Skip to main content
Top
Published in: BMC Oral Health 1/2023

Open Access 01-12-2023 | Research

Investigation on the association between serum lipid levels and periodontitis: a bidirectional Mendelian randomization analysis

Authors: Zhihong Chen, Jukun Song, Liszen Tang

Published in: BMC Oral Health | Issue 1/2023

Login to get access

Abstract

Objective

Several research has considered the potential correlation between periodontitis and serum lipids. However, serum lipid profiles correlation with periodontitis remains largely unknown. The investigation objective was to examine periodontitis correlation with serum lipid levels using a bidirectional Mendelian randomization (MR) analysis.

Methods

The study employed a bidirectional MR analysis with two samples, utilizing a freely accessible genome-wide association study (GWAS). Furthermore, the primary analysis employed the inverse variance weighted (IVW) method. To determine whether the lipid profiles were associated with periodontitis, a variety of sensitivity analyses (including MR-Egger regression, MR-PRESSO, and weighted median), as well as multivariable MR, were employed.

Results

MR analysis performed by IVW did not reveal any relationship between periodontitis and low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglycerides (TG), or total cholesterol (TC). It was also found that LDL, HDL, TG, and TC were not associated to periodontitis. Furthermore, the MR estimations exhibited consistency with other MR sensitivity and multivariate MR (MVMR) analyses. These results show that the correlation between serum lipid levels and periodontitis could not be established.

Conclusion

The finding indicates a negligible link between periodontitis and serum lipid levels were identified, despite previous observational studies reporting a link between periodontitis and serum lipid levels.
Appendix
Available only for authorised users
Literature
1.
go back to reference Loe H, Theilade E, Jensen SB. Experimental Gingivitis in Man. J Periodontol (1930). 1965;36:177–87.PubMedCrossRef Loe H, Theilade E, Jensen SB. Experimental Gingivitis in Man. J Periodontol (1930). 1965;36:177–87.PubMedCrossRef
2.
go back to reference Persson GR. What has ageing to do with periodontal health and Disease? Int Dent J. 2006;56:240–9.PubMedCrossRef Persson GR. What has ageing to do with periodontal health and Disease? Int Dent J. 2006;56:240–9.PubMedCrossRef
3.
go back to reference Brown LJ, Oliver RC, Loe H. Evaluating periodontal status of US employed adults. J Am Dent Assoc. 1990;121:226–32.PubMedCrossRef Brown LJ, Oliver RC, Loe H. Evaluating periodontal status of US employed adults. J Am Dent Assoc. 1990;121:226–32.PubMedCrossRef
4.
5.
go back to reference Chaffee BW, Weston SJ. Association between chronic periodontal Disease and obesity: a systematic review and meta-analysis. J Periodontol. 2010;81:1708–24.PubMedPubMedCentralCrossRef Chaffee BW, Weston SJ. Association between chronic periodontal Disease and obesity: a systematic review and meta-analysis. J Periodontol. 2010;81:1708–24.PubMedPubMedCentralCrossRef
6.
go back to reference Mizutani K, Park K, Mima A, Katagiri S, King GL. Obesity-associated Gingival vascular inflammation and insulin resistance. J Dent Res. 2014;93:596–601.PubMedPubMedCentralCrossRef Mizutani K, Park K, Mima A, Katagiri S, King GL. Obesity-associated Gingival vascular inflammation and insulin resistance. J Dent Res. 2014;93:596–601.PubMedPubMedCentralCrossRef
7.
8.
go back to reference Pirih FQ, Monajemzadeh S, Singh N, et al. Association between metabolic syndrome and periodontitis: the role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87:50–75.PubMedPubMedCentralCrossRef Pirih FQ, Monajemzadeh S, Singh N, et al. Association between metabolic syndrome and periodontitis: the role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 2000. 2021;87:50–75.PubMedPubMedCentralCrossRef
9.
go back to reference Rodriguez-Mortera R, Caccavello R, Hermo R, Garay-Sevilla ME, Gugliucci A. Higher hepcidin levels in adolescents with obesity are Associated with metabolic syndrome dyslipidemia and visceral Fat. Antioxid (Basel). 2021. 10. Rodriguez-Mortera R, Caccavello R, Hermo R, Garay-Sevilla ME, Gugliucci A. Higher hepcidin levels in adolescents with obesity are Associated with metabolic syndrome dyslipidemia and visceral Fat. Antioxid (Basel). 2021. 10.
10.
go back to reference Tian Z, Li Y, Mao Z, et al. Sex-specific relationship between visceral fat index and dyslipidemia in Chinese rural adults: the Henan Rural Cohort Study. Prev Med. 2018;116:104–11.PubMedCrossRef Tian Z, Li Y, Mao Z, et al. Sex-specific relationship between visceral fat index and dyslipidemia in Chinese rural adults: the Henan Rural Cohort Study. Prev Med. 2018;116:104–11.PubMedCrossRef
11.
go back to reference Gomez-Delgado F, Katsiki N, Lopez-Miranda J, Perez-Martinez P. Dietary habits, lipoprotein metabolism and Cardiovascular Disease: from individual foods to dietary patterns. Crit Rev Food Sci Nutr. 2021;61:1651–69.PubMedCrossRef Gomez-Delgado F, Katsiki N, Lopez-Miranda J, Perez-Martinez P. Dietary habits, lipoprotein metabolism and Cardiovascular Disease: from individual foods to dietary patterns. Crit Rev Food Sci Nutr. 2021;61:1651–69.PubMedCrossRef
13.
go back to reference Pearson GJ, Thanassoulis G, Anderson TJ, et al. 2021 Canadian Cardiovascular Society Guidelines for the management of Dyslipidemia for the Prevention of Cardiovascular Disease in adults. Can J Cardiol. 2021;37:1129–50.PubMedCrossRef Pearson GJ, Thanassoulis G, Anderson TJ, et al. 2021 Canadian Cardiovascular Society Guidelines for the management of Dyslipidemia for the Prevention of Cardiovascular Disease in adults. Can J Cardiol. 2021;37:1129–50.PubMedCrossRef
14.
go back to reference Lucchi T. Dyslipidemia and prevention of atherosclerotic Cardiovascular Disease in the elderly. Minerva Med. 2021;112:804–16.PubMed Lucchi T. Dyslipidemia and prevention of atherosclerotic Cardiovascular Disease in the elderly. Minerva Med. 2021;112:804–16.PubMed
15.
go back to reference Feingold KR, Grunfeld C. The effect of inflammation and Infection on lipids and lipoproteins. In: Feingold KR, Anawalt B, Boyce A, et al. editors. Endotext. South Dartmouth (MA); 2000. Feingold KR, Grunfeld C. The effect of inflammation and Infection on lipids and lipoproteins. In: Feingold KR, Anawalt B, Boyce A, et al. editors. Endotext. South Dartmouth (MA); 2000.
16.
go back to reference Augustemak de Lima LR, Petroski EL, Moreno YMF, et al. Dyslipidemia, chronic inflammation, and subclinical Atherosclerosis in children and adolescents infected with HIV: the PositHIVe Health Study. PLoS ONE. 2018;13:e0190785.PubMedPubMedCentralCrossRef Augustemak de Lima LR, Petroski EL, Moreno YMF, et al. Dyslipidemia, chronic inflammation, and subclinical Atherosclerosis in children and adolescents infected with HIV: the PositHIVe Health Study. PLoS ONE. 2018;13:e0190785.PubMedPubMedCentralCrossRef
17.
go back to reference Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: is oxidative stress a common link? J Dent Res. 2009;88:503–18.PubMedCrossRef Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: is oxidative stress a common link? J Dent Res. 2009;88:503–18.PubMedCrossRef
18.
go back to reference Ebersole JL, Cappelli D, Mott G, Kesavalu L, Holt SC, Singer RE. Systemic manifestations of periodontitis in the non-human primate. J Periodontal Res. 1999;34:358–62.PubMedCrossRef Ebersole JL, Cappelli D, Mott G, Kesavalu L, Holt SC, Singer RE. Systemic manifestations of periodontitis in the non-human primate. J Periodontal Res. 1999;34:358–62.PubMedCrossRef
19.
go back to reference Awartani F, Atassi F. Evaluation of periodontal status in subjects with hyperlipidemia. J Contemp Dent Pract. 2010;11:033–40.PubMedCrossRef Awartani F, Atassi F. Evaluation of periodontal status in subjects with hyperlipidemia. J Contemp Dent Pract. 2010;11:033–40.PubMedCrossRef
20.
go back to reference Katz J, Bhattacharyya I, Farkhondeh-Kish F, Perez FM, Caudle RM, Heft MW. Expression of the receptor of advanced glycation end products in gingival tissues of type 2 Diabetes patients with chronic periodontal Disease: a study utilizing immunohistochemistry and RT-PCR. J Clin Periodontol. 2005;32:40–4.PubMedCrossRef Katz J, Bhattacharyya I, Farkhondeh-Kish F, Perez FM, Caudle RM, Heft MW. Expression of the receptor of advanced glycation end products in gingival tissues of type 2 Diabetes patients with chronic periodontal Disease: a study utilizing immunohistochemistry and RT-PCR. J Clin Periodontol. 2005;32:40–4.PubMedCrossRef
21.
go back to reference Nibali L, D’Aiuto F, Griffiths G, Patel K, Suvan J, Tonetti MS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol. 2007;34:931–7.PubMedCrossRef Nibali L, D’Aiuto F, Griffiths G, Patel K, Suvan J, Tonetti MS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol. 2007;34:931–7.PubMedCrossRef
22.
go back to reference Valentaviciene G, Paipaliene P, Nedzelskiene I, Zilinskas J, Anuseviciene OV. The relationship between blood serum lipids and periodontal condition. Stomatologija. 2006;8:96–100.PubMed Valentaviciene G, Paipaliene P, Nedzelskiene I, Zilinskas J, Anuseviciene OV. The relationship between blood serum lipids and periodontal condition. Stomatologija. 2006;8:96–100.PubMed
23.
go back to reference Machado AC, Quirino MR, Nascimento LF. Relation between chronic periodontal Disease and plasmatic levels of triglycerides, total cholesterol and fractions. Braz Oral Res. 2005;19:284–9.PubMedCrossRef Machado AC, Quirino MR, Nascimento LF. Relation between chronic periodontal Disease and plasmatic levels of triglycerides, total cholesterol and fractions. Braz Oral Res. 2005;19:284–9.PubMedCrossRef
24.
go back to reference Losche W, Marshal GJ, Apatzidou DA, Krause S, Kocher T, Kinane DF. Lipoprotein-associated phospholipase A2 and plasma lipids in patients with destructive periodontal Disease. J Clin Periodontol. 2005;32:640–4.PubMedCrossRef Losche W, Marshal GJ, Apatzidou DA, Krause S, Kocher T, Kinane DF. Lipoprotein-associated phospholipase A2 and plasma lipids in patients with destructive periodontal Disease. J Clin Periodontol. 2005;32:640–4.PubMedCrossRef
25.
go back to reference Montebugnoli L, Servidio D, Miaton RA, Prati C, Tricoci P, Melloni C. Poor oral health is associated with coronary Heart Disease and elevated systemic inflammatory and haemostatic factors. J Clin Periodontol. 2004;31:25–9.PubMedCrossRef Montebugnoli L, Servidio D, Miaton RA, Prati C, Tricoci P, Melloni C. Poor oral health is associated with coronary Heart Disease and elevated systemic inflammatory and haemostatic factors. J Clin Periodontol. 2004;31:25–9.PubMedCrossRef
26.
go back to reference Richmond RC, Davey Smith G. Mendelian randomization: concepts and scope. Cold Spring Harb Perspect Med 2022; 12. Richmond RC, Davey Smith G. Mendelian randomization: concepts and scope. Cold Spring Harb Perspect Med 2022; 12.
28.
go back to reference Shungin D, Haworth S, Divaris K, et al. Genome-wide analysis of dental caries and periodontitis combining clinical and self-reported data. Nat Commun. 2019;10:2773.PubMedPubMedCentralCrossRef Shungin D, Haworth S, Divaris K, et al. Genome-wide analysis of dental caries and periodontitis combining clinical and self-reported data. Nat Commun. 2019;10:2773.PubMedPubMedCentralCrossRef
29.
go back to reference Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007;78:1387–99.PubMedCrossRef Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007;78:1387–99.PubMedCrossRef
30.
go back to reference Nolde M, Holtfreter B, Kocher T, et al. No bidirectional relationship between depression and periodontitis: a genetic correlation and mendelian randomization study. Front Immunol. 2022;13:918404.PubMedPubMedCentralCrossRef Nolde M, Holtfreter B, Kocher T, et al. No bidirectional relationship between depression and periodontitis: a genetic correlation and mendelian randomization study. Front Immunol. 2022;13:918404.PubMedPubMedCentralCrossRef
31.
go back to reference Jiang L, Zheng Z, Fang H, Yang J. A generalized linear mixed model association tool for biobank-scale data. Nat Genet. 2021;53:1616–21.PubMedCrossRef Jiang L, Zheng Z, Fang H, Yang J. A generalized linear mixed model association tool for biobank-scale data. Nat Genet. 2021;53:1616–21.PubMedCrossRef
32.
go back to reference Papapanou PN, Mariano S, Nurcan B, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World workshop on the classification of Periodontal and Peri-implant Diseases and conditions: classification and case definitions for periodontitis. J Clin Periodontol. 2018;45:162–S170.CrossRef Papapanou PN, Mariano S, Nurcan B, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World workshop on the classification of Periodontal and Peri-implant Diseases and conditions: classification and case definitions for periodontitis. J Clin Periodontol. 2018;45:162–S170.CrossRef
34.
go back to reference Bowden J, Davey Smith G, Haycock PC, Burgess S. Consistent estimation in mendelian randomization with some Invalid instruments using a weighted median estimator. Genet Epidemiol. 2016;40:304–14.PubMedPubMedCentralCrossRef Bowden J, Davey Smith G, Haycock PC, Burgess S. Consistent estimation in mendelian randomization with some Invalid instruments using a weighted median estimator. Genet Epidemiol. 2016;40:304–14.PubMedPubMedCentralCrossRef
35.
36.
go back to reference Chapple IL, Bouchard P, Cagetti MG, et al. Interaction of lifestyle, behaviour or systemic Diseases with dental caries and periodontal Diseases: consensus report of group 2 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal Diseases. J Clin Periodontol. 2017;44(Suppl 18):39–S51. Chapple IL, Bouchard P, Cagetti MG, et al. Interaction of lifestyle, behaviour or systemic Diseases with dental caries and periodontal Diseases: consensus report of group 2 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal Diseases. J Clin Periodontol. 2017;44(Suppl 18):39–S51.
37.
go back to reference Morris AP, Voight BF, Teslovich TM, et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 Diabetes. Nat Genet. 2012;44:981–90.PubMedPubMedCentralCrossRef Morris AP, Voight BF, Teslovich TM, et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 Diabetes. Nat Genet. 2012;44:981–90.PubMedPubMedCentralCrossRef
38.
39.
go back to reference Liu M, Jiang Y, Wedow R, et al. Association studies of up to 1.2 million individuals yield new insights into the genetic etiology of Tobacco and alcohol use. Nat Genet. 2019;51:237–44.PubMedPubMedCentralCrossRef Liu M, Jiang Y, Wedow R, et al. Association studies of up to 1.2 million individuals yield new insights into the genetic etiology of Tobacco and alcohol use. Nat Genet. 2019;51:237–44.PubMedPubMedCentralCrossRef
40.
go back to reference Hanaoka Y, Soejima H, Yasuda O, et al. Level of serum antibody against a periodontal pathogen is associated with Atherosclerosis and Hypertension. Hypertens Res. 2013;36:829–33.PubMedCrossRef Hanaoka Y, Soejima H, Yasuda O, et al. Level of serum antibody against a periodontal pathogen is associated with Atherosclerosis and Hypertension. Hypertens Res. 2013;36:829–33.PubMedCrossRef
41.
go back to reference Ansell BJ, Watson KE, Fogelman AM, Navab M, Fonarow GC. High-density lipoprotein function recent advances. J Am Coll Cardiol. 2005;46:1792–8.PubMedCrossRef Ansell BJ, Watson KE, Fogelman AM, Navab M, Fonarow GC. High-density lipoprotein function recent advances. J Am Coll Cardiol. 2005;46:1792–8.PubMedCrossRef
42.
go back to reference Singh IM, Shishehbor MH, Ansell BJ. High-density lipoprotein as a therapeutic target: a systematic review. JAMA. 2007;298:786–98.PubMedCrossRef Singh IM, Shishehbor MH, Ansell BJ. High-density lipoprotein as a therapeutic target: a systematic review. JAMA. 2007;298:786–98.PubMedCrossRef
43.
go back to reference Korhonen S, Saxlin T, Suominen L, Jula A, Knuuttila M, Ylostalo P. Serum cholesterol ratios and periodontal Infection: results of the Health 2000 Survey. J Clin Periodontol. 2011;38:787–94.PubMedCrossRef Korhonen S, Saxlin T, Suominen L, Jula A, Knuuttila M, Ylostalo P. Serum cholesterol ratios and periodontal Infection: results of the Health 2000 Survey. J Clin Periodontol. 2011;38:787–94.PubMedCrossRef
44.
go back to reference Saxlin T, Suominen-Taipale L, Kattainen A, Marniemi J, Knuuttila M, Ylostalo P. Association between serum lipid levels and periodontal Infection. J Clin Periodontol. 2008;35:1040–7.PubMedCrossRef Saxlin T, Suominen-Taipale L, Kattainen A, Marniemi J, Knuuttila M, Ylostalo P. Association between serum lipid levels and periodontal Infection. J Clin Periodontol. 2008;35:1040–7.PubMedCrossRef
45.
go back to reference Nepomuceno R, Pigossi SC, Finoti LS, et al. Serum lipid levels in patients with periodontal Disease: a meta-analysis and meta-regression. J Clin Periodontol. 2017;44:1192–207.PubMedCrossRef Nepomuceno R, Pigossi SC, Finoti LS, et al. Serum lipid levels in patients with periodontal Disease: a meta-analysis and meta-regression. J Clin Periodontol. 2017;44:1192–207.PubMedCrossRef
46.
go back to reference Choi YH, Kosaka T, Ojima M, et al. Relationship between the burden of major periodontal bacteria and serum lipid profile in a cross-sectional Japanese study. BMC Oral Health. 2018;18:77.PubMedPubMedCentralCrossRef Choi YH, Kosaka T, Ojima M, et al. Relationship between the burden of major periodontal bacteria and serum lipid profile in a cross-sectional Japanese study. BMC Oral Health. 2018;18:77.PubMedPubMedCentralCrossRef
47.
go back to reference Nakarai H, Yamashita A, Takagi M, et al. Periodontal Disease and hypertriglyceridemia in Japanese subjects: potential association with enhanced lipolysis. Metabolism. 2011;60:823–9.PubMedCrossRef Nakarai H, Yamashita A, Takagi M, et al. Periodontal Disease and hypertriglyceridemia in Japanese subjects: potential association with enhanced lipolysis. Metabolism. 2011;60:823–9.PubMedCrossRef
48.
go back to reference Ylostalo P, Suominen-Taipale L, Reunanen A, Knuuttila M. Association between body weight and periodontal Infection. J Clin Periodontol. 2008;35:297–304.PubMedCrossRef Ylostalo P, Suominen-Taipale L, Reunanen A, Knuuttila M. Association between body weight and periodontal Infection. J Clin Periodontol. 2008;35:297–304.PubMedCrossRef
49.
go back to reference Iacopino AM, Cutler CW. Pathophysiological relationships between periodontitis and systemic Disease: recent concepts involving serum lipids. J Periodontol. 2000;71:1375–84.PubMedCrossRef Iacopino AM, Cutler CW. Pathophysiological relationships between periodontitis and systemic Disease: recent concepts involving serum lipids. J Periodontol. 2000;71:1375–84.PubMedCrossRef
Metadata
Title
Investigation on the association between serum lipid levels and periodontitis: a bidirectional Mendelian randomization analysis
Authors
Zhihong Chen
Jukun Song
Liszen Tang
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2023
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-023-03575-x

Other articles of this Issue 1/2023

BMC Oral Health 1/2023 Go to the issue