Commensal and pathogenic biofilms differently modulate peri‐implant oral mucosa in an organotypic model

Ingendoh-Tsakmakidis, Alexandra; Mikolai, Carina; Winkel, Andreas; Szafrański, Szymon P.; Falk, Christine S.; Rossi, Angela Maria Gabriella; Walles, Heike; Stiesch, Meike

doi:10.1111/cmi.13078

Cited by 34 publications

(29 citation statements)

References 65 publications

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“…In conclusion, the neutrophil responses, NET formation, ROS production and MMPs secretion were different to the various bacterial species grown as monospecies biofilm. The commensal S. oralis induced a balance-like neutrophil response -which is consistent with the concept that commensals protect the host against the overgrowth of pathogenic bacteria and are required to maintain oral health [23,76]. The pathogenic biofilms induced different neutrophil responses.…”

Section: Resultssupporting

confidence: 81%

Neutrophils exhibit an individual response to different oral bacterial biofilms

Mikolai

Branitzki‐Heinemann

Ingendoh-Tsakmakidis

et al. 2020

Journal of Oral Microbiology

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Oral innate immunity is led by neutrophils. It is still unclear how their main antimicrobial mechanisms against different biofilms may contribute to balance or dysregulation in the oral cavity. We investigated the capacity of commensal ( Streptococcus oralis ) and pathogenic ( Porphyromonas gingivalis or Aggregatibacter actinomycetemcomitans ) monospecies biofilms to induce or to inhibit selected antimicrobial mechanisms of neutrophils. S. oralis induced neutrophil extracellular traps (NETs) formation, reactive oxygen species (ROS) production, and matrix metalloproteinases (MMPs) 8 and 9 secretion. However, these responses were partially reduced in PMA-activated neutrophils indicating a balance-like neutrophil response, which might be important for the maintenance of oral health. P. gingivalis generally induced ROS. Reduced NET formation and significantly decreased MMP secretion were detectable in activated neutrophils highlighting P. gingivalis’ nucleolytic and proteolytic activity, which might support bacterial colonization and pathogenesis of periodontitis. In contrast, A. actinomycetemcomitans did not affect the levels of antimicrobial factors in activated neutrophils and induced NET formation, ROS production, and secretion of MMP-8 and -9 in neutrophils alone, which might contribute to tissue destruction and disease progression. In summary, neutrophil responses to biofilms were species-specific and might support either maintenance of oral health or pathogenesis of periodontitis depending on the species.

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Section: Resultssupporting

confidence: 81%

Neutrophils exhibit an individual response to different oral bacterial biofilms

Mikolai

Branitzki‐Heinemann

Ingendoh-Tsakmakidis

et al. 2020

Journal of Oral Microbiology

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“…Only very few studies have previously exposed RHG (but not RHS) to commensal microbes, and none have shown such well‐preserved tissue integrity after 24 hours of co‐culture. For example, a recent study described gene regulation in RHG after Streptococcus oralis biofilm exposure via a titanium implant inserted into the RHG for 24 hours; however, no data on tissue viability and limited data on tissue integrity were shown 57 . Another study described biofilm formation and invasion into the epithelial layers when exposed to streptococci and Candida albicans for 24 hours.…”

Section: Discussionmentioning

confidence: 99%

Differential influence ofStreptococcus mitison host response to metals in reconstructed human skin and oral mucosa

et al. 2020

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Background: Skin and oral mucosa are continuously exposed to potential metal sensitizers while hosting abundant microbes, which may influence the host response to sensitizers. This host response may also be influenced by the route of exposure that is skin or oral mucosa, due to their different immune properties. Objective: Determine how commensal Streptococcus mitis influences the host response to nickel sulfate (sensitizer) and titanium(IV) bis(ammonium lactato) dihydroxide (questionable sensitizer) in reconstructed human skin (RHS) and gingiva (RHG). Methods: RHS/RHG was exposed to nickel or titanium, in the presence or absence of S. mitis for 24 hours. Histology, cytokine secretion, and Toll-like receptors (TLRs) expression were assessed. Results: S. mitis increased interleukin (IL)-6, CXCL8, CCL2, CCL5, and CCL20 secretion in RHS but not in RHG; co-application with nickel further increased cytokine secretion. In contrast, titanium suppressed S. mitis-induced cytokine secretion in RHS and had no influence on RHG. S. mitis and metals differentially regulated TLR1 and TLR4 in RHS, and predominantly TLR4 in RHG. Conclusion: Co-exposure of S. mitis and nickel resulted in a more potent innate immune response in RHS than in RHG, whereas titanium remained inert. These results indicate the important influence of commensal microbes and the route of exposure on the host's response to metals.

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“…Ingendoh-Tsakmakidis et al [ 22 ] investigated the response of peri-implant oral mucosa to oral bacterial biofilms using an in vitro, peri-implant, mucosa–biofilm model. In this study, a titanium disc (implant material) was inserted into the engineered connective tissue layer, consisting of collagen-embedded human gingival fibroblasts (HGFs), and then oral keratinocytes (OKF6/TERT-2) were added around the titanium on top of the fibroblast–collagen gel.…”

Section: Discussionmentioning

confidence: 99%

Implant Soft-Tissue Attachment Using 3D Oral Mucosal Models—A Pilot Study

et al. 2020

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Purpose: The aim of this study was to investigate soft-tissue attachment to different metal, ceramic, and polymer implant surfaces using an inflamed, three-dimensional (3D), tissue-engineered, human oral mucosal model, as well as multiple-endpoint qualitative and quantitative biological approaches. Methods: Normal human oral fibroblasts, OKF6/TERT-2 keratinocytes and THP-1 monocytes were cultured, and full-thickness, 3D oral mucosal models were engineered inside tissue culture inserts. Sand-blasted and acid-etched (SLA) and machined (M) titanium–zirconium alloy (TiZr; commercially known as Roxolid; Institut Straumann AG, Switzerland), ceramic (ZrO2), and polyether ether ketone (PEEK) rods (Ø 4 mm × 8 mm) were inserted into the center of tissue-engineered oral mucosa following a Ø 4mm punch biopsy. Inflammation was simulated with addition of the lipopolysaccharide (LPS) of Escherichia coli (E. coli) and tumor necrosis factor (TNF)-alpha to the culture medium. Implant soft-tissue attachment was assessed using histology, an implant pull-test with PrestoBlue assay, and scanning electron microscopy (SEM). Results: Inflamed, full-thickness, 3D human oral mucosal models with inserted implants were successfully engineered and histologically characterized. The implant pull-test with PrestoBlue assay showed higher viability of the tissue that remained attached to the TiZr-SLA surface compared to the other test groups. This difference was statistically significant (p < 0.05). SEM analysis showed evidence of epithelial cell attachment on different implant surfaces. Conclusions: The inflamed, 3D, oral mucosal model has the potential to be used as a suitable in vitro test system for visualization and quantification of implant soft-tissue attachment. The results of our study indicate greater soft tissue attachment to TiZr-SLA compared to TiZr-M, ceramic, and PEEK surfaces.

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Commensal and pathogenic biofilms differently modulate peri‐implant oral mucosa in an organotypic model

Cited by 34 publications

References 65 publications

Neutrophils exhibit an individual response to different oral bacterial biofilms

Neutrophils exhibit an individual response to different oral bacterial biofilms

Differential influence ofStreptococcus mitison host response to metals in reconstructed human skin and oral mucosa

Implant Soft-Tissue Attachment Using 3D Oral Mucosal Models—A Pilot Study

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