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Effect of adjuvant probiotic therapy (Lactobacillus reuteri) in the treatment of periodontitis associated with diabetes mellitus: clinical, controlled, and randomized study

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Abstract

Objectives

Subgingival instrumentation (SI) with probiotics may be a proposal for the treatment of periodontitis (P), for patients with type 2 diabetes mellitus (T2DM). The Lactobacillus reuteri probiotic as an adjunctive therapy in the treatment of P associated with T2DM was evaluated.

Materials and methods

Forty diabetic participants diagnosed with P (stage III and IV, grade B) were randomized into SI + Placebo (n = 20): subgingival instrumentation plus placebo lozenges and SI + Probi (n = 20): subgingival instrumentation plus probiotics. Probing depth (PD), gingival recession (GR), clinical attachment level (CAL), plaque index (PI), bleeding on probing (BoP), and PISA index were performed at baseline and 30, 90, and 180 days. Cytokine concentration in the gingival crevicular fluid, subgingival biofilm sample, and LDL and HDL subfractions were evaluated.

Results

In the deep pockets, PD in SI + Probi showed increased values (p = 0.02) compared to SI + Placebo at 90 days. For CAL, SI + Probi showed increased values compared to SI + Placebo, with a significant difference at 30 days (p = 0.03), 90 days (p = 0.02), and 180 days (p = 0.04). At #PD ≥ 7 mm, SI + Probi had a more frequent number of sites (p = 0.03) compared to SI + Placebo only at baseline. For the PISA, SI + Probi showed a significant difference (p = 0.04) compared to SI + Placebo at 90 days. For cytokines, SI + Probi showed higher quantification than SI + Placebo for IL-10 (p < 0.001) at 90 days, IL-12 (p = 0.010) at 90 days, IL-1β (p = 0.035) at 90 days, and IL-8 (p = 0.003) at baseline. SI + Placebo showed higher quantification of IL-1β (p = 0.041) compared to SI + Probi only at 30 days. There was a reduction in all microbial complexes. SI + Probi improved LDL size (246.7 nm vs 260.4 nm; p < 0.001), while large HDL subfractions were reduced aft 180 days of treatment (24.0% vs 20.3%; p = 0.022) when compared with SI + Placebo; this response was dependent of probiotics (1.0 mg/dL vs − 6.2 mg/dL; p = 0.002).

Conclusion

Subgingival instrumentation improved the clinical periodontal parameters in patients with T2DM. The use of L. reuteri probiotics had no additional effects compared with the placebo; however, there was a positive effect on the lipoprotein subfraction.

Clinical relevance

Scientific rationale for study: subgingival instrumentation with probiotics may be a proposal for the treatment of periodontitis (P), especially for patients with type 2 diabetes mellitus (T2DM). Principal findings: the use of L. reuteri probiotics had no additional effects compared with the placebo; however, there was a positive effect on the lipoprotein subfraction. 

Practical implications: L. reuteri as an adjunct to subgingival instrumentation may have significant therapeutic implications in dyslipidemia.

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Data Availability

The data that support the findings of this study are available on request from the corresponding author, [MANJ]. The data are not publicly available due to their containing information that could compromise the privacy of research participants.

References

  1. Brugués A, Bromuri S, Barry M, Del Toro ÓJ, Mazurkiewicz MR, Kardas P, Pegueroles J, Schumacher M (2016) Processing diabetes mellitus composite events in MAGPIE. J Med Syst 40(2):44. https://doi.org/10.1007/s10916-015-0377-1

    Article  PubMed  Google Scholar 

  2. Cervino G, Terranova A, Briguglio F, De Stefano R, Fama` F, D’Amico C et al (2019) Diabetes: oral health related quality of life and oral alterations Biomed Res Int. https://doi.org/10.1155/2019/5907195

  3. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 286(3):327–34. https://doi.org/10.1001/jama.286.3.327

    Article  PubMed  CAS  Google Scholar 

  4. Taylor JJ, Preshaw PM, Lalla E (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 40(Suppl 14):S113–S134. https://doi.org/10.1111/jcpe.12059

    Article  PubMed  Google Scholar 

  5. Marruganti C, Suvan JE, D'Aiuto F (2023) Periodontitis and metabolic diseases (diabetes and obesity): tackling multimorbidity. Periodontol 2000:16. https://doi.org/10.1111/prd.12536. Online ahead of print

  6. Hariharan R, Odjidja EN, Scott D, Shivappa N, Hébert JR, Hodge A, de Courten B (2022) The dietary inflammatory index, obesity, type 2 diabetes, and cardiovascular risk factors and diseases. Obes Rev. 23(1):e13349. https://doi.org/10.1111/obr.13349

    Article  PubMed  CAS  Google Scholar 

  7. Brazilian Diabetes Society (BSD) (2017) Brazilian Diabetes Society guidelines:2017–2018. Clannad, São Paulo

    Google Scholar 

  8. Scott R, Donoghoe M, Watts GF, O’Brien R, Pardy C, Taskinen MR, Davis TM, Colman PG, Manning P, Fulcher G, Keech AC, FIELD Study Investigators (2011) Impact of metabolic syndrome and its components on cardiovascular disease event rates in 4900 patients with type 2 diabetes assigned to placebo in the FIELD randomised trial. Cardiovasc Diabetol. 10:102. https://doi.org/10.1186/1475-2840-10-102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Dentino A, Lee S, Mailhot J, Hefti AF (2013) Principles of periodontology. Periodontol 61(1):16–53. https://doi.org/10.1111/j.1600-0757.2011.00397.x

    Article  Google Scholar 

  10. Khanuja PK, Narula SC, Rajput R, Sharma RK, Tewari S (2017) Association of periodontal disease with glycemic control in patients with type2 diabetes in Indian population. Front Med. https://doi.org/10.1007/s11684-016-0484-5

  11. Acharya AB, Thakur S, Muddapur MV (2015) Effect of scaling and root planing on serum interleukin-10 levels and glycemic control in chronic periodontitis and type 2 diabetes mellitus. J Indian Soc Periodontol Mar-Apr 19(2):188–193. https://doi.org/10.4103/0972-124X.148644

    Article  Google Scholar 

  12. Bascones-Martinez A, Matesanz-Perez P, Escribano-Bermejo M, González- Moles MÁ, Bascones-Ilundain J, Meurman JH (2011) Periodontal disease and diabetes- review of the literature. Med Oral Patol Oral Cir Bucal 16(6):e722-729. https://doi.org/10.4317/medoral.17032

    Article  PubMed  Google Scholar 

  13. Frencken JE, Sharma P, Stenhouse L, Green D, Laverty D, Dietrich T (2017) Global epidemiology of dental caries and severe periodontitis–a comprehensive review. J Clin Periodontol 44:S94–S105. https://doi.org/10.1111/jcpe.12677

    Article  PubMed  Google Scholar 

  14. Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, Herrera D, Jepsen S, Lione L, Madianos P, Mathur M, Montanya E, Shapira L, Tonetti M, Vegh D (2018) Scientific evidence on the links between periodontal diseases and diabetes: consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol 45(2):138–149. https://doi.org/10.1111/jcpe.12808

    Article  PubMed  CAS  Google Scholar 

  15. Miranda TS, Feres M, Retamal-Valdés B, Perez-Chaparro PJ, Maciel SS, Duarte PM (2017) Influence of glycemic control on the levels of subgingival periodontal pathogens in patients with generalized chronic periodontitis and type 2 diabetes. J Appl Oral Sci 25(1):82–89. https://doi.org/10.1590/167877572016-0302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Aemaimanan P, Amimanan P, Taweechaisupapong S (2013) Quantification of key periodontal pathogens in insulin-dependent type 2 diabetic and non-diabetic patients with generalized chronic periodontitis. Anaerobe 22:64–8. https://doi.org/10.1016/j.anaerobe.2013.06.010

    Article  PubMed  CAS  Google Scholar 

  17. Kurgan S (2000) Kantarci A (2018) Molecular basis for immunohistochemical and inflammatory changes during progression of gingivitis to periodontitis. Periodontol 76(1):51–67. https://doi.org/10.1111/prd.12146. (Epub 2017 Nov 29)

    Article  Google Scholar 

  18. Mizutani K, Park K, Mima A, Katagiri S, King GL (2014) Obesity-associated gingival vascular inflammation and insulin resistance. J Dent Res 93(6):596–601. https://doi.org/10.1177/0022034514532102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Jain N, Jain GK, Javed S, Iqbal Z, Talegaonkar S, Ahmad FJ, Khar RK (2008) Recent approaches for the treatment of periodontitis. Drug Discov Today 13(21–22):932–43. https://doi.org/10.1016/j.drudis.2008.07.010

    Article  PubMed  CAS  Google Scholar 

  20. Darby I (2000) (2022) Risk factors for periodontitis & peri-implantitis. Periodontol 90(1):9–12. https://doi.org/10.1111/prd.12447

    Article  Google Scholar 

  21. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ (2001) De Nardin E (2001) Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 72(9):1221–1227. https://doi.org/10.1902/jop.2000.72.9.1221

    Article  PubMed  CAS  Google Scholar 

  22. Pirih FQ, Monajemzadeh S, Singh N, Sinacola RS, Shin JM, Chen T, Fenno JC, Kamarajan P, Rickard AH, Travan S, Paster BJ (2000) Kapila Y (2021) Association between metabolic syndrome and periodontitis: the role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontol 87(1):50–75. https://doi.org/10.1111/prd.12379

    Article  Google Scholar 

  23. Kobayashi Y, Niu K, Guan L, Momma H, Guo H, Cui Y, Nagatomi R (2012) Oral health behavior and metabolic syndrome and its components in adults. J Dent Res 91(5):479–84. https://doi.org/10.1177/0022034512440707

    Article  PubMed  CAS  Google Scholar 

  24. D’Aiuto F, Sabbah W, Netuveli G, Donos N, Hingorani AD, Deanfield J (2008) Tsakos G (2008) Association of the metabolic syndrome with severe periodontitis in a large U.S. population-based survey. J Clin Endocrinol Metab 93(10):3989–94. https://doi.org/10.1210/jc.2007-2522

    Article  PubMed  CAS  Google Scholar 

  25. Lotfollahi Z, Mello APQ, Costa ES, Oliveira CLP, Damasceno NRT, Izar MC, Neto AMF (2020) Green-banana biomass consumption by diabetic patients improves plasma low-density lipoprotein particle functionality. Sci Rep 10(1):12269. https://doi.org/10.1038/s41598-020-69288-1

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  26. Lotfollahi Z, Mello APQ, Fonseca FAH, Machado LO, Mathias AF, Izar MC, Damasceno NRT, Oliveira CLP, Neto AMF (2022) Changes in lipoproteins associated with lipid-lowering and antiplatelet strategies in patients with acute myocardial infarction. PLoS One 17(8):e0273292. https://doi.org/10.1371/journal.pone.0273292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Kontush A (2014) HDL-mediated mechanisms of protection in cardiovascular disease. Cardiovasc Res 103(3):341–9. https://doi.org/10.1093/cvr/cvu147

    Article  PubMed  CAS  Google Scholar 

  28. Kontush A, Chapman MJ (2010) Antiatherogenic function of HDL particle subpopulations: focus on antioxidative activities. Curr Opin Lipidol 21(4):312–8. https://doi.org/10.1097/MOL.0b013e32833bcdc1

    Article  PubMed  CAS  Google Scholar 

  29. Dias GD, Cartolano FC, Freitas MCP, Santa-Helena E, Markus MRP, Santos RD, Damasceno NRT (2021) Adiponectin predicts the antioxidant capacity and size of high-density lipoprotein (HDL) in individuals with diabetes mellitus. J Diabetes Complications 35(5):107856. https://doi.org/10.1016/j.jdiacomp.2021.107856

    Article  PubMed  CAS  Google Scholar 

  30. Nibali L, Rizzo M, Li Volti G, D’Aiuto F, Giglio RV, Barbagallo I, Pelekos G, Donos N (2015) Lipid subclasses profiles and oxidative stress in aggressive periodontitis before and after treatment. J Periodontal Res 50(6):890–6. https://doi.org/10.1111/jre.12283

    Article  PubMed  CAS  Google Scholar 

  31. Pamuk F, Kantarci A (2022) Inflammation as a link between periodontal disease and obesity. Periodontol 2000 90(1):186–196. https://doi.org/10.1111/prd.12457

    Article  PubMed  Google Scholar 

  32. Sanz M, Herrera D, Kebschull M, Chapple I, Jepsen S, Beglundh T, Sculean A, Tonetti MS (2020) EFP Workshop Participants and Methodological Consultants. Treatment of stage I-III periodontitis-the EFP S3 level clinical practice guideline. J Clin Periodontol 47 Suppl 22(Suppl 22):4–60. https://doi.org/10.1111/jcpe.13290. Erratum in: J Clin Periodontol. 2021 Jan;48(1):163

  33. Stamatova I (2000) Meurman JH (2009) Probiotics and periodontal disease. Periodontol 51:141–151. https://doi.org/10.1111/j.1600-0757.2009.00305.x

    Article  Google Scholar 

  34. Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksen- Blicks C (2009) Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand 67:19–24. https://doi.org/10.1080/00016350802516170

    Article  PubMed  CAS  Google Scholar 

  35. Slawik S, Staufenbiel I, Schilke R, Nicksch S, Weinspach K, Stiesch M et al (2011) (2011) Probiotics affect the clinical inflammatory parameters of experimental gingivitis in humans. Eur J ClinNutr 65:857–863. https://doi.org/10.1038/ejcn.2011.45

    Article  CAS  Google Scholar 

  36. Szkaradkiewicz AK, Stopa J, Karpiński TM (2014) Effect of oral administration involving a probiotic strain of Lactobacillus reuteri on pro-inflammatory cytokineresponse in patients with chronic periodontitis. Arch ImmunolTherExp (Warsz) 62:495–500. https://doi.org/10.1007/s00005-014-0277-y

    Article  CAS  Google Scholar 

  37. Tekce M, Ince G, Gursoy H, DirikanIpci S, Cakar G, Kadir T et al (2015) Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol 42:363–372. https://doi.org/10.1111/jcpe.12387

    Article  PubMed  Google Scholar 

  38. Vicario M, Santos A, Violant D, Nart J, Giner L (2013) Clinical changes in periodontal subjects with the probiotic Lactobacillus reuteri Prodentis: a preliminar randomized clinical trial. Acta Odontol Scand 71:813–819. https://doi.org/10.3109/00016357.2012.734404

    Article  PubMed  Google Scholar 

  39. Vivekananda MR, Vandana KL, Bhat KG (2010) Lactobacilus reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. J Oral Microbiol 2:2. https://doi.org/10.3402/jom.v2i0.5344

    Article  Google Scholar 

  40. 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. J Clin Diagn Res 7:595–600. https://doi.org/10.7860/JCDR/2013/5225.2834

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hallström H, Lindgren S, Yucel-Lindberg T, Dahlén G, Renvert S, Twetman S (2013) Effect of probiotic lozenges on inflammatory reactions and oral biofilm during experimental gingivitis. Acta Odontol Scand 71:828–833. https://doi.org/10.3109/00016357.2012.734406

    Article  PubMed  CAS  Google Scholar 

  42. Iniesta M, Herrera D, Montero E, Zurbriggen M, Matos AR, Marín MJ et al (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 39:736–744. https://doi.org/10.1111/j.1600-051X.2012.01914.x

    Article  PubMed  Google Scholar 

  43. 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 40:1025–1035. https://doi.org/10.1111/jcpe.12155

    Article  PubMed  PubMed Central  Google Scholar 

  44. Jones SE, Versalovic J (2009) Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 11(9):35. https://doi.org/10.1186/1471-2180-9-35

    Article  CAS  Google Scholar 

  45. Jayaram P, Chatterjee A, Raghunathan V (2016) Probiotics in the treatment of periodontal disease: a systematic review. J Indian Soc Periodontol 20(5):488–495. https://doi.org/10.4103/0972-124X.207053

    Article  PubMed  PubMed Central  Google Scholar 

  46. Moher D, Hopewell S, Schulz KF, Montori V, Gøtzsche PC, Devereaux PJ, Elbourne D, Egger M, Altman DG (2010) CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials. BMJ 340:c869. https://doi.org/10.1136/bmj.c869

    Article  PubMed  PubMed Central  Google Scholar 

  47. Borgnakke WS, Ylöstalo PV, Taylor GW, Genco RJ (2013) Effect of periodontal disease on diabetes: systematic review of epidemiologic observational evidence. J Periodontol 84(4 Suppl):S135-52. https://doi.org/10.1902/jop.2013.1340013

    Article  PubMed  Google Scholar 

  48. Wennström JL, Tomasi C, Bertelle A, Dellasega E (2005) Full-mouth ultrasonic debridement versus quadrant scaling and root planing as an initial approach in the treatment of chronic periodontitis. J Clin Periodontol 32(8):851–9. https://doi.org/10.1111/j.1600-051X.2005.00776.x

    Article  PubMed  Google Scholar 

  49. Seminario-Amez M, López-López J, Estrugo-Devesa A, Ayuso-Montero R, Jané-Salas E (2017) Probiotics and oral health: a systematic review. Med Oral Patol Oral Cir Bucal 22(3):e282–e288. https://doi.org/10.4317/medoral.21494

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Ince G, Gürsoy H, Ipçi SD, Cakar G, Emekli-Alturfan E, Yilmaz S (2015) Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol 86:746–754. https://doi.org/10.1902/jop.2015.14061

    Article  PubMed  Google Scholar 

  51. Kraft-Bodi E, Jørgensen MR, Keller MK, Kragelund C, Twetman S (2015) Effect of probiotic bacteria on oral candida in frail elderly. J Dent ResSep 94(9 Suppl):181S-S186. https://doi.org/10.1177/0022034515595950

    Article  CAS  Google Scholar 

  52. Ramos TCS, Boas MLV, Nunes CMM, Ferreira CL, Pannuti CM, Santamaria MP, Jardini MAN (2022) Effect of systemic antibiotic and probiotic therapies as adjuvant treatments of subgingival instrumentation for periodontitis: a randomized controlled clinical study. J Appl Oral Sci 30:e20210583. https://doi.org/10.1590/1678-7757-2021-0583

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. AdhenkavilRadhakrishnan R, Joseph Vadakkekuttical R, Radhakrishnan C (2022) Proportion and severity of periodontitis and correlation of periodontal inflamed surface area with glycemic status in patients with type 2 diabetic neuropathy with and without diabetic foot. J Periodontol 93(5):687–696. https://doi.org/10.1002/JPER.21-0174

    Article  CAS  Google Scholar 

  54. Glurich I, Acharya A (2019) Updates from the evidence base examining association between periodontal disease and type 2 diabetes mellitus: current status and clinical relevance. Curr DiabRep 19:121. https://doi.org/10.1007/s11892-019-1228-0

    Article  Google Scholar 

  55. Rodríguez-Hernández AP, Márquez-Corona ML, Pontigo-Loyola AP, Medina-Solís CE, Ximenez-Fyvie LA (2019) Subgingival microbiota of Mexicans with type 2 diabetes with different periodontal and metabolic conditions. Int J Environ Res Public Health 16(17):3184. https://doi.org/10.3390/ijerph16173184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Herrera D, Sanz M, Shapira L, Brotons C, Chapple I, Frese T, Graziani F, Hobbs FDR, Huck O, Hummers E, Jepsen S, Kravtchenko O, Madianos P, Molina A, Ungan M, Vilaseca J, Windak A, Vinker S (2023) Association between periodontal diseases and cardiovascular diseases, diabetes and respiratory diseases: consensus report of the Joint Workshop by the European Federation of Periodontology (EFP) and the European arm of the World Organization of Family Doctors (WONCA Europe). J Clin Periodontol 19. https://doi.org/10.1111/jcpe.13807

  57. Teeuw WJ, Slot DE, Susanto H, Gerdes VE, Abbas F, D’Aiuto F, Kastelein JJ, Loos BG (2014) Treatment of periodontitis improves the atherosclerotic profile: a systematic review and meta-analysis. J Clin Periodontol 41(1):70–79. https://doi.org/10.1111/jcpe.12171

    Article  PubMed  CAS  Google Scholar 

  58. Lamarche B, Lemieux I, Després JP (1999) The small, dense LDL phenotype and the risk of coronary heart disease: epidemiology, patho-physiology and therapeutic aspects. Diabetes Metab. 25(3):199–211

    PubMed  CAS  Google Scholar 

  59. de Queiroz Mello AP, da Silva IT, Oliveira AS, Nunes VS, Abdalla DS, Gidlund M (2010) Damasceno NR (2010) Electronegative low-density lipoprotein is associated with dense low-density lipoprotein in subjects with different levels of cardiovascular risk. Lipids 45(7):619–625. https://doi.org/10.1007/s11745-010-3439-7

    Article  PubMed  CAS  Google Scholar 

  60. Cartolano FC, Dias GD, de Freitas MCP, Figueiredo Neto AM, Damasceno NRT (2017) Insulin resistance predicts atherogenic lipoprotein profile in nondiabetic subjects. J Diabetes Res. 1018796. https://doi.org/10.1155/2017/1018796

  61. Kosmas CE, Bousvarou MD, Kostara CE, Papakonstantinou EJ, Salamou E, Guzman E (2023) Insulin resistance and cardiovascular diseasE. J Int Med Res 51(3):3000605231164548. https://doi.org/10.1177/03000605231164548

    Article  PubMed  Google Scholar 

  62. Darabi M, Kontush A. High-density lipoproteins (HDL): Novel function and therapeutic applications (2022) Biochim Biophys Acta Mol Cell Biol Lipids 1867(1):159058. https://doi.org/10.1016/j.bbalip.2021.159058

  63. Kontush A, Lindahl M, Lhomme M, Calabresi L, Chapman MJ (2015) Davidson WS (2015) Structure of HDL: particle subclasses and molecular components. Handb Exp Pharmacol 224:3–51. https://doi.org/10.1007/978-3-319-09665-0_1

    Article  PubMed  CAS  Google Scholar 

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Funding

The work was financed in part by the Coordination for the Improvement of Higher Education Personnel–Brasil (CAPES)–Finance Code 001, National Council for Scientific and Technological Development from Brazil, National Institute of Science and Technology Complex Fluids (INCT-FCx)-(CNPq–465259/2014–6), and São Paulo Research Foundation (FAPESP–2014/50983–3 and 2016/24531–3).

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Authors and Affiliations

  1. Department of Diagnosis and Surgery, Institute of Science and Technology of São José Dos Campos, Universidade Estadual Paulista (Unesp), São José Dos Campos, SP, Brazil

    Maria Aparecida Neves Jardini, Juliana Fatima Pedroso & Camilla Magnoni Moretto Nunes

  2. Department of Dentistry, Universidade de Taubaté (UNITAU), Taubaté, SP, Brazil

    Camila Lopes Ferreira

  3. Lipids, Oxidation and Cell Biology Team-LIM-19, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, São Paulo, SP, Brazil

    Cadiele Oliana Reichert & Debora Levy

  4. Department of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil

    Marlene Nunez Aldin & Nagila Raquel Teixeira Damasceno

  5. Institute of Physics, University of São Paulo, São Paulo, SP, Brazil

    Antonio Martins Figueiredo Neto

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  1. Maria Aparecida Neves Jardini
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Contributions

All authors contributed to the study conception and design. Conceptualization: MANJ and JFP; methodology: MANJ, JFP, CLF, CMMN, COR, MNA, AMFN, DL, NRTD; formal analysis and investigation: JFP, CLF, CMMN, COR, MNA, DL, NRTD; writing—original draft preparation: MANJ, CLF, CMMN; writing—review and editing: MANJ, JFP, CLF, CMMN; funding acquisition: AMFN, MANJ, DL, NRTD; resources: for the biological assays: MANJ, AMFN, DL, NRTD; supervision: MANJ. The manuscript was written by MANJ, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Maria Aparecida Neves Jardini.

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Ethics approval and consent to participate

The present study followed the rules of the new CONSORT statement and SPIRIT statement. It was approved by the Human Research Ethics Committee of the Dentistry course in São José dos Campos–UNESP, under number 2.708.923 and Register Number RBR-8t4qqx, in the Brazilian Registry of Clinical Trials (ReBEC).

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The authors declare no competing interests.

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Jardini, M.A.N., Pedroso, J.F., Ferreira, C.L. et al. Effect of adjuvant probiotic therapy (Lactobacillus reuteri) in the treatment of periodontitis associated with diabetes mellitus: clinical, controlled, and randomized study. Clin Oral Invest 28, 80 (2024). https://doi.org/10.1007/s00784-023-05441-0

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  • DOI: https://doi.org/10.1007/s00784-023-05441-0

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