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Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients

Received: 21 February 2024    Accepted: 4 March 2024    Published: 13 March 2024
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Abstract

Objective: Periodontitis and cardiovascular disease are prevalent entities that often coexist, with a common pro-inflammatory pathway. The objective of this study was to evaluate the association between periodontitis and cardiovascular pro-inflammatory parameters rarely considered within risk factors. Methods: Forty-three participants aged between 38-82 years were examined. An association between mean probing depth (MPD), mean attachment loss (MAL), bleeding on probing (BOP), and periodontal inflamed surface area (PISA) was correlated with the following cardiovascular disease factors and inflammatory promoters: neutrophil-to-lymphocyte ratio (NLR), 24h ambulatory blood pressure, global cardiovascular risk, daily salt intake, night-time systolic blood pressure (nSBP), and pulse wave velocity (PWV). A two-way ANOVA and multiple comparison tests were performed using SPSS statistics software. Results: A highly significant correlation (p<0.05) was found between BOP, MPD, and MAL with high salt intake, global cardiovascular risk estimation, nSBP, and PISA. Also, significantly statistical correlation (p<0.05) was found between BOP, NLR, and PWV while PISA was only associated with NLR. Logistic regression analysis identified absolute values of nSBP, salt intake and NLR as possible independent contributors to the increase in the log odds of developing BOP. Conclusions: Several periodontal disease parameters are linked to cardiovascular risk factors such as hypertension, neutrophil-to-lymphocyte ratio, daily salt intake and night-time systolic blood pressure.

Published in Cardiology and Cardiovascular Research (Volume 8, Issue 1)
DOI 10.11648/j.ccr.20240801.16
Page(s) 35-45
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Periodontal Disease, Inflammation, Salt Intake, Hypertension, Cardiovascular Risk, Pulse Wave Velocity

References
[1] Petersen PE, Ogawa H. The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontol 2000. 2012; 60(1): 15-39. https://doi.org/10.1111/j.1600-0757.2011.00425.x
[2] Vaduganathan M, Mensah GA, Turco JV, Fuster V, Roth GA. The Global Burden of Cardiovascular Diseases and Risk: A Compass for Future Health. J Am Coll Cardiol. 2022; 80(25): 2361-2371. https://doi.org/10.1016/j.jacc.2022.11.005
[3] Lockhart PB, Bolger AF, Papapanou PN, et al. Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association?: a scientific statement from the American Heart Association. Circulation. 2012; 125(20): 2520-2544. https://doi.org/10.1161/CIR.0b013e31825719f3
[4] Andriankaja OM, Genco RJ, Dorn J, et al. Periodontal disease and risk of myocardial infarction: the role of gender and smoking. Eur J Epidemiol. 2007; 22(10): 699-705. https://doi.org/10.1007/s10654-007-9166-6
[5] Bahekar AA, Singh S, Saha S, Molnar J, Arora R. The prevalence and incidence of coronary heart disease is significantly increased in periodontitis: a meta-analysis. Am Heart J. 2007; 154(5): 830-837. https://doi.org/10.1016/j.ahj.2007.06.037
[6] Cairo F, Castellani S, Gori AM, et al. Severe periodontitis in young adults is associated with sub-clinical atherosclerosis. J Clin Periodontol. 2008; 35(6): 465-472. https://doi.org/10.1111/j.1600-051X.2008.01228.x
[7] Friedewald VE, Kornman KS, Beck JD, et al. The American Journal of Cardiology and Journal of Periodontology editors' consensus: periodontitis and atherosclerotic cardiovascular disease. J Periodontol. 2009; 80(7): 1021-1032. https://doi.org/10.1902/jop.2009.097001
[8] Sanz M, Marco Del Castillo A, Jepsen S, et al. Periodontitis and cardiovascular diseases: Consensus report. J Clin Periodontol. 2020; 47(3): 268-288. https://doi.org/10.1111/jcpe.13189
[9] Kozarov E, Sweier D, Shelburne C, Progulske-Fox A, Lopatin D. Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect. 2006; 8(3): 687-693. https://doi.org/10.1016/j.micinf.2005.09.004
[10] Moreno S, Parra B, Botero JE, et al. [Periodontal microbiota and microorganisms isolated from heart valves in patients undergoing valve replacement surgery in a clinic in Cali, Colombia]. Biomedica. 2017; 37(4): 516-525. https://doi.org/10.7705/biomedica.v37i4.3232
[11] Nakano K, Inaba H, Nomura R, et al. Detection of cariogenic Streptococcus mutans in extirpated heart valve and atheromatous plaque specimens. J Clin Microbiol. 2006; 44(9): 3313-3317. https://doi.org/10.1128/JCM.00377-06
[12] de Araujo Nobre M, Malo P. Prevalence of periodontitis, dental caries, and peri-implant pathology and their relation with systemic status and smoking habits: Results of an open-cohort study with 22009 patients in a private rehabilitation center. J Dent. 2017; 67: 36-42. https://doi.org/10.1016/j.jdent.2017.07.013
[13] Hwang SY, Oh H, Rhee MY, Kang S, Kim HY. Association of periodontitis, missing teeth, and oral hygiene behaviors with the incidence of hypertension in middle-aged and older adults in Korea: A 10-year follow-up study. J Periodontol. 2022; 93(9): 1283-1293. https://doi.org/10.1002/JPER.21-0706
[14] Carrizales-Sepulveda EF, Ordaz-Farias A, Vera-Pineda R, Flores-Ramirez R. Periodontal Disease, Systemic Inflammation and the Risk of Cardiovascular Disease. Heart Lung Circ. 2018; 27(11): 1327-1334. https://doi.org/10.1016/j.hlc.2018.05.102
[15] 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 Suppl): 2075-2084. https://doi.org/10.1902/jop.2005.76.11-S.2075
[16] Kim J, Chun BJ, Moon JM, Cho Y. Prognostic value of neutrophil to lymphocyte ratio in the diagnosis of neurotoxicity after glufosinate ammonium poisoning. J Toxicol Environ Health A. 2022; 85(12): 511-519. https://doi.org/10.1080/15287394.2022.2040670
[17] Lee MJ, Park SD, Kwon SW, et al. Relation Between Neutrophil-to-Lymphocyte Ratio and Index of Microcirculatory Resistance in Patients With ST-Segment Elevation Myocardial Infarction Undergoing Primary Percutaneous Coronary Intervention. Am J Cardiol. 2016; 118(9): 1323-1328. https://doi.org/10.1016/j.amjcard.2016.07.072
[18] Salles GF, Reboldi G, Fagard RH, et al. Prognostic Effect of the Nocturnal Blood Pressure Fall in Hypertensive Patients: The Ambulatory Blood Pressure Collaboration in Patients With Hypertension (ABC-H) Meta-Analysis. Hypertension. 2016; 67(4): 693-700. https://doi.org/10.1161/HYPERTENSIONAHA.115.06981
[19] Sega R, Facchetti R, Bombelli M, et al. Prognostic value of ambulatory and home blood pressures compared with office blood pressure in the general population: follow-up results from the Pressioni Arteriose Monitorate e Loro Associazioni (PAMELA) study. Circulation. 2005; 111(14): 1777-1783. https://doi.org/10.1161/01.CIR.0000160923.04524.5B
[20] He FJ, Tan M, Ma Y, MacGregor GA. Salt Reduction to Prevent Hypertension and Cardiovascular Disease: JACC State-of-the-Art Review. J Am Coll Cardiol. 2020; 75(6): 632-647. https://doi.org/10.1016/j.jacc.2019.11.055
[21] Wilck N, Matus MG, Kearney SM, et al. Salt-responsive gut commensal modulates T(H)17 axis and disease. Nature. 2017; 551(7682): 585-589. https://doi.org/10.1038/nature24628
[22] American Heart Association Rheumatic Fever E. Prevention Guidelines Tool CV Risk Calculator. 2018; https://static.heart.org/riskcalc/app/index.html#!/baseline-risk. Accessed 25.05.2023, 2023.
[23] Carranza FA. Carranza'S Clinical Periodontology (10Th Edition). Elsevier (A Divisionof Reed Elsevier India Pvt. Limited); 2006.
[24] Grant D. SI, Listgarten M. Periodontics. Vol 6th ed. 1988.
[25] Goldman, H. M., and Cohen, W. D.: Periodontal Therapy, 4th ed, St. Louis, C. V. Mosby Co., 1968, p 245
[26] Baelum V, Manji F, Wanzala P, Fejerskov O. Relationship between CPITN and periodontal attachment loss findings in an adult population. J Clin Periodontol. 1995; 22(2): 146-152. https://doi.org/10.1111/j.1600-051x.1995.tb00126.x
[27] Dye BA, Selwitz RH. The relationship between selected measures of periodontal status and demographic and behavioural risk factors. J Clin Periodontol. 2005; 32(7): 798-808. https://doi.org/10.1111/j.1600-051X.2005.00742.x
[28] Nesse W, Abbas F, van der Ploeg I, Spijkervet FK, Dijkstra PU, Vissink A. Periodontal inflamed surface area: quantifying inflammatory burden. J Clin Periodontol. 2008; 35(8): 668-673. https://doi.org/10.1111/j.1600-051X.2008.01249.x
[29] Jockel-Schneider Y, Bechtold M, Haubitz I, et al. Impact of anti-infective periodontal therapy on parameters of vascular health. J Clin Periodontol. 2018; 45(3): 354-363. https://doi.org/10.1111/jcpe.12849
[30] Susanto H, Nesse W, Dijkstra PU, et al. Periodontal inflamed surface area and C-reactive protein as predictors of HbA1c: a study in Indonesia. Clin Oral Investig. 2012; 16(4): 1237-1242. https://doi.org/10.1007/s00784-011-0621-0
[31] Monteiro A, Castro P, Pereira G, et al. Could salt intake directly affect the cerebral microvasculature in hypertension? J Stroke Cerebrovasc Dis. 2022; 31(9): 106632. https://doi.org/10.1016/j.jstrokecerebrovasdis.2022.106632
[32] Polonia J, Martins L, Pinto F, Nazare J. Prevalence, awareness, treatment and control of hypertension and salt intake in Portugal: changes over a decade. The PHYSA study. J Hypertens. 2014 32(6): 1211-1221. https://doi.org/10.1097/HJH.0000000000000162
[33] Cutress TW, Ainamo J, Sardo-Infirri J. The community periodontal index of treatment needs (CPITN) procedure for population groups and individuals. Int Dent J. 1987; 37(4): 222-233.
[34] Caton JG, Armitage G, Berglundh T, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Clin Periodontol. 2018; 45 Suppl 20: S1-S8. https://doi.org/10.1111/jcpe.12935
[35] Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975; 25(4): 229-235.
[36] Rouxinol-Dias A, Araujo S, Silva JA, Barbosa L, Polonia J. Association between ambulatory blood pressure values and central aortic pressure in a large population of normotensive and hypertensive patients. Blood Press Monit. 2018; 23(1): 24-32. https://doi.org/10.1097/MBP.0000000000000287
[37] Williams B, Mancia G, Spiering W, et al. 2018 Practice Guidelines for the management of arterial hypertension of the European Society of Hypertension and the European Society of Cardiology: ESH/ESC Task Force for the Management of Arterial Hypertension. J Hypertens. 2018; 36(12): 2284-2309. https://doi.org/10.1097/HJH.0000000000001961
[38] Li LH, Chen CT, Chang YC, Chen YJ, Lee IH, How CK. Prognostic role of neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, and systemic immune inflammation index in acute ischemic stroke: A STROBE-compliant retrospective study. Medicine (Baltimore). 2021; 100(25): e26354. https://doi.org/10.1097/MD.0000000000026354
[39] Li W, Hou M, Ding Z, Liu X, Shao Y, Li X. Prognostic Value of Neutrophil-to-Lymphocyte Ratio in Stroke: A Systematic Review and Meta-Analysis. Front Neurol. 2021; 12: 686983. https://doi.org/10.3389/fneur.2021.686983
[40] Polonia JJ, Magalhaes MT, Senra D, Barbosa L, Silva JA, Ribeiro SM. Association of 24-h urinary salt excretion with central haemodynamics and assessment of food categories contributing to salt consumption in Portuguese patients with hypertension. Blood Press Monit. 2013; 18(6): 303-310. https://doi.org/10.1097/MBP.0000000000000005
[41] Jayedi A, Ghomashi F, Zargar MS, Shab-Bidar S. Dietary sodium, sodium-to-potassium ratio, and risk of stroke: A systematic review and nonlinear dose-response meta-analysis. Clin Nutr. 2019; 38(3): 1092-1100. https://doi.org/10.1016/j.clnu.2018.05.017
[42] Beck JD, Eke P, Heiss G, et al. Periodontal disease and coronary heart disease: a reappraisal of the exposure. Circulation. 2005; 112(1): 19-24. https://doi.org/10.1161/CIRCULATIONAHA.104.511998
[43] Eke PI, Borgnakke WS, Genco RJ. Recent epidemiologic trends in periodontitis in the USA. Periodontol 2000. 2020; 82(1): 257-267. https://doi.org/10.1111/prd.12323
[44] Munoz Aguilera E, Suvan J, Buti J, et al. Periodontitis is associated with hypertension: a systematic review and meta-analysis. Cardiovasc Res. 2020; 116(1): 28-39. https://doi.org/10.1093/cvr/cvz201
[45] Krzeminska J, Wronka M, Mlynarska E, Franczyk B, Rysz J. Arterial Hypertension-Oxidative Stress and Inflammation. Antioxidants (Basel). 2022; 11(1). https://doi.org/10.3390/antiox11010172
[46] Lanau N, Mareque-Bueno J, Zabalza M. Does Periodontal Treatment Help in Arterial Hypertension Control? A Systematic Review of Literature. Eur J Dent. 2021; 15(1): 168-173. https://doi.org/10.1055/s-0040-1718244
Cite This Article
  • APA Style

    Pinto-Ribeiro, T., Faria-Almeida, R., Monteiro, A., Souza, J. C. M., Felino, A., et al. (2024). Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients. Cardiology and Cardiovascular Research, 8(1), 35-45. https://doi.org/10.11648/j.ccr.20240801.16

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    ACS Style

    Pinto-Ribeiro, T.; Faria-Almeida, R.; Monteiro, A.; Souza, J. C. M.; Felino, A., et al. Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients. Cardiol. Cardiovasc. Res. 2024, 8(1), 35-45. doi: 10.11648/j.ccr.20240801.16

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    AMA Style

    Pinto-Ribeiro T, Faria-Almeida R, Monteiro A, Souza JCM, Felino A, et al. Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients. Cardiol Cardiovasc Res. 2024;8(1):35-45. doi: 10.11648/j.ccr.20240801.16

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  • @article{10.11648/j.ccr.20240801.16,
      author = {Tiago Pinto-Ribeiro and Ricardo Faria-Almeida and Ana Monteiro and Júlio César Matias Souza and António Felino and Jorge Polónia},
      title = {Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients},
      journal = {Cardiology and Cardiovascular Research},
      volume = {8},
      number = {1},
      pages = {35-45},
      doi = {10.11648/j.ccr.20240801.16},
      url = {https://doi.org/10.11648/j.ccr.20240801.16},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ccr.20240801.16},
      abstract = {Objective: Periodontitis and cardiovascular disease are prevalent entities that often coexist, with a common pro-inflammatory pathway. The objective of this study was to evaluate the association between periodontitis and cardiovascular pro-inflammatory parameters rarely considered within risk factors. Methods: Forty-three participants aged between 38-82 years were examined. An association between mean probing depth (MPD), mean attachment loss (MAL), bleeding on probing (BOP), and periodontal inflamed surface area (PISA) was correlated with the following cardiovascular disease factors and inflammatory promoters: neutrophil-to-lymphocyte ratio (NLR), 24h ambulatory blood pressure, global cardiovascular risk, daily salt intake, night-time systolic blood pressure (nSBP), and pulse wave velocity (PWV). A two-way ANOVA and multiple comparison tests were performed using SPSS statistics software. Results: A highly significant correlation (plog odds of developing BOP. Conclusions: Several periodontal disease parameters are linked to cardiovascular risk factors such as hypertension, neutrophil-to-lymphocyte ratio, daily salt intake and night-time systolic blood pressure.
    },
     year = {2024}
    }
    

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  • TY  - JOUR
    T1  - Association of Periodontitis with Ambulatory Blood Pressure, Salt Intake, and Neutrophil-Lymphocyte Ratio in High-Risk Hypertensive Patients
    AU  - Tiago Pinto-Ribeiro
    AU  - Ricardo Faria-Almeida
    AU  - Ana Monteiro
    AU  - Júlio César Matias Souza
    AU  - António Felino
    AU  - Jorge Polónia
    Y1  - 2024/03/13
    PY  - 2024
    N1  - https://doi.org/10.11648/j.ccr.20240801.16
    DO  - 10.11648/j.ccr.20240801.16
    T2  - Cardiology and Cardiovascular Research
    JF  - Cardiology and Cardiovascular Research
    JO  - Cardiology and Cardiovascular Research
    SP  - 35
    EP  - 45
    PB  - Science Publishing Group
    SN  - 2578-8914
    UR  - https://doi.org/10.11648/j.ccr.20240801.16
    AB  - Objective: Periodontitis and cardiovascular disease are prevalent entities that often coexist, with a common pro-inflammatory pathway. The objective of this study was to evaluate the association between periodontitis and cardiovascular pro-inflammatory parameters rarely considered within risk factors. Methods: Forty-three participants aged between 38-82 years were examined. An association between mean probing depth (MPD), mean attachment loss (MAL), bleeding on probing (BOP), and periodontal inflamed surface area (PISA) was correlated with the following cardiovascular disease factors and inflammatory promoters: neutrophil-to-lymphocyte ratio (NLR), 24h ambulatory blood pressure, global cardiovascular risk, daily salt intake, night-time systolic blood pressure (nSBP), and pulse wave velocity (PWV). A two-way ANOVA and multiple comparison tests were performed using SPSS statistics software. Results: A highly significant correlation (plog odds of developing BOP. Conclusions: Several periodontal disease parameters are linked to cardiovascular risk factors such as hypertension, neutrophil-to-lymphocyte ratio, daily salt intake and night-time systolic blood pressure.
    
    VL  - 8
    IS  - 1
    ER  - 

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Author Information
  • Department of Oral Surgery and Periodontology, Faculty of Dental Medicine (FMDUP), University of Porto, Porto, Portugal

  • Department of Oral Surgery and Periodontology, Faculty of Dental Medicine (FMDUP), University of Porto, Porto, Portugal; Associated Laboratory for Green Chemistry (LAQV) of the Network of Chemistry and Technology (REQUIMTE), Porto, Portugal

  • Department of Clinical Neurosciences and Mental Health, Faculty of Medicine, University of Porto, Porto, Portugal; Hospital Lusíadas Braga, Braga, Portugal; Blueclinical, Matosinhos, Portugal

  • Center for MicroElectroMechanical Systems (CMEMS-UMINHO), University of Minho, Campus Azurém, Guimarães, Portugal; LABBELS Associate Laboratory, University of Minho, Guimarães, Braga, Portugal; Center for Interdisciplinary Research in Health (CIIS), Faculty of Dental Medicine (FMD), Catholic University of Portugal (UCP), Viseu, Portugal

  • Department of Oral Surgery and Periodontology, Faculty of Dental Medicine (FMDUP), University of Porto, Porto, Portugal

  • Department of Medicine, CINTESIS, Faculty of Medicine, University of Porto, Porto, Portugal; Blood Pressure Unit, Hospital Pedro Hispano, Matosinhos, Portugal

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