Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology

Gomes, Brenda Paula Figueiredo de Almeida; Herrera, Daniel Rodrigo

doi:10.1590/1807-3107bor-2018.vol32.0069

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Critical Review, Endodontic Therapy • Braz. oral. res. 32 (suppl 1) • 2018 • https://doi.org/10.1590/1807-3107bor-2018.vol32.0069 copy

Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract:

Evidence shows the polymicrobial etiology of endodontic infections, in which bacteria and their products are the main agents for the development, progression, and dissemination of apical periodontitis. Microbial factors in necrotic root canals (e.g., endotoxin) may spread into apical tissue, evoking and supporting a chronic inflammatory load. Thus, apical periodontitis is the result of the complex interplay between microbial factors and host defense against invasion of periradicular tissues. This review of the literature aims to discuss the complex network between endodontic infectious content and host immune response in apical periodontitis. A better understanding of the relationship of microbial factors with clinical symptomatology is important to establish appropriate therapeutic procedures for a more predictable outcome of endodontic treatment.

Keywords:
Periapical Periodontitis; Periapical Diseases; Lipopolysaccharides; Cytokines; Matrix Metalloproteinases

Bacteria morphology	Obligate anaerobes	Facultative anaerobes
Gram-positive cocci	Finegoldia	Enterococcus
	Parvimonas	Gemella
	Peptoniphilus	Staphylococcus
	Peptostreptococcus	Streptococcus ^* * Some species can also be strict anaerobes.
Gram-negative cocci	Veillonella	Neisseria
Gram-positive rods	Actinomyces
	Eggertella
	Eubacterium	Actinomyces ^* * Some species can also be strict anaerobes.
	Filifactor	Corynebacterium
	Lactobacillus	Lactobacillus ^* * Some species can also be strict anaerobes.
	Olsenella	Propionibacterium ^* * Some species can also be strict anaerobes.
	Propionibacterium
	Pseudoramibacter
Gram-negative rods	Alloprevotella
	Bacteroides
	Camphylobacter
	Dialister	Capnocytophaga
	Fretibacterium	Eikenella
	Fusobacterium	Haemophilus
	Porphyromonas
	Prevotella
	Tannerella
	Treponema

Firmicutes	Actinobacteria	Fusobacteria	Proteobacteria	Spirochaetes	Bacteroidetes	Synergistetes
Dialister pneumosintes	Actinomyces gerencseriae	Fusobacterium necrophorum	Campylobacter gracilis	Treponema amylovorum	Alloprevotella tannerae
Dialister invisus	Actinomyces israelii	Fusobacterium nucleatum ssp nucleatum	Campylobacter rectus	Treponema. denticola	Porphyromonas endodontalis	Pyramidobacter piscolens
Eggerthella lenta	Actinomyces naeslundii	Fusobacterium nucleatum ssp polymorphum	Eikenella corrodens	Treponema lecithinolyticum	Porphyromonas gingivalis
Enterococcus. faecalis	Actinomyces odontolyticus		Haemophilus aphrophilus	Treponema maltophilum	Prevotella denticola
Filifactor alocis	Actinomyces viscosus			Treponema medium	Prevotella intermedia
Finegoldia magna	Propionibacterium acnes			Treponema pectinovorum	Prevotella melaninogenica
Parvimonas micra	Propionibacterium propionicum			Treponema socranskii	Prevotella nigrescens
Peptoniphilus asaccharolyticus	Slackia exigua			Treponema vincentii	Tannerella forsythia
Peptostreptococcus anaerobius
Pseudoramibacter alactolyticus
Selenomonas sputigena
Streptococcus anginosus
Streptococcus constellatus
Streptococcus intermedius
Streptococcus mitis
Streptococcus sanguis
Veillonella parvulla

Author	Pulpal / Periodontal tissue status	LAL Method	Endotoxin concentration
Schein and Schilder (1975)¹³13. Schein B, Schilder H. Endotoxin content in endodontically involved teeth. J Endod. 1975 Jan;1(1):19-21. https://doi.org/10.1016/S0099-2399(75)80244-5 PMID:1061764 https://doi.org/10.1016/S0099-2399(75)80...	Vital pulp / healthy periodontium	Gel clot	0.007 µg/mL
	Irreversible pulpitis / healthy periodontium	Gel clot	0.075 µg/mL
Schein and Schilder (1975)¹³13. Schein B, Schilder H. Endotoxin content in endodontically involved teeth. J Endod. 1975 Jan;1(1):19-21. https://doi.org/10.1016/S0099-2399(75)80244-5 PMID:1061764 https://doi.org/10.1016/S0099-2399(75)80...	Pulp necrosis / apical periodontitis	Gel clot	0.192 µg/mL
Jacinto et al. (2005)¹⁵15. Jacinto RC, Gomes BP, Shah HN, Ferraz CC, Zaia AA, Souza-Filho FJ. Quantification of endotoxins in necrotic root canals from symptomatic and asymptomatic teeth. J Med Microbiol. 2005 Aug;54(Pt 8):777-83. https://doi.org/10.1099/jmm.0.45976-0 https://doi.org/10.1099/jmm.0.45976-0...		QCL	18016.50 EU/mL
Vianna et al. (2007)¹³³133. Vianna ME, Horz HP, Conrads G, Zaia AA, Souza-Filho FJ, Gomes BP. Effect of root canal procedures on endotoxins and endodontic pathogens. Oral Microbiol Immunol. 2007 Dec;22(6):411-8. https://doi.org/10.1111/j.1399-302X.2007.00379.x https://doi.org/10.1111/j.1399-302X.2007...		QCL	151.61 EU/mL
Martinho and Gomes (2008)¹⁶16. Martinho FC, Gomes BP. Quantification of endotoxins and cultivable bacteria in root canal infection before and after chemomechanical preparation with 2.5% sodium hypochlorite. J Endod. 2008 Mar;34(3):268-72. https://doi.org/10.1016/j.joen.2007.11.015 https://doi.org/10.1016/j.joen.2007.11.0...		QCL	323.27 EU/mL
Gomes et al. 2009⁽¹¹³113. Gomes BP, Martinho FC, Vianna ME. Comparison of 2.5% sodium hypochlorite and 2% chlorhexidine gel on oral bacterial lipopolysaccharide reduction from primarily infected root canals. J Endod. 2009 Oct;35(10):1350-3. https://doi.org/10.1016/j.joen.2009.06.011 https://doi.org/10.1016/j.joen.2009.06.0... ⁾		QCL	212.23 EU/mL
Martinho et al. (2010a)¹¹11. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenic activity of bacterial endodontic contents from primary root canal infection with periapical lesions against macrophage in the release of interleukin-1beta and tumor necrosis factor alpha. J Endod. 2010a Sep;36(9):1467-74. https://doi.org/10.1016/j.joen.2010.06.012 https://doi.org/10.1016/j.joen.2010.06.0...		TKA	9.19 EU/mL
Martinho et al. (2010b),¹³⁴134. Martinho FC, Chiesa WM, Marinho AC, Zaia AA, Ferraz CC, Almeida JF et al. Clinical investigation of the efficacy of chemomechanical preparation with rotary nickel-titanium files for removal of endotoxin from primarily infected root canals. J Endod. 2010b Nov;36(11):1766-9. https://doi.org/10.1016/j.joen.2010.08.019 https://doi.org/10.1016/j.joen.2010.08.0... (2012),¹⁷17. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Correlation between clinical/radiographic features and inflammatory cytokine networks produced by macrophages stimulated with endodontic content. J Endod. 2012 Jun;38(6):740-5. https://doi.org/10.1016/j.joen.2012.02.021 https://doi.org/10.1016/j.joen.2012.02.0... (2014)²⁵25. Martinho FC, Leite FR, Nascimento GG, Cirelli JA, Gomes BP. Clinical investigation of bacterial species and endotoxin in endodontic infection and evaluation of root canal content activity against macrophages by cytokine production. Clin Oral Investig. 2014 Dec;18(9):2095-102. https://doi.org/10.1007/s00784-014-1198-1 https://doi.org/10.1007/s00784-014-1198-...		TKA	7490.00 pg/mL
Martinho et al. (2011b)¹⁴¹141. Martinho FC, Chiesa WM, Zaia AA, Ferraz CC, Almeida JF, Souza-Filho FJ et al. Comparison of endotoxin levels in previous studies on primary endodontic infections. J Endod. 2011b Feb;37(2):163-7. https://doi.org/10.1016/j.joen.2010.11.020 https://doi.org/10.1016/j.joen.2010.11.0...		QCL	34.20 EU/mL
Martinho et al. (2011b)¹⁴¹141. Martinho FC, Chiesa WM, Zaia AA, Ferraz CC, Almeida JF, Souza-Filho FJ et al. Comparison of endotoxin levels in previous studies on primary endodontic infections. J Endod. 2011b Feb;37(2):163-7. https://doi.org/10.1016/j.joen.2010.11.020 https://doi.org/10.1016/j.joen.2010.11.0...		KQCL	7.49 EU/mL
Martinho et al. (2011b)¹⁴¹141. Martinho FC, Chiesa WM, Zaia AA, Ferraz CC, Almeida JF, Souza-Filho FJ et al. Comparison of endotoxin levels in previous studies on primary endodontic infections. J Endod. 2011b Feb;37(2):163-7. https://doi.org/10.1016/j.joen.2010.11.020 https://doi.org/10.1016/j.joen.2010.11.0...		TKA	9.19 EU/mL
Oliveira et al. (2011)¹³⁵135. Oliveira LD, Carvalho CA, Carvalho AS, Alves JS, Valera MC, Jorge AO. Efficacy of endodontic treatment for endotoxin reduction in primarily infected root canals and evaluation of cytotoxic effects. J Endod. 2012 Aug;38(8):1053-7. https://doi.org/10.1016/j.joen.2012.04.015 https://doi.org/10.1016/j.joen.2012.04.0...		KQCL	192.37 EU/mL
Gomes et al. (2012)²⁰20. Gomes BP, Endo MS, Martinho FC. Comparison of endotoxin levels found in primary and secondary endodontic infections. J Endod. 2012 Aug;38(8):1082-6. https://doi.org/10.1016/j.joen.2012.04.021 https://doi.org/10.1016/j.joen.2012.04.0...		TKA	7.49 EU/mL
Xavier et al. (2013)¹³⁶136. Xavier AC, Martinho FC, Chung A, Oliveira LD, Jorge AO, Valera MC et al. One-visit versus two-visit root canal treatment: effectiveness in the removal of endotoxins and cultivable bacteria. J Endod. 2013 Aug;39(8):959-64. https://doi.org/10.1016/j.joen.2013.04.027 https://doi.org/10.1016/j.joen.2013.04.0...		KQCL	153.13 EU/mL
Marinho et al. (2014)¹³⁷137. Marinho AC, Martinho FC, Zaia AA, Ferraz CC, Gomes BP. Monitoring the effectiveness of root canal procedures on endotoxin levels found in teeth with chronic apical periodontitis. J Appl Oral Sci. 2014 Nov-Dec;22(6):490-5. https://doi.org/10.1590/1678-775720130664 https://doi.org/10.1590/1678-77572013066...		TKA	18.70 EU/mL
Marinho et al. (2015)²⁹29. Marinho AC, Martinho FC, Leite FR, Nascimento GG, Gomes BP. Proinflammatory activity of primarily infected endodontic content against macrophages after different phases of the root canal therapy. J Endod. 2015 Jun;41(6):817-23. https://doi.org/10.1016/j.joen.2015.01.017 https://doi.org/10.1016/j.joen.2015.01.0...		TKA	32.43 EU/mL
Herrera et al. (2015)³⁰30. Herrera DR, Silva EJ, Santos CC, Zaia AA, Ferraz CC, Almeida JF, et al. Root canal content from primary endodontic infection and upregulation of gelatinases in fibroblast cells. Int Endod J. 2015 Dec;48(12):1168-74. https://doi.org/10.1111/iej.12421 https://doi.org/10.1111/iej.12421...		TKA	21.83 EU/mL
Cardoso et al. (2015)¹³¹131. Cardoso FG, Ferreira NS, Martinho FC, Nascimento GG, Manhães Junior LR, Rocco MA et al. Correlation between volume of apical periodontitis determined by cone-beam computed tomography analysis and endotoxin levels found in primary root canal infection. J Endod. 2015 Jul;41(7):1015-9. https://doi.org/10.1016/j.joen.2015.02.005 https://doi.org/10.1016/j.joen.2015.02.0...		KQCL	10.92 EU/mL
Herrera et al. (2017)¹³⁹139. Herrera DR, Martinho FC, de-Jesus-Soares A, Zaia AA, Ferraz CC, Almeida JF et al. Clinical efficacy of EDTA ultrasonic activation in the reduction of endotoxins and cultivable bacteria. Int Endod J. 2017 Oct;50(10):933-40. https://doi.org/10.1111/iej.12713 https://doi.org/10.1111/iej.12713...		TKA	27.72 EU/mL
Endo et al. (2012),¹⁹19. Endo MS, Martinho FC, Zaia AA, Ferraz CC, Almeida JF, Gomes BP. Quantification of cultivable bacteria and endotoxin in post-treatment apical periodontitis before and after chemo-mechanical preparation. Eur J Clin Microbiol Infect Dis. 2012 Oct;31(10):2575-83. https://doi.org/10.1007/s10096-012-1598-6 https://doi.org/10.1007/s10096-012-1598-... Gomes et al. (2012)²⁰20. Gomes BP, Endo MS, Martinho FC. Comparison of endotoxin levels found in primary and secondary endodontic infections. J Endod. 2012 Aug;38(8):1082-6. https://doi.org/10.1016/j.joen.2012.04.021 https://doi.org/10.1016/j.joen.2012.04.0...	Previous root canal treatment / apical periodontitis	TKA	3.96 EU/mL
Duque et al. (2018)¹⁴⁰140. Duque TM, Prado M, Herrera DR, Gomes BP. Periodontal and endodontic infectious/inflammatory profile in primary periodontal lesions with secondary endodontic involvement after a calcium hydroxide-based intracanal medication. Clin Oral Investig. 2018 Mar. https://doi.org/10.1007/s00784-018-2401-6 https://doi.org/10.1007/s00784-018-2401-...	Vital pulp / chronic periodontal disease	TKA	0.10 EU/mL

Author	Biomarker	Primary function	Significant association with clinical features
Author	Biomarker	Primary function	POP	TTP	EX	> SRL
Martinho et al. (2010a),¹¹11. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenic activity of bacterial endodontic contents from primary root canal infection with periapical lesions against macrophage in the release of interleukin-1beta and tumor necrosis factor alpha. J Endod. 2010a Sep;36(9):1467-74. https://doi.org/10.1016/j.joen.2010.06.012 https://doi.org/10.1016/j.joen.2010.06.0... (2014),²⁵25. Martinho FC, Leite FR, Nascimento GG, Cirelli JA, Gomes BP. Clinical investigation of bacterial species and endotoxin in endodontic infection and evaluation of root canal content activity against macrophages by cytokine production. Clin Oral Investig. 2014 Dec;18(9):2095-102. https://doi.org/10.1007/s00784-014-1198-1 https://doi.org/10.1007/s00784-014-1198-... Cardoso et al. (2016)¹³²132. Cardoso FG, Chung A, Martinho FC, Camargo CH, Carvalho CA, Gomes BP et al. Investigation of bacterial contents from persistent endodontic infection and evaluation of their inflammatory potential. Braz Dent J. 2016 Jul-Aug;27(4):412-8. https://doi.org/10.1590/0103-6440201600520 https://doi.org/10.1590/0103-64402016005...	IL-1β	Expression of adhesion factors, diapedesis, fever	+	+	+	+
Martinho et al. (2012)¹⁷17. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Correlation between clinical/radiographic features and inflammatory cytokine networks produced by macrophages stimulated with endodontic content. J Endod. 2012 Jun;38(6):740-5. https://doi.org/10.1016/j.joen.2012.02.021 https://doi.org/10.1016/j.joen.2012.02.0...	IL-6	Acute phase response, fever				+
Martinho et al. (2010a),¹¹11. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenic activity of bacterial endodontic contents from primary root canal infection with periapical lesions against macrophage in the release of interleukin-1beta and tumor necrosis factor alpha. J Endod. 2010a Sep;36(9):1467-74. https://doi.org/10.1016/j.joen.2010.06.012 https://doi.org/10.1016/j.joen.2010.06.0... (2012),¹⁷17. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Correlation between clinical/radiographic features and inflammatory cytokine networks produced by macrophages stimulated with endodontic content. J Endod. 2012 Jun;38(6):740-5. https://doi.org/10.1016/j.joen.2012.02.021 https://doi.org/10.1016/j.joen.2012.02.0... (2014),²⁵25. Martinho FC, Leite FR, Nascimento GG, Cirelli JA, Gomes BP. Clinical investigation of bacterial species and endotoxin in endodontic infection and evaluation of root canal content activity against macrophages by cytokine production. Clin Oral Investig. 2014 Dec;18(9):2095-102. https://doi.org/10.1007/s00784-014-1198-1 https://doi.org/10.1007/s00784-014-1198-... Cardoso et al. (2016)¹³²132. Cardoso FG, Chung A, Martinho FC, Camargo CH, Carvalho CA, Gomes BP et al. Investigation of bacterial contents from persistent endodontic infection and evaluation of their inflammatory potential. Braz Dent J. 2016 Jul-Aug;27(4):412-8. https://doi.org/10.1590/0103-6440201600520 https://doi.org/10.1590/0103-64402016005...	TNF-α	Cardinal signs of inflammation, fever	+	+	+	+
Martinho et al. (2011)¹²12. Martinho FC, Chiesa WM, Leite FR, Cirelli JA, Gomes BP. Antigenicity of primary endodontic infection against macrophages by the levels of PGE(2) production. J Endod. 2011a May;37(5):602-7. https://doi.org/10.1016/j.joen.2010.12.005 https://doi.org/10.1016/j.joen.2010.12.0...	PGE2	Vasodilatation, Collagen degradation		+	+
Shin et al. (2002),¹⁷⁰170. Shin SJ, Lee JI, Baek SH, Lim SS. Tissue levels of matrix metalloproteinases in pulps and periapical lesions. J Endod. 2002 Apr;28(4):313-5. https://doi.org/10.1097/00004770-200204000-00013 https://doi.org/10.1097/00004770-2002040... Martinho et al. (2016a)²⁷27. Martinho FC, Teixeira FF, Cardoso FG, Ferreira NS, Nascimento GG, Carvalho CA, et al. Clinical investigation of matrix metalloproteinases, tissue inhibitors of matrix metalloproteinases, and matrix metalloproteinase/tissue inhibitors of matrix metalloproteinase complexes and their networks in apical periodontitis. J Endod. 2016a Jul;42(7):1082-8. https://doi.org/10.1016/j.joen.2016.04.001 https://doi.org/10.1016/j.joen.2016.04.0...	MMP-1	Collagen degradation				+
Martinho et al. (2016a)²⁷27. Martinho FC, Teixeira FF, Cardoso FG, Ferreira NS, Nascimento GG, Carvalho CA, et al. Clinical investigation of matrix metalloproteinases, tissue inhibitors of matrix metalloproteinases, and matrix metalloproteinase/tissue inhibitors of matrix metalloproteinase complexes and their networks in apical periodontitis. J Endod. 2016a Jul;42(7):1082-8. https://doi.org/10.1016/j.joen.2016.04.001 https://doi.org/10.1016/j.joen.2016.04.0...	MMP-2	Collagen degradation		+		+
Martinho et al. (2016a)²⁷27. Martinho FC, Teixeira FF, Cardoso FG, Ferreira NS, Nascimento GG, Carvalho CA, et al. Clinical investigation of matrix metalloproteinases, tissue inhibitors of matrix metalloproteinases, and matrix metalloproteinase/tissue inhibitors of matrix metalloproteinase complexes and their networks in apical periodontitis. J Endod. 2016a Jul;42(7):1082-8. https://doi.org/10.1016/j.joen.2016.04.001 https://doi.org/10.1016/j.joen.2016.04.0...	MMP-9	Collagen degradation	+			+

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[1] Corresponding Author: Brenda Paula Figueiredo de Almeida Gomes, bpgomes@fop.unicamp.br