Skip to main content

Advertisement

SpringerLink
Log in

Primary versus post-treatment apical periodontitis: microbial composition, lipopolysaccharides and lipoteichoic acid levels, signs and symptoms

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

To compare the microbial load and composition and to determine the lipopolysaccharides (LPS) and lipoteichoic acid (LTA) concentrations found in primary apical periodontitis (PAP) and post-treatment apical periodontitis (PTAP), correlating these findings with clinical/tomographic features.

Material and methods

Sixty patients with PAP (31) and PTAP (29) were submitted to clinical and tomographic assessment. Samples were collected from each root canal using paper points for microbiological assessment (culture technique and Checkerboard DNA-DNA hybridization) and determination of LPS and LTA levels (limulus amebocyte lysate and enzyme-linked immunosorbent assays, respectively). Data were correlated with clinical/tomographic findings and statistically analyzed using the Mann-Whitney and Pearson correlation tests (α = 5%).

Results

A higher number of cultivable bacteria and LPS were found in PAP (p < 0.05). The median number of species per root canal found in PAP and PTAP was 9 and 22, respectively (p < 0.05). LPS was positively correlated with a larger periapical lesion volume (p < .05). LTA levels were similar in both infections and had no correlation with signs and symptoms. In PAP, gram-positive bacteria were correlated with spontaneous pain (p < .05) and exudate (p < .05). Tenderness to percussion and pain on palpation were correlated to the presence of both gram-positive and negative bacteria. In PTAP, a positive correlation was observed between both gram-positive and gram-negative bacteria with exudate and periapical lesion volume (p < .05).

Conclusions

PAP had higher contents of microbial load and LPS compared with PTAP. However, PTAP presented a more diverse microbiota compared with PAP. Higher content of LPS was positively correlated with larger periapical bone destruction, whereas signs and symptoms with specific microorganisms.

Clinical relevance

It was verified that PAP and PTAP are polymicrobial infections with predominance of gram-negative bacteria and a more diverse bacterial population found in PTAP. A wide interaction of specific microbial species resulted in different clinical features in both infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Francisco PA, Delboni MG, Lima AR, Xiao Y, Siqueira WL, Gomes BPFA (2018) Proteomic profile of root canal contents in teeth with post-treatment endodontic disease. Int Endod J. https://doi.org/10.1111/iej.13021

  2. Cavalli D, Toia CC, Flores Orozco EI, Khoury RD, Cardoso FG d R, Alves MC, CAT C, Valera MC (2017) Effectiveness in the removal of endotoxins and microbiological profile in primary endodontic infections using 3 different instrumentation systems: a randomized clinical study. J Endod 43:1237–1245. https://doi.org/10.1016/j.joen.2017.03.032

    Article  PubMed  Google Scholar 

  3. Chugal NM, Clive JM, Spångberg LSW (2001) A prognostic model for assessment of the outcome of endodontic treatment: effect of biologic and diagnostic variables. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 91:342–352. https://doi.org/10.1067/moe.2001.113106

    Article  PubMed  Google Scholar 

  4. Chávez de Paz LE, Bergenholtz G, Svensäter G (2010) The effects of antimicrobials on endodontic biofilm bacteria. J Endod 36:70–77. https://doi.org/10.1016/j.joen.2009.09.017

    Article  PubMed  Google Scholar 

  5. Ng Y-L, Mann V, Gulabivala K (2011) A prospective study of the factors affecting outcomes of nonsurgical root canal treatment: part 1: periapical health. Int Endod J 44:583–609. https://doi.org/10.1111/j.1365-2591.2011.01872.x

    Article  PubMed  Google Scholar 

  6. Gomes BPFA, Pinheiro ET, Gadê-Neto CR, Sousa ELR, Ferraz CCR, Zaia AA, Teixeira FB, Souza-Filho FJ (2004) Microbiological examination of infected dental root canals. Oral Microbiol Immunol 19:71–76

    Article  Google Scholar 

  7. Siqueira JF Jr, Rôças IN (2007) Bacterial pathogenesis and mediators in apical periodontitis. Braz Dent J 18:267–280. https://doi.org/10.1590/S0103-64402007000400001

    Article  PubMed  Google Scholar 

  8. Rietschel ET, Brade H (1992) Bacterial endotoxins. Sci Am 267:54–61

    Article  Google Scholar 

  9. Martinho FC, Chiesa WMM, Leite FRM, Cirelli JA, Gomes BPFA (2011) Antigenicity of primary endodontic infection against macrophages by the levels of PGE(2) production. J Endod 37:602–607. https://doi.org/10.1016/j.joen.2010.12.005

    Article  PubMed  Google Scholar 

  10. Cardoso FGR, Ferreira NS, Martinho FC, Nascimento GG, Manhães LRC, Rocco MA, Carvalho CAT, Valera MC (2015) Correlation between volume of apical periodontitis determined by cone-beam computed tomography analysis and endotoxin levels found in primary root canal infection. J Endod 41:1015–1019. https://doi.org/10.1016/j.joen.2015.02.005

    Article  PubMed  Google Scholar 

  11. Morath S, Geyer A, Spreitzer I, Hermann C, Hartung T (2002) Structural decomposition and heterogeneity of commercial lipoteichoic acid preparations. Infect Immun 70:938–944

    Article  Google Scholar 

  12. Gao JJ, Xue Q, Zuvanich EG, Haghi KR, Morrison DC (2001) Commercial preparations of lipoteichoic acid contain endotoxin that contributes to activation of mouse macrophages in vitro. Infect Immun 69:751–757. https://doi.org/10.1128/IAI.69.2.751-757.2001

    Article  PubMed  PubMed Central  Google Scholar 

  13. Speers AM, Cologgi DL, Reguera G (2009) Anaerobic cell culture. In: Current protocols in microbiology. Wiley, Hoboken, p appendix 4F

    Google Scholar 

  14. Petti CA, Polage CR, Schreckenberger P (2005) The role of 16S rRNA gene sequencing in identification of microorganisms misidentified by conventional methods. J Clin Microbiol 43:6123–6125. https://doi.org/10.1128/JCM.43.12.6123-6125.2005

    Article  PubMed  PubMed Central  Google Scholar 

  15. Ferreira NS, Martinho FC, Cardoso FGR, Nascimento GG, Carvalho CAT, Valera MC (2015) Microbiological profile resistant to different intracanal medications in primary endodontic infections. J Endod 41:824–830. https://doi.org/10.1016/j.joen.2015.01.031

    Article  PubMed  Google Scholar 

  16. Möller AJ (1966) Microbiological examination of root canals and periapical tissues of human teeth. Methodological studies. Odontol Tidskr 74(Suppl):1–380

    Google Scholar 

  17. Socransky SS, Haffajee AD, Smith C, Martin L, Haffajee JA, Uzel NG, Goodson JM (2004) Use of checkerboard DNA-DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 19:352–362. https://doi.org/10.1111/j.1399-302x.2004.00168.x

    Article  PubMed  Google Scholar 

  18. Blome B, Braun A, Sobarzo V, Jepsen S (2008) Molecular identification and quantification of bacteria from endodontic infections using real-time polymerase chain reaction. Oral Microbiol Immunol 23:384–390. https://doi.org/10.1111/j.1399-302X.2008.00440.x

    Article  PubMed  Google Scholar 

  19. Cogulu D, Uzel A, Oncag O, Aksoy SC, Eronat C (2007) Detection of enterococcus faecalis in necrotic teeth root canals by culture and polymerase chain reaction methods. Eur J Dent 1:216–221

    Article  Google Scholar 

  20. Schirrmeister JF, Liebenow A-L, Braun G, Wittmer A, Hellwig E, Al-Ahmad A (2007) Detection and eradication of microorganisms in root-filled teeth associated with periradicular lesions: an in vivo study. J Endod 33:536–540. https://doi.org/10.1016/j.joen.2007.01.012

    Article  PubMed  Google Scholar 

  21. Schirrmeister JF, Liebenow A-L, Pelz K, Wittmer A, Serr A, Hellwig E, Al-Ahmad A (2009) New bacterial compositions in root-filled teeth with periradicular lesions. J Endod 35:169–174. https://doi.org/10.1016/j.joen.2008.10.024

    Article  PubMed  Google Scholar 

  22. Akpata ES (1976) Effect of endodontic procedures on the population of viable microorganisms in the infected root canal. J Endod 2:369–373. https://doi.org/10.1016/S0099-2399(76)80099-4

    Article  PubMed  Google Scholar 

  23. Sathorn C, Parashos P, Messer H (2007) How useful is root canal culturing in predicting treatment outcome? J Endod 33:220–225. https://doi.org/10.1016/j.joen.2006.11.006

    Article  PubMed  Google Scholar 

  24. Gomes BP, Drucker DB, Lilley JD (1994) Associations of specific bacteria with some endodontic signs and symptoms. Int Endod J 27:291–298

    Article  Google Scholar 

  25. Ahn SH, Song J-E, Kim S, Cho S-H, Lim YK, Kook J-K, Kook M-S, Lee T-H (2016) NOX1/2 activation in human gingival fibroblasts by Fusobacterium nucleatum facilitates attachment of Porphyromonas gingivalis. Arch Microbiol 198:573–583. https://doi.org/10.1007/s00203-016-1223-7

    Article  PubMed  Google Scholar 

  26. Enersen M, Nakano K, Amano A (2013) Porphyromonas gingivalis fimbriae. J Oral Microbiol 5:20265. https://doi.org/10.3402/jom.v5i0.20265

    Article  Google Scholar 

  27. Li X, Kolltveit KM, Tronstad L, Olsen I (2000) Systemic diseases caused by oral infection. Clin Microbiol Rev 13:547–558

    Article  Google Scholar 

  28. Stuart C, Schwartz S, Beeson T, Owatz C (2006) Enterococcus faecalis: its role in root canal treatment failure and current concepts in retreatment. J Endod 32:93–98. https://doi.org/10.1016/j.joen.2005.10.049

    Article  PubMed  Google Scholar 

  29. Zoletti GO, Pereira EM, Schuenck RP, Teixeira LM, Siqueira JF, dos Santos KRN (2011) Characterization of virulence factors and clonal diversity of Enterococcus faecalis isolates from treated dental root canals. Res Microbiol 162:151–158. https://doi.org/10.1016/j.resmic.2010.09.018

    Article  PubMed  Google Scholar 

  30. Gomes BPFA, Pinheiro ET, Jacinto RC, Zaia AA, Ferraz CCR, Souza-Filho FJ (2008) Microbial analysis of canals of root-filled teeth with periapical lesions using polymerase chain reaction. J Endod 34:537–540. https://doi.org/10.1016/j.joen.2008.01.016

    Article  PubMed  Google Scholar 

  31. Gomes BPFA, Pinheiro ET, Sousa ELR, Jacinto RC, Zaia AA, Ferraz CCR, de Souza-Filho FJ (2006) Enterococcus faecalis in dental root canals detected by culture and by polymerase chain reaction analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102:247–253. https://doi.org/10.1016/j.tripleo.2005.11.031

    Article  PubMed  Google Scholar 

  32. Pourhajibagher M, Bahador A (2018) Diagnostic accuracy of multiplex real-time PCR approaches compared with cultivation -based detection methods: monitoring the endopathogenic microbiota pre and post photo-activated disinfection. Photodiagn Photodyn Ther 22:140–146. https://doi.org/10.1016/j.pdpdt.2018.03.003

    Article  Google Scholar 

  33. Sjogren U, Hagglund B, Sundqvist G, Wing K (1990) Factors affecting the long-term results of endodontic treatment. J Endod 16:498–504. https://doi.org/10.1016/S0099-2399(07)80180-4

    Article  PubMed  Google Scholar 

  34. Pratt I, Aminoshariae A, Montagnese TA, Williams KA, Khalighinejad N, Mickel A (2016) Eight-year retrospective study of the critical time lapse between root canal completion and crown placement: its influence on the survival of endodontically treated teeth. J Endod 42:1598–1603. https://doi.org/10.1016/j.joen.2016.08.006

    Article  PubMed  Google Scholar 

  35. Pai SF, Yang SF, Sue WL, Chueh LH, Rivera EM (1999) Microleakage between endodontic temporary restorative materials placed at different times. J Endod 25:453–456. https://doi.org/10.1016/S0099-2399(99)80278-7

    Article  PubMed  Google Scholar 

  36. Tennert C, Eismann M, Goetz F, Woelber JP, Hellwig E, Polydorou O (2015) A temporary filling material used for coronal sealing during endodontic treatment may cause tooth fractures in large class II cavities in vitro. Int Endod J 48:84–88. https://doi.org/10.1111/iej.12280

    Article  PubMed  Google Scholar 

  37. Siqueira JF, Rôças IN, Souto R, de Uzeda M, Colombo AP (2000) Checkerboard DNA-DNA hybridization analysis of endodontic infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 89:744–748

    Article  Google Scholar 

  38. Baumgartner JC (2004) Microbiological and molecular analysis of endodontic infections. Endod Top 7:35–51. https://doi.org/10.1111/j.1601-1546.2004.00061.x

    Article  Google Scholar 

  39. Anderson AC, Hellwig E, Vespermann R, Wittmer A, Schmid M, Karygianni L, Al-Ahmad A (2012) Comprehensive analysis of secondary dental root canal infections: a combination of culture and culture-independent approaches reveals new insights. PLoS One 7:e49576. https://doi.org/10.1371/journal.pone.0049576

    Article  PubMed  PubMed Central  Google Scholar 

  40. Baumgartner J, Siqueira JRJ, Xia T, Roças I (2004) Geographical differences in bacteria detected in endodontic infections using polymerase chain reaction. J Endod 30:141–144. https://doi.org/10.1097/00004770-200403000-00004

    Article  PubMed  Google Scholar 

  41. Harbarth S, Samore MH (2005) Antimicrobial resistance determinants and future control. Emerg Infect Dis 11:794–801. https://doi.org/10.3201/eid1106.050167

    Article  PubMed  PubMed Central  Google Scholar 

  42. Gomes BPFA, Endo MS, Martinho FC (2012) Comparison of endotoxin levels found in primary and secondary endodontic infections. J Endod 38:1082–1086. https://doi.org/10.1016/j.joen.2012.04.021

    Article  PubMed  Google Scholar 

  43. Yang J, Park O-J, Kim J, Baik JE, Yun C-H, Han SH (2016) Lipoteichoic acid of Enterococcus faecalis inhibits the differentiation of macrophages into osteoclasts. J Endod 42:570–574. https://doi.org/10.1016/j.joen.2016.01.012

    Article  PubMed  Google Scholar 

  44. Mörmann M, Thederan M, Nackchbandi I, Giese T, Wagner C, Hänsch GM (2008) Lipopolysaccharides (LPS) induce the differentiation of human monocytes to osteoclasts in a tumour necrosis factor (TNF) α-dependent manner: a link between infection and pathological bone resorption. Mol Immunol 45:3330–3337. https://doi.org/10.1016/j.molimm.2008.04.022

    Article  PubMed  Google Scholar 

  45. Boyce BF, Xing L (2008) Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473:139–146. https://doi.org/10.1016/j.abb.2008.03.018

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The work was supported by the Programa Nacional de Cooperação Acadêmica da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES/Brasil and the Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP (grant numbers. 2015/05397-1 and 2018/01703-9).

Author information

Authors and Affiliations

  1. Department of Restorative Dentistry, Endodontic Division, Institute of Science and Technology, São Paulo State University (Unesp), São José dos Campos, Brazil

    Felipe Paiva Machado, Rayana Duarte Khoury, Cassia Cestari Toia, Esteban Isai Flores Orozco, Flávia Goulart da Rosa Cardoso & Marcia Carneiro Valera

  2. Department of Biosciences and Oral Diagnosis, Institute of Science and Technology, São Paulo State University (Unesp), São José dos Campos, Brazil

    Felipe Eduardo de Oliveira & Luciane Dias de Oliveira

Authors
  1. Felipe Paiva Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rayana Duarte Khoury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cassia Cestari Toia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esteban Isai Flores Orozco
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Felipe Eduardo de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luciane Dias de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Flávia Goulart da Rosa Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marcia Carneiro Valera
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcia Carneiro Valera.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the local Institute Review Board (São Paulo State University (Unesp), Institute of Science and Technology, São José dos Campos, Brazil) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Machado, F.P., Khoury, R.D., Toia, C.C. et al. Primary versus post-treatment apical periodontitis: microbial composition, lipopolysaccharides and lipoteichoic acid levels, signs and symptoms. Clin Oral Invest 24, 3169–3179 (2020). https://doi.org/10.1007/s00784-019-03191-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-019-03191-6

Keywords

Search

Navigation