Longitudinal effects of systemic inflammation markers on periodontitis
Aim Systemic low‐grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated. Materials a...
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| Published in: | Journal of clinical periodontology Vol. 42; no. 11; pp. 988 - 997 |
|---|---|
| Main Authors: | , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Blackwell Publishing Ltd
01.11.2015
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| ISSN: | 0303-6979, 1600-051X, 1600-051X |
| Online Access: | Get full text |
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| Abstract | Aim
Systemic low‐grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated.
Materials and Methods
The study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11‐year follow‐up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition.
Results
Multilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11‐year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11).
Conclusions
Fibrinogen levels and WBC counts showed consistent long‐term associations with PD, CAL and the CDC/AAP case definition. Results indicate that systemic low‐grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis. |
|---|---|
| AbstractList | Aim Systemic low-grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated. Materials and Methods The study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11-year follow-up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition. Results Multilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11-year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11). Conclusions Fibrinogen levels and WBC counts showed consistent long-term associations with PD,CAL and the CDC/AAP case definition. Results indicate that systemic low-grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis. Aim Systemic low‐grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated. Materials and Methods The study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11‐year follow‐up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition. Results Multilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11‐year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11). Conclusions Fibrinogen levels and WBC counts showed consistent long‐term associations with PD, CAL and the CDC/AAP case definition. Results indicate that systemic low‐grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis. Systemic low-grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated.AIMSystemic low-grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated.The study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11-year follow-up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition.MATERIALS AND METHODSThe study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11-year follow-up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition.Multilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11-year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11).RESULTSMultilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11-year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11).Fibrinogen levels and WBC counts showed consistent long-term associations with PD, CAL and the CDC/AAP case definition. Results indicate that systemic low-grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis.CONCLUSIONSFibrinogen levels and WBC counts showed consistent long-term associations with PD, CAL and the CDC/AAP case definition. Results indicate that systemic low-grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis. Systemic low-grade inflammation represents a central hallmark of chronic diseases and has been proposed as the underlying mechanism linking factors like obesity or diabetes with periodontitis. However, the impact of inflammatory markers on periodontitis has not yet been investigated. The study population comprised 1784 subjects from the Study of Health in Pomerania with complete 11-year follow-up. Fibrinogen and white blood cell (WBC) counts were measured as markers of inflammation. Periodontitis was assessed by probing depth (PD), clinical attachment loss (CAL) and the CDC/AAP case definition. Multilevel regression analyses revealed significant coefficients for the impact of both inflammation markers on the percentage of sites with PD/CAL ≥ 3 mm. Increases in fibrinogen about 1 g/l were associated with 3.0% and 2.7% more sites with PD/CAL ≥ 3 mm respectively. Consistent associations were found using mean values of PD/CAL but not using missing teeth or caries. Regarding the CDC/AAP case definition, 11-year changes in fibrinogen and WBC counts were significantly associated with ≥1 category progression (OR: 1.36 and 1.11). Fibrinogen levels and WBC counts showed consistent long-term associations with PD, CAL and the CDC/AAP case definition. Results indicate that systemic low-grade inflammation might indeed represent one possible pathway for effects of obesity, diabetes or other chronic inflammatory conditions on periodontitis. |
| Author | Meisel, Peter Kocher, Thomas Grotevendt, Anne Dörr, Marcus Markus, Marcello R. P. Pink, Christiane Jablonowski, Lukasz Nauck, Matthias Holtfreter, Birte |
| Author_xml | – sequence: 1 givenname: Christiane surname: Pink fullname: Pink, Christiane organization: Unit of Periodontology, Department of Restorative Dentistry, Periodontology, Endodontology, Pedodontics and Primary Prevention, University Medicine Greifswald, Greifswald, Germany – sequence: 2 givenname: Thomas surname: Kocher fullname: Kocher, Thomas organization: Unit of Periodontology, Department of Restorative Dentistry, Periodontology, Endodontology, Pedodontics and Primary Prevention, University Medicine Greifswald, Greifswald, Germany – sequence: 3 givenname: Peter surname: Meisel fullname: Meisel, Peter organization: Unit of Periodontology, Department of Restorative Dentistry, Periodontology, Endodontology, Pedodontics and Primary Prevention, University Medicine Greifswald, Greifswald, Germany – sequence: 4 givenname: Marcus surname: Dörr fullname: Dörr, Marcus organization: Department of Internal Medicine B, University Medicine Greifswald, Greifswald, Germany – sequence: 5 givenname: Marcello R. P. surname: Markus fullname: Markus, Marcello R. P. organization: Department of Internal Medicine B, University Medicine Greifswald, Greifswald, Germany – sequence: 6 givenname: Lukasz surname: Jablonowski fullname: Jablonowski, Lukasz organization: Unit of Periodontology, Department of Restorative Dentistry, Periodontology, Endodontology, Pedodontics and Primary Prevention, University Medicine Greifswald, Greifswald, Germany – sequence: 7 givenname: Anne surname: Grotevendt fullname: Grotevendt, Anne organization: Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, Greifswald, Germany – sequence: 8 givenname: Matthias surname: Nauck fullname: Nauck, Matthias organization: Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, Greifswald, Germany – sequence: 9 givenname: Birte surname: Holtfreter fullname: Holtfreter, Birte email: Address:, birte.holtfreter@uni-greifswald.de organization: Unit of Periodontology, Department of Restorative Dentistry, Periodontology, Endodontology, Pedodontics and Primary Prevention, University Medicine Greifswald, Greifswald, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26472626$$D View this record in MEDLINE/PubMed |
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| Keywords | fibrinogen inflammation periodontitis cohort studies diabetes mellitus leukocyte count obesity |
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| Notes | Ministry of Education ArticleID:JCPE12473 Figure S1. The main directed acyclic graph (DAG) to evaluate the association between systemic inflammation and periodontitis. Table S1. Association between 11-year change in inflammation markers and 11-year change in extent PD ≥ 3 mm and in extent CAL ≥ 3 mm. Table S2. Multilevel logistic regression models evaluating the long-term association between inflammation markers and the prevalence of having at least two sites with PD ≥ 5 mm/CAL ≥ 6 mm. Table S3. Multilevel linear regression models evaluating the long-term association between inflammation markers and extent PD ≥ 3 mm and extent CAL ≥ 3 mm for those subjects without anti-inflammatory medication. Figure S2. Predicted mean values (with 95% CI) of probing depth (PD; grey circle) and clinical attachment loss (CAL; black triangle) according to quartiles of fibrinogen (A) and WBC count (B) resulting from fully adjusted multilevel analyses as well as predicted change in mean values (with 95% CI) of PD and CAL according to quartiles of change in fibrinogen (C) and WBC count (D) resulting from 11-year change-on-change analyses. Table S4. Comparison of the SHIP-0 participants who were included in the study and those who were excluded Research and Cultural Affairs as well as the Ministry of Social Affairs of the Federal State of Mecklenburg-West Pomerania istex:AC75041FA8FA1038C0058C1D0FDD22ACCE82503A ark:/67375/WNG-5NGKVXPD-V German Federal Ministry of Education and Research - No. 01ZZ96030; No. 01ZZ0701 of the University of Greifswald, Germany, which is funded by the German Federal Ministry of Education and Research (BMBF) (grant 01ZZ96030, 01ZZ0701), the Ministry of Education, Research and Cultural Affairs as well as the Ministry of Social Affairs of the Federal State of Mecklenburg‐West Pomerania. GABA, Switzerland, provided an unlimited educational grant to support B.H. and C.P. SHIP is part of the Community Medicine Research net The authors declare that there are no conflicts of interest in this study. www.medizin.uni-greifswald.de/cm ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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| Publisher | Blackwell Publishing Ltd |
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| References | Van Dyke, T. E. & van Winkelhoff, A. J. (2013) Infection and inflammatory mechanisms. Journal of Clinical Periodontology 40 (Suppl 14), S1-S7. van Dijk, W. D., Akkermans, R., Heijdra, Y., Weel, C., Schermer, T. R., Scheepers, P. T. & Lenders, J. W. (2013) The acute effect of cigarette smoking on the high-sensitivity CRP and fibrinogen biomarkers in chronic obstructive pulmonary disease patients. Biomarkers in Medicine 7, 211-219. Howell, T. H. & Williams, R. C. (1993) Nonsteroidal antiinflammatory drugs as inhibitors of periodontal disease progression. Critical Reviews in Oral Biology and Medicine 4, 177-196. Taylor, J. J., Preshaw, P. M. & Lalla, E. (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. Journal of Clinical Periodontology 40 (Suppl 14), S113-S134. Williams, R. C., Jeffcoat, M. K., Howell, T. H., Rolla, A., Stubbs, D., Teoh, K. W., Reddy, M. S. & Goldhaber, P. (1989) Altering the progression of human alveolar bone loss with the non-steroidal anti-inflammatory drug flurbiprofen. Journal of Periodontology 60, 485-490. Gocke, C., Holtfreter, B., Meisel, P., Grotevendt, A., Jablonowski, L., Nauck, M., Markus, M. R. & Kocher, T. (2014) Abdominal obesity modifies long-term associations between periodontitis and markers of systemic inflammation. Atherosclerosis 235, 351-357. Merchant, A. T. & Pitiphat, W. (2002) Directed acyclic graphs (DAGs): an aid to assess confounding in dental research. Community Dentistry and Oral Epidemiology 30, 399-404. Fernandez, J. A., Prats, J. M., Artero, J. V., Mora, A. C., Farinas, A. V., Espinal, A. & Mendez, J. A. (2012) Systemic inflammation in 222.841 healthy employed smokers and nonsmokers: white blood cell count and relationship to spirometry. Tobacco Induced Diseases 10, 7. Saltevo, J., Vanhala, M., Kautiainen, H., Kumpusalo, E. & Laakso, M. (2008) Gender differences in C-reactive protein, interleukin-1 receptor antagonist and adiponectin levels in the metabolic syndrome: a population-based study. Diabetic Medicine 25, 747-750. Dandona, P., Aljada, A. & Bandyopadhyay, A. (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends in Immunology 25, 4-7. Demmer, R. T., Kocher, T., Schwahn, C., Volzke, H., Jacobs, D. R. Jr & Desvarieux, M. (2008) Refining exposure definitions for studies of periodontal disease and systemic disease associations. Community Dentistry and Oral Epidemiology 36, 493-502. John, U., Greiner, B., Hensel, E., Ludemann, J., Piek, M., Sauer, S., Adam, C., Born, G., Alte, D., Greiser, E., Haertel, U., Hense, H. W., Haerting, J., Willich, S. & Kessler, C. (2001) Study of Health In Pomerania (SHIP): a health examination survey in an east German region: objectives and design. Sozial- und Präventivmedizin 46, 186-194. WHO (2013) Oral health surveys: basic methods, 5th edition. Geneva: World Health Organization. Zuza, E. P., Barroso, E. M., Carrareto, A. L., Pires, J. R., Carlos, I. Z., Theodoro, L. H. & Toledo, B. E. (2011) The role of obesity as a modifying factor in patients undergoing non-surgical periodontal therapy. Journal of Periodontology 82, 676-682. Buhlin, K., Hultin, M., Norderyd, O., Persson, L., Pockley, A. G., Rabe, P., Klinge, B. & Gustafsson, A. (2009) Risk factors for atherosclerosis in cases with severe periodontitis. Journal of Clinical Periodontology 36, 541-549. Woodhouse, P. R., Khaw, K. T., Plummer, M., Foley, A. & Meade, T. W. (1994) Seasonal variations of plasma fibrinogen and factor VII activity in the elderly: winter infections and death from cardiovascular disease. Lancet (London, England) 343, 435-439. Alabdulkarim, M., Bissada, N., Al-Zahrani, M., Ficara, A. & Siegel, B. (2005) Alveolar bone loss in obese subjects. Journal of the International Academy of Periodontology 7, 34-38. Kopp, H. P., Kopp, C. W., Festa, A., Krzyzanowska, K., Kriwanek, S., Minar, E., Roka, R. & Schernthaner, G. (2003) Impact of weight loss on inflammatory proteins and their association with the insulin resistance syndrome in morbidly obese patients. Arteriosclerosis, Thrombosis, and Vascular Biology 23, 1042-1047. Monteiro, A. M., Jardini, M. A. N., Alves, S., Giampaoli, V., Aubin, E. C. Q., Figueiredo Neto, A. M. & Gidlund, M. (2009) Cardiovascular disease parameters in periodontitis. Journal of Periodontology 80, 378-388. Page, R. C. & Eke, P. I. (2007) Case definitions for use in population-based surveillance of periodontitis. Journal of Periodontology 78, 1387-1399. Textor, J., Hardt, J. & Knuppel, S. (2011) DAGitty: a graphical tool for analyzing causal diagrams. Epidemiology 22, 745. Zhu, M. & Nikolajczyk, B. S. (2014) Immune cells link obesity-associated type 2 diabetes and periodontitis. Journal of Dental Research 93, 346-352. Bruun, J. M., Verdich, C., Toubro, S., Astrup, A. & Richelsen, B. (2003) Association between measures of insulin sensitivity and circulating levels of interleukin-8, interleukin-6 and tumor necrosis factor-alpha. Effect of weight loss in obese men. European Journal of Endocrinology 148, 535-542. Drenos, F., Miller, G. J. & Humphries, S. E. (2007) Increase of plasma fibrinogen levels and variability with age in a sample of middle aged healthy men. Annals of Human Genetics 71, 43-53. Hensel, E., Gesch, D., Biffar, R., Bernhardt, O., Kocher, T., Splieth, C., Born, G. & John, U. (2003) Study of Health in Pomerania (SHIP): a health survey in an East German region. Objectives and design of the oral health section. Quintessence International 34, 370-378. Suvan, J., Petrie, A., Moles, D. R., Nibali, L., Patel, K., Darbar, U., Donos, N., Tonetti, M. & D'Aiuto, F. (2014) Body mass index as a predictive factor of periodontal therapy outcomes. Journal of Dental Research 93, 49-54. Alberti, K. G., Eckel, R. H., Grundy, S. M., Zimmet, P. Z., Cleeman, J. I., Donato, K. A., Fruchart, J. C., James, W. P., Loria, C. M. & Smith, S. C. Jr (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120, 1640-1645. Hunter, K. A., Garlick, P. J., Broom, I., Anderson, S. E. & McNurlan, M. A. (2001) Effects of smoking and abstention from smoking on fibrinogen synthesis in humans. Clinical Science (London, England: 1979) 100, 459-465. Adamu, A. N. (2011) Comparative performance of HbA1c 6.5% for FPG>/=7.0 vs 2 hr PG>/=11.1 criteria for diagnosis of type 2 diabetes. African Health Sciences 11, 421-426. Duncan, B. B., Schmidt, M. I., Pankow, J. S., Ballantyne, C. M., Couper, D., Vigo, A., Hoogeveen, R., Folsom, A. R. & Heiss, G. (2003) Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 52, 1799-1805. Salazar, M. G., Jehmlich, N., Murr, A., Dhople, V. M., Holtfreter, B., Hammer, E., Volker, U. & Kocher, T. (2013) Identification of periodontitis associated changes in the proteome of whole human saliva by mass spectrometric analysis. Journal of Clinical Periodontology 40, 825-832. Tonetti, M. S. & Chapple, I. L. (2011) Biological approaches to the development of novel periodontal therapies - consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology 38 (Suppl 11), 114-118. Naqvi, A. Z., Hasturk, H., Mu, L., Phillips, R. S., Davis, R. B., Halem, S., Campos, H., Goodson, J. M., Van Dyke, T. E. & Mukamal, K. J. (2014) Docosahexaenoic acid and periodontitis in adults: a randomized controlled trial. Journal of Dental Research 93, 767-773. StataCorp (2013) Stata statistical software: release 13. College Station, TX: StataCorp LP. Boesing, F., Patino, J. S., da Silva, V. R. & Moreira, E. A. (2009) The interface between obesity and periodontitis with emphasis on oxidative stress and inflammatory response. Obesity Reviews 10, 290-297. Negrato, C. A., Tarzia, O., Jovanovic, L. & Chinellato, L. E. (2013) Periodontal disease and diabetes mellitus. Journal of Applied Oral Science 21, 1-12. Al-Zahrani, M. S., Bissada, N. F. & Borawskit, E. A. (2003) Obesity and periodontal disease in young, middle-aged, and older adults. Journal of Periodontology 74, 610-615. Huttunen, R. & Syrjanen, J. (2013) Obesity and the risk and outcome of infection. International Journal of Obesity (2005) 37, 333-340. Rexrode, K. M., Pradhan, A., Manson, J. E., Buring, J. E. & Ridker, P. M. (2003) Relationship of total and abdominal adiposity with CRP and IL-6 in women. Annals of Epidemiology 13, 674-682. Alte, D., Ludemann, J., Piek, M., Adam, C., Rose, H. J. & John, U. (2003) Distribution and dose response of laboratory markers to alcohol consumption in a general population: results of the Study of Health in Pomerania (SHIP). Journal of Studies on Alcohol 64, 75-82. Nishida, N., Tanaka, M., Hayashi, N., Nagata, H., Takeshita, T., Nakayama, K., Morimoto, K. & Shizukuishi, S. (2005) Determination of smoking and obesity as periodontitis risks using the classification and regression tree method. Journal of Periodontology 76, 923-928. Park, H. S., Park, J. Y. & Yu, R. (2005) Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Research and Clinical Practice 69, 29-35. Demmer, R. T., Trinquart, L., Zuk, A., Fu, B. C., Blomkvist, J., Michalowicz, B. S., Ravaud, P. & Desvarieux, M. (2013) The influence of anti-infective periodontal treatment on C-reactive protein: a systematic review and meta-analysis of randomized controlled trials. PLoS One 8, e77441. Linden, G. J., McClean, K., Young, I., Evans, A. & Kee, F. (2008) Persistently raised C-reactive protein levels are associated with advanced periodontal disease. Journal of Clinical Periodontology 35, 741-747. 2001; 100 1989; 60 2002; 30 2011 2009; 80 2013; 21 2004; 25 2013; 40 2011; 82 2008; 36 2003; 13 2011; 11 2008; 35 2007; 71 2013; 7 2013; 8 2011; 38 2001; 46 2003; 74 2003; 52 2007; 78 2012; 10 2014; 235 1993; 4 2003; 34 2005; 69 1994; 343 2009; 36 2013; 37 2009; 10 2008; 25 2005; 7 2011; 22 2005; 76 2009; 120 2013 2003; 148 2014; 93 2003; 64 2003; 23 e_1_2_6_32_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_30_1 Van Dyke T. E. (e_1_2_6_41_1) 2013; 40 e_1_2_6_13_1 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_11_1 e_1_2_6_34_1 StataCorp (e_1_2_6_36_1) 2013 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_43_1 e_1_2_6_21_1 e_1_2_6_20_1 e_1_2_6_40_1 e_1_2_6_9_1 e_1_2_6_8_1 e_1_2_6_5_1 e_1_2_6_4_1 e_1_2_6_7_1 e_1_2_6_6_1 Glockmann E. (e_1_2_6_17_1) 2011 e_1_2_6_25_1 e_1_2_6_24_1 e_1_2_6_23_1 Hensel E. (e_1_2_6_19_1) 2003; 34 e_1_2_6_22_1 e_1_2_6_29_1 WHO (e_1_2_6_42_1) 2013 e_1_2_6_44_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_27_1 e_1_2_6_46_1 Adamu A. N. (e_1_2_6_2_1) 2011; 11 Alabdulkarim M. (e_1_2_6_3_1) 2005; 7 e_1_2_6_26_1 27938701 - J Evid Based Dent Pract. 2016 Dec;16(4):251-253 |
| References_xml | – reference: Zhu, M. & Nikolajczyk, B. S. (2014) Immune cells link obesity-associated type 2 diabetes and periodontitis. Journal of Dental Research 93, 346-352. – reference: Alte, D., Ludemann, J., Piek, M., Adam, C., Rose, H. J. & John, U. (2003) Distribution and dose response of laboratory markers to alcohol consumption in a general population: results of the Study of Health in Pomerania (SHIP). Journal of Studies on Alcohol 64, 75-82. – reference: Naqvi, A. Z., Hasturk, H., Mu, L., Phillips, R. S., Davis, R. B., Halem, S., Campos, H., Goodson, J. M., Van Dyke, T. E. & Mukamal, K. J. (2014) Docosahexaenoic acid and periodontitis in adults: a randomized controlled trial. Journal of Dental Research 93, 767-773. – reference: Tonetti, M. S. & Chapple, I. L. (2011) Biological approaches to the development of novel periodontal therapies - consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology 38 (Suppl 11), 114-118. – reference: Gocke, C., Holtfreter, B., Meisel, P., Grotevendt, A., Jablonowski, L., Nauck, M., Markus, M. R. & Kocher, T. (2014) Abdominal obesity modifies long-term associations between periodontitis and markers of systemic inflammation. Atherosclerosis 235, 351-357. – reference: Suvan, J., Petrie, A., Moles, D. R., Nibali, L., Patel, K., Darbar, U., Donos, N., Tonetti, M. & D'Aiuto, F. (2014) Body mass index as a predictive factor of periodontal therapy outcomes. Journal of Dental Research 93, 49-54. – reference: Adamu, A. N. (2011) Comparative performance of HbA1c 6.5% for FPG>/=7.0 vs 2 hr PG>/=11.1 criteria for diagnosis of type 2 diabetes. African Health Sciences 11, 421-426. – reference: Al-Zahrani, M. S., Bissada, N. F. & Borawskit, E. A. (2003) Obesity and periodontal disease in young, middle-aged, and older adults. Journal of Periodontology 74, 610-615. – reference: Fernandez, J. A., Prats, J. M., Artero, J. V., Mora, A. C., Farinas, A. V., Espinal, A. & Mendez, J. A. (2012) Systemic inflammation in 222.841 healthy employed smokers and nonsmokers: white blood cell count and relationship to spirometry. Tobacco Induced Diseases 10, 7. – reference: Page, R. C. & Eke, P. I. (2007) Case definitions for use in population-based surveillance of periodontitis. Journal of Periodontology 78, 1387-1399. – reference: Buhlin, K., Hultin, M., Norderyd, O., Persson, L., Pockley, A. G., Rabe, P., Klinge, B. & Gustafsson, A. (2009) Risk factors for atherosclerosis in cases with severe periodontitis. Journal of Clinical Periodontology 36, 541-549. – reference: Park, H. S., Park, J. Y. & Yu, R. (2005) Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Research and Clinical Practice 69, 29-35. – reference: Negrato, C. A., Tarzia, O., Jovanovic, L. & Chinellato, L. E. (2013) Periodontal disease and diabetes mellitus. Journal of Applied Oral Science 21, 1-12. – reference: Drenos, F., Miller, G. J. & Humphries, S. E. (2007) Increase of plasma fibrinogen levels and variability with age in a sample of middle aged healthy men. Annals of Human Genetics 71, 43-53. – reference: Hensel, E., Gesch, D., Biffar, R., Bernhardt, O., Kocher, T., Splieth, C., Born, G. & John, U. (2003) Study of Health in Pomerania (SHIP): a health survey in an East German region. Objectives and design of the oral health section. Quintessence International 34, 370-378. – reference: Dandona, P., Aljada, A. & Bandyopadhyay, A. (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends in Immunology 25, 4-7. – reference: Saltevo, J., Vanhala, M., Kautiainen, H., Kumpusalo, E. & Laakso, M. (2008) Gender differences in C-reactive protein, interleukin-1 receptor antagonist and adiponectin levels in the metabolic syndrome: a population-based study. Diabetic Medicine 25, 747-750. – reference: Demmer, R. T., Trinquart, L., Zuk, A., Fu, B. C., Blomkvist, J., Michalowicz, B. S., Ravaud, P. & Desvarieux, M. (2013) The influence of anti-infective periodontal treatment on C-reactive protein: a systematic review and meta-analysis of randomized controlled trials. PLoS One 8, e77441. – reference: Alabdulkarim, M., Bissada, N., Al-Zahrani, M., Ficara, A. & Siegel, B. (2005) Alveolar bone loss in obese subjects. Journal of the International Academy of Periodontology 7, 34-38. – reference: Kopp, H. P., Kopp, C. W., Festa, A., Krzyzanowska, K., Kriwanek, S., Minar, E., Roka, R. & Schernthaner, G. (2003) Impact of weight loss on inflammatory proteins and their association with the insulin resistance syndrome in morbidly obese patients. Arteriosclerosis, Thrombosis, and Vascular Biology 23, 1042-1047. – reference: van Dijk, W. D., Akkermans, R., Heijdra, Y., Weel, C., Schermer, T. R., Scheepers, P. T. & Lenders, J. W. (2013) The acute effect of cigarette smoking on the high-sensitivity CRP and fibrinogen biomarkers in chronic obstructive pulmonary disease patients. Biomarkers in Medicine 7, 211-219. – reference: Bruun, J. M., Verdich, C., Toubro, S., Astrup, A. & Richelsen, B. (2003) Association between measures of insulin sensitivity and circulating levels of interleukin-8, interleukin-6 and tumor necrosis factor-alpha. Effect of weight loss in obese men. European Journal of Endocrinology 148, 535-542. – reference: Zuza, E. P., Barroso, E. M., Carrareto, A. L., Pires, J. R., Carlos, I. Z., Theodoro, L. H. & Toledo, B. E. (2011) The role of obesity as a modifying factor in patients undergoing non-surgical periodontal therapy. Journal of Periodontology 82, 676-682. – reference: Huttunen, R. & Syrjanen, J. (2013) Obesity and the risk and outcome of infection. International Journal of Obesity (2005) 37, 333-340. – reference: Linden, G. J., McClean, K., Young, I., Evans, A. & Kee, F. (2008) Persistently raised C-reactive protein levels are associated with advanced periodontal disease. Journal of Clinical Periodontology 35, 741-747. – reference: John, U., Greiner, B., Hensel, E., Ludemann, J., Piek, M., Sauer, S., Adam, C., Born, G., Alte, D., Greiser, E., Haertel, U., Hense, H. W., Haerting, J., Willich, S. & Kessler, C. (2001) Study of Health In Pomerania (SHIP): a health examination survey in an east German region: objectives and design. Sozial- und Präventivmedizin 46, 186-194. – reference: Rexrode, K. M., Pradhan, A., Manson, J. E., Buring, J. E. & Ridker, P. M. (2003) Relationship of total and abdominal adiposity with CRP and IL-6 in women. Annals of Epidemiology 13, 674-682. – reference: Salazar, M. G., Jehmlich, N., Murr, A., Dhople, V. M., Holtfreter, B., Hammer, E., Volker, U. & Kocher, T. (2013) Identification of periodontitis associated changes in the proteome of whole human saliva by mass spectrometric analysis. Journal of Clinical Periodontology 40, 825-832. – reference: Monteiro, A. M., Jardini, M. A. N., Alves, S., Giampaoli, V., Aubin, E. C. Q., Figueiredo Neto, A. M. & Gidlund, M. (2009) Cardiovascular disease parameters in periodontitis. Journal of Periodontology 80, 378-388. – reference: Van Dyke, T. E. & van Winkelhoff, A. J. (2013) Infection and inflammatory mechanisms. Journal of Clinical Periodontology 40 (Suppl 14), S1-S7. – reference: Williams, R. C., Jeffcoat, M. K., Howell, T. H., Rolla, A., Stubbs, D., Teoh, K. W., Reddy, M. S. & Goldhaber, P. (1989) Altering the progression of human alveolar bone loss with the non-steroidal anti-inflammatory drug flurbiprofen. Journal of Periodontology 60, 485-490. – reference: Woodhouse, P. R., Khaw, K. T., Plummer, M., Foley, A. & Meade, T. W. (1994) Seasonal variations of plasma fibrinogen and factor VII activity in the elderly: winter infections and death from cardiovascular disease. Lancet (London, England) 343, 435-439. – reference: Nishida, N., Tanaka, M., Hayashi, N., Nagata, H., Takeshita, T., Nakayama, K., Morimoto, K. & Shizukuishi, S. (2005) Determination of smoking and obesity as periodontitis risks using the classification and regression tree method. Journal of Periodontology 76, 923-928. – reference: WHO (2013) Oral health surveys: basic methods, 5th edition. Geneva: World Health Organization. – reference: Alberti, K. G., Eckel, R. H., Grundy, S. M., Zimmet, P. Z., Cleeman, J. I., Donato, K. A., Fruchart, J. C., James, W. P., Loria, C. M. & Smith, S. C. Jr (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120, 1640-1645. – reference: Howell, T. H. & Williams, R. C. (1993) Nonsteroidal antiinflammatory drugs as inhibitors of periodontal disease progression. Critical Reviews in Oral Biology and Medicine 4, 177-196. – reference: Hunter, K. A., Garlick, P. J., Broom, I., Anderson, S. E. & McNurlan, M. A. (2001) Effects of smoking and abstention from smoking on fibrinogen synthesis in humans. Clinical Science (London, England: 1979) 100, 459-465. – reference: StataCorp (2013) Stata statistical software: release 13. College Station, TX: StataCorp LP. – reference: Merchant, A. T. & Pitiphat, W. (2002) Directed acyclic graphs (DAGs): an aid to assess confounding in dental research. Community Dentistry and Oral Epidemiology 30, 399-404. – reference: Duncan, B. B., Schmidt, M. I., Pankow, J. S., Ballantyne, C. M., Couper, D., Vigo, A., Hoogeveen, R., Folsom, A. R. & Heiss, G. (2003) Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 52, 1799-1805. – reference: Textor, J., Hardt, J. & Knuppel, S. (2011) DAGitty: a graphical tool for analyzing causal diagrams. Epidemiology 22, 745. – reference: Demmer, R. T., Kocher, T., Schwahn, C., Volzke, H., Jacobs, D. R. Jr & Desvarieux, M. (2008) Refining exposure definitions for studies of periodontal disease and systemic disease associations. Community Dentistry and Oral Epidemiology 36, 493-502. – reference: Boesing, F., Patino, J. S., da Silva, V. R. & Moreira, E. A. (2009) The interface between obesity and periodontitis with emphasis on oxidative stress and inflammatory response. Obesity Reviews 10, 290-297. – reference: Taylor, J. J., Preshaw, P. M. & Lalla, E. (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. Journal of Clinical Periodontology 40 (Suppl 14), S113-S134. – year: 2011 – volume: 25 start-page: 747 year: 2008 end-page: 750 article-title: Gender differences in C‐reactive protein, interleukin‐1 receptor antagonist and adiponectin levels in the metabolic syndrome: a population‐based study publication-title: Diabetic Medicine – volume: 74 start-page: 610 year: 2003 end-page: 615 article-title: Obesity and periodontal disease in young, middle‐aged, and older adults publication-title: Journal of Periodontology – volume: 30 start-page: 399 year: 2002 end-page: 404 article-title: Directed acyclic graphs (DAGs): an aid to assess confounding in dental research publication-title: Community Dentistry and Oral Epidemiology – volume: 37 start-page: 333 year: 2013 end-page: 340 article-title: Obesity and the risk and outcome of infection publication-title: International Journal of Obesity (2005) – volume: 69 start-page: 29 year: 2005 end-page: 35 article-title: Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF‐alpha and IL‐6 publication-title: Diabetes Research and Clinical Practice – volume: 148 start-page: 535 year: 2003 end-page: 542 article-title: Association between measures of insulin sensitivity and circulating levels of interleukin‐8, interleukin‐6 and tumor necrosis factor‐alpha. Effect of weight loss in obese men publication-title: European Journal of Endocrinology – volume: 25 start-page: 4 year: 2004 end-page: 7 article-title: Inflammation: the link between insulin resistance, obesity and diabetes publication-title: Trends in Immunology – volume: 52 start-page: 1799 year: 2003 end-page: 1805 article-title: Low‐grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study publication-title: Diabetes – volume: 23 start-page: 1042 year: 2003 end-page: 1047 article-title: Impact of weight loss on inflammatory proteins and their association with the insulin resistance syndrome in morbidly obese patients publication-title: Arteriosclerosis, Thrombosis, and Vascular Biology – volume: 76 start-page: 923 year: 2005 end-page: 928 article-title: Determination of smoking and obesity as periodontitis risks using the classification and regression tree method publication-title: Journal of Periodontology – volume: 71 start-page: 43 year: 2007 end-page: 53 article-title: Increase of plasma fibrinogen levels and variability with age in a sample of middle aged healthy men publication-title: Annals of Human Genetics – volume: 93 start-page: 346 year: 2014 end-page: 352 article-title: Immune cells link obesity‐associated type 2 diabetes and periodontitis publication-title: Journal of Dental Research – volume: 40 start-page: S1 issue: Suppl 14 year: 2013 end-page: S7 article-title: Infection and inflammatory mechanisms publication-title: Journal of Clinical Periodontology – volume: 34 start-page: 370 year: 2003 end-page: 378 article-title: Study of Health in Pomerania (SHIP): a health survey in an East German region. 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| Title | Longitudinal effects of systemic inflammation markers on periodontitis |
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