Interkingdom interactions on the denture surface: implications for oral hygiene

Christopher Delaney, Lindsay E. O'Donnell, Ryan Kean, Leighann Sherry, Jason L. Brown, Gareth Calvert, Christopher J. Nile, Laura Cross, David J. Bradshaw, Bernd W. Brandt, Douglas Robertson, Gordon Ramage

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Abstract

Background: Evidence to support the role of Candida species in oral disease is limited. Often considered a commensal, this opportunistic yeast has been shown to play a role in denture related disease, though whether it is an active participant or innocent bystander remains to be determined. This study sought to understand the role of Candida species alongside the bacterial microbiome in a denture patient cohort, exploring how the microbiology of the denture was affected by oral hygiene practices.
Materials and methods: In vitro denture cleansing studies were performed on a complex 9-species interkingdom denture biofilm model, with quantitative assessment of retained bacterial and fungal viable bioburdens. Patient hygiene measures were also collected from 131 patients, including OHIP, frequency of denture cleansing, oral hygiene measure and patient demographics. The bacterial microbiome was analysed from each patient, alongside quantitative PCR assessment of ITS (fungal) and 16S (bacterial) bioburden from denture, mucosa and intact dentition.
Results: It was shown that following in vitro denture cleansing C. albicans were unresponsive to treatment, whereas bacterial biofilms could repopulate 100-fold, but were susceptible to subsequent treatment. Within the patient cohort, oral hygiene did not impact candidal or bacterial composition, nor diversity. The levels of Candida did not significantly influence the bacterial microbiome, though an observed gradient was suggestive of a microbial composition change in response to Candida load, indicating interkingdom interaction rather than an oral hygiene effect. Indeed, correlation analysis was able to show significant correlations between Candida species and key genera (Lactobacillus, Scardovia, Fusobacterium).
Conclusions: Overall, this study has shown that the denture microbiome/mycobiome is relatively resilient to oral hygiene challenges, but that Candida species have potential interactions with key oral genera. These interactions may have a bearing on shaping community structure and a shift from health to disease when the opportunity arises.
Original languageEnglish
Article number100002
Number of pages9
JournalBiofilm
Volume1
Early online date27 Jun 2019
DOIs
Publication statusE-pub ahead of print - 27 Jun 2019

Fingerprint

Dentures
Oral Hygiene
Candida
Microbiota
Biofilms
Mouth Diseases
Fusobacterium
Dentition
Lactobacillus
Microbiology
Hygiene
Mucous Membrane
Yeasts
Demography
Polymerase Chain Reaction
Health
Therapeutics

Keywords

  • microbiome
  • Candida
  • denture
  • oral hygiene

Cite this

Delaney, C., O'Donnell, L. E., Kean, R., Sherry, L., Brown, J. L., Calvert, G., ... Ramage, G. (2019). Interkingdom interactions on the denture surface: implications for oral hygiene. Biofilm, 1, [100002]. https://doi.org/10.1016/j.bioflm.2019.100002
Delaney, Christopher ; O'Donnell, Lindsay E. ; Kean, Ryan ; Sherry, Leighann ; Brown, Jason L. ; Calvert, Gareth ; Nile, Christopher J. ; Cross, Laura ; Bradshaw, David J. ; Brandt, Bernd W. ; Robertson, Douglas ; Ramage, Gordon. / Interkingdom interactions on the denture surface: implications for oral hygiene. In: Biofilm. 2019 ; Vol. 1.
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abstract = "Background: Evidence to support the role of Candida species in oral disease is limited. Often considered a commensal, this opportunistic yeast has been shown to play a role in denture related disease, though whether it is an active participant or innocent bystander remains to be determined. This study sought to understand the role of Candida species alongside the bacterial microbiome in a denture patient cohort, exploring how the microbiology of the denture was affected by oral hygiene practices. Materials and methods: In vitro denture cleansing studies were performed on a complex 9-species interkingdom denture biofilm model, with quantitative assessment of retained bacterial and fungal viable bioburdens. Patient hygiene measures were also collected from 131 patients, including OHIP, frequency of denture cleansing, oral hygiene measure and patient demographics. The bacterial microbiome was analysed from each patient, alongside quantitative PCR assessment of ITS (fungal) and 16S (bacterial) bioburden from denture, mucosa and intact dentition.Results: It was shown that following in vitro denture cleansing C. albicans were unresponsive to treatment, whereas bacterial biofilms could repopulate 100-fold, but were susceptible to subsequent treatment. Within the patient cohort, oral hygiene did not impact candidal or bacterial composition, nor diversity. The levels of Candida did not significantly influence the bacterial microbiome, though an observed gradient was suggestive of a microbial composition change in response to Candida load, indicating interkingdom interaction rather than an oral hygiene effect. Indeed, correlation analysis was able to show significant correlations between Candida species and key genera (Lactobacillus, Scardovia, Fusobacterium).Conclusions: Overall, this study has shown that the denture microbiome/mycobiome is relatively resilient to oral hygiene challenges, but that Candida species have potential interactions with key oral genera. These interactions may have a bearing on shaping community structure and a shift from health to disease when the opportunity arises.",
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Delaney, C, O'Donnell, LE, Kean, R, Sherry, L, Brown, JL, Calvert, G, Nile, CJ, Cross, L, Bradshaw, DJ, Brandt, BW, Robertson, D & Ramage, G 2019, 'Interkingdom interactions on the denture surface: implications for oral hygiene', Biofilm, vol. 1, 100002. https://doi.org/10.1016/j.bioflm.2019.100002

Interkingdom interactions on the denture surface: implications for oral hygiene. / Delaney, Christopher; O'Donnell, Lindsay E.; Kean, Ryan; Sherry, Leighann; Brown, Jason L.; Calvert, Gareth; Nile, Christopher J.; Cross, Laura; Bradshaw, David J.; Brandt, Bernd W.; Robertson, Douglas; Ramage, Gordon.

In: Biofilm, Vol. 1, 100002, 12.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Interkingdom interactions on the denture surface: implications for oral hygiene

AU - Delaney, Christopher

AU - O'Donnell, Lindsay E.

AU - Kean, Ryan

AU - Sherry, Leighann

AU - Brown, Jason L.

AU - Calvert, Gareth

AU - Nile, Christopher J.

AU - Cross, Laura

AU - Bradshaw, David J.

AU - Brandt, Bernd W.

AU - Robertson, Douglas

AU - Ramage, Gordon

N1 - Acceptance from webpage OA article

PY - 2019/6/27

Y1 - 2019/6/27

N2 - Background: Evidence to support the role of Candida species in oral disease is limited. Often considered a commensal, this opportunistic yeast has been shown to play a role in denture related disease, though whether it is an active participant or innocent bystander remains to be determined. This study sought to understand the role of Candida species alongside the bacterial microbiome in a denture patient cohort, exploring how the microbiology of the denture was affected by oral hygiene practices. Materials and methods: In vitro denture cleansing studies were performed on a complex 9-species interkingdom denture biofilm model, with quantitative assessment of retained bacterial and fungal viable bioburdens. Patient hygiene measures were also collected from 131 patients, including OHIP, frequency of denture cleansing, oral hygiene measure and patient demographics. The bacterial microbiome was analysed from each patient, alongside quantitative PCR assessment of ITS (fungal) and 16S (bacterial) bioburden from denture, mucosa and intact dentition.Results: It was shown that following in vitro denture cleansing C. albicans were unresponsive to treatment, whereas bacterial biofilms could repopulate 100-fold, but were susceptible to subsequent treatment. Within the patient cohort, oral hygiene did not impact candidal or bacterial composition, nor diversity. The levels of Candida did not significantly influence the bacterial microbiome, though an observed gradient was suggestive of a microbial composition change in response to Candida load, indicating interkingdom interaction rather than an oral hygiene effect. Indeed, correlation analysis was able to show significant correlations between Candida species and key genera (Lactobacillus, Scardovia, Fusobacterium).Conclusions: Overall, this study has shown that the denture microbiome/mycobiome is relatively resilient to oral hygiene challenges, but that Candida species have potential interactions with key oral genera. These interactions may have a bearing on shaping community structure and a shift from health to disease when the opportunity arises.

AB - Background: Evidence to support the role of Candida species in oral disease is limited. Often considered a commensal, this opportunistic yeast has been shown to play a role in denture related disease, though whether it is an active participant or innocent bystander remains to be determined. This study sought to understand the role of Candida species alongside the bacterial microbiome in a denture patient cohort, exploring how the microbiology of the denture was affected by oral hygiene practices. Materials and methods: In vitro denture cleansing studies were performed on a complex 9-species interkingdom denture biofilm model, with quantitative assessment of retained bacterial and fungal viable bioburdens. Patient hygiene measures were also collected from 131 patients, including OHIP, frequency of denture cleansing, oral hygiene measure and patient demographics. The bacterial microbiome was analysed from each patient, alongside quantitative PCR assessment of ITS (fungal) and 16S (bacterial) bioburden from denture, mucosa and intact dentition.Results: It was shown that following in vitro denture cleansing C. albicans were unresponsive to treatment, whereas bacterial biofilms could repopulate 100-fold, but were susceptible to subsequent treatment. Within the patient cohort, oral hygiene did not impact candidal or bacterial composition, nor diversity. The levels of Candida did not significantly influence the bacterial microbiome, though an observed gradient was suggestive of a microbial composition change in response to Candida load, indicating interkingdom interaction rather than an oral hygiene effect. Indeed, correlation analysis was able to show significant correlations between Candida species and key genera (Lactobacillus, Scardovia, Fusobacterium).Conclusions: Overall, this study has shown that the denture microbiome/mycobiome is relatively resilient to oral hygiene challenges, but that Candida species have potential interactions with key oral genera. These interactions may have a bearing on shaping community structure and a shift from health to disease when the opportunity arises.

KW - microbiome

KW - Candida

KW - denture

KW - oral hygiene

U2 - 10.1016/j.bioflm.2019.100002

DO - 10.1016/j.bioflm.2019.100002

M3 - Article

VL - 1

M1 - 100002

ER -

Delaney C, O'Donnell LE, Kean R, Sherry L, Brown JL, Calvert G et al. Interkingdom interactions on the denture surface: implications for oral hygiene. Biofilm. 2019 Dec;1. 100002. https://doi.org/10.1016/j.bioflm.2019.100002