Current Diabetes Reports

, 15:93 | Cite as

Is There a Relationship Between Oral Health and Diabetic Neuropathy?

  • Wenche S. BorgnakkeEmail author
  • Patricia F. Anderson
  • Carol Shannon
  • Anca Jivanescu
Microvascular Complications—Neuropathy (R Pop-Busui, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Microvascular Complications—Neuropathy


Diabetic neuropathy is the most common microvascular complication of diabetes mellitus with high morbidity and mortality, and low quality of life. It has a broad spectrum of clinical forms, although distal symmetrical polyneuropathy is the most prevalent. Several oral complications including burning mouth syndrome, dry mouth, and impairment of the senses taste and smell are less-known manifestations of diabetic neuropathy and often overlooked. Periodontitis, tooth loss, and temporomandibular joint dysfunction may be also present in these patients and are equally debilitating. Periodontitis was declared the sixth complication of diabetes in 1993 and may contribute to poor glucose control. Hence, periodontitis and diabetes mutually and adversely affect each other. This review summarizes the available body of scientific literature that discusses oral manifestations in patients with diabetic neuropathy and identifies important areas where more research is needed.


Burning mouth syndrome Diabetic neuropathies Dysgeusia Glossodynia Hyposalivation Inflammation Interprofessional relations Mouth dryness Periodontitis Periodontal treatment Xerostomia 


Compliance with Ethics Guidelines

Conflict of Interest

Wenche S. Borgnakke, Patricia F. Anderson, Carol Shannon, and Anca Jivanescu declare that they have no conflict 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.


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

  1. 1.••
    Albers JW, Pop-Busui R. Diabetic neuropathy: mechanisms, emerging treatments, and subtypes. Curr Neurol Neurosci Rep. 2014;14:473. doi: 10.1007/s11910-014-0473-5. Excellent, recent, evidence based descriptions of the various types of diabetic neuropathy, their underlying mechanisms, and therapeutic options. Figure 1 illustrates in a conceptual model the mechanisms underlying diabetic distal symmetric polyneuropathy via the inflammatory cascade, which is identical to the inflammation initiated by the bacterial dental plaque in periodontitis.CrossRefPubMedGoogle Scholar
  2. 2.
    Deli G, Bosnyak E, Pusch G, Komoly S, Feher G. Diabetic neuropathies: diagnosis and management. Neuroendocrinology. 2013;98:267–80. doi: 10.1159/000358728.CrossRefPubMedGoogle Scholar
  3. 3.
    Edwards JL, Vincent AM, Cheng HT, Feldman EL. Diabetic neuropathy: mechanisms to management. Pharmacol Ther. 2008;120:1–34. doi: 10.1016/j.pharmthera.2008.05.005.PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285–93. doi: 10.2337/dc10-1303.PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care. 1993;16:329–34.CrossRefPubMedGoogle Scholar
  6. 6.••
    Borgnakke WS, Ylöstalo PV, Taylor GW, Genco RJ. Effect of periodontal disease on diabetes: systematic review of epidemiologic observational evidence. J Periodontol. 2013;84:S135–52. doi: 10.1902/jop.2013.1340013. This is the first systematic review of the evidence for the effects of periodontal infection on blood glucose levels in health, prediabetes, type 1 and type 2 diabetes, and gestational diabetes as well as on development of new type 2 and gestational diabetes.CrossRefPubMedGoogle Scholar
  7. 7.
    Borgnakke WS. Ch. 6. Hyperglycemia/diabetes mellitus and periodontal infection adversely affect each other. In: Genco RJ, Williams RC, editors. Periodontal disease and overall health: A clinician’s guide. 2nd ed. Yardley, PA: Professional Audience Communications; 2014 p. 99-122. Available at: Http://www.Colgateprofessional.Com/professional-education/articles/periodontal-disease-and-overall-health-a-clinicians-guide-second-edition. Accessed August 22, 2015.
  8. 8.••
    Borgnakke W. Does treatment of periodontal disease influence systemic disease? Dent Clin North Am. 2015;59(4):n/a. doi: 10.1016/j.cden.2015.06.007. Provides current evidence for effects of periodontal therapy on cumulative bacerial load and inflammatory mediators, diabetes, cerebrocardiovascular disease, rheumatoid arthritis, diseases of the respiratory tract, chronic kidney disease, and adverse pregnancy outcomes. Included is a tabular summary of all meta-analyses on the effect of non-surgical periodontal treatment on glycated hemoglobin levels in type 2 diabetes published by June 1, 2015.
  9. 9.
    Borgnakke WS, Chapple IL, Genco RJ, Armitage G, Bartold PM, D’Aiuto F, et al. The multi-center randomized controlled trial (RCT) published by the Journal of the American Medical Association (JAMA) on the effect of periodontal therapy on glycated hemoglobin (HbA1c) has fundamental problems. J Evid Based Dent Pract. 2014;14:127–32. doi: 10.1016/j.jebdp.2014.04.017.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    American Diabetes Association. 3. Initial evaluation and diabetes management planning. Diabetes Care. 2015;38:S17–9. doi: 10.2337/dc15-S006.CrossRefGoogle Scholar
  11. 11.
    Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366:1809–20. doi: 10.1016/S0140-6736(05)67728-8.CrossRefPubMedGoogle Scholar
  12. 12.
    Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJL, Marcenes W. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res. 2014;93:1045–53. doi: 10.1177/0022034514552491.CrossRefPubMedGoogle Scholar
  13. 13.
    Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol. 2015;86:611–22. doi: 10.1902/jop.2015.140520.CrossRefPubMedGoogle Scholar
  14. 14.•
    Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ, On behalf of the participating members of the CDC Periodontal Disease Surveillance Workgroup. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res. 2012;91:914–20. doi: 10.1177/0022034512457373. For the first time in a US nationally representative survey, periodontitis was assessed by gold standard, full-mouth periodontal probing at six sites around each tooth. The prevalence of almost 50% of adults 30 years and older was much higher than previously estimated based probing two or three sites per tooth in random half jaws.CrossRefPubMedGoogle Scholar
  15. 15.
    Lamster IB, Lalla E, Borgnakke WS, Taylor GW. The relationship between oral health and diabetes mellitus. J Am Dent Assoc. 2008;139(10 Suppl 5):19S–24.CrossRefPubMedGoogle Scholar
  16. 16.
    Kowall B, Holtfreter B, Volzke H, Schipf S, Mundt T, Rathmann W, et al. Pre-diabetes and well-controlled diabetes are not associated with periodontal disease: the SHIP trend study. J Clin Periodontol. 2015;42(5):422–30. doi: 10.1111/jcpe.12391.CrossRefPubMedGoogle Scholar
  17. 17.
    Lin SY, Lin CL, Liu JH, Wang IK, Hsu WH, Chen CJ, et al. Association between periodontitis needing surgical treatment and subsequent diabetes risk: a population-based cohort study. J Periodontol. 2014;85:779–86. doi: 10.1902/jop.2013.130357.CrossRefPubMedGoogle Scholar
  18. 18.
    Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, et al. Years lived with disability (YLDS) for 1160 sequelae of 289 diseases and injuries 1990-2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2013;380:2163–96. doi: 10.1016/s0140-6736(12)61729-2.CrossRefGoogle Scholar
  19. 19.
    Dyck PJ, Albers JW, Andersen H, Arezzo JC, Biessels GJ, Bril V, et al. Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev. 2011;27:620–8. doi: 10.1002/dmrr.1226.CrossRefPubMedGoogle Scholar
  20. 20.
    Lu B, Hu J, Wen J, Zhang Z, Zhou L, Li Y, et al. Determination of peripheral neuropathy prevalence and associated factors in Chinese subjects with diabetes and pre-diabetes - ShangHai Diabetic neuRopathy Epidemiology and Molecular Genetics Study (SH-DREAMS). PLoS One. 2013;8:e61053. doi: 10.1371/journal.pone.0061053.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Papanas N, Vinik AI, Ziegler D. Neuropathy in prediabetes: does the clock start ticking early? Nat Rev Endocrinol. 2011;7:682–90. doi: 10.1038/nrendo.2011.113.CrossRefPubMedGoogle Scholar
  22. 22.
    Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43:817–24.CrossRefPubMedGoogle Scholar
  23. 23.
    Deshpande AD, Harris-Hayes M, Schootman M. Epidemiology of diabetes and diabetes-related complications. Phys Ther. 2008;88:1254–64. doi: 10.2522/ptj.20080020.PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000. 2013;62:59–94. doi: 10.1111/j.1600-0757.2012.00457.x.CrossRefPubMedGoogle Scholar
  25. 25.
    Van Dyke TE, Van Winkelhoff AJ. Infection and inflammatory mechanisms. J Clin Periodontol. 2013;40 Suppl 14:S1–7. doi: 10.1111/jcpe.12088.PubMedGoogle Scholar
  26. 26.
    Han YW, Wang X. Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J Dent Res. 2013;92:485–91. doi: 10.1177/0022034513487559.PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Borgnakke WS. Ch 4. The traveling oral microbiome. In: Glick M, editor. The oral-systemic health connection: a guide to patient care. 312 pp. Chicago: Quintessence; 2014. p. 61–102.Google Scholar
  28. 28.
    Stanley CM, Wang Y, Pal S, Klebe RJ, Harkless LB, Xu X, et al. Fibronectin fragmentation is a feature of periodontal disease sites and diabetic foot and leg wounds and modifies cell behavior. J Periodontol. 2008;79:861–75. doi: 10.1902/jop.2008.070492.PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Rosenthal IM, Abrams H, Kopczyk A. The relationship of inflammatory periodontal disease to diabetic status in insulin-dependent diabetes mellitus patients. J Clin Periodontol. 1988;15:425–9.CrossRefPubMedGoogle Scholar
  30. 30.
    Al-Shammari KF, Al-Ansari JM, Moussa NM, Ben-Nakhi A, Al-Arouj M, Wang HL. Association of periodontal disease severity with diabetes duration and diabetic complications in patients with type 1 diabetes mellitus. J Int Acad Periodontol. 2006;8:109–14.PubMedGoogle Scholar
  31. 31.
    Moore PA, Weyant RJ, Mongelluzzo MB, Myers DE, Rossie K, Guggenheimer J, et al. Type 1 diabetes mellitus and oral health: assessment of tooth loss and edentulism. J Public Health Dent. 1998;58:135–42.CrossRefPubMedGoogle Scholar
  32. 32.
    Moore PA, Weyant RJ, Mongelluzzo MB, Myers DE, Rossie K, Guggenheimer J, et al. Type 1 diabetes mellitus and oral health: assessment of periodontal disease. J Periodontol. 1999;70:409–17. doi: 10.1902/jop.1999.70.4.409.CrossRefPubMedGoogle Scholar
  33. 33.
    Bajaj S, Prasad S, Gupta A, Singh VB. Oral manifestations in type-2 diabetes and related complications. Indian J Endocrinol Metab. 2012;16:777–9. doi: 10.4103/2230-8210.100673.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Sandberg GE, Wikblad KF. Oral dryness and peripheral neuropathy in subjects with type 2 diabetes. J Diabetes Complicat. 2003;17:192–8. doi: 10.1016/S1056-8727(02)00220-9.CrossRefPubMedGoogle Scholar
  35. 35.
    Menchaca-Diaz R, Bogarin-Lopez B, Zamudio-Gomez MA, Anzaldo-Campos MC. Severe periodontitis, edentulism and neuropathy in patients with type 2 diabetes mellitus. [Spanish]. Gac Med Mex. 2012;148:34–41.PubMedGoogle Scholar
  36. 36.•
    Abrao L, Chagas JK, Schmid H. Periodontal disease and risk for neuropathic foot ulceration in type 2 diabetes. Diabetes Res Clin Pract. 2010;90:34–9. doi: 10.1016/j.diabres.2010.06.014. A unique report exploring the links between periodontitis and neuropathic foot ulceration.CrossRefPubMedGoogle Scholar
  37. 37.
    Collin HL, Niskanen L, Uusitupa M, Toyry J, Collin P, Koivisto AM, et al. Oral symptoms and signs in elderly patients with type 2 diabetes mellitus. A focus on diabetic neuropathy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;90:299–305. doi: 10.1067/moe.2000.107536.CrossRefPubMedGoogle Scholar
  38. 38.
    Glore RJ, Spiteri-Staines K, Paleri V. A patient with dry mouth. Clin Otolaryngol. 2009;34:358–63. doi: 10.1111/j.1749-4486.2009.01930.x.CrossRefPubMedGoogle Scholar
  39. 39.
    Sreebny LM, Vissink A, editors. Dry mouth, the malevolent symptom: a clinical guide. Singapore: Wiley-Blackwell. 268 pp. 2010.Google Scholar
  40. 40.
    Sreebny LM, Yu A, Green A, Valdini A. Xerostomia in diabetes mellitus. Diabetes Care. 1992;15(7):900–4.CrossRefPubMedGoogle Scholar
  41. 41.
    Moore PA, Guggenheimer J, Etzel KR, Weyant RJ, Orchard T. Type 1 diabetes mellitus, xerostomia, and salivary flow rates. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001;92:281–91. doi: 10.1067/moe.2001.117815.CrossRefPubMedGoogle Scholar
  42. 42.
    Zakrzewska JM, Forssell H, Glenny AM. Interventions for the treatment of burning mouth syndrome. Cochrane Database Syst Rev 2005:CD002779. doi: 10.1002/14651858.CD002779.pub2.
  43. 43.••
    Kolkka-Palomaa M, Jaaskelainen SK, Laine MA, Teerijoki-Oksa T, Sandell M, Forssell H. Pathophysiology of primary burning mouth syndrome with special focus on taste dysfunction: a review. Oral Dis. 2015. doi: 10.1111/odi.12345. Published online June 25, 2015. Up-to-date critical review of the literature on pathophysiology of burning mouth syndromewith special focus on interactions between the taste and pain systems. Finds convincing evidence for neuropathic involvement at several levels of the somatosensory system.PubMedGoogle Scholar
  44. 44.
    Moore PA, Guggenheimer J, Orchard T. Burning mouth syndrome and peripheral neuropathy in patients with type 1 diabetes mellitus. J Diabetes Complicat. 2007;21:397–402. doi: 10.1016/j.jdiacomp.2006.08.001.CrossRefPubMedGoogle Scholar
  45. 45.
    Arap A, Siqueira SR, Silva CB, Teixeira MJ, Siqueira JT. Trigeminal pain and quantitative sensory testing in painful peripheral diabetic neuropathy. Arch Oral Biol. 2010;55:486–93. doi: 10.1016/j.archoralbio.2010.03.021.CrossRefPubMedGoogle Scholar
  46. 46.
    Le Floch JP, Le Lievre G, Verroust J, Philippon C, Peynegre R, Perlemuter L. Factors related to the electric taste threshold in type 1 diabetic patients. Diabet Med. 1990;7:526–31. doi: 10.1111/j.1464-5491.1990.tb01436.x.CrossRefPubMedGoogle Scholar
  47. 47.
    Satoh-Kuriwada S, Shoji N, Kawai M, Uneyama H, Kaneta N, Sasano T. Hyposalivation strongly influences hypogeusia in the elderly. J Health Sci. 2009;55:689–98. doi: 10.1248/jhs.55.689.CrossRefGoogle Scholar
  48. 48.
    Le Floch JP, Le Lievre G, Labroue M, Peynegre R, Perlemuter L. Early detection of diabetic patients at risk of developing degenerative complications using electric gustometry: a five-year follow-up study. Eur J Med. 1992;1:208–14.PubMedGoogle Scholar
  49. 49.
    Abbasi AA. Diabetes: diagnostic and therapeutic significance of taste impairment. Geriatrics. 1981;36:73–4. 77-8.PubMedGoogle Scholar
  50. 50.
    Perros P, Macfarlane TW, Counsell C, Frier BM. Altered taste sensation in newly-diagnosed NIDDM. Diabetes Care. 1996;19:768–70. doi: 10.2337/diacare.19.7.768.CrossRefPubMedGoogle Scholar
  51. 51.
    Stolbova K, Hahn A, Benes B, Andel M, Treslova L. Gustometry of diabetes mellitus patients and obese patients. Int Tinnitus J. 1999;5:135–40.PubMedGoogle Scholar
  52. 52.
    Fomina EI, Pozharitskaia MM, Davydov AL, Starosel’tseva LK, Budylina SM, Simakova TG. Changes of gustatory perception in elderly patients with type II sugar diabetes. Surgical section. [Russian]. Stomatologiia (Mosk). 2007;86:30–4.Google Scholar
  53. 53.
    Casamassimo PS, Tucker-Lammertse JE. Diabetic polyradiculopathy with trigeminal nerve involvement; a case report. Oral Surg Oral Med Oral Pathol. 1988;66:315–7.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Wenche S. Borgnakke
    • 4
    Email author
  • Patricia F. Anderson
    • 1
  • Carol Shannon
    • 2
  • Anca Jivanescu
    • 3
  1. 1.Emerging Technologies Informationist, Taubman Health Sciences LibraryUniversity of MichiganAnn ArborUSA
  2. 2.Informationist, Academic & Clinical Engagement, Taubman Health Sciences LibraryUniversity of MichiganAnn ArborUSA
  3. 3.Department of Prosthodontics, Faculty of DentistryUniversity of Medicine and Pharmacy “Victor Babes” TimisoaraTimisoaraRomania
  4. 4.Department of Periodontics and Oral MedicineUniversity of Michigan School of DentistryAnn ArborUSA

Personalised recommendations