Oral Lactobacillus species and their probiotic capabilities in patients with periodontitis and periodontally healthy individuals

Arghavan Etebarian, Tahere Sheshpari, Kourosh Kabir, Hanieh Sadeghi, Abouzar Moradi, Avin Hafedi, Arghavan Etebarian, Tahere Sheshpari, Kourosh Kabir, Hanieh Sadeghi, Abouzar Moradi, Avin Hafedi

Abstract

Objectives: This study aimed to identify oral Lactobacillus species and characterize their adhesion properties and antibacterial activity in patients with periodontitis compared with periodontally healthy individuals.

Materials and methods: Three hundred and fifty-four isolates from the saliva, subgingival, and tongue plaque of 59 periodontitis patients and 59 healthy individuals were analyzed. Oral Lactobacillus species were identified through the culture method in the modified MRS medium and confirmed by molecular testing. Moreover, the radial diffusion assay and cell culture methods were used to determine the antibacterial activities of oral strains against oral pathogens and their adhesion activity in vitro.

Results: 67.7% of the cases and 75.7% of the control samples were positive for the Lactobacillus species. Lacticaseibacillus paracasei and Limosilactobacillus fermentum were the dominant species in the case group, whereas Lacticaseibacillus casei and Lactiplantibacillus plantarum were dominant in the control group. Lactobacillus crispatus and Lactobacillus gasseri had higher antibacterial effects against oral pathogens. Moreover, Ligilactobacillus salivarius and L. fermentum demonstrated the highest ability to adhere to oral mucosal cells and salivary-coated hydroxyapatite.

Conclusion: L. crispatus, L. gasseri, L. fermentum, and L. salivarius can be introduced as probiotic candidates since they demonstrated appropriate adherence to oral mucosal cells and salivary-coated hydroxyapatite and also antibacterial activities. However, further studies should be conducted to assess the safety of probiotic interventions using these strains in patients with periodontal disease.

Keywords: lactobacillus; oral cavity; periodontitis; probiotics.

© 2023 The Authors. Clinical and Experimental Dental Research published by John Wiley & Sons Ltd.

References

REFERENCES

    1. Abdel-Daim, A., Hassouna, N., Hafez, M., Ashor, M., & Aboulwafa, M. M. (2012). Screening of Lactobacillus isolates for their adherence capabilities to mammalian cells and their acid and bile tolerance.
    1. Ahrné, S., Nobaek, S., Jeppsson, B., Adlerberth, I., Wold, A. E., & Molin, G. (1998). The normal Lactobacillus flora of healthy human rectal and oral mucosa. Journal of Applied Microbiology, 85(1), 88-94.
    1. Allaker, R. P., & Stephen, A. S. (2017). Use of probiotics and oral health. Current Oral Health Reports, 4(4), 309-318.
    1. Aranishi, F., Okimoto, T., & Izumi, S. (2005). Identification of gadoid species (Pisces, Gadidae) by PCR-RFLP analysis. Journal of Applied Genetics, 46(1), 69-73.
    1. Azizian, K., Osquee, H. O., Pourlak, T., Hosseinpour, R., Asgharzadeh, M., Ganvarov, K., & Kafil, H. S. (2021). Genetic diversity of Lactobacillus spp. isolates from oral cavity and their probiotic and antimicrobial properties. Gene Reports, 24, 101231.
    1. Balouiri, M., Sadiki, M., & Ibnsouda, S. K. (2016). Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis, 6(2), 71-79.
    1. Ben Taheur, F., Kouidhi, B., Fdhila, K., Elabed, H., Ben Slama, R., Mahdouani, K., Bakhrouf, A., & Chaieb, K. (2016). Anti-bacterial and anti-biofilm activity of probiotic bacteria against oral pathogens. Microbial Pathogenesis, 97, 213-220.
    1. Bosch, M., Nart, J., Audivert, S., Bonachera, M. A., Alemany, A. S., Fuentes, M. C., & Cuñé, J. (2012). Isolation and characterization of probiotic strains for improving oral health. Archives of Oral Biology, 57(5), 539-549.
    1. Bustamante, M., Oomah, B. D., Mosi-Roa, Y., Rubilar, M., & Burgos-Díaz, C. (2020). Probiotics as an adjunct therapy for the treatment of halitosis, dental caries and periodontitis. Probiotics and Antimicrobial Proteins, 12(2), 325-34.
    1. Caton, J. G., Armitage, G., Berglundh, T., Chapple, I. L. C., Jepsen, S., Kornman, K. S., Mealey, B. L., Papapanou, P. N., Sanz, M., & Tonetti, M. S. (2018). A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. Journal of Clinical Periodontology, 45, S1-S8.
    1. Chacon-Cortes, D., Haupt, L. M., Lea, R. A., & Griffiths, L. R. (2012). Comparison of genomic DNA extraction techniques from whole blood samples: A time, cost and quality evaluation study. Molecular Biology Reports, 39(5), 5961-5966.
    1. Colloca, M., Ahumada, M., López, M., & Nader-Macías, M. (2000). Surface properties of lactobacilli isolated from healthy subjects. Oral Diseases, 6(4), 227-233.
    1. Cuozzo, S. A., Sesma, F., Palacios, J. M., Ruíz Holgado, A. P., & Raya, R. (2000). Identification and nucleotide sequence of genes involved in the synthesis of lactocin 705, a two-peptide bacteriocin from Lactobacillus casei CRL 705. FEMS Microbiology Letters, 185(2), 157-161.
    1. Curtis, M. A., Diaz, P. I., & Van Dyke, T. E. (2020). The role of the microbiota in periodontal disease. Periodontology 2000, 83(1), 14-25.
    1. Damgaard, C., Danielsen, A. K., Enevold, C., Reinholdt, J., Holmstrup, P., Nielsen, C. H., & Massarenti, L. (2021). Circulating antibodies against leukotoxin A as marker of periodontitis Grades B and C and oral infection with Aggregatibacter actinomycetemcomitans. Journal of Periodontology, 92(12), 1795-1804.
    1. Ellen, R. P. (1976). Establishment and distribution of Actinomyces viscosus and Actinomyces naeslundii in the human oral cavity. Infection and Immunity, 14(5), 1119-1124.
    1. FAO/WHO. (2002). Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report.
    1. Ferreira, M. C., Dias-Pereira, A. C., Branco-de-Almeida, L. S., Martins, C. C., & Paiva, S. M. (2017). Impact of periodontal disease on quality of life: A systematic review. Journal of Periodontal Research, 52(4), 651-65.
    1. Gomes-Filho, I. S., Trindade, S. C., Passos-Soares, J. S., Figueiredo, A. C. M. G., Vianna, M. I. P., Hintz, A. M., Batista, éE. T., Orrico, G. S., Conceição, S. S., Coelho, J. M. F., Santos, N. P., Nascimento, M. T., Miranda, S. S., Xavier Ramos, M., Lima Porto, E. C., alencar Cruz, C., Carvalho, S. S., & Seixas da Cruz, S. (2018). Critical appraisal of systematic and narrative reviews of literature in the field of orthodontics. Journal of Dental Health, Oral Disorders & Therapy, 9(5), 354-356.
    1. Gupta, G. (2011). Probiotics and periodontal health. Journal of Medicine and Life, 4(4), 387-394.
    1. Hirasawa, M., & Kurita-Ochia, T. (2020). Probiotic potential of lactobacilli isolated from saliva of periodontally healthy individuals. Oral Health & Preventive Dentistry, 18(1), 563-70.
    1. Johnston, W., Rosier, B. T., Artacho, A., Paterson, M., Piela, K., Delaney, C., Brown, J. L., Ramage, G., Mira, A., & Culshaw, S. (2021). Mechanical biofilm disruption causes microbial and immunological shifts in periodontitis patients. Scientific Reports, 11(1):9796.
    1. Kelly, N., Winning, L., Irwin, C., Lundy, F. T., Linden, D., McGarvey, L., Linden, G. J., & El Karim, I. A. (2021). Periodontal status and chronic obstructive pulmonary disease (COPD) exacerbations: A systematic review. BMC Oral Health, 21(1):425.
    1. Kolenbrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S., & Palmer, R. J., Jr. (2002). Communication among oral bacteria. Microbiology and Molecular Biology Reviews, 66(3), 486-505.
    1. Koll-Klais, P., Mandar, R., Leibur, E., Marcotte, H., Hammarstrom, L., & Mikelsaar, M. (2005). Oral lactobacilli in chronic periodontitis and periodontal health: Species composition and antimicrobial activity. Oral Microbiology and Immunology, 20(6), 354-361.
    1. Kuru, B. E., Laleman, I., Yalnızoğlu, T., Kuru, L., & Teughels, W. (2017). The influence of a Bifidobacterium animalis probiotic on gingival health: A randomized controlled clinical trial. Journal of Periodontology, 88(11), 1115-23.
    1. Laleman, I., Pauwels, M., Quirynen, M., & Teughels, W. (2020). A dual-strain Lactobacilli reuteri probiotic improves the treatment of residual pockets: A randomized controlled clinical trial. Journal of Clinical Periodontology, 47(1), 43-53.
    1. Lu, K., Dong, S., Wu, X., Jin, R., & Chen, H. (2021). Probiotics in cancer. Frontiers in Oncology, 11, 638148.
    1. Mashimo, C., Yamane, K., Yamanaka, T., Maruyama, H., Wang, P. L., Komasa, S., Okazaki, J., & Nambu, T. (2016). Genome sequence of Actinomyces naeslundii strain ATCC 27039, isolated from an abdominal wound abscess. Genome Announcements, 4(6):e01443-16.
    1. Myneni, S. R., Brocavich, K., & Wang, H. (2020). Biological strategies for the prevention of periodontal disease: Probiotics and vaccines. Periodontology 2000, 84(1), 161-175.
    1. Na, H. S., Kim, S. Y., Han, H., Kim, H.-J., Lee, J.-Y., Lee, J.-H., & Chung, J. (2020). Identification of potential oral microbial biomarkers for the diagnosis of periodontitis. Journal of Clinical Medicine, 9(5):1549.
    1. Navazesh, M. (1993). Methods for collecting saliva. Annals of the New York Academy of Sciences, 694, 72-77.
    1. Nikolic, M. (2008). Characterization of lactic acid bacteria isolated from Bukuljac, a homemade goat's milk cheese. International Journal of Food Microbiology, 122(1-2), 162-170.
    1. Patel, R. (2016). New developments in clinical bacteriology laboratories. Mayo Clinic Proceedings, 91(10), 1448-1459.
    1. Pelekos, G., Acharya, A., Eiji, N., Hong, G., Leung, W. K., & McGrath, C. (2020). Effects of adjunctive probiotic L. reuteri lozenges on S/RSD outcomes at molar sites with deep pockets. Journal of Clinical Periodontology, 47(9), 1098-107.
    1. Pirih, F. Q., Monajemzadeh, S., Singh, N., Sinacola, R. S., Shin, J. M., Chen, T., Fenno, J. C., Kamarajan, P., Rickard, A. H., Travan, S., Paster, B. J., & Kapila, Y. (2021). Association between metabolic syndrome and periodontitis: The role of lipids, inflammatory cytokines, altered host response, and the microbiome. Periodontology 2000, 87(1), 50-75.
    1. Raghuwanshi, S., Misra, S., & Bisen, P. (2015). Indian perspective for probiotics: A review. Indian Journal of Dairy Science, 68(3), 195-205.
    1. Rahne, M., Basic, A., & Almståhl, A. (2021). Explorative study on Lactobacillus species and their acid-producing capacity and anti-microbial activity in head and neck cancer patients. Clinical and Experimental Dental Research, 7(5), 924-933.
    1. Samot, J., & Badet, C. (2013). Antibacterial activity of probiotic candidates for oral health. Anaerobe, 19, 34-38.
    1. Sankarapandian, V., Venmathi Maran, B. A., Rajendran, R. L., Jogalekar, M. P., Gurunagarajan, S., Krishnamoorthy, R., Gangadaran, P., & Ahn, B. C. (2022). An update on the effectiveness of probiotics in the prevention and treatment of cancer. Life, 12(1):59.
    1. Sanz, M., Marco Del Castillo, A., Jepsen, S., Gonzalez-Juanatey, J. R., D'Aiuto, F., Bouchard, P., Chapple, I., Dietrich, T., Gotsman, I., Graziani, F., Herrera, D., Loos, B., Madianos, P., Michel, J. B., Perel, P., Pieske, B., Shapira, L., Shechter, M., Tonetti, M., … Wimmer, G. (2020). Periodontitis and cardiovascular diseases: Consensus report. Journal of Clinical Periodontology, 47(3), 268-288.
    1. Schlagenhauf, U., Rehder, J., Gelbrich, G., & Jockel-Schneider, Y. (2020). Consumption of Lactobacillus reuteri-containing lozenges improves periodontal health in navy sailors at sea: A randomized controlled trial. Journal of Periodontology, 91(10), 1328-1338.
    1. Shimauchi, H., Mayanagi, G., Nakaya, S., Minamibuchi, M., Ito, Y., Yamaki, K., & Hirata, H. (2008). Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: A randomized, double-blind, placebo-controlled study. Journal of Clinical Periodontology, 35(10), 897-905.
    1. Shokryazdan, P., Sieo, C. C., Kalavathy, R., Liang, J. B., Alitheen, N. B., Faseleh Jahromi, M., & Ho, Y. W. (2014). Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. BioMed Research International, 2014, 927268.
    1. Silva, G. A., Moreira, A. L. G., Silva, P. H. F., Salvador, S. L., Casarin, R. C. V., Vicente, R. M., Ferreira, G. C., Tanus-Santos, J. E., Furlaneto, F. A. C., & Messora, M. R. (2022). The use of probiotics can reduce the severity of experimental periodontitis in rats with metabolic syndrome: An immunoenzymatic and microtomographic study. Journal of Periodontology, 93(2), e1-e12.
    1. Sookkhee, S., Chulasiri, M., & Prachyabrued, W. (2001). Lactic acid bacteria from healthy oral cavity of Thai volunteers: Inhibition of oral pathogens. Journal of Applied Microbiology, 90(2), 172-179.
    1. Sornplang, P., & Piyadeatsoontorn, S. (2016). Probiotic isolates from unconventional sources: A review. Journal of Animal Science and Technology, 58, 26.
    1. Suzuki, J. B., & Delisle, A. L. (1984). Pulmonary actinomycosis of periodontal origin. Journal of Periodontology, 55(10), 581-584.
    1. Terai, T., Okumura, T., Imai, S., Nakao, M., Yamaji, K., Ito, M., Nagata, T., Kaneko, K., Miyazaki, K., Okada, A., Nomura, Y., & Hanada, N. (2015). Screening of probiotic candidates in human oral bacteria for the prevention of dental disease. PLoS One, 10(6):e0128657.
    1. Testa, M. M., Ruiz de Valladares, R., & Benito de Cardenas, I. L. (2003). Antagonistic interactions among Fusobacterium nucleatum and Prevotella intermedia with oral lactobacilli. Research in Microbiology, 154(10), 669-675.
    1. Teughels, W., Durukan, A., Ozcelik, O., Pauwels, M., Quirynen, M., & Haytac, M. C. (2013). Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study. Journal of Clinical Periodontology, 40(11), 1025-1035.
    1. Zhang, X., Ali Esmail, G., Fahad Alzeer, A., Valan Arasu, M., Vijayaraghavan, P., Choon Choi, K., & Abdullah Al-Dhabi, N. (2020). Probiotic characteristics of Lactobacillus strains isolated from cheese and their antibacterial properties against gastrointestinal tract pathogens. Saudi Journal of Biological Sciences, 27(12), 3505-13.

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