Periodontitis and Diabetes Mellitus: Directional Relationship

Şükran Acıpınar; Meltem Karşıyaka Hendek; Ebru Olgun Erdemir

doi:10.24938/kutfd.321684

Review

Periodontitis and Diabetes Mellitus: Directional Relationship

Year 2017, , 103 - 113, 31.08.2017

Şükran Acıpınar , Meltem Karşıyaka Hendek , Ebru Olgun Erdemir

https://doi.org/10.24938/kutfd.321684

Abstract

Periodontitis
and diabetes mellitus (DM) are common chronic diseases in the society.
Periodontitis is a chronic inflammatory condition that can result in tooth loss
due to destruction of the supporting tissues (periodontal ligament and bone) of
the teeth resulting from impaired balance between bacterial plaque and host
immune response. Diabetes mellitus is an impairment of carbohydrate, fat and
protein metabolism, manifested by the absence of insulin hormone secretion /
insufficiency or by various complications of insulin resistance. Periodontitis has recently become one of the classic complications of diabetes. Epidemiological
data suggest that diabetes is a major risk factor for periodontitis and that
diabetics are more likely to be periodontitis than non-diabetics. It is known
that there is a mutual relationship between these two chronic diseases.
Although the role of various cellular, immunological pathways and cytokines has
been determined, the mechanism is still not fully understood.

Keywords

Diabetes Mellitus, inflammation, periodontitis

References

1. Loe H. Periodontal disease:The sixth complication of diabetes mellitus. Diabetes Care. 1993; 16(1): 329–34.
2. Scannapieco FA , Cantos A. Oral inflammation and infection, and chronic medical diseases: implications for the elderly. Periodontology 2000. 2016; 72(1): 153–75.
3. Schmidt MI, Duncan BB, Sharrett AR et al. Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study. Lancet. 1999; 353 (9165): 1649-52.
4. Kornman KS. Mapping the pathogenesis of periodontitis: a new look. Journal of Periodontology. 2008; 79(8 Suppl): 1560-8.
5. Graves D. Cytokines that promote periodontal tissue destruction. Journal of Periodontology. 2008; 79(8 Suppl): 1585-91.
6. Chavarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009: 7(2): 107–27.
7. Mealey BL. Diabetes and periodontal disease: two sides of a coin. Compend Contin Educ Dent. 2000; 21(11) 943–6, 948, 950.
8. Nagpal R, Yamashiro Y, Izumi Y. The Two-Way Association of Periodontal Infection with Systemic Disorders: An Overview. Mediators Inflamm. 2015; 2015:793898.
9. Yan SF, Ramasamy R, Schmidt AM. Receptor for AGE (RAGE) and its ligands-cast into leading roles in diabetes and the inﬂammatory response. Journal of Molecular Medicine (Berl). 2009; 87: 235–47.
10. Kumar M, Mishra L, Mohanty R, Nayak R. Diabetes and gum disease: the diabolic duo. Diabetes& Metabolic Syndrome: Clinical Research & Reviews . 2014; 8(4): 255-8.
11. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circulation Research 2010; 107(9): 1058–70.
12. Ryan ME, Carnu O, Kamer A. The influence of diabetes on the periodontal tissues. J Am Dent Assoc 2003; 134: 34-40.
13. Ryan ME, Ramamurthy S, Golub LM. Matrix metalloproteinases and their inhibition in periodontal treatment. Curr Opin Periodontol 1996; 3: 85-96.
14. Mealey BI, Oates TW. Diabetes mellitus and periodontal diseases. J Periodontol 2006; 77(8): 1289-303.
15. Gurav A, Jadhav V. Periodontitis and risk of diabetes mellitus. J Diabetes 2011;3(1): 21-8.
16. Engebretson SP , Vossughi F, Hey-Hadavi J, Emingil G, Grbic JT. The inﬂuence of diabetes on gingival crevicular ﬂuid beta-glucuronidase and interleukin-8. Journal of Clinical Periodontology 2006; 33(11): 784–90.
17. Ilan Y, Maron R, Tukpah AM et al. Induction of regulatory T cells decreases adipose inﬂammation and alleviates insulin resistance in ob/ob mice. Proceedings of the National Academy of Sciences USA 2010;107(21): 9765–70.
18. Allen EM, Matthews JB, O’Halloran DJ, Grifﬁths HR, Chapple IL. Oxidative and inﬂammatory status in Type 2 diabetes patients with periodontitis. Journal of Clinical Periodontology 2011; 38(10): 894–901.
19. Aemaimanan P, Amimanan P, Taweechaisupapong S. Quantiﬁcation of key periodontal pathogens in insulin-dependent type 2 diabetic and non-diabetic patients with generalized chronic periodontitis. Anaerobe 2013; 22: 64–8.
20. Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Frontiers in Bioscience 2008; 13: 1227–39.
21. Bullon P, Newman HN, Battino M. Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction? Periodontology 2000. 2014; 64(1): 139–53.
22. Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL,Newman HN, Battino M. “Metabolic syndrome and periodontitis: is oxidative stress a common link?” Journal of Dental Research 2009; 88(6): 503–18.
23. Rosen P, Nawroth PP, King G, Moller W, Tritsnochler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCOMCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001; 17(3): 189–212.
24. Taylor WG. The effects of periodontal treatment on diabetes. J Am Dent Assoc 2003; 134: 41-8.
25. Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inﬂammation. Diabetologia 2010; 53(1): 10–20.
26. Atieh MA, Faggion CMJr, Seymour GJ. Cytokines in patients with type 2 diabetes and chronic periodontitis: A systemic review and meta-analysis. Diabetes Res Clin Pract. 2014; 104(2): 38-45.
27. Ribeiro FV, de Mendonca AC, Santos VR, Bastos MF, Figueiredo LC, Duarte PM. Cytokines and bone-related factors in systemically healthy patients with chronic periodontitis and patients with type 2 diabetes and chronic periodontitis. Journal of Periodontology 2011; 82(8): 1187–96.
28. Renvert S, Pettersson T, Ohlsson O, Persson GR. Bacterial proﬁle and burden of periodontal infection in subjects with a diagnosis of acute coronary syndrome. Journal of Periodontology 2006;77(7) :1110–9.
29. Pizzo G, Guiglia R, Lo Russo L, Campisi G. Dentistry and internal medicine: from the focal infection theory to the periodontal medicine concept. European Journal of Internal Medicine 2010; 21(6): 496–502.
30. Preshaw PM, Alba AL, Herrera D et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012; 55(1): 21–31.
31. Brownlee M. A radical explanation for glucose- induced beta cell dysfunction. J Clin Invest 2003; 112(12): 1788-90.
32. Haffner S, Temprosa M,Crandall J et al. Intensive lifestyle intervention or metformin on inflammation and coagulation in participants with impaired glucose tolerance. Diabetes 2005; 54(5): 1566-72.
33. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. Journal of Biological Chemistry 2003; 278(46): 45777–84.
34. Duarte PM, Santos VR, Dos Santos FA, de Lima Pereira SA, Rodrigues DB, Napimoga MH. Role of smoking and type 2 diabetes in the immunobalance of advanced chronic periodontitis. Journal of Periodontology 2011; 82(3): 429–38.
35. Liu R, Desta T, He H, Graves DT. Diabetes alters the response to bacteria by enhancing ﬁbroblast apoptosis. Endocrinology 2004; 145(6): 2997–3003.
36. Schmidt AM, Weidman E, Lalla, E et al. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. Journal of Periodontal Research 1996; 31(7): 508–15.
37. Yoon MS, Jankowski V, Montag S et al. Characterisation of advanced glycation endproducts in saliva from patients with diabetes mellitus. Biochemical and Biophysical Research Communications 2004; 323(2): 377–81.
38. Takeda M, Ojima M, Yoshioka H et al. Relationship of serum advanced glycation end products with deterioration of periodontitis in type 2 diabetes patients. Journal of Periodontology 2006; 77(1): 15-20.
39. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM. A murine model of accelerated periodontal disease in diabetes. J Periodontal Res. 1998; 33(7): 387-99.
40. Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non-surgical periodontal therapy on clinical and immunological response and glycaemic control in type 2 diabetic patients with moderate periodontitis. J Clin Periodontol 2007; 34(10): 835-43.
41. Loos BG, Craandiji J, Hoek FJ, Wertheim -van Dillen PME, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 2000; 71(10): 1528-34.
42. Andriankaja OM, Barros S P, Moss K et al. Levels of serum interleukin (IL)-6 and gingival crevicular ﬂuid of IL-1beta and prostaglandin E(2) among non-smoking subjects with gingivitis and type 2 diabetes. Journal of Periodontology 2009; 80(2): 307-16.
43. Sakallıoğlu EE, Ayas B, Lütfioğlu M, Keleş GC, Açıkgöz G, Fıratlı E. Gingival levels of monocyte chemoattractant protein-1 (MCP-1) in diabetes mellitus and periodontitis: an experimental study in rats. Clin Oral Investig. 2008; 12(1): 83-9.
44. Bastos AS, Graves DT, Loureiro AP et al. Lipid peroxidation is associated with the severity of periodontal disease and local inﬂammatory markers in patients with type 2 diabetes. Journal of Clinical Endocrinology and Metabolism 2012; 97(8): 1353–62.
45. D’Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative stress, systemic inﬂammation, and severe periodontitis. Journal of Dental Research 2010; 89(11): 1241–6.
46. Demmer RT, Desvarieux M, Holtfreter B et al. Periodontal status and A1C change: longitudinal results from the study of health in Pomerania (SHIP). Diabetes Care 2010; 33(5): 1037–43.
47. Ou L, Li RF. Effect of periodontal treatment on glycosylated hemoglobin levels in elderly patients with periodontal disease and type 2 diabetes. Chin Med J (Engl) 2011; 124(19): 3070–3.
48. Y. Iwamoto, F. Nishimura, M. Nakagawa et al. The effect of antimicrobial periodontal treatment on circulating tumor necrosis factor-alpha and glycated hemoglobin level in patients with type 2 diabetes. J. Periodontol. 2001;72(6): 774–8.
49. Munenaga Y, Hiroshima Study Group, Yamashina T, Tanaka J, Nishimura F. Improvement of glycated hemoglobin in Japanese subjects with type 2 diabetes by resolution of periodontal inﬂammation using adjunct topical antibiotics: results from the Hiroshima Study. Diabetes Res. Clin. Pract. 2013; 100(1): 53–60.
50. Sgolastra F, Severino M, Pietropaoli D, Gatto R, Monaco A. Effectiveness of periodontal treatment to improve metabolic control in patients with chronic periodontitis and type 2 diabetes: a meta-analysis of randomized clinical trials. J. Periodontol. 2013; 84(7): 958–73.
51. Costa FO, Miranda Cota LO, Pereira Lages EJ et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84(5): 595–605.
52. Janket SJ, Wightman A, Baird AE, Van Dyke TE, Jones JA. Does periodontal treatment improve glycemic control in diabetic patients? A metaanalysis of intervention studies. J Dent Res 2005;84(12): 1154-9.
53. Santos Tunes R, Foss-Freitas MC, Nogueira-Filho Gda R. Impact of periodontitis on the diabetes-related inﬂammatory status. J Can Dent Assoc 2010; 76: 35.
54. Stratton IM, Adler AI, Neil HA et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000; 321(7258): 405–12.
55. Jones JA, Miller DR, Wehler CJ et al. Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. J Clin Periodontol 2007; 34(1): 46-52.
56. Llambes F, Silvestre FJ, Hernandez-Mijares A, Guiha R, Caffesse R. The effect of periodontal treatment on metabolic control of type 1 diabetes mellitus. Clin Oral Investig 2008; 12(4): 337-43.

PERİODONTİTİS VE DİABETES MELLİTUS: ÇİFT YÖNLÜ İLİŞKİ

Year 2017, , 103 - 113, 31.08.2017

Şükran Acıpınar , Meltem Karşıyaka Hendek , Ebru Olgun Erdemir

https://doi.org/10.24938/kutfd.321684

Abstract

Periodontitis ve diabetes mellitus (DM) toplumda
yaygın görülen kronik hastalıklardır. Periodontitis bakteriyel plak ve konak
immün yanıtı arasındaki dengenin bozulmasından kaynaklanan dişlerin destek
dokularının (periodontal ligament ve kemik) yıkımıyla karakterize diş kaybıyla
sonuçlanabilen kronik inflamatuar bir durumdur. Diabetes mellitus insülin
hormon sekresyonunun yokluğu / yetersizliği veya insülin direnci ile
karakterize çeşitli komplikasyonlarla kendini gösteren karbonhidrat, yağ ve
protein metabolizma bozukluğu hastalığıdır. Periodontitis son dönemlerde
diyabetin klasik komplikasyonlarından biri halini almıştır. Epidemiyolojik
veriler diyabetin periodontitis için majör risk faktörü olduğunu ve
diyabetiklerin diyabetik olmayanlara göre periodontitise daha yatkın olduğunu
göstermektedir. Bu iki kronik hastalık arasında karşılıklı ilişki olduğu
bilinmektedir. Çeşitli hücresel, immünolojik yolların ve sitokinlerin rolü
olduğu belirlenmiş olsa da mekanizma halen tam olarak anlaşılamamıştır.

Keywords

Diabetes Mellitus, Periodontitis, inflamasyon

References

1. Loe H. Periodontal disease:The sixth complication of diabetes mellitus. Diabetes Care. 1993; 16(1): 329–34.
2. Scannapieco FA , Cantos A. Oral inflammation and infection, and chronic medical diseases: implications for the elderly. Periodontology 2000. 2016; 72(1): 153–75.
3. Schmidt MI, Duncan BB, Sharrett AR et al. Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study. Lancet. 1999; 353 (9165): 1649-52.
4. Kornman KS. Mapping the pathogenesis of periodontitis: a new look. Journal of Periodontology. 2008; 79(8 Suppl): 1560-8.
5. Graves D. Cytokines that promote periodontal tissue destruction. Journal of Periodontology. 2008; 79(8 Suppl): 1585-91.
6. Chavarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009: 7(2): 107–27.
7. Mealey BL. Diabetes and periodontal disease: two sides of a coin. Compend Contin Educ Dent. 2000; 21(11) 943–6, 948, 950.
8. Nagpal R, Yamashiro Y, Izumi Y. The Two-Way Association of Periodontal Infection with Systemic Disorders: An Overview. Mediators Inflamm. 2015; 2015:793898.
9. Yan SF, Ramasamy R, Schmidt AM. Receptor for AGE (RAGE) and its ligands-cast into leading roles in diabetes and the inﬂammatory response. Journal of Molecular Medicine (Berl). 2009; 87: 235–47.
10. Kumar M, Mishra L, Mohanty R, Nayak R. Diabetes and gum disease: the diabolic duo. Diabetes& Metabolic Syndrome: Clinical Research & Reviews . 2014; 8(4): 255-8.
11. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circulation Research 2010; 107(9): 1058–70.
12. Ryan ME, Carnu O, Kamer A. The influence of diabetes on the periodontal tissues. J Am Dent Assoc 2003; 134: 34-40.
13. Ryan ME, Ramamurthy S, Golub LM. Matrix metalloproteinases and their inhibition in periodontal treatment. Curr Opin Periodontol 1996; 3: 85-96.
14. Mealey BI, Oates TW. Diabetes mellitus and periodontal diseases. J Periodontol 2006; 77(8): 1289-303.
15. Gurav A, Jadhav V. Periodontitis and risk of diabetes mellitus. J Diabetes 2011;3(1): 21-8.
16. Engebretson SP , Vossughi F, Hey-Hadavi J, Emingil G, Grbic JT. The inﬂuence of diabetes on gingival crevicular ﬂuid beta-glucuronidase and interleukin-8. Journal of Clinical Periodontology 2006; 33(11): 784–90.
17. Ilan Y, Maron R, Tukpah AM et al. Induction of regulatory T cells decreases adipose inﬂammation and alleviates insulin resistance in ob/ob mice. Proceedings of the National Academy of Sciences USA 2010;107(21): 9765–70.
18. Allen EM, Matthews JB, O’Halloran DJ, Grifﬁths HR, Chapple IL. Oxidative and inﬂammatory status in Type 2 diabetes patients with periodontitis. Journal of Clinical Periodontology 2011; 38(10): 894–901.
19. Aemaimanan P, Amimanan P, Taweechaisupapong S. Quantiﬁcation of key periodontal pathogens in insulin-dependent type 2 diabetic and non-diabetic patients with generalized chronic periodontitis. Anaerobe 2013; 22: 64–8.
20. Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Frontiers in Bioscience 2008; 13: 1227–39.
21. Bullon P, Newman HN, Battino M. Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction? Periodontology 2000. 2014; 64(1): 139–53.
22. Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL,Newman HN, Battino M. “Metabolic syndrome and periodontitis: is oxidative stress a common link?” Journal of Dental Research 2009; 88(6): 503–18.
23. Rosen P, Nawroth PP, King G, Moller W, Tritsnochler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCOMCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001; 17(3): 189–212.
24. Taylor WG. The effects of periodontal treatment on diabetes. J Am Dent Assoc 2003; 134: 41-8.
25. Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inﬂammation. Diabetologia 2010; 53(1): 10–20.
26. Atieh MA, Faggion CMJr, Seymour GJ. Cytokines in patients with type 2 diabetes and chronic periodontitis: A systemic review and meta-analysis. Diabetes Res Clin Pract. 2014; 104(2): 38-45.
27. Ribeiro FV, de Mendonca AC, Santos VR, Bastos MF, Figueiredo LC, Duarte PM. Cytokines and bone-related factors in systemically healthy patients with chronic periodontitis and patients with type 2 diabetes and chronic periodontitis. Journal of Periodontology 2011; 82(8): 1187–96.
28. Renvert S, Pettersson T, Ohlsson O, Persson GR. Bacterial proﬁle and burden of periodontal infection in subjects with a diagnosis of acute coronary syndrome. Journal of Periodontology 2006;77(7) :1110–9.
29. Pizzo G, Guiglia R, Lo Russo L, Campisi G. Dentistry and internal medicine: from the focal infection theory to the periodontal medicine concept. European Journal of Internal Medicine 2010; 21(6): 496–502.
30. Preshaw PM, Alba AL, Herrera D et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012; 55(1): 21–31.
31. Brownlee M. A radical explanation for glucose- induced beta cell dysfunction. J Clin Invest 2003; 112(12): 1788-90.
32. Haffner S, Temprosa M,Crandall J et al. Intensive lifestyle intervention or metformin on inflammation and coagulation in participants with impaired glucose tolerance. Diabetes 2005; 54(5): 1566-72.
33. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. Journal of Biological Chemistry 2003; 278(46): 45777–84.
34. Duarte PM, Santos VR, Dos Santos FA, de Lima Pereira SA, Rodrigues DB, Napimoga MH. Role of smoking and type 2 diabetes in the immunobalance of advanced chronic periodontitis. Journal of Periodontology 2011; 82(3): 429–38.
35. Liu R, Desta T, He H, Graves DT. Diabetes alters the response to bacteria by enhancing ﬁbroblast apoptosis. Endocrinology 2004; 145(6): 2997–3003.
36. Schmidt AM, Weidman E, Lalla, E et al. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. Journal of Periodontal Research 1996; 31(7): 508–15.
37. Yoon MS, Jankowski V, Montag S et al. Characterisation of advanced glycation endproducts in saliva from patients with diabetes mellitus. Biochemical and Biophysical Research Communications 2004; 323(2): 377–81.
38. Takeda M, Ojima M, Yoshioka H et al. Relationship of serum advanced glycation end products with deterioration of periodontitis in type 2 diabetes patients. Journal of Periodontology 2006; 77(1): 15-20.
39. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM. A murine model of accelerated periodontal disease in diabetes. J Periodontal Res. 1998; 33(7): 387-99.
40. Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non-surgical periodontal therapy on clinical and immunological response and glycaemic control in type 2 diabetic patients with moderate periodontitis. J Clin Periodontol 2007; 34(10): 835-43.
41. Loos BG, Craandiji J, Hoek FJ, Wertheim -van Dillen PME, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 2000; 71(10): 1528-34.
42. Andriankaja OM, Barros S P, Moss K et al. Levels of serum interleukin (IL)-6 and gingival crevicular ﬂuid of IL-1beta and prostaglandin E(2) among non-smoking subjects with gingivitis and type 2 diabetes. Journal of Periodontology 2009; 80(2): 307-16.
43. Sakallıoğlu EE, Ayas B, Lütfioğlu M, Keleş GC, Açıkgöz G, Fıratlı E. Gingival levels of monocyte chemoattractant protein-1 (MCP-1) in diabetes mellitus and periodontitis: an experimental study in rats. Clin Oral Investig. 2008; 12(1): 83-9.
44. Bastos AS, Graves DT, Loureiro AP et al. Lipid peroxidation is associated with the severity of periodontal disease and local inﬂammatory markers in patients with type 2 diabetes. Journal of Clinical Endocrinology and Metabolism 2012; 97(8): 1353–62.
45. D’Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative stress, systemic inﬂammation, and severe periodontitis. Journal of Dental Research 2010; 89(11): 1241–6.
46. Demmer RT, Desvarieux M, Holtfreter B et al. Periodontal status and A1C change: longitudinal results from the study of health in Pomerania (SHIP). Diabetes Care 2010; 33(5): 1037–43.
47. Ou L, Li RF. Effect of periodontal treatment on glycosylated hemoglobin levels in elderly patients with periodontal disease and type 2 diabetes. Chin Med J (Engl) 2011; 124(19): 3070–3.
48. Y. Iwamoto, F. Nishimura, M. Nakagawa et al. The effect of antimicrobial periodontal treatment on circulating tumor necrosis factor-alpha and glycated hemoglobin level in patients with type 2 diabetes. J. Periodontol. 2001;72(6): 774–8.
49. Munenaga Y, Hiroshima Study Group, Yamashina T, Tanaka J, Nishimura F. Improvement of glycated hemoglobin in Japanese subjects with type 2 diabetes by resolution of periodontal inﬂammation using adjunct topical antibiotics: results from the Hiroshima Study. Diabetes Res. Clin. Pract. 2013; 100(1): 53–60.
50. Sgolastra F, Severino M, Pietropaoli D, Gatto R, Monaco A. Effectiveness of periodontal treatment to improve metabolic control in patients with chronic periodontitis and type 2 diabetes: a meta-analysis of randomized clinical trials. J. Periodontol. 2013; 84(7): 958–73.
51. Costa FO, Miranda Cota LO, Pereira Lages EJ et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84(5): 595–605.
52. Janket SJ, Wightman A, Baird AE, Van Dyke TE, Jones JA. Does periodontal treatment improve glycemic control in diabetic patients? A metaanalysis of intervention studies. J Dent Res 2005;84(12): 1154-9.
53. Santos Tunes R, Foss-Freitas MC, Nogueira-Filho Gda R. Impact of periodontitis on the diabetes-related inﬂammatory status. J Can Dent Assoc 2010; 76: 35.
54. Stratton IM, Adler AI, Neil HA et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000; 321(7258): 405–12.
55. Jones JA, Miller DR, Wehler CJ et al. Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. J Clin Periodontol 2007; 34(1): 46-52.
56. Llambes F, Silvestre FJ, Hernandez-Mijares A, Guiha R, Caffesse R. The effect of periodontal treatment on metabolic control of type 1 diabetes mellitus. Clin Oral Investig 2008; 12(4): 337-43.

There are 56 citations in total.

Details

Subjects	Health Care Administration
Journal Section	Review
Authors	Şükran Acıpınar Meltem Karşıyaka Hendek Ebru Olgun Erdemir
Publication Date	August 31, 2017
Submission Date	June 15, 2017
Published in Issue	Year 2017

Cite

APA	Acıpınar, Ş., Karşıyaka Hendek, M., & Olgun Erdemir, E. (2017). Periodontitis and Diabetes Mellitus: Directional Relationship. The Journal of Kırıkkale University Faculty of Medicine, 19(2), 103-113. https://doi.org/10.24938/kutfd.321684
AMA	Acıpınar Ş, Karşıyaka Hendek M, Olgun Erdemir E. Periodontitis and Diabetes Mellitus: Directional Relationship. Kırıkkale Üni Tıp Derg. August 2017;19(2):103-113. doi:10.24938/kutfd.321684
Chicago	Acıpınar, Şükran, Meltem Karşıyaka Hendek, and Ebru Olgun Erdemir. “Periodontitis and Diabetes Mellitus: Directional Relationship”. The Journal of Kırıkkale University Faculty of Medicine 19, no. 2 (August 2017): 103-13. https://doi.org/10.24938/kutfd.321684.
EndNote	Acıpınar Ş, Karşıyaka Hendek M, Olgun Erdemir E (August 1, 2017) Periodontitis and Diabetes Mellitus: Directional Relationship. The Journal of Kırıkkale University Faculty of Medicine 19 2 103–113.
IEEE	Ş. Acıpınar, M. Karşıyaka Hendek, and E. Olgun Erdemir, “Periodontitis and Diabetes Mellitus: Directional Relationship”, Kırıkkale Üni Tıp Derg, vol. 19, no. 2, pp. 103–113, 2017, doi: 10.24938/kutfd.321684.
ISNAD	Acıpınar, Şükran et al. “Periodontitis and Diabetes Mellitus: Directional Relationship”. The Journal of Kırıkkale University Faculty of Medicine 19/2 (August 2017), 103-113. https://doi.org/10.24938/kutfd.321684.
JAMA	Acıpınar Ş, Karşıyaka Hendek M, Olgun Erdemir E. Periodontitis and Diabetes Mellitus: Directional Relationship. Kırıkkale Üni Tıp Derg. 2017;19:103–113.
MLA	Acıpınar, Şükran et al. “Periodontitis and Diabetes Mellitus: Directional Relationship”. The Journal of Kırıkkale University Faculty of Medicine, vol. 19, no. 2, 2017, pp. 103-1, doi:10.24938/kutfd.321684.
Vancouver	Acıpınar Ş, Karşıyaka Hendek M, Olgun Erdemir E. Periodontitis and Diabetes Mellitus: Directional Relationship. Kırıkkale Üni Tıp Derg. 2017;19(2):103-1.

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