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The role of Enterococcus faecalis in apical periodontitis

https://doi.org/10.33925/1683-3759-2021-26-4-275-283

Abstract

Relevance. Apical periodontitis is one of the most common periodontal diseases. Enterococcus faecalis, which naturally inhabits the intestine, relatively rarely colonizes the oral mucosa of healthy individuals – in 1-20% of cases. However, 68% of patients with oral infectious diseases (caries, pulpitis, periodontitis, etc.) demonstrate it, especially patients with comorbidity, e.g., diabetes mellitus (60% of cases). It may change the risk profile of the inflammatory periodontal disease progression caused by the appearance of unusual pathogens in the oral cavity. In the primary apical periodontitis, microorganisms usually spread into the periodontium from necrotized tissues of the tooth pulp, in secondary periodontitis – from the endodontically treated root canals. E faecalis has unique properties, i.e. resistance to physical and chemical factors, nutrient deficiency, which leads to the selection of this microorganism during the development of secondary apical periodontitis. 30-90% of root canals demonstrate this microorganism in this pathology. 33% of secondary apical periodontitis treatment fail due to this microorganism infection. E. faecalis exhibits natural and often acquired resistance to local and systemic antimicrobial drugs.
Thus, successful treatment of apical periodontitis requires identifying the microorganism and/or determining the composition of the microbial community that caused its development and determination of sensitivity to antimicrobial drugs due to the high frequency of association of this disease with i nfection of the affected area of E. faecalis.

About the Authors

N. E. Barantsevitch
Almazov National Medical Research Centre, Saint Petersburg
Russian Federation

Natalya E. Barantsevich, Researcher

Saint Petersburg



L. Yu. Orekhova
Pavlov First Saint Petersburg State Medical University
Russian Federation

Liudmila Yu. Orekhova, DMD, PhD, DSc, Professor, Head of the Department of Restorative Dentistry and  Periodontology, President of the Russian Periodontal Association

Saint Petersburg



E. P. Barantsevitch
Almazov National Medical Research Centre, Saint Petersburg
Russian Federation

Barantsevich Elena Petrovna, MD, PhD, DSc, Head of the Research Department of Microbiology and Nosocomial Infections

Saint Petersburg



References

1. Nair PN. On the causes of persistent apical periodontitis: a review. International Endodontic Journal. 2006;39(4):249-81. https://doi.org/10.1111/j.1365-2591.2006.01099.x

2. Braz-Silva PH, Bergamini ML, Mardegan AP, De Rosa CS, Hasseus B, Jonasson P. Inflammatory profile of chronic apical periodontitis: a literature review. Acta odontologica Scandinavica. 2019;77(3):173-180. doi: 10.1080/00016357.2018.1521005

3. Waal SV van der, Lappin DF, Crielaard W. Does apical periodontitis have systemic consequences? The need for well-planned and carefully conducted clinical studies. British Dental Journal. 2015;218(9):513-6. doi: 10.1038/sj.bdj.2015.340

4. Asgary S, Roghanizadeh L. Partial Necrosis Consequence of the Infection Spreading from an Adjacent Apical Periodontitis: A Case Report. Iranian Endodontic Journal. 2018;13(3):420-423. doi: 10.22037/iej.v13i3.22089

5. Vieyra JP, Machado R, Enriquez FJJ, Acosta FO Endodontic Treatments of Teeth with Necrotic Pulp and Apical Periodontitis – A Critical Analysis. Otolaryngol (Sunnyvale) 2016;6:281. doi: 10.4172/2161-119X.1000281

6. El Ouarti I, Chala S, Sakout M, Abdallaoui F. Prevalence and risk factors of Apical periodontitis in endodontically treated teeth: cross-sectional study in an Adult Moroccan subpopulation. BMC Oral Health. 2021;21(1):124. doi: 10.1186/s12903-021-01491-6

7. Bouillaguet S, Manoil D, Girard M, Louis J, Gaïa N, Leo S, Schrenzel J, Lazarevic V. Root Microbiota in Primary and Secondary Apical Periodontitis. Frontiers in Microbiology. 2018;9:2374. doi: 10.3389/fmicb.2018.02374

8. Vengerfeldt V, Mändar R, Nguyen MS, Saukas S, Saag M. Apical periodontitis in southern Estonian population: prevalence and associations with quality of root canal fillings and coronal restorations. BMC Oral Health. 2017;17(1):147. doi: 10.1186/s12903-017-0429-7

9. Huumonen S, Suominen AL, Vehkalahti MM. Prevalence of apical periodontitis in root filled teeth: findings from a nationwide survey in Finland. International Endodontic Journal. 2017;50(3):229-236. doi: 10.1111/iej.12625

10. Radaic A, Kapila YL. The oralome and its dysbiosis: New insights into oral microbiome-host interactions. Computational and Structural Biotechnology Journal. 2021;19:1335-1360. doi:10.1016/j.csbj.2021.02.010

11. Zaatout N. Presence of non-oral bacteria in the oral cavity. Archives of Microbiology. 2021;203:2747-2760. doi: 10.1007/s00203-021-02300-y

12. Burcham ZM, Garneau NL, Comstock SS. et al. Patterns of Oral Microbiota Diversity in Adults and Children: A Crowdsourced Population Study. Scientific Reports. 2020;10:2133. doi:10.1038/s41598-020-59016-0

13. van Winkelhoff AJ, Rurenga P, Wekema-Mulder GJ, Singadji ZM, Rams TE. Non-oral gram-negative facultative rods in chronic periodontitis microbiota. Microbial Pathogenesis. 2016 May;94:117-22. doi: 10.1016/j.micpath.2016.01.020

14. Arirachakaran P, Luangworakhun S, Charalampakis G, Dahlén G. Non-oral, aerobic, Gram-negative bacilli in the oral cavity of Thai HIV-positive patients on Highly-active anti-retrovirus therapy medication. Journal of Investigative and Clinical Dentistry. 2019 May;10(2):e12387. doi: 10.1111/jicd.12387

15. Chinnasamy A, Ramalingam K, Chopra P, Gopinath V, Bishnoi GP, Chawla G. Chronic nail biting, orthodontic treatment and Enterobacteriaceae in the oral cavity. Journal of Clinical and Experimental Dentistry. 2019;11(12):e1157-e1162. doi: 10.4317/jced.56059

16. Thurnheer T, Belibasakis GN. Integration of non-oral bacteria into in vitro oral biofilms. Virulence. 2015;6(3):258-64. doi: 10.4161/21505594.2014.967608

17. Kilian M, Chapple I, Hannig M. et al. The oral microbiome – an update for oral healthcare professionals. British dental journal official journal of the British Dental Association: BDJ online. 2016;221:657-666. doi: 10.1038/sj.bdj.2016.865

18. Kriebel K, Hieke C, Müller-Hilke B, Nakata M, Kreikemeyer B. Oral Biofilms from Symbiotic to Pathogenic Interactions and Associated Disease – Connection of Periodontitis and Rheumatic Arthritis by Peptidylarginine Deiminase. Frontiers in Microbiology. 2018;9:53. doi:10.3389/fmicb.2018.00053

19. Bernardi S, Anderson A, Macchiarelli G, Hellwig E, Cieplik F, Vach K, Al-Ahmad A. Subinhibitory Antibiotic Concentrations Enhance Biofilm Formation of Clinical Enterococcus faecalis Isolates. Antibiotics. 2021;10(7):874. doi: 10.3390/antibiotics10070874

20. Chen Y, Li X, Wu J, Lu W, Xu W, Wu B. Dental pulp stem cells from human teeth with deep caries displayed an enhanced angiogenesis potential in vitro. Journal of Dental Sciences. 2021;16(1):318-326. doi: 10.1016/j.jds.2020.03.007

21. Yong D, Cathro P. Conservative pulp therapy in the management of reversible and irreversible pulpitis. Australian Dental Journal. 2021;66 Suppl 1:S4-S14. doi: 10.1111/adj.12841

22. Sunitha V R, Emmadi P, Namasivayam A, Thyegarajan R, Rajaraman V. The periodontal – endodontic continuum: A review. Journal of Conservative Dentistry. 2008;11(2):54-62. doi:10.4103/0972-0707.44046

23. Singh P. Endo-perio dilemma: a brief review. Dental Research Journal. 2011;8(1):39-47. Available from: https://pdfs.semanticscholar.org/b3d2/b4423820c46c00dbd94667b20ee0800d659c.pdf?_ga=2.16943865.1327773124.1639943689-915071902.1634290539

24. Gomes BPFA, Herrera DR. Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology. Brazilian Oral Research. 2018;32(suppl 1):e69. doi: 10.1590/1807-3107bor-2018.vol32.0069

25. Persoon IF, Özok AR. Definitions and Epidemiology of Endodontic Infections. Current Oral Health Reports. 2017;4(4):278-285. doi: 10.1007/s40496-017-0161-z

26. Shah D, Lynd T, Ho D, Chen J, Vines J, Jung HD, Kim JH, et al. Pulp-Dentin Tissue Healing Response: A Discussion of Current Biomedical Approaches. Journal of Clinical Medicine. 2020;9(2):434. doi: 10.3390/jcm9020434

27. Zero DT, Zandona AF, Vail MM, Spolnik KJ. Dental caries and pulpal disease. Dental Clinics of North America. 2011;55(1):29-46. doi: 10.1016/j.cden.2010.08.010

28. Liang Y, Ma R, Chen L, Dai X, Zuo S, Jiang W, Hu N, et al. Efficacy of i-PRF in regenerative endodontics therapy for mature permanent teeth with pulp necrosis: study protocol for a multicentre randomised controlled trial. Trials. 2021;22(1):436. doi: 10.1186/s13063-021-05401-7

29. Bordagaray MJ, Fernández A, Garrido M, Astorga J, Hoare A, Hernández M. Systemic and Extraradicular Bacterial Translocation in Apical Periodontitis. Frontiers in Cellular and Infection Microbiology. 2021;11:649925. doi: 10.3389/fcimb.2021.649925

30. Krawczyk B, Wityk P, Gałęcka M, Michalik M. The Many Faces of Enterococcus spp. Commensal, Probiotic and Opportunistic Pathogen. Microorganisms. 2021;9(9):1900. doi:10.3390/microorganisms9091900

31. Carrero Martínez C, Gonzáliez Gilbert MC, Martínez Lapiolo MA, Serna Varona F, Díez Ortega H, Rodríguez Ciodaro A. Low frequency of Enterococcus faecalis in the oral mucosa of subjects attending dental consultation. Revista Facultad de Odontología. 2015;26(2):261-270. Available from: http://www.scielo.org.co/pdf/rfoua/v26n2/v26n2a03.pdf

32. Komiyama EY, Lepesqueur LS, Yassuda CG, Samaranayake LP, Parahitiyawa NB, Balducci I, Koga-Ito CY. Enterococcus Species in the Oral Cavity: Prevalence, Virulence Factors and Antimicrobial Susceptibility. PLoS One. 2016;11(9):e0163001. doi:10.1371/journal.pone.0163001

33. Salah R, Dar-Odeh N, Abu Hammad O, Shehabi AA. Prevalence of putative virulence factors and antimicrobial susceptibility of Enterococcus faecalis isolates from patients with dental Diseases. BMC Oral Health. 2008;8:17. doi: 10.1186/1472-6831-8-17

34. Kaklamanos EG, Charalampidou M, Menexes G, Topitsoglou V, Kalfas S. Transient oral microflora in Greeks attending day centres for the elderly and residents in homes for the elderly. Gerodontology. 2005;22(3):158-167. doi:10.1111/j.1741-2358.2005.00069.x

35. Anderson AC, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, Arweiler N, et al. Enterococcus faecalis from Food, Clinical Specimens, and Oral Sites: Prevalence of Virulence Factors in Association with Biofilm Formation. Frontiers in Microbiology. 2016;6:1534. doi:10.3389/fmicb.2015.01534

36. Wang Z, Yang G, Ren B, Gao Y, Peng X, Li M, H.K.Xu H, et al. Effect of Antibacterial Root Canal Sealer on Persistent Apical Periodontitis. Antibiotics. 2021;10(6):741. doi:10.3390/antibiotics10060741

37. Saffari F, Sobhanipoor MH, Shahravan A, Ahmadrajabi R. Virulence Genes, Antibiotic Resistance and Capsule Locus Polymorphisms in Enterococcus faecalis isolated from Canals of Root-Filled Teeth with Periapical Lesions. Journal of Infection and Chemotherapy. 2018;50(4):340-345. doi:10.3947/ic.2018.50.4.340

38. Rôças IN, Siqueira JF Jr, Santos KR. Association of Enterococcus faecalis with different forms of periradicular diseases. Journal of Endodontics. 2004 May;30(5):315-20. doi:10.1097/00004770-200405000-00004

39. Molander A, Reit C, Dahlén G, Kvist T. Microbiological docks of root-filled teeth with apical periodontitis. International Endodontic Journal. 1998;31(1): 1-7. https://doi.org/10.1046/j.1365-2591.1998.t01-1-00111.x

40. Ross KM, Mehr JS, Greeley RD, Montoya LA, Kulkarni PA, Frontin S, Weigle TJ, et al. Outbreak of bacterial endocarditis associated with an oral surgery practice: New Jersey public health surveillance, 2013 to 2014. Journal of the American Dental Association. 2018;149(3):191-201. doi: 10.1016/j.adaj.2017.10.002

41. Farahani A. State of Globe: Enterococci: Virulence Factors and Biofilm Formation. Journal of Global Infectious Diseases. 2016;8(1):1-2. doi: 10.4103/0974-777X.176139

42. Kayaoglu G, Ørstavik D. Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Critical reviews in oral biology and medicine: an official publication of the American Association of Oral Biologists. 2004;15(5):308-20. doi:10.1177/154411130401500506

43. Zheng JX, Wu Y, Lin ZW, Pu ZY, Yao WM, Chen Z, Li DY, et al. Characteristics of and Virulence Factors Associated with Biofilm Formation in Clinical Enterococcus faecalis Isolates in China. Frontiers in Microbiology. 2017;8:2338. doi: 10.3389/fmicb.2017.02338

44. Thurlow LR, Thomas VC, Narayanan S, Olson S, Fleming SD, Hancock LE. Gelatinase contributes to the pathogenesis of endocarditis caused by Enterococcus faecalis. Infection and Immunity. 2010;78(11):4936-43. doi: 10.1128/IAI.01118-09

45. Ali L, Goraya MU, Arafat Y, Ajmal M, Chen JL, Yu D. Molecular Mechanism of Quorum-Sensing in Enterococcus faecalis: Its Role in Virulence and Therapeutic Approaches. International Journal of Molecular Sciences. 2017;18(5):960. doi: 10.3390/ijms18050960

46. Comerlato CB, Resende MC, Caierão J, d'Azevedo PA. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Memórias do Instituto Oswaldo Cruz. 2013;108(5):590-595. doi: 10.1590/S0074-02762013000500009

47. Chuang-Smith ON, Wells CL, Henry-Stanley MJ, Dunny GM. Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS One. 2010;5(12):e15798. doi: 10.1371/journal.pone.0015798

48. Hashem YA, Abdelrahman KA, Aziz RK. Phenotype–Genotype Correlations and Distribution of Key Virulence Factors in Enterococcus faecalis Isolated from Patients with Urinary Tract Infections. Infection and Drug Resistance. 2021;14:1713-1723. doi:10.2147/IDR.S305167

49. Cirrincione S, Neumann B, Zühlke D, Riedel K, Pessione E. Detailed Soluble Proteome Analyses of a Dairy- Isolated Enterococcus faecalis: A Possible Approach to Assess Food Safety and Potential Probiotic Value. Frontiers in Nutrition. 2019;6:71. doi: 10.3389/fnut.2019.00071

50. Giraffa G. Enterococci from foods. FEMS Microbiology Reviews. 2002 Jun;26(2):163-71. doi: 10.1111/j.1574-6976.2002.tb00608.x

51. Dapkevicius MLE, Sgardioli B, Câmara SPA, Poeta P, Malcata FX. Current Trends of Enterococci in Dairy Products: A Comprehensive Review of Their Multiple Roles. Foods. 2021;10(4):821. doi: 10.3390/foods10040821

52. Tan SC, Chong CW, Teh CSJ, Ooi PT, Thong KL. Occurrence of virulent multidrug-resistant Enterococcus faecalis and Enterococcus faecium in the pigs, farmers and farm environments in Malaysia. PeerJ. 2018;6:e5353. doi: 10.7717/peerj.5353

53. Kim HJ, Koo M. Occurrence, Antimicrobial Resistance and Molecular Diversity of Enterococcus faecium in Processed Pork Meat Products in Korea. Foods. 2020;9(9):1283. doi: 10.3390/foods9091283

54. Razavi A, Gmür R, Imfeld T, Zehnder M. Recovery of Enterococcus faecalis from cheese in the oral cavity of healthy subjects. Oral Microbiology and Immunology. 2007;22(4):248-51. doi:10.1111/j.1399-302X.2006.00349.x

55. Vidana R, Sullivan A, Billström H, Ahlquist M, Lund B. Enterococcus faecalis infection in root canals – host-derived or exogenous source? Letters in Applied Microbiology. 2011;52(2):109-15. doi:10.1111/j.1472-765X.2010.02972.x

56. Miller WR, Munita JM, Arias CA. Mechanisms of antibiotic resistance in enterococci. Expert Review of Anti-infective Therapy. 2014;12(10):1221-1236. doi: 10.1586/14787210.2014.956092

57. Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in enterococcus. Virulence. 2012;3(5):421-433. doi: 10.4161/viru.21282

58. Segura-Egea JJ, Martín-González J, Jiménez-Sánchez MDC, Crespo-Gallardo I, Saúco-Márquez JJ, Velasco- Ortega E. Worldwide pattern of antibiotic prescription in endodontic infections. International Dental Journal. 2017;67(4):197-205. doi: 10.1111/idj.12287

59. Cieplik F, Jakubovics NS, Buchalla W, Maisch T, Hellwig E, Al-Ahmad A. Resistance Toward Chlorhexidine in Oral Bacteria - Is There Cause for Concern? Frontiers in Microbiology. 2019;10:587. doi:10.3389/fmicb.2019.00587

60. Faras F, Abo-Alhassan F, Sadeq A, Burezq H. Complication of improper management of sodium hypochlorite accident during root canal treatment. Journal of International Society of Preventive and Community Dentistry. 2016;6(5):493-496. doi: 10.4103/2231-0762.192939

61. Brookes ZLS, Bescos R, Belfield LA, Ali K, Roberts A. Current uses of chlorhexidine for management of oral disease: a narrative review. Journal of Dentistry. 2020;103:103497. doi:10.1016/j.jdent.2020.103497

62. Chia Shi Zhe G, Green A, Fong YT, Lee HY, Ho SF. Rare case of type I hypersensitivity reaction to sodium hypochlorite solution in a healthcare setting. BMJ Case Reports. 2016;2016:bcr2016217228. doi: 10.1136/bcr-2016-217228

63. Gomes BP, Ferraz CC, Vianna ME, Berber VB, Teixeira FB, Souza-Filho FJ. In vitro antimicrobial activity of several concentrations of sodium hypochlorite and chlorhexidine gluconate in the elimination of Enterococcus faecalis. International Endodontic Journal. 2001;34(6):424-8. doi: 10.1046/j.1365-2591.2001.00410.x

64. Mallya L, Shenoy R, Mala K, Shenoy S. Evaluation of the antimicrobial efficacy of 20% Punica granatum, 0.2% chlorhexidine gluconate, and 2.5% sodium hypochlorite used alone or in combinations against Enterococcus faecalis: An in-vitro study. Journal of Conservative Dentistry. 2019;22(4):367-370. doi:10.4103/JCD.JCD_43_19

65. Noites R, Pina-Vaz C, Rocha R, Carvalho MF, Gonçalves A, Pina-Vaz I. Synergistic antimicrobial action of chlorhexidine and ozone in endodontic treatment. BioMed Research International. 2014;2014:592423. doi: 10.1155/2014/592423

66. Shahriari S, Mohammadi Z, Mokhtari MM, Yousefi R. Effect of hydrogen peroxide on the antibacterial substantivity of chlorhexidine. International Journal of Dentistry. 2010;2010:946384. doi: 10.1155/2010/946384

67. Kitagawa H, Izutani N, Kitagawa R, Maezono H, Yamaguchi M, Imazato S. Evolution of resistance to cationic biocides in Streptococcus mutans and Enterococcus faecalis. Journal of Dentistry. 2016;47:18-22. doi: 10.1016/j.jdent.2016.02.008

68. Cope AL, Francis N, Wood F, Chestnutt IG. Systemic antibiotics for symptomatic apical periodontitis and acute apical abscess in adults. Cochrane database of systematic reviews. 2018;9(9):CD010136. doi: 10.1002/14651858.CD010136.pub3

69. Pöntinen AK, Top J, Arredondo-Alonso S, Tonkin-Hill G, Freitas AR, Novais C, Gladstone RA, et al. Apparent nosocomial adaptation of Enterococcus faecalis predates the modern hospital era. Nature Communications. 2021. Mar 9;12(1):1523. doi: 10.1038/s41467-021-21749-5

70. Kitagawa D, Komatsu M, Nakamura A, Suzuki S, Oka M, Masuo K, Hamanaka E, et al. Nosocomial infections caused by vancomycin-resistant Enterococcus in a Japanese general hospital and molecular genetic analysis. Journal of Infection and Chemotherapy. 2021 Dec;27(12):1689-1693. doi: 10.1016/j.jiac.2021.08.004

71. Kampmeier S, Tönnies H, Correa-Martinez CL, Mellmann A, Schwierzeck V. A nosocomial cluster of vancomycin resistant enterococci among COVID-19 patients in an intensive care unit. Antimicrobial Resistance & Infection Control. 2020;9(1):154. doi: 10.1186/s13756-020-00820-8

72. Abele-Horn M, Vogel U, Klare I, Konstabel C, Trabold R, Kurihara R, Witte W, et al. Molecular epidemiology of hospital- acquired vancomycin-resistant enterococci. Journal of Clinical Microbiology. 2006 Nov;44(11):4009-13. doi: 10.1128/JCM.00195-06

73. Preethee T, Kandaswamy D, Hannah R. Molecular identification of an Enterococcus faecalis endocarditis antigen efaA in root canals of therapy-resistant endodontic infections. Journal of Conservative Dentistry. 2012;15(4):319-22. doi: 10.4103/0972-0707.101886

74. Royer G, Roisin L, Demontant V, Lo S, Coutte L, Lim P, Pawlotsky JM, et al. Microdiversity of Enterococcus faecalis isolates in cases of infective endocarditis: selection of non-synonymous mutations and large deletions is associated with phenotypic modifications. Emerging Microbes and Infections. 2021;10(1):929-938. doi: 10.1080/22221751.2021.1924865

75. Herrera-Hidalgo L, de Alarcón A, López-Cortes LE, Luque-Márquez R, López-Cortes LF, Gutiérrez-Valencia A, Gil-Navarro MV. Enterococcus faecalis Endocarditis and Outpatient Treatment: A Systematic Review of Current Alternatives. Antibiotics. 2020;9(10):657. doi: 10.3390/antibiotics9100657


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Barantsevitch NE, Orekhova LY, Barantsevitch EP. The role of Enterococcus faecalis in apical periodontitis. Parodontologiya. 2021;26(4):275-283. (In Russ.) https://doi.org/10.33925/1683-3759-2021-26-4-275-283

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