SpringerLink
Log in

Preventive and Therapeutic Potential of Streptococcus cristatus CA119 in Experimental Periodontitis in Rats

  • Research
  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Periodontitis is an inflammatory condition of the oral cavity caused by a mixed infection of various bacteria, which not only severely affects the alveolar bone and connective tissues but also displays potential correlations with distal intestinal inflammation. In this study, we aimed to elucidate the therapeutic effects of Streptococcus cristatus CA119 on experimental periodontitis in rats and its impact on intestinal morphology. The results demonstrate that CA119 is capable of colonizing the oral cavity and exerting antagonistic effects on Porphyromonas gingivalis and Fusobacterium nucleatum, thus leading to a significant reduction in the oral pathogen load. Following CA119 intervention, there was a significant alleviation of weight loss in rats induced by periodontitis (P < 0.001). CA119 also regulated the expression of IL-6 (P < 0.05), IL-1β (P < 0.001), IL-18 (P < 0.001), COX-2 (P < 0.001), iNOS (P < 0.001), and MCP-1 (P < 0.01) in the gingival tissue. Additionally, CA119 reduced oxidative stress levels in rats and enhanced their antioxidant capacity. Microcomputed tomography (micro-CT) and histological analysis revealed that CA119 significantly reduced alveolar bone loss and reversed the downregulation of OPG/RANKL (P < 0.001). Furthermore, CA119 exhibited a significant protective effect against intestinal inflammation induced by periodontal disease and improved the colonic morphology in rats. In conclusion, this study demonstrates the role of CA119 as a potential oral probiotic in the prevention and treatment of experimental periodontitis, underscoring the potential of probiotics as a complementary approach to traditional periodontal care.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Data will be made available on request.

References

  1. Slots J (2017) Periodontitis: facts, fallacies and the future. Periodontol 2000 75:7–23. https://doi.org/10.1111/prd.12221

    Article  Google Scholar 

  2. Zhang Y, Wang X, Li H, Ni C, Du Z, Yan F (2018) Human oral microbiota and its modulation for oral health. Biomed Pharmacother 99:883–893. https://doi.org/10.1016/j.biopha.2018.01.146

    Article  PubMed  Google Scholar 

  3. Reyes L (2021) Porphyromonas gingivalis. Trends In. Microbiology 29:376–377. https://doi.org/10.1016/j.tim.2021.01.010

    Article  CAS  Google Scholar 

  4. Kinane DF, Stathopoulou PG, Papapanou PN (2017) Periodont Dis Nat Rev Dis Primers 3:17038. https://doi.org/10.1038/nrdp.2017.38

    Article  Google Scholar 

  5. de Andrade KQ, Almeida-da-Silva CLC, Coutinho-Silva R (2019) Immunological pathways triggered by Porphyromonas gingivalis and Fusobacterium nucleatum: therapeutic possibilities? Mediators Inflamm 2019:7241312. https://doi.org/10.1155/2019/7241312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Monasterio G, Fernández B, Castillo F, Rojas C, Cafferata EA, Rojas L et al (2019) Capsular-defective Porphyromonas gingivalis mutant strains induce less alveolar bone resorption than W50 wild-type strain due to a decreased Th1/Th17 immune response and less osteoclast activity. J Periodontol 90:522–534. https://doi.org/10.1002/JPER.18-0079

    Article  CAS  PubMed  Google Scholar 

  7. Signat B, Roques C, Poulet P, Duffaut D (2011) Fusobacterium nucleatum in periodontal health and disease. Curr Issues Mol Biol 13:25–36

    CAS  PubMed  Google Scholar 

  8. Bolstad AI, Jensen HB, Bakken V (1996) Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev 9:55–71. https://doi.org/10.1128/CMR.9.1.55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Dannewitz B, Holtfreter B, Eickholz P (2021) Periodontitis-therapy of a widespread disease. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 64:931–940. https://doi.org/10.1007/s00103-021-03373-2

    Article  PubMed  PubMed Central  Google Scholar 

  10. Haque MM, Yerex K, Kelekis-Cholakis A, Duan K (2022) Advances in novel therapeutic approaches for periodontal diseases. BMC Oral Health 22:492. https://doi.org/10.1186/s12903-022-02530-6

    Article  PubMed  PubMed Central  Google Scholar 

  11. Nguyen T, Brody H, Radaic A (2000) Kapila Y (2021) Probiotics for periodontal health-current molecular findings. Periodontol 87:254–267. https://doi.org/10.1111/prd.12382

    Article  Google Scholar 

  12. Zaura E, Twetman S (2019) Critical appraisal of oral pre- and probiotics for caries prevention and care. Caries Res 53:514–526. https://doi.org/10.1159/000499037

    Article  PubMed  Google Scholar 

  13. Ho M-H, Lamont RJ, **e H (2017) A novel peptidic inhibitor derived from Streptococcus cristatus ArcA attenuates virulence potential of Porphyromonas gingivalis. Sci Rep 7:16217. https://doi.org/10.1038/s41598-017-16522-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Van Holm W, Carvalho R, Delanghe L, Eilers T, Zayed N, Mermans F et al (2023) Antimicrobial potential of known and novel probiotics on in vitro periodontitis biofilms. NPJ Biofilms Microbiomes 9:3. https://doi.org/10.1038/s41522-023-00370-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhang G, Rudney JD (2011) Streptococcus cristatus attenuates Fusobacterium nucleatum-induced cytokine expression by influencing pathways converging on nuclear factor-κB. Mol Oral Microbiol 26:150–163. https://doi.org/10.1111/j.2041-1014.2010.00600.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zhang Q, Xu W, Xu X, Lu W, Zhao J, Zhang H et al (2021) Effects of Limosilactobacillus fermentum CCFM1139 on experimental periodontitis in rats. Food Funct 12:4670–4678. https://doi.org/10.1039/d1fo00409c

    Article  CAS  PubMed  Google Scholar 

  17. Invernici MM, Salvador SL, Silva PHF, Soares MSM, Casarin R, Palioto DB et al (2018) Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: a randomized clinical trial. J Clin Periodontol 45:1198–1210. https://doi.org/10.1111/jcpe.12995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Song B, **an W, Sun Y, Gou L, Guo Q, Zhou X et al (2023) Akkermansia muciniphila inhibited the periodontitis caused by Fusobacterium nucleatum. NPJ Biofilms Microbiomes 9:49. https://doi.org/10.1038/s41522-023-00417-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Huck O, Mulhall H, Rubin G, Kizelnik Z, Iyer R, Perpich JD et al (2020) Akkermansia muciniphila reduces Porphyromonas gingivalis-induced inflammation and periodontal bone destruction. J Clin Periodontol 47:202–212. https://doi.org/10.1111/jcpe.13214

    Article  CAS  PubMed  Google Scholar 

  20. Wang B-y, Wu J, Lamont RJ, Lin X, **e H (2009) Negative correlation of distributions of Streptococcus cristatus and Porphyromonas gingivalis in subgingival plaque. J Clin Microbiol 47:3902–3906. https://doi.org/10.1128/JCM.00072-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wang Q, Wang B-Y, Pratap S, **e H (2024) Oral microbiome associated with differential ratios of Porphyromonas gingivalis and Streptococcus cristatus. Microbiology Spectrum 12:e0348223. https://doi.org/10.1128/spectrum.03482-23

    Article  CAS  PubMed  Google Scholar 

  22. Wang B-Y, Lu T, Cai Q, Ho M-H, Sheng S, Meng H-W et al (2021) Potential microbiological risk factors associated with periodontitis and periodontal health disparities. Front Cell Infect Microbiol 11:789919. https://doi.org/10.3389/fcimb.2021.789919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rosier BT, Marsh PD, Mira A (2018) Resilience of the oral microbiota in health: mechanisms that prevent dysbiosis. J Dent Res 97:371–380. https://doi.org/10.1177/0022034517742139

    Article  CAS  PubMed  Google Scholar 

  24. Anusha RL, Umar D, Basheer B, Baroudi K (2015) The magic of magic bugs in oral cavity: probiotics. J Adv Pharm Technol Res 6:43–47. https://doi.org/10.4103/2231-4040.154526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Seminario-Amez M, López-López J, Estrugo-Devesa A, Ayuso-Montero R, Jané-Salas E (2017) Probiotics and oral health: a systematic review. Medicina oral, patologia oral y cirugia bucal 22:e282–e288. https://doi.org/10.4317/medoral.21494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Homayouni Rad A, Pourjafar H, Mirzakhani E (2023) A comprehensive review of the application of probiotics and postbiotics in oral health. Front Cell Infect Microbiol 13:1120995. https://doi.org/10.3389/fcimb.2023.1120995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Navarro-López V, Ramírez-Boscá A, Ramón-Vidal D, Ruzafa-Costas B, Genovés-Martínez S, Chenoll-Cuadros E et al (2018) Effect of oral administration of a mixture of probiotic strains on SCO RAD index and use of topical steroids in young patients with moderate atopic dermatitis: a randomized clinical trial. JAMA Dermatol 154:37–43. https://doi.org/10.1001/jamadermatol.2017.3647

    Article  PubMed  Google Scholar 

  28. Wendel U (2021) Assessing viability and stress tolerance of probiotics-a review. Front Microbiol 12:818468. https://doi.org/10.3389/fmicb.2021.818468

    Article  PubMed  Google Scholar 

  29. Zhao L, Duan F, Gong M, Tian X, Guo Y, Jia L et al (2021) (+)-Terpinen-4-ol inhibits Bacillus cereus biofilm formation by upregulating the interspecies quorum sensing signals diketopiperazines and diffusing signaling factors. J Agric Food Chem 69:3496–3510. https://doi.org/10.1021/acs.jafc.0c07826

    Article  CAS  PubMed  Google Scholar 

  30. Krishnapriya S, Babu DV (2015) Isolation and identification of bacteria to improve the strength of concrete. Microbiol Res 174:48–55. https://doi.org/10.1016/j.micres.2015.03.009

    Article  CAS  PubMed  Google Scholar 

  31. Li M, Zhao D, Guo J, Pan T, Niu T, Jiang Y et al (2024) Bacillus halotolerans SW207 alleviates enterotoxigenic Escherichia coli-induced inflammatory responses in weaned piglets by modulating the intestinal epithelial barrier, the TLR4/MyD88/NF-κB pathway, and intestinal microbiota. Microbiology Spectrum 12:e0398823. https://doi.org/10.1128/spectrum.03988-23

    Article  PubMed  PubMed Central  Google Scholar 

  32. Bian X, Evivie SE, Muhammad Z, Luo G-W, Liang H-Z, Wang N-N et al (2016) In vitro assessment of the antimicrobial potentials of Lactobacillus helveticus strains isolated from traditional cheese in Sinkiang China a gainst food-borne pathogens. Food Funct 7:789–797. https://doi.org/10.1039/c5fo01041a

    Article  CAS  PubMed  Google Scholar 

  33. Du H, Yao W, Kulyar MF-EA, Ding Y, Zhu H, Pan H et al (2022) Effects of Bacillus amyloliquefaciens TL106 isolated from Tibetan pigs on probiotic potential and intestinal microbes in weaned piglets. Microbiol Spectr 10:e0120521. https://doi.org/10.1128/spectrum.01205-21

    Article  PubMed  Google Scholar 

  34. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. https://doi.org/10.1186/1471-2164-12-402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics (Oxford, England) 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153

    Article  CAS  PubMed  Google Scholar 

  36. Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Galperin MY, Wolf YI, Makarova KS, Vera Alvarez R, Landsman D, Koonin EV (2021) COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res 49:D274–D281. https://doi.org/10.1093/nar/gkaa1018

    Article  CAS  PubMed  Google Scholar 

  38. Vieco-Saiz N, Belguesmia Y, Vachée A, Le Maréchal C, Salvat G, Drider D (2020) Antibiotic resistance, genome analysis and further safe traits of Clostridium perfringens ICVB082; a strain capable of producing an inhibitory compound directed only against a closely related pathogenic strain. Anaerobe 62:102177. https://doi.org/10.1016/j.anaerobe.2020.102177

    Article  CAS  PubMed  Google Scholar 

  39. Tsigkrimani M, Panagiotarea K, Paramithiotis S, Bosnea L, Pappa E, Drosinos EH et al (2022) Microbial ecology of sheep milk, artisanal feta, and kefalograviera cheeses. Part II: technological, safety, and probiotic attributes of lactic acid bacteria isolates. Foods (Basel, Switzerland) 11:459. https://doi.org/10.3390/foods11030459

  40. Gatej SM, Marino V, Bright R, Fitzsimmons TR, Gully N, Zilm P et al (2018) Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clin Periodontol 45:204–212. https://doi.org/10.1111/jcpe.12838

    Article  CAS  PubMed  Google Scholar 

  41. Rodrigues SF, de Oliveira MA, Martins JO, Sannomiya P, de Cássia TR, Nigro D et al (2006) Differential effects of chloral hydrate- and ketamine/xylazine-induced anesthesia by the s.c. route. Life Sci 79:1630–1637. https://doi.org/10.1016/j.lfs.2006.05.019

    Article  CAS  PubMed  Google Scholar 

  42. Nie Q, Wan X, Tao H, Yang Q, Zhao X, Liu H et al (2023) Multi-function screening of probiotics to improve oral health and evaluating their efficacy in a rat periodontitis model. Front Cell Infect Microbiol 13:1261189. https://doi.org/10.3389/fcimb.2023.1261189

    Article  PubMed  PubMed Central  Google Scholar 

  43. Yasmin I, Saeed M, Khan WA, Khaliq A, Chughtai MFJ, Iqbal R et al (2020) In vitro probiotic potential and safety evaluation (hemolytic, cytotoxic activity) of Bifidobacterium strains isolated from raw camel milk. Microorganisms 8:354. https://doi.org/10.3390/microorganisms8030354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Bendyk A, Marino V, Zilm PS, Howe P, Bartold PM (2009) Effect of dietary omega-3 polyunsaturated fatty acids on experimental periodontitis in the mouse. J Periodontal Res 44:211–216. https://doi.org/10.1111/j.1600-0765.2008.01108.x

    Article  CAS  PubMed  Google Scholar 

  45. Kesavalu L, Sathishkumar S, Bakthavatchalu V, Matthews C, Dawson D, Steffen M et al (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75:1704–1712. https://doi.org/10.1128/IAI.00733-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Du Q, Ren B, He J, Peng X, Guo Q, Zheng L et al (2021) Candida albicans promotes tooth decay by inducing oral microbial dysbiosis. ISME J 15:894–908. https://doi.org/10.1038/s41396-020-00823-8

    Article  CAS  PubMed  Google Scholar 

  47. Savijoki K, San-Martin-Galindo P, Pitkänen K, Edelmann M, Sillanpää A, vander Velde C, et al (2022) Food-grade bacteria combat pathogens by blocking AHL-mediated quorum sensing and biofilm formation. Foods (Basel, Switzerland) 12:90. https://doi.org/10.3390/foods12010090

    Article  CAS  PubMed  Google Scholar 

  48. ** Y-B, Cao X, Shi C-W, Feng B, Huang H-B, Jiang Y-L et al (2021) Lactobacillus rhamnosus GG promotes early B lineage development and IgA production in the lamina propria in piglets. J Immunol (Baltimore Md : 1950) 207:2179–2191. https://doi.org/10.4049/jimmunol.2100102

    Article  CAS  Google Scholar 

  49. Zou Y, Xue W, Luo G, Deng Z, Qin P, Guo R et al (2019) 1,520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses. Nat Biotechnol 37:179–185. https://doi.org/10.1038/s41587-018-0008-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Depamede SN, Asri N, Julisaniah NI, Suryadi BF, Kisworo D (2012) Isolation and partial purification of lysozyme from saliva of Bali cattle (Bos sondaicus) using an aqueous mixture of polyethylene glycol (PEG) with sodium sulfate. Afr J Biotech 11:1977–1980

    Article  CAS  Google Scholar 

  51. Jespersgaard C, Hajishengallis G, Russell MW, Michalek SM (2002) Identification and characterization of a nonimmunoglobulin factor in human saliva that inhibits Streptococcus mutans glucosyltransferase. Infect Immun 70:1136–1142. https://doi.org/10.1128/IAI.70.3.1136-1142.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cafferata EA, Terraza-Aguirre C, Barrera R, Faúndez N, González N, Rojas C et al (2020) Interleukin-35 inhibits alveolar bone resorption by modulating the Th17/Treg imbalance during periodontitis. J Clin Periodontol 47:676–688. https://doi.org/10.1111/jcpe.13282

    Article  CAS  PubMed  Google Scholar 

  53. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ et al (2017) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502. https://doi.org/10.1038/nrgastro.2017.75

    Article  PubMed  Google Scholar 

  54. Katsiki P, Nazmi K, Loos BG, Laine ML, Schaap K, Hepdenizli E et al (2021) Comparing periodontitis biomarkers in saliva, oral rinse and gingival crevicular fluid: a pilot study. J Clin Periodontol 48:1250–1259. https://doi.org/10.1111/jcpe.13479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ragland SA, Criss AK (2017) From bacterial killing to immune modulation: recent insights into the functions of lysozyme. PLoS Pathog 13:e1006512. https://doi.org/10.1371/journal.ppat.1006512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Peters VBM, van de Steeg E, van Bilsen J, Meijerink M (2019) Mechanisms and immunomodulatory properties of pre- and probiotics. Beneficial Microbes 10:225–236. https://doi.org/10.3920/BM2018.0066

    Article  CAS  PubMed  Google Scholar 

  57. Yang X, Peng Z, He M, Li Z, Fu G, Li S et al (2024) Screening, probiotic properties, and inhibition mechanism of a Lactobacillus antagonistic to Listeria monocytogenes. Sci Total Environ 906:167587. https://doi.org/10.1016/j.scitotenv.2023.167587.

    Article  CAS  PubMed  Google Scholar 

  58. Jansen PM, Abdelbary MMH, Conrads G (2021) A concerted probiotic activity to inhibit periodontitis-associated bacteria. PLoS ONE 16:e0248308. https://doi.org/10.1371/journal.pone.0248308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Liu T-H, Tsai T-Y, Pan T-M (2018) Effects of an ethanol extract from Lactobacillus paracasei subsp. paracasei NTU 101 fermented skimmed milk on lipopolysaccharide-induced periodontal inflammation in rats. Food Funct 9:4916–4925. https://doi.org/10.1039/c8fo01303a

    Article  CAS  PubMed  Google Scholar 

  60. Zhao Z, Wu X, Chen H, Liu Y, **ao Y, Chen H et al (2021) Evaluation of a strawberry fermented beverage with potential health benefits. PeerJ 9:e11974. https://doi.org/10.7717/peerj.11974

    Article  PubMed  PubMed Central  Google Scholar 

  61. Han Y, Huang Y, Gao P, Yang Q, Jia L, Zheng Y et al (2022) Leptin aggravates periodontitis by promoting M1 polarization via NLRP3. J Dent Res 101:675–685. https://doi.org/10.1177/00220345211059418

    Article  CAS  PubMed  Google Scholar 

  62. Cekici A, Kantarci A, Hasturk H (2000) Van Dyke TE (2014) Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 64:57–80. https://doi.org/10.1111/prd.12002

    Article  Google Scholar 

  63. Mombelli A (2000) (2018) Microbial colonization of the periodontal pocket and its significance for periodontal therapy. Periodontol 76:85–96. https://doi.org/10.1111/prd.12147

    Article  Google Scholar 

  64. Xu, WQ (2021) Epidemiological survey of three intestinal protozoa in domestic animals. (M.S.), JNU. https://doi.org/10.27169/d.cnki.gwqgu.2021.000227. (In Chinese)

  65. Ye, YH (2023) Evaluation of clinical effect and mechanism of Lactobacillus fermentans CCFM1139 in relieving periodontitis. (M.S.), JNU. https://doi.org/10.27169/d.cnki.gwqgu.2023.001102. (In Chinese)

  66. Sakanaka A, Kuboniwa M, Shimma S, Alghamdi SA, Mayumi S, Lamont RJ et al (2022) Fusobacterium nucleatum metabolically integrates commensals and pathogens in oral biofilms. MSystems 7:e0017022. https://doi.org/10.1128/msystems.00170-22

    Article  CAS  PubMed  Google Scholar 

  67. Lamont RJ, Hajishengallis G (2015) Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 21:172–183. https://doi.org/10.1016/j.molmed.2014.11.004

    Article  CAS  PubMed  Google Scholar 

  68. Romandini M, Laforí A, Romandini P, Baima G, Cordaro M (2018) Periodontitis and platelet count: a new potential link with cardiovascular and other systemic inflammatory diseases. J Clin Periodontol 45:1299–1310. https://doi.org/10.1111/jcpe.13004

    Article  CAS  PubMed  Google Scholar 

  69. Irwandi RA, Kuswandani SO, Harden S, Marletta D, D’Aiuto F (2022) Circulating inflammatory cell profiling and periodontitis: a systematic review and meta-analysis. J Leukoc Biol 111:1069–1096. https://doi.org/10.1002/JLB.5RU1021-524R

    Article  CAS  PubMed  Google Scholar 

  70. Araújo AAD, Pereira ADSBF, Medeiros CACXD, Brito GADC, Leitão RFDC, Araújo LDS et al (2017) Effects of metformin on inflammation, oxidative stress, and bone loss in a rat model of periodontitis. PLoS One 12:e0183506. https://doi.org/10.1371/journal.pone.0183506

  71. Plachokova AS, Andreu-Sánchez S, Noz MP, Fu J, Riksen NP (2021) Oral microbiome in relation to periodontitis severity and systemic inflammation. Int J Mol Sci 22:5876. https://doi.org/10.3390/ijms22115876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Sui L, Wang J, **ao Z, Yang Y, Yang Z, Ai K (2020) ROS-scavenging nanomaterials to treat periodontitis. Front Chem 8:595530. https://doi.org/10.3389/fchem.2020.595530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kang J, Postigo-Fernandez J, Kim K, Zhu C, Yu J, Meroni M et al (2023) Notch-mediated hepatocyte MCP-1 secretion causes liver fibrosis. JCI insight 8:e165369. https://doi.org/10.1172/jci.insight.165369

    Article  PubMed  PubMed Central  Google Scholar 

  74. Chen M, Cai W, Zhao S, Shi L, Chen Y, Li X et al (2019) Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol 46:608–622. https://doi.org/10.1111/jcpe.13112

    Article  CAS  PubMed  Google Scholar 

  75. Hu W, He Z, Du L, Zhang L, Li J, Ma Y et al (2023) Biomarkers of oxidative stress in broiler chickens attacked by lipopolysaccharide: a systematic review and meta-analysis. Ecotoxicol Environ Saf 266:115606. https://doi.org/10.1016/j.ecoenv.2023.115606

    Article  CAS  PubMed  Google Scholar 

  76. Jeong Y-J, Jung J-I, Kim Y, Kang C-H, Imm J-Y (2023) Effects of Lactobacillus reuteri MG5346 on receptor activator of nuclear factor-kappa B ligand (RANKL)-induced osteoclastogenesis and ligature-induced experimental periodontitis rats. Food Sci Anim Resour 43:157–169. https://doi.org/10.5851/kosfa.2022.e68

    Article  PubMed  PubMed Central  Google Scholar 

  77. Boyce BF, **ng 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  CAS  PubMed  PubMed Central  Google Scholar 

  78. Ohazama A, Courtney JM, Sharpe PT (2004) Opg, Rank, and Rankl in tooth development: co-ordination of odontogenesis and osteogenesis. J Dent Res 83:241–244. https://doi.org/10.1177/154405910408300311

    Article  CAS  PubMed  Google Scholar 

  79. Messora MR, Pereira LJ, Foureaux R, Oliveira LFF, Sordi CG, Alves AJN et al (2016) Favourable effects of Bacillus subtilis and Bacillus licheniformis on experimental periodontitis in rats. Arch Oral Biol 66:108–119. https://doi.org/10.1016/j.archoralbio.2016.02.014

    Article  PubMed  Google Scholar 

  80. Grilc NK, Zidar A, Kocbek P, Rijavec T, Colja T, Lapanje A et al (2023) Nanofibers with genotyped Bacillus strains exhibiting antibacterial and immunomodulatory activity. J Control Release: Official J Control Release Soc 355:371–384. https://doi.org/10.1016/j.jconrel.2023.01.082

    Article  CAS  Google Scholar 

  81. Wu F, Fang B, Wuri G, Zhao L, Liu F, Zhang M (2022) Metagenomic analysis reveals a mitigating role for Lactobacillus paracasei and Bifidobacterium animalis in experimental periodontitis. Nutrients 14:2125. https://doi.org/10.3390/nu14102125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Messora MR, Oliveira LFF, Foureaux RC, Taba M Jr, Zangerônimo MG, Furlaneto FAC et al (2013) Probiotic therapy reduces periodontal tissue destruction and improves the intestinal morphology in rats with ligature-induced periodontitis. J Periodontol 84:1818–1826. https://doi.org/10.1902/jop.2013.120644

    Article  PubMed  Google Scholar 

  83. Bao J, Li L, Zhang Y, Wang M, Chen F, Ge S et al (2022) Periodontitis may induce gut microbiota dysbiosis via salivary microbiota. Int J Oral Sci 14:32. https://doi.org/10.1038/s41368-022-00183-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Key R&D Program of China (2023YFD1800302), National Natural Science Foundation of China (32072888, U21A20261, 32202819), the China Agriculture Research System of MOF and MARA (CARS-35), and the Science and Technology Development Program of Jilin Province (20220202057NC, 20230101346JC, 20230202080NC, YDZJ202102CXJD029, YDZJ202301ZYTS326).

Author information

Author notes

  1. Dongyu Zhao and Ming-Han Li contributed equally to this work.

Authors and Affiliations

  1. College of Veterinary Medicine, Jilin Agricultural University, Changchun, China

    Dongyu Zhao, Ming-Han Li, Tianxu Pan, Jialin Guo, Junyi Li, Chunwei Shi, Nan Wang, Haibin Huang, Chunfeng Wang & Guilian Yang

  2. Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, China

    Dongyu Zhao, Ming-Han Li, Tianxu Pan, Jialin Guo, Junyi Li, Chunwei Shi, Nan Wang, Haibin Huang, Chunfeng Wang & Guilian Yang

  3. Engineering Research Center of Microecological Vaccines (Drugs) for Major Animal Diseases, Ministry of Education, Jilin Agricultural University, Changchun, China

    Dongyu Zhao, Ming-Han Li, Tianxu Pan, Jialin Guo, Junyi Li, Chunwei Shi, Nan Wang, Haibin Huang, Chunfeng Wang & Guilian Yang

Authors
  1. Dongyu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming-Han Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tianxu Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jialin Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junyi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunwei Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haibin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chunfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Guilian Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Dongyu Zhao: writing—original draft, software, conceptualization, formal analysis. Minghan Li: methodology, writing—review and editing, visualization. Tianxu Pan: data curation, formal analysis, writing—review and editing. Jialin Guo: software. Junyi Li: writing—review and editing. Chunwei Shi: funding acquisition. Nan Wang: writing—review and editing. Haibin Huang: visualization, writing—review and editing. Chunfeng Wang: resources, investigation, supervision. Guilian Yang: resources, investigation, supervision, funding acquisition, project administration.

Corresponding authors

Correspondence to Chunfeng Wang or Guilian Yang.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 68 KB)

Supplementary file2 (XLSX 12 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, D., Li, MH., Pan, T. et al. Preventive and Therapeutic Potential of Streptococcus cristatus CA119 in Experimental Periodontitis in Rats. Probiotics & Antimicro. Prot. (2024). https://doi.org/10.1007/s12602-024-10254-y

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12602-024-10254-y

Keywords

Search

Navigation