Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Scoping Review

Effectiveness of Probiotic Therapy in the Management of Periodontal Disease in Diabetic Patients: A Scoping Review

Author(s): Luanny de Brito Avelino, Katryne Targino Rodrigues, Natália Teixeira da Silva Cruz, Agnes Andrade Martins and Ana Rafaela Luz de Aquino Martins*

Volume 20, Issue 9, 2024

Published on: 28 November, 2023

Article ID: e281123223961 Pages: 13

DOI: 10.2174/0115733998271193231108054254

Price: $65

Abstract

Background: Probiotics can compete with periodontal pathogens in the formation of dental biofilm, and they are able to modulate local and systemic immune responses. Thus, its use in diabetic patients with periodontal disease (PD) can overcome the limitations of conventional periodontal treatment.

Objective: This scoping review aimed to understand the extent and type of evidence in relation to the effects of probiotic therapy on periodontal and glycaemic parameters of diabetic patients with PD.

Methods: An electronic search was performed in the following databases: Cochrane Library, EMBASE, Virtual Health Library (including LILACS and BBO), PubMed (including Medline), Scopus, Web of Science, and Google Scholar. The review included clinical trials on patients with type 2 diabetes, diagnosed with gingivitis or periodontitis, who received probiotic therapy as a single therapy or adjuvant to scaling and root planning, and on whom the analyses of clinical periodontal, immunological, microbiological, or glycaemic parameters were performed.

Results: The electronic search yielded a total of 1165 articles. After removing duplicate titles and performing systematic screening, 6 studies were included in the qualitative summary. Probiotic administration improved clinical periodontal parameters (bleeding on probing and probing depth), oxidative stress markers, and inflammatory cytokines (IL-8, IL-10, and TNF-α) in relation to control groups. Experimental groups were also more advantageous in reducing the frequency of periodontopathogenic bacteria. However, the evidence of probiotics in decreasing glycated hemoglobin is still uncertain.

Conclusion: Probiotics may provide safe additional benefits to periodontal parameters of patients with type 2 diabetes and periodontal disease.

Keywords: Diabetes mellitus, gingivitis, inflammation, periodontitis, periodontal diseases, probiotics.

[1]
Clark D, Kotronia E, Ramsay SE. Frailty, aging, and periodontal disease: Basic biologic considerations. Periodontol 2000 2021; 87(1): 143-56.
[http://dx.doi.org/10.1111/prd.12380] [PMID: 34463998]
[2]
Sedghi LM, Bacino M, Kapila YL. Periodontal disease: The good, the bad, and the unknown. Front Cell Infect Microbiol 2021; 11: 766944.
[http://dx.doi.org/10.3389/fcimb.2021.766944] [PMID: 34950607]
[3]
Nazir MA, Sabatini S, Lauritano D, Candotto V, Silvestre FJ, Nardi GM. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci 2017; 11(2): 72-80.
[PMID: 28539867]
[4]
Trombelli L, Farina R, Silva CO, Tatakis DN. Plaque‐induced gingivitis: Case definition and diagnostic considerations. J Clin Periodontol 2018; 45(S20): S44-67.
[http://dx.doi.org/10.1111/jcpe.12939] [PMID: 29926492]
[5]
Kaczor-Urbanowicz KE, Trivedi HM, Lima PO, et al. Salivary exRNA biomarkers to detect gingivitis and monitor disease regression. J Clin Periodontol 2018; 45(7): 806-17.
[http://dx.doi.org/10.1111/jcpe.12930] [PMID: 29779262]
[6]
Kim JJ, Kim CJ, Camargo PM. Salivary biomarkers in the diagnosis of periodontal diseases. J Calif Dent Assoc 2013; 41(2): 119-24.
[http://dx.doi.org/10.1080/19424396.2013.12222285] [PMID: 23505757]
[7]
Offenbacher S, Barros S, Mendoza L, et al. Changes in gingival crevicular fluid inflammatory mediator levels during the induction and resolution of experimental gingivitis in humans. J Clin Periodontol 2010; 37(4): 324-33.
[http://dx.doi.org/10.1111/j.1600-051X.2010.01543.x] [PMID: 20447255]
[8]
Murakami S, Mealey BL, Mariotti A, Chapple ILC. Dental plaque–induced gingival conditions. J Periodontol 2018; 89(S1): S17-27.
[http://dx.doi.org/10.1002/JPER.17-0095] [PMID: 29926958]
[9]
Reddy MS, Geurs NC, Jeffcoat RL, Proskin H, Jeffcoat MK. Periodontal disease progression. J Periodontol 2000; 71(10): 1583-90.
[http://dx.doi.org/10.1902/jop.2000.71.10.1583] [PMID: 11063391]
[10]
Nemoto T, Shiba T, Komatsu K, et al. Discrimination of bacterial community structures among healthy, gingivitis, and periodontitis statuses through integrated metatranscriptomic and network analyses. mSystems 2021; 6(6): e00886-21.
[http://dx.doi.org/10.1128/mSystems.00886-21] [PMID: 34698525]
[11]
Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri‐implant diseases and conditions. J Periodontol 2018; 89(S1) (Suppl. 1): S173-82.
[http://dx.doi.org/10.1002/JPER.17-0721] [PMID: 29926951]
[12]
Shaddox LM, Morford LA, Nibali L. Periodontal health and disease: The contribution of genetics. Periodontol 2000 2021; 85(1): 161-81.
[http://dx.doi.org/10.1111/prd.12357] [PMID: 33226705]
[13]
Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers 2017; 3(1): 17038.
[http://dx.doi.org/10.1038/nrdp.2017.38] [PMID: 28805207]
[14]
Scannapieco FA, Gershovich E. The prevention of periodontal disease—An overview. Periodontol 2000 2020; 84(1): 9-13.
[http://dx.doi.org/10.1111/prd.12330] [PMID: 32844421]
[15]
Gloyn AL, Drucker DJ. Precision medicine in the management of type 2 diabetes. Lancet Diabetes Endocrinol 2018; 6(11): 891-900.
[http://dx.doi.org/10.1016/S2213-8587(18)30052-4] [PMID: 29699867]
[16]
Cloete L. Diabetes mellitus: An overview of the types, symptoms, complications and management. Nurs Stand 2022; 37(1): 61-6.
[http://dx.doi.org/10.7748/ns.2021.e11709] [PMID: 34708622]
[17]
Tinajero MG, Malik VS. An update on the epidemiology of type 2 diabetes. Endocrinol Metab Clin North Am 2021; 50(3): 337-55.
[http://dx.doi.org/10.1016/j.ecl.2021.05.013] [PMID: 34399949]
[18]
Ortiz-Martínez M, González-González M, Martagón AJ, Hlavinka V, Willson RC, Rito-Palomares M. Recent developments in biomarkers for diagnosis and screening of type 2 diabetes mellitus. Curr Diab Rep 2022; 22(3): 95-115.
[http://dx.doi.org/10.1007/s11892-022-01453-4] [PMID: 35267140]
[19]
Khan MAB, Hashim MJ, King JK, Govender RD, Mustafa H, Al Kaabi J. Epidemiology of type 2 diabetes – global burden of disease and forecasted trends. J Epidemiol Glob Health 2019; 10(1): 107-11.
[http://dx.doi.org/10.2991/jegh.k.191028.001] [PMID: 32175717]
[20]
Javed Shaikh MA. S, R.; Singh, H.; Rawat, S.; Pathak, S.; Mishra, A.; Gupta, G. Role of various gene expressions in etiopathogenesis of type 2 diabetes mellitus. Adv Mind Body Med 2021; 35(3): 31-9.
[PMID: 34237027]
[21]
Chatterjee S, Khunti K, Davies MJ. Type 2 diabetes. Lancet 2017; 389(10085): 2239-51.
[http://dx.doi.org/10.1016/S0140-6736(17)30058-2] [PMID: 28190580]
[22]
Galicia-Garcia U, Benito-Vicente A, Jebari S, et al. Pathophysiology of type 2 diabetes mellitus. Int J Mol Sci 2020; 21(17): 6275.
[http://dx.doi.org/10.3390/ijms21176275] [PMID: 32872570]
[23]
Weir GC, Gaglia J, Bonner-Weir S. β-cell secretory dysfunction: A key cause of type 2 diabetes – Authors’ reply. Lancet Diabetes Endocrinol 2020; 8(5): 370-1.
[http://dx.doi.org/10.1016/S2213-8587(20)30120-0] [PMID: 32333872]
[24]
Stanimirovic J, Radovanovic J, Banjac K, et al. Role of C-reactive protein in diabetic inflammation. Mediators Inflamm 2022; 2022: 1-15.
[http://dx.doi.org/10.1155/2022/3706508] [PMID: 35620114]
[25]
Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: A tale of two common interrelated diseases. Nat Rev Endocrinol 2011; 7(12): 738-48.
[http://dx.doi.org/10.1038/nrendo.2011.106] [PMID: 21709707]
[26]
Salhi L, Reners M. Update on the bidirectional link between diabetes and periodontitis. Adv Exp Med Biol 2022; 1373: 231-40.
[http://dx.doi.org/10.1007/978-3-030-96881-6_12] [PMID: 35612801]
[27]
Sanz M, Ceriello A, Buysschaert M, et al. 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 2018; 45(2): 138-49.
[http://dx.doi.org/10.1111/jcpe.12808] [PMID: 29280174]
[28]
Simpson TC, Clarkson JE, Worthington HV, et al. Treatment of periodontitis for glycaemic control in people with diabetes mellitus. Cochrane Database Syst Rev 2022; 4(4): CD004714.
[PMID: 35420698]
[29]
Wu C, Yuan Y, Liu H, et al. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health 2020; 20(1): 204.
[http://dx.doi.org/10.1186/s12903-020-01180-w] [PMID: 32652980]
[30]
Andriankaja OM, Barros SP, Moss K, et al. Levels of serum interleukin (IL)-6 and gingival crevicular fluid of IL-1beta and prostaglandin E(2) among non-smoking subjects with gingivitis and type 2 diabetes. J Periodontol 2009; 80(2): 307-16.
[http://dx.doi.org/10.1902/jop.2009.080385] [PMID: 19186972]
[31]
Polak D, Shapira L. An update on the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 2018; 45(2): 150-66.
[http://dx.doi.org/10.1111/jcpe.12803] [PMID: 29280184]
[32]
Nascimento GG, Leite FRM, Vestergaard P, Scheutz F, López R. Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies. Acta Diabetol 2018; 55(7): 653-67.
[http://dx.doi.org/10.1007/s00592-018-1120-4] [PMID: 29502214]
[33]
Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jané-Salas E, López-López J, Viñas M. Benefits of non‐surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: A randomized controlled trial. J Clin Periodontol 2018; 45(3): 345-53.
[http://dx.doi.org/10.1111/jcpe.12858] [PMID: 29265454]
[34]
Kocher T, König J, Borgnakke WS, Pink C, Meisel P. Periodontal complications of hyperglycemia/diabetes mellitus: Epidemiologic complexity and clinical challenge. Periodontol 2000 2018; 78(1): 59-97.
[http://dx.doi.org/10.1111/prd.12235] [PMID: 30198134]
[35]
Zhang X, Wang M, Wang X, et al. Relationship between periodontitis and microangiopathy in type 2 diabetes mellitus: A meta‐analysis. J Periodontal Res 2021; 56(6): 1019-27.
[http://dx.doi.org/10.1111/jre.12916] [PMID: 34254680]
[36]
Baeza M, Morales A, Cisterna C, et al. Effect of periodontal treatment in patients with periodontitis and diabetes: systematic review and meta-analysis. J Appl Oral Sci 2020; 28: e20190248.
[http://dx.doi.org/10.1590/1678-7757-2019-0248] [PMID: 31939522]
[37]
Balta MG, Papathanasiou E, Blix IJ, Van Dyke TE. Host modulation and treatment of periodontal disease. J Dent Res 2021; 100(8): 798-809.
[http://dx.doi.org/10.1177/0022034521995157] [PMID: 33655803]
[38]
Golub LM, Lee HM. Periodontal therapeutics: Current host‐modulation agents and future directions. Periodontol 2000 2020; 82(1): 186-204.
[http://dx.doi.org/10.1111/prd.12315] [PMID: 31850625]
[39]
Figuero E, Herrera D, Tobías A, et al. Efficacy of adjunctive anti‐plaque chemical agents in managing gingivitis: A systematic review and network meta‐analyses. J Clin Periodontol 2019; 46(7): 723-39.
[http://dx.doi.org/10.1111/jcpe.13127] [PMID: 31058336]
[40]
Figuero E, Roldán S, Serrano J, Escribano M, Martín C, Preshaw PM. Efficacy of adjunctive therapies in patients with gingival inflammation: A systematic review and meta‐analysis. J Clin Periodontol 2020; 47(S22): 125-43.
[http://dx.doi.org/10.1111/jcpe.13244] [PMID: 31869441]
[41]
Donos N, Calciolari E, Brusselaers N, Goldoni M, Bostanci N, Belibasakis GN. The adjunctive use of host modulators in non‐surgical periodontal therapy. A systematic review of randomized, placebo‐controlled clinical studies. J Clin Periodontol 2020; 47(S22): 199-238.
[http://dx.doi.org/10.1111/jcpe.13232] [PMID: 31834951]
[42]
da Costa LFNP, Amaral CSF, Barbirato DS, Leão ATT, Fogacci MF. Chlorhexidine mouthwash as an adjunct to mechanical therapy in chronic periodontitis. J Am Dent Assoc 2017; 148(5): 308-18.
[http://dx.doi.org/10.1016/j.adaj.2017.01.021] [PMID: 28284417]
[43]
Gruner D, Paris S, Schwendicke F. Probiotics for managing caries and periodontitis: Systematic review and meta-analysis. J Dent 2016; 48: 16-25.
[http://dx.doi.org/10.1016/j.jdent.2016.03.002] [PMID: 26965080]
[44]
Sang-Ngoen T, Czumbel LM, Sadaeng W, et al. Orally administered probiotics decrease aggregatibacter actinomycetemcomitans but not other periodontal pathogenic bacteria counts in the oral cavity: A systematic review and meta-analysis. Front Pharmacol 2021; 12: 682656.
[http://dx.doi.org/10.3389/fphar.2021.682656] [PMID: 34447307]
[45]
Martín R, Langella P. Emerging health concepts in the probiotics field: Streamlining the definitions. Front Microbiol 2019; 10: 1047.
[http://dx.doi.org/10.3389/fmicb.2019.01047] [PMID: 31164874]
[46]
Barbosa SJA, Oliveira MMB, Ribeiro SB, et al. The beneficial effects of Lacticaseibacillus casei on the small intestine and colon of Swiss mice against the deleterious effects of 5-fluorouracil. Front Immunol 2022; 13: 954885.
[http://dx.doi.org/10.3389/fimmu.2022.954885] [PMID: 36341441]
[47]
Yadav H, Jain S, Sinha PR. Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition 2007; 23(1): 62-8.
[http://dx.doi.org/10.1016/j.nut.2006.09.002] [PMID: 17084593]
[48]
Zheng HJ, Guo J, Jia Q, et al. The effect of probiotic and synbiotic supplementation on biomarkers of inflammation and oxidative stress in diabetic patients: A systematic review and meta-analysis of randomized controlled trials. Pharmacol Res 2019; 142: 303-13.
[http://dx.doi.org/10.1016/j.phrs.2019.02.016] [PMID: 30794924]
[49]
Milajerdi A, Mousavi SM, Sadeghi A, et al. The effect of probiotics on inflammatory biomarkers: A meta-analysis of randomized clinical trials. Eur J Nutr 2020; 59(2): 633-49.
[http://dx.doi.org/10.1007/s00394-019-01931-8] [PMID: 30854594]
[50]
Kazemi A, Soltani S, Ghorabi S, et al. Effect of probiotic and synbiotic supplementation on inflammatory markers in health and disease status: A systematic review and meta-analysis of clinical trials. Clin Nutr 2020; 39(3): 789-819.
[http://dx.doi.org/10.1016/j.clnu.2019.04.004] [PMID: 31060892]
[51]
Shadnoush M, Shaker Hosseini R, Mehrabi Y, et al. Probiotic yogurt affects pro- and anti-inflammatory factors in patients with inflammatory bowel disease. Iran J Pharm Res 2013; 12(4): 929-36.
[PMID: 24523774]
[52]
Dai Y, Quan J, Xiong L, Luo Y, Yi B. Probiotics improve renal function, glucose, lipids, inflammation and oxidative stress in diabetic kidney disease: a systematic review and meta-analysis. Ren Fail 2022; 44(1): 862-80.
[http://dx.doi.org/10.1080/0886022X.2022.2079522] [PMID: 35611435]
[53]
Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksén-Blicks C. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand 2009; 67(1): 19-24.
[http://dx.doi.org/10.1080/00016350802516170] [PMID: 18985460]
[54]
Furlaneto F, Ishikawa KH, Messora MR, Mayer MPA. Probiotics during the therapeutic management of periodontitis. Adv Exp Med Biol 2022; 1373: 353-75.
[http://dx.doi.org/10.1007/978-3-030-96881-6_19] [PMID: 35612808]
[55]
Tricco AC, Lillie E, Zarin W, et al. PRISMA extension for scoping reviews (PRISMA-ScR): Checklist and explanation. Ann Intern Med 2018; 169(7): 467-73.
[http://dx.doi.org/10.7326/M18-0850] [PMID: 30178033]
[56]
Sabatini S, Lauritano D, Candotto V, Silvestre FJ, Nardi GM. Oral probiotics in the management of gingivitis in diabetic patients: A double blinded randomized controlled study. J Biol Regul Homeost Agents 2017; 31(2): 197-202.
[PMID: 28691473]
[57]
Hu B, Qu J, Han T, Leng J. Effect of basic periodontal therapy combined with probiotics on oral microecology and blood sugar control in patients with diabetes and periodontitis. Pak J Zool 2023; 55(3): 1109.
[http://dx.doi.org/10.17582/journal.pjz/20210715070747]
[58]
Elsadek MF, Ahmed BM, Alkhawtani DM, Zia Siddiqui A. A comparative clinical, microbiological and glycemic analysis of photodynamic therapy and Lactobacillus reuteri in the treatment of chronic periodontitis in type-2 diabetes mellitus patients. Photodiagn Photodyn Ther 2020; 29: 101629.
[http://dx.doi.org/10.1016/j.pdpdt.2019.101629] [PMID: 31870899]
[59]
Pedroso JdF Effect of probiotic therapy (Lactobacillus reuteri) as an adjunct in the treatment of periodontitis associated with Diabetes Mellitus: clinical, controlled and randomized study Paulista State University. Unesp 2021.
[60]
Malyshev ME, Iordanishvili AK, Prisyazhnyuk OV, Bumai AO. The effect of probiotics on the secretory immunity of saliva in patients with type 2 diabetes. Stomatologia 2019; 98(6): 26-9.
[http://dx.doi.org/10.17116/stomat20199806126] [PMID: 31922506]
[61]
Bazyar H, Maghsoumi-Norouzabad L, Yarahmadi M, et al. The impacts of synbiotic supplementation on periodontal indices and biomarkers of oxidative stress in type 2 diabetes mellitus patients with chronic periodontitis under non-surgical periodontal therapy. A double-blind, placebo-controlled trial. Diabetes Metab Syndr Obes 2020; 13(1): 19-29.
[http://dx.doi.org/10.2147/DMSO.S230060] [PMID: 32021348]
[62]
Zommiti M, Feuilloley MGJ, Connil N. Update of probiotics in human world: A nonstop source of benefactions till the end of time. Microorganisms 2020; 8(12): 1907.
[http://dx.doi.org/10.3390/microorganisms8121907] [PMID: 33266303]
[63]
Preshaw PM, De Silva N, McCracken GI, et al. Compromised periodontal status in an urban Sri Lankan population with type 2 diabetes. J Clin Periodontol 2010; 37(2): 165-71.
[http://dx.doi.org/10.1111/j.1600-051X.2009.01519.x] [PMID: 20653819]
[64]
Stanko P, Izakovicova Holla L. Bidirectional association between diabetes mellitus and in-flammatory periodontal disease. A review Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2014; 158(1): 035-8.
[http://dx.doi.org/10.5507/bp.2014.005]
[65]
Sanz M, Herrera D, Kebschull M, et al. Treatment of stage I–III periodontitis—The EFP S3 level clinical practice guideline. J Clin Periodontol 2020; 47(S22) (Suppl. 22): 4-60.
[http://dx.doi.org/10.1111/jcpe.13290] [PMID: 32383274]
[66]
Albeshri S, Greenstein G. Efficacy of nonsurgical periodontal therapy for treatment of periodontitis: Practical application of current knowledge. Gen Dent 2022; 70(5): 12-9.
[PMID: 35993928]
[67]
Kwon T, Lamster IB, Levin L. Current concepts in the management of periodontitis. Int Dent J 2021; 71(6): 462-76.
[http://dx.doi.org/10.1111/idj.12630] [PMID: 34839889]
[68]
Costa FO, Miranda Cota LO, Pereira Lages EJ, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: A 5-year follow-up study. J Periodontol 2013; 84(5): 595-605.
[http://dx.doi.org/10.1902/jop.2012.120255] [PMID: 22769441]
[69]
Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non‐surgical periodontal therapy on clinical and immunological response and glycaemic control in type 2 diabetic patients with moderate periodontitis. J Clin Periodontol 2007; 34(10): 835-43.
[http://dx.doi.org/10.1111/j.1600-051X.2007.01127.x] [PMID: 17850602]
[70]
Aboodi GM, Goldberg MB, Glogauer M. Refractory periodontitis population characterized by a hyperactive oral neutrophil phenotype. J Periodontol 2011; 82(5): 726-33.
[http://dx.doi.org/10.1902/jop.2010.100508] [PMID: 21080789]
[71]
Fine N, Hassanpour S, Borenstein A, et al. Distinct oral neutrophil subsets define health and periodontal disease States. J Dent Res 2016; 95(8): 931-8.
[http://dx.doi.org/10.1177/0022034516645564] [PMID: 27270666]
[72]
Hajishengallis G, Chavakis T, Hajishengallis E, Lambris JD. Neutrophil homeostasis and inflammation: Novel paradigms from studying periodontitis. J Leukoc Biol 2015; 98(4): 539-48.
[http://dx.doi.org/10.1189/jlb.3VMR1014-468R] [PMID: 25548253]
[73]
Figueredo CMS, Fischer RG, Gustafsson A. Aberrant neutrophil reactions in periodontitis. J Periodontol 2005; 76(6): 951-5.
[http://dx.doi.org/10.1902/jop.2005.76.6.951] [PMID: 15948690]
[74]
Asemi Z, Zare Z, Shakeri H, Sabihi S, Esmaillzadeh A. Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 2013; 63(1-2): 1-9.
[http://dx.doi.org/10.1159/000349922] [PMID: 23899653]
[75]
Bagarolli RA, Tobar N, Oliveira AG, et al. Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J Nutr Biochem 2017; 50: 16-25.
[http://dx.doi.org/10.1016/j.jnutbio.2017.08.006] [PMID: 28968517]
[76]
Kobyliak N, Falalyeyeva T, Mykhalchyshyn G, Kyriienko D, Komissarenko I. Effect of alive probiotic on insulin resistance in type 2 diabetes patients: Randomized clinical trial. Diabetes Metab Syndr 2018; 12(5): 617-24.
[http://dx.doi.org/10.1016/j.dsx.2018.04.015] [PMID: 29661605]
[77]
Razmpoosh E, Javadi A, Ejtahed HS, Mirmiran P, Javadi M, Yousefinejad A. The effect of probiotic supplementation on glycemic control and lipid profile in patients with type 2 diabetes: A randomized placebo controlled trial. Diabetes Metab Syndr 2019; 13(1): 175-82.
[http://dx.doi.org/10.1016/j.dsx.2018.08.008] [PMID: 30641692]
[78]
Calle MC, Fernandez ML. Inflammation and type 2 diabetes. Diabetes Metab 2012; 38(3): 183-91.
[http://dx.doi.org/10.1016/j.diabet.2011.11.006] [PMID: 22252015]
[79]
Knight ET, Liu J, Seymour GJ, Faggion CM Jr, Cullinan MP. Risk factors that may modify the innate and adaptive immune responses in periodontal diseases. Periodontol 2000 2016; 71(1): 22-51.
[http://dx.doi.org/10.1111/prd.12110] [PMID: 27045429]
[80]
Liu C, Feng X, Li Q, Wang Y, Li Q, Hua M. Adiponectin, TNF-α and inflammatory cytokines and risk of type 2 diabetes: A systematic review and meta-analysis. Cytokine 2016; 86: 100-9.
[http://dx.doi.org/10.1016/j.cyto.2016.06.028] [PMID: 27498215]
[81]
David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505(7484): 559-63.
[http://dx.doi.org/10.1038/nature12820] [PMID: 24336217]
[82]
Salgaço MK, Oliveira LGS, Costa GN, Bianchi F, Sivieri K. Relationship between gut microbiota, probiotics, and type 2 diabetes mellitus. Appl Microbiol Biotechnol 2019; 103(23-24): 9229-38.
[http://dx.doi.org/10.1007/s00253-019-10156-y] [PMID: 31664483]
[83]
Naseri K, Saadati S, Ghaemi F, et al. The effects of probiotic and synbiotic supplementation on inflammation, oxidative stress, and circulating adiponectin and leptin concentration in subjects with prediabetes and type 2 diabetes mellitus: a GRADE-assessed systematic review, meta-analysis, and meta-regression of randomized clinical trials. Eur J Nutr 2023; 62(2): 543-61.
[PMID: 36239789]
[84]
Bohlouli J, Namjoo I, Borzoo-Isfahani M, Hojjati Kermani MA, Balouch Zehi Z, Moravejolahkami AR. Effect of probiotics on oxidative stress and inflammatory status in diabetic nephropathy: A systematic review and meta-analysis of clinical trials. Heliyon 2021; 7(1): e05925.
[http://dx.doi.org/10.1016/j.heliyon.2021.e05925] [PMID: 33490683]
[85]
Ardeshirlarijani E, Tabatabaei-Malazy O, Mohseni S, Qorbani M, Larijani B, Baradar Jalili R. Effect of probiotics supplementation on glucose and oxidative stress in type 2 diabetes mellitus: a meta-analysis of randomized trials. Daru 2019; 27(2): 827-37.
[http://dx.doi.org/10.1007/s40199-019-00302-2] [PMID: 31691101]
[86]
Balakumar M, Prabhu D, Sathishkumar C, et al. Improvement in glucose tolerance and insulin sensitivity by probiotic strains of Indian gut origin in high-fat diet-fed C57BL/6J mice. Eur J Nutr 2018; 57(1): 279-95.
[http://dx.doi.org/10.1007/s00394-016-1317-7] [PMID: 27757592]
[87]
Park KY, Kim B, Hyun CK. <i>Lactobacillus rhamnosus</i> GG improves glucose tolerance through alleviating ER stress and suppressing macrophage activation in db/db mice. J Clin Biochem Nutr 2015; 56(3): 240-6.
[http://dx.doi.org/10.3164/jcbn.14-116] [PMID: 26060355]
[88]
Trøseid M, Nestvold TK, Rudi K, Thoresen H, Nielsen EW, Lappegård KT. Plasma lipopolysaccharide is closely associated with glycemic control and abdominal obesity: Evidence from bariatric surgery. Diabetes Care 2013; 36(11): 3627-32.
[http://dx.doi.org/10.2337/dc13-0451] [PMID: 23835694]
[89]
Amar J, Chabo C, Waget A, et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: Molecular mechanisms and probiotic treatment. EMBO Mol Med 2011; 3(9): 559-72.
[http://dx.doi.org/10.1002/emmm.201100159] [PMID: 21735552]
[90]
O’Connor S, Chouinard-Castonguay S, Gagnon C, Rudkowska I. Prebiotics in the management of components of the metabolic syndrome. Maturitas 2017; 104: 11-8.
[http://dx.doi.org/10.1016/j.maturitas.2017.07.005] [PMID: 28923170]
[91]
Firouzi S, Majid HA, Ismail A, Kamaruddin NA, Barakatun-Nisak MY. Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: A randomized controlled trial. Eur J Nutr 2017; 56(4): 1535-50.
[http://dx.doi.org/10.1007/s00394-016-1199-8] [PMID: 26988693]
[92]
Chen M, Cai W, Zhao S, et al. Oxidative stress‐related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: A systematic review and meta‐analysis. J Clin Periodontol 2019; 46(6): 608-22.
[http://dx.doi.org/10.1111/jcpe.13112] [PMID: 30989678]
[93]
Miricescu D, Totan A, Calenic B, et al. Salivary biomarkers: Relationship between oxidative stress and alveolar bone loss in chronic periodontitis. Acta Odontol Scand 2014; 72(1): 42-7.
[http://dx.doi.org/10.3109/00016357.2013.795659] [PMID: 23869629]
[94]
Trivedi S, Lal N, Mahdi A, Singh B, Pandey S. Association of salivary lipid peroxidation levels, antioxidant enzymes, and chronic periodontitis. Int J Periodontics Restorative Dent 2015; 35(2): e14-9.
[http://dx.doi.org/10.11607/prd.2079] [PMID: 25738349]
[95]
Wei D, Zhang X-L, Wang Y-Z, Yang C-X, Chen G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust Dent J 2010; 55(1): 70-8.
[http://dx.doi.org/10.1111/j.1834-7819.2009.01123.x] [PMID: 20415915]
[96]
Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A. Mechanisms of action of probiotics. Adv Nutr 2019; 10: S49-66.
[http://dx.doi.org/10.1093/advances/nmy063] [PMID: 30721959]
[97]
Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 2019; 103(16): 6463-72.
[http://dx.doi.org/10.1007/s00253-019-09978-7] [PMID: 31267231]
[98]
Gordon DM. The potential of bacteriocin-producing probiotics and associated caveats. Future Microbiol 2009; 4(8): 941-3.
[http://dx.doi.org/10.2217/fmb.09.78] [PMID: 19824784]
[99]
Silva DR, Sardi JCO, Pitangui NS, Roque SM, Silva ACB, Rosalen PL. Probiotics as an alternative antimicrobial therapy: Current reality and future directions. J Funct Foods 2020; 73: 104080.
[http://dx.doi.org/10.1016/j.jff.2020.104080]
[100]
Jäsberg H, Söderling E, Endo A, Beighton D, Haukioja A. Bifidobacteria inhibit the growth of Porphyromonas gingivalis but not of Streptococcus mutans in an in vitro biofilm model. Eur J Oral Sci 2016; 124(3): 251-8.
[http://dx.doi.org/10.1111/eos.12266] [PMID: 27061393]
[101]
Fagnant HS, Isidean SD, Wilson L, et al. Orally ingested probiotic, prebiotic, and synbiotic interventions as countermeasures for gastrointestinal tract infections in nonelderly adults: A systematic review and meta-analysis. Adv Nutr 2023; 14(3): 539-54.
[http://dx.doi.org/10.1016/j.advnut.2023.02.002] [PMID: 36822240]
[102]
Wang G, Chen Y, Xia Y, Song X, Ai L. Characteristics of probiotic preparations and their applications. Foods 2022; 11(16): 2472.
[http://dx.doi.org/10.3390/foods11162472] [PMID: 36010472]
[103]
Bollero P, Di Renzo L, Franco R, et al. Effects of new probiotic mouthwash in patients with diabetes mellitus and cardiovascular diseases. Eur Rev Med Pharmacol Sci 2017; 21(24): 5827-36.
[PMID: 29272020]
[104]
Godovanets OI, Kotelban AV, Moroz PV, Vitkovskyi OO, Kitsak TS, Navolskyi NM. Clinical and immunologic assessment of a complex of therapeutic-preventive measures concerning chronic catarrhal gingivitis in children with comorbid diabetes mellitus. Wiad Lek 2020; 73(2): 298-301.
[http://dx.doi.org/10.36740/WLek202002117] [PMID: 32248163]
[105]
Kotelban A, Moroz P, Hrynkevych L, Romaniuk D, Muryniuk T. Microbiological and immunological assessment of a complex of therapeutic-preventive measures for chronic catarrhal gingivitis in children with diabetes mellitus. Georgian Med News 2019; 294(294): 72-6.
[PMID: 31687953]
[106]
Lai S, Lingström P, Cagetti MG, et al. Effect of Lactobacillus brevis CD2 containing lozenges and plaque pH and cariogenic bacteria in diabetic children: a randomised clinical trial. Clin Oral Investig 2021; 25(1): 115-23.
[http://dx.doi.org/10.1007/s00784-020-03342-0] [PMID: 33083852]
[107]
Predieri B, Cenciarelli V, Bruzzi P, et al. Lactobacillus reuteri oral administration improves periodontal disease in children and adolescents with type 1 diabetes. Pediatr Diabetes 2017; 18(S25): 91-2.
[108]
Scattarella A, Esposito G, Di Giorgio R, Nardi GM. Prevention protocols for diabetic patients. Prev Assist Dent 2010; 36: 121-5.
[http://dx.doi.org/10.1016/j.pad.2009.06.005]
[109]
de O Silva V.; Lobato, R.V.; Andrade, E.F.; Orlando, D.R.; Borges, B.D.B.; Zangeronimo, M.G.; de Sousa, R.V.; Pereira, L.J. Effects of β-glucans ingestion on alveolar bone loss, intestinal morphology, systemic inflammatory profile, and pancreatic β-cell function in rats with periodontitis and diabetes. Nutrients 2017; 9(9): 1016-28.
[http://dx.doi.org/10.3390/nu9091016] [PMID: 28906456]
[110]
Isacco CG, Ballini A, De Vito D, et al. Rebalancing the oral microbiota as an efficient tool in endocrine, metabolic and immune disorders. Endocr Metab Immune Disord Drug Targets 2021; 21(5): 777-84.
[http://dx.doi.org/10.2174/22123873MTA4CNjQs0 ] [PMID: 32727337]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy