, Jentsch H. Nutritional intervention in patients with periodontal disease: clinical, immunological and microbiological variables during 12 months. Br J Nutr. 2009;101:879–85.

    CAS  PubMed  Google Scholar 

  83. Kondo K, Ishikado A, Morino K, Nishio Y, Ugi S, Kajiwara S, et al. A high-fiber, low-fat diet improves periodontal disease markers in high-risk subjects: a pilot study. Nutr Res. 2014;34:491–8.

    CAS  PubMed  Google Scholar 

  84. Gokhale NH, Acharya AB, Patil VS, Trivedi DJ, Thakur SL. A short-term evaluation of the relationship between plasma ascorbic acid levels and periodontal disease in systemically healthy and type 2 diabetes mellitus subjects. J Diet Suppl. 2013;10:93–104.

    CAS  PubMed  Google Scholar 

  85. Zare Javid A, Hormoznejad R, Yousefimanesh HA, Zakerkish M, Haghighi-Zadeh MH, Dehghan P, et al. The impact of resveratrol supplementation on blood glucose, insulin, insulin resistance, triglyceride, and periodontal markers in type 2 diabetic patients with chronic periodontitis. Phytother Res. 2017;31:108–14.

    CAS  PubMed  Google Scholar 

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Funding

This study was supported in part by the Japan Foundation for Applied Enzymology (to KK).

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Authors and Affiliations

  1. Department of Medicine, Shiga University of Medical Science, Seta, Tsukinowa, Otsu, Shiga, 520-2192, Japan

    Atsushi Ishikado, Hiroshi Maegawa & Katsutaro Morino

  2. R&D Department, Sunstar Inc., 3-1 Asahi-machi, Takatsuki, Osaka, 569-1195, Japan

    Atsushi Ishikado

  3. Department of Public Health, Shiga University of Medical Science, Seta, Tsukinowa, Otsu, Shiga, 520-2192, Japan

    Keiko Kondo

  4. Institutional Research Office, Shiga University of Medical Science, Seta, Tsukinowa, Otsu, Shiga, 520-2192, Japan

    Katsutaro Morino

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  1. Atsushi Ishikado
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  4. Katsutaro Morino
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AI wrote the draft. KK, HM, and KM reviewed and edited the manuscript. All authors approved the final manuscript.

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Correspondence to Katsutaro Morino.

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AI is an employee of Sunstar Inc. HM and KM received research support unrelated to this study from Sunstar Inc. No other potential conflicts of interest relevant to this study are declared.

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Ishikado, A., Kondo, K., Maegawa, H. et al. Nutrition and Periodontal Health in the Patients with Diabetes Mellitus: a Review from the Viewpoint of Endothelial Function. Curr Oral Health Rep 8, 67–74 (2021). https://doi.org/10.1007/s40496-021-00297-3

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