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Published in: Clinical Oral Investigations 7/2017

01-09-2017 | Original Article

Salivary oxidative stress biomarkers in chronic periodontitis and acute coronary syndrome

Authors: Thuy T. Nguyen, Lan Q. Ngo, Ananya Promsudthi, Rudee Surarit

Published in: Clinical Oral Investigations | Issue 7/2017

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Abstract

Objectives

The study aimed at assessing oxidative stress (OS) biomarker levels in the saliva of patients with chronic periodontitis (CP) and acute coronary syndrome (ACS) and establishing their correlation to periodontal parameters and markers for cardiovascular events.

Materials and methods

The present study enrolled 24 patients with ACS and CP (the ACSCP group), 24 patients with ACS only (the ACS group), 24 patients with CP only (the CP group), and 24 healthy controls. Plaque index (PI), gingival index, bleeding on probing, probing pocket depth (PPD), and clinical attachment loss were recorded. Markers for cardiovascular events included serum high sensitivity C-reactive protein (hsCRP) and plasma fibrinogen. 8-Hydroxydeoxyguanosine (8-OHdG), protein carbonyl (PC), malondialdehyde (MDA), and total antioxidant capacity (TAOC) were used as OS biomarkers.

Results

Salivary 8-OHdG, MDA, and PC levels were significantly higher in the ACSCP, ACS, and CP groups than in healthy controls (p < 0.05). There were significant correlations between salivary PC levels and PI or PPD (p < 0.05) as well as between salivary 8-OHdG levels and all periodontal parameters (p < 0.05). TAOC levels in saliva were correlated to both serum hsCRP and plasma fibrinogen (p < 0.05). Salivary MDA levels were correlated to all periodontal parameters and biomarkers for cardiovascular events (p < 0.05).

Conclusions

Salivary OS biomarker levels were higher in diseased groups compared to control. They also correlated to clinical periodontal parameters and markers for cardiovascular events in ACS patients, with or without CP.

Clinical relevance

Salivary OS biomarkers could potentially serve as diagnostic tools for cardiovascular and/or periodontal diseases.
Literature
2.
go back to reference Khan R, Harvey D, Leistikow B, Haque K, Stewart C (2015) Relationship between obesity and coronary heart disease among urban Bangladeshi men and women. Integr Obes Diabetes 1(3):49–55PubMedPubMedCentral Khan R, Harvey D, Leistikow B, Haque K, Stewart C (2015) Relationship between obesity and coronary heart disease among urban Bangladeshi men and women. Integr Obes Diabetes 1(3):49–55PubMedPubMedCentral
6.
go back to reference Buczko P, Zalewska A, Szarmach I (2015) Saliva and oxidative stress in oral cavity and in some systemic disorders. J Physiol Pharmacol 66(1):3–9PubMed Buczko P, Zalewska A, Szarmach I (2015) Saliva and oxidative stress in oral cavity and in some systemic disorders. J Physiol Pharmacol 66(1):3–9PubMed
9.
go back to reference Fentoglu O, Kirzioglu FY, Bulut MT, Kumbul Doguc D, Kulac E, Onder C, Gunhan M (2015) Evaluation of lipid peroxidation and oxidative DNA damage in patients with periodontitis and hyperlipidemia. J Periodontol 86(5):682–688. doi:10.1902/jop.2015.140561 CrossRefPubMed Fentoglu O, Kirzioglu FY, Bulut MT, Kumbul Doguc D, Kulac E, Onder C, Gunhan M (2015) Evaluation of lipid peroxidation and oxidative DNA damage in patients with periodontitis and hyperlipidemia. J Periodontol 86(5):682–688. doi:10.​1902/​jop.​2015.​140561 CrossRefPubMed
10.
go back to reference El-Shinnawi U, Soory M (2015) Actions of adjunctive nutritional antioxidants in periodontitis and prevalent systemic inflammatory diseases. Endocr Metab Immune Disord Drug Targets 15(4):261–276CrossRefPubMed El-Shinnawi U, Soory M (2015) Actions of adjunctive nutritional antioxidants in periodontitis and prevalent systemic inflammatory diseases. Endocr Metab Immune Disord Drug Targets 15(4):261–276CrossRefPubMed
11.
go back to reference Wheatley-Price P, Asomaning K, Reid A, Zhai R, Su L, Zhou W, Zhu A, Ryan DP, Christiani DC, Liu G (2008) Myeloperoxidase and superoxide dismutase polymorphisms are associated with an increased risk of developing pancreatic adenocarcinoma. Cancer 112(5):1037–1042. doi:10.1002/cncr.23267 CrossRefPubMed Wheatley-Price P, Asomaning K, Reid A, Zhai R, Su L, Zhou W, Zhu A, Ryan DP, Christiani DC, Liu G (2008) Myeloperoxidase and superoxide dismutase polymorphisms are associated with an increased risk of developing pancreatic adenocarcinoma. Cancer 112(5):1037–1042. doi:10.​1002/​cncr.​23267 CrossRefPubMed
12.
14.
16.
go back to reference Dede FO, Ozden FO, Avci B (2013) 8-Hydroxy-deoxyguanosine levels in gingival crevicular fluid and saliva in patients with chronic periodontitis after initial periodontal treatment. J Periodontol 84(6):821–828. doi:10.1902/jop.2012.120195 CrossRefPubMed Dede FO, Ozden FO, Avci B (2013) 8-Hydroxy-deoxyguanosine levels in gingival crevicular fluid and saliva in patients with chronic periodontitis after initial periodontal treatment. J Periodontol 84(6):821–828. doi:10.​1902/​jop.​2012.​120195 CrossRefPubMed
17.
go back to reference Trivedi S, Lal N, Mahdi AA, Singh B, Pandey S (2015) Association of salivary lipid peroxidation levels, antioxidant enzymes, and chronic periodontitis. Int J Periodontics Restorative Dent 35(2):e14–e19. doi:10.11607/prd.2079 CrossRefPubMed Trivedi S, Lal N, Mahdi AA, Singh B, Pandey S (2015) Association of salivary lipid peroxidation levels, antioxidant enzymes, and chronic periodontitis. Int J Periodontics Restorative Dent 35(2):e14–e19. doi:10.​11607/​prd.​2079 CrossRefPubMed
18.
go back to reference Kurgan S, Onder C, Altingoz SM, Bagis N, Uyanik M, Serdar MA, Kantarci A (2015) High sensitivity detection of salivary 8-hydroxy deoxyguanosine levels in patients with chronic periodontitis. J Periodontal Res 50(6):766–774. doi:10.1111/jre.12263 CrossRefPubMed Kurgan S, Onder C, Altingoz SM, Bagis N, Uyanik M, Serdar MA, Kantarci A (2015) High sensitivity detection of salivary 8-hydroxy deoxyguanosine levels in patients with chronic periodontitis. J Periodontal Res 50(6):766–774. doi:10.​1111/​jre.​12263 CrossRefPubMed
19.
go back to reference Miricescu D, Totan A, Calenic B, Mocanu B, Didilescu A, Mohora M, Spinu T, Greabu M (2014) Salivary biomarkers: relationship between oxidative stress and alveolar bone loss in chronic periodontitis. Acta Odontol Scand 72(1):42–47. doi:10.3109/00016357.2013.795659 CrossRefPubMed Miricescu D, Totan A, Calenic B, Mocanu B, Didilescu A, Mohora M, Spinu T, Greabu M (2014) Salivary biomarkers: relationship between oxidative stress and alveolar bone loss in chronic periodontitis. Acta Odontol Scand 72(1):42–47. doi:10.​3109/​00016357.​2013.​795659 CrossRefPubMed
20.
go back to reference Wei D, Zhang XL, Wang YZ, Yang CX, Chen G (2010) Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust Dent J 55(1):70–78. doi:10.1111/j.1834-7819.2009.01123.x CrossRefPubMed Wei D, Zhang XL, Wang YZ, Yang CX, Chen G (2010) Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust Dent J 55(1):70–78. doi:10.​1111/​j.​1834-7819.​2009.​01123.​x CrossRefPubMed
22.
go back to reference Simon AS, Chithra V, Vijayan A, Dinesh RD, Vijayakumar T (2013) Altered DNA repair, oxidative stress and antioxidant status in coronary artery disease. J Biosci 38(2):385–389CrossRefPubMed Simon AS, Chithra V, Vijayan A, Dinesh RD, Vijayakumar T (2013) Altered DNA repair, oxidative stress and antioxidant status in coronary artery disease. J Biosci 38(2):385–389CrossRefPubMed
23.
go back to reference Turan T, Mentese U, Agac MT, Akyuz AR, Kul S, Aykan AC, Bektas H, Korkmaz L, Oztas Mentese S, Dursun I, Celik S (2015) The relation between intensity and complexity of coronary artery lesion and oxidative stress in patients with acute coronary syndrome. Anatol J Cardiol 15(10):795–800. doi:10.5152/akd.2014.5761 CrossRefPubMed Turan T, Mentese U, Agac MT, Akyuz AR, Kul S, Aykan AC, Bektas H, Korkmaz L, Oztas Mentese S, Dursun I, Celik S (2015) The relation between intensity and complexity of coronary artery lesion and oxidative stress in patients with acute coronary syndrome. Anatol J Cardiol 15(10):795–800. doi:10.​5152/​akd.​2014.​5761 CrossRefPubMed
24.
26.
go back to reference Mutlu-Turkoglu U, Akalin Z, Ilhan E, Yilmaz E, Bilge A, Nisanci Y, Uysal M (2005) Increased plasma malondialdehyde and protein carbonyl levels and lymphocyte DNA damage in patients with angiographically defined coronary artery disease. Clin Biochem 38(12):1059–1065. doi:10.1016/j.clinbiochem.2005.07.001 CrossRefPubMed Mutlu-Turkoglu U, Akalin Z, Ilhan E, Yilmaz E, Bilge A, Nisanci Y, Uysal M (2005) Increased plasma malondialdehyde and protein carbonyl levels and lymphocyte DNA damage in patients with angiographically defined coronary artery disease. Clin Biochem 38(12):1059–1065. doi:10.​1016/​j.​clinbiochem.​2005.​07.​001 CrossRefPubMed
33.
go back to reference Sculley DV, Langley-Evans SC (2003) Periodontal disease is associated with lower antioxidant capacity in whole saliva and evidence of increased protein oxidation. Clin Sci (Lond) 105(2):167–172. doi:10.1042/CS20030031 CrossRef Sculley DV, Langley-Evans SC (2003) Periodontal disease is associated with lower antioxidant capacity in whole saliva and evidence of increased protein oxidation. Clin Sci (Lond) 105(2):167–172. doi:10.​1042/​CS20030031 CrossRef
34.
36.
go back to reference Zare Javid A, Seal CJ, Heasman P, Moynihan PJ (2014) Impact of a customised dietary intervention on antioxidant status, dietary intakes and periodontal indices in patients with adult periodontitis. J Hum Nutr Diet 27(6):523–532. doi:10.1111/jhn.12184 CrossRefPubMed Zare Javid A, Seal CJ, Heasman P, Moynihan PJ (2014) Impact of a customised dietary intervention on antioxidant status, dietary intakes and periodontal indices in patients with adult periodontitis. J Hum Nutr Diet 27(6):523–532. doi:10.​1111/​jhn.​12184 CrossRefPubMed
37.
go back to reference Braunwald E, Antman EM, Beasley JW, Califf RM, Cheitlin MD, Hochman JS, Jones RH, Kereiakes D, Kupersmith J, Levin TN, Pepine CJ, Schaeffer JW, Smith EE 3rd, Steward DE, Theroux P, Gibbons RJ, Alpert JS, Eagle KA, Faxon DP, Fuster V, Gardner TJ, Gregoratos G, Russell RO, Smith SC Jr (2000) ACC/AHA guidelines for the management of patients with unstable angina and non-ST-segment elevation myocardial infarction: executive summary and recommendations. A report of the American College of Cardiology/American Heart Association task force on practice guidelines (committee on the management of patients with unstable angina). Circulation 102(10):1193–1209CrossRefPubMed Braunwald E, Antman EM, Beasley JW, Califf RM, Cheitlin MD, Hochman JS, Jones RH, Kereiakes D, Kupersmith J, Levin TN, Pepine CJ, Schaeffer JW, Smith EE 3rd, Steward DE, Theroux P, Gibbons RJ, Alpert JS, Eagle KA, Faxon DP, Fuster V, Gardner TJ, Gregoratos G, Russell RO, Smith SC Jr (2000) ACC/AHA guidelines for the management of patients with unstable angina and non-ST-segment elevation myocardial infarction: executive summary and recommendations. A report of the American College of Cardiology/American Heart Association task force on practice guidelines (committee on the management of patients with unstable angina). Circulation 102(10):1193–1209CrossRefPubMed
38.
go back to reference Antman EM, Anbe DT, Armstrong PW, Bates ER, Green LA, Hand M, Hochman JS, Krumholz HM, Kushner FG, Lamas GA, Mullany CJ, Ornato JP, Pearle DL, Sloan MA, Smith SC Jr, Alpert JS, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Gregoratos G, Halperin JL, Hiratzka LF, Hunt SA, Jacobs AK, Ornato JP (2004) ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction; a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Revise the 1999 Guidelines for the Management of patients with acute myocardial infarction). J Am Coll Cardiol 44(3):E1–E211. doi:10.1016/j.jacc.2004.07.014 CrossRefPubMed Antman EM, Anbe DT, Armstrong PW, Bates ER, Green LA, Hand M, Hochman JS, Krumholz HM, Kushner FG, Lamas GA, Mullany CJ, Ornato JP, Pearle DL, Sloan MA, Smith SC Jr, Alpert JS, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Gregoratos G, Halperin JL, Hiratzka LF, Hunt SA, Jacobs AK, Ornato JP (2004) ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction; a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Revise the 1999 Guidelines for the Management of patients with acute myocardial infarction). J Am Coll Cardiol 44(3):E1–E211. doi:10.​1016/​j.​jacc.​2004.​07.​014 CrossRefPubMed
40.
go back to reference Silness J, Löe H (1964) Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135CrossRefPubMed Silness J, Löe H (1964) Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135CrossRefPubMed
41.
go back to reference Löe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38:610–616CrossRef Löe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38:610–616CrossRef
42.
go back to reference Joss A, Adler R, Lang NP (1994) Bleeding on probing. A parameter for monitoring periodontal conditions in clinical practice. J Clin Periodontol 21:402–408CrossRefPubMed Joss A, Adler R, Lang NP (1994) Bleeding on probing. A parameter for monitoring periodontal conditions in clinical practice. J Clin Periodontol 21:402–408CrossRefPubMed
44.
go back to reference Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358CrossRefPubMed Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358CrossRefPubMed
45.
go back to reference Mackie IJ, Kitchen S, Machin SJ, Lowe GD, Haemostasis, Thrombosis Task Force of the British Committee for Standards in H (2003) Guidelines on fibrinogen assays. Br J Haematol 121(3):396–404CrossRefPubMed Mackie IJ, Kitchen S, Machin SJ, Lowe GD, Haemostasis, Thrombosis Task Force of the British Committee for Standards in H (2003) Guidelines on fibrinogen assays. Br J Haematol 121(3):396–404CrossRefPubMed
47.
go back to reference Dietrich T, Sharma P, Walter C, Weston P, Beck J (2013) The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. J Periodontol 84(4-s):S70–S84. doi:10.1902/jop.2013.134008 CrossRefPubMed Dietrich T, Sharma P, Walter C, Weston P, Beck J (2013) The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. J Periodontol 84(4-s):S70–S84. doi:10.​1902/​jop.​2013.​134008 CrossRefPubMed
49.
go back to reference Henson B, Wong D (2010) Collection, storage, and processing of saliva samples for downstream molecular applications. In: Seymour GJ, Cullinan MP, Heng NCK (eds) Oral biology: molecular techniques and applications, vol 666. Humana, New York, pp 21–30CrossRef Henson B, Wong D (2010) Collection, storage, and processing of saliva samples for downstream molecular applications. In: Seymour GJ, Cullinan MP, Heng NCK (eds) Oral biology: molecular techniques and applications, vol 666. Humana, New York, pp 21–30CrossRef
50.
52.
go back to reference Lee M-S, Flammer AJ, Li J, Lennon RJ, Delacroix S, Kim H, Lerman A (2015) Comparison of time trends of cardiovascular disease risk factors and Framingham risk score between patients with and without acute coronary syndrome undergoing percutaneous intervention over the last 17 years: from the Mayo Clinic percutaneous coronary intervention registry. Clin Cardiol 38(12):747–756. doi:10.1002/clc.22484 CrossRefPubMed Lee M-S, Flammer AJ, Li J, Lennon RJ, Delacroix S, Kim H, Lerman A (2015) Comparison of time trends of cardiovascular disease risk factors and Framingham risk score between patients with and without acute coronary syndrome undergoing percutaneous intervention over the last 17 years: from the Mayo Clinic percutaneous coronary intervention registry. Clin Cardiol 38(12):747–756. doi:10.​1002/​clc.​22484 CrossRefPubMed
54.
go back to reference Ridker PM (2003) Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107(3):363–369CrossRefPubMed Ridker PM (2003) Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107(3):363–369CrossRefPubMed
55.
go back to reference Shojaie M, Pourahmad M, Eshraghian A, Izadi HR, Naghshvar F (2009) Fibrinogen as a risk factor for premature myocardial infarction in Iranian patients: a case control study. Vasc Health Risk Manag 5:673–676PubMedPubMedCentral Shojaie M, Pourahmad M, Eshraghian A, Izadi HR, Naghshvar F (2009) Fibrinogen as a risk factor for premature myocardial infarction in Iranian patients: a case control study. Vasc Health Risk Manag 5:673–676PubMedPubMedCentral
Metadata
Title
Salivary oxidative stress biomarkers in chronic periodontitis and acute coronary syndrome
Authors
Thuy T. Nguyen
Lan Q. Ngo
Ananya Promsudthi
Rudee Surarit
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 7/2017
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-2029-3

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