EVALUATİON OF OXİDATİVE STATUS İN PATİENTS WİTH CHRONİC PERİODONTİTİS AND ADDİTİONAL TOBACCO ABUSE: A CROSS-SECTİONAL STUDY

Yıl 2020, Cilt: 30 Sayı: 4, 536 - 544, 15.10.2020

Didem Özkal Eminoğlu Varol Çanakçı

https://doi.org/10.17567/ataunidfd.778795

Öz

Aim: The aim of the present study was to investigate the 8-hydroxy-2´deoxyguanosine (8-OHdG) and melatonin (MLT) levels in saliva as well as myeloperoxidase (MPO) levels in gingival clevicular fluid (GCF) in smoker and nonsmoker chronic periodontitis (CP) patients and periodontally healthy individuals.
Methods: 4 groups of 15 applicants were formed in accordance with the research protocole as follows; periodontally healthy nonsmokers (CP-S-), periodontally healthy smokers (CP-S+), nonsmoker periodontitis patients (CP+S-) and smoker periodontitis patients (CP+S+). Clinical periodontal parameters were recorded before taking the GCF and saliva samples. 8-OHdG, MLT and MPO levels were measured biochemically.
Results: The lowest 8-OHdG and MPO levels were recorded in the (CP-S-) group (p<0.05). 8-OHdG and MPO levels were statistically higher in (CP-S+) group than (CP-S-) group (p<0.05). MLT levels in saliva were statistically higher in periodontally healthy (CP-) groups than CP groups (p<0.05).
Conclusions: CP causes a significant difference on the parameters connected with oxidative stress. For periodontally healthy applicants, smoking leads to statistically significant changes on the parameters in general; while the effect of smoking to the parameters was found insignificant in the CP groups. Findings of this study reveal the role of smoking on the development of periodontitis, due to negatively affecting the parameters linked to oxidative stress, that are crucial in the patogenesis of periodontal diseases.
KEY WORDS: 8-hydroxy-2´-deoxyguanosine (8-OHdG), chronic periodontitis (CP), melatonin (MLT), myeloperoxidase (MPO), oxidative stres (OS), smoking, tobacco.

Kronik Periodontitis Ve Sigara Kullananımının Oksidatif Durum Üzerine Olan Etkisinin Değerlendirilmesi
Öz
Amaç: Bu çalışmanın amacı; kronik periodontitisli ve periodontal açıdan sağlıklı bireylerin DOS ve tükürük numunelerinde sigaranın MLT, MPO ve 8-OHdG düzeyleri üzerine muhtemel etkilerinin değerlendirilmesidir.
Gereç ve yöntem : Çalışma protokolü gereği her biri 15 katılımcıdan oluşan 4 grup oluşturuldu; periodontal olarak sağlıklı ve sigara içemeyen grup (P-S-), periodontal olarak sağlıklı ve sigara içen grup (P-S+), kronik periodontitisli ve sigara içmeyen grup (P+S-) ile kronik periodontitisli ve sigara içen grup (P+S+). DOS ve tükürük örnekleri alınmadan önce klinik periodontal parametreler kaydedildi. MLT, MPO ve 8-OHdG düzeyleri biyokimyasal ve olarak ölçüldü.
Bulgular : En yüksek MPO ve 8-OHdGdüzeyleri ile en düşük MLT düzeyleri (P+S+) grubunda tespit edildi. En yüksek MLT düzeyi ise (P-S-) grubunda gözlendi. Sigara kullanımı ve kronik periodontitisin biyokimyasal ve histopatolojik parametreleri benzer şekilde etkilediği tespit edildi.
Sonuç : KP’nin oksidatif stres ile ilişkili parametrelerde anlamlı düzeyde farklılık oluşturduğu gözlendi. Sigara kullanımının genel olarak periodontal sağlıklı bireylerde parametrelerde belirgin bir değişime yol açtığı, periodontitisli gruplarda ise bu değişimin istatistiksel olarak anlamlı olmadığı görüldü. Bulgularımız, sigara içmenin periodontal hastalıkların patogenezinde rol alan oksitatif parametreleri olumsuz yönde etkileyerek periodontitis gelişiminde rol oynayabileceğini göstermektedir.
Anahtar Kelimeler: Isı şok proteinleri 60-70, kronik periodontitis, melatonin, myeloperoksidaz, oksitatif stress, sigara, 8-hydroxy-2'-deoxyguanosine.

Anahtar Kelimeler

8-hydroxy-2´-deoxyguanosine (8-OHdG), chronic periodontitis (CP), melatonin (MLT)

EVALUATION OF THE EFFECT OF CHRONIC PERIODONTITIS AND ADDITIONAL TOBACCO ABUSE ON OXIDATIVE STATUS : A CROSS-SECTIONAL STUDY

Öz

Aim: The aim of the present study was to investigate the 8-hydroxy-2´deoxyguanosine (8-OHdG) and melatonin (MLT) levels in saliva as well as myeloperoxidase (MPO) levels in gingival clevicular fluid (GCF) in smoker and nonsmoker chronic periodontitis (CP) patients and periodontally healthy individuals.
Methods: 4 groups of 15 applicants were formed in accordance with the research protocole as follows; periodontally healthy nonsmokers (CP-S-), periodontally healthy smokers (CP-S+), nonsmoker periodontitis patients (CP+S-) and smoker periodontitis patients (CP+S+). Clinical periodontal parameters were recorded before taking the GCF and saliva samples. 8-OHdG, MLT and MPO levels were measured biochemically.
Results: The lowest 8-OHdG and MPO levels were recorded in the (CP-S-) group (p<0.05). 8-OHdG and MPO levels were statistically higher in (CP-S+) group than (CP-S-) group (p<0.05). MLT levels in saliva were statistically higher in periodontally healthy (CP-) groups than CP groups (p<0.05).
Conclusions: CP causes a significant difference on the parameters connected with oxidative stress. For periodontally healthy applicants, smoking leads to statistically significant changes on the parameters in general; while the effect of smoking to the parameters was found insignificant in the CP groups. Findings of this study reveal the role of smoking on the development of periodontitis, due to negatively affecting the parameters linked to oxidative stress, that are crucial in the patogenesis of periodontal diseases.
KEY WORDS: 8-hydroxy-2´-deoxyguanosine (8-OHdG), chronic periodontitis (CP), melatonin (MLT), myeloperoxidase (MPO), oxidative stres (OS), smoking, tobacco.

Kronik Periodontitis Ve Sigara Kullananımının Oksidatif Durum Üzerine Olan Etkisinin Değerlendirilmesi
Öz
Amaç: Bu çalışmanın amacı; kronik periodontitisli ve periodontal açıdan sağlıklı bireylerin DOS ve tükürük numunelerinde sigaranın MLT, MPO ve 8-OHdG düzeyleri üzerine muhtemel etkilerinin değerlendirilmesidir.
Gereç ve yöntem : Çalışma protokolü gereği her biri 15 katılımcıdan oluşan 4 grup oluşturuldu; periodontal olarak sağlıklı ve sigara içemeyen grup (P-S-), periodontal olarak sağlıklı ve sigara içen grup (P-S+), kronik periodontitisli ve sigara içmeyen grup (P+S-) ile kronik periodontitisli ve sigara içen grup (P+S+). DOS ve tükürük örnekleri alınmadan önce klinik periodontal parametreler kaydedildi. MLT, MPO ve 8-OHdG düzeyleri biyokimyasal ve olarak ölçüldü.
Bulgular : En yüksek MPO ve 8-OHdGdüzeyleri ile en düşük MLT düzeyleri (P+S+) grubunda tespit edildi. En yüksek MLT düzeyi ise (P-S-) grubunda gözlendi. Sigara kullanımı ve kronik periodontitisin biyokimyasal ve histopatolojik parametreleri benzer şekilde etkilediği tespit edildi.
Sonuç : KP’nin oksidatif stres ile ilişkili parametrelerde anlamlı düzeyde farklılık oluşturduğu gözlendi. Sigara kullanımının genel olarak periodontal sağlıklı bireylerde parametrelerde belirgin bir değişime yol açtığı, periodontitisli gruplarda ise bu değişimin istatistiksel olarak anlamlı olmadığı görüldü. Bulgularımız, sigara içmenin periodontal hastalıkların patogenezinde rol alan oksitatif parametreleri olumsuz yönde etkileyerek periodontitis gelişiminde rol oynayabileceğini göstermektedir.
Anahtar Kelimeler: Isı şok proteinleri 60-70, kronik periodontitis, melatonin, myeloperoksidaz, oksitatif stress, sigara, 8-hydroxy-2'-deoxyguanosine.

Anahtar Kelimeler

8-hydroxy-2´-deoxyguanosine (8-OHdG), chronic periodontitis (CP)

Kaynakça

• 1. Brown LJ, Loe H. Prevalence, extent, severity and progression of periodontal disease. Periodontology 2000. 1993;2:57-71. Epub 1993/06/01.
• 2. Periodontology. TAao. The pathogenesis of periodontal diseases (position paper). Journal of Periodontology. 1999;70:457-70.
• 3. Gasner NS, Schure RS. Periodontal Disease. StatPearls. Treasure Island (FL)2020.
• 4. Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontology 2000. 2007;43:160-232. Epub 2007/01/12.
• 5. Martinez-Herrera M, Abad-Jimenez Z, Silvestre FJ, Lopez-Domenech S, Marquez-Arrico CF, Silvestre-Rangil J, et al. Effect of Non-Surgical Periodontal Treatment on Oxidative Stress Markers in Leukocytes and Their Interaction with the Endothelium in Obese Subjects with Periodontitis: A Pilot Study. Journal of clinical medicine. 2020;9(7). Epub 2020/07/09.
• 6. Tonetti MS. Cigarette smoking and periodontal diseases: etiology and management of disease. Annals of periodontology. 1998;3(1):88-101. Epub 1998/09/02.
• 7. Fredriksson MI, Figueredo CM, Gustafsson A, Bergstrom KG, Asman BE. Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol. 1999;70(11):1355-60. Epub 1999/12/10.
• 8. Periodontology AAo. Tobacco use and the periodontal patient (position paper). Journal of Periodontology. 1996;67:51-6.
• 9. Bergstrom J. Tobacco smoking and chronic destructive periodontal disease. Odontology. 2004;92(1):1-8. Epub 2004/10/19.
• 10. Lu X, Cai J, Kong H, Wu M, Hua R, Zhao M, et al. Analysis of cigarette smoke condensates by comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry I acidic fraction. Analytical chemistry. 2003;75(17):4441-51. Epub 2003/11/25.
• 11. Guentsch A, Preshaw PM, Bremer-Streck S, Klinger G, Glockmann E, Sigusch BW. Lipid peroxidation and antioxidant activity in saliva of periodontitis patients: effect of smoking and periodontal treatment. Clinical oral investigations. 2008;12(4):345-52. Epub 2008/05/30.
• 12. Canakci CF, Cicek Y, Canakci V. Reactive oxygen species and human inflammatory periodontal diseases. Biochemistry Biokhimiia. 2005;70(6):619-28. Epub 2005/07/26.
• 13. Ahmed NJ, Husen AZ, Khoshnaw N, Getta HA, Hussein ZS, Yassin AK, et al. The Effects of Smoking on IgE, Oxidative Stress and Haemoglobin Concentration. Asian Pacific journal of cancer prevention : APJCP. 2020;21(4):1069-72. Epub 2020/04/27.
• 14. Halliwell B. Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free radical research. 1999;31(4):261-72. Epub 1999/10/12.
• 15. Hugoson A, Laurell L. A prospective longitudinal study on periodontal bone height changes in a Swedish population. Journal of clinical periodontology. 2000;27(9):665-74. Epub 2000/09/13.
• 16. Ozmeric N. Advances in periodontal disease markers. Clinica chimica acta; international journal of clinical chemistry. 2004;343(1-2):1-16. Epub 2004/04/30.
• 17. Graille M, Wild P, Sauvain JJ, Hemmendinger M, Guseva Canu I, Hopf NB. Urinary 8-OHdG as a Biomarker for Oxidative Stress: A Systematic Literature Review and Meta-Analysis. International journal of molecular sciences. 2020;21(11). Epub 2020/05/30.
• 18. Su H, Gornitsky M, Velly AM, Yu H, Benarroch M, Schipper HM. Salivary DNA, lipid, and protein oxidation in nonsmokers with periodontal disease. Free radical biology & medicine. 2009;46(7):914-21. Epub 2009/03/13.
• 19. Slots J. Subgingival microflora and periodontal disease. Journal of clinical periodontology. 1979;6(5):351-82. Epub 1979/10/01.
• 20. Kose O, Kurt Bayrakdar S, Akyildiz K, Altin A, Arabaci T, Yemenoglu H, et al. Melatonin ameliorates periodontitis related inflammatory stress at cardiac left ventricular tissues in rats. Journal of periodontology. 2020. Epub 2020/04/13.
• 21. Haffajee AD, Socransky SS. Microbiology of periodontal diseases: introduction. Periodontology 2000. 2005;38:9-12. Epub 2005/04/28.
• 22. Zare Javid A, Hosseini SA, Gholinezhad H, Moradi L, Haghighi-Zadeh MH, Bazyar H. Antioxidant and Anti-Inflammatory Properties of Melatonin in Patients with Type 2 Diabetes Mellitus with Periodontal Disease Under Non-Surgical Periodontal Therapy: A Double-Blind, Placebo-Controlled Trial. Diabetes, metabolic syndrome and obesity : targets and therapy. 2020;13:753-61. Epub 2020/04/08.
• 23. Offenbacher S. Periodontal diseases: pathogenesis. Annals of periodontology. 1996;1(1):821-78. Epub 1996/11/01.
• 24. Dickerhof N, Huang J, Min E, Michaelsson E, Lindstedt EL, Pearson JF, et al. Myeloperoxidase inhibition decreases morbidity and oxidative stress in mice with cystic fibrosis-like lung inflammation. Free radical biology & medicine. 2020;152:91-9. Epub 2020/03/07.
• 25. Ojima M, Hanioka T, Tanaka K, Inoshita E, Aoyama H. Relationship between smoking status and periodontal conditions: findings from national databases in Japan. Journal of periodontal research. 2006;41(6):573-9. Epub 2006/11/02.
• 26. Amaranath BJ, Das N, Gupta I, Gupta R, John B, Devi MP. Types of bone destruction and its severity in chronic periodontitis patients with tobacco smoking habit using periapical radiographs and transgingival probing: A cross-sectional study. Journal of Indian Society of Periodontology. 2020;24(1):20-5. Epub 2020/01/28.
• 27. Hanioka T, Tanaka M, Ojima M, Takaya K, Matsumori Y, Shizukuishi S. Oxygen sufficiency in the gingiva of smokers and non-smokers with periodontal disease. J Periodontol. 2000;71(12):1846-51. Epub 2001/01/13.
• 28. Loe H. The Gingival Index, the Plaque Index and the Retention Index Systems. J Periodontol. 1967;38(6):Suppl:610-6. Epub 1967/11/01.
• 29. Silness J, Loe H. Periodontal Disease in Pregnancy. Ii. Correlation between Oral Hygiene and Periodontal Condtion. Acta odontologica Scandinavica. 1964;22:121-35. Epub 1964/02/01.
• 30. Page RC, Eke PI. Case definitions for use in population - Based surveillance of periodontitis. Journal of Periodontology. 2007;78(7):1387-99.
• 31. Flemmig TF. Periodontitis. Annals of periodontology. 1999;4(1):32-8. Epub 2000/06/23.
• 32. Lehr HA, Kress E, Menger MD, Friedl HP, Hubner C, Arfors KE, et al. Cigarette smoke elicits leukocyte adhesion to endothelium in hamsters: inhibition by CuZn-SOD. Free radical biology & medicine. 1993;14(6):573-81. Epub 1993/06/01.
• 33. Oba S, Inaba Y, Shibuya T, Oshima J, Seyama K, Kobayashi T, et al. Changes in oxidative stress levels during two weeks of smoking cessation treatment and their association with nutritional characteristics in Japanese smokers. Experimental and therapeutic medicine. 2019;17(4):2757-64. Epub 2019/04/02.
• 34. Badran M, Laher I. Waterpipe (shisha, hookah) smoking, oxidative stress and hidden disease potential. Redox biology. 2020;34:101455. Epub 2020/02/23.
• 35. Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol. 1994;65(3):260-7. Epub 1994/03/01.
• 36. Barnett ML, Baker RL, Yancey JM, MacMillan DR, Kotoyan M. Absence of periodontitis in a population of insulin-dependent diabetes mellitus (IDDM) patients. J Periodontol. 1984;55(7):402-5. Epub 1984/07/01.
• 37. Haber J, Wattles J, Crowley M, Mandell R, Joshipura K, Kent RL. Evidence for cigarette smoking as a major risk factor for periodontitis. J Periodontol. 1993;64(1):16-23. Epub 1993/01/01.
• 38. Grossi SG, Genco RJ, Machtei EE, Ho AW, Koch G, Dunford R, et al. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol. 1995;66(1):23-9. Epub 1995/01/01.
• 39. Takane M, Sugano N, Iwasaki H, Iwano Y, Shimizu N, Ito K. New biomarker evidence of oxidative DNA damage in whole saliva from clinically healthy and periodontally diseased individuals. J Periodontol. 2002;73(5):551-4. Epub 2002/05/25.
• 40. Anusuya S, Mlv P, Lazarus F, Bhavikatti SK, Babrawala IS. Estimation of 8-Hydroxy-deoxyguanosine (8-OHdG) in Saliva as a Marker of Oxidative Stress in Patients with Chronic Periodontitis: Preliminary Data. Journal of the International Academy of Periodontology. 2017;19(3):95-100. Epub 2017/07/01.
• 41. Paredes-Sanchez E, Montiel-Company JM, Iranzo-Cortes JE, Almerich-Torres T, Bellot-Arcis C, Almerich-Silla JM. Meta-Analysis of the Use of 8-OHdG in Saliva as a Marker of Periodontal Disease. Disease markers. 2018;2018:7916578. Epub 2018/06/02.
• 42. Takane M, Sugano N, Ezawa T, Uchiyama T, Ito K. A marker of oxidative stress in saliva: association with periodontally-involved teeth of a hopeless prognosis. Journal of oral science. 2005;47(1):53-7. Epub 2005/05/11.
• 43. Wolfram RM, Budinsky AC, Eder A, Presenhuber C, Nell A, Sperr W, et al. Salivary isoprostanes indicate increased oxidation injury in periodontitis with additional tobacco abuse. Biofactors. 2006;28(1):21-31. Epub 2007/02/01.
• 44. Kulikowska-Karpinska E, Czerw K. [Estimation of 8-hydroxy-2'-deoxyguanosine (8-OHdG) concentration in the urine of cigarette smokers]. Wiad Lek. 2015;68(1):32-8. Epub 2015/06/23. Ocena stezenia 8-hydroksy-2'-deoksyguanozyny (8-OHdG) w moczu osob palacych papierosy.
• 45. Canakci CF, Canakci V, Tatar A, Eltas A, Sezer U, Cicek Y, et al. Increased salivary level of 8-hydroxydeoxyguanosine is a marker of premature oxidative mitochondrial DNA damage in gingival tissue of patients with periodontitis. Archivum immunologiae et therapiae experimentalis. 2009;57(3):205-11. Epub 2009/05/30.
• 46. Canakci CF, Cicek Y, Yildirim A, Sezer U, Canakci V. Increased levels of 8-hydroxydeoxyguanosine and malondialdehyde and its relationship with antioxidant enzymes in saliva of periodontitis patients. European journal of dentistry. 2009;3(2):100-6. Epub 2009/05/08.
• 47. Aoshiba K, Nagai A. Oxidative stress, cell death, and other damage to alveolar epithelial cells induced by cigarette smoke. Tobacco induced diseases. 2003;1(3):219-26. Epub 2003/01/01.
• 48. Konopka T, Krol K, Kopec W. [Influence of tobacco smoking and periodontitis on selected factors of oxidative stress]. Wiad Lek. 2006;59(7-8):463-70. Epub 2007/01/11. Wplyw nikotynizmu i zapalen przyzebia na wybrane parametry stresu oksydacyjnego.
• 49. Lodovici M, Casalini C, Cariaggi R, Michelucci L, Dolara P. Levels of 8-hydroxydeoxyguanosine as a marker of DNA damage in human leukocytes. Free radical biology & medicine. 2000;28(1):13-7. Epub 2000/02/03.
• 50. Sorensen LT, Jorgensen S, Petersen LJ, Hemmingsen U, Bulow J, Loft S, et al. Acute effects of nicotine and smoking on blood flow, tissue oxygen, and aerobe metabolism of the skin and subcutis. The Journal of surgical research. 2009;152(2):224-30. Epub 2008/05/13.
• 51. An AR, Kim KM, Park HS, Jang KY, Moon WS, Kang MJ, et al. Association between Expression of 8-OHdG and Cigarette Smoking in Non-small Cell Lung Cancer. Journal of pathology and translational medicine. 2019;53(4):217-24. Epub 2019/03/12.
• 52. Cutando A, Gomez-Moreno G, Arana C, Acuna-Castroviejo D, Reiter RJ. Melatonin: potential functions in the oral cavity. J Periodontol. 2007;78(6):1094-102. Epub 2007/06/02.
• 53. Mayo JC, Sainz RM. Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019. International journal of molecular sciences. 2020;21(10). Epub 2020/05/28.
• 54. Goldberg DJ, Robinson DM, Granger C. Clinical evidence of the efficacy and safety of a new 3-in-1 anti-aging topical night serum-in-oil containing melatonin, bakuchiol, and ascorbyl tetraisopalmitate: 103 females treated from 28 to 84 days. Journal of cosmetic dermatology. 2019;18(3):806-14. Epub 2019/03/30.
• 55. Cutando A, Galindo P, Gomez-Moreno G, Arana C, Bolanos J, Acuna-Castroviejo D, et al. Relationship between salivary melatonin and severity of periodontal disease. J Periodontol. 2006;77(9):1533-8. Epub 2006/09/02.
• 56. Mates JM. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology. 2000;153(1-3):83-104. Epub 2000/11/25.
• 57. Tinto M, Sartori M, Pizzi I, Verga A, Longoni S. Melatonin as host modulating agent supporting nonsurgical periodontal therapy in patients affected by untreated severe periodontitis: A preliminary randomized, triple-blind, placebo-controlled study. Journal of periodontal research. 2020;55(1):61-7. Epub 2019/08/14.
• 58. Bazyar H, Gholinezhad H, Moradi L, Salehi P, Abadi F, Ravanbakhsh M, et al. The effects of melatonin supplementation in adjunct with non-surgical periodontal therapy on periodontal status, serum melatonin and inflammatory markers in type 2 diabetes mellitus patients with chronic periodontitis: a double-blind, placebo-controlled trial. Inflammopharmacology. 2019;27(1):67-76. Epub 2018/10/18.
• 59. Tekbas OF, Ogur R, Korkmaz A, Kilic A, Reiter RJ. Melatonin as an antibiotic: new insights into the actions of this ubiquitous molecule. Journal of pineal research. 2008;44(2):222-6. Epub 2008/02/22.
• 60. Kose O, Arabaci T, Kizildag A, Erdemci B, Ozkal Eminoglu D, Gedikli S, et al. Melatonin prevents radiation-induced oxidative stress and periodontal tissue breakdown in irradiated rats with experimental periodontitis. Journal of periodontal research. 2017;52(3):438-46. Epub 2016/08/12.
• 61. Burgess HJ, Fogg LF. Individual differences in the amount and timing of salivary melatonin secretion. PloS one. 2008;3(8):e3055. Epub 2008/08/30.
• 62. Halliwell B. Oral inflammation and reactive species: a missed opportunity? Oral diseases. 2000;6(3):136-7. Epub 2000/05/24.
• 63. Qaddoumi MG, Alanbaei M, Hammad MM, Al Khairi I, Cherian P, Channanath A, et al. Investigating the Role of Myeloperoxidase and Angiopoietin-like Protein 6 in Obesity and Diabetes. Scientific reports. 2020;10(1):6170. Epub 2020/04/12.
• 64. Yamalik N, Caglayan F, Kilinc K, Kilinc A, Tumer C. The importance of data presentation regarding gingival crevicular fluid myeloperoxidase and elastase-like activity in periodontal disease and health status. J Periodontol. 2000;71(3):460-7. Epub 2000/04/25.
• 65. Wei PF, Ho KY, Ho YP, Wu YM, Yang YH, Tsai CC. The investigation of glutathione peroxidase, lactoferrin, myeloperoxidase and interleukin-1beta in gingival crevicular fluid: implications for oxidative stress in human periodontal diseases. Journal of periodontal research. 2004;39(5):287-93. Epub 2004/08/25.
• 66. Chen S, Chen H, Du Q, Shen J. Targeting Myeloperoxidase (MPO) Mediated Oxidative Stress and Inflammation for Reducing Brain Ischemia Injury: Potential Application of Natural Compounds. Frontiers in physiology. 2020;11:433. Epub 2020/06/09.
• 67. Smith QT, Au GS, Freese PL, Osborn JB, Stoltenberg JL. Five parameters of gingival crevicular fluid from eight surfaces in periodontal health and disease. Journal of periodontal research. 1992;27(5):466-75. Epub 1992/09/01.
• 68. Uslu MO, Eltas A, Marakoglu I, Dundar S, Sahin K, Ozercan IH. Effects of diode laser application on inflammation and mpo in periodontal tissues in a rat model. Journal of applied oral science : revista FOB. 2018;26:e20170266. Epub 2018/07/19.
• 69. Abu-Amsha Caccetta R, Burke V, Mori TA, Beilin LJ, Puddey IB, Croft KD. Red wine polyphenols, in the absence of alcohol, reduce lipid peroxidative stress in smoking subjects. Free radical biology & medicine. 2001;30(6):636-42. Epub 2001/04/11.
• 70. Bolzan AD, Bianchi MS, Bianchi NO. Superoxide dismutase, catalase and glutathione peroxidase activities in human blood: influence of sex, age and cigarette smoking. Clinical biochemistry. 1997;30(6):449-54. Epub 1997/08/01.