EFFECTS OF PERIODONTAL THERAPY ON SERUM LIPID LEVELS: A PROSPECTIVE INTERVENTIONAL TRIAL

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Rajendra Kumar Meena, Swarga Jyoti Das*, “EFFECTS OF PERIODONTAL THERAPY ON SERUM LIPID LEVELS: A PROSPECTIVE INTERVENTIONAL TRIAL”, ijmhs, vol. 9, no. 8, pp. 566–577, Aug. 2019.
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Abstract

Background: In periodontitis, the inflammatory cells synthesized and secreted
proinflammatory mediators, namely interleukin 1? and ?, and tumour necrosis factor
?, interleukin 6, prostaglandins. A great interest has been developed regarding the
systemic effect of these proinflammatory cytokines. Evidence suggests that they
cause a state of altered lipid metabolism, manifested as dyslipidemia, either of
heperlipidemia or hypolipidemia. Thus, a close association of periodontal disease
and systemic conditions related to dyslipidemia is suggested, though not established
yet.
Objectives: The present study was designed to evaluate the effects of nonsurgical
periodontal therapy on serum lipid levels in the subjects with moderate
to severe generalized chronic periodontitis by comparing the serum levels of total
cholesterol, triglyceride, LDL and HDL before and after
periodontal therapy.
Materials and Methods: The selected subjects (n= 40) were randomly divided
into two groups: Treatment group (treated with scaling and root planing +
systemic Doxycycline (200 mg first day orally followed by 100 mg daily for 14
days) and Control (received no treatment). The periodontal parameters
considered were gingival index, probing pocket depth and clinical attachment
level, while the metabolic parameters were serum triglyceride, cholesterol, LDL
cholesterol, HDL cholesterol (together called as serum lipid levels). The parameters
were recorded on day 0 and 90.
Results: Serum triglyceride, serum cholesterol and LDL cholesterol levels were
reduced with significant improvement in gingival health, pocket depth and clinical
attachment level after periodontal therapy.
Conclusion: Periodontal therapy is effective in reducing the serum lipid levels,
thereby reduces the risk of associated systemic diseases.
Key words: Cytokines, Periodontitis, Serum Cholesterol, Triglycerid,
Prostaglandin, Pocket Depth, Clinical Attachment Level

KEYWORDS:

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References

1.Newman MG, Takei HH, KlokkevoldPR, Carranza FA. Carranza’s ClinicalPeriodontology, Saunders Pub. 2007. 2.Socransky SS, Haffajee AD. Thebacterial etiology of destructiveperiodontal disease: current concepts.Journal of Periodontology. 1992; 63:322-31. 3.De Nardin E. The role of inflammatoryand immunological mediators inperiodontitis and cardiovascular diseases.Annals of Periodontology. 2001; 6: 30-40. 4.Van Dyke TE, Serhan CN. Resolution ofinflammation: a new paradigm for thepathogenesis of periodontal diseases.Journal of Dental Research. 2003; 82: 82-90. 5.Page RC. Milestones in periodontalresearch and the remaining critical issues.Journal of Periodontal Research. 1999;34:331-339. 6.Fukushima R, Saito H, Taniwake K.Different roles of IL-1 and TNF onhemodynamics and interorgan amino acidmetabolism in awake dogs. AmericanJournal of Physiology. 1992; 262: E275-281. 7.Imura H, Fukata J, Mori T. Cytokinesand endocrine function: An interactionbetween the immune and neuroendocrine systems. Clinical Endocrinology. 1991; 35: 107-115. 8.Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. New EnglandJournal of Medicine. 1995; 332: 1351-1362. 9.Feingold KR, Grunfeld C. Tumornecrosis factor alpha stimulates hepaticlipogensesis in the rat in vivo. Journal ofClinical Investigation. 1987; 80: 184-190. 10.Divertie GD. Jensen MD, Miles JM.Stimulation of lipolysis in humans byphysiological hypercortisolemia.Diabetes. 1991; 40: 1228-1232. 11.Kurpad A, Khan K, Calders AG,Coppack S, Frayn K, Macdonald I, EliaM. Effect of noradrenaline on glycerolturnover and lipolysis in the whole bodyand subcutaneous adipose tissue inhumans in vivo. Clinical Science. 1994;86: 177-184. 12.Fried SK, Zechner R. Cachectin/tumornecrosis factor decreases human adiposetissue lipoprotein lipase mRNA levels,synthesis, and activity. Journal of LipidResearch. 1989; 30: 1917-1923. 13.RosatoEF, Vemulapalli P, Lang CH, Lanza-Jacoby S. Insulin stimulates lipoprotein lipase activity and synthesis in adipocytes from septic rats. Journal of Surgical Research. 1997; 73: 73 - 79. 14.Jacobson MS. Heart healthy diets for allchildren: no longer controversial. Journalof Pediatrics. 1998; 133: 1-2. 15.Cutler CW, Shinedling EA, Nunn M,Jotwani R, Kim BO, Nares S, IacopinoAM. Association between periodontitisand hyperlipidemia: cause or effect?Journal of Periodontology. 1999; 70:1429-34. 16.Losche W, Karapetow F, Pohl A, Pohl C,Kocher T. Plasma lipid and bloodglucose levels in patients with destructive periodontal disease. Journal of Clinical Periodontology. 2000; 27:537-541. 17.Meurman JH, Sanz M, Janket SJ. Oralhealth, atherosclerosis, andcardiovascular disease. Critical Reviewsin Oral Biology and Medicine. 2004; 15:403-413. 18.Losche W, Marshal GJ, Apatzidou DA,Krause S, Kocher T, Kinane DF.Lipoprotein-associated phospholipase A2and plasma lipids in patients withdestructive periodontal disease. Journalof Clinical Periodontology. 2005; 32:640-644. 19.Tandon S, Dhingra MS, Lamba AK,Verma M, Munjal A, Faraz F. Effect ofperiodontal therapy on serum lipid levels.Indian Journal Medical Specialities.2010; 1:19-25. 20.Kamil W, Al Habashneh R, Khader Y, AlBayati L, Taani D. Effect of nonsurgicalperiodontal therapy on C-reactive proteinand serum lipids in Jordanian adults withadvanced periodontitis. Journal ofPeriodontal Research. 2011; 46: 616-21. 21.Subramanian K, Shriraam M, Bharath R,Muthukumaran J, Kumaravel V. LDL-cholesterol: Friedewald calculated versusdirect measurement-study from a largeIndian laboratory database. IndianJournal of Endocrinology andMetabolism. 2014; 18: 502–504. J.BERSOLE 22.Ebersole JL, Machen RL, Steffen MJ,Willmann DE. Systemic acute-phasereactants, C-reactive protein andhaptoglobin, in adult periodontitis.Clinical and Experimental Immunology.1997; 107: 347-352. 23.Loos BG, Craandijk J, Hoek FJ,Wertheim PM, Velden U. Elevation ofsystemic markers related tocardiovascular diseases in the peripheralblood of periodontitis patients. Journal of Periodontology. 2000; 71: 1528-1534. 24.Noack B, Genco RJ, Trevisan M, GrossiS, Zambon JJ, DeNardin E. Periodontalinfections contribute to elevated systemicc-reactive protein level. Journal ofPeriodontology. 2001; 72: 1221-1227. 25.Katz J, Flugelman MY, Goldberg A, HeftM. Association between periodontalpockets and elevated cholesterol and lowdensity lipoprotein cholesterol levels.Journal of Periodontology. 2002; 73:494-500. 26.Memon RA, Grunfeld C, Moser AH,Feingold KR. Tumor necrosis factormediates the effects of endotoxin oncholesterol and triglyceride metabolismin mice. Endocrinology. 1993; 132: 2246-2253. 27.Doxey DL, Cutler CW, Iacopino AM.Diabetes prevents periodontitis–inducedincreases in gingival platelet derivedgrowth factor-B and interleukin-1 beta ina rat model. Journal of Periodontology.1998; 69: 113-119. 28.Marita M, Horiuchi M, Kinoshita Y,Yamamoto T, Watanabe T. Relationshipbetween blood triglyceride levels andperiodontal status. Community DentalHealth. 2004; 21: 32-36. 29.Sharma S, Lamsal M, Sharma SK,Niraula SR, Koirala B. Association ofserum LDL cholesterol level withperiodontitis among patients visiting atertiary-care hospital. Journal of theNepal Medical Association. 2011; 51:104-108. 30.Sangwan A, Tewari S, Singh H, SharmaRK and Narula SC. Periodontal statusand hyperlipidemia: statin users versusnon-users. Journal of Periodontology.2013; 84: 3-12. 31.Duan JY, Ou-Yang XY, Zhou YX. Effectof periodontal initial therapy on the serum levels of lipid in the patients with both periodontitis and hyperlipidemia. Journal of Peking University. 2009; 41: 36 - 39. 32.Rao NS, Bajaj P, Naik SB, Pradeep AR.Effect of non surgical periodontal therapyon serum lipid levels in chronicperiodontitis. Archives of Oral Sciencesand Research. 2011; 1: 60-64. 33.Machado AC, Quirino MR, NascimentoLF. Relation between chronic periodontaldisease and plasmatic levels oftriglycerides, total cholesterol andfractions. Brazilian Oral Research. 2005;19: 284 - 289. 34.Valentaviciene G, Paipaliene P,Nedzelskiene I, Zilinskas J, AnusevicienOV. The relationship between bloodserum lipids and periodontal condition.Stomatologija, Baltic Dental andMaxillofacial Journal. 2005; 8: 96-100. 35.Flemmig TF. Periodontitis. Annals ofPeriodontology. 1999; 4: 32-38. 36.Page RC. The pathobiology ofperiodontal diseases may affect systemicdiseases: inversion of a paradigm. Annalsof Periodontology. 1998; 3: 108-120. 37.Johnson GK, Slach NA. Impact oftobacco use on periodontal status. Journalof Dental Education. 2001; 65: 313-321. 38.Golub LM, Ryan ME, Williams RC.Modulation of the host response in thetreatment of periodontitis. DentistryToday. 1998; 17:102-109. 39.Tripathi KD. Essentials of MedicalPharmacology, Jaypee brothers medicalpublishers (p) Ltd. 2008. 40.Armitage GC. The complete periodontalexamination. Periodontology 2000. 2004;34: 22-33. 41.Morrison EC, Ramfjord SP, Hill RW.Short-term effects of initial, nonsurgicalperiodontal treatment (hygienic phase). Journal of Clinical Periodontology.1980; 7:199-211. 42.Badersten A, Nilveus R, Egelberg J.Effect of nonsurgical periodontal therapyI. Moderately advanced periodontitis.Journal of Clinical Periodontology. 1981;8: 57-72. 43.D’Aiuto F, Parkar M, Andreou G, SuvanJ, Brett PM, Ready D, Tonetti MS.Periodontitis and systemic inflammation:control of the local infection is associatedwith a reduction in serum inflammatorymarkers. Journal of Dental Research.2004; 83:156-160. 44.Offenbacher S, Lin D, Strauss R,McKaig R, Irving J, Barros SP, Moss K,Barrow DA, Hefti A, Beck JD. Effects ofperiodontal therapy during pregnancy onperiodontal status, biologic parameters,and pregnancy outcomes: a pilot study.Journal of Periodontology. 2006; 77:2011-2024. 45.Radafshar G, Torabi F, Mirfarhadi N.Short-term effects of intensive non-surgical periodontal therapy and low-dose doxycycline on serum levels of IL-6, TNF-? and lipid profile in advancedperiodontitis. African Journal ofMicrobiology Research. 2012; 6: 355-360. 46.D’Aiuto F, Nibali L, Parkar M, Suvan J,Tonetti MS. Short-term effects ofintensive periodontal therapy on seruminflammatory markers and cholesterol.Journal of Dental Research. 2005; 84:269-273. 47.Oz SG, Fentoglu O, Kilicarslan A, GuvenGS, Tanrtover MD, Aykac Y, Sozen T.Beneficial effects of periodontaltreatment on metabolic control ofhypercholesterolemia. Southern MedicalAssociation Journal. 2007; 100: 686-691. 48.Fentoglu O, Sozen T, Oz SG., Kale B,Sonmez Y, Tonguc MO, Gurgan CA,Aykaç Y, Kirzio?lu FY. Short-term effects of periodontal therapy as an adjunct to anti-lipemic treatment. Oral Disease. 2010; 16: 648-654. 49.Pussinen PJ, Jauhiainen M, RautiainenTV, Sundvall J, Vesanen M, Mattila K, Palosuo T, Alfthan G, Asikainen S.Periodontitis decreases theantiatherogenic potency of high densitylipoprotein. Journal of Lipid Research.2004; 45: 139-147.

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References

1.Newman MG, Takei HH, KlokkevoldPR, Carranza FA. Carranza’s ClinicalPeriodontology, Saunders Pub. 2007.
2.Socransky SS, Haffajee AD. Thebacterial etiology of destructiveperiodontal disease: current concepts.Journal of Periodontology. 1992; 63:322-31.
3.De Nardin E. The role of inflammatoryand immunological mediators inperiodontitis and cardiovascular diseases.Annals of Periodontology. 2001; 6: 30-40.
4.Van Dyke TE, Serhan CN. Resolution ofinflammation: a new paradigm for thepathogenesis of periodontal diseases.Journal of Dental Research. 2003; 82: 82-90.
5.Page RC. Milestones in periodontalresearch and the remaining critical issues.Journal of Periodontal Research. 1999;34:331-339.
6.Fukushima R, Saito H, Taniwake K.Different roles of IL-1 and TNF onhemodynamics and interorgan amino acidmetabolism in awake dogs. AmericanJournal of Physiology. 1992; 262: E275-281.
7.Imura H, Fukata J, Mori T. Cytokinesand endocrine function: An interactionbetween the immune and neuroendocrine systems. Clinical Endocrinology. 1991; 35: 107-115.
8.Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. New EnglandJournal of Medicine. 1995; 332: 1351-1362.
9.Feingold KR, Grunfeld C. Tumornecrosis factor alpha stimulates hepaticlipogensesis in the rat in vivo. Journal ofClinical Investigation. 1987; 80: 184-190.
10.Divertie GD. Jensen MD, Miles JM.Stimulation of lipolysis in humans byphysiological hypercortisolemia.Diabetes. 1991; 40: 1228-1232.
11.Kurpad A, Khan K, Calders AG,Coppack S, Frayn K, Macdonald I, EliaM. Effect of noradrenaline on glycerolturnover and lipolysis in the whole bodyand subcutaneous adipose tissue inhumans in vivo. Clinical Science. 1994;86: 177-184.
12.Fried SK, Zechner R. Cachectin/tumornecrosis factor decreases human adiposetissue lipoprotein lipase mRNA levels,synthesis, and activity. Journal of LipidResearch. 1989; 30: 1917-1923.
13.RosatoEF, Vemulapalli P, Lang CH, Lanza-Jacoby S. Insulin stimulates lipoprotein lipase activity and synthesis in adipocytes from septic rats. Journal of Surgical Research. 1997; 73: 73 - 79.
14.Jacobson MS. Heart healthy diets for allchildren: no longer controversial. Journalof Pediatrics. 1998; 133: 1-2.
15.Cutler CW, Shinedling EA, Nunn M,Jotwani R, Kim BO, Nares S, IacopinoAM. Association between periodontitisand hyperlipidemia: cause or effect?Journal of Periodontology. 1999; 70:1429-34.
16.Losche W, Karapetow F, Pohl A, Pohl C,Kocher T. Plasma lipid and bloodglucose levels in patients with destructive periodontal disease. Journal of Clinical Periodontology. 2000; 27:537-541.
17.Meurman JH, Sanz M, Janket SJ. Oralhealth, atherosclerosis, andcardiovascular disease. Critical Reviewsin Oral Biology and Medicine. 2004; 15:403-413.
18.Losche W, Marshal GJ, Apatzidou DA,Krause S, Kocher T, Kinane DF.Lipoprotein-associated phospholipase A2and plasma lipids in patients withdestructive periodontal disease. Journalof Clinical Periodontology. 2005; 32:640-644.
19.Tandon S, Dhingra MS, Lamba AK,Verma M, Munjal A, Faraz F. Effect ofperiodontal therapy on serum lipid levels.Indian Journal Medical Specialities.2010; 1:19-25.
20.Kamil W, Al Habashneh R, Khader Y, AlBayati L, Taani D. Effect of nonsurgicalperiodontal therapy on C-reactive proteinand serum lipids in Jordanian adults withadvanced periodontitis. Journal ofPeriodontal Research. 2011; 46: 616-21.
21.Subramanian K, Shriraam M, Bharath R,Muthukumaran J, Kumaravel V. LDL-cholesterol: Friedewald calculated versusdirect measurement-study from a largeIndian laboratory database. IndianJournal of Endocrinology andMetabolism. 2014; 18: 502–504. J.BERSOLE
22.Ebersole JL, Machen RL, Steffen MJ,Willmann DE. Systemic acute-phasereactants, C-reactive protein andhaptoglobin, in adult periodontitis.Clinical and Experimental Immunology.1997; 107: 347-352.
23.Loos BG, Craandijk J, Hoek FJ,Wertheim PM, Velden U. Elevation ofsystemic markers related tocardiovascular diseases in the peripheralblood of periodontitis patients. Journal of Periodontology. 2000; 71: 1528-1534.
24.Noack B, Genco RJ, Trevisan M, GrossiS, Zambon JJ, DeNardin E. Periodontalinfections contribute to elevated systemicc-reactive protein level. Journal ofPeriodontology. 2001; 72: 1221-1227.
25.Katz J, Flugelman MY, Goldberg A, HeftM. Association between periodontalpockets and elevated cholesterol and lowdensity lipoprotein cholesterol levels.Journal of Periodontology. 2002; 73:494-500.
26.Memon RA, Grunfeld C, Moser AH,Feingold KR. Tumor necrosis factormediates the effects of endotoxin oncholesterol and triglyceride metabolismin mice. Endocrinology. 1993; 132: 2246-2253.
27.Doxey DL, Cutler CW, Iacopino AM.Diabetes prevents periodontitis–inducedincreases in gingival platelet derivedgrowth factor-B and interleukin-1 beta ina rat model. Journal of Periodontology.1998; 69: 113-119.
28.Marita M, Horiuchi M, Kinoshita Y,Yamamoto T, Watanabe T. Relationshipbetween blood triglyceride levels andperiodontal status. Community DentalHealth. 2004; 21: 32-36.
29.Sharma S, Lamsal M, Sharma SK,Niraula SR, Koirala B. Association ofserum LDL cholesterol level withperiodontitis among patients visiting atertiary-care hospital. Journal of theNepal Medical Association. 2011; 51:104-108.
30.Sangwan A, Tewari S, Singh H, SharmaRK and Narula SC. Periodontal statusand hyperlipidemia: statin users versusnon-users. Journal of Periodontology.2013; 84: 3-12.
31.Duan JY, Ou-Yang XY, Zhou YX. Effectof periodontal initial therapy on the serum levels of lipid in the patients with both periodontitis and hyperlipidemia. Journal of Peking University. 2009; 41: 36 - 39.
32.Rao NS, Bajaj P, Naik SB, Pradeep AR.Effect of non surgical periodontal therapyon serum lipid levels in chronicperiodontitis. Archives of Oral Sciencesand Research. 2011; 1: 60-64.
33.Machado AC, Quirino MR, NascimentoLF. Relation between chronic periodontaldisease and plasmatic levels oftriglycerides, total cholesterol andfractions. Brazilian Oral Research. 2005;19: 284 - 289.
34.Valentaviciene G, Paipaliene P,Nedzelskiene I, Zilinskas J, AnusevicienOV. The relationship between bloodserum lipids and periodontal condition.Stomatologija, Baltic Dental andMaxillofacial Journal. 2005; 8: 96-100.
35.Flemmig TF. Periodontitis. Annals ofPeriodontology. 1999; 4: 32-38.
36.Page RC. The pathobiology ofperiodontal diseases may affect systemicdiseases: inversion of a paradigm. Annalsof Periodontology. 1998; 3: 108-120.
37.Johnson GK, Slach NA. Impact oftobacco use on periodontal status. Journalof Dental Education. 2001; 65: 313-321.
38.Golub LM, Ryan ME, Williams RC.Modulation of the host response in thetreatment of periodontitis. DentistryToday. 1998; 17:102-109.
39.Tripathi KD. Essentials of MedicalPharmacology, Jaypee brothers medicalpublishers (p) Ltd. 2008.
40.Armitage GC. The complete periodontalexamination. Periodontology 2000. 2004;34: 22-33.
41.Morrison EC, Ramfjord SP, Hill RW.Short-term effects of initial, nonsurgicalperiodontal treatment (hygienic phase).
Journal of Clinical Periodontology.1980; 7:199-211.
42.Badersten A, Nilveus R, Egelberg J.Effect of nonsurgical periodontal therapyI. Moderately advanced periodontitis.Journal of Clinical Periodontology. 1981;8: 57-72.
43.D’Aiuto F, Parkar M, Andreou G, SuvanJ, Brett PM, Ready D, Tonetti MS.Periodontitis and systemic inflammation:control of the local infection is associatedwith a reduction in serum inflammatorymarkers. Journal of Dental Research.2004; 83:156-160.
44.Offenbacher S, Lin D, Strauss R,McKaig R, Irving J, Barros SP, Moss K,Barrow DA, Hefti A, Beck JD. Effects ofperiodontal therapy during pregnancy onperiodontal status, biologic parameters,and pregnancy outcomes: a pilot study.Journal of Periodontology. 2006; 77:2011-2024.
45.Radafshar G, Torabi F, Mirfarhadi N.Short-term effects of intensive non-surgical periodontal therapy and low-dose doxycycline on serum levels of IL-6, TNF-? and lipid profile in advancedperiodontitis. African Journal ofMicrobiology Research. 2012; 6: 355-360.
46.D’Aiuto F, Nibali L, Parkar M, Suvan J,Tonetti MS. Short-term effects ofintensive periodontal therapy on seruminflammatory markers and cholesterol.Journal of Dental Research. 2005; 84:269-273.
47.Oz SG, Fentoglu O, Kilicarslan A, GuvenGS, Tanrtover MD, Aykac Y, Sozen T.Beneficial effects of periodontaltreatment on metabolic control ofhypercholesterolemia. Southern MedicalAssociation Journal. 2007; 100: 686-691.
48.Fentoglu O, Sozen T, Oz SG., Kale B,Sonmez Y, Tonguc MO, Gurgan CA,Aykaç Y, Kirzio?lu FY. Short-term effects of periodontal therapy as an adjunct to anti-lipemic treatment. Oral Disease. 2010; 16: 648-654.
49.Pussinen PJ, Jauhiainen M, RautiainenTV, Sundvall J, Vesanen M, Mattila K,
Palosuo T, Alfthan G, Asikainen S.Periodontitis decreases theantiatherogenic potency of high densitylipoprotein. Journal of Lipid Research.2004; 45: 139-147.

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