Clinical Oral Investigations

, Volume 20, Issue 6, pp 1133–1141 | Cite as

Association between diabetes and the prevalence of radiolucent periapical lesions in root-filled teeth: systematic review and meta-analysis

  • Juan J. Segura-EgeaEmail author
  • Jenifer Martín-González
  • Daniel Cabanillas-Balsera
  • Ashraf F. Fouad
  • Eugenio Velasco-Ortega
  • José López-López



The question of whether diabetes mellitus can influence the outcome of root canal treatment (RCT) remains unclear. The aim of this systematic review and meta-analysis was to analyze scientific available evidence on the association between diabetes and the presence of radiolucent periapical lesions (RPLs) in root-filled teeth (RFT).


The review question was as follows: in adult patients who had endodontically treated teeth, does the absence or presence of diabetes result in an increase in the prevalence of RPL associated to RFT? A systematic MEDLINE/PubMed, Wiley Online Database, Web of Science, and Scopus search was conducted using the following MeSH and keywords: Diabetes Mellitus OR Diabetes OR Diabetic OR Hyperglycemia, AND Endodontics, Periapical Periodontitis, Periapical Diseases, Apical Periodontitis, Periradicular Lesion, Periapical Radiolucency, Radiolucent Periapical Lesion, Root Canal Treatment, Root Canal Preparation, Root Canal Therapy, Root Filled Teeth, Endodontically Treated Teeth. Seven studies reporting data on the prevalence of RPL associated to RFT both in diabetic and control subjects were included.


After the study selection, seven epidemiological studies fulfilled the inclusion criteria, representing data from 1593 root canal treatments, 1011 in non-diabetic control subjects, and 582 in diabetic patients. The calculated pooled odds ratio (OR = 1.42; 95 % CL = 1.11–1.80; p = 0.0058) indicates that diabetic patients have higher prevalence of RFT with RPLs than controls.


Available scientific evidence indicates that diabetes is significantly associated to higher prevalence of periapical radiolucencies in endodontically treated teeth, being an important putative pre-operative prognostic factor in RCT.

Clinical relevance

Taking into account that diabetes is the third most prevalent chronic medical condition among dental patients, endodontic providers should be aware of the relationship between the outcome of endodontic treatment and diabetes.


Diabetes mellitus Meta-analysis Periapical inflammation Persistent apical periodontitis Root canal treatment outcome Root-filled teeth 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


The work was supported by the Department of Stomatology, Endodontics Section, University of Sevilla, Seville, Spain.

Ethical approval

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

Informed consent

For this type of study, formal consent is not required.


  1. 1.
    Siqueira JRJF, Rôças IN (2014) Present status and future directions in endodontic microbiology. Endod Topics 30:3–22CrossRefGoogle Scholar
  2. 2.
    Bender IB, Seltzer S (2003) Roentgenographic and direct observation of experimental lesions in bone: I. 1961. J Endod 29:702–706CrossRefPubMedGoogle Scholar
  3. 3.
    Figdor D (2002) Apical periodontitis: a very prevalent problem. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94:651–652CrossRefPubMedGoogle Scholar
  4. 4.
    Buckley M, Spångberg LS (1995) The prevalence and technical quality of endodontic treatment in an American subpopulation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 79:92–100CrossRefPubMedGoogle Scholar
  5. 5.
    Chen CY, Hasselgren G, Serman N, Elkind MS, Desvarieux M, Engebretson SP (2007) Prevalence and quality of endodontic treatment in the Northern Manhattan elderly. J Endod 33:230–234CrossRefPubMedGoogle Scholar
  6. 6.
    Caplan DJ, Chasen JB, Krall EA, et al. (2006) Lesions of endodontic origin and risk of coronary heart disease. J Dent Res 85:996–1000CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Jiménez-Pinzón A, Segura-Egea JJ, Poyato M, Velasco E, Ríos JV (2004) Prevalence of apical periodontitis and frequency of root-filled teeth in an adult Spanish population. Int Endod J 37:167–173CrossRefPubMedGoogle Scholar
  8. 8.
    López-López J, Jané-Salas E, Estrugo-Devesa A, et al. (2012) Frequency and distribution of root filled teeth and apical periodontitis in an adult population of Barcelona, Spain. Int Dental J 62:40–46CrossRefGoogle Scholar
  9. 9.
    Eriksen HM (1998) Epidemiology of apical periodontitis. In: Ørstavik D, Pitt Ford TR (eds) Essential Endodontology. Prevention and treatment of apical periodontitis. Blackwell Science, London, pp. pp.179–pp.191Google Scholar
  10. 10.
    Ørstavik D, Pitt Ford T (2007) Apical periodontitis: microbial infection and host responses. In: Ørstavik D, Pitt Ford TR (eds) Essential Endodontology. Prevention and treatment of apical periodontitis, 2nd edn. Wiley-Blackwell, London, UK, pp. pp:179–pp:191Google Scholar
  11. 11.
    Winward BJ, Yaccino JM, Kirkpatrick TC (2014) A panoramic survey of air force basic trainees: how research translates into clinical practice. J Endod 40:1332–1337CrossRefPubMedGoogle Scholar
  12. 12.
    Sundqvist G, Figdor D (1998) Endodontic treatment of apical periodontitis. In: Ørstavik D, Pitt Ford TR (eds) Essential Endodontology. Blackwell, Oxford, pp. pp:242–pp:277Google Scholar
  13. 13.
    Nair PNR (2006) On the causes of persistent apical periodontitis: a review. Int Endod J 39:249–281CrossRefPubMedGoogle Scholar
  14. 14.
    Segura-Egea JJ, Martín-González J, Castellanos-Cosano L (2015) Endodontic medicine: connections between apical periodontitis and systemic diseases. Int Endod J 48:933–951CrossRefPubMedGoogle Scholar
  15. 15.
    Love RM, Firth N (2009) Histopathological profile of surgically removed persistent periapical radiolucent lesions of endodontic origin. Int Endod J 42:198–202CrossRefPubMedGoogle Scholar
  16. 16.
    Koivisto T, Bowles WR, Rohrer M (2012) Frequency and distribution of radiolucent jaw lesions: a retrospective analysis of 9723 cases. J Endod 38:729–732CrossRefPubMedGoogle Scholar
  17. 17.
    Ng YL, Mann V, Gulabivala K (2011) A prospective study of the factors affecting outcomes of non-surgical root canal treatment: part 2: tooth survival. Int Endod J 44:610–625CrossRefPubMedGoogle Scholar
  18. 18.
    Marending M, Peters OA, Zehnder M (2005) Factors affecting the outcome of orthograde root canal therapy in a general dentistry hospital practice. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 99:119–124CrossRefPubMedGoogle Scholar
  19. 19.
    Segura-Egea JJ, Castellanos-Cosano L, Machuca G, et al. (2012) Diabetes mellitus, periapical inflammation and endodontic treatment outcome. Med Oral Patol Oral Cir Bucal 17:e356–e361CrossRefPubMedGoogle Scholar
  20. 20.
    Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2000) Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 23(Suppl.1):S4–S19Google Scholar
  21. 21.
    Mealey BL, Oates TW (2006) American Academy of Periodontology. Diabetes mellitus and periodontal diseases. J Periodon 77:1289–1303CrossRefGoogle Scholar
  22. 22.
    Iacopino AM (2001) Periodontitis and diabetes interrelationships: role of inflammation. Ann Periodontol 6:125–137CrossRefPubMedGoogle Scholar
  23. 23.
    Fouad AF, Huang GT-J (2015) Chapter 9: inflammation and Immunological response, in Ingle’s Endodontics 7th Ed. Rotstein I. Editor (in press)Google Scholar
  24. 24.
    Delamaire M, Maugendre D, Moreno M, Le Goff MC, Allannic H, Genetet B (1997) Impaired leucocyte functions in diabetic patients. Diabetes Med 14:29–34CrossRefGoogle Scholar
  25. 25.
    Salvi GE, Carollo-Bittel B, Lang NP (2008) Effects of diabetes mellitus on periodontal and peri-implant conditions: update on associations and risks. J Clin Periodontol 35(8 Suppl):398–409CrossRefPubMedGoogle Scholar
  26. 26.
    Bender IB, Seltzer S, Freedland J (1963) The relationship of systemic diseases to endodontic failures and treatment procedures. Oral Surg Oral Med Oral Pathol 16:1102–1115CrossRefPubMedGoogle Scholar
  27. 27.
    Bender IB, Bender AB (2003) Diabetes mellitus and the dental pulp. J Endod 29:383–389CrossRefPubMedGoogle Scholar
  28. 28.
    Stroup DF, Berlin JA, Morton SC, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. J Am Med Assoc 283:2008–2012CrossRefGoogle Scholar
  29. 29.
    Bader JD (2004) Systematic reviews and their implications for dental practice. Tex Dent J 121:380–387PubMedGoogle Scholar
  30. 30.
    Pak JG, Fayazi S, White SN (2012) Prevalence of periapical radiolucency and root canal treatment: a systematic review of cross-sectional studies. J Endod 38:1170–1176CrossRefPubMedGoogle Scholar
  31. 31.
    Centre for Evidence Based Medicine (2005) Critical Appraisal for therapy articles. University of Oxford. Medical Sciences Division. Available at:
  32. 32.
    Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558CrossRefPubMedGoogle Scholar
  33. 33.
    L’Abbé KA, Detsky AS, O’Rourke K (1987) Meta-analysis in clinical research. Ann Intern Med 107:224–233CrossRefPubMedGoogle Scholar
  34. 34.
    Lewis S, Clarke M (2001) Forest plots: trying to see the woods and the trees. BMJ 322:479–480CrossRefGoogle Scholar
  35. 35.
    Freemantle N (2000) CD: StatsDirect—statistical software for medical research in the 21st century. Bmj 321(7275):1536.
  36. 36.
    Mohamed HG, Idris SB, Ahmed MF, et al. (2013) Association between oral health status and type 2 diabetes mellitus among Sudanese adults: a matched case-control study. PLoS One 12:e82158CrossRefGoogle Scholar
  37. 37.
    Lin PY, Huang SH, Chang HJ, Chi LY (2014) The effect of rubber dam usage on the survival rate of teeth receiving initial root canal treatment: a nationwide population-based study. J Endod 40:1733–1737CrossRefPubMedGoogle Scholar
  38. 38.
    Iqbal MK, Kim S (2008) A review of factors influencing treatment planning decisions of single-tooth implants versus preserving natural teeth with nonsurgical endodontic therapy. J Endod 34:519–529CrossRefPubMedGoogle Scholar
  39. 39.
    Ilgüy M, Ilgüy D, Bayirli G (2007) Dental lesions in adult diabetic patients. N Y State Dent J 73:58–60PubMedGoogle Scholar
  40. 40.
    Ueta E, Osaki T, Yoneda K, Yamamoto T (1993) Prevalence of diabetes mellitus in odontogenic infections and oral candidiasis: an analysis of neutrophil suppression. J Oral Pathol Med 22:168–174CrossRefPubMedGoogle Scholar
  41. 41.
    Doyle SL, Hodges JS, Pesun IJ, Baisden MK, Bowles WR (2007) Factors affecting outcomes for single-tooth implants and endodontic restorations. J Endod 33:399–402CrossRefPubMedGoogle Scholar
  42. 42.
    Wang CH, Chueh LH, Chen SC, Feng YC, Hsiao CK, Chiang CP (2011) Impact of diabetes mellitus, hypertension, and coronary artery disease on tooth extraction after nonsurgical endodontic treatment. J Endod 37:1–5CrossRefPubMedGoogle Scholar
  43. 43.
    Mindiola MJ, Mickel AK, Sami C, Jones JJ, Lalumandier JA, Nelson SS (2006) Endodontic treatment in an American Indian population: a 10-year retrospective study. J Endod 32:828–832CrossRefPubMedGoogle Scholar
  44. 44.
    Falk H, Hugoson A, Thorstensson H (1989) Number of teeth, prevalence of caries and periapical lesions in insulin-dependent diabetics. Scand J Dental Res 97:198–206Google Scholar
  45. 45.
    Fouad AF, Burleson J (2003) The effect of diabetes mellitus on endodontic treatment outcome: data from an electronic patient record. JADA 134:43–51PubMedGoogle Scholar
  46. 46.
    Britto LR, Katz J, Guelmann M, Heft M (2003) Periradicular radiographic assessment in diabetic and control individuals. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 96:449–452CrossRefPubMedGoogle Scholar
  47. 47.
    Segura-Egea JJ, Jiménez-Pinzón A, Ríos-Santos JV, Velasco-Ortega E, Cisneros-Cabello R, Poyato-Ferrera M (2005) High prevalence of apical periodontitis amongst type 2 diabetic patients. Int Endod J 38:564–569CrossRefPubMedGoogle Scholar
  48. 48.
    López-López J, Jané-Salas E, Estrugo-Devesa A, et al. (2011) Periapical and endodontic status of type 2 diabetic patients in Catalonia, Spain: a cross-sectional study. J Endod 37:598–601CrossRefPubMedGoogle Scholar
  49. 49.
    Marotta PS, Fontes TV, Armada L, Lima KC, Rôças IN, Siqueira JF Jr (2012) Type 2 diabetes mellitus and the prevalence of apical periodontitis and endodontic treatment in an adult Brazilian population. J Endod 38:297–300CrossRefPubMedGoogle Scholar
  50. 50.
    Marques-Ferreira M, Carrilho E, Carrilho F (2014) Diabetes mellitus and its influence on the success of endodontic treatment: a retrospective clinical study. Act Med Portuguesa 27:15–22CrossRefGoogle Scholar
  51. 51.
    Strindberg LZ (1956) The dependence of the results of pulp therapy on certain factors. Acta Odontol Scand 14(suppl 21):1–75Google Scholar
  52. 52.
    Ørstavik D, Kerekes K, Eriksen HM (1986) The periapical index: a scoring system for radiographic assessment of apical periodontitis. Endod Dent Traumatol 2:20–34CrossRefPubMedGoogle Scholar
  53. 53.
    Kohsaka T, Kumazawa M, Yamasaki M, Nakamura H (1996) Periapical lesions in rats with streptozotocin-induced diabetes. J Endod 22:418–421CrossRefPubMedGoogle Scholar
  54. 54.
    Fouad A, Barry J, Russo J, Radolf J, Zhu Q (2002) Periapical lesion progression with controlled microbial inoculation in a type I diabetic mouse model. J Endod 28:8–16CrossRefPubMedGoogle Scholar
  55. 55.
    Bain JL, Lester SR, Henry WD, Naftel JP, Johnson RB (2009) Effects of induced periapical abscesses on rat pregnancy outcomes. Arch Oral Biol 54:162–171CrossRefPubMedGoogle Scholar
  56. 56.
    Kodama Y, Matsuura M, Sano T, et al. (2011) Diabetes enhances dental caries and apical periodontitis in caries-susceptible WBN/KobSlc rats. Comp Med 61:53–59PubMedPubMedCentralGoogle Scholar
  57. 57.
    Astolphi RD, Curbete MM, Colombo NH, et al. (2013) Periapical lesions decrease insulin signal and cause insulin resistance. J Endod 39:648–652CrossRefPubMedGoogle Scholar
  58. 58.
    Cintra LT, da Silva Facundo AC, Azuma MM, et al. (2013) Pulpal and periodontal diseases increase triglyceride levels in diabetic rats. Clin Oral Invest 17:1595–1599CrossRefGoogle Scholar
  59. 59.
    Cintra LT, da Silva Facundo AC, Prieto AK, et al. (2014) Blood profile and histology in oral infections associated with diabetes. J Endod 40:1139–1144CrossRefPubMedGoogle Scholar
  60. 60.
    Pereira RF, de Oliveira da Mota MS, de Lima Coutinho Mattera MS, et al. (2015) Periapical lesions decrease Akt serine phosphorylation and plasma membrane GLUT4 content in rat skeletal muscle. Clin Oral Investig Nov 23. (Epub ahead of print)Google Scholar
  61. 61.
    Sánchez-Domínguez B, López-López J, Jané-Salas E, Castellanos-Cosano L, Velasco-Ortega E, Segura-Egea JJ (2015) Glycated haemoglobin levels and prevalence of apical periodontitis in type 2 diabetic patients. J Endod 41:601–606CrossRefPubMedGoogle Scholar
  62. 62.
    Patel S (2009) New dimensions in endodontic imaging: part 2. Cone beam computed tomography. Int Endod J 42:463–475CrossRefPubMedGoogle Scholar
  63. 63.
    Walter C, Rodriguez FR, Taner B, Hecker H, Weiger R (2012) Association of tobacco use and periapical pathosis – a systematic review. Int Endod J 45:1065–1073CrossRefPubMedGoogle Scholar
  64. 64.
    Garber SE, Shabahang S, Escher AP, Torabinejad M (2009) The effect of hyperglycemia on pulpal healing in rats. J Endod 35:60–62CrossRefPubMedGoogle Scholar
  65. 65.
    Gurav AN (2013) Advanced glycation end products: a link between periodontitis and diabetes mellitus? Curr Diabetes Rev 9:355–361CrossRefPubMedGoogle Scholar
  66. 66.
    Dhanuthai K, Sappayatosok K, Bijaphala P, Kulvitit S, Sereerat T (2009) Prevalence of medically compromised conditions in dental patients. Med Oral Patol Oral Cir Bucal 14:e287–e291PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Endodontic Section, Department of Stomatology, School of DentistryUniversity of SevillaSevilleSpain
  2. 2.Facultad de OdontologíaUniversidad de SevillaSevilleSpain
  3. 3.Department of EndodonticsUniversity of North CarolinaChapel HillUSA
  4. 4.Comprehensive Dentistry, Department of Stomatology, School of DentistryUniversity of SevillaSevilleSpain
  5. 5.Oral Medicine, Department of Odontostomatology, School of DentistryUniversity of BarcelonaBarcelonaSpain

Personalised recommendations