Physiological Approaches to the Control of Oral Biofilms
Abstract
Evidence that physiological strategies may be potential routes for oral biofilm control has come from (i) observations of the variations in the intra-oral distribution of members of the resident oral microflora, (ii) changes in plaque composition in health and disease, and (iii) data from laboratory model systems. Key physiological factors that were identified as significant in modulating the microflora included the local pH, redox potential (Eh), and nutrient availability. Increases in mutans streptococci and lactobacilli occur at sites with caries; growth of these species is selectively enhanced at low pH. In contrast, periodontal diseases are associated with plaque accumulation, followed by an inflammatory host response. The increases in Gram-negative, proteolytic, and obligately anaerobic bacteria reflect a low redox potential and a change in nutrient status due to the increased flow of gingival crevicular fluid (GCF). Consequently, physiological strategies for oral biofilm control should focus on reducing the frequency of low pH in plaque by (i) inhibiting acid production, (ii) using sugar substitutes, and (iii) promoting alkali generation from arginine or urea supplements. Similarly, strategies to make the pocket environment less favorable to periodontopathogens include (i) anti-inflammatory agents to reduce the flow of (and hence nutrient supply by) GCF, (ii) bacterial protease inhibitors, and (iii) redox agents to raise the Eh h locally. Most laboratory and clinical findings support the concept of physiological control. However, some data suggest that the ordered structure and metabolically interactive organization of mature dental plaque could generate a community with a high level of homeostasis that is relatively resistant to deliberate external manipulation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Biofilms, with anaerobic centers and aerobic peripheries, exhibit gradients of oxygenation.
“Biofilms, with anaerobic centers and aerobic peripheries, exhibit gradients of oxygenation.60, 61”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [60]
Cites
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.mi.49.100195.003431 · Cited by 4,718 · see citing works
Role of Streptococcus mutans in human dental decay
Loesche, W. J. (1986) · Microbiological Reviews · doi:10.1128/mr.50.4.353-380.1986 · Cited by 3,363 · see citing works
Microbial ecology of dental plaque and its significance in health and disease
Marsh, P. D. (1994) · Advances in Dental Research · doi:10.1177/08959374940080022001 · Cited by 1,278 · see citing works
Self-citationBiofilms, the customized microniche
Costerton, J. W., Lewandowski, Z., de Beer, D., Caldwell, D. E., Korber, D. R., & James, G. A. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.8.2137-2142.1994 · Cited by 999 · see citing works
Adhere today, here tomorrow: oral bacterial adherence
Kolenbrander, P. E., & London, J. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.11.3247-3252.1993 · Cited by 717 · see citing works
Bacterial Adhesion to Oral Tissues: A Model for Infectious Diseases
Gibbons, R. J. (1989) · Journal of Dental Research · doi:10.1177/00220345890680050101 · Cited by 462 · see citing works
The Effect of Female Sex Hormones on Subgingival Plaque
Jensen, J. R., Liljemark, W. F., & Bloomquist, C. G. (1981) · Journal of Periodontology · doi:10.1902/jop.1981.52.10.599 · Cited by 222 · see citing works
Metabolic cooperation in oral microbial communities during growth on mucin
Bradshaw, D. J., Homer, K. A., Marsh, P. D., & Beighton, D. (1994) · Microbiology · doi:10.1099/13500872-140-12-3407 · Cited by 199 · see citing works
Self-citationBradshaw, D. J., McKee, A. S., & Marsh, P. D. (1989) · Journal of Dental Research · doi:10.1177/00220345890680090101 · Cited by 199 · see citing works
Self-citationLoesche, W. J., Gusberti, F. A., Mettraux, G., Higgins, T., & Syed, S. A. (1983) · Infection and Immunity · doi:10.1128/iai.42.2.659-667.1983 · Cited by 196 · see citing works
On the relative importance of specific and non-specific approaches to oral microbial adhesion
Busscher, H. J., Cowan, M. M., & van der Mei, H. C. (1992) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1992.tb04988.x · Cited by 137 · see citing works
Effect of oxygen, inoculum composition and flow rate on development of mixed-culture oral biof ilms
Bradshaw, D. J., Marsh, P. D., Allison, C., & Schilling, K. (1996) · Microbiology · doi:10.1099/13500872-142-3-623 · Cited by 135 · see citing works
Self-citationSissons, C. H., Cutress, T. W., Hoffman, M. P., & Wakefield, J. S. J. (1991) · Journal of Dental Research · doi:10.1177/00220345910700110301 · Cited by 131 · see citing works
Kinniment, S. L., WIMPENNY, J. W. T., Adams, D., & Marsh, P. D. (1996) · Microbiology · doi:10.1099/13500872-142-3-631 · Cited by 117 · see citing works
Self-citationThe pH of gingival crevices and periodontal pockets in children, teenagers and adults
Eggert, F. M., Drewell, L., Bigelow, J. A., Speck, J. E., & Goldner, M. (1991) · Archives of Oral Biology · doi:10.1016/0003-9969(91)90091-8 · Cited by 108 · see citing works
Sugar, fluoride, pH and microbial homeostasis in dental plaque.
Marsh, P. (1991) · PubMed · Cited by 103 · see citing works
Self-citationA modified chemostat system to study the ecology of oral biofilms
Bradshaw, D. J., Marsh, P., Schilling, K., & Cummins, D. (1996) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1996.tb03199.x · Cited by 97 · see citing works
Self-citationter Steeg, P. F., van der Hoeven, J. S., Jong, M. H. D., Munster, P. J. J. V., & Jansen, M. J. H. (1987) · Antonie van Leeuwenhoek · doi:10.1007/bf00393933 · Cited by 94 · see citing works
Cummins, D. (1991) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1991.tb02316.x · Cited by 83 · see citing works
Beighton, D., Smith, K., & Hayday, H. (1986) · Archives of Oral Biology · doi:10.1016/0003-9969(86)90137-8 · Cited by 78 · see citing works
Bradshaw, D. J., & Marsh, P. D. (2009) · Caries Research · doi:10.1159/000261977 · Cited by 71 · see citing works
Self-citationBradshaw, D. J., McKee, A. S., & Marsh, P. (1990) · Journal of Dental Research · doi:10.1177/00220345900690020301 · Cited by 66 · see citing works
Self-citationBeckers, H. J., & van der Hoeven, J. S. (1982) · Infection and Immunity · doi:10.1128/iai.35.2.583-587.1982 · Cited by 65 · see citing works
van der Hoeven, J. S., & Camp, P. J. M. (1991) · Journal of Dental Research · doi:10.1177/00220345910700070401 · Cited by 64 · see citing works
Li, Y. H., & Bowden, G. H. (1994) · Journal of Dental Research · doi:10.1177/00220345940730100601 · Cited by 64 · see citing works
Modelling the Gingival Pocket by Enrichment of Subgingival Microflora in Human Serum in Chemostats
ter Steeg, P. F., van der Hoeven, J. S., Jong, M. H. D., Munster, P. J. J. V., & Jansen, M. J. H. (1988) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v1i2.7397 · Cited by 63 · see citing works
Marsh, P., Keevil, C. W., McDermid, A. S., Williamson, M. I., & Ellwood, D. C. (1983) · Archives of Oral Biology · doi:10.1016/0003-9969(83)90152-8 · Cited by 62 · see citing works
Self-citationBowden, G. H., & Hamilton, I. R. (1987) · Canadian Journal of Microbiology · doi:10.1139/m87-143 · Cited by 61 · see citing works
Isokangas, P., Tenovuo, J. O., Söderling, E. M., et al. (2009) · Caries Research · doi:10.1159/000261408 · Cited by 53 · see citing works
Hamilton, I. R., & Bowden, G. H. W. (1982) · Infection and Immunity · doi:10.1128/iai.36.1.255-262.1982 · Cited by 53 · see citing works
Littleton, N. W., McCabe, R. M., & Carter, C. H. (1967) · Archives of Oral Biology · doi:10.1016/0003-9969(67)90079-9 · Cited by 46 · see citing works
Efficacy of Sweeteners and Sugar Substitutes in Caries Prevention
Imfeld, T. N. (2009) · Caries Research · doi:10.1159/000261603 · Cited by 44 · see citing works
Petersson, L., Birkhed, D., Gleerup, A., et al. (2009) · Caries Research · doi:10.1159/000261346 · Cited by 43 · see citing works
Competition between Streptococcus mutans and Lactobacillus casei in mixed continuous culture
Bowden, G. H., & Hamilton, I. R. (1989) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1989.tb00100.x · Cited by 42 · see citing works
Beighton, D., & Hayday, H. (1986) · Archives of Oral Biology · doi:10.1016/0003-9969(86)90018-x · Cited by 42 · see citing works
A preliminary evaluation of the use of a redox agent in the treatment of chronic periodontitis
Wilson, M. J., Gibson, M., Strahan, D., et al. (1992) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.1992.tb01826.x · Cited by 33 · see citing works
Coordinately repressible arginine deiminase system inStreptococcus sanguis
Ferro, K. J., Bender, G. R., & Marquis, R. E. (1983) · Current Microbiology · doi:10.1007/bf01567287 · Cited by 33 · see citing works
Svanberg, M. L., & Birkhed, D. (2009) · Caries Research · doi:10.1159/000261409 · Cited by 33 · see citing works
Beckers, H. J. A., & van der Hoeven, J. S. (1984) · Archives of Oral Biology · doi:10.1016/0003-9969(84)90060-8 · Cited by 32 · see citing works
Reduction of Proteolytic Degradation by Chlorhexidine
Grenier, D. (1993) · Journal of Dental Research · doi:10.1177/00220345930720031301 · Cited by 31 · see citing works
The development of an altered gingival crevicular microflora in the alloxan-diabetic rat
McNamara, T. F., Ramamurthy, N., Mulvihill, J. E., et al. (1982) · Archives of Oral Biology · doi:10.1016/0003-9969(82)90055-3 · Cited by 29 · see citing works
pH gradients induced by urea metabolism in ‘artificial mouth’ microcosm plaques
Sissons, C. H., Wong, L., Hancock, E. M., et al. (1994) · Archives of Oral Biology · doi:10.1016/0003-9969(94)90147-3 · Cited by 26 · see citing works
The Effect of Fluorhydroxyapatite-derived Fluoride on Acid Production by Streptococci
Guha‐Chowdhury, N., Iwami, Y., YAMADA, T., et al. (1995) · Journal of Dental Research · doi:10.1177/00220345950740091901 · Cited by 24 · see citing works
Streptococcus mutans in plaque after mouth‐rinsing with buffers of varying pH value
Svanberg, M. L. (1980) · European Journal Of Oral Sciences · doi:10.1111/j.1600-0722.1980.tb00723.x · Cited by 24 · see citing works
The pH response to urea and the effect of liquid flow in ‘artificial mouth’ microcosm plaques
Sissons, C. H., Wong, L., Hancock, E. M., et al. (1994) · Archives of Oral Biology · doi:10.1016/0003-9969(94)90146-5 · Cited by 23 · see citing works
Effect of utilization of substrates on the composition of dental plaque
van der Hoeven, J. S., Jong, M. H., & Rogers, A. H. (1985) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1985.tb01140.x · Cited by 23 · see citing works
Beckers, H. J., & van der Hoeven, J. S. (1982) · Infection and Immunity · doi:10.1128/iai.38.1.8-13.1982 · Cited by 23 · see citing works
Rogers, A. H., Zilm, P. S., & Gully, N. J. (1987) · Microbial Ecology · doi:10.1007/bf02012940 · Cited by 21 · see citing works
Factors Controlling the Microflora of the Healthy Mouth
Theilade, E. (2020) · CRC Press eBooks · doi:10.1201/9781003068020-1 · Cited by 21 · see citing works
Grenby, T. H., & Saldanha, M. G. (2009) · Caries Research · doi:10.1159/000260914 · Cited by 18 · see citing works
Chlorhexidine affects arginine metabolism as well as glycolysis in a strain of Streptococcus sanguis
Rogers, A. H., Zilm, P. S., Gully, N. J., et al. (1987) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1987.tb00303.x · Cited by 14 · see citing works
Utilization of nitrogenous compounds by oral bacteria
Rogers, A. H. (1990) · Australian Dental Journal · doi:10.1111/j.1834-7819.1990.tb05432.x · Cited by 11 · see citing works
The effect of a redox agent, methylene blue, on the survival ofPorphyromonas gingivalis in vitro
Fletcher, J. M., & Wilson, M. J. (1993) · Current Microbiology · doi:10.1007/bf01577341 · Cited by 11 · see citing works
Wu-Yuan, C. D. (1991) · PubMed · Cited by 11 · see citing works
Effect of utilization of substrates on the composition of dental plaque
VANDERHOEVEN, J., DEJONG, M., & Rogers, A. H. (1985) · FEMS Microbiology Letters · doi:10.1016/0378-1097(85)90013-8 · Cited by 11 · see citing works
Interaction of Saccharin with Hexitol Metabolism by Streptococcus mutans
Best, G. M., & Brown, A. T. (2009) · Caries Research · doi:10.1159/000261023 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Are dental diseases examples of ecological catastrophes?
Marsh, P. D. (2003) · Microbiology · doi:10.1099/mic.0.26082-0 · Cited by 1,256 · see citing works
Self-citationSegata, N., Haake, S. K., Mannon, P., Lemon, K. P., Waldron, L., Gevers, D., Huttenhower, C., & Izard, J. (2012) · Genome Biology · doi:10.1186/gb-2012-13-6-r42 · Cited by 1,076 · see citing works
Oral Microbial Communities: Biofilms, Interactions, and Genetic Systems
Kolenbrander, P. E. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.413 · Cited by 894 · see citing works
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
Mass Transport of Macromolecules within an In Vitro Model of Supragingival Plaque
Thurnheer, T., Gmür, R., Shapiro, S., & Guggenheim, B. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.3.1702-1709.2003 · Cited by 145 · see citing works
Advancements toward a systems level understanding of the human oral microbiome
McLean, J. S. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00098 · Cited by 108 · see citing works
Edlund, A., Yang, Y., Yooseph, S., Hall, A. P., Nguyen, D. D., Dorrestein, P. C., Nelson, K. E., He, X., Lux, R., Shi, W., et al. (2015) · The ISME Journal · doi:10.1038/ismej.2015.72 · Cited by 84 · see citing works
- Authors
- Marsh, P. D., & Bradshaw, D. J.
- Affiliations
- Leeds Dental Hospital (GB)
- Centre for Applied Microbiology & Research Research Division Salisbury, SP4 OJG
- Venue
- Advances in Dental Research
- Publisher
- SAGE Publications
- Published
- 1997-04
- Volume
- 11
- Issue
- 1
- Pages
- 176-185
- ISSN
- 0895-9374 (ISSN-L)
- 1544-0737
- OpenAlex
- W2070541275
- Cited by
- 132
- References
- 56
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 2 · 2018: 3 · 2017: 9 · 2016: 4 · 2015: 5 · 2014: 10 · 2013: 6 · 2012: 3
- FWCI
- 6.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Advances in Dental Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Health Sciences › Dentistry › Periodontics › Dental Health and Care Utilization
- Keywords
- dental plaque, oral microbiota, mutans streptococci, lactobacilli, dental caries, periodontal disease, plaque pH, redox potential, gingival crevicular fluid, gingivitis, redox agents, artificial sweeteners, anti-inflammatory agents
- MeSH terms
- Animals, Bacteria, Dental Caries, Dental Plaque, Dietary Carbohydrates, Homeostasis, Humans, Hydrogen-Ion Concentration, Oxidation-Reduction, Periodontal Diseases, Sweetening Agents, Ecosystem, Biofilms
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
