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Published in: BMC Oral Health 1/2015

Open Access 01-12-2015 | Research article

Influence of type 2 diabetes on local production of inflammatory molecules in adults with and without chronic periodontitis: a cross-sectional study

Authors: Hasaan G. Mohamed, Shaza B. Idris, Mutaz F. Ahmed, Anne N. Åstrøm, Kamal Mustafa, Salah O. Ibrahim, Manal Mustafa

Published in: BMC Oral Health | Issue 1/2015

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Abstract

Background

Pathological changes in periodontal tissues are mediated by the interaction between microorganisms and the host immune-inflammatory response. Hyperglycemia may interfere with this process. The aim of this study was to compare the levels of 27 inflammatory molecules in the gingival crevicular fluid (GCF) of patients with type 2 diabetes, with and without chronic periodontitis, and of chronic periodontitis subjects without diabetes. A putative correlation between glycated haemoglobin (HbA1c) and levels of the inflammatory molecules was also investigated.

Methods

The study population comprised a total of 108 individuals, stratified into: 54 with type 2 diabetes and chronic periodontitis (DM + CP), 30 with chronic periodontitis (CP) and 24 with type 2 diabetes (DM). Participants were interviewed with the aid of structured questionnaire. Periodontal parameters (dental plaque, bleeding on probing and periodontal pocket depth) were recorded. The GCF levels of the 27 inflammatory molecules were measured using multiplex micro-bead immunoassay. A glycated haemoglobin (HbA1c) test was performed for patients with diabetes by boronate affinity chromatography.

Results

After adjustment for potential confounders, the DM + CP group had higher levels of IL-8 and MIP-1β, and lower levels of TNF-α, IL-4, INF-γ, RANTES and IL-7 compared to the CP group. Moreover, the DM + CP group had lower levels of IL-6, IL-7 and G-CSF compared to the DM group. The DM group had higher levels of IL-10, VEGF, and G-CSF compared to the CP group. The levels of MIP-1α and FGF were lower in diabetes patients (regardless of their periodontal status) than in chronic periodontitis subjects without diabetes. Diabetes patients (DM + CP and DM) had higher Th-2/Th-1 ratio compared to the CP group. HbA1c correlated positively with the pro-inflammatory cytokines (Pearson correlation coefficient = 0.27, P value: 0.02).

Conclusion

Type 2 diabetes and chronic periodontitis may influence the GCF levels of inflammatory molecules synergistically as well as independently. Type 2 diabetes was associated with high Th-2/Th-1 ratio, and modulated the local expression of molecules involved in the anti-inflammatory and healing processes.
Literature
1.
go back to reference Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15(7):539–53.CrossRefPubMed Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15(7):539–53.CrossRefPubMed
2.
go back to reference American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2014, 37 Suppl 1:S81-90. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2014, 37 Suppl 1:S81-90.
3.
go back to reference International Diabetes Federation. IDF Diabetes Atlas update poster, 6th edn. Brussels, Belgium. International Diabetes Federation 2014. International Diabetes Federation. IDF Diabetes Atlas update poster, 6th edn. Brussels, Belgium. International Diabetes Federation 2014.
4.
go back to reference Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4–14.CrossRefPubMed Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4–14.CrossRefPubMed
5.
go back to reference Abdelgadir M, Elbagir M, Eltom M, Berne C. The influence of glucose self-monitoring on glycaemic control in patients with diabetes mellitus in Sudan. Diabetes Res Clin Pract. 2006;74(1):90–4.CrossRefPubMed Abdelgadir M, Elbagir M, Eltom M, Berne C. The influence of glucose self-monitoring on glycaemic control in patients with diabetes mellitus in Sudan. Diabetes Res Clin Pract. 2006;74(1):90–4.CrossRefPubMed
6.
go back to reference Sima C, Glogauer M. Diabetes mellitus and periodontal diseases. Curr Diab Rep. 2013;13(3):445–52.CrossRefPubMed Sima C, Glogauer M. Diabetes mellitus and periodontal diseases. Curr Diab Rep. 2013;13(3):445–52.CrossRefPubMed
7.
8.
go back to reference Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol 2000. 2004;34:9–21.CrossRefPubMed Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol 2000. 2004;34:9–21.CrossRefPubMed
9.
go back to reference Preshaw PM, Taylor JJ. How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? J Clin Periodontol. 2011;38 Suppl 11:60–84.CrossRefPubMed Preshaw PM, Taylor JJ. How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? J Clin Periodontol. 2011;38 Suppl 11:60–84.CrossRefPubMed
10.
go back to reference Kornman KS. Mapping the pathogenesis of periodontitis: a new look. J Periodontol. 2008;79(8 Suppl):1560–8.CrossRefPubMed Kornman KS. Mapping the pathogenesis of periodontitis: a new look. J Periodontol. 2008;79(8 Suppl):1560–8.CrossRefPubMed
11.
go back to reference Hanes PJ, Krishna R. Characteristics of inflammation common to both diabetes and periodontitis: are predictive diagnosis and targeted preventive measures possible? The EPMA journal. 2010;1(1):101–16.CrossRefPubMedPubMedCentral Hanes PJ, Krishna R. Characteristics of inflammation common to both diabetes and periodontitis: are predictive diagnosis and targeted preventive measures possible? The EPMA journal. 2010;1(1):101–16.CrossRefPubMedPubMedCentral
12.
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 Periodontol. 2013;84(4 Suppl):S113–134.PubMed Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Periodontol. 2013;84(4 Suppl):S113–134.PubMed
13.
go back to reference King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol. 2008;79(8 Suppl):1527–34.CrossRefPubMed King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol. 2008;79(8 Suppl):1527–34.CrossRefPubMed
14.
go back to reference Abbass MM, Korany NS, Salama AH, Dmytryk JJ, Safiejko-Mroczka B. The relationship between receptor for advanced glycation end products expression and the severity of periodontal disease in the gingiva of diabetic and non diabetic periodontitis patients. Arch Oral Biol. 2012;57(10):1342–54.CrossRefPubMed Abbass MM, Korany NS, Salama AH, Dmytryk JJ, Safiejko-Mroczka B. The relationship between receptor for advanced glycation end products expression and the severity of periodontal disease in the gingiva of diabetic and non diabetic periodontitis patients. Arch Oral Biol. 2012;57(10):1342–54.CrossRefPubMed
15.
go back to reference Nathan D, Turgeon H, Regan S. Relationship between glycated haemoglobin levels and mean glucose levels over time. Diabetologia. 2007;50(11):2239–44.CrossRefPubMed Nathan D, Turgeon H, Regan S. Relationship between glycated haemoglobin levels and mean glucose levels over time. Diabetologia. 2007;50(11):2239–44.CrossRefPubMed
16.
go back to reference Lamster IB, Ahlo JK. Analysis of gingival crevicular fluid as applied to the diagnosis of oral and systemic diseases. Ann N Y Acad Sci. 2007;1098:216–29.CrossRefPubMed Lamster IB, Ahlo JK. Analysis of gingival crevicular fluid as applied to the diagnosis of oral and systemic diseases. Ann N Y Acad Sci. 2007;1098:216–29.CrossRefPubMed
17.
go back to reference Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000. 2003;31:32–42.CrossRefPubMed Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000. 2003;31:32–42.CrossRefPubMed
18.
go back to reference Mohamed HG, Idris SB, Ahmed MF, Bøe OE, Mustafa K, Ibrahim SO, et al. Association between Oral Health Status and Type 2 Diabetes Mellitus among Sudanese Adults: A Matched Case-Control Study. PloS one. 2013;8(12):e82158. Mohamed HG, Idris SB, Ahmed MF, Bøe OE, Mustafa K, Ibrahim SO, et al. Association between Oral Health Status and Type 2 Diabetes Mellitus among Sudanese Adults: A Matched Case-Control Study. PloS one. 2013;8(12):e82158.
19.
go back to reference ADA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2008;31 Suppl 1:S55–60. ADA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2008;31 Suppl 1:S55–60.
20.
21.
go back to reference Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta odontologica Scandinavica. 1964;22:121–35.CrossRefPubMed Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta odontologica Scandinavica. 1964;22:121–35.CrossRefPubMed
22.
go back to reference Katagiri S, Nagasawa T, Kobayashi H, Takamatsu H, Bharti P, Izumiyama H, et al. Improvement of glycemic control after periodontal treatment by resolving gingival inflammation in type 2 diabetic patients with periodontal disease. J Diabetes Invest. 2012;3(4):402–9. Katagiri S, Nagasawa T, Kobayashi H, Takamatsu H, Bharti P, Izumiyama H, et al. Improvement of glycemic control after periodontal treatment by resolving gingival inflammation in type 2 diabetic patients with periodontal disease. J Diabetes Invest. 2012;3(4):402–9.
23.
go back to reference Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ. Update of the case definitions for population-based surveillance of periodontitis. J Periodontol. 2012;83(12):1449–54.CrossRefPubMed Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ. Update of the case definitions for population-based surveillance of periodontitis. J Periodontol. 2012;83(12):1449–54.CrossRefPubMed
24.
go back to reference Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas. 1960;20:37–46.CrossRef Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas. 1960;20:37–46.CrossRef
26.
go back to reference Thunell DH, Tymkiw KD, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res. 2010;45(1):148–52. Thunell DH, Tymkiw KD, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res. 2010;45(1):148–52.
28.
go back to reference Duarte PM, de Oliveira MC, Tambeli CH, Parada CA, Casati MZ, Nociti FHJr. Overexpression of interleukin-1beta and interleukin-6 may play an important role in periodontal breakdown in type 2 diabetic patients. J Periodontal Res. 2007;42(4):377–81. Duarte PM, de Oliveira MC, Tambeli CH, Parada CA, Casati MZ, Nociti FHJr. Overexpression of interleukin-1beta and interleukin-6 may play an important role in periodontal breakdown in type 2 diabetic patients. J Periodontal Res. 2007;42(4):377–81.
29.
go back to reference Atieh MA, Faggion CMJr, Seymour GJ. Cytokines in patients with type 2 diabetes and chronic periodontitis: A systematic review and meta-analysis. Diabetes Res Clin Pract. 2014;104(2):e38–45. Atieh MA, Faggion CMJr, Seymour GJ. Cytokines in patients with type 2 diabetes and chronic periodontitis: A systematic review and meta-analysis. Diabetes Res Clin Pract. 2014;104(2):e38–45.
30.
go back to reference Correa FO, Goncalves D, Figueredo CM, Gustafsson A, Orrico SR. The short-term effectiveness of non-surgical treatment in reducing levels of interleukin-1beta and proteases in gingival crevicular fluid from patients with type 2 diabetes mellitus and chronic periodontitis. J Periodontol. 2008;79(11):2143–50.CrossRefPubMed Correa FO, Goncalves D, Figueredo CM, Gustafsson A, Orrico SR. The short-term effectiveness of non-surgical treatment in reducing levels of interleukin-1beta and proteases in gingival crevicular fluid from patients with type 2 diabetes mellitus and chronic periodontitis. J Periodontol. 2008;79(11):2143–50.CrossRefPubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference Duarte PM, Bezerra JP, Miranda TS, Feres M, Chambrone L, Shaddox LM. Local levels of inflammatory mediators in uncontrolled type 2 diabetic subjects with chronic periodontitis. J Clin Periodontol. 2014;41(1):11–8.CrossRefPubMed Duarte PM, Bezerra JP, Miranda TS, Feres M, Chambrone L, Shaddox LM. Local levels of inflammatory mediators in uncontrolled type 2 diabetic subjects with chronic periodontitis. J Clin Periodontol. 2014;41(1):11–8.CrossRefPubMed
33.
go back to reference Engebretson SP, Hey-Hadavi J, Ehrhardt FJ, Hsu D, Celenti RS, Grbic JT, et al. Gingival crevicular fluid levels of interleukin-1beta and glycemic control in patients with chronic periodontitis and type 2 diabetes. J Periodontol. 2004;75(9):1203–8.CrossRefPubMed Engebretson SP, Hey-Hadavi J, Ehrhardt FJ, Hsu D, Celenti RS, Grbic JT, et al. Gingival crevicular fluid levels of interleukin-1beta and glycemic control in patients with chronic periodontitis and type 2 diabetes. J Periodontol. 2004;75(9):1203–8.CrossRefPubMed
34.
go back to reference Kinane DF, Preshaw PM, Loos BG. Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions--consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38 Suppl 11:44–8.CrossRefPubMed Kinane DF, Preshaw PM, Loos BG. Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions--consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38 Suppl 11:44–8.CrossRefPubMed
35.
go back to reference Kishimoto T. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res Ther. 2006;8 Suppl 2:S2.CrossRefPubMed Kishimoto T. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res Ther. 2006;8 Suppl 2:S2.CrossRefPubMed
36.
go back to reference Hosokawa Y, Shindo S, Hosokawa I, Ozaki K, Matsuo T. IL-6 trans-signaling enhances CCL20 production from IL-1beta-stimulated human periodontal ligament cells. Inflammation. 2014;37(2):381–6.CrossRefPubMed Hosokawa Y, Shindo S, Hosokawa I, Ozaki K, Matsuo T. IL-6 trans-signaling enhances CCL20 production from IL-1beta-stimulated human periodontal ligament cells. Inflammation. 2014;37(2):381–6.CrossRefPubMed
37.
go back to reference Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994;83(1):113–8.PubMed Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994;83(1):113–8.PubMed
38.
go back to reference Khosravi R, Ka K, Huang T, Khalili S, Nguyen BH, Nicolau B, et al. Tumor necrosis factor- alpha and interleukin-6: potential interorgan inflammatory mediators contributing to destructive periodontal disease in obesity or metabolic syndrome. Mediators Inflamm. 2013;2013:728987. Khosravi R, Ka K, Huang T, Khalili S, Nguyen BH, Nicolau B, et al. Tumor necrosis factor- alpha and interleukin-6: potential interorgan inflammatory mediators contributing to destructive periodontal disease in obesity or metabolic syndrome. Mediators Inflamm. 2013;2013:728987.
39.
go back to reference Javed F, Al-Askar M, Al-Hezaimi K. Cytokine profile in the gingival crevicular fluid of periodontitis patients with and without type 2 diabetes: a literature review. J Periodontol. 2012;83(2):156–61.CrossRefPubMed Javed F, Al-Askar M, Al-Hezaimi K. Cytokine profile in the gingival crevicular fluid of periodontitis patients with and without type 2 diabetes: a literature review. J Periodontol. 2012;83(2):156–61.CrossRefPubMed
40.
go back to reference Ribeiro FV, de Mendonça 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. J Periodontol. 2011;82(8):1187–96.CrossRefPubMed Ribeiro FV, de Mendonça 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. J Periodontol. 2011;82(8):1187–96.CrossRefPubMed
41.
go back to reference Chamberlain CS, Leiferman EM, Frisch KE, Wang S, Yang X, Brickson SL, et al. The influence of interleukin-4 on ligament healing. Wound Repair Regen. 2011;19(3):426–35. Chamberlain CS, Leiferman EM, Frisch KE, Wang S, Yang X, Brickson SL, et al. The influence of interleukin-4 on ligament healing. Wound Repair Regen. 2011;19(3):426–35.
42.
43.
go back to reference Longo PL, Artese HP, Rabelo MS, Kawamoto D, Foz AM, Romito GA, et al. Serum levels of inflammatory markers in type 2 diabetes patients with chronic periodontitis. J Appl Oral Sci. 2014;22(2):103–8. Longo PL, Artese HP, Rabelo MS, Kawamoto D, Foz AM, Romito GA, et al. Serum levels of inflammatory markers in type 2 diabetes patients with chronic periodontitis. J Appl Oral Sci. 2014;22(2):103–8.
44.
go back to reference Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol. 2004;36(10):1882–6.CrossRefPubMed Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol. 2004;36(10):1882–6.CrossRefPubMed
46.
go back to reference Sonmez AB, Castelnuovo J. Applications of basic fibroblastic growth factor (FGF-2, bFGF) in dentistry. Dent Traumatol. 2014;30(2):107–11.CrossRefPubMed Sonmez AB, Castelnuovo J. Applications of basic fibroblastic growth factor (FGF-2, bFGF) in dentistry. Dent Traumatol. 2014;30(2):107–11.CrossRefPubMed
47.
go back to reference Barrientos S, Brem H, Stojadinovic O, Tomic-Canic M. Clinical application of growth factors and cytokines in wound healing. Wound Repair Regen. 2014;22(5):569–78.CrossRefPubMedPubMedCentral Barrientos S, Brem H, Stojadinovic O, Tomic-Canic M. Clinical application of growth factors and cytokines in wound healing. Wound Repair Regen. 2014;22(5):569–78.CrossRefPubMedPubMedCentral
48.
go back to reference Moriya J, Ferrara N. Inhibiting the response to VEGF in diabetes. Sci Signal. 2014;7(307):e1.CrossRef Moriya J, Ferrara N. Inhibiting the response to VEGF in diabetes. Sci Signal. 2014;7(307):e1.CrossRef
49.
go back to reference Sakallioglu EE, Aliyev E, Lutfioglu M, Yavuz U, Acikgoz G. Vascular endothelial growth factor (VEGF) levels of gingiva and gingival crevicular fluid in diabetic and systemically healthy periodontitis patients. Clin Oral Investig. 2007;11(2):115–20.CrossRefPubMed Sakallioglu EE, Aliyev E, Lutfioglu M, Yavuz U, Acikgoz G. Vascular endothelial growth factor (VEGF) levels of gingiva and gingival crevicular fluid in diabetic and systemically healthy periodontitis patients. Clin Oral Investig. 2007;11(2):115–20.CrossRefPubMed
50.
go back to reference Guneri P, Unlu F, Yesilbek B, Bayraktar F, Kokuludag A, Hekimgil M, et al. Vascular endothelial growth factor in gingival tissues and crevicular fluids of diabetic and healthy periodontal patients. J Periodontol. 2004;75(1):91–7. Guneri P, Unlu F, Yesilbek B, Bayraktar F, Kokuludag A, Hekimgil M, et al. Vascular endothelial growth factor in gingival tissues and crevicular fluids of diabetic and healthy periodontal patients. J Periodontol. 2004;75(1):91–7.
51.
go back to reference Van Dyke TE, van Winkelhoff AJ. Infection and inflammatory mechanisms. J Clin Periodontol. 2013;40 Suppl 14:S1–7.PubMed Van Dyke TE, van Winkelhoff AJ. Infection and inflammatory mechanisms. J Clin Periodontol. 2013;40 Suppl 14:S1–7.PubMed
53.
go back to reference Van Dyke TE. Cellular and molecular susceptibility determinants for periodontitis. Periodontol 2000. 2007;45:10–3.CrossRefPubMed Van Dyke TE. Cellular and molecular susceptibility determinants for periodontitis. Periodontol 2000. 2007;45:10–3.CrossRefPubMed
54.
go back to reference Garlet GP. Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J Dent Res. 2010;89(12):1349–63.CrossRefPubMed Garlet GP. Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J Dent Res. 2010;89(12):1349–63.CrossRefPubMed
55.
go back to reference Wu Y, Liu F, Zhang X, Shu L. Insulin modulates cytokines expression in human periodontal ligament cells. Arch Oral Biol. 2014;59(12):1301–6.CrossRefPubMed Wu Y, Liu F, Zhang X, Shu L. Insulin modulates cytokines expression in human periodontal ligament cells. Arch Oral Biol. 2014;59(12):1301–6.CrossRefPubMed
56.
go back to reference Preshaw PM, Foster N, Taylor JJ. Cross-susceptibility between periodontal disease and type 2 diabetes mellitus: an immunobiological perspective. Periodontol 2000. 2007;45:138–57.CrossRefPubMed Preshaw PM, Foster N, Taylor JJ. Cross-susceptibility between periodontal disease and type 2 diabetes mellitus: an immunobiological perspective. Periodontol 2000. 2007;45:138–57.CrossRefPubMed
57.
go back to reference Fernandez y Mostajo M, Zaura E, Crielaard W, Beertsen W. Does routine analysis of subgingival microbiota in periodontitis contribute to patient benefit? Eur J Oral Sci. 2011;119(4):259–64.CrossRefPubMed Fernandez y Mostajo M, Zaura E, Crielaard W, Beertsen W. Does routine analysis of subgingival microbiota in periodontitis contribute to patient benefit? Eur J Oral Sci. 2011;119(4):259–64.CrossRefPubMed
58.
go back to reference Kinney JS, Morelli T, Oh M, Braun TM, Ramseier CA, Sugai JV, et al. Crevicular fluid biomarkers and periodontal disease progression. J Clin Periodontol. 2014;41(2):113–20. Kinney JS, Morelli T, Oh M, Braun TM, Ramseier CA, Sugai JV, et al. Crevicular fluid biomarkers and periodontal disease progression. J Clin Periodontol. 2014;41(2):113–20.
59.
go back to reference Petropoulos G, McKay IJ, Hughes FJ. The association between neutrophil numbers and interleukin-1alpha concentrations in gingival crevicular fluid of smokers and non-smokers with periodontal disease. J Clin Periodontol. 2004;31(5):390–5.CrossRefPubMed Petropoulos G, McKay IJ, Hughes FJ. The association between neutrophil numbers and interleukin-1alpha concentrations in gingival crevicular fluid of smokers and non-smokers with periodontal disease. J Clin Periodontol. 2004;31(5):390–5.CrossRefPubMed
60.
go back to reference Burstyn I, Yang Y, Schnatter AR. Effects of non-differential exposure misclassification on false conclusions in hypothesis-generating studies. Int J Environ Res Public Health. 2014;11(10):10951–66.CrossRefPubMedPubMedCentral Burstyn I, Yang Y, Schnatter AR. Effects of non-differential exposure misclassification on false conclusions in hypothesis-generating studies. Int J Environ Res Public Health. 2014;11(10):10951–66.CrossRefPubMedPubMedCentral
61.
go back to reference Zhong Y, Slade GD, Beck JD, Offenbacher S. Gingival crevicular fluid interleukin-1beta, prostaglandin E2 and periodontal status in a community population. J Clin Periodontol. 2007;34(4):285–93.CrossRefPubMed Zhong Y, Slade GD, Beck JD, Offenbacher S. Gingival crevicular fluid interleukin-1beta, prostaglandin E2 and periodontal status in a community population. J Clin Periodontol. 2007;34(4):285–93.CrossRefPubMed
62.
go back to reference Lopez R, Dahlen G, Baelum V. Subgingival microbial consortia and the clinical features of periodontitis in adolescents. European journal of oral sciences. 2011;119(6):455–62.CrossRefPubMed Lopez R, Dahlen G, Baelum V. Subgingival microbial consortia and the clinical features of periodontitis in adolescents. European journal of oral sciences. 2011;119(6):455–62.CrossRefPubMed
63.
go back to reference Zimmermann H, Hagenfeld D, Diercke K, El-Sayed N, Fricke J, Greiser KH, et al. Pocket depth and bleeding on probing and their associations with dental, lifestyle, socioeconomic and blood variables: a cross-sectional, multicenter feasibility study of the German National Cohort. BMC oral health. 2015;15:7. Zimmermann H, Hagenfeld D, Diercke K, El-Sayed N, Fricke J, Greiser KH, et al. Pocket depth and bleeding on probing and their associations with dental, lifestyle, socioeconomic and blood variables: a cross-sectional, multicenter feasibility study of the German National Cohort. BMC oral health. 2015;15:7.
Metadata
Title
Influence of type 2 diabetes on local production of inflammatory molecules in adults with and without chronic periodontitis: a cross-sectional study
Authors
Hasaan G. Mohamed
Shaza B. Idris
Mutaz F. Ahmed
Anne N. Åstrøm
Kamal Mustafa
Salah O. Ibrahim
Manal Mustafa
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2015
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-015-0073-z

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