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

Open Access 01-12-2023 | Coronary Heart Disease | Research

MicroRNA‐155 (miR-155) as an accurate biomarker of periodontal status and coronary heart disease severity: a case–control study

Authors: Zina A. Daily, Batool Hassan Al-Ghurabi, Ahmed Makki A. Al-Qarakhli, Ryan Moseley

Published in: BMC Oral Health | Issue 1/2023

Login to get access

Abstract

Background

Increasing evidence supports associations between periodontal disease and coronary heart disease (CHD). This case–control study evaluated whether inflammatory regulator, microRNA-155 (miR-155), could be utilised as a biomarker of periodontitis and/or CHD.

Methods

Of 120 participants, 30 patients had clinically healthy periodontium (controls, C), 30 patients had generalized periodontitis (P), 30 patients had CHD and clinically healthy periodontium (AS-C); and 30 patients had CHD with generalized periodontitis (AS-P). Patient demographic and periodontal characteristics (plaque index, bleeding on probing, probing pocket depth and clinical attachment loss), were collected. Patient whole blood and saliva levels of miR-155 and pro-inflammatory cytokine (interleukin-1β), were quantified by quantitative real time polymerase chain reaction (qRT-PCR) and enzyme-linked immunosorbent assay (ELISA). One-way ANOVA with post-hoc Tukey test was used to determine differences among the four groups. Chi Square test was used for participant gender comparisons. Pearson correlation tests and multiple linear regression analyses were used to assess associations between the demographic and clinical variables analysed, versus IL-1β and miR-155 levels. miR-155 and IL-1β accuracy in differentiating healthy versus other patient groups were analysed using receiver operating characteristic (ROC) curves, by calculating area under the curve (AUC) values and sensitivity and specificity cut-off points using Youden’s index. Statistical tests of sensitivity and specificity were conducted using the McNemar test.

Results

Whole blood miR-155 levels were elevated in periodontitis/non-periodontitis patients with CHD (AS-P, AS-C), and periodontitis patients alone (P) (p < 0.001). Receiver operating characteristic (ROC) and area under the curve (AUC) analyses confirmed miR-155 accuracy in discriminating P, AS-C and AS-P groups (AUC 0.6861–0.9944, p < 0.0001–0.05), coupled with high sensitivity (76.7–100.0%), specificity (53.3–96.7%) and cut-off points (> 0.955- > 2.915 a.u.; p < 0.0001). miR-155 levels further distinguished between CHD (AS-C, AS-P) and periodontitis (P) patients (AUC ≥ 0.8378, sensitivity ≥ 88.7%, specificity ≥ 73.3%, cut-off > 2.82 a.u; p < 0.0001), and between AS-C and AS-P patients (AUC 0.7578, sensitivity 80.0%, specificity 50.0%, cut-off > 7.065 a.u; p < 0.001). Subsequent analyses identified positive correlations between miR-155 and the various patient demographics, salivary interleukin-1β and periodontal parameters assessed.

Conclusions

This study advocates miR-155 as an accurate diagnostic/prognostic biomarker of periodontitis and/or CHD severity, thereby improving detection and treatment for both conditions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Tonetti MS, Jepsen S, Jin L, Otomo-Corgel J. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: A call for global action. J Clin Periodontol. 2017;44(5):456–62.PubMed Tonetti MS, Jepsen S, Jin L, Otomo-Corgel J. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: A call for global action. J Clin Periodontol. 2017;44(5):456–62.PubMed
2.
go back to reference Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases Nat Revs Dis Primers. 2017;3:17038. Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases Nat Revs Dis Primers. 2017;3:17038.
3.
go back to reference Abusleme L, Hoare A, Hong BY, Diaz PI. Microbial signatures of health, gingivitis, and periodontitis. Periodontol 2000. 2021;86(1):57–78.PubMed Abusleme L, Hoare A, Hong BY, Diaz PI. Microbial signatures of health, gingivitis, and periodontitis. Periodontol 2000. 2021;86(1):57–78.PubMed
4.
go back to reference Hajishengallis G, Chavakis T, Lambris JD. Current understanding of periodontal disease pathogenesis and targets for host-modulation therapy. Periodontol 2000. 2020;84(1):14–34.PubMedPubMedCentral Hajishengallis G, Chavakis T, Lambris JD. Current understanding of periodontal disease pathogenesis and targets for host-modulation therapy. Periodontol 2000. 2020;84(1):14–34.PubMedPubMedCentral
5.
go back to reference Van Dyke TE, Bartold PM, Reynolds EC. The nexus between periodontal inflammation and dysbiosis. Front Immunol. 2020;11:511.PubMedPubMedCentral Van Dyke TE, Bartold PM, Reynolds EC. The nexus between periodontal inflammation and dysbiosis. Front Immunol. 2020;11:511.PubMedPubMedCentral
6.
go back to reference Hajishengallis G, Lamont RJ. Polymicrobial communities in periodontal disease: Their quasi-organismal nature and dialogue with the host. Periodontol 2000. 2021;86(1):210–30.PubMedPubMedCentral Hajishengallis G, Lamont RJ. Polymicrobial communities in periodontal disease: Their quasi-organismal nature and dialogue with the host. Periodontol 2000. 2021;86(1):210–30.PubMedPubMedCentral
7.
go back to reference Sanz M, Marco Del Castillo A, Jepsen S, et al. Periodontitis and cardiovascular diseases: Consensus report. J Clin Periodontol. 2019;47(3):268–88. Sanz M, Marco Del Castillo A, Jepsen S, et al. Periodontitis and cardiovascular diseases: Consensus report. J Clin Periodontol. 2019;47(3):268–88.
8.
go back to reference Frencken JE, Sharma P, Stenhouse L, Green D, Laverty D, Dietrich T. Global epidemiology of dental caries and severe periodontitis - A comprehensive review. J Clin Periodontol. 2017;44(18):S94-105.PubMed Frencken JE, Sharma P, Stenhouse L, Green D, Laverty D, Dietrich T. Global epidemiology of dental caries and severe periodontitis - A comprehensive review. J Clin Periodontol. 2017;44(18):S94-105.PubMed
9.
go back to reference Xu S, Song M, Xiong Y, Liu X, He Y, Qin Z. The association between periodontal disease and the risk of myocardial infarction: A pooled analysis of observational studies. BMC Cardiovasc Disord. 2017;17(1):50.PubMedPubMedCentral Xu S, Song M, Xiong Y, Liu X, He Y, Qin Z. The association between periodontal disease and the risk of myocardial infarction: A pooled analysis of observational studies. BMC Cardiovasc Disord. 2017;17(1):50.PubMedPubMedCentral
10.
go back to reference Zardawi F, Gul S, Abdulkareem A, Sha A, Yates J. Association between periodontal disease and atherosclerotic cardiovascular diseases: Revisited. Front Cardiovasc Med. 2021;7: 625579.PubMedPubMedCentral Zardawi F, Gul S, Abdulkareem A, Sha A, Yates J. Association between periodontal disease and atherosclerotic cardiovascular diseases: Revisited. Front Cardiovasc Med. 2021;7: 625579.PubMedPubMedCentral
11.
go back to reference Hamaya R, Yonetsu T, Aoyama N, et al. Contribution of periodontal health in cardiovascular secondary prevention: Analyses on hospitalized patients in cardiology units. J Clin Periodontol. 2023;50(6):708–16.PubMed Hamaya R, Yonetsu T, Aoyama N, et al. Contribution of periodontal health in cardiovascular secondary prevention: Analyses on hospitalized patients in cardiology units. J Clin Periodontol. 2023;50(6):708–16.PubMed
12.
go back to reference Schenkein HA, Loos BG. Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. J Periodontol. 2013;84(4):S51-69.PubMed Schenkein HA, Loos BG. Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. J Periodontol. 2013;84(4):S51-69.PubMed
13.
go back to reference Demmer RT, Trinquart L, Zuk A, et al. The influence of anti-infective periodontal treatment on C-reactive protein: A systematic review and meta-analysis of randomized controlled trials. PLoS ONE. 2013;8(10): e77441.ADSPubMedPubMedCentral Demmer RT, Trinquart L, Zuk A, et al. The influence of anti-infective periodontal treatment on C-reactive protein: A systematic review and meta-analysis of randomized controlled trials. PLoS ONE. 2013;8(10): e77441.ADSPubMedPubMedCentral
14.
go back to reference Montenegro MM, Ribeiro IWJ, Kampits C, et al. Randomized controlled trial of the effect of periodontal treatment on cardiovascular risk biomarkers in patients with stable coronary artery disease: Preliminary findings of 3 months. J Clin Periodontol. 2019;46(3):321–31.PubMed Montenegro MM, Ribeiro IWJ, Kampits C, et al. Randomized controlled trial of the effect of periodontal treatment on cardiovascular risk biomarkers in patients with stable coronary artery disease: Preliminary findings of 3 months. J Clin Periodontol. 2019;46(3):321–31.PubMed
15.
16.
go back to reference Almehmadi AH, Alghamdi F. Biomarkers of alveolar bone resorption in gingival crevicular fluid: A systematic review. Arch Oral Biol. 2018;93:12–21.PubMed Almehmadi AH, Alghamdi F. Biomarkers of alveolar bone resorption in gingival crevicular fluid: A systematic review. Arch Oral Biol. 2018;93:12–21.PubMed
17.
go back to reference Henein MY, Vancheri S, Longo G, Vancheri F. The role of inflammation in cardiovascular disease. Int J Mol Sci. 2022;23(21):12906.PubMedPubMedCentral Henein MY, Vancheri S, Longo G, Vancheri F. The role of inflammation in cardiovascular disease. Int J Mol Sci. 2022;23(21):12906.PubMedPubMedCentral
18.
go back to reference Hoelscher SC, Doppler SA, Dreßen M, Lahm H, Lange R, Krane M. MicroRNAs: Pleiotropic players in congenital heart disease and regeneration. J Thorac Dis. 2017;9(1):S64-81.PubMedPubMedCentral Hoelscher SC, Doppler SA, Dreßen M, Lahm H, Lange R, Krane M. MicroRNAs: Pleiotropic players in congenital heart disease and regeneration. J Thorac Dis. 2017;9(1):S64-81.PubMedPubMedCentral
19.
go back to reference Collins L, Binder P, Chen H, Wang X. Regulation of long non-coding RNAs and microRNAs in heart disease: Insight into mechanisms and therapeutic approaches. Front Physiol. 2020;11:798.PubMedPubMedCentral Collins L, Binder P, Chen H, Wang X. Regulation of long non-coding RNAs and microRNAs in heart disease: Insight into mechanisms and therapeutic approaches. Front Physiol. 2020;11:798.PubMedPubMedCentral
20.
21.
go back to reference Santonocito S, Polizzi A, Palazzo G, Isola G. The emerging role of microRNA in periodontitis: Pathophysiology, clinical potential and future molecular perspectives. Int J Mol Sci. 2021;22(11):5456.PubMedPubMedCentral Santonocito S, Polizzi A, Palazzo G, Isola G. The emerging role of microRNA in periodontitis: Pathophysiology, clinical potential and future molecular perspectives. Int J Mol Sci. 2021;22(11):5456.PubMedPubMedCentral
22.
go back to reference O’Brien J, Hayder H, Zayed Y, Peng C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol. 2018;9:402. O’Brien J, Hayder H, Zayed Y, Peng C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol. 2018;9:402.
23.
go back to reference Lee YH, Na HS, Jeong SY, Jeong SH, Park HR, Chung J. Comparison of inflammatory microRNA expression in healthy and periodontitis tissues. Biocell. 2011;35(2):43–9.PubMed Lee YH, Na HS, Jeong SY, Jeong SH, Park HR, Chung J. Comparison of inflammatory microRNA expression in healthy and periodontitis tissues. Biocell. 2011;35(2):43–9.PubMed
24.
go back to reference Micó-Martínez P, Almiñana-Pastor PJ, Alpiste-Illueca F, López-Roldán A. MicroRNAs and periodontal disease: A qualitative systematic review of human studies. J Periodont Impl Sci. 2021;51(6):386–97. Micó-Martínez P, Almiñana-Pastor PJ, Alpiste-Illueca F, López-Roldán A. MicroRNAs and periodontal disease: A qualitative systematic review of human studies. J Periodont Impl Sci. 2021;51(6):386–97.
25.
go back to reference Luan X, Zhou X, Fallah P, et al. MicroRNAs: Harbingers and shapers of periodontal inflammation. Semin Cell Dev Biol. 2022;124:85–98.PubMed Luan X, Zhou X, Fallah P, et al. MicroRNAs: Harbingers and shapers of periodontal inflammation. Semin Cell Dev Biol. 2022;124:85–98.PubMed
26.
go back to reference Wojciechowska A, Braniewska A, Kozar-Kamińska K. MicroRNA in cardiovascular biology and disease. Adv Clin Exp Med. 2017;26(5):865–74.PubMed Wojciechowska A, Braniewska A, Kozar-Kamińska K. MicroRNA in cardiovascular biology and disease. Adv Clin Exp Med. 2017;26(5):865–74.PubMed
27.
go back to reference Solly EL, Dimasi CG, Bursill CA, Psaltis PJ, Tan JTM. MicroRNAs as therapeutic targets and clinical biomarkers in atherosclerosis. J Clin Med. 2019;8(12):2199.PubMedPubMedCentral Solly EL, Dimasi CG, Bursill CA, Psaltis PJ, Tan JTM. MicroRNAs as therapeutic targets and clinical biomarkers in atherosclerosis. J Clin Med. 2019;8(12):2199.PubMedPubMedCentral
28.
go back to reference Mahesh G, Biswas R. MicroRNA-155: A master regulator of inflammation. J Interfer Cytokine Res. 2019;39(6):321–30. Mahesh G, Biswas R. MicroRNA-155: A master regulator of inflammation. J Interfer Cytokine Res. 2019;39(6):321–30.
29.
go back to reference Radović N, Nikolić Jakoba N, Petrović N, Milosavljević A, Brković B, Roganović J. MicroRNA-146a and microRNA-155 as novel crevicular fluid biomarkers for periodontitis in non-diabetic and type 2 diabetic patients. J Clin Periodontol. 2018;45(6):663–71.PubMed Radović N, Nikolić Jakoba N, Petrović N, Milosavljević A, Brković B, Roganović J. MicroRNA-146a and microRNA-155 as novel crevicular fluid biomarkers for periodontitis in non-diabetic and type 2 diabetic patients. J Clin Periodontol. 2018;45(6):663–71.PubMed
30.
go back to reference Al-Rawi NH, Al-Marzooq F, Al-Nuaimi AS, Hachim MY, Hamoudi R. Salivary microRNA 155, 146a/b and 203: A pilot study for potentially non-invasive diagnostic biomarkers of periodontitis and diabetes mellitus. PLoS ONE. 2020;15(8): e0237004.PubMedPubMedCentral Al-Rawi NH, Al-Marzooq F, Al-Nuaimi AS, Hachim MY, Hamoudi R. Salivary microRNA 155, 146a/b and 203: A pilot study for potentially non-invasive diagnostic biomarkers of periodontitis and diabetes mellitus. PLoS ONE. 2020;15(8): e0237004.PubMedPubMedCentral
31.
go back to reference Wu P, Feng J, Wang W. Expression of miR-155 and miR-146a in the saliva of patients with periodontitis and its clinical value. Am J Transl Res. 2021;13(6):6670–7.PubMedPubMedCentral Wu P, Feng J, Wang W. Expression of miR-155 and miR-146a in the saliva of patients with periodontitis and its clinical value. Am J Transl Res. 2021;13(6):6670–7.PubMedPubMedCentral
32.
go back to reference Qiu XK, Ma J. Alteration in microRNA-155 level correspond to severity of coronary heart disease. Scand J Clin Lab Invest. 2018;78(3):219–23.PubMed Qiu XK, Ma J. Alteration in microRNA-155 level correspond to severity of coronary heart disease. Scand J Clin Lab Invest. 2018;78(3):219–23.PubMed
33.
go back to reference Zhang B, Li B, Qin F, Bai F, Sun C, Liu Q. Expression of serum microRNA-155 and its clinical importance in patients with heart failure after myocardial infarction. J Int Med Res. 2019;47(12):6294–302.PubMedPubMedCentral Zhang B, Li B, Qin F, Bai F, Sun C, Liu Q. Expression of serum microRNA-155 and its clinical importance in patients with heart failure after myocardial infarction. J Int Med Res. 2019;47(12):6294–302.PubMedPubMedCentral
34.
go back to reference Fitzsimons S, Oggero S, Bruen R, et al. MicroRNA-155 is decreased during atherosclerosis regression and is increased in urinary extracellular vesicles during atherosclerosis progression. Front Immunol. 2020;11: 576516.PubMedPubMedCentral Fitzsimons S, Oggero S, Bruen R, et al. MicroRNA-155 is decreased during atherosclerosis regression and is increased in urinary extracellular vesicles during atherosclerosis progression. Front Immunol. 2020;11: 576516.PubMedPubMedCentral
35.
go back to reference Orlandi M, Graziani F, D`Aiuto F. Periodontal therapy and cardiovascular risk. J Periodontol. 2020;83:107–24. Orlandi M, Graziani F, D`Aiuto F. Periodontal therapy and cardiovascular risk. J Periodontol. 2020;83:107–24.
36.
go back to reference Charan J, Biswas T. How to calculate sample size for different study designs in medical research? Ind J Psychol Med. 2013;35:121–6. Charan J, Biswas T. How to calculate sample size for different study designs in medical research? Ind J Psychol Med. 2013;35:121–6.
37.
go back to reference Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(1):S159–72.PubMed Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(1):S159–72.PubMed
38.
go back to reference Chapple ILC, Mealey BL, Van Dyke TE, et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: Consensus report of Workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89(1):S74-84.PubMed Chapple ILC, Mealey BL, Van Dyke TE, et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: Consensus report of Workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89(1):S74-84.PubMed
39.
go back to reference Temelli B, Yetkin Ay Z, Savas H, Aksoy F, Kumbul Doğuç D, Uskun E, et al. Circulation levels of acute phase proteins pentraxin 3 and serum amyloid A in atherosclerosis have correlations with periodontal inflamed surface area. J Appl Oral Sci. 2018;26: e20170322.PubMedPubMedCentral Temelli B, Yetkin Ay Z, Savas H, Aksoy F, Kumbul Doğuç D, Uskun E, et al. Circulation levels of acute phase proteins pentraxin 3 and serum amyloid A in atherosclerosis have correlations with periodontal inflamed surface area. J Appl Oral Sci. 2018;26: e20170322.PubMedPubMedCentral
40.
go back to reference Bagavad Gita J, George AV, Pavithra N, Chandrasekaran SC, Latchumanadhas K, Gnanamani A. Dysregulation of miR-146a by periodontal pathogens: A risk for acute coronary syndrome. J Periodontol. 2019;90(7):756–65.PubMed Bagavad Gita J, George AV, Pavithra N, Chandrasekaran SC, Latchumanadhas K, Gnanamani A. Dysregulation of miR-146a by periodontal pathogens: A risk for acute coronary syndrome. J Periodontol. 2019;90(7):756–65.PubMed
41.
go back to reference Yagnik K, Mahendra J, Kurian VM. The Periodontal-Cardiovascular alliance: Evaluation of miRNA-146a in subgingival plaque samples of chronic periodontitis patients with and without coronary heart disease. J Invest Clin Dent. 2019;10(4): e12442. Yagnik K, Mahendra J, Kurian VM. The Periodontal-Cardiovascular alliance: Evaluation of miRNA-146a in subgingival plaque samples of chronic periodontitis patients with and without coronary heart disease. J Invest Clin Dent. 2019;10(4): e12442.
42.
go back to reference Al-Taweel FBH, Saliem SS, Abd OH, Whawell SA. Assessment of serum interleukin-1β and interleukin-6 levels in patients with chronic periodontitis and coronary heart disease. Eur J Gen Dent. 2021;10(2):78–83. Al-Taweel FBH, Saliem SS, Abd OH, Whawell SA. Assessment of serum interleukin-1β and interleukin-6 levels in patients with chronic periodontitis and coronary heart disease. Eur J Gen Dent. 2021;10(2):78–83.
43.
go back to reference Mühlemann H, Son S. Gingival sulcus bleeding - A leading symptom in initial gingivitis. Helv Odontol Acta. 1971;15(2):107–13.PubMed Mühlemann H, Son S. Gingival sulcus bleeding - A leading symptom in initial gingivitis. Helv Odontol Acta. 1971;15(2):107–13.PubMed
44.
go back to reference O’Leary T, Drake R, Naylor J. The plaque control record. J Periodontol. 1972;43(1):38.PubMed O’Leary T, Drake R, Naylor J. The plaque control record. J Periodontol. 1972;43(1):38.PubMed
45.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods. 2001;25(4):402–8.PubMed Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods. 2001;25(4):402–8.PubMed
46.
go back to reference Naqvi RA, Gupta M, George A, Naqvi AR. MicroRNAs in shaping the resolution phase of inflammation. Semin Cell Dev Biol. 2022;124:48–62.PubMed Naqvi RA, Gupta M, George A, Naqvi AR. MicroRNAs in shaping the resolution phase of inflammation. Semin Cell Dev Biol. 2022;124:48–62.PubMed
47.
go back to reference Sun HX, Zeng DY, Li RT, et al. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension. 2012;60(6):1407–14.PubMed Sun HX, Zeng DY, Li RT, et al. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension. 2012;60(6):1407–14.PubMed
48.
go back to reference Pankratz F, Bemtgen X, Zeiser R, et al. MicroRNA-155 exerts cell-specific antiangiogenic but proarteriogenic effects during adaptive neovascularization. Circulation. 2015;131(18):1575–89.PubMed Pankratz F, Bemtgen X, Zeiser R, et al. MicroRNA-155 exerts cell-specific antiangiogenic but proarteriogenic effects during adaptive neovascularization. Circulation. 2015;131(18):1575–89.PubMed
49.
go back to reference Sadik NA, Rashed LA, Abd-El Mawla MA. Circulating miR-155 and JAK2/STAT3 axis in acute ischemic stroke patients and its relation to post-ischemic inflammation and associated ischemic stroke risk factors. Int J Gen Med. 2021;14:1469–84. Sadik NA, Rashed LA, Abd-El Mawla MA. Circulating miR-155 and JAK2/STAT3 axis in acute ischemic stroke patients and its relation to post-ischemic inflammation and associated ischemic stroke risk factors. Int J Gen Med. 2021;14:1469–84.
50.
go back to reference Yang Z, Zheng B, Zhang Y, et al. miR-155-dependent regulation of mammalian sterile 20-like kinase 2 (MST2) coordinates inflammation, oxidative stress and proliferation in vascular smooth muscle cells. Biochim Biophys Acta. 2015;1852(7):1477–89.PubMed Yang Z, Zheng B, Zhang Y, et al. miR-155-dependent regulation of mammalian sterile 20-like kinase 2 (MST2) coordinates inflammation, oxidative stress and proliferation in vascular smooth muscle cells. Biochim Biophys Acta. 2015;1852(7):1477–89.PubMed
51.
go back to reference Zhang J, Fei Z, Xiaoling Y, Xiang L, Guofeng Z. MicroRNA-155 modulates the proliferation of vascular smooth muscle cells by targeting endothelial nitric oxide synthase. Int J Mol Med. 2015;35(6):1708–14.PubMed Zhang J, Fei Z, Xiaoling Y, Xiang L, Guofeng Z. MicroRNA-155 modulates the proliferation of vascular smooth muscle cells by targeting endothelial nitric oxide synthase. Int J Mol Med. 2015;35(6):1708–14.PubMed
52.
go back to reference Cheng R, Wu Z, Li M, Shao M, Hu T. Interleukin-1β is a potential therapeutic target for periodontitis: A narrative review. Int J Oral Sci. 2020;12(1):2.PubMedPubMedCentral Cheng R, Wu Z, Li M, Shao M, Hu T. Interleukin-1β is a potential therapeutic target for periodontitis: A narrative review. Int J Oral Sci. 2020;12(1):2.PubMedPubMedCentral
53.
go back to reference Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol. 2005;76(11):2075–84.PubMed Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol. 2005;76(11):2075–84.PubMed
54.
go back to reference Meurman JH, Sanz M, Janket SJ. Oral health, atherosclerosis, and cardiovascular disease. Crit Revs Oral Biol Med. 2004;15(6):403–13. Meurman JH, Sanz M, Janket SJ. Oral health, atherosclerosis, and cardiovascular disease. Crit Revs Oral Biol Med. 2004;15(6):403–13.
55.
go back to reference Schulz S, Schlitt A, Hofmann B, Schaller H, Reichert S. Periodontal pathogens and their role in cardiovascular outcome. J Clin Periodontol. 2020;47(2):173–81.PubMed Schulz S, Schlitt A, Hofmann B, Schaller H, Reichert S. Periodontal pathogens and their role in cardiovascular outcome. J Clin Periodontol. 2020;47(2):173–81.PubMed
56.
go back to reference Marfil-Álvarez R, Mesa F, Arrebola-Moreno A, et al. Acute myocardial infarct size is related to periodontitis extent and severity. J Dent Res. 2014;93(10):993–8.PubMedPubMedCentral Marfil-Álvarez R, Mesa F, Arrebola-Moreno A, et al. Acute myocardial infarct size is related to periodontitis extent and severity. J Dent Res. 2014;93(10):993–8.PubMedPubMedCentral
57.
go back to reference Zoheir N, Kurushima Y, Lin GH, Nibali L. Periodontal infectogenomics: A systematic review update of associations between host genetic variants and subgingival microbial detection. Clin Oral Invest. 2022;26(3):2209–21. Zoheir N, Kurushima Y, Lin GH, Nibali L. Periodontal infectogenomics: A systematic review update of associations between host genetic variants and subgingival microbial detection. Clin Oral Invest. 2022;26(3):2209–21.
Metadata
Title
MicroRNA‐155 (miR-155) as an accurate biomarker of periodontal status and coronary heart disease severity: a case–control study
Authors
Zina A. Daily
Batool Hassan Al-Ghurabi
Ahmed Makki A. Al-Qarakhli
Ryan Moseley
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/s12903-023-03584-w

Other articles of this Issue 1/2023

BMC Oral Health 1/2023 Go to the issue