Int J Stomatol

Int J Stomatol ›› 2020, Vol. 47 ›› Issue (2): 225-234.doi: 10.7518/gjkq.2020048

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Progress in pathogenic factors and mechanisms of Enterococcus faecalis in oral and systemic diseases

Shui Yusen1,Lü Xiaoying1,Li Jingya1,Yang Ran2()   

  1. 1. State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & West China School of Stomatology, Sichuan University, Chengdu 610041, China
    2. State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Dept. of Pediatric Dentistry, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China
  • Received:2019-05-05 Revised:2019-09-10 Online:2020-03-01 Published:2020-03-12
  • Contact: Ran Yang E-mail:yangran@scu.edu.cn
  • Supported by:
    This study was supported by National Natural Science Foundation of China(81800989)

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Abstract:

Enterococcus faecalis (E. faecalis) is the main pathogen of root canal reinfection and persistent periapical periodontitis in human oral cavity. This species can survive for a long time in the harsh environment of a root canal. E. faecalis has a certain resistance to most root canal therapy drugs, as well as cleaning and disinfection methods. This species presents a major challenge in root canal therapy at present. In addition, E. faecalis is associated with some systemic infections, such as gastrointestinal and urinary tract infection. Its pathogenesis is related to its initial adhesion to the host, biofilm formation, invasive infection, and immune escape. E. faecalis expresses various proteins, glycolipids, and other adhesion to achieve initial adhesion. This species can regulates the expression of various biofilm-associated genes to form a mature biofilm to fight against the body’s deterioration, and realize the communication between cells subsequently. Eventually, E. faecalis colonizes a local area or even the whole body to cause infection. The present review focuses on the pathogenic factors and pathogenesis of E. faecalis.

Key words: Enterococcus faecalis, root canal reinfection, persistent periapical periodontitis, systemic infection

CLC Number: 

  • R780.2

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[1] Castro MS, Molina MA, Azpiroz MB , et al. Probiotic activity of Enterococcus faecalis CECT7121: effects on mucosal immunity and intestinal epithelial cells[J]. J Appl Microbiol, 2016,121(4):1117-1129.
[2] Molina MA, Díaz AM, Hesse C , et al. Immunosti-mulatory effects triggered by Enterococcus faecalis CECT7121 probiotic strain involve activation of dendritic cells and interferon-gamma production[J]. PLoS One, 2015,10(5):e0127262.
[3] Goh HMS, Yong MHA, Chong KKL , et al. Model systems for the study of Enterococcal colonization and infection[J]. Virulence, 2017,8(8):1525-1562.
[4] Zheng JX, Wu Y, Lin ZW , et al. Characteristics of and virulence factors associated with biofilm for-mation in clinical Enterococcus faecalis isolates in China[J]. Front Microbiol, 2017,8:2338.
[5] Ch’ng JH, Chong KKL, Lam LN , et al. Biofilm-as-sociated infection by Enterococci[J]. Nat Rev Micro-biol, 2019,17(2):82-94.
[6] Singh KV, La Rosa SL, Somarajan SR , et al. The fi- bronectin-binding protein EfbA contributes to patho-genesis and protects against infective endocarditis caused by Enterococcus faecalis[J]. Infect Immun, 2015,83(12):4487-4494.
[7] Torelli R, Serror P, Bugli F , et al. The PavA-like fi-bronectin-binding protein of Enterococcus faecalis, EfbA, is important for virulence in a mouse model of ascending urinary tract infection[J]. J Infect Dis, 2012,206(6):952-960.
[8] Isenmann R, Schwarz M, Rozdzinski E , et al. In-teraction of fibronectin and aggregation substance promotes adherence of Enterococcus faecalis to human colon[J]. Dig Dis Sci, 2002,47(2):462-468.
[9] Diederich AK, Wobser D, Spiess M , et al. Role of glycolipids in the pathogenesis of Enterococcus fae-calis urinary tract infection[J]. PLoS One, 2014,9(5):e96295.
[10] Montealegre MC, La Rosa SL, Roh JH , et al. The Enterococcus faecalis EbpA pilus protein: attenua-tion of expression, biofilm formation, and adherence to fibrinogen start with the rare initiation codon ATT[J]. MBio, 2015,6(3):e00467-15.
[11] Ahmadrajabi R, Dalfardi MS, Farsinejad A , et al. Distribution of Ebp pili among clinical and fecal isolates of Enterococcus faecalis and evaluation for human platelet activation[J]. APMIS, 2018,126(4):314-319.
[12] Wang QQ, Zhang CF, Chu CH , et al. Prevalence of Enterococcus faecalis in saliva and filled root canals of teeth associated with apical periodontitis[J]. Int J Oral Sci, 2012,4(1):19-23.
[13] Kowalski WJ, Kasper EL, Hatton JF , et al. Entero-coccus faecalis adhesin, Ace, mediates attachment to particulate dentin[J]. J Endod, 2006,32(7):634-637.
[14] Rahimi N, Poursina F, sadat Ghaziasgar F , et al. Pre-sence of virulence factor genes (gelE and esp) and biofilm formation in clinical Enterococcus faecalis and Enterococcus faecium isolated from urinary tract infection in Isfahan, Iran[J]. Gene Rep, 2018,13:72-75.
[15] Saffari F, Dalfardi MS, Mansouri S , et al. Survey for correlation between biofilm formation and virulence determinants in a collection of pathogenic and fecal Enterococcus faecalis isolates[J]. Infect Chemother, 2017,49(3):176-183.
[16] Waters CM, Hirt H, McCormick JK , et al. An amino-terminal domain of Enterococcus faecalis aggrega-tion substance is required for aggregation, bacterial internalization by epithelial cells and binding to lipoteichoic acid[J]. Mol Microbiol, 2004,52(4):1159-1171.
[17] La Rosa SL, Montealegre MC, Singh KV , et al. Ente-rococcus faecalis Ebp pili are important for cell-cell aggregation and intraspecies gene transfer[J]. Micro-biology, 2016,162(5):798-802.
[18] Afonina I, Lim XN, Tan R , et al. Planktonic interference and biofilm alliance between aggregation substance and endocarditis-and biofilm-associated pili in Ente-rococcus faecalis[J]. J Bacteriol, 2018,200(24):e00361-18.
[19] Liu HY, Xu Q, Huo LJ , et al. Chemical composition of Enterococcus faecalis in biofilm cells initiated from different physiologic states[J]. Folia Microbiol, 2014,59(5):447-453.
[20] Ran SJ, Jiang W, Zhu CL , et al. Exploration of the mechanisms of biofilm formation by Enterococcus faecalis in glucose starvation environments[J]. Aust Dent J, 2015,60(2):143-153.
[21] Keogh D, Lam LN, Doyle LE , et al. Extracellular electron transfer powers Enterococcus faecalis bio-film metabolism[J]. MBio, 2018,9(2):e00626-17.
[22] Colomer-Winter C, Flores-Mireles AL, Baker SP , et al. Manganese acquisition is essential for virulence of Enterococcus faecalis[J]. PLoS Pathog, 2018,14(9):e1007102.
[23] Shuping GB, Orstavik D, Sigurdsson A , et al. Re-duction of intracanal bacteria using nickel-titanium rotary instrumentation and various medications[J]. J Endod, 2000,26(12):751-755.
[24] Sum C, Mohanty S, Gupta PK , et al. Influence of endodontic chemical treatment on Enterococcus faecalis adherence to collagen studied with laser scanning confocal microscopy and optical tweezers: a preliminary study[J]. J Biomed Opt, 2008,13(4):044017.
[25] Wu SZ, Liu YJ, Zhang H , et al. The susceptibility to calcium hydroxide modulated by the essential walR gene reveals the role for Enterococcus faecalis biofilm aggregation[J]. J Endod, 2019,45(3):295-301.
[26] Stenhouse M, Zilm P, Ratnayake J , et al. Investiga-tion of the effect of rapid and slow external pH in-creases on Enterococcus faecalis biofilm grown on dentine[J]. Aust Dent J, 2018,63(2):224-230.
[27] Ran SJ, He ZY, Liang JP . Survival of Enterococcus faecalis during alkaline stress: changes in morpho-logy, ultrastructure, physiochemical properties of the cell wall and specific gene transcripts[J]. Arch Oral Biol, 2013,58(11):1667-1676.
[28] Chen WX, Liang JP, He ZY , et al. Differences in the chemical composition of Enterococcus faecalis bio-film under conditions of starvation and alkalinity[J]. Bioengineered, 2017,8(1):1-7.
[29] Baik JE, Choe HI, Hong SW , et al. Human salivary proteins with affinity to lipoteichoic acid of Entero-coccus faecalis[J]. Mol Immunol, 2016,77:52-59.
[30] Guneser MB, Eldeniz AU . The effect of gelatinase production of Enterococcus faecalis on adhesion to dentin after irrigation with various endodontic irri-gants[J]. Acta Biomater Odontol Scand, 2016,2(1):144-149.
[31] Marashdeh MQ, Gitalis R, Levesque C , et al. Ente-rococcus faecalis hydrolyzes dental resin composites and adhesives[J]. J Endod, 2018,44(4):609-613.
[32] Walton RE, Perez F, Calas P , et al. Effect of dentin treatment on in vitro root tubule bacterial invasion[J]. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 1996,82(4):446-451.
[33] 黄晓晶, 郭晓霞, 王燕煌 . 粪肠球菌牛牙感染根管模型的建立和电镜观察[J]. 重庆医科大学学报, 2012,37(1):43-46.
Huang XJ, Guo XX, Wang YH . A model of Entero-coccus faecalis in bovine dentinal tubules and SEM evaluation[J]. J Chongqing Med Univ, 2012,37(1):43-46.
[34] Kirsch J, Basche S, Neunzehn J , et al. Is it really penetration? Locomotion of devitalized Enterococcus faecalis cells within dentinal tubules of bovine teeth[J]. Arch Oral Biol, 2017,83:289-296.
[35] Ran S, Wang J, Jiang W , et al. Assessment of den-tinal tubule invasion capacity of Enterococcus fae-calis under stress conditions ex vivo[J]. Int Endod J, 2015,48(4):362-372.
[36] Ran SJ, Gu SS, Wang J , et al. Dentin tubule invasion by Enterococcus faecalis under stress conditions ex vivo[J]. Eur J Oral Sci, 2015,123(5):362-368.
[37] 赵洁, 曹祥莉, 钟晓波 . 根管预备对粪肠球菌感染根管形成细菌渗漏的影响[J]. 重庆医学, 2015,44(21):2907-2909.
Zhao J, Cao XL, Zhong XB . The in vitro study of the bacterial leakage from infected root canal and the effect of the root canal preparation[J]. Chongqing Med, 2015,44(21):2907-2909.
[38] Xu JL, He JZ, Shen Y , et al. Influence of endodontic procedure on the adherence of Enterococcus faecalis[J]. J Endod, 2019,45(7):943-949.
[39] 张琛, 杨玥, 侯本祥 . 持续性根尖周炎优势菌粪肠球菌生物膜形成能力的体外研究[J]. 北京口腔医学, 2016,24(1):1-5.
Zhang C, Yang Y, Hou BX . Biofilm formation of Enterococcus faecalis isolated from persistent periodontitis[J]. Beijing J Stomatol, 2016,24(1):1-5.
[40] 郭惠杰, 岳林 . 粪肠球菌在根管内定植模式的体外研究[J]. 北京大学学报(医学版), 2009,41(6):699-701.
Guo HJ, Yue L . Patterns of Enterococcus faecalis in infected root canals: an in vitro study[J]. J Peking Univ (Heal Sci), 2009,41(6):699-701.
[41] Park OJ, Kim J, Yang J , et al. Enterococcus faecalis inhibits osteoblast differentiation and induces che-mokine expression[J]. J Endod, 2015,41(9):1480-1485.
[42] Yang HH, Jun HK, Jung YJ , et al. Enterococcus fae-calis activates caspase-1 leading to increased inter-leukin-1 beta secretion in macrophages[J]. J Endod, 2014,40(10):1587-1592.
[43] 卢煜, 刘成霞, 刘忠俊 . TRAF6在粪肠球菌感染人成骨样细胞炎症反应中的作用[J]. 口腔疾病防治, 2017,25(7):420-425.
Lu Y, Liu CX, Liu ZJ . Role of TRAF6 in inflamma-tory responses of human osteoblast-like cells with Enterococcus faecalis[J]. J Prev Treat Stomatol Dis, 2017,25(7):420-425.
[44] 王丽娜, 叶丹丹, 王娇娇 , 等. 粪肠球菌LTA通过促进ROS的高表达活化NLRP3炎性体[J]. 口腔医学研究, 2018,34(2):112-116.
Wang LN, Ye DD, Wang JJ , et al. Enterococcus fae-calis LTA activates NLRP3 inflammasome by pro-moting high expression of ROS[J]. J Oral Sci Res, 2018,34(2):112-116.
[45] Bachtiar BM, Bachtiar EW . Proinflammatory MG-63 cells response infection with Enterococcus faecalis cps2 evaluated by the expression of TLR-2, IL-1β, and iNOS mRNA[J]. BMC Res Notes, 2017,10(1):401.
[46] 张明, 卢冰铃, 张金秀 , 等. 溶血与非溶血型粪肠球菌对大鼠再感染根尖周炎炎症进程的影响[J]. 口腔医学研究, 2015,31(10):965-968, 973.
Zhang M, Lu BL, Zhang JX , et al. Effect of cytolysin of Enterococcus faecalis on the inflammatory pro-gress of rat reinfected periapical periodontitis[J]. J Oral Sci Res, 2015,31(10):965-968, 973.
[47] Lu BL, Zhang JX, Huang XJ , et al. Expression of interleukin-1β and matrix metalloproteinase-8 in cytolytic and noncytolytic Enterococcus faecalis-induced persistent apical periodontitis: a comparative study in the rat[J]. J Endod, 2015,41(8):1288-1293.
[48] Wang S, Deng ZH, Seneviratne CJ , et al. Enterococcus faecalis promotes osteoclastogenesis and semaphorin 4D expression[J]. Innate Immun, 2015,21(7):726-735.
[49] 左美娜, 王丽娜, 仉红 , 等. BTK在粪肠球菌介导的炎症环境中的破骨作用[J]. 中国微生态学杂志, 2018,30(9):1029-1032.
Zuo MN, Wang LN, Zhang H , et al. Role of BTK in osteoclasts stimulated by Enterococcus faecalis[J]. Chin J Microecol, 2018,30(9):1029-1032.
[50] Xu ZZ, Tong ZC, Neelakantan P , et al. Enterococcus faecalis immunoregulates osteoclastogenesis of ma-crophages[J]. Exp Cell Res, 2018,362(1):152-158.
[51] Park OJ, Yang J, Kim J , et al. Enterococcus faecalis attenuates the differentiation of macrophages into osteoclasts[J]. J Endod, 2015,41(5):658-662.
[52] Wang S, Heng BC, Qiu SQ , et al. Lipoteichoic acid of Enterococcus faecalis inhibits osteoclastogenesis via transcription factor RBP-[J][J]. Innate Immun, 2019,25(1):13-21.
[53] Li Y, Tong ZC, Ling JQ . Effect of the three Enteroco-ccus faecalis strains on apoptosis in MC3T3 cells[J]. Oral Dis, 2019,25(1):309-318.
[54] Ran S, Chu M, Gu S , et al. Enterococcus faecalis induces apoptosis and pyroptosis of human osteoblastic MG63 cells via the NLRP3 inflammasome[J]. Int Endod J, 2019,52(1):44-53.
[55] Tong ZC, Ma JL, Tan JL , et al. Effects of inactivated Enterococcus faecalis on the proliferation and osteo-genic induction of osteoblasts[J]. Mol Med Rep, 2016,14(6):5125-5133.
[56] Steck N, Hoffmann M, Sava IG , et al. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation[J]. Gastroenterology, 2011,141(3):959-971.
[57] Maharshak N, Huh EY, Paiboonrungruang C , et al. Enterococcus faecalis gelatinase mediates intestinal permeability via protease-activated receptor 2[J]. Infect Immun, 2015,83(7):2762-2770.
[58] Peng Z, Krey V, Wei H , et al. Impact of actin on ad-hesion and translocation of Enterococcus faecalis[J]. Arch Microbiol, 2014,196(2):109-117.
[59] Tan QL, Xu HY, Xu F , et al. Survival, distribution, and translocation of Enterococcus faecalis and im-plications for pregnant mice[J]. FEMS Microbiol Lett, 2013,349(1):32-39.
[60] Guiton PS, Hannan TJ, Ford B , et al. Enterococcus faecalis overcomes foreign body-mediated inflam-mation to establish urinary tract infections[J]. Infect Immun, 2013,81(1):329-339.
[61] Shon W, Lim S, Bae K , et al. The expression of α4 integrins by human polymorphonuclear neutrophils in response to sonicated extracts of Enterococcus faecalis[J]. J Endod, 2005,31(5):369-372.
[62] Horsley H, Malone-Lee J, Holland D , et al. Entero-coccus faecalis subverts and invades the host urothelium in patients with chronic urinary tract infection[J]. PLoS One, 2013,8(12):e83637.
[63] Li X, Kolltveit KM, Tronstad L , et al. Systemic di-seases caused by oral infection[J]. Clin Microbiol Rev, 2000,13(4):547-558.
[64] Mulliken RA, Casner MJ . Oral manifestations of systemic disease[J]. Emerg Med Clin N Am, 2000,18(3):565-575.
[65] Tsuda Y, Shigematsu K, Kobayashi M , et al. Role of polymorphonuclear neutrophils on infectious com-plications stemming from Enterococcus faecalis oral infection in thermally injured mice[J]. J Immunol, 2008,180(6):4133-4138.
[66] Mathew S, Yaw-Chyn L, Kishen A . Immunogenic potential of Enterococcus faecalis biofilm under simulated growth conditions[J]. J Endod, 2010,36(5):832-836.
[67] Somma F, Castagnola R, Bollino D , et al. Oral in-flammatory process and general health. Part 2: how does the periapical inflammatory process compromise general health[J]. Eur Rev Med Pharmacol Sci, 2011,15(1):35-51.
[68] Saffari F, Sobhanipoor MH, Shahravan A , et al. Viru-lence genes, antibiotic resistance and capsule locus polymorphisms in Enterococcus faecalis isolated from canals of root-filled teeth with periapical lesions[J]. Infect Chemother, 2018,50(4):340-345.
[69] Vidana R . Origin of intraradicular infection with Enterococcus faecalis in endodontically treated teeth[M]. Stockholm: Karolinska Institute, 2015: 55.
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[1] . [J]. Foreign Med Sci: Stomatol, 1999, 26(06): .
[2] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[3] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[4] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[5] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[6] . [J]. Foreign Med Sci: Stomatol, 1999, 26(04): .
[7] . [J]. Foreign Med Sci: Stomatol, 2005, 32(06): 458 -460 .
[8] . [J]. Foreign Med Sci: Stomatol, 2005, 32(06): 452 -454 .
[9] . [J]. Inter J Stomatol, 2008, 35(S1): .
[10] . [J]. Inter J Stomatol, 2008, 35(S1): .