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Association between Periodontitis and Hyperglycemia

Associação entre Periodontite e Hiperglicemia

ABSTRACT

Objective:

The objective of this study was to analyze the prevalence of undiagnosed hyperglycemia in individuals with periodontitis.

Methods:

The sample was composed of randomly selected individuals that had signed-up for treatment at the Newton Paiva University dental clinic. The volunteers were divided in two groups, the first composed by individuals without periodontitis (n = 30) and the second by individuals with periodontitis (n = 20). All participants answered a questionnaire about habits and overall health condition. Salivary flow was quantified and periodontal examination evaluated bleeding when probed, probing depth and clinical attachment level. Through laboratory tests, the fasting glucose and the glycated hemoglobin levels were quantified.

Results:

In the sample studied a higher percentage of individuals with hyperglycemia among those with periodontitis than those without periodontitis was identified.

Conclusion:

It is suggested, therefore, that the request of laboratory tests to check glucose levels becomes a part of the dental treatment protocol of individuals with periodontitis.

Indexing terms:
Complications; Diabetes Mellitus; Periodontitis

RESUMO

Objetivo:

O objetivo desse estudo foi analisar a prevalência de hiperglicemia não diagnosticada em indivíduos com periodontite.

Métodos:

A amostra foi composta por indivíduos selecionados aleatoriamente que se inscreveram para tratamento no Curso de Odontologia do Centro Universitário Newton Paiva, Belo Horizonte, Minas Gerais. A amostra foi dividida em dois grupos, o dos indivíduos sem periodontite (n=30) e o dos indivíduos com periodontite (n=20). Todos responderam a um questionário sobre hábitos e condição de saúde geral. Também tiveram o fluxo salivar quantificado e passaram por um exame periodontal para avaliação do sangramento gengival, da profundidade de sondagem e do nível de inserção clínica. Através de exames laboratoriais, quantificou-se a glicemia em jejum e os níveis de hemoglobina glicada.

Resultados:

Na amostra estudada foi identificado maior percentual de indivíduos com hiperglicemia no grupo com periodontite do que no grupo sem periodontite.

Conclusão:

Sugere-se, portanto, que a solicitação de exames laboratoriais para avaliação dos níveis glicêmicos faça parte do protocolo odontológico de atendimento dos indivíduos com periodontite.

Termos de indexação:
Complicações; Diabetes Mellitus; Periodontite

INTRODUCTION

Diabetes Mellitus (DM) constitutes of a group of alterations characterized by hyperglycemia, resulting from the deficiency of production and/or resistance to the role of insulin [11 Chávarry NGM, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive disease: a meta-analysis. Oral Health Prev Dent. 2009;7:107-127.]. It represents one of the main public health problems, being the fourth cause of death in Brazil [22 Pace AE, Nunes PD, Ochoa-vigo K. O conhecimento dos familiares acerca da problemática do portador de diabetes mellitus. Rev Lat-am Enf. 2003;11(3):312-9.]. DM is classified, according to its etiopathogeny, in type 1 DM, type 2 DM, gestational DM and other specific types [33 American Diabetes Association. Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2014; 37(1):81-90. doi: 10.2337/dc10-S062.
https://doi.org/10.2337/dc10-S062...
].

According to the World Health Organization, the average prevalence of DM worldwide is of 10% [44 World Health Organization. Diabetes. Geneva: World Health Organization; 2014.]. In Brazil, nearly five million individuals are diabetic, having an expectancy of a 50% increase to that number by 2025 [55 Moreira PL, Dupas G. Vivendo com diabetes: a experiência contada pela criança. Rev Lat-am Enf. 2006;14(1):25-32.]. According to studies made by the Ministry of Health, the total number of individuals with the disease increased 40% between 2006 and 2012 [66 Brasil. Ministério da Saúde. Vigitel Brasil 2012: vigilância de fatores de risco e proteção para doenças crônicas por inquérito telefônico. 2013 [citado 2017 Set 15]. Disponível em: <http://bvsms.saude.gov.br/bvs/publicacoes/vigitel_brasil_2012_vigilancia_risco.pdf>.
http://bvsms.saude.gov.br/bvs/publicacoe...
]. Around the world, nearly 4 million deaths per year are directly related to DM, since it also favors the worsening of systemic diseases [77 Barnes VM, Kennedy AD, Panagakos F, Devizio W, Trivedi HM, Jönsson T, et al. Global Metabolomic analysis of human saliva and plasma from healthy and diabetic subjects, with and without periodontal disease. PLoS One. 2014;9(8):1051-81. doi: 10.1371/journal.pone.0105181
https://doi.org/10.1371/journal.pone.010...
,88 Weidlich P. Association between periodontal diseases and systemic diseases. Braz Oral Res. 2008;22(11):32-43. doi: 10.1590/S1806-83242008000500006
https://doi.org/10.1590/S1806-8324200800...
].

Hyperglycemia contributes for the development of classic complications associated to DM, such as visual changes, nephropathies, cardiovascular diseases, neuropathies, susceptibility to infections and periodontitis [33 American Diabetes Association. Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2014; 37(1):81-90. doi: 10.2337/dc10-S062.
https://doi.org/10.2337/dc10-S062...
].

Immune-inflammatory alterations present in diabetic individuals increase the susceptibility of developing periodontitis, inflammatory disease that affects the supporting tissues of the teeth, being considered the sixth classic complication of DM. Epidemiological studies have emphasized that DM is a risk factor for periodontitis, increasing its probability of occurring by three times [99 Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis - impact on periodontal pathosis. Periodontol 2000. 2007;45(1):128-137. doi: 10.1111/j.1600-0757.2007.00219.x
https://doi.org/10.1111/j.1600-0757.2007...
,1010 Preshaw PM, Alba AL, Herrea D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: a two-way relationsheep. Diabetologia. 2012;55(1):21-31. doi: 10.1007/s00125-011-2342-y
https://doi.org/10.1007/s00125-011-2342-...
]. DM is also associated with greater severity of periodontitis [1111 Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000. 2000;23(1):50-62. doi: 10.1034/j.1600-0757.2000.2230104.x
https://doi.org/10.1034/j.1600-0757.2000...
]. The immune-inflammatory process resulting from the bacterial aggression, is the main responsible for the damage observed on the periodontal tissues, clinically characterized by bleeding to probing (BP), increase in probing depth (PD) and insertion loss, followed by bone tissue destruction. The evolution of periodontitis may eventually lead to loss of the dental element [1212 Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS. Advances in the pathogenesis of periodontitis: summary of developments, clinical implication and future directions. Periodontol 2000. 1997;14(1):216-248. doi: 10.1111/j.1600-0757.1997.tb00199.x
https://doi.org/10.1111/j.1600-0757.1997...
,1313 Kinane DF. Causation and pathogenesis of periodontal disease. Periodontol 2000. 2001;25:8-20. doi.: 10.1034/j.1600-0757.2001.22250102.x
https://doi.org/10.1034/j.1600-0757.2001...
].

The present study aims to evaluate the prevalence of hyperglycemia not yet diagnosed in individuals with periodontitis.

METHODS

Sample

The convenience sample was composed by 50 randomly selected individuals from those that had signed up for dental treatment at the Newton Paiva University Center dentistry course, between the months of August and November 2015. The individuals were subdivided into two groups: without periodontitis (n=30) and with periodontitis (n=20). All the participants were informed about the objectives of the study and were only included as part of the study after manifesting interests by signing an informed consent form (ICF).

The inclusion factors were the presence of a minimum of 12 teeth, 18 years of age or older and absence of any contraindication for periodontal examination. Any individuals previously diagnosed with DM, submitted to antibiotic therapy or periodontal therapy during the last three months and carriers of the acquired immune deficiency syndrome (AIDS), were excluded.

The study was previously submitted and approved by the Ethics Committee under the number CAAE 37644314.6.0000.5097.

Behavioral and biological social characteristics

With a structured questionnaire, the following data were collected: gender, age, tobacco use, hypertension and family history of DM. The participants were also questioned about the presence of the following symptoms that are characteristic to DM: polydipsia, polyuria, polyphagia, unexplained wait loss and visual alteration.

Medical data

Weight and height of the participating individuals were registered to calculate the body mass index (BMI). According the BMI the individuals were classified as underweight (BMI below 18.5), normal weight (BMI between 18.5 and 24.9), overweight (BMI between 25.0 and 29.9) and obesity (BMI above 30.0) [44 World Health Organization. Diabetes. Geneva: World Health Organization; 2014.].

All the participants performed, at the same laboratory, the fasting glycaemia and glycated hemoglobin (A1c) exams. Glycaemia was considered altered for fasting glycaemia and glycated hemoglobin values above 99mg/dL and 5.6%, respectively [33 American Diabetes Association. Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2014; 37(1):81-90. doi: 10.2337/dc10-S062.
https://doi.org/10.2337/dc10-S062...
].

Sialometry

Sialometry was employed for quantitative analysis of resting and stimulated saliva. In order to collect the saliva the participants remained 30 minutes without eating or drinking and 2 minutes without performing any chewing, swallowing or talking movements. For resting and stimulated sialometry, the individuals collected, in a millimeter tube, all the saliva produced during 5 minutes. During the stimulated sialometry the individuals chewed on sialogogo. The quantity of saliva and foam produced was verified directly on the collector during the five minutes. The total volume collected was divided by 5, obtaining a result in mL/min. The participants were grouped, according to the obtained salivary flow, in normal (flow from 1.5 to 3.0 mL/min), hypossalivation (flow from 0.05 to 1.45 mL/min) and sialorrhea (flow above 3.0 mL/min) [1414 Conceição MD, Marocchio LS, Fagundes RL. Técnica de sialometria para uso na prática clínica diária. Rev Assoc Paul Cir Dent. 2006;60(5):350-354.].

Periodontal clinical examination

The periodontal exam was performed to analyze the clinical parameters of BP, PD and clinical attachment level (CAL) of all teeth present. Mesial, distal, buccal and lingual measurements were registered for each tooth. The periodontal exam was performed by two researchers (MTGO and PGSF), who were previously calibrated, using a millimeter probe, model UNC-15 North Carolina (Hu-Friedy, Chicago, USA).

The inability to determine the cementoenamel limit, presence of gingival morphology alteration, extensive carious lesion, iatrogenic restorative procedures or excess calculus that could difficult the periodontal exam were considered exclusion criteria for the teeth [1515 Costa FO, Cota LOM, Costa JE, Pordeus IA. Periodontal disease progression among young subjects with no preventive dental care: A 52-month follow-up study. J Periodontol. 2007;78(1):198-203. doi: 10.1590/S1806-83242010000200017
https://doi.org/10.1590/S1806-8324201000...
].

The bleeding exam was conducted while probing, by gently and carefully introducing the probe into the gingival sulcus until reaching its base. The bleeding was analyzed 30 to 60 seconds after probing. The occurrence of BP was registered for each surface in a dichotomy manner, indicating its presence or absence. The probing depth was obtained by measuring the distance from the gingival margin to the sulcus base or periodontal pocket. The CAL was determined by the distance between the cementoenamel junction and the periodontal sulcus or pocket base. The criteria used to diagnose periodontitis was the presence of four or more teeth with at least one site PD ≥ 4 mm and CAL ≥ 3 mm associated to BP at the same site [1616 Gomes-Filho IS, Cruz SS, Rezende EJC, dos Santos CAST, Soledade KR, Magalhaes MA, et al. Exposure measurement in the association between periodontal disease and prematurity/low birth weight. J Clin Periodontal. 2007;34(1):957-963. doi: 10.1111/j.1600-051X.2007.01141.x
https://doi.org/10.1111/j.1600-051X.2007...
].

Statistical analysis

The comparison between the groups for the variables of interest was performed by the Chi-square, Mann-Whitney and Fishers’ Exact tests when appropriate. The results were considered significant with a probability below 5% (p < 0.05). All the statistical analysis was made with SPSS program (version 17.0).

RESULTS

Table 1 presents the characterization of the sample in the groups with and without periodontitis. The groups were considered similar according to the majority of the evaluated criteria. Among the DM symptoms investigated, visual alteration was more frequently reported by the individuals with periodontitis. The individuals from the group with periodontitis had significantly higher average fasting glycaemia than the individuals without periodontitis. However, when fasting glycaemia was categorically measured the difference was not maintained. The same occurred with glycated hemoglobin, when evaluated quantitatively and categorically. The participants with periodontitis presented a 97.7 mg/dL average fasting glycaemia, while for the participants without periodontitis the average was 85.5 mg/dL.

Table 1
Characterization of the sample groups with and without periodontitis.

The characterization of the periodontal condition of the sample in the groups with and without periodontitis is presented in table 2. As expected, individuals with periodontitis presented greater percent of locations with altered PD and with BP, although the total number of teeth were similar between groups.

Table 2
Characterization of the periodontal condition in the groups with and without periodontitis.

When the sample was characterized considering the groups of patients with normal and altered fasting glycaemia (table 3), the individuals with altered fasting glycaemia presented greater PD, prevalence of periodontitis and lower amount of teeth present, although these differences were not statistically significant. The percent of sites with BP was statistically higher for the group with altered fasting glycaemia (p=0.007). For the analysis of the sample considering the groups of individuals with normal and altered glycated hemoglobin there was no statistically significant difference between the groups with regards to the evaluated periodontal parameters, with exception to the number of teeth which was significantly higher in the group of individuals with normal levels of glycated hemoglobin (table 4).

Table 3
Characterization of the periodontal condition of the sample for the groups with normal and altered fasting glycaemia.

Table 4
Characterization of the periodontal condition of the sample for the groups with normal and altered glycated hemoglobin.

DISCUSSION

DM is a prevalent condition with high rates of morbidity and mortality. Its early diagnosis can contribute to the reduction of associated diseases and an improvement in prognosis. The fact that DM presents, in the majority of cases, a chronic evolution makes it remain undiagnosed for a long period of time, until symptoms and classic complications manifest themselves [99 Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis - impact on periodontal pathosis. Periodontol 2000. 2007;45(1):128-137. doi: 10.1111/j.1600-0757.2007.00219.x
https://doi.org/10.1111/j.1600-0757.2007...
]. Periodontitis is a known complication to DM [1717 Matthews DC. The relationship between diabetes and periodontal disease. J Can Dent Assoc. 2002 Mar;68(3):161-4.,1818 Esteves Lima RP, Miranda Cota LO, Costa FO. Association between periodontitis and gestational diabetes mellitus: a case-control study. J Periodontol. 2013;84(1):1257-1265. doi: 10.1902/jop.2012.120350
https://doi.org/10.1902/jop.2012.120350...
] and can aid in the detection of undiagnosed hyperglycemia.

The results from the present study evidence that individuals with periodontitis present increased levels of blood glucose than individuals without periodontitis. Average fasting glycaemia values were higher for individuals with periodontitis when compared to individuals without periodontitis. Although there was no statistical significance, glycated hemoglobin levels were more elevated in individuals with periodontitis. The reduced sample size is a limitation to the study that can explain the difference among the statistical results for the fasting glycaemia and glycated hemoglobin exams. However, the two exams present high level of agreement and are indicated for diagnosis of hyperglycemia [33 American Diabetes Association. Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2014; 37(1):81-90. doi: 10.2337/dc10-S062.
https://doi.org/10.2337/dc10-S062...
].

Due to the multifactorial character of DM, scientific studies must consider the presence of confounding variables that could compromise the results. Increased age and high BMI, for example, are considered risk factors for DM [1919 Kahn SE, Cooper ME, Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet. 2014;383(1):1068-1083. doi: 10.1016/S0140-6736(13)62154-6
https://doi.org/10.1016/S0140-6736(13)62...
]. In this study, however, the individuals with and without periodontitis were considered to be similar with regards to age and BMI, which increases the credibility in the obtained results.

In contrast, smoking is a risk factor for periodontitis [2020 Warmakulasuriya S, Dietrich T, Bornstein MM, Casals Peidro E, Preshaw PM, Walter C, et al. Oral health risks of tobacco use and effects of cessation. Int Dent J. 2010;60(1):7-30. doi: 10.1922/IDJ_2532Warnakulasuriya24
https://doi.org/10.1922/IDJ_2532Warnakul...
]. The habit of smoking interferes on the pathogenesis of periodontitis by altering vascularization, immune-inflammatory response and homeostasis of the tissues, increasing the susceptibility to the disease and causing greater destruction of periodontal tissues [2121 Palmer RM, Wilson RF, Hansan AS, Scott DA. Mechanisms of action of environmental factors-tobacco smoking. J Clin Periodontol. 2005;32(1)180-195. doi: 10.1111/j.1600-051X.2005.00786.x
https://doi.org/10.1111/j.1600-051X.2005...
]. In the present study there was a greater prevalence of smokers in the group with periodontitis, although this difference was not statistically significant.

Additionally, DM is proved to be a risk factor for periodontitis. Immune and inflammatory system alterations are associated to the prevalence and increased severity of periodontitis in individuals with hyperglycemia. The neutrophils have reduced functioning, while monocytes and macrophages are found to be hyper reactive with increased production of proinflammatory cytocines [2222 Mealey BL, Oates TW. Diabetes mellitus and periodontal diseases. J Periodont. 2006;77:1289-1303. doi: 10.1902/jop.2006.050459
https://doi.org/10.1902/jop.2006.050459...
]. The results evidenced that the prevalence of periodontitis was bigger for individuals with increased glycemic levels, although not statistically significant. Again, the reduced sample size could have affected the identification of the statistical significance.

Even though periodontitis is the most prevalent DM oral complication, some studies have also shown a reduction to salivary flow in individuals with hyperglycemia [1717 Matthews DC. The relationship between diabetes and periodontal disease. J Can Dent Assoc. 2002 Mar;68(3):161-4.]. However, the elevated age that is a risk factor for diabetes must be considered because it may be associated to the reduction of salivary flow, which could difficult result interpretation [1919 Kahn SE, Cooper ME, Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet. 2014;383(1):1068-1083. doi: 10.1016/S0140-6736(13)62154-6
https://doi.org/10.1016/S0140-6736(13)62...
]. On the other hand, other studies have not identified salivary flow reduction among diabetic individuals. In the present study there was not salivary flow difference between groups with or without periodontitis.

CONCLUSION

Periodontitis is a classic complication of DM and its presence can help identify glycemic alterations not yet diagnosed. In the sample studied a greater prevalence of individuals with undiagnosed hyperglycemia in the group with periodontitis was identified. Therefor, dental appointments can be opportune moments to monitor periodontal patients’ glycemic levels. It is believed that periodontitis diagnosis can be an important indicator of the presence of hyperglycemia and a tool capable of identifying future candidate to develop DM. It is suggested, therefore, that the request of exams to evaluate glycemic levels becomes part of the dental appointment service protocol of individuals with periodontitis.

REFERENCES

  • 1
    Chávarry NGM, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive disease: a meta-analysis. Oral Health Prev Dent. 2009;7:107-127.
  • 2
    Pace AE, Nunes PD, Ochoa-vigo K. O conhecimento dos familiares acerca da problemática do portador de diabetes mellitus. Rev Lat-am Enf. 2003;11(3):312-9.
  • 3
    American Diabetes Association. Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2014; 37(1):81-90. doi: 10.2337/dc10-S062.
    » https://doi.org/10.2337/dc10-S062
  • 4
    World Health Organization. Diabetes. Geneva: World Health Organization; 2014.
  • 5
    Moreira PL, Dupas G. Vivendo com diabetes: a experiência contada pela criança. Rev Lat-am Enf. 2006;14(1):25-32.
  • 6
    Brasil. Ministério da Saúde. Vigitel Brasil 2012: vigilância de fatores de risco e proteção para doenças crônicas por inquérito telefônico. 2013 [citado 2017 Set 15]. Disponível em: <http://bvsms.saude.gov.br/bvs/publicacoes/vigitel_brasil_2012_vigilancia_risco.pdf>.
    » http://bvsms.saude.gov.br/bvs/publicacoes/vigitel_brasil_2012_vigilancia_risco.pdf
  • 7
    Barnes VM, Kennedy AD, Panagakos F, Devizio W, Trivedi HM, Jönsson T, et al. Global Metabolomic analysis of human saliva and plasma from healthy and diabetic subjects, with and without periodontal disease. PLoS One. 2014;9(8):1051-81. doi: 10.1371/journal.pone.0105181
    » https://doi.org/10.1371/journal.pone.0105181
  • 8
    Weidlich P. Association between periodontal diseases and systemic diseases. Braz Oral Res. 2008;22(11):32-43. doi: 10.1590/S1806-83242008000500006
    » https://doi.org/10.1590/S1806-83242008000500006
  • 9
    Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis - impact on periodontal pathosis. Periodontol 2000. 2007;45(1):128-137. doi: 10.1111/j.1600-0757.2007.00219.x
    » https://doi.org/10.1111/j.1600-0757.2007.00219.x
  • 10
    Preshaw PM, Alba AL, Herrea D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: a two-way relationsheep. Diabetologia. 2012;55(1):21-31. doi: 10.1007/s00125-011-2342-y
    » https://doi.org/10.1007/s00125-011-2342-y
  • 11
    Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000. 2000;23(1):50-62. doi: 10.1034/j.1600-0757.2000.2230104.x
    » https://doi.org/10.1034/j.1600-0757.2000.2230104.x
  • 12
    Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS. Advances in the pathogenesis of periodontitis: summary of developments, clinical implication and future directions. Periodontol 2000. 1997;14(1):216-248. doi: 10.1111/j.1600-0757.1997.tb00199.x
    » https://doi.org/10.1111/j.1600-0757.1997.tb00199.x
  • 13
    Kinane DF. Causation and pathogenesis of periodontal disease. Periodontol 2000. 2001;25:8-20. doi.: 10.1034/j.1600-0757.2001.22250102.x
    » https://doi.org/10.1034/j.1600-0757.2001.22250102.x
  • 14
    Conceição MD, Marocchio LS, Fagundes RL. Técnica de sialometria para uso na prática clínica diária. Rev Assoc Paul Cir Dent. 2006;60(5):350-354.
  • 15
    Costa FO, Cota LOM, Costa JE, Pordeus IA. Periodontal disease progression among young subjects with no preventive dental care: A 52-month follow-up study. J Periodontol. 2007;78(1):198-203. doi: 10.1590/S1806-83242010000200017
    » https://doi.org/10.1590/S1806-83242010000200017
  • 16
    Gomes-Filho IS, Cruz SS, Rezende EJC, dos Santos CAST, Soledade KR, Magalhaes MA, et al. Exposure measurement in the association between periodontal disease and prematurity/low birth weight. J Clin Periodontal. 2007;34(1):957-963. doi: 10.1111/j.1600-051X.2007.01141.x
    » https://doi.org/10.1111/j.1600-051X.2007.01141.x
  • 17
    Matthews DC. The relationship between diabetes and periodontal disease. J Can Dent Assoc. 2002 Mar;68(3):161-4.
  • 18
    Esteves Lima RP, Miranda Cota LO, Costa FO. Association between periodontitis and gestational diabetes mellitus: a case-control study. J Periodontol. 2013;84(1):1257-1265. doi: 10.1902/jop.2012.120350
    » https://doi.org/10.1902/jop.2012.120350
  • 19
    Kahn SE, Cooper ME, Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet. 2014;383(1):1068-1083. doi: 10.1016/S0140-6736(13)62154-6
    » https://doi.org/10.1016/S0140-6736(13)62154-6
  • 20
    Warmakulasuriya S, Dietrich T, Bornstein MM, Casals Peidro E, Preshaw PM, Walter C, et al. Oral health risks of tobacco use and effects of cessation. Int Dent J. 2010;60(1):7-30. doi: 10.1922/IDJ_2532Warnakulasuriya24
    » https://doi.org/10.1922/IDJ_2532Warnakulasuriya24
  • 21
    Palmer RM, Wilson RF, Hansan AS, Scott DA. Mechanisms of action of environmental factors-tobacco smoking. J Clin Periodontol. 2005;32(1)180-195. doi: 10.1111/j.1600-051X.2005.00786.x
    » https://doi.org/10.1111/j.1600-051X.2005.00786.x
  • 22
    Mealey BL, Oates TW. Diabetes mellitus and periodontal diseases. J Periodont. 2006;77:1289-1303. doi: 10.1902/jop.2006.050459
    » https://doi.org/10.1902/jop.2006.050459

Publication Dates

  • Publication in this collection
    Sept 2018

History

  • Received
    10 Aug 2017
  • Reviewed
    12 Sept 2017
  • Accepted
    07 Nov 2017
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