Comparison Between Different Delivery Vehicles for the Probiotic Bifidobacterium animalis subsp. lactis HN019 on Experimental Periodontitis in Rats.
Milk
Periodontitis
Probiotic
Rats
Water
Journal
Probiotics and antimicrobial proteins
ISSN: 1867-1314
Titre abrégé: Probiotics Antimicrob Proteins
Pays: United States
ID NLM: 101484100
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
accepted:
11
02
2022
pubmed:
10
3
2022
medline:
21
4
2022
entrez:
9
3
2022
Statut:
ppublish
Résumé
This study aimed to assess the effects of the probiotic (PROB) Bifidobacterium animalis subsp. lactis HN019 in two different delivery vehicles in experimental periodontitis (EP), including the gene expression for IL-10, IFN-γ, and FOXP3. In total, 32 rats were assigned into groups (n=8): C (control), EP, EP-PROB/Water, and EP-PROB/Milk. The probiotic was administered for 4 weeks, from baseline to euthanasia. Periodontitis was induced by ligatures 14 days after baseline. Data were statistically analyzed (p<0.05). Both probiotic groups presented decreased alveolar bone loss and increased interproximal attachment level than group EP. Also, these parameters were significantly improved in the Milk group when compared with the Water group. EP-PROB/Milk showed higher gene expression for IL-10 and lower for FOXP3 in relation to EP-PROB/Water and EP groups. The use of milk was able to potentiate the protective effects of B. lactis HN019 in rats under EP.
Identifiants
pubmed: 35260963
doi: 10.1007/s12602-022-09930-8
pii: 10.1007/s12602-022-09930-8
doi:
Substances chimiques
Forkhead Transcription Factors
0
Water
059QF0KO0R
Interleukin-10
130068-27-8
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
313-325Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJ, Marcenes W (2014) Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression. J Dent Res 93(11):1045–1053. https://doi.org/10.1177/0022034514552491
doi: 10.1177/0022034514552491
Raitapuro-Murray T, Molleson TI, Hughes FJ (2014) The prevalence of periodontal disease in a Romano-British population c. 200-400 AD. Br Dent J 217(8):459–466. https://doi.org/10.1038/sj.bdj.2014.908
Hajishengallis G (2015) Periodontitis: from microbial immune subversion to systemic inflammation. Nature reviews. Immunology 15(1):30–44. https://doi.org/10.1038/nri3785
doi: 10.1038/nri3785
Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet (London, England) 366(9499):1809–1820. https://doi.org/10.1016/S0140-6736(05)67728-87
doi: 10.1016/S0140-6736(05)67728-87
Suvan JE (2005) Effectiveness of mechanical nonsurgical pocket therapy. Periodontology 2000(37):48–71. https://doi.org/10.1111/j.1600-0757.2004.03794.x
doi: 10.1111/j.1600-0757.2004.03794.x
Berezow AB, Darveau RP (2011) Microbial shift and periodontitis. Periodontology 2000 55(1):36–47. https://doi.org/10.1111/j.1600-0757.2010.00350.x
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66
Kumar PS, Leys EJ, Bryk JM, Martinez FJ, Moeschberger ML, Griffen AL (2006) Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 44(10):3665–3673. https://doi.org/10.1128/JCM.00317-06
doi: 10.1128/JCM.00317-06
Bermudez-Brito M, Muñoz-Quezada S, Gomez-Llorente C, Matencio E, Bernal MJ, Romero F, Gil A (2012) Human intestinal dendritic cells decrease cytokine release against Salmonella infection in the presence of Lactobacillus paracasei upon TLR activation. PloS One 7(8):e43197. https://doi.org/10.1371/journal.pone.0043197
Invernici MM, Salvador SL, Silva P, Soares M, Casarin R, Palioto DB, Souza S, Taba M Jr, Novaes AB Jr, Furlaneto F, Messora MR (2018) Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: a randomized clinical trial. J Clin Periodontol 45(10):1198–1210. https://doi.org/10.1111/jcpe.12995
doi: 10.1111/jcpe.12995
Invernici MM, Furlaneto F, Salvador SL, Ouwehand AC, Salminen S, Mantziari A, Vinderola G, Ervolino E, Santana SI, Silva P, Messora MR (2020) Bifidobacterium animalis subsp lactis HN019 presents antimicrobial potential against periodontopathogens and modulates the immunological response of oral mucosa in periodontitis patients. PloS One 15(9):e0238425. https://doi.org/10.1371/journal.pone.0238425
İnce G, Gürsoy H, İpçi ŞD, Cakar G, Emekli-Alturfan E, Yılmaz S (2015) Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol 86(6):746–754. https://doi.org/10.1902/jop.2015.140612
doi: 10.1902/jop.2015.140612
Shah MP, Gujjari SK, Chandrasekhar VS (2013) Evaluation of the effect of probiotic (inersan®) alone, combination of probiotic with doxycycline and doxycycline alone on aggressive periodontitis - a clinical and microbiological study. Journal of clinical and diagnostic research : JCDR 7(3):595–600. https://doi.org/10.7860/JCDR/2013/5225.2834
doi: 10.7860/JCDR/2013/5225.2834
Teughels W, Durukan A, Ozcelik O, Pauwels M, Quirynen M, Haytac MC (2013) Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: a randomized placebo-controlled study. J Clin Periodontol 40(11):1025–1035. https://doi.org/10.1111/jcpe.12155
doi: 10.1111/jcpe.12155
Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, Yılmaz S (2015) Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol 42(4):363–372. https://doi.org/10.1111/jcpe.12387
doi: 10.1111/jcpe.12387
Vivekananda MR, Vandana KL, Bhat KG (2010) Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. J Oral Microbiol 2. https://doi.org/10.3402/jom.v2i0.5344
Ikram S, Hassan N, Raffat MA, Mirza S, Akram Z (2018) Systematic review and meta-analysis of double-blind, placebo-controlled, randomized clinical trials using probiotics in chronic periodontitis. J Investig Clin Dent 9(3):e12338. https://doi.org/10.1111/jicd.12338
Martin-Cabezas R, Davideau JL, Tenenbaum H, Huck O (2016) Clinical efficacy of probiotics as an adjunctive therapy to non-surgical periodontal treatment of chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol 43(6):520–530. https://doi.org/10.1111/jcpe.12545
doi: 10.1111/jcpe.12545
Vives-Soler A, Chimenos-Küstner E (2020) Effect of probiotics as a complement to non-surgical periodontal therapy in chronic periodontitis: a systematic review. Med Oral Patol Oral Cir Bucal 25(2):e161–e167. https://doi.org/10.4317/medoral.23147
doi: 10.4317/medoral.23147
Donos N, Calciolari E, Brusselaers N, Goldoni M, Bostanci N, Belibasakis GN (2020) The adjunctive use of host modulators in non-surgical periodontal therapy. A systematic review of randomized, placebo-controlled clinical studies. J Clin Periodontol 47(22):199–238. https://doi.org/10.1111/jcpe.13232
Matsubara VH, Bandara HM, Ishikawa KH, Mayer MP, Samaranayake LP (2016) The role of probiotic bacteria in managing periodontal disease: a systematic review. Expert Rev Anti Infect Ther 14(7):643–655. https://doi.org/10.1080/14787210.2016.1194198
doi: 10.1080/14787210.2016.1194198
Teughels W, Loozen G, Quirynen M (2011) Do probiotics offer opportunities to manipulate the periodontal oral microbiota?. J Clin Periodontol 38(Suppl 11):159–177. https://doi.org/10.1111/j.1600-051X.2010.01665.x
doi: 10.1111/j.1600-051X.2010.01665.x
Teughels W, Feres M, Oud V, Martín C, Matesanz P, Herrera D (2020) Adjunctive effect of systemic antimicrobials in periodontitis therapy: a systematic review and meta-analysis. J Clin Periodontol 47(Suppl 22):257–281. https://doi.org/10.1111/jcpe.13264
doi: 10.1111/jcpe.13264
Sanders ME, Marco ML (2010) Food formats for effective delivery of probiotics. Annu Rev Food Sci Technol 1:65–85. https://doi.org/10.1146/annurev.food.080708.100743
doi: 10.1146/annurev.food.080708.100743
Sanders ME, Klaenhammer TR, Ouwehand AC, Pot B, Johansen E, Heimbach JT, Marco ML, Tennilä J, Ross RP, Franz C, Pagé N, Pridmore RD, Leyer G, Salminen S, Charbonneau D, Call E, Lenoir-Wijnkoop I (2014) Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics. Ann N Y Acad Sci 1309:1–18. https://doi.org/10.1111/nyas.12363
doi: 10.1111/nyas.12363
Senaka Ranadheera C, Evans CA, Adams MC, Baines SK (2012) In vitro analysis of gastrointestinal tolerance and intestinal cell adhesion of probiotics in goat’s milk ice cream and yogurt. Food Res Int 49(2):619–625. https://doi.org/10.1016/j.foodres.2012.09.007
doi: 10.1016/j.foodres.2012.09.007
Ranadheera RDCS, Baines SK, Adams MC (2010) Importance of food in probiotic efficacy. Food Res Int 43:1–7. https://doi.org/10.1016/j.foodres.2009.09.009
doi: 10.1016/j.foodres.2009.09.009
Johnson IH (1975) Effects of local irritation and dextran sulphate administration on the periodontium of the rat. J Periodontal Res 10(6):332–345. https://doi.org/10.1111/j.1600-0765.1975.tb00042
doi: 10.1111/j.1600-0765.1975.tb00042
Marchesan J, Girnary MS, Jing L, Miao MZ, Zhang S, Sun L, Morelli T, Schoenfisch MH, Inohara N, Offenbacher S, Jiao Y (2018) An experimental murine model to study periodontitis. Nat Protoc 13(10):2247-2267. https://doi.org/10.1038/s41596-018-0035-4
Abe T, Hajishengallis G (2013) Optimization of the ligature-induced periodontitis model in mice. J Immunol Methods 394:49–54. https://doi.org/10.1016/j.jim.2013.05.002
doi: 10.1016/j.jim.2013.05.002
Oliveira LF, Salvador SL, Silva PH, Furlaneto FA, Figueiredo L, Casarin R, Ervolino E, Palioto DB, Souza SL, Taba Jr M, Novaes Jr AB, Messora MR (2017) Benefits of Bifidobacterium animalis subsp. lactis probiotic in experimental periodontitis. J Periodontol 88(2):197–208. https://doi.org/10.1902/jop.2016.160217
Jäsberg H, Söderling E, Endo A, Beighton D, Haukioja A (2016) Bifidobacteria inhibit the growth of Porphyromonas gingivalis but not of Streptococcus mutans in an in vitro biofilm model. Eur J Oral Sci 124(3):251–258. https://doi.org/10.1111/eos.12266
doi: 10.1111/eos.12266
Panesar P (2011) Fermented dairy products: starter cultures and potential nutritional benefits. Food Nutr Sci 2(1):47–51. https://doi.org/10.4236/fns.2011.21006
doi: 10.4236/fns.2011.21006
Ricoldi M, Furlaneto F, Oliveira L, Teixeira GC, Pischiotini JP, Moreira A, Ervolino E, de Oliveira MN, Bogsan C, Salvador SL, Messora MR (2017) Effects of the probiotic Bifidobacterium animalis subsp. lactis on the non-surgical treatment of periodontitis. A histomorphometric, microtomographic and immunohistochemical study in rats. PloS One 12(6):e0179946. https://doi.org/10.1371/journal.pone.0179946
Barouei J, Moussavi M, Hodgson DM (2012) Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PloS One 7(10):e46051. https://doi.org/10.1371/journal.pone.0046051
Cardoso RS, Messora MR, Silva P, Oliveira LF, Leite-Panissi C, Salvador S, Casarin R, Novaes Jr AB, Palioto DB, Furlaneto F (2020) Effects of Bifidobacterium animalis subsp. lactis HN019 on ligature-induced periodontitis in rats with experimental rheumatoid arthritis. Benefic Microbes 11(1):33–46. https://doi.org/10.3920/BM2019.0038
Lisboa MR, Gondim DV, Ervolino E, Vale ML, Frota NP, Nunes NL, Mariguela VC, Taba M Jr, Messora MR, Furlaneto FA (2015) Effects of electroacupuncture on experimental periodontitis in rats. J Periodontol 86(6):801–11. https://doi.org/10.1902/jop.2015.140630 (Epub 2015 Mar 5 PMID:25741581)
doi: 10.1902/jop.2015.140630
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G (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(8):491–502. https://doi.org/10.1038/nrgastro.2017.75
doi: 10.1038/nrgastro.2017.75
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods (San Diego, Calif) 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Iniesta M, Herrera D, Montero E, Zurbriggen M, Matos AR, Marín MJ, Sanz M (2012) Probiotic effects of orally administered Lactobacillus reuteri‐containing tablets on the subgingival and salivary microbiota in patients with gingivitis. A randomized clinical trial. J Clin Periodontol 39(8):736–744. https://doi.org/10.1111/j.1600-051X.2012.01914.x
Mottet C, Michetti P (2005) Probiotics: wanted dead or alive. Dig Liver Dis 37(1):3–6. https://doi.org/10.1016/j.dld.2004.09.010 PMID:15702852
McNulty NP, Yatsunenko T, Hsiao A, Faith JJ, Muegge BD, Goodman AL, Henrissat B, Oozeer R, Cools-Portier S, Gobert G, Chervaux C, Knights D, Lozupone CA, Knight R, Duncan AE, Bain JR, Muehlbauer MJ, Newgard CB, Heath AC, Gordon JI (2011) The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 3(106):106ra106. https://doi.org/10.1126/scitranslmed.3002701
Khasenbekova Z, Saduakhasova S, Gulayev A, Kushugulova A, Kozhakhmetov S, Shakhabayeva G, Tynybayeva I, Nurgozhin T, Zhumadilov Z (2014) Effect of Probiotic consortium on the local inflammatory process in chronic periodontitis. Cent Asian J Glob Health 2(Suppl):109. https://doi.org/10.5195/cajgh.2013.109
Penala S, Kalakonda B, Pathakota KR, Jayakumar A, Koppolu P, Lakshmi BV, Pandey R, Mishra A (2016) Efficacy of local use of probiotics as an adjunct to scaling and root planing in chronic periodontitis and halitosis: a randomized controlled trial. J Res Pharm Pract 5(2):86–93. https://doi.org/10.4103/2279-042X.179568
doi: 10.4103/2279-042X.179568
Ikram S, Hassan N, Baig S, Borges KJJ, Raffat MA, Akram Z (2019) Effect of local probiotic (Lactobacillus reuteri) vs systemic antibiotic therapy as an adjunct to non-surgical periodontal treatment in chronic periodontitis. J Investig Clin Dent 10(2):e12393. https://doi.org/10.1111/jicd.12393 (PMID:30663271)
Minić I, Pejčić A, Bradić-Vasić M (2021) Effect of the local probiotics in the therapy of periodontitis. A randomized prospective study. Int J Dent Hyg 8. https://doi.org/10.1111/idh.12509
Ruiz L, Ruas-Madiedo P, Gueimonde M, de Los Reyes-Gavilán CG, Margolles A, Sánchez B (2011) How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences. Genes Nutr 6(3):307–318. https://doi.org/10.1007/s12263-010-0207-5
doi: 10.1007/s12263-010-0207-5
Fontana L, Bermudez-Brito M, Plaza-Diaz J, Muñoz-Quezada S, Gil A (2013) Sources, isolation, characterisation and evaluation of probiotics. Br J Nutr 109(Suppl 2):S35–S50. https://doi.org/10.1017/S0007114512004011
doi: 10.1017/S0007114512004011
Flach J, van der Waal MB, van den Nieuwboer M, Claassen E, Larsen O (2018) The underexposed role of food matrices in probiotic products: reviewing the relationship between carrier matrices and product parameters. Crit Rev Food Sci Nutr 58(15):2570–2584. https://doi.org/10.1080/10408398.2017.1334624
doi: 10.1080/10408398.2017.1334624
Burgain J, Scher J, Francius G, Borges F, Corgneau M, Revol-Junelles AM, Cailliez-Grimal C, Gaiani C (2014) Lactic acid bacteria in dairy food: surface characterization and interactions with food matrix components. Adv Colloid Interface Sci 213:21–35. https://doi.org/10.1016/j.cis.2014.09.00
doi: 10.1016/j.cis.2014.09.00
Lee B, Yin X, Griffey SM, Marco ML (2015) Attenuation of colitis by Lactobacillus casei BL23 is dependent on the dairy delivery matrix. Appl Environ Microbiol 81(18):6425–6435. https://doi.org/10.1128/AEM.01360-15
doi: 10.1128/AEM.01360-15
Azcarate-Peril MA, Tallon R, Klaenhammer TR (2009) Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J Dairy Sci 92(3):870–886. https://doi.org/10.3168/jds.2008-1457
doi: 10.3168/jds.2008-1457
Gomand F, Borges F, Burgain J, Guerin J, Revol-Junelles AM, Gaiani C (2019) Food matrix design for effective lactic acid bacteria delivery. Annu Rev Food Sci Technol 10:285–310. https://doi.org/10.1146/annurev-food-032818-121140
doi: 10.1146/annurev-food-032818-121140
Bove P, Russo P, Capozzi V, Gallone A, Spano G, Fiocco D (2013) Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: carrier matrix effect and transcriptional analysis of genes associated to stress and probiosis. Microbiol Res 168(6):351–359. https://doi.org/10.1016/j.micres.2013.01.004
doi: 10.1016/j.micres.2013.01.004
Saarela M, Virkajärvi I, Alakomi HL, Sigvart-Mattila P, Mättö J (2006) Stability and functionality of freeze-dried probiotic Bifidobacterium cells during storage in juice and milk. Int Dairy J 16:1477–1482. https://doi.org/10.1016/j.idairyj.2005.12.007
Valerio F, De Bellis P, Lonigro SL, Morelli L, Visconti A, Lavermicocca P (2006) In vitro and in vivo survival and transit tolerance of potentially probiotic strains carried by artichokes in the gastrointestinal tract. Appl Environ Microbiol 72(4):3042–3045. https://doi.org/10.1128/AEM.72.4.3042-3045.2006
doi: 10.1128/AEM.72.4.3042-3045.2006
Bernini LJ, Simão AN, Alfieri DF, Lozovoy MA, Mari NL, de Souza CH, Dichi I, Costa GN (2016) Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: a randomized trial. Effects of probiotics on metabolic syndrome. Nutrition (Burbank, Los Angeles County, Calif) 32(6):716–719. https://doi.org/10.1016/j.nut.2015.11.001
Vinderola G, Zacarías MF, Bockelmann W, Neve H, Reinheimer J, Heller KJ (2012) Preservation of functionality of Bifidobacterium animalis subsp. lactis INL1 after incorporation of freeze-dried cells into different food matrices. Food Microbiol 30(1):274–280. https://doi.org/10.1016/j.fm.2011.12.004
Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84(5):759–768. https://doi.org/10.1046/j.1365-2672.1998.00407.x
doi: 10.1046/j.1365-2672.1998.00407.x
Arunachalam K, Gill HS, Chandra RK (2000) Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr 54(3):263–267. https://doi.org/10.1038/sj.ejcn.1600938
doi: 10.1038/sj.ejcn.1600938
de Vrese M, Kristen H, Rautenberg P, Laue C, Schrezenmeir J (2011) Probiotic lactobacilli and bifidobacteria in a fermented milk product with added fruit preparation reduce antibiotic associated diarrhea and Helicobacter pylori activity. J Dairy Res 78(4):396–403. https://doi.org/10.1017/S002202991100063X
doi: 10.1017/S002202991100063X
He Y, Lawlor NT, Newburg DS (2016) Human milk components modulate toll-like receptor-mediated inflammation. 7:102–111. https://doi.org/10.3945/an.115.010090
Saad N, Delattre C, Urdaci M, Schmitter JM, Bressollier P (2013) An overview of the last advances in probiotic and prebiotic field. LWT- Food Sci Technol 50:1–16. https://doi.org/10.1016/j.lwt.2012.05.014
doi: 10.1016/j.lwt.2012.05.014
de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111:1–66. https://doi.org/10.1007/10_2008_097
doi: 10.1007/10_2008_097
Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133(5):775–787. https://doi.org/10.1016/j.cell.2008.05.009
doi: 10.1016/j.cell.2008.05.009
Han YK, Jin Y, Miao YB, Shi T, Lin XP (2018) CD8+ Foxp3+ T cells affect alveolar bone homeostasis via modulating Tregs/Th17 during induced periodontitis: an adoptive transfer experiment. Inflammation 41(5):1791–1803. https://doi.org/10.1007/s10753-018-0822-7
doi: 10.1007/s10753-018-0822-7
Okui T, Aoki Y, Ito H, Honda T, Yamazaki K (2012) The presence of IL-17+/FOXP3+ double-positive cells in periodontitis. J Dental Res 91(6):574–579. https://doi.org/10.1177/0022034512446341
doi: 10.1177/0022034512446341
Dutzan N, Gamonal J, Silva A, Sanz M, Vernal R (2009) Over-expression of forkhead box P3 and its association with receptor activator of nuclear factor-kappa B ligand, interleukin (IL) -17, IL-10 and transforming growth factor-beta during the progression of chronic periodontitis. J Clin Periodontol 36(5):396–403. https://doi.org/10.1111/j.1600-051X.2009.01390.x
doi: 10.1111/j.1600-051X.2009.01390.x
Čitar M, Hacin B, Tompa G, Štempelj M, Rogelj I, Dolinšek J, Narat M, Matijašić BB (2015) Human intestinal mucosa-associated Lactobacillus and Bifidobacterium strains with probiotic properties modulate IL-10, IL-6 and IL-12 gene expression in THP-1 cells. Benefic Microbes 6(3):325–336. https://doi.org/10.3920/BM2014.0081
doi: 10.3920/BM2014.0081
Teles RP, Gursky LC, Faveri M, Rosa EA, Teles FR, Feres M, Socransky SS, Haffajee AD (2010) Relationships between subgingival microbiota and GCF biomarkers in generalized aggressive periodontitis. J Clin Periodontol 37(4):313–323. https://doi.org/10.1111/j.1600-051X.2010.01534.x
doi: 10.1111/j.1600-051X.2010.01534.x
Nagasawa T, Kiji M, Yashiro R, Hormdee D, Lu H, Kunze M, Suda T, Koshy G, Kobayashi H, Oda S, Nitta H, Ishikawa I (2007) Roles of receptor activator of nuclear factor-kappaB ligand (RANKL) and osteoprotegerin in periodontal health and disease. Periodontology 2000(43):65–84. https://doi.org/10.1111/j.1600-0757.2006.00185.x
doi: 10.1111/j.1600-0757.2006.00185.x
Fiorillo L, Cervino G, Herford AS, Lauritano F, D’Amico C, Lo Giudice R, Laino L, Troiano G, Crimi S, Cicciù M (2018) Interferon crevicular fluid profile and correlation with periodontal disease and wound healing: a systemic review of recent data. Int J Mol Sci 19(7):1908. https://doi.org/10.3390/ijms19071908
doi: 10.3390/ijms19071908
So JS, Song MK, Kwon HK, Lee CG, Chae CS, Sahoo A, Jash A, Lee SH, Park ZY, Im SH (2011) Lactobacillus casei enhances type II collagen/glucosamine-mediated suppression of inflammatory responses in experimental osteoarthritis. Life Sci 88(7–8):358–366. https://doi.org/10.1016/j.lfs.2010.12.013
doi: 10.1016/j.lfs.2010.12.013
Drakes M, Blanchard T, Czinn S (2004) Bacterial probiotic modulation of dendritic cells. Infect Immun 72(6):3299–3309. https://doi.org/10.1128/IAI.72.6.3299-3309.2004
doi: 10.1128/IAI.72.6.3299-3309.2004
Kuru BE, Laleman I, Yalnızoğlu T, Kuru L, Teughels W (2017) The influence of a Bifidobacterium animalis probiotic on gingival health: a randomized controlled clinical trial. J Periodontol 88(11):1115–1123. https://doi.org/10.1902/jop.2017.170213
doi: 10.1902/jop.2017.170213
Akram Z, Shafqat SS, Aati S, Kujan O, Fawzy A (2020) Clinical efficacy of probiotics in the treatment of gingivitis: a systematic review and meta-analysis. Aust Dent J 65(1):12–20. https://doi.org/10.1111/adj.12733 . Epub 2019 Nov 29