Advertisement

Current Oral Health Reports

, Volume 5, Issue 2, pp 108–115 | Cite as

Periodontal Host Response in Subjects with Obesity

  • Hideaki Hayashida
  • Reiko FurugenEmail author
  • Toshiyuki Saito
Oral Disease and Nutrition (F Nishimura, Section Editor)
  • 51 Downloads
Part of the following topical collections:
  1. Topical Collection on Oral Disease and Nutrition

Abstract

Purpose of Review

This review focuses on recent advances in understanding the periodontal host response in obese subjects.

Recent Findings

Increased pro-inflammatory adipokines such as leptin, progranulin, resistin, and visfatin and decreased anti-inflammatory adipokines such as adiponectin, exacerbated inflammatory response, alveolar bone resorption, and inhibition of tissue regeneration have been observed in the periodontal tissue in obese subjects. Elevated oxidative stress also affects progression of periodontitis. Obesity may affect the expression of microRNAs related to inflammatory and metabolic mRNA targets in periodontal tissue.

Summary

Although obesity may promote the progression of periodontitis in multiple manners, additional studies are needed to clarify the periodontal host response in obesity.

Keywords

Periodontal host response Obesity Adipokine Oxidative stress MicroRNA 

Notes

Compliance with Ethics Standards

Conflict of Interest

All authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance, •• Of major importance

  1. 1.
    World Health Organization: Obesity and overweight. 2016. http://who.int/mediacentre/factsheets/fs311/en/. Accessed 12 Jan 2018.
  2. 2.
    Kopelman PG. Obesity as a medical problem. Nature. 2000;6(404):635–43.  https://doi.org/10.1038/35007508.CrossRefGoogle Scholar
  3. 3.
    Haffner SM. Relationship of metabolic risk factors and development of cardiovascular disease and diabetes. Obesity (Silver Spring). 2006;14(Suppl 3):121S–7S.  https://doi.org/10.1038/oby.2006.291.CrossRefGoogle Scholar
  4. 4.
    Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. N Engl J Med. 1998;339:482–3.  https://doi.org/10.1056/NEJM199808133390717.CrossRefPubMedGoogle Scholar
  5. 5.
    Guerre-Millo M. Adipose tissue hormones. J Endocrinol Investig. 2002;25:855–6.  https://doi.org/10.1007/BF03344048.CrossRefGoogle Scholar
  6. 6.
    Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752–61.  https://doi.org/10.1172/JCI21625.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    • Dursun E, Akalin FA, Genc T, Cinar N, Erel O, Yildiz BO. Oxidative stress and periodontal disease in obesity. Medicine (Baltimore). 2016;95:e3136.  https://doi.org/10.1097/MD.0000000000003136. This manuscript reported that early stage of periodontal diseases was correlated with systemic and periodontal oxidant status in obese. CrossRefGoogle Scholar
  8. 8.
    •• Marques-Rocha JL, Samblas M, Milagro FI, Bressan J, Martínez JA, Marti A. Noncoding RNAs, cytokines, and inflammation-related diseases. FASEB J. 2015;29:3595–611.  https://doi.org/10.1096/fj.14-260323. This manuscript reviewed the possible role of miRNAs in inflammation-related diseases such as obesity and periodontitis. CrossRefPubMedGoogle Scholar
  9. 9.
    Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (adipose most abundant gene transcript 1). Biochem Biophys Res Commun. 1996;221:286–9.  https://doi.org/10.1006/bbrc.1996.0587.CrossRefPubMedGoogle Scholar
  10. 10.
    Cheng KK, Lam KS, Wang B, Xu A. Signaling mechanisms underlying the insulin-sensitizing effects of adiponectin. Best Pract Res Clin Endocrinol Metab. 2014;28:3–13.  https://doi.org/10.1016/j.beem.2013.06.006.CrossRefPubMedGoogle Scholar
  11. 11.
    Liu M, Liu F. Regulation of adiponectin multimerization, signaling and function. Best Pract Res Clin Endocrinol Metab. 2014;28:25–31.  https://doi.org/10.1016/j.beem.2013.06.003.CrossRefPubMedGoogle Scholar
  12. 12.
    Yamauchi T, Iwabu M, Okada-Iwabu M, Kadowaki T. Adiponectin receptors: a review of their structure, function and how they work. Best Pract Res Clin Endocrinol Metab. 2014;28:15–23.  https://doi.org/10.1016/j.beem.2013.09.003.CrossRefPubMedGoogle Scholar
  13. 13.
    Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie. 2012;94:2143–9.  https://doi.org/10.1016/j.biochi.2012.06.030.CrossRefPubMedGoogle Scholar
  14. 14.
    Kraus D, Winter J, Jepsen S, Jäger A, Meyer R, Deschner J. Interactions of adiponectin and lipopolysaccharide from Porphyromonas gingivalis on human oral epithelial cells. PLoS One. 2012;7:e30716.  https://doi.org/10.1371/journal.pone.0030716.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Fiaschi T, Magherini F, Gamberi T, Modesti PA, Modesti A. Adiponectin as a tissue regenerating hormone: more than a metabolic function. Cell Mol Life Sci. 2014;71:1917–25.  https://doi.org/10.1007/s00018-013-1537-4.CrossRefPubMedGoogle Scholar
  16. 16.
    Zhang L, Meng S, Tu Q, Yu L, Tang Y, Dard MM, et al. Adiponectin ameliorates experimental periodontitis in diet-induced obesity mice. PLoS One. 2014;9:e97824.  https://doi.org/10.1371/journal.pone.0097824. eCollection 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    McGuire MK, Cochran DL. Evaluation of human recession defects treated with coronally advanced flaps and either enamel matrix derivative or connective tissue. Part 2: histological evaluation. J Periodontol. 2003;74:1126–35.  https://doi.org/10.1902/jop.2003.74.8.1126.CrossRefPubMedGoogle Scholar
  18. 18.
    Sculean A, Alessandri R, Miron R, Salvi GE, Bosshardt DD. Enamel matrix proteins and periodontal wound healing and regeneration. Clin Adv Periodontics. 2011;1:101–17.  https://doi.org/10.1902/cap.2011.110047.CrossRefGoogle Scholar
  19. 19.
    Yukna RA, Mellonig JT. Histologic evaluation of periodontal healing in humans following regenerative therapy with enamel matrix derivative. A 10-case series. J Periodontol. 2000;7:752–9.  https://doi.org/10.1902/jop.2000.71.5.752.CrossRefGoogle Scholar
  20. 20.
    Bosshardt DD. Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels. J Clin Periodontol. 2008;35:87–105.  https://doi.org/10.1111/j.1600-051X.2008.01264.x.CrossRefPubMedGoogle Scholar
  21. 21.
    Johnson DL, Carnes D, Steffensen B, Cochran DL. Cellular effects of enamel matrix derivative are associated with different molecular weight fractions following separation by size-exclusion chromatography. J Periodontol. 2009;80:648–56.  https://doi.org/10.1902/jop.2009.070420.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Nokhbehsaim M, Keser S, Nogueira AV, Cirelli JA, Jepsen S, Jäger A, et al. Beneficial effects of adiponectin on periodontal ligament cells under normal and regenerative conditions. J Diabetes Res. 2014;2014:796565–11.  https://doi.org/10.1155/2014/796565.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    White RT, Damm D, Hancock N, Rosen BS, Lowell BB, Usher P, et al. Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue. J Biol Chem. 1992;267(13):9210–3.PubMedGoogle Scholar
  24. 24.
    Nashef A, Abu-Toamih Atamni HJ, Buchnik Y, Hasturk H, Kantarci A, Stephens D, et al. Collaborative cross mouse population for studying alveolar bone changes and impaired glucose tolerance comorbidity after high-fat diet consumption. J Periodontol. 2017;88(9):e150–8.  https://doi.org/10.1902/jop.2017.170075.CrossRefPubMedGoogle Scholar
  25. 25.
    Tabata M, Kadomatsu T, Fukuhara S, Miyata K, Ito Y, Endo M, et al. Angiopoietin-like protein 2 promotes chronic adipose tissue in annimation and obesity-related systemic insulin resistance. Cell Metab. 2009;10:178–88.  https://doi.org/10.1016/j.cmet.2009.08.003.CrossRefPubMedGoogle Scholar
  26. 26.
    Ohno T, Yamamoto G, Hayashi J, Nishida E, Goto H, Sasaki Y, et al. Angiopoietin-like protein 2 regulates Porphyromonas gingivalis lipopolysaccharide-induced inflammatory response in human gingival epithelial cells. PLoS One. 2017;12(9):e0184825.  https://doi.org/10.1371/journal.pone.0184825.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Takano A, Fukuda T, Shinjo T, Iwashita M, Matsuzaki E, Yamamichi K, et al. Angiopoietin-like protein 2 is a positive regulator of osteoblast differentiation. Metabolism. 2017;69:157–70.  https://doi.org/10.1016/j.metabol.2017.01.006.CrossRefPubMedGoogle Scholar
  28. 28.
    Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature. 1998;395:763–70.  https://doi.org/10.1038/27376.CrossRefPubMedGoogle Scholar
  29. 29.
    Procaccini C, Lourenco EV, Matarese G, La Cava A. Leptin signaling: a key pathway in immune responses. Curr Signal Transduction Ther. 2009;4:22–30.  https://doi.org/10.2174/157436209787048711.CrossRefGoogle Scholar
  30. 30.
    Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005;115:911–9.  https://doi.org/10.1016/j.jaci.2005.02.023.CrossRefPubMedGoogle Scholar
  31. 31.
    Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334:292–5.  https://doi.org/10.1056/NEJM199602013340503.CrossRefPubMedGoogle Scholar
  32. 32.
    Li W, Huang B, Liu K, Hou J, Meng H. Upregulated leptin in periodontitis promotes inflammatory cytokine expression in periodontal ligament cells. J Periodontol. 2015;86:917–26.  https://doi.org/10.1902/jop.2015.150030.CrossRefPubMedGoogle Scholar
  33. 33.
    Bartold PM, Narayanan AS. Molecular and cell biology of healthy and diseased periodontal tissues. Periodontol. 2006;40:29–49.  https://doi.org/10.1111/j.1600-0757.2005.00140.x.CrossRefGoogle Scholar
  34. 34.
    • Williams RC, Skelton AJ, Todryk SM, Rowan AD, Preshaw PM, Taylor JJ. Leptin and pro-inflammatory stimuli synergistically upregulate MMP-1 and MMP-3 secretion in human gingival fibroblasts. PLoS One. 2016;11:e0148024.  https://doi.org/10.1371/journal.pone.0148024. This manuscript reported that leptin and IL-6 synergistically upregulates MMPs degrading collagens in human gingival fibroblast. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nokhbehsaim M, Keser S, Nogueira AV, Jäger A, Jepsen S, Cirelli JA, et al. Leptin effects on the regenerative capacity of human periodontal cells. Int J Endocrinol. 2014;2014:180304–13.  https://doi.org/10.1155/2014/180304.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Korolczuk A, Bełtowski J. Progranulin: a new adipokine at the crossroads of metabolic syndrome, diabetes, dyslipidemia and hypertension. Curr Pharm Des. 2017;23:1533–9.  https://doi.org/10.2174/1381612823666170124114524.CrossRefPubMedGoogle Scholar
  37. 37.
    Daniel R, Daniels E, He Z, Bateman A. Progranulin (acrogranin/PC cell-derived growth factor/granulin-epithelin precursor) is expressed in the placenta, epidermis, microvasculature, and brain during murine development. Dev Dyn. 2003;227:593–9.  https://doi.org/10.1002/dvdy.10341.CrossRefPubMedGoogle Scholar
  38. 38.
    He Z, Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med. 2003;81:600–12.  https://doi.org/10.1007/s00109-003-0474-3.CrossRefPubMedGoogle Scholar
  39. 39.
    He Z, Ong CH, Halper J, Bateman A. Progranulin is a mediator of the wound response. Nat Med. 2003;9:225–9.  https://doi.org/10.1038/nm816.CrossRefPubMedGoogle Scholar
  40. 40.
    Youn BS, Bang SI, Klöting N, Park JW, Lee N, Oh JE, et al. Serum progranulin concentrations may be associated with macrophage infiltration into omental adipose tissue. Diabetes. 2009;58:627–36.  https://doi.org/10.2337/db08-1147.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Pradeep AR, Priyanka N, Prasad MV, Kalra N, Kumari M. Association of progranulin and high sensitivity CRP concentrations in gingival crevicular fluid and serum in chronic periodontitis subjects with and without obesity. Dis Markers. 2012;33:207–13.  https://doi.org/10.3233/DMA-2012-0926.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Savage DB, Sewter CP, Klenk ES, Segal DG, Vidal-Puig A, Considine RV, et al. Resistin/fizz3 expression in relation to obesity and peroxisome proliferator-activated receptor-gamma action in humans. Diabetes. 2001;50:2199–202.  https://doi.org/10.2337/diabetes.50.10.2199.CrossRefPubMedGoogle Scholar
  43. 43.
    Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ. Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kB-dependent pathway. Biochem Biophys Res Commun. 2005;334:1092–101.  https://doi.org/10.1016/j.bbrc.2005.06.202.CrossRefPubMedGoogle Scholar
  44. 44.
    Lu SC, Shieh WY, Chen CY, Hsu SC, Chen HL. Lipopolysaccharide increases resistin gene expression in vivo and in vitro. FEBS Lett. 2002;530:158–62.  https://doi.org/10.1016/S0014-5793(02)03450-6.CrossRefPubMedGoogle Scholar
  45. 45.
    Furugen R, Hayashida H, Yamaguchi N, Yoshihara A, Ogawa H, Miyazaki H, et al. The relationship between periodontal condition and serum levels of resistin and adiponectin in elderly Japanese. J Periodontal Res. 2008;43:556–62.  https://doi.org/10.1111/j.1600-0765.2008.01085.x.CrossRefPubMedGoogle Scholar
  46. 46.
    Saito T, Yamaguchi N, Shimazaki Y, Hayashida H, Yonemoto K, Doi Y, et al. Serum levels of resistin and adiponectin in women with periodontitis: the Hisayama study. J Dent Res. 2008;87:319–22.  https://doi.org/10.1177/154405910808700416.CrossRefPubMedGoogle Scholar
  47. 47.
    Thommesen L, Stunes AK, Monjo M, Grosvik K, Tamburstuen MV, Kjobli E, et al. Expression and regulation of resistin in osteoblasts and osteoclasts indicate a role in bone metabolism. J Cell Biochem. 2006;99:824–34.  https://doi.org/10.1002/jcb.20915.CrossRefPubMedGoogle Scholar
  48. 48.
    Suresh S, Mahendra J, Singh G, Pradeep A, Sundaravikram SH. Comparative analysis of GCF resistin levels in obese subjects with and without periodontal disease. J Clin Diagn Res. 2016;10:ZC71–4.  https://doi.org/10.7860/JCDR/2016/19066.7802.PubMedPubMedCentralGoogle Scholar
  49. 49.
    He W, Wang ML, Jiang HQ, Steppan CM, Shin ME, Thurnheer MC, et al. Bacterial colonization leads to the colonic secretion of RELMbeta/FIZZ2, a novel goblet cell-specific protein. Gastroenterology. 2003;125(5):1388–97.CrossRefPubMedGoogle Scholar
  50. 50.
    Mishra A, Wang M, Schlotman J, Nikolaidis NM, DeBrosse CW, Karow ML, et al. Resistin-like molecule-beta is an allergen-induced cytokine with inflammatory and remodeling activity in the murine lung. Am J Physiol Lung Cell Mol Physiol. 2007;293(2):L305–13.  https://doi.org/10.1152/ajplung.00147.CrossRefPubMedGoogle Scholar
  51. 51.
    Kushiyama A, Sakoda H, Oue N, Okubo M, Nakatsu Y, Ono H, et al. Resistin-like molecule β is abundantly expressed in foam cells and is involved in atherosclerosis development. Arterioscler Thromb Vasc Biol. 2013;33(8):1986–93.  https://doi.org/10.1161/ATVBAHA.113.301546.CrossRefPubMedGoogle Scholar
  52. 52.
    Samal B, Sun Y, Stearns G, Xie C, Suggs S, McNiece I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol Cell Biol. 1994;14:1431–7.  https://doi.org/10.1128/MCB.14.2.1431.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Jia SH, Li Y, Parodo J, Kapus A, Fan L, Rotstein OD, et al. Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis. J Clin Invest. 2004;113:1318–27.  https://doi.org/10.1172/JCI19930.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Rongvaux A, Shea RJ, Mulks MH, Gigot D, Urbain J, Leo O, et al. Pre-B-cell colony-enhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur J Immunol. 2002;32:3225–34.  https://doi.org/10.1002/1521-4141(200211)32:11<3225::AID-IMMU3225>3.0.CO;2-L.CrossRefPubMedGoogle Scholar
  55. 55.
    Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 2005;307:426–30.  https://doi.org/10.1126/science.1097243.CrossRefPubMedGoogle Scholar
  56. 56.
    Moschen AR, Gerner RR, Tilg H. Pre-B cell colony enhancing factor/NAMPT/visfatin in inflammation and obesity related disorders. Curr Pharm Des. 2010;16:1913–20.  https://doi.org/10.2174/138161210791208947.CrossRefPubMedGoogle Scholar
  57. 57.
    Pradeep AR, Raghavendra NM, Prasad MV, Kathariya R, Patel SP, Sharma A. Gingival crevicular fluid and serum visfatin concentration: their relationship in periodontal health and disease. J Periodontol. 2011;82:1314–9.  https://doi.org/10.1902/jop.2011.100690.CrossRefPubMedGoogle Scholar
  58. 58.
    Nokhbehsaim M, Keser S, Jäger A, Jepsen S, Deschner J. Regulation of regenerative periodontal healing by NAMPT. Mediat Inflamm. 2013;2013:202530–11.  https://doi.org/10.1155/2013/202530.Google Scholar
  59. 59.
    Nogueira AV, Nokhbehsaim M, Eick S, Bourauel C, Jäger A, Jepsen S, et al. Regulation of visfatin by microbial and biomechanical signals in PDL cells. Clin Oral Investig. 2014;18:171–8.  https://doi.org/10.1007/s00784-013-0935-1.CrossRefPubMedGoogle Scholar
  60. 60.
    Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies. Metab Syndr Relat Disord. 2015;13:423–44.  https://doi.org/10.1089/met.2015.0095.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol. 2007;43:160–232.  https://doi.org/10.1111/j.1600-0757.2006.00178.x.CrossRefGoogle Scholar
  62. 62.
    Tomofuji T, Yamamoto T, Tamaki N, Ekuni D, Azuma T, Sanbe T, et al. Effects of obesity on gingival oxidative stress in a rat model. J Periodontol. 2009;80:1324–9.  https://doi.org/10.1902/jop.2009.080621.CrossRefPubMedGoogle Scholar
  63. 63.
    Öngöz Dede F, Bozkurt Doğan Ş, Ballı U, Avcı B, Durmuşlar MC. The effect of initial periodontal treatment on plasma, gingival crevicular fluid and salivary levels of 8-hydroxy-deoxyguanosine in obesity. Arch Oral Biol. 2016;62:80–5.  https://doi.org/10.1016/j.archoralbio.2015.11.014.CrossRefPubMedGoogle Scholar
  64. 64.
    Atabay VE, Lutfioğlu M, Avci B, Sakallioglu EE, Aydoğdu A. Obesity and oxidative stress in patients with different periodontal status: a case-control study. J Periodontal Res. 2017;52:51–60.  https://doi.org/10.1111/jre.12368.CrossRefPubMedGoogle Scholar
  65. 65.
    Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–33.  https://doi.org/10.1016/j.cell.2009.01.002.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Perri R, Nares S, Zhang S, Barros SP, Offenbacher S. MicroRNA modulation in obesity and periodontitis. J Dent Res. 2012;91:33–8.  https://doi.org/10.1177/0022034511425045.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Kalea AZ, Hoteit R, Suvan J, Lovering RC, Palmen J, Cooper JA, et al. Upregulation of gingival tissue miR-200b in obese periodontitis subjects. J Dent Res. 2015;94(Suppl 3):59S–69S.  https://doi.org/10.1177/0022034514568197.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Hideaki Hayashida
    • 1
  • Reiko Furugen
    • 1
    Email author
  • Toshiyuki Saito
    • 1
  1. 1.Department of Oral Health, Unit of Social Medicine, Graduate School of Biomedical SciencesNagasaki UniversityNagasakiJapan

Personalised recommendations