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Published in: Diabetes Therapy 11/2020

Open Access 01-11-2020 | Gingival Diseases | Original Research

Periodontal Disease in Diabetes Mellitus: A Case–Control Study in Smokers and Non-Smokers

Authors: Emese Battancs, Dorottya Gheorghita, Szabolcs Nyiraty, Csaba Lengyel, Gabriella Eördegh, Zoltán Baráth, Tamás Várkonyi, Márk Antal

Published in: Diabetes Therapy | Issue 11/2020

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Abstract

Introduction

It is well established that periodontal disease (PD) and diabetes mellitus (DM) can have a detrimental effect on each other’s disease course, and that cigarette smoking exacerbates both conditions. However, literature on the periodontal status of smokers with DM is scarce, and the studies conducted to date did not use healthy controls or non-smokers with DM as controls. Consequently, the individual effects of smoking and DM on PD are difficult to untangle and estimate.

Methods

A total of 128 participants were recruited to this study and their data analyzed. They were assigned to four groups: smoking patients with DM (SDM); non-smoking patients with DM (NSDM); smokers without DM (control group, SC) and (4) non-smokers without DM (control group, NSC). Each group consisted of 32 age-matched participants. The periodontal status of the participants was assessed by full oral examination. To express periodontal status, we used the four-stage classification introduced by Fernandes and colleagues (J Periodontol. 80(7):1062–1068, 2009). The control of DM was estimated by measuring hemoglobin A1c (HbA1c) levels in the peripheral blood.

Results

A significant difference in the severity of PD was found between the SC and NSC groups (p = 0.027) and between the NSC and SDM groups (p = 0.000), while the difference between the NSDM and SDM groups approached significance (p = 0.052). No person in the smoker groups could be classified as having a healthy periodontal status. The four-stage classification followed a normal distribution in the healthy, non-smoking controls (NSC). Smoking caused a shift toward medium-severe PD, while a marked shift toward the most severe stage was observed when both smoking and DM were present (SDM). There was no significant association between the type of DM and periodontal status, nor between diabetes control and the severity of PD. Persons in the SDM group had significantly fewer teeth than those in the NSC group (mean ± standard deviation: 16.0 ± 7.9 vs. 20.7 ± 5.6; p = 0.02).

Conclusion

Smoking damages the periodontium of even healthy individuals, but the damage is multiplied in a smoker who has DM, even though the effect of DM alone on periodontium health is relatively mild. Our results suggest a synergy between DM and smoking in terms of damage to the periodontal tissues, but the limited sample size of this study does not allow any hard conclusion to be drawn.
Literature
1.
go back to reference Molloy J, Wolff LF, Lopez-Guzman A, Hodges JS. The association of periodontal disease parameters with systemic medical conditions and tobacco use. J Clin Periodontol. 2004;31(8):625–32.PubMedCrossRef Molloy J, Wolff LF, Lopez-Guzman A, Hodges JS. The association of periodontal disease parameters with systemic medical conditions and tobacco use. J Clin Periodontol. 2004;31(8):625–32.PubMedCrossRef
3.
go back to reference Cheng Z, Meade J, Mankia K, Emery P, Devine DA. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31(1):19–30.PubMedCrossRef Cheng Z, Meade J, Mankia K, Emery P, Devine DA. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31(1):19–30.PubMedCrossRef
4.
go back to reference Heredia PA, Lafaurie GI, Bautista-Molano W, et al. Predictive factors related to the progression of periodontal disease in patients with early rheumatoid arthritis: a cohort study. BMC Oral Health. 2019;19(1):240.CrossRef Heredia PA, Lafaurie GI, Bautista-Molano W, et al. Predictive factors related to the progression of periodontal disease in patients with early rheumatoid arthritis: a cohort study. BMC Oral Health. 2019;19(1):240.CrossRef
5.
go back to reference Loutan L, Alpizar-Rodriguez D, Courvoisier DS, Finckh A, Mombelli A, Giannopoulou C. Periodontal status correlates with anti-citrullinated protein antibodies in first-degree relatives of individuals with rheumatoid arthritis. J Clin Periodontol. 2019;46(7):690–8.PubMed Loutan L, Alpizar-Rodriguez D, Courvoisier DS, Finckh A, Mombelli A, Giannopoulou C. Periodontal status correlates with anti-citrullinated protein antibodies in first-degree relatives of individuals with rheumatoid arthritis. J Clin Periodontol. 2019;46(7):690–8.PubMed
7.
go back to reference Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol. 2013;40(Suppl 14):S8–19.PubMed Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol. 2013;40(Suppl 14):S8–19.PubMed
8.
go back to reference Tsioufis C, Kasiakogias A, Thomopoulos C, Stefanadis C. Periodontitis and blood pressure: the concept of dental hypertension. Atherosclerosis. 2011;219(1):1–9.PubMedCrossRef Tsioufis C, Kasiakogias A, Thomopoulos C, Stefanadis C. Periodontitis and blood pressure: the concept of dental hypertension. Atherosclerosis. 2011;219(1):1–9.PubMedCrossRef
9.
go back to reference Mashalkar VN, Suragimath G, Zope SA, Varma SA. A cross-sectional study to assess and correlate osteoporosis and periodontitis among postmenopausal women: a dual energy X-ray absorptiometry study. J Midlife Health. 2018;9(1):2–7.PubMedPubMedCentral Mashalkar VN, Suragimath G, Zope SA, Varma SA. A cross-sectional study to assess and correlate osteoporosis and periodontitis among postmenopausal women: a dual energy X-ray absorptiometry study. J Midlife Health. 2018;9(1):2–7.PubMedPubMedCentral
10.
go back to reference Yamada J, Amar S, Petrungaro P. Psoriasis-associated periodontitis: a case report. J Periodontol. 1992;63(10):854–7.PubMedCrossRef Yamada J, Amar S, Petrungaro P. Psoriasis-associated periodontitis: a case report. J Periodontol. 1992;63(10):854–7.PubMedCrossRef
11.
12.
go back to reference Hobbins S, Chapple IL, Sapey E, Stockley RA. Is periodontitis a comorbidity of COPD or can associations be explained by shared risk factors/behaviors? Int J Chron Obstruct Pulmon Dis. 2017;12:1339–49.PubMedPubMedCentralCrossRef Hobbins S, Chapple IL, Sapey E, Stockley RA. Is periodontitis a comorbidity of COPD or can associations be explained by shared risk factors/behaviors? Int J Chron Obstruct Pulmon Dis. 2017;12:1339–49.PubMedPubMedCentralCrossRef
13.
go back to reference Radnai M, Gorzo I, Nagy E, Urban E, Novak T, Pal A. A possible association between preterm birth and early periodontitis. A pilot study. J Clin Periodontol. 2004;31(9):736–41.PubMedCrossRef Radnai M, Gorzo I, Nagy E, Urban E, Novak T, Pal A. A possible association between preterm birth and early periodontitis. A pilot study. J Clin Periodontol. 2004;31(9):736–41.PubMedCrossRef
14.
go back to reference Marakoglu I, Gursoy UK, Marakoglu K, Cakmak H, Ataoglu T. Periodontitis as a risk factor for preterm low birth weight. Yonsei Med J. 2008;49(2):200–3.PubMedPubMedCentralCrossRef Marakoglu I, Gursoy UK, Marakoglu K, Cakmak H, Ataoglu T. Periodontitis as a risk factor for preterm low birth weight. Yonsei Med J. 2008;49(2):200–3.PubMedPubMedCentralCrossRef
15.
go back to reference Battancs E, Gorzo I, Pal A, et al. Pregnant women's oral hygiene knowledge and habits after the second millennium in South-East Hungary. Fogorv Sz. 2011;104(3):75–9.PubMed Battancs E, Gorzo I, Pal A, et al. Pregnant women's oral hygiene knowledge and habits after the second millennium in South-East Hungary. Fogorv Sz. 2011;104(3):75–9.PubMed
16.
go back to reference Fernandes JK, Wiegand RE, Salinas CF, et al. Periodontal disease status in gullah african americans with type 2 diabetes living in South Carolina. J Periodontol. 2009;80(7):1062–8.PubMedPubMedCentralCrossRef Fernandes JK, Wiegand RE, Salinas CF, et al. Periodontal disease status in gullah african americans with type 2 diabetes living in South Carolina. J Periodontol. 2009;80(7):1062–8.PubMedPubMedCentralCrossRef
17.
go back to reference Seymour GJ, Powell RN, Davies WI. The immunopathogenesis of progressive chronic inflammatory periodontal disease. J Oral Pathol. 1979;8(5):249–65.PubMedCrossRef Seymour GJ, Powell RN, Davies WI. The immunopathogenesis of progressive chronic inflammatory periodontal disease. J Oral Pathol. 1979;8(5):249–65.PubMedCrossRef
18.
go back to reference Hirschfeld J, Howait M, Movila A, et al. Assessment of the involvement of the macrophage migration inhibitory factor-glucocorticoid regulatory dyad in the expression of matrix metalloproteinase-2 during periodontitis. Eur J Oral Sci. 2017;125(5):345–54.PubMedPubMedCentralCrossRef Hirschfeld J, Howait M, Movila A, et al. Assessment of the involvement of the macrophage migration inhibitory factor-glucocorticoid regulatory dyad in the expression of matrix metalloproteinase-2 during periodontitis. Eur J Oral Sci. 2017;125(5):345–54.PubMedPubMedCentralCrossRef
19.
go back to reference Kalakonda B, Koppolu P, Baroudi K, Mishra A. Periodontal systemic connections-novel associations-a review of the evidence with implications for medical practitioners. Int J Health Sci (Qassim). 2016;10(2):293–307. Kalakonda B, Koppolu P, Baroudi K, Mishra A. Periodontal systemic connections-novel associations-a review of the evidence with implications for medical practitioners. Int J Health Sci (Qassim). 2016;10(2):293–307.
21.
go back to reference Pham MN, Hawa MI, Pfleger C, et al. Pro- and anti-inflammatory cytokines in latent autoimmune diabetes in adults, type 1 and type 2 diabetes patients: action LADA 4. Diabetologia. 2011;54(7):1630–8.PubMedCrossRef Pham MN, Hawa MI, Pfleger C, et al. Pro- and anti-inflammatory cytokines in latent autoimmune diabetes in adults, type 1 and type 2 diabetes patients: action LADA 4. Diabetologia. 2011;54(7):1630–8.PubMedCrossRef
22.
go back to reference The Emerging Risk Factors Collaboration, Sarwar N, Gao P, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375(9733):2215–22. The Emerging Risk Factors Collaboration, Sarwar N, Gao P, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375(9733):2215–22.
23.
go back to reference Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care. 1993;16(1):329–34. Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care. 1993;16(1):329–34.
24.
go back to reference Graziani F, Gennai S, Solini A, Petrini M. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes an update of the EFP-AAP review. J Clin Periodontol. 2018;45(2):167–87.PubMedCrossRef Graziani F, Gennai S, Solini A, Petrini M. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes an update of the EFP-AAP review. J Clin Periodontol. 2018;45(2):167–87.PubMedCrossRef
25.
go back to reference Baeza M, Morales A, Cisterna C, et al. Effect of periodontal treatment in patients with periodontitis and diabetes: systematic review and meta-analysis. J Appl Oral Sci. 2020;28:e20190248.PubMedCrossRef Baeza M, Morales A, Cisterna C, et al. Effect of periodontal treatment in patients with periodontitis and diabetes: systematic review and meta-analysis. J Appl Oral Sci. 2020;28:e20190248.PubMedCrossRef
26.
go back to reference Mataftsi M, Koukos G, Sakellari D. Prevalence of undiagnosed diabetes and pre-diabetes in chronic periodontitis patients assessed by an HbA1c chairside screening protocol. Clin Oral Investig. 2019;23(12):4365–70.PubMedCrossRef Mataftsi M, Koukos G, Sakellari D. Prevalence of undiagnosed diabetes and pre-diabetes in chronic periodontitis patients assessed by an HbA1c chairside screening protocol. Clin Oral Investig. 2019;23(12):4365–70.PubMedCrossRef
27.
go back to reference Lappin DF, Eapen B, Robertson D, Young J, Hodge PJ. Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus. J Clin Periodontol. 2009;36(8):634–41.PubMedCrossRef Lappin DF, Eapen B, Robertson D, Young J, Hodge PJ. Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus. J Clin Periodontol. 2009;36(8):634–41.PubMedCrossRef
28.
go back to reference Salvi GE, Franco LM, Braun TM, et al. Pro-inflammatory biomarkers during experimental gingivitis in patients with type 1 diabetes mellitus: a proof-of-concept study. J Clin Periodontol. 2010;37(1):9–16.PubMedCrossRef Salvi GE, Franco LM, Braun TM, et al. Pro-inflammatory biomarkers during experimental gingivitis in patients with type 1 diabetes mellitus: a proof-of-concept study. J Clin Periodontol. 2010;37(1):9–16.PubMedCrossRef
29.
go back to reference Sanz M, Ceriello A, Buysschaert M, et al. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol. 2018;45(2):138–49.PubMedCrossRef Sanz M, Ceriello A, Buysschaert M, et al. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol. 2018;45(2):138–49.PubMedCrossRef
30.
go back to reference Lim LP, Tay FB, Sum CF, Thai AC. Relationship between markers of metabolic control and inflammation on severity of periodontal disease in patients with diabetes mellitus. J Clin Periodontol. 2007;34(2):118–23.PubMedCrossRef Lim LP, Tay FB, Sum CF, Thai AC. Relationship between markers of metabolic control and inflammation on severity of periodontal disease in patients with diabetes mellitus. J Clin Periodontol. 2007;34(2):118–23.PubMedCrossRef
31.
go back to reference Taboza ZA, Costa KL, Silveira VR, et al. Periodontitis, edentulism and glycemic control in patients with type 2 diabetes: a cross-sectional study. BMJ Open Diabetes Res Care. 2018;6(1):e000453.PubMedPubMedCentralCrossRef Taboza ZA, Costa KL, Silveira VR, et al. Periodontitis, edentulism and glycemic control in patients with type 2 diabetes: a cross-sectional study. BMJ Open Diabetes Res Care. 2018;6(1):e000453.PubMedPubMedCentralCrossRef
32.
go back to reference Lalla E, Cheng B, Lal S, et al. Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol. 2007;34(4):294–8.PubMedCrossRef Lalla E, Cheng B, Lal S, et al. Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol. 2007;34(4):294–8.PubMedCrossRef
33.
go back to reference Hodge PJ, Robertson D, Paterson K, Smith GL, Creanor S, Sherriff A. Periodontitis in non-smoking type 1 diabetic adults: a cross-sectional study. J Clin Periodontol. 2012;39(1):20–9.PubMedCrossRef Hodge PJ, Robertson D, Paterson K, Smith GL, Creanor S, Sherriff A. Periodontitis in non-smoking type 1 diabetic adults: a cross-sectional study. J Clin Periodontol. 2012;39(1):20–9.PubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference Garcia D, Tarima S, Okunseri C. Periodontitis and glycemic control in diabetes: NHANES 2009 to 2012. J Periodontol. 2015;86(4):499–506.PubMedCrossRef Garcia D, Tarima S, Okunseri C. Periodontitis and glycemic control in diabetes: NHANES 2009 to 2012. J Periodontol. 2015;86(4):499–506.PubMedCrossRef
36.
go back to reference Kim EK, Lee SG, Choi YH, et al. Association between diabetes-related factors and clinical periodontal parameters in type-2 diabetes mellitus. BMC Oral Health. 2013;13:64.PubMedPubMedCentralCrossRef Kim EK, Lee SG, Choi YH, et al. Association between diabetes-related factors and clinical periodontal parameters in type-2 diabetes mellitus. BMC Oral Health. 2013;13:64.PubMedPubMedCentralCrossRef
37.
go back to reference Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21–31.PubMedCrossRef Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21–31.PubMedCrossRef
38.
go back to reference Casanova L, Hughes FJ, Preshaw PM. Diabetes and periodontal disease: a two-way relationship. Br Dent J. 2014;217(8):433–7.PubMedCrossRef Casanova L, Hughes FJ, Preshaw PM. Diabetes and periodontal disease: a two-way relationship. Br Dent J. 2014;217(8):433–7.PubMedCrossRef
39.
go back to reference Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol. 2001;6(1):99–112.PubMedCrossRef Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol. 2001;6(1):99–112.PubMedCrossRef
40.
go back to reference Correa FO, Goncalves D, Figueredo CM, Bastos AS, Gustafsson A, Orrico SR. Effect of periodontal treatment on metabolic control, systemic inflammation and cytokines in patients with type 2 diabetes. J Clin Periodontol. 2010;37(1):53–8.PubMedCrossRef Correa FO, Goncalves D, Figueredo CM, Bastos AS, Gustafsson A, Orrico SR. Effect of periodontal treatment on metabolic control, systemic inflammation and cytokines in patients with type 2 diabetes. J Clin Periodontol. 2010;37(1):53–8.PubMedCrossRef
41.
go back to reference Engebretson S, Kocher T. Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Clin Periodontol. 2013;40(Suppl 14):S153–S163163.PubMed Engebretson S, Kocher T. Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Clin Periodontol. 2013;40(Suppl 14):S153–S163163.PubMed
42.
go back to reference Koromantzos PA, Makrilakis K, Dereka X, Katsilambros N, Vrotsos IA, Madianos PN. A randomized, controlled trial on the effect of non-surgical periodontal therapy in patients with type 2 diabetes. Part I: effect on periodontal status and glycaemic control. J Clin Periodontol. 2011;38(2):142–7. Koromantzos PA, Makrilakis K, Dereka X, Katsilambros N, Vrotsos IA, Madianos PN. A randomized, controlled trial on the effect of non-surgical periodontal therapy in patients with type 2 diabetes. Part I: effect on periodontal status and glycaemic control. J Clin Periodontol. 2011;38(2):142–7.
43.
go back to reference Quintero AJ, Chaparro A, Quirynen M, et al. Effect of two periodontal treatment modalities in patients with uncontrolled type 2 diabetes mellitus: a randomized clinical trial. J Clin Periodontol. 2018;45(9):1098–106.PubMedCrossRef Quintero AJ, Chaparro A, Quirynen M, et al. Effect of two periodontal treatment modalities in patients with uncontrolled type 2 diabetes mellitus: a randomized clinical trial. J Clin Periodontol. 2018;45(9):1098–106.PubMedCrossRef
44.
go back to reference Kocher T, Holtfreter B, Petersmann A, et al. Effect of periodontal treatment on HbA1c among patients with prediabetes. J Dent Res. 2019;98(2):171–9.PubMedCrossRef Kocher T, Holtfreter B, Petersmann A, et al. Effect of periodontal treatment on HbA1c among patients with prediabetes. J Dent Res. 2019;98(2):171–9.PubMedCrossRef
45.
go back to reference Parker DR, Fallone D, Martin RA, et al. The relation between smoking status and medical conditions among incarcerated adults. J Addict Med. 2014;8(2):90–5.PubMedPubMedCentralCrossRef Parker DR, Fallone D, Martin RA, et al. The relation between smoking status and medical conditions among incarcerated adults. J Addict Med. 2014;8(2):90–5.PubMedPubMedCentralCrossRef
46.
go back to reference Heydarpour P, Manouchehrinia A, Beiki O, et al. Smoking and worsening disability in multiple sclerosis: a meta-analysis. Acta Neurol Scand. 2018;138(1):62–9.PubMedCrossRef Heydarpour P, Manouchehrinia A, Beiki O, et al. Smoking and worsening disability in multiple sclerosis: a meta-analysis. Acta Neurol Scand. 2018;138(1):62–9.PubMedCrossRef
47.
go back to reference Fagard RH, Nilsson PM. Smoking and diabetes—the double health hazard! Prim Care Diabetes. 2009;3(4):205–9.PubMedCrossRef Fagard RH, Nilsson PM. Smoking and diabetes—the double health hazard! Prim Care Diabetes. 2009;3(4):205–9.PubMedCrossRef
48.
go back to reference Cignarelli M, Lamacchia O, Di Paolo S, Gesualdo L. Cigarette smoking and kidney dysfunction in diabetes mellitus. J Nephrol. 2008;21(2):180–9.PubMed Cignarelli M, Lamacchia O, Di Paolo S, Gesualdo L. Cigarette smoking and kidney dysfunction in diabetes mellitus. J Nephrol. 2008;21(2):180–9.PubMed
49.
go back to reference Obradovic R, Kesic LJ, Gasic J, Petrovic M, Zivkovic N. Role of smoking in periodontal disease among diabetic patients. West Indian Med J. 2012;61(1):98–101.PubMed Obradovic R, Kesic LJ, Gasic J, Petrovic M, Zivkovic N. Role of smoking in periodontal disease among diabetic patients. West Indian Med J. 2012;61(1):98–101.PubMed
50.
go back to reference Gupta N, Gupta ND, Garg S, et al. The effect of type 2 diabetes mellitus and smoking on periodontal parameters and salivary matrix metalloproteinase-8 levels. J Oral Sci. 2016;58(1):1–6.PubMedCrossRef Gupta N, Gupta ND, Garg S, et al. The effect of type 2 diabetes mellitus and smoking on periodontal parameters and salivary matrix metalloproteinase-8 levels. J Oral Sci. 2016;58(1):1–6.PubMedCrossRef
51.
go back to reference Orbak R, Tezel A, Canakci V, Demir T. The influence of smoking and non-insulin-dependent diabetes mellitus on periodontal disease. J Int Med Res. 2002;30(2):116–25.PubMedCrossRef Orbak R, Tezel A, Canakci V, Demir T. The influence of smoking and non-insulin-dependent diabetes mellitus on periodontal disease. J Int Med Res. 2002;30(2):116–25.PubMedCrossRef
52.
go back to reference Javed F, Al-Kheraif AA, Salazar-Lazo K, et al. Periodontal inflammatory conditions among smokers and never-smokers with and without type 2 diabetes mellitus. J Periodontol. 2015;86(7):839–46.PubMedCrossRef Javed F, Al-Kheraif AA, Salazar-Lazo K, et al. Periodontal inflammatory conditions among smokers and never-smokers with and without type 2 diabetes mellitus. J Periodontol. 2015;86(7):839–46.PubMedCrossRef
53.
go back to reference Antal M, Battancs E, Bocskai M, Braunitzer G, Kovacs L. An observation on the severity of periodontal disease in past cigarette smokers suffering from rheumatoid arthritis- evidence for a long-term effect of cigarette smoke exposure? BMC Oral Health. 2018;18(1):82.PubMedPubMedCentralCrossRef Antal M, Battancs E, Bocskai M, Braunitzer G, Kovacs L. An observation on the severity of periodontal disease in past cigarette smokers suffering from rheumatoid arthritis- evidence for a long-term effect of cigarette smoke exposure? BMC Oral Health. 2018;18(1):82.PubMedPubMedCentralCrossRef
54.
go back to reference Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000. 2013;62(1):59–94. Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000. 2013;62(1):59–94.
55.
56.
go back to reference Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91.PubMedCrossRef Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91.PubMedCrossRef
57.
go back to reference American DA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2011;34(Suppl 1):S62–S69.CrossRef American DA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2011;34(Suppl 1):S62–S69.CrossRef
58.
go back to reference Lin CY, Chen F, Hariri A, et al. Photoacoustic imaging for noninvasive periodontal probing depth measurements. J Dent Res. 2018;97(1):23–30.PubMedCrossRef Lin CY, Chen F, Hariri A, et al. Photoacoustic imaging for noninvasive periodontal probing depth measurements. J Dent Res. 2018;97(1):23–30.PubMedCrossRef
59.
60.
go back to reference Souto MLS, Rovai ES, Ganhito JA, Holzhausen M, Chambrone L, Pannuti CM. Efficacy of systemic antibiotics in nonsurgical periodontal therapy for diabetic subjects: a systematic review and meta-analysis. Int Dent J. 2018;68(4):207–20.PubMedCrossRef Souto MLS, Rovai ES, Ganhito JA, Holzhausen M, Chambrone L, Pannuti CM. Efficacy of systemic antibiotics in nonsurgical periodontal therapy for diabetic subjects: a systematic review and meta-analysis. Int Dent J. 2018;68(4):207–20.PubMedCrossRef
61.
go back to reference Nibali L, Krajewski A, Donos N, et al. The effect of furcation involvement on tooth loss in a population without regular periodontal therapy. J Clin Periodontol. 2017;44(8):813–21.PubMedCrossRef Nibali L, Krajewski A, Donos N, et al. The effect of furcation involvement on tooth loss in a population without regular periodontal therapy. J Clin Periodontol. 2017;44(8):813–21.PubMedCrossRef
63.
64.
go back to reference Leite FRM, Nascimento GG, Scheutz F, Lopez R. Effect of smoking on periodontitis: a systematic review and meta-regression. Am J Prev Med. 2018;54(6):831–41.PubMedCrossRef Leite FRM, Nascimento GG, Scheutz F, Lopez R. Effect of smoking on periodontitis: a systematic review and meta-regression. Am J Prev Med. 2018;54(6):831–41.PubMedCrossRef
66.
go back to reference Abdullah A, Peeters A, de Courten M, Stoelwinder J. The magnitude of association between overweight and obesity and the risk of diabetes: a meta-analysis of prospective cohort studies. Diabetes Res Clin Pract. 2010;89(3):309–19.PubMedCrossRef Abdullah A, Peeters A, de Courten M, Stoelwinder J. The magnitude of association between overweight and obesity and the risk of diabetes: a meta-analysis of prospective cohort studies. Diabetes Res Clin Pract. 2010;89(3):309–19.PubMedCrossRef
67.
go back to reference Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol. 2013;40(Suppl 14):S113–S134.PubMed Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol. 2013;40(Suppl 14):S113–S134.PubMed
68.
go back to reference Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jane-Salas E, Lopez-Lopez J, Vinas M. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: a randomized controlled trial. J Clin Periodontol. 2018;45(3):345–53.PubMedCrossRef Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jane-Salas E, Lopez-Lopez J, Vinas M. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: a randomized controlled trial. J Clin Periodontol. 2018;45(3):345–53.PubMedCrossRef
69.
go back to reference World Health Organization. Use of glycated haemoglobin (HbA1c) in the diagnosis of diabetes mellitus. Abbreviated report of a WHO consultation. Geneva: World Health Organization; 2011. World Health Organization. Use of glycated haemoglobin (HbA1c) in the diagnosis of diabetes mellitus. Abbreviated report of a WHO consultation. Geneva: World Health Organization; 2011.
Metadata
Title
Periodontal Disease in Diabetes Mellitus: A Case–Control Study in Smokers and Non-Smokers
Authors
Emese Battancs
Dorottya Gheorghita
Szabolcs Nyiraty
Csaba Lengyel
Gabriella Eördegh
Zoltán Baráth
Tamás Várkonyi
Márk Antal
Publication date
01-11-2020
Publisher
Springer Healthcare
Published in
Diabetes Therapy / Issue 11/2020
Print ISSN: 1869-6953
Electronic ISSN: 1869-6961
DOI
https://doi.org/10.1007/s13300-020-00933-8

Other articles of this Issue 11/2020

Diabetes Therapy 11/2020 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.