Obesity, metabolic syndrome, and atherosclerosis are linked with an increased acute-phase response. Severe periodontal disease is associated with cardiovascular disease as sequelae of a systemic inflammatory response.
Objective:
The aim of this study was to assess changes in measures of systemic inflammation induced by periodontal therapy in periodontally diseased individuals with metabolic syndrome, compared to those induced in a systemically healthy group.
Methods:
A total of 31 subjects with chronic generalized periodontitis, including 16 subjects with metabolic syndrome (group A) and 15 systemically healthy subjects (group B), underwent nonsurgical periodontal therapy. Serum high-sensitivity C-reactive protein (hsCRP), total leukocyte count, and measures of lipid metabolism were measured at baseline and at 2 months after periodontal therapy. Baseline data for comparison was also obtained from 15 systemically and periodontally healthy individuals (group C).
Results:
Baseline periodontal parameters and serum CRP were significantly higher in group A than in group B. In group A, following periodontal therapy, a significant decrease was noted in mean serum CRP (3.28 ± 1.4 mg/L to 2.6 ± 1.5 mg/L), total leukocyte counts (8,322 ± 1,888 cells/mm3 to 6,361 ± 1,426 cells/mm3), serum triglycerides (153.3 ± 38 mg/dL to 121.0 ± 28.57mg/dL), along with a significant rise in serum high-density lipoprotein (HDL) (41.1 ± 5.2 mg/dL to 44.37 ± 6.7 mg/dL). In group B, changes in these parameters were not statistically significant. Mean serum low-density lipoprotein (LDL) and mean cholesterol levels did not change significantly in either group.
Conclusions:
Periodontal therapy produced significant modulation of serum hsCRP, total leukocytes, serum triglycerides, and HDL, and thus may benefit individuals affected with both metabolic syndrome and advanced periodontal disease.
GuptaR, DeedwaniaPC, GuptaA, RastogiS, PanwarRB, KothariK. Prevalence of metabolic syndrome in an Indian urban population. Int J Cardiol, 2004; 97:257–261.
3.
SaitoT, ShimazakiY, KogaT, TsuzukiMOhshima. A Relationship between upper body obesity and periodontitis. J Dent Res, 2001; 80:1631–1636.
4.
SaitoT, ShimazakiY, KiyoharaY, KatoI, KuboM, IidaM, YamashitaY. Relationship between obesity, glucose tolerance, and periodontal disease in Japanese women: The Hisayama study. J Periodontal Res, 2005; 40:346–353.
5.
D'AiutoF, SabbahW, NetuveliG, DonosN, HingoraniAD, DeanfieldJ, TsakosG. Association of the metabolic syndrome with severe periodontitis in a large U.S population-based survey. J Clin Endocrinol Metab, 2008; 93:3989–3994.
6.
ShimazakiY, SaitoT, YonemotoK, KiyoharaY, IidaM, YamashitaY. Relationship of metabolic syndrome to periodontal disease in Japanese women: The Hisayama Study. J Dent Res, 2007; 86:271–275.
7.
KushiyamaM, ShimazakiY, YamashitaY. Relationship between metabolic syndrome and periodontal disease in Japanese adults. J Periodontal, 2009; 80:1610–1615.
8.
D'AiutoF, NibaliL, ParkerM, SuvanJ, TonettiMS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res, 2005; 84:269–273.
9.
IdeM, JagdevD, CowardPY, CrookM, BarclayGR, WilsonRF. The short-term effects of treatment of chronic periodontitis on circulating levels of endotoxin, C-reactive protein, tumor necrosis factor-alpha, and interleukin-6. J Periodontol, 2004; 75:420–428.
10.
IoannidouE, MalakzadehT, BagdzoglouA. Effect of Periodontal treatment on serum C reactive protein levels: A systematic review and meta-analysis. J Periodontol, 2006; 77:1635–1642
11.
IwamotoY, NishimuraF, SogaY, TakeuchiK, KuriharaM, TakashibaS, MurayamaY. Antimicrobial periodontal treatment decreases serum C-reactive protein, tumor necrosis factor-alpha, but not adiponectin levels in patients with chronic periodontitis. J Periodontol, 2003; 74:1231–1236.
12.
IacopinoAM, CutlerCW. Pathophysiological relationships between periodontitis and systemic disease: recent concepts involving serum lipids. J Periodontol, 2000; 71:1375–1384.
13.
BullonP, MorilloJM, Ramirez-TortosaMC, QuilesJL, NewmanHN, BattinoM. Metabolic syndrome, and periodontitis: Is oxidative stress a common link?J Dent Res, 2009; 88:503–518.
14.
BertzWA, WeyantRJ, CorbyPM, RenD, WeissfeldL, KirtchevskySB, HarrisT, KurellaM, SatterfieldS, VisserM, NewmanAB. Systemic inflammatory markers, periodontal diseases, and periodontal infections in an elderly population. J Am Geriatr Soc, 2005; 53:1532–1537.
15.
GrundySM, CleemanJI, DanielsSR, DonatoKA, EckelRH, FranklinBA, GordonDJ, KraussRM, SavagePJ, SmithSCJr, SpertusJA, CostaF, American HeartAssociation, NationalHeart. Lung, Blood Institute. Diagnosis and management of the metabolic syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation, 2005; 112:2735–2752.
16.
D'AiutoF, SabbahW, NetuveliG, DonosN, HingoraniAD, DeanfieldJ, TsakosG. Association of the metabolic syndrome with severe periodontitis in a large U.S. population-based survey. J Clin Endocrinol Metab, 2008; 93:3989–3994.
17.
LakkaHM, LaaksonenDE, LakkaTA, NiskanenLK, KumpusaloE, TuomilehtoJ, SalonenJT. The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA, 2002; 288:2709–2716.
18.
LiP, HeL, ShaYQ, LuanQX. Relationship of metabolic syndrome to chronic periodontitis. J Periodontol, 2009; 80:541–549.
19.
TamakoshiK, YatsuyaH, KondoT, HoriY, IshikawaM, ZhangH, MurataC, OtsukaR, ZhuS, ToyoshimaH. The metabolic syndrome is associated with elevated circulating C-reactive protein in healthy reference range, a systemic low-grade inflammatory state. Int J Obes Relat Metab Disord, 2003; 27:443–449.
20.
CraigRG, YipJK, SoMK, BoylanRJ, SocranksySS, HaffajeeAD. Relationship of destructive periodontal disease to the acute phase response. J Periodontol, 2003; 74:1007–1016.
21.
NoackB, GencoRJ, TrevisanM, GrossiS, ZambonJJ, De NardinE. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol, 2001; 72:1221–1227.
22.
PearsonTA, MensahGA, AlexanderRW, AndersonJL, CannonRO, CriquiM, FadlYY, FortmannSP, HongY, MyersGL, RifaiN, SmithSC, TaubertK, TracyRP, VinicorF. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation, 2003; 107:499–511.
23.
RidkerPM, HennekensCH, BuringJE, RifaiN. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med, 2000; 342:836–843.
24.
RidkerPM, BuringJE, CookNR, RifaiN. C-Reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: An 8-year follow-up of 14,719 initially healthy American women. Circulation, 2003; 107:391–397.
25.
BaoYQ, JiaWP, ChenL, LuJX, XiangKS. Association between C-reactive protein level and metabolic syndrome and components thereof. Zhonghua Yi Xue Za Zhi, 2006; 86:2105–2109.
26.
PasceriV, WillersonJT, YehET. Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation, 2000; 102:2165–2168.
27.
DaneshJ, CollinsR, ApplebyP, PetoR. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: Meta-analyses of prospective studies. JAMA, 1998; 279:1477–1482.
28.
SweetnamPM, ThomasHF, YarnellJWG, BakerIA, ElwoodPC. Total and differential leukocyte counts as predictors of ischemic heart disease: The Caerphilly and Speedwell Studies. Am J Epidemiol, 145:416–421.
29.
BléA, PalmieriE, VolpatoS, CostantiniF, FellinR, ZulianiG. White blood cell count is associated with some features of metabolic syndrome in a very old population. Nutr Metab Cardiovasc Dis, 2001; 11:221–226.
30.
NagasawaN, TamakoshiK, YatsuyaH, HoriY, IshikawaM, MurataC, ZhangH, WadaK, OtsukaR, MabuchiT, KondoT, ToyoshimaH. Association of white blood cell count and clustered components of metabolic syndrome in Japanese men. Circ J, 2004; 68:892–897.
31.
AmarS, GokceN, MorganS, LoukideliM, Van DykeTE, VitaJA. Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol, 2003; 23:1245–1249.
32.
ZhuJ, QuyyumiAA, NormanJE, CsakoG, WaclawiwMA, ShearerG M, EpsteinSE. Effects of total pathogen burden on coronary artery disease and C-reactive protein levels. Am J Cardiol, 2000; 85:140–146.
33.
LindyO, SuomalainenK, MakelaM, LindyS. Statin use is associated with fewer periodontal lesions: A retrospective study. BMC Oral Health, 2008; 8:16.
34.
RidkerPM, BuringJE, CookNR, RifaiN. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: An 8-year follow-up of 14 719 initially healthy American women. Circulation, 2003; 107:391–397.
35.
MalikS, WongND, FranklinS, PioJ, FairchildC, ChenR. Cardiovascular disease in U.S. patients with metabolic syndrome, diabetes, and elevated C-reactive protein. Diabetes Care, 2005; 28:690–693.
36.
KoenigW, SundM, FrohlichM, FischerHG, LowelH, DoringA, HutchinsonWL, PepysMB. C-reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: Results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation, 1999; 99:237–242.
37.
ChristianC, DietrichT, HagervaldS, KageA, BernimoulinJP. White blood cell count in generalized aggressive periodontitis after non-surgical therapy. J Clin Periodontol, 2002; 29:201–206.
38.
LoosBG. Systemic markers of inflammation in periodontitis. J Periodontol, 2005; 76:ll–s, 2106–2115.
39.
HorneBD, AndersonJL, JohnJM, WeaverA, BairTL, JensenKR, RenlundDG, MuhlesteinJB. Intermountain Heart Collaborative Study Group. Which white blood cell subtypes predict increased cardiovascular risk?J Am Coll Cardiol, 2005; 45:1638–1643.
40.
WaterhouseD, CahillR, SheehanF. Prediction of calculated future cardiovascular disease by monocyte count in an asymptomatic population. Vasc Health Risk Manag, 2008; 4:177–187.
41.
DuanJY, Ou-YangXY, ZhouYX. Effect of periodontal initial therapy on the serum level of lipid in the patients with both periodontitis and hyperlipidemia. Beijing Da Xue Xue Bao, 2009; 41:36–39.
D'AiutoF, ParkarM, BrettPM, ReadyD, TonettiMS. Gene polymorphisms in pro-inflammatory cytokines are associated with systemic inflammation in patients with severe periodontal infections. Cytokine, 2004; 28:29–34.
44.
BullonP, MorilloJM, Ramirez-TortosaMC, QuilesJL, NewmanHN, BattinoM. Metabolic syndrome and periodontitis: Is oxidative stress a common link?J Dent Res, 2009; 88:503–518.
