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Bacteria of healthy periodontal tissues as candidates of probiotics: a systematic review

European Journal of Medical Research volume 29, Article number: 328 (2024) Cite this article

Abstract

Objectives

The use of probiotics could promote the balance of the subgingival microbiota to contribute to periodontal health. This study aimed to identify the potential of bacteria commonly associated with healthy periodontal tissues as probiotic candidates.

Material and methods

A systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines using the PubMed, Scopus, Science Direct, ProQuest, and Ovid databases as well as the combination of Medical Subject Headings (MeSH) and non-MeSH terms. Based on the selection criteria, original studies published in English and identifying the microorganisms present in the periodontium of healthy individuals and patients with periodontitis using the high-throughput 16S ribosomal gene sequencing technique were included.

Results

Out of 659 articles, 12 met the criteria for this review. These articles were published from 2012 to 2020 and mainly originated from the United States, China, and Spain. Most of these studies reported adequate criteria for selecting participants, using standardized clinical criteria, and compliance with quality based on the tools used. In periodontal healthy tissue were identified species like Actinomyces viscosus, Actinomyces naeslundii, Haemophilus parainfluenzae, Rothia dentocariosa, Streptococcus sanguinis, Streptococcus mitis, Streptococcus oralis, Streptococcus gordonii, Streptococcus intermedius, and Prevotella nigrescens which have recognized strains with a capacity to inhibit periodontopathogens.

Conclusions

S. sanguinis, S. oralis, S. mitis, and S. gordonii are among the bacterial species proposed as potential probiotics because some strains can inhibit periodontopathogens and have been reported as safe for humans.

Introduction

Periodontitis is a chronic and inflammatory disease of bacterial etiology that results in loss of periodontal attachment [1]. In periodontitis, the gums detach from the teeth, and the supporting tissues are destroyed in the most advanced and severe stages, thereby leading to bone and tooth loss [2]. Moreover, this disease has been associated with several other important conditions, such as diabetes, cardiovascular diseases, and Alzheimer’s disease [3]. Periodontitis affects approximately 50% of the adult population worldwide [4] with varying degrees of severity and approximately 11% of this population has severe periodontitis [5]. In Colombia, 61.8% of the population has periodontitis, and 10.6% of cases are classified as severe periodontitis [6].

Microbiological and molecular studies were used to distinguish the microbiota associated with healthy periodontium from those associated with diseased periodontium [7]. For example, gram-positive and some gram-negative bacteria have been associated with a healthy state. Actinomyces and Streptococcus species are the first colonizers of pristine tooth surfaces and co-aggregate to form early dental biofilm. Notably, bacteria identified in healthy periodontal tissue samples include Peptostreptococcus, Gemella, Veillonella, Capnocytophaga, Neisseria, Rothia, and Corynebacterium [7,8,9]. Bacteria such as Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola have been identified in patients with periodontal disease. In addition, these patients had bacteria characterized by the presence of virulence factors associated with alteration in the tissue immune response (e.g., activation of destructive proinflammatory patterns or evasion of the immune response) and destruction of periodontal tissues (e.g., by lytic enzymes), promoting the onset and development of severe diseases [9, 10].

Other microbiological features of periodontitis are the presence of a greater diversity of bacteria and significant differences between the functional profiles of these microorganisms and those of healthy periodontium. In addition, a decrease, but not disappearance, in the proportion of some bacterial genera and species associated with healthy periodontium has been observed [9, 11]. These properties reflect the approach to disease onset: instead of a few pathogens, a dysbiotic polymicrobial community is considered to generate harmful inflammatory responses that perpetuate the imbalance or dysbiosis of the microbiota and its environment [11].

In addition to the accumulation of a diverse bacterial population in the sulcus of the gingiva, other risk factors are known to be involved in the occurrence of dysbiosis in systemically healthy individuals. These include unhealthy diet, smoking, and other habits that alter the environment of the tissues, i.e., the availability of oxygen and nutrients [12]. This promotes the emergence of a range of microorganisms, mainly bacteria, which act synergistically to enhance their metabolic activities, causing changes in the composition of the microbiota and thereby damaging periodontal tissues [7, 11, 13, 14].

Among the novel treatments being investigated for controlling periodontitis and maintaining a healthy periodontium, probiotics have been proposed as adjuvants to traditional treatments. Probiotics include live beneficial microorganisms that benefit the host when administered in sufficient quantity because they have properties that inhibit pathogenic microorganisms through the production of antimicrobial components or competition for host nutrients or tissue-binding sites. Furthermore, they may have immunomodulation properties, further strengthening the immune response [15].

The bacterial genera Lactobacillus and Bifidobacterium are most widely studied as probiotics to prevent periodontitis or as adjuvants during its treatment. Notably, these bacteria can inhibit periodontal pathogens and are safe for human consumption. However, even after examining the same probiotic strains, not all studies have discovered beneficial or consistent outcomes in clinical indices and/or in controlling the pathogenic microbiota [16,17,18]. This can be explained by various factors, such as the different administration routes, doses, and quantities; combinations with other probiotics; administration times; and/or sample sizes of clinical studies [16,17,18]. In addition, these bacteria are not normally abundant in periodontal tissues [8, 11], and some bacteria are of intestinal origin, which may affect their ability to colonize the oral cavity [19]. This further limits their effectiveness as probiotics; thus, further studies are needed to identify or investigate probiotics suitable for this tissue and periodontal health.

Bacteria that are more frequently in the microbiota of the healthy periodontium and have probiotic characteristics could be analyzed as possible probiotic candidates [20, 21]. Therefore, this review aimed to identify bacteria with probiotic characteristics in the microbiota of the healthy periodontium for treating periodontitis.

Material and methods

Type of study and search strategy

We conducted a systematic review of the literature as per the updated quality criteria of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement. The PubMed, ScienceDirect, Scopus, and Ovid databases were used to search for articles from July 2012 to April 2022 using both Medical Subject Headings (MeSH) and non-MeSH terms (Table 1); in addition, the associated filters for year and type of study were used. Furthermore, we conducted a manual search of information.

Table 1 Keywords and combinations according to the database
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The PICO format, Population (healthy population), Intervention (metagenomic analysis), Comparison (patients with periodontitis), Outcome (group of potential probiotics for the treatment of periodontitis), was used to formulate our clinical question: Which bacteria with probiotic characteristics for the treatment of periodontitis predominate in the microbiota of the periodontium of healthy patients? Inclusion criterion was original studies published in English that identified microorganisms present in subgingival tissue samples of healthy individuals using the high-throughput sequencing technique of the 16S ribosomal gene. Studies that did not identify bacteria in samples from healthy adults and patients with periodontitis in the same analysis and articles that did not report the nationality and/or sex of the patients were excluded. In addition, we selected studies that excluded patients with systemic diseases, those treated with antibiotics or other types of drugs, or those who were receiving periodontal treatment for at least 3 months before collecting the subgingival tissue samples.

Selection of the studies and collection of data

First, studies with unique titles were identified, their abstracts were read, and, eventually, those related to the purpose of the present study were selected. The selected studies were then thoroughly read to verify compliance with the selection criteria, leaving the final articles for review. This process was carried out by two researchers (MPAD and DM).

Finally, the studies were synthesized using the defined variables, including authors, origin, and type of the study; clinical parameters of the patients; selection criteria; analyzed samples; amplified sequence; and periodontal tissue bacteria identified in healthy individuals.

Level of evidence and risk of bias

The quality of the articles included in this review was assessed by two researchers (MPAD and CF) using the Joanna Briggs Institute (JBI) scale for case–control and cross-sectional studies. This scale enabled the evaluation of reliability, relevance, and results of the selected articles.

Results

Selection of studies and characteristics of the studies

Overall, 659 unique articles were found based on the information search; of these, 23 were selected for full reading, and 12 that met the selection criteria were eventually selected for review (Fig. 1). Most investigations were conducted in the United States (n = 4), followed by China (n = 2) and Spain (n = 2). The remaining four studies were conducted in Chile, Germany, Japan, and the Czech Republic (Table 2). The most common study types were case–control (58.3%, n = 7) and cross-sectional (41.6%, n = 5) studies (Fig. 1). Neither of the selected studies was a randomized clinical trial (Table 2).

Fig. 1
figure 1

Information flowchart of the different stages of a systematic review

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Table 2 Characteristics of the included studies
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Regarding patient selection, in addition to the exclusion criteria established in this study, some authors excluded pregnant and lactating patients, patients who had recently undergone prophylactic procedures, patients receiving oral antiseptics, smokers (only one study), patients with a certain number of natural teeth, etc. (Table 2).

Clinical criteria for the selection of healthy individuals were as follows: probing depth (PD) of < 2 to < 4 mm, clinical attachment level/loss (CAL) of 0 to < 4 mm, no bleeding on probing (BOP) or BOP in at least 10–20% of measured sites, no radiographic evidence of alveolar bone loss, and/or no evidence of inflammation. In most studies, samples were collected using paper points (66.7%, n = 8), whereas only two studies used curettes for sample collection (Table 2).

Regarding the most used amplified regions to identify bacteria, V1–V3 were predominantly used, followed by V4 (Table 2). Other regions used were V1–V2, V3, V3–V4, V4–V5, and V7–V9.

Bacteria of periodontal healthy tissue

Bacteria that were frequently identified by their presence and/or abundance in healthy periodontal tissue in the different reviewed studies included those from the genera Acinetobacter, Actinomyces, Aggregatibacter, Capnocytophaga, Corynebacterium, Gemella, Granulicatella, Haemophilus, Lautropia, Leptotrichia, Neisseria, Porphyromonas, Prevotella, Rothia, Streptococcus, and Veillonella. In particular, the species identified in each of these genera were Acinetobacter junii, A. antiviralis, A. baumannii, A. calcoaceticus, A. rhizosphaerae, Actinomyces naeslundii, A. viscosus, A. massiliensis, A. meyeri, Aggregatibacter aphrophilus, Capnocytophaga gingivalis, Corynebacterium matruchotti, Gemella morbillorum, Gemella haemolysans, Granulicatella adiacens, Haemophillus parainfluenzae, H. haemolyticus, H. parahaemolyticus, H. sputorum, Lautropia mirabilis, Neisseria lactamica, N. flava, N. subflava, N. oralis, Porphyromonas catoniae, Prevotella histicola, P. nigrescens, Rothia aeria, R. dentocariosa, Streptococcus sanguinis, S. mitis, S. intermedius, S. oralis, S. tigurinus, S. infantis, S. gordonii, Veillonella atypica, and V. dispar/V. parvula (Table 2, Fig. 2).

Fig. 2
figure 2

Summary of bacteria of healthy periodontal tissues as candidates of probiotics

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Bacteria like A. viscosus, A. naeslundii, G. haemolysans, H. parainfluenzae, P. nigrescens, R. dentocariosa, S. sanguinis, S. mitis, S. oralis, S. gordonii, and S. intermedius have characteristics like probiotics because they permit modulate the periodontal pathogenic microbiota. However, some strains have been associated with oral or systemic infections, particularly in patients with immune deficiencies. Also, these strains have shown antibiotic resistance (Table 3, Fig. 2).

Table 3 Bacteria that were frequently identified by their presence and/or abundance in healthy periodontal tissue and probiotics properties
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Level of evidence and risk of bias

Based on the JBI tool assessment, most studies met most quality criteria. Only two case–control studies and one cross-sectional study did not meet the identification criteria for confounding factors. Furthermore, the findings of one case–control and two cross-sectional studies were unclear in identifying the confounding factors (Appendix A1 and Appendix A2).

Discussion

Bacteria must meet certain requirements to be candidates for probiotics, including the ability to colonize the tissues in which they will act [76]; therefore, it is important to identify commensal bacteria that are common or abundant in healthy periodontal tissues [77]. In the present review, we found that both gram-positive and gram-negative bacteria were associated with the subgingival biofilm of healthy periodontium in the reviewed studies. These bacteria mainly comprised facultative anaerobes, including those from the genera Acinetobacter, Actinomyces, Aggregatibacter, Capnocytophaga, Corynebacterium, Gemella, Granulicatella, Haemophilus, Lautropia, Leptotrichia, Neisseria, Porphyromonas, Prevotella, Rothia, Streptococcus, and Veillonella.

Furthermore, bacteria of genera, such as Gemella (G. haemolysans), Granulicatella (G. adiacens), Haemophilus (H. parainfluenzae), Lautropia (L. mirabilis), Neisseria (N. flava, N. subflava, and N. oralis), Rothia (R. aeria and Rothia dentocariosa), Streptococcus (S. sanguinis, S. mitis, S. oralis, S. gordonii, and S. intermedius), Porphyromonas (P. catoniae), and Prevotella (P. nigrescens), were also reported as bacteria specific to patients with healthy periodontium in investigations excluded from this review based on the defined selection criteria [7, 10, 78,79,80,81,82,83]. In contrast, other genera, such as Acinetobacter (A. junii, A. antiviralis, A. baumannii, A. calcoaceticus, and A. rhizosphaerae), have been relatively frequently associated with disease conditions [84, 85].

Another frequently reported genus is Actinomyces spp., with the species having favorable properties for periodontal health, e.g., A. viscosus and A. naeslundii, and the species associated with periodontal disease, e.g., A. massiliensis, A. odontolyticus/meyeri, and, again, A. naeslundii [86].

Other bacteria that lead to discrepancies since they are associated with health or disease conditions are Aggregatibacter (A. aphrophilus), Capnocytophaga (C. gingivalis), Corynebacterium (C. matruchotti), and Veillonella (V. atypica, V. dispar/V. parvula) [7, 87]. These discrepancies may be attributed to the fact that the microbiome of healthy periodontal tissue demonstrates greater interpersonal variability than that of patients with periodontitis or gingivitis. This may indicate that the microbiome's composition can be influenced by environmental factors. Other factors that may affect the composition are as follows: diagnosis by selecting healthy controls, which may have caused an imbalance in the microbiota, as such individuals have no clinical symptoms; differences in criteria or clinical measures used to define healthy individuals, as noted in this review; differences in the individual experiences of the examiners; and differences in the sequenced region [8].

Another characteristic of probiotics is the ability to inhibit pathogens by producing antimicrobial agents or competing for nutrients, space, or environmental conditions [88]. Notably, the metatranscriptome analysis of subgingival plaque collected from healthy individuals revealed the expression of genes associated with competition, bacteriocin production (mutation), and quorum sensing [89]. Of the bacteria identified in the present review, A. viscosus, A. naeslundii, G. haemolysans, H. parainfluenzae, P. nigrescens, R. dentocariosa, S. sanguinis, S. mitis, S. oralis, S. gordonii, and S. intermedius have been reported as those capable of inhibiting the growth of periodontopathogens [50, 68, 90, 91]. For example, G. haemolysans produces an inhibitor of P. gingivalis; however, it does not inhibit other periodontal pathogens, such as F. nucleatum and T. denticola [45]. Notably, H. parainfluenzae has been reported to have the ability to inhibit the adhesion of periodontopathogenic bacteria, particularly P. gingivalis [48]. Streptococcus strains secrete substances that cause the lysis of P. gingivalis or eliminate its ability to generate a biofilm by affecting the expression of fimA and mfa-1, which are the components of the fimbria of P. gingivalis [66]. Regarding P. nigrescens, antimicrobial activity has been demonstrated against Actinomyces spp., P. gingivalis, P. intermedia, and T. forsythensis by a bacteriocin called nigrescin [68].

Bacteria must also meet other requirements to be candidates for probiotics; these include being harmless, having no pathogenic genes, and showing no characteristics of acquired antibiotic resistance [92, 93]. Some strains of the bacteria that were identified as possible candidates in the present review were found to cause endocarditis and opportunistic infections, as observed with G. haemolysans and H. parainfluenzae [46, 49]. In addition, P. nigrescens belongs to a genus of bacteria associated with pulp infections, periodontitis, and abscesses of dental and periodontal origin, and it is resistant to antibiotics [94]. In a study comparing different species of Prevotella (P. intermedia, P. nigrescens, and P. melaninogenica), P. nigrescens showed the greatest ability to resist amoxicillin/clavulanic acid, amoxicillin, and clindamycin, and it had more resistant genes to beta-lactams, tetracyclines, and lincosamides [94].

The genus Streptococcus includes a wide variety of species previously established as probiotics for human consumption owing to their proven safety [95, 96]. These bacteria are easy to culture under in vitro conditions. For example, the bacterium S. oralis, specifically the KJ3 strain, is used in a commercial product with proven safety for human consumption [63]. In addition, S. mitis strain YIT 12322 has been studied and found safe for humans [97]. Therefore, Streptococcus is a genus with strains such as those identified in the actual review (S. oralis, S. mitis, S. sanguinis, and S. gordonii) that could be used in future clinical trials. The strain KJ3 of S. oralis, along with S. uberis strain KJ2 and S. rattus strain JH145, constitutes a commercial product named ProBiora®. This product has shown to reduce pathogenic bacteria like S. mutans, Campylobacter rectus, and P. gingivalis in saliva and dental biofilm from young individuals [98]. Another strain of S. oralis is the sub-species dentisani strain 7746, which can adhere to the tooth to stabilize the pH through arginolytic activities and the production of bacteriocin which inhibits the growth of cariogenic bacteria and periodontopathogens [99]. Through a clinical study, strain 7746 was applied to a dental alginate ferrule every 48 h for one month in patients between 18 and 65 years old. The authors found improved clinical parameters like dental biofilm index, gingival index, and salivary flux [100].

Other bacteria suggested as probiotic candidates are S. mitis and S. sanguinis, which are primary colonizers of the oral cavity; these bacteria are characterized by inhibiting the adhesion of P. gingivalis, A. actinomycetemcomitans, P. gingivalis y P. intermedia to producing H2O2 [101]. These bacteria were used in replacement therapy for periodontitis in an animal model (dog), where the authors found, after a treatment of 12 weeks, a significant increase in the bone level in the treated periodontal pocket [102].

Finally, another probiotic candidate is S. gordonii which promotes the homeostasis of the biofilm through the inhibition of periodontopathogens like T. denticola, and P. gingivalis [103]. Also, S. gordonii causes a beneficial effect on the oral epithelium, stimulating the immune system (activating antigen-presenting cells) [104]. S. gordonii can modulate the expression of genes of gingival epithelial cells and decrease the expression of proinflammatory cytokines, indicating an anti-inflammatory potential [105].

However, some strains of the oral streptococci have been isolated from patients with infective endocarditis and other opportunistic infections [106, 107], underscoring the importance of evaluating the safety of bacterial strains as candidate probiotics before conducting clinical trials.

For the prevention or adjuvant treatment of periodontal disease through probiotics, the candidates must be able to maintain or restore the periodontal microecological balance. For this reason, it is necessary to combine several bacterial strains, which, in addition to possessing properties for the control of periodontopathogenic bacteria and regulation of the immune response of the host, comply with the corresponding safety for its use and ease of production at the industrial level.

This study has some limitations. First, not all studies included some factors affecting the microbiota, and therefore, they did not exclude patients who were smokers or pregnant and/or breastfeeding. Second, not all studies used the same number of healthy teeth, similar durations of treatment with antibiotics or other drugs, or similar clinical measures that distinguished between healthy individuals and patients with periodontitis. Finally, although species of bacteria with probiotic properties were identified, not all strains of the same species have the same properties. Nevertheless, this information allows us to focus our studies on the species identified, to isolate and study the most appropriate strains as probiotics.

Conclusion

There are several important variations in the microbiota associated with healthy periodontal tissue—an area where several of these bacteria have also been reported in disease conditions. This is not only related to the methodological differences between the studies but also to the characteristics of the patients and the nature of their native bacterial strains as well as their virulence factors and the metabolic interactions triggered. Therefore, it is important to reconsider the probiotic strategy because these agents favor the presence of beneficial native bacteria in these tissues.

This study identified bacteria that could be key candidates for maintaining the oral microbiota of periodontal tissues owing to their association with health conditions and their antimicrobial properties. These bacteria include those of the genus Streptococcus, such as S. sanguinis, S. oralis, and S. mitis, which have been studied as probiotics for oral health, but these bacterial strains must be selected based on their safety for human consumption.

Availability of data and materials

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  1. Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Clin Periodontol. 2018;45(20):S149–61. https://doi.org/10.1111/jcpe.12945.

    Article  PubMed  Google Scholar 

  2. American Academy of Periodontology. Gume disease information. https://www.perio.org/for-patients/gum-disease-information/. Accessed 16 Jan 2023.

  3. Bui FQ, Almeida-da-Silva CLC, Huynh B, Trinh A, Liu J, Woodward J, Asadi H, Ojcius DM. Association between periodontal pathogens and systemic disease. Biomed J. 2019;42(1):27–35. https://doi.org/10.1016/j.bj.2018.12.001.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sanz M, D’Aiuto F, Deanfield J, Fernandez-Avilés F. European workshop in periodontal health and cardiovascular diseases. Eur Heart. 2010;12(B):3–12. https://doi.org/10.1093/eurheartj/suq003.

    Article  Google Scholar 

  5. Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJL, Marcenes W. Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression. J Dent Res. 2014;93(11):1045–53. https://doi.org/10.1177/0022034514552491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ministerio de Salud y Protección Social. IV Estudio Nacional de Salud Bucal ENSAB IV. Ministerio de Salud y Protección Social, Bogotá. 2014. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ENSAB-IV-Situacion-Bucal-Actual.pdf.

  7. Curtis MA, Diaz PI. Van Dyke TE (2020) The role of the microbiota in periodontal disease. Periodontol. 2000;83(1):14–25. https://doi.org/10.1111/prd.12296.

    Article  Google Scholar 

  8. Lenartova M, Tesinska B, Janatova T, Hrebicek O, Mysak J, Janata J, Najmanova L. The oral microbiome in periodontal health. Front Cell Infect Microbiol. 2021;11: 629723. https://doi.org/10.3389/fcimb.2021.629723.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Meuric V, Le Gall-David S, Boyer E, Acuña-Amador L, Martin B, Fong SB, Barloy-Hubler F, Bonnaure-Mallet M. Signature of microbial dysbiosis in periodontitis. Appl Environ Microbiol. 2017;83(14):e00462-e517. https://doi.org/10.1128/AEM.00462-17.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–44. https://doi.org/10.1111/j.1600-051X.1998.tb02419.x.

    Article  CAS  PubMed  Google Scholar 

  11. Abusleme L, Hoare A, Hong BY, Diaz PI. Microbial signatures of health, gingivitis, and periodontitis. Periodontol. 2021;86(1):57–78. https://doi.org/10.1111/prd.12362.

    Article  Google Scholar 

  12. AlJehani YA. Risk factors of periodontal disease: review of the literature. Int J Dent. 2014;2014: 182513. https://doi.org/10.1155/2014/182513.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res. 1994;8(2):263–71. https://doi.org/10.1177/08959374940080022001.

    Article  CAS  PubMed  Google Scholar 

  14. Lamont RJ, Koo H, Hajishengallis G. The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol. 2018;16(12):745–59. https://doi.org/10.1038/s41579-018-0089-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gheisary Z, Mahmood R, Harri Shivanantham A, Liu J, Lieffers JRL, Papagerakis P, Papagerakis S. The clinical, microbiological, and immunological effects of probiotic supplementation on prevention and treatment of periodontal diseases: a systematic review and meta-analysis. Nutrients. 2022;14(5):1036. https://doi.org/10.3390/nu14051036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ng E, Tay JRH, Ong MMA, Bostanci N, Belibasakis GN, Seneviratne CJ. Probiotic therapy for periodontal and peri-implant health—silver bullet or sham? Benef Microbes. 2021;12(3):215–30. https://doi.org/10.3920/BM2020.0182.

    Article  CAS  PubMed  Google Scholar 

  17. Ng E, Tay JRH, Saffari SE, Lim LP, Chung KM, Ong MMA. Adjunctive probiotics after periodontal debridement versus placebo: a systematic review and meta-analysis. Acta Odontol Scand. 2022;80(2):81–90. https://doi.org/10.1080/00016357.2021.1942193.

    Article  PubMed  Google Scholar 

  18. Hardan L, Bourgi R, Cuevas-Suárez CE, Flores-Rodríguez M, Omaña-Covarrubias A, Nicastro M, Lazarescu F, Zarow M, Monteiro P, Jakubowicz N, Proc P, Lukomska-Szymanska M. The use of probiotics as adjuvant therapy of periodontal treatment: a systematic review and meta-analysis of clinical trials. Pharmaceutics. 2022;14(5):1017. https://doi.org/10.3390/pharmaceutics14051017.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Marsh PD. In sickness and in health-what does the oral microbiome mean to us? An ecological perspective. Adv Dent Res. 2018;29(1):60–5. https://doi.org/10.1177/0022034517735295.

    Article  CAS  PubMed  Google Scholar 

  20. Hirasawa M, Kurita-Ochia T. Probiotic potential of lactobacilli isolated from saliva of periodontally healthy individuals. Oral Health Prev Dent. 2020;18(1):563–70. https://doi.org/10.3290/j.ohpd.a44693.

    Article  PubMed  Google Scholar 

  21. Bazireh H, Shariati P, Azimzadeh Jamalkandi S, Ahmadi A, Boroumand MA. Isolation of novel probiotic Lactobacillus and Enterococcus strains from human salivary and fecal sources. Front Microbiol. 2020;11: 597946. https://doi.org/10.3389/fmicb.2020.597946.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK, Podar M, Leys EJ. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 2012;6(6):1176–85. https://doi.org/10.1038/ismej.2011.191.

    Article  CAS  PubMed  Google Scholar 

  23. Kumar PS, Mason MR, Brooker MR, O’Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol. 2012;39(5):425–33. https://doi.org/10.1111/j.1600-051X.2012.01856.x.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, Gamonal J, Diaz PI. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013;7(5):1016–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Li Y, He J, He Z, Zhou Y, Yuan M, Xu X, Sun F, Liu C, Li J, Xie W, Deng Y, Qin Y, VanNostrand JD, Xiao L, Wu L, Zhou J, Shi W, Zhou X. Phylogenetic and functional gene structure shifts of the oral microbiomes in periodontitis patients. ISME J. 2014;8(9):1879–91. https://doi.org/10.1038/ismej.2014.28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kirst ME, Li EC, Alfant B, Chi YY, Walker C, Magnusson I, Wang GP. Dysbiosis and alterations in predicted functions of the subgingival microbiome in chronic periodontitis. Appl Environ Microbiol. 2015;81(2):783–9. https://doi.org/10.1128/AEM.02712-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Camelo-Castillo AJ, Mira A, Pico A, Nibali L, Henderson B, Donos N, Tomás I. Subgingival microbiota in health compared to periodontitis and the influence of smoking. Front Microbiol. 2015;6:119. https://doi.org/10.3389/fmicb.2015.00119.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Chen C, Hemme C, Beleno J, Shi ZJ, Ning D, Qin Y, Tu Q, Jorgensen M, He Z, Wu L, Zhou J. Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy. ISME J. 2018;12(5):1210–24. https://doi.org/10.1038/s41396-017-0037-1.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Schulz S, Porsch M, Grosse I, Hoffmann K, Schaller HG, Reichert S. Comparison of the oral microbiome of patients with generalized aggressive periodontitis and periodontitis-free subjects. Arch Oral Biol. 2019;99:169–76. https://doi.org/10.1016/j.archoralbio.2019.01.015.

    Article  CAS  PubMed  Google Scholar 

  30. López-Martínez J, Chueca N, Padial-Molina M, Fernandez-Caballero JA, García F, O’Valle F, Galindo-Moreno P. Bacteria associated with periodontal disease are also increased in health. Med Oral Patol Oral Cir Bucal. 2020;25(6):e745–51. https://doi.org/10.4317/medoral.23766.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ikeda E, Shiba T, Ikeda Y, Suda W, Nakasato A, Takeuchi Y, Azuma M, Hattori M, Izumi Y. Japanese subgingival microbiota in health vs disease and their roles in predicted functions associated with periodontitis. Odontology. 2020;108(2):280–91. https://doi.org/10.1007/s10266-019-00452-4.

    Article  CAS  PubMed  Google Scholar 

  32. Lu C, Chu Y, Liu JR, Liu WY, Ouyang XY. Subgingival microbial profiles of young chinese adults with stage i/ii periodontitis, gingivitis and periodontal health status. Chin J Dent Res. 2021;24(3):167–75. https://doi.org/10.3290/j.cjdr.b1965003.

    Article  PubMed  Google Scholar 

  33. Hung YT, Lee YT, Huang LJ, Chen TL, Yu KW, Fung CP, Cho WL, Liu CY. Clinical characteristics of patients with Acinetobacter junii infection. J Microbiol Immunol Infect. 2009;42(1):47–53.

    PubMed  Google Scholar 

  34. Al Atrouni A, Joly-Guillou ML, Hamze M, Kempf M. Reservoirs of non-baumannii Acinetobacter species. Front Microbiol. 2016;7:49. https://doi.org/10.3389/fmicb.2016.00049.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ayoub Moubareck C, Hammoudi Halat D. Insights into Acinetobacter baumannii: A review of microbiological, virulence, and resistance traits in a threatening nosocomial pathogen. Antibiotics. 2020;9(3):119. https://doi.org/10.3390/antibiotics9030119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hunt JP, Buechter KJ, Fakhry SM. Acinetobacter calcoaceticus pneumonia and the formation of pneumatoceles. J Trauma. 2000;48(5):964–70. https://doi.org/10.1097/00005373-200005000-00027.

    Article  CAS  PubMed  Google Scholar 

  37. Raphael E, Riley LW. Infections caused by antimicrobial drug-resistant saprophytic gram-negative bacteria in the environment. Front Med. 2017;4:183. https://doi.org/10.3389/fmed.2017.00183.

    Article  Google Scholar 

  38. Guo Y, Wei C, Liu C, Li D, Sun J, Huang H, Zhou H. Inhibitory effects of oral Actinomyces on the proliferation, virulence and biofilm formation of Candida albicans. Arch Oral Biol. 2015;60(9):1368–74. https://doi.org/10.1016/j.archoralbio.2015.06.015.

    Article  PubMed  Google Scholar 

  39. Hsiao YC, Lee YH, Ho CM, Tseng CH, Wang JH. Clinical characteristics of Actinomyces viscosus bacteremia. Medicina. 2021;57(10):1064. https://doi.org/10.3390/medicina57101064.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Habib S, Siddiqui AH, Azam M, Siddiqui F, Chalhoub M. Actinomyces viscosus causing disseminated disease in a patient on methotrexate. Respir Med Case Rep. 2018;25:158–60. https://doi.org/10.1016/j.rmcr.2018.08.009.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Coleman RM, Georg LK. Comparative pathogenicity of Actinomyces naeslundii and Actinomyces israelii. Appl Microbiol. 1969;18(3):427–32. https://doi.org/10.1128/am.18.3.427-432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Supriya BG, Harisree S, Savio J, Ramachandran P. Actinomyces naeslundii causing pulmonary endobronchial Actinomycosis-A case report. Indian J Pathol Microbiol. 2019;62(2):326–8. https://doi.org/10.4103/IJPM.IJPM_706_17.

    Article  CAS  PubMed  Google Scholar 

  43. Könönen E, Wade WG. Actinomyces and related organisms in human infections. Clin Microbiol Rev. 2015;28(2):419–42. https://doi.org/10.1128/CMR.00100-14.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Khaledi M, Sameni F, Afkhami H, Hemmati J, Asareh Zadegan Dezfuli A, Sanae MJ, Validi M. Infective endocarditis by HACEK: a review. J Cardiothorac Surg. 2022;17(1):185. https://doi.org/10.1186/s13019-022-01932-5.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Miyoshi T, Oge S, Nakata S, Ueno Y, Ukita H, Kousaka R, Miura Y, Yoshinari N, Yoshida A. Gemella haemolysans inhibits the growth of the periodontal pathogen Porphyromonas gingivalis. Sci Rep. 2021;11(1):11742. https://doi.org/10.1038/s41598-021-91267-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kodaka S, Uchida T, Gomi H. Gemella haemolysans as an emerging pathogen for bacteremia among the elderly. J Gen Fam Med. 2021;23(2):110–2. https://doi.org/10.1002/jgf2.497.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Dao K, Patel P, Udani K, Pollock E, Gondal M. Granulicatella adiacens subacute bacterial endocarditis presenting as diffuse alveolar hemorrhage and infection-related glomerulonephritis. Case Rep Infect Dis. 2022;2022:5565906. https://doi.org/10.1155/2022/5565906.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Van Hoogmoed CG, Geertsema-Doornbusch GI, Teughels W, Quirynen M, Busscher HJ, Van der Mei HC. Reduction of periodontal pathogens adhesion by antagonistic strains. Oral Microbiol Immunol. 2008;23(1):43–8. https://doi.org/10.1111/j.1399-302X.2007.00388.x.

    Article  PubMed  Google Scholar 

  49. Olagunju A, Martinez J, Kenny D, Gideon P, Mookadam F, Unzek S. Virulent endocarditis due to Haemophilus parainfluenzae: a systematic review of the literature. World J Cardiol. 2022;14(10):546–56. https://doi.org/10.4330/wjc.v14.i10.546.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Calheiros Cruz G, Sousa M, Vilela S, Teixeira E Costa F, Silva FJ. Lautropia mirabilis: an exceedingly rare cause of peritoneal dialysis-associated peritonitis. Case Rep Nephrol Dial. 2022;12(2):81–4. https://doi.org/10.1159/000524494.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ranganath N, Shirley JD, Challener DW, Stevens RW, Kind DR, Comba IY, Patel R, Schuetz AN, Shah AS. Leptotrichia bacteremia: 10-year retrospective clinical analysis and antimicrobial susceptibility profiles. J Clin Microbiol. 2023;61(2): e0173322. https://doi.org/10.1128/jcm.01733-22.

    Article  CAS  PubMed  Google Scholar 

  52. Feder HM Jr, Garibaldi RA. The significance of nongonococcal, nonmeningococcal Neisseria isolates from blood cultures. Rev Infect Dis. 1984;6(2):181–8. https://doi.org/10.1093/clinids/6.2.181.

    Article  PubMed  Google Scholar 

  53. Baraldès MA, Domingo P, Barrio JL, Pericas R, Gurguí M, Vazquez G. Meningitis due to Neisseria subflava: case report and review. Clin Infect Dis. 2000;30(3):615–7. https://doi.org/10.1086/313700.

    Article  PubMed  Google Scholar 

  54. Baniulyte G, Svirpliene S, Eccleston A, Arjunan S, Connor M. Neisseria oralis septicaemia in a newborn: first recorded case. Paediatr Int Child Health. 2021;41(3):226–7. https://doi.org/10.1080/20469047.2020.1826780.

    Article  PubMed  Google Scholar 

  55. Greve D, Moter A, Kleinschmidt MC, Pfäfflin F, Stegemann MS, Kursawe L, Grubitzsch H, Falk V, Kikhney J. Rothia aeria and Rothia dentocariosa as biofilm builders in infective endocarditis. Int J Med Microbiol. 2021;311(2): 151478. https://doi.org/10.1016/j.ijmm.2021.151478.

    Article  CAS  PubMed  Google Scholar 

  56. Rosier BT, Moya-Gonzalvez EM, Corell-Escuin P, Mira A. Isolation and characterization of nitrate-reducing bacteria as potential probiotics for oral and systemic health. Front Microbiol. 2020;11: 555465. https://doi.org/10.3389/fmicb.2020.555465.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Stingu CS, Eschrich K, Rodloff AC, Schaumann R, Jentsch H. Periodontitis is associated with a loss of colonization by Streptococcus sanguinis. J Med Microbiol. 2008;57(Pt4):495–9. https://doi.org/10.1099/jmm.0.47649-0.

    Article  PubMed  Google Scholar 

  58. Martini AM, Moricz BS, Woods LJ, Jones BD. Type IV pili of Streptococcus sanguinis contribute to pathogenesis in experimental infective endocarditis. Microbiol Spectr. 2021;9(3): e0175221. https://doi.org/10.1128/Spectrum.01752-21.

    Article  PubMed  Google Scholar 

  59. van Essche M, Loozen G, Godts C, Boon N, Pauwels M, Quirynen M, Teughels W. Bacterial antagonism against periodontopathogens. J Periodontol. 2013;84(6):801–11. https://doi.org/10.1902/jop.2012.120261.

    Article  CAS  PubMed  Google Scholar 

  60. Mitchell J. Streptococcus mitis: walking the line between commensalism and pathogenesis. Mol Oral Microbiol. 2011;26(2):89–98. https://doi.org/10.1111/j.2041-1014.2010.00601.x.

    Article  CAS  PubMed  Google Scholar 

  61. Teughels W, Kinder Haake S, Sliepen I, Pauwels M, Van Eldere J, Cassiman JJ, Quirynen M. Bacteria interfere with A. actinomycetemcomitans colonization. J Dent Res. 2007;86(7):611–7. https://doi.org/10.1177/154405910708600706.

    Article  CAS  PubMed  Google Scholar 

  62. Basaranoglu ST, Ozsurekci Y, Aykac K, Aycan AE, Bıcakcigil A, Altun B, Sancak B, Cengiz AB, Kara A, Ceyhan M. Streptococcus mitis/oralis causing blood stream infections in pediatric patients. Jpn J Infect Dis. 2018;72(1):1–6. https://doi.org/10.7883/yoken.JJID.2018.074.

    Article  PubMed  Google Scholar 

  63. Hillman JD, McDonell E, Hillman CH, Zahradnik RT, Soni MG. Safety assessment of ProBiora3, a probiotic mouthwash: subchronic toxicity study in rats. Int J Toxicol. 2009;28(5):357–67. https://doi.org/10.1177/1091581809340705.

    Article  CAS  PubMed  Google Scholar 

  64. Kreth J, Zhang Y, Herzberg MC. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol. 2008;190(13):4632–40. https://doi.org/10.1128/JB.00276-08.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Jc Y, Belkhir L, Jonckheere S, Wilmes D, Cornu O, Vandercam B, Rodriguez-Villalobos H. Streptococcus gordonii septic arthritis: two cases and review of literature. BMC Infect Dis. 2012;12:215. https://doi.org/10.1186/1471-2334-12-215.

    Article  Google Scholar 

  66. Christopher AB, Arndt A, Cugini C, Davey ME. A streptococcal effector protein that inhibits Porphyromonas gingivalis biofilm development. Microbiol Read Engl. 2010;156:3469–77. https://doi.org/10.1099/mic.0.042671-0.

    Article  CAS  Google Scholar 

  67. Tkacz K, Piwowarczyk A, Podsiadły E, Kuchar E. Streptococcus intermedius acute meningitis in an immunocompetent child. Pediatr Infect Dis J. 2022;41(10):e428–9. https://doi.org/10.1097/INF.0000000000003613.

    Article  PubMed  Google Scholar 

  68. Kaewsrichan J, Douglas CWI, Nissen-Meyer J, Fimland G, Teanpaisan R. Characterization of a bacteriocin produced by Prevotella nigrescens ATCC 25261. Lett Appl Microbiol. 2004;39(5):451–8. https://doi.org/10.1111/j.1472-765X.2004.01608.x.

    Article  CAS  PubMed  Google Scholar 

  69. Derouane F, Lambert M, De Greef J, Malghem J, Lecouvet FE. Primary infectious costochondritis due to Prevotella nigrescens in an immunocompetent patient: clinical and imaging findings. Skeletal Radiol. 2019;48(8):1305–9. https://doi.org/10.1007/s00256-019-3148-0.

    Article  PubMed  Google Scholar 

  70. Ehrmann E, Jolivet-Gougeon A, Bonnaure-Mallet M, Fosse T. Multidrug-resistant oral Capnocytophaga gingivalis responsible for an acute exacerbation of chronic obstructive pulmonary disease: case report and literature review. Anaerobe. 2016;42:50–4. https://doi.org/10.1016/j.anaerobe.2016.08.003.

    Article  PubMed  Google Scholar 

  71. Naradasu D, Miran W, Okamoto A. Metabolic current production by an oral biofilm pathogen Corynebacterium matruchotii. Molecules. 2020;25(14):3141. https://doi.org/10.3390/molecules25143141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Preece KE, Glávits R, Murbach TS, Endres JR, Hirka G, Vértesi A, Béres E, Szakonyiné IP. Safety evaluation of Veillonella atypica FB0054 with genotoxicity and subchronic toxicological studies. J Appl Toxicol. 2023;43(6):808–27. https://doi.org/10.1002/jat.4426.

    Article  CAS  PubMed  Google Scholar 

  73. Ito Y, Nakayama H, Niitsu Y, Kaneko N, Otsuka M, Sawada Y, Takeuchi Y, Sekido N. The first case of Veillonella atypica bacteremia in a patient with renal pelvic tumor. Anaerobe. 2022;73: 102491. https://doi.org/10.1016/j.anaerobe.2021.102491.

    Article  PubMed  Google Scholar 

  74. Hillier D, Ballal M, Sanger R, Qazzafi Z. Veillonella dispar and Streptococcus bovis septic arthritis in a native shoulder joint. Shoulder Elbow. 2011;3(4):219–21. https://doi.org/10.1111/j.1758-5740.2011.00134.x.

    Article  Google Scholar 

  75. Richards T, Stephen J, Lui CL. Severe disseminated Veillonella parvula infection including endocarditis, bilateral psoas abscess, discitis, and osteomyelitis but sparing spinal and hip prostheses: a case report. J Med Case Rep. 2022;16(1):157. https://doi.org/10.1186/s13256-022-03386-8.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Vuotto C, Longo F, Donelli G. Probiotics to counteract biofilm-associated infections: promising and conflicting data. Int J Oral Sci. 2014;6(4):189–94. https://doi.org/10.1038/ijos.2014.52.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Cosseau C, Devine DA, Dullaghan E, Gardy JL, Chikatamarla A, Gellatly S, Yu LL, Pistolic J, Falsafi R, Tagg J, Hancock RE. The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun. 2008;76(9):4163–75. https://doi.org/10.1128/IAI.00188-08.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lourenço TG, Heller D, Silva-Boghossian CM, Cotton SL, Paster BJ, Colombo AP. Microbial signature profiles of periodontally healthy and diseased patients. J Clin Periodontol. 2014;41(11):1027–36. https://doi.org/10.1111/jcpe.12302.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Colombo AP, Boches SK, Cotton SL, Goodson JM, Kent R, Haffajee AD, Socransky SS, Hasturk H, Van Dyke TE, Dewhirst F, Paster BJ. Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J Periodontol. 2009;80(9):1421–32. https://doi.org/10.1902/jop.2009.090185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Acharya A, Chen T, Chan Y, Watt RM, Jin L, Mattheos N. Species-level salivary microbial indicators of well-resolved periodontitis: a preliminary investigation. Front Cell Infect Microbiol. 2019;9:347. https://doi.org/10.3389/fcimb.2019.00347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Relvas M, Regueira-Iglesias A, Balsa-Castro C, Salazar F, Pacheco JJ, Cabral C, Henriques C, Tomás I. Relationship between dental and periodontal health status and the salivary microbiome: bacterial diversity, co-occurrence networks and predictive models. Sci Rep. 2021;11(1):929. https://doi.org/10.1038/s41598-020-79875-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Payungporn S, Arirachakaran P, Poomipak W, Praianantathavorn K, Charalampakis G, Poovorawan Y. Identification of bacteria associated with a periodontal disease in Thai patients based on next-generation sequencing. Jundishapur J Microbiol. 2017;10(6): e13646. https://doi.org/10.5812/jjm.13646.

    Article  CAS  Google Scholar 

  83. Maeda N, Okamoto M, Kondo K, Ishikawa H, Osada R, Tsurumoto A, Fujita H. Incidence of Prevotella intermedia and Prevotella nigrescens in periodontal health and disease. Microbiol Immunol. 1998;42(9):583–9. https://doi.org/10.1111/j.1348-0421.1998.tb02328.x.

    Article  CAS  PubMed  Google Scholar 

  84. Souto R, Silva-Boghossian CM, Colombo AP. Prevalence of Pseudomonas aeruginosa and Acinetobacter spp. in subgingival biofilm and saliva of subjects with chronic periodontal infection. Braz J Microbiol. 2014;45(2):495–501. https://doi.org/10.1590/s1517-83822014000200017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Miller DP, Wang Q, Weinberg A, Lamont RJ. Transcriptome analysis of Porphyromona gingivalis and Acinetobacter baumannii in polymicrobial communities. Mol Oral Microbiol. 2018;33(5):364–77. https://doi.org/10.1111/omi.12238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Vielkind P, Jentsch H, Eschrich K, Rodloff AC, Stingu CS. Prevalence of Actinomyces spp. in patients with chronic periodontitis. Int J Med Microbiol. 2015;305(7):682–8. https://doi.org/10.1016/j.ijmm.2015.08.018.

    Article  PubMed  Google Scholar 

  87. Hong BY, Furtado Araujo MV, Strausbaugh LD, Terzi E, Ioannidou E, Diaz PI. Microbiome profiles in periodontitis in relation to host and disease characteristics. PLoS ONE. 2015;10(5): e0127077. https://doi.org/10.1371/journal.pone.0148893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Chug P, Dutt R, Sharma A, Bhagat N, Dhar M. A critical appraisal of the effects of probiotics on oral health. J Funct Foods. 2020;70: 103985. https://doi.org/10.1016/j.jff.2020.103985.

    Article  CAS  Google Scholar 

  89. Solbiati J, Frias-Lopez J. Metatranscriptome of the oral microbiome in health and disease. J Dent Res. 2018;97(5):492–500. https://doi.org/10.1177/0022034518761644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Zhang Y, Ding Y, Guo Q. Probiotic species in the management of periodontal diseases: an overview. Front Cell Infect Microbiol. 2022;12: 806463. https://doi.org/10.3389/fcimb.2022.806463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Jiao Y, Hasegawa M, Inohara N. The role of oral pathobionts in dysbiosis during periodontitis development. J Dent Res. 2014;93(6):539–46. https://doi.org/10.1177/0022034514528212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Snydman DR. The safety of probiotics. Clin Infect Dis. 2008;46(2):S104-111. https://doi.org/10.1086/523331.

    Article  PubMed  Google Scholar 

  93. Hempel S, Newberry S, Ruelaz A, Wang Z, Miles JN, Suttorp MJ, Johnsen B, Shanman R, Slusser W, Fu N, Smith A, Roth B, Polak J, Motala A, Perry T, Shekelle PG. Safety of probiotics used to reduce risk and prevent or treat disease. Evid Rep Technol Assess. 2011;200:1–645.

    Google Scholar 

  94. Castillo Y, Delgadillo NA, Neuta Y, Hernández A, Acevedo T, Cárdenas E, Montaño A, Lafaurie GI, Castillo DM. Antibiotic susceptibility and resistance genes in oral clinical isolates of Prevotella intermedia, Prevotella nigrescens, and Prevotella melaninogenica. Antibiotics. 2022. https://doi.org/10.3390/antibiotics11070888.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Li X, Fields FR, Ho M, Marshall-Hudson A, Gross R, Casser ME, Naito M. Safety assessment of Streptococcus salivarius DB-B5 as a probiotic candidate for oral health. Food Chem Toxicol. 2021;153: 112277. https://doi.org/10.1016/j.fct.2021.112277.

    Article  CAS  PubMed  Google Scholar 

  96. Ban OH, Oh S, Park C, Bang WY, Lee BS, Yang SY, Chae SA, Jung YH, Yang J. Safety assessment of Streptococcus thermophilus IDCC 2201 used for product manufacturing in Korea. Food Sci Nutr. 2020;8(11):6269–74. https://doi.org/10.1002/fsn3.1925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Terai T, Okumura T, Imai S, Nakao M, Yamaji K, Ito M, Nagata T, Kaneko K, Miyazaki K, Okada A, Nomura Y, Hanada N. Screening of probiotic candidates in human oral bacteria for the prevention of dental disease. PLoS ONE. 2015;10(6): e0128657. https://doi.org/10.1371/journal.pone.0128657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Zahradnik RT, Magnusson I, Walker C, McDonell E, Hillman CH, Hillman JD. Preliminary assessment of safety and effectiveness in humans of ProBiora3, a probiotic mouthwash. J Appl Microbiol. 2009;107(2):682–90. https://doi.org/10.1111/j.1365-2672.2009.04243.x.

    Article  CAS  PubMed  Google Scholar 

  99. Conrads G, Westenberger J, Lürkens M, Abdelbary MMH. Isolation and bacteriocin-related typing of Streptococcus dentisani. Front Cell Infect Microbiol. 2019;9:110. https://doi.org/10.3389/fcimb.2019.00110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Ferrer MD, López-López A, Nicolescu T, Perez-Vilaplana S, Boix-Amorós A, Dzidic M, Garcia S, Artacho A, Llena C, Mira A. Topic application of the probiotic Streptococcus dentisani improves clinical and microbiological parameters associated with oral health. Front Cell Infect Microbiol. 2020;10:465. https://doi.org/10.3389/fcimb.2020.00465.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Herrero ER, Slomka V, Bernaerts K, Boon N, Hernandez-Sanabria E, Passoni BB, Quirynen M, Teughels W. Antimicrobial effects of commensal oral species are regulated by environmental factors. J Dent. 2016;47:23–33. https://doi.org/10.1016/j.jdent.2016.02.007.

    Article  PubMed  Google Scholar 

  102. Nackaerts O, Jacobs R, Quirynen M, Rober M, Sun Y, Teughels W. Replacement therapy for periodontitis: pilot radiographic evaluation in a dog model. J Clin Periodontol. 2008;35(12):1048–52. https://doi.org/10.1111/j.1600-051X.2008.01333.x.

    Article  PubMed  Google Scholar 

  103. Shu Y, Upara C, Ding Q, Zhu M, Zeng E, Banas JA, Hong L. Spent culture supernatant of Streptococcus gordonii mitigates inflammation of human periodontal cells and inhibits proliferation of pathogenic oral microbes. J Periodontol. 2023;94(4):575–85. https://doi.org/10.1002/JPER.22-0333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kotloff KL, Wasserman SS, Jones KF, Livio S, Hruby DE, Franke CA, Fischetti VA. Clinical and microbial responses of volunteers to combines intranasal and oral inoculation with a Streptococcus gordonii carrier strain intended for future use as a group A streptococcus vaccine. Infect Immun. 2005;73(4):2360–6. https://doi.org/10.1128/IAI.73.4.2360-2366.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Mans JJ, von Lackum K, Dorsey C, Willis S, Wallet SM, Baker HV, Lamont RJ, Handfield M. The degree of microbiome complexity influences the epithelial response to infection. BMC Genom. 2009. https://doi.org/10.1186/1471-2164-10-380.

    Article  Google Scholar 

  106. Douglas CW, Heath J, Hampton KK, Preston FE. Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol. 1993;39:179–82. https://doi.org/10.1099/00222615-39-3-179.

    Article  CAS  PubMed  Google Scholar 

  107. Martini AM, Moricz BS, Ripperger AK, Tran PM, Sharp ME, Forsythe AN, Kulhankova K, Salgado-Pabón W, Jones BD. Association of novel Streptococcus sanguinis virulence factors with pathogenesis in a native valve infective endocarditis model. Front Microbiol. 2020;11:10. https://doi.org/10.3389/fmicb.2020.00010.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Universidad Cooperativa de Colombia [INV1506 and INV3011].

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Authors and Affiliations

  1. GIOMET Group, Faculty of Dentistry, Universidad Cooperativa de Colombia, Campus Villavicencio, Carrera 35 # 36 99, Villavicencio, Colombia

    María del Pilar Angarita-Díaz

  2. Ciencia y Pedagogía Group, School of Medicine, Universidad Cooperativa de Colombia, Campus Santa Marta, Santa Marta, Colombia

    Cristian Fong

  3. School of Dentistry, Universidad Cooperativa de Colombia, Campus Villavicencio, Villavicencio, Colombia

    Daniela Medina

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  1. María del Pilar Angarita-Díaz
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María del Pilar Angarita-Díaz contributed to conceptualization, methodology, and data extraction and drafted the manuscript. Cristian Fong was involved in data extraction and level of evidence and drafted the manuscript. Daniela Medina performed data extraction.

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del Pilar Angarita-Díaz, M., Fong, C. & Medina, D. Bacteria of healthy periodontal tissues as candidates of probiotics: a systematic review. Eur J Med Res 29, 328 (2024). https://doi.org/10.1186/s40001-024-01908-2

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European Journal of Medical Research

ISSN: 2047-783X

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