Cited by 145Oral microbiology and periodontitis researchBacterial biofilms and quorum sensingDental Health and Care Utilization

The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.

Mass Transport of Macromolecules within an In Vitro Model of Supragingival Plaque

Open access

Thurnheer, Thomas, Gmür, Rudolf, Shapiro, Stuart, Guggenheim, Bernhard·2003·Applied and Environmental Microbiology

DOI 10.1128/aem.69.3.1702-1709.2003PMC PMC150054

Open this paper in CoChat — free account

Abstract

The aim of this study was to examine the diffusion of macromolecules through an in vitro biofilm model of supragingival plaque. Polyspecies biofilms containing Actinomyces naeslundii , Fusobacterium nucleatum , Streptococcus oralis , Streptococcus sobrinus , Veillonella dispar , and Candida albicans were formed on sintered hydroxyapatite disks and then incubated at room temperature for defined periods with fluorescent markers with molecular weights ranging from 3,000 to 900,000. Subsequent examination by confocal laser scanning microscopy revealed that the mean square penetration depths for all tested macromolecules except immunoglobulin M increased linearly with time, diffusion coefficients being linearly proportional to the cube roots of the molecular weights of the probes (range, 10,000 to 240,000). Compared to diffusion in bulk water, diffusion in the biofilms was markedly slower. The rate of diffusion for each probe appeared to be constant and not a function of biofilm depth. Analysis of diffusion phenomena through the biofilms suggested tortuosity as the most probable explanation for retarded diffusion. Selective binding of probes to receptors present in the biofilms could not explain the observed extent of retardation of diffusion. These results are relevant to oral health, as selective attenuated diffusion of fermentable carbohydrates and acids produced within dental plaque is thought to be essential for the development of carious lesions.

Integrity signals

Registry

Crossref · 10.1128/aem.69.3.1702-1709.2003

Cites

62 of 62 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen
Einstein, A. (1905) · Annalen der Physik · doi:10.1002/andp.19053220806 · Cited by 8,762
MICROBIAL BIOFILMS
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 4,921
An Introduction to Error Analysis
Taylor, J. R. (1982) · Medical Entomology and Zoology · Cited by 2,807
An Introduction to Error Analysis: The Study of Uncertainties in Physical Measurements
Taylor, J. R., & Thompson, W. (1998) · Physics Today · doi:10.1063/1.882103 · Cited by 2,734
Zur kinetischen Theorie der Brownschen Molekularbewegung und der Suspensionen
Smoluchowski, M. (1906) · Annalen der Physik · doi:10.1002/andp.19063261405 · Cited by 1,515
Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum.
Nicholson, C., & Phillips, J. M. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013981 · Cited by 785
Diffusion and related transport mechanisms in brain tissue
Nicholson, C. (2001) · Reports on Progress in Physics · doi:10.1088/0034-4885/64/7/202 · Cited by 498
Validation of an in vitro Biofilm Model of Supragingival Plaque
Guggenheim, B., Giertsen, E., Schüpbach, P., & Shapiro, S. (2001) · Journal of Dental Research · doi:10.1177/00220345010800011201 · Cited by 358
Self-citation
Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes
Ramsing, N. B., Kuhl, M. E., & Jørgensen, B. B. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.11.3840-3849.1993 · Cited by 275
Salivary α-Amylase: Role in Dental Plaque and Caries Formation
Scannapieco, F. A., Torres, G., & Levine, M. J. (1993) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411930040030701 · Cited by 272
Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging
Nicholson, C., & Tao, L. (1993) · Biophysical Journal · doi:10.1016/s0006-3495(93)81324-9 · Cited by 266
Hereditary fructose intolerance
Froesch, E. R., Wolf, H. P., Baitsch, H., Prader, A., & Labhart, A. (1963) · The American Journal of Medicine · doi:10.1016/0002-9343(63)90050-0 · Cited by 254
Food Starches and Dental Caries
Lingström, P., van Houte, J., & Kashket, S. (2000) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411000110030601 · Cited by 238
Determination of Diffusion Coefficients in Biofilms by Confocal Laser Microscopy
Lawrence, J. R., Wolfaardt, G. M., & Korber, D. R. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.4.1166-1173.1994 · Cited by 209
An in vitro Oral Biofilm Model for Comparing the Efficacy of Antimicrobial Mouthrinses
Shapiro, S., Giertsen, E., & Guggenheim, B. (2002) · Caries Research · doi:10.1159/000057866 · Cited by 189
Self-citation
Immobilized cells: basics and applications.
Wijffels, R. H., Buitelaar, R. M., Bucke, C., & TRAMPER, J. (1996) · Socio-Environmental Systems Modeling · Cited by 188
Entropic trapping of macromolecules by mesoscopic periodic voids in a polymer hydrogel
Liu, L., Li, P., & Asher, S. A. (1999) · Nature · doi:10.1038/16426 · Cited by 186
Antigenic heterogeneity of Bacteroides intermedius as recognized by monoclonal antibodies
Gmür, R., & Guggenheim, B. (1983) · Infection and Immunity · doi:10.1128/iai.42.2.459-470.1983 · Cited by 183
Self-citation
Distribution of Sulfate-Reducing and Methanogenic Bacteria in Anaerobic Aggregates Determined by Microsensor and Molecular Analyses
Santegoeds, C. M., Damgaard, L. R., Hesselink, G., Zopfi, J., Lens, P. N. L., Gerard Muyzer, C., & de Beer, D. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.10.4618-4629.1999 · Cited by 153
Sugar and Dental Caries: A Review of Human Studies
Newbrun, E. (1982) · Science · doi:10.1126/science.7046052 · Cited by 137
Physiological Approaches to the Control of Oral Biofilms
Marsh, P. D., & Bradshaw, D. J. (1997) · Advances in Dental Research · doi:10.1177/08959374970110010901 · Cited by 132
Microelectrode measurements of local mass transport rates in heterogeneous biofilms
Rasmussen, K., & Lewandowski, Z. (1998) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19980805)59:3 · Cited by 130
Diffusional transport of macromolecules in developing nerve processes
Popov, S., & Poo, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00077.1992 · Cited by 120
Isolation of a glucan-binding domain of glucosyltransferase (1,6-alpha-glucan synthase) from Streptococcus sobrinus
Mooser, G., & Wong, C. (1988) · Infection and Immunity · doi:10.1128/iai.56.4.880-884.1988 · Cited by 114
Dental plaque revisited: oral biofilms in health and disease
Wilson, M., & Wilson, M. (1998) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.1998.tb02341.x · Cited by 114
Carbohydrates in Pooled Dental Plaque
Hotz, P., Guggenheim, B., & Schmid, R. (2009) · Caries Research · doi:10.1159/000259783 · Cited by 110
Self-citation
Local macromolecule diffusion coefficients in structurally non-uniform bacterial biofilms using fluorescence recovery after photobleaching (FRAP)
Bryers, J. D., & Drummond, F. (1998) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19981120)60:4 · Cited by 110
Heterogeneity of Diffusion Inside Microbial Biofilms Determined by Fluorescence Correlation Spectroscopy Under Two-photon Excitation¶
Guiot, E., Georges, P., Brun, A., Fontaine‐Aupart, M., Bellon‐Fontaine, M., & Briandet, R. (2002) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2002)0750570hodimb2.0.co2 · Cited by 99
Evidence that tropical soil environment can support the growth of Escherichia coli
Byappanahalli, M. N., & Fujioka, R. S. (1998) · Water Science & Technology · doi:10.2166/wst.1998.0533 · Cited by 91
Spatial Arrangements and Associative Behavior of Species in an In Vitro Oral Biofilm Model
Guggenheim, M., Shapiro, S., Gmür, R., & Guggenheim, B. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.3.1343-1350.2001 · Cited by 84
Self-citation
Diffusion in Pseudomonas aeruginosa biofilms: a pulsed field gradient NMR study
Vogt, M., Flemming, H., & Veeman, W. S. (2000) · Journal of Biotechnology · doi:10.1016/s0168-1656(99)00213-8 · Cited by 82
Dental plaque revisited--oral biofilms in health and disease.
Newman, H., & Wilson, M. M. (2000) · PubMed · Cited by 80
Diffusion of Dextran in Aqueous (Hydroxypropyl)cellulose
Bu, Z., & Russo, P. S. (1994) · Macromolecules · doi:10.1021/ma00083a017 · Cited by 75
Measurement of local effective diffusivity in heterogeneous biofilms
Beyenal, H., Tanyolaç, A., & Lewandowski, Z. (1998) · Water Science & Technology · doi:10.2166/wst.1998.0804 · Cited by 74
Macromolecules released from polymers: diffusion into unstirred fluids
Radomsky, M. L., Whaley, K. J., Ra, C., & Saltzman, W. M. (1990) · Biomaterials · doi:10.1016/0142-9612(90)90018-l · Cited by 73
Bacterial Metabolism in Dental Biofilms
Carlsson, J. (1997) · Advances in Dental Research · doi:10.1177/08959374970110012001 · Cited by 67
Integration of Raman microscopy, differential interference contrast microscopy, and attenuated total reflection Fourier transform infrared spectroscopy to investigate chlorhexidine spatial and temporal distribution in Candida albicans biofilms
Suci, P. A., Geesey, G. G., & Tyler, B. J. (2001) · Journal of Microbiological Methods · doi:10.1016/s0167-7012(01)00268-8 · Cited by 65
A Chemical and Histological Study of Artificial Caries in Human Dental Enamel in vitro
Ingram, G. S., & Silverstone, L. M. (2009) · Caries Research · doi:10.1159/000260543 · Cited by 62
Crystallohydrodynamics for solving the hydration problem for multi-domain proteins: open physiological conformations for human IgG
Carrasco, B., de la Torre, J. G., Davis, K. G., Jones, S., Athwal, D., Walters, C., Burton, D. R., & Harding, S. E. (2001) · Biophysical Chemistry · doi:10.1016/s0301-4622(01)00220-4 · Cited by 62
Diffusion of sugars and carboxylic acids through human dental plaque in vitro
Dibdin, G. H. (1981) · Archives of Oral Biology · doi:10.1016/0003-9969(81)90010-8 · Cited by 59
The Discovery of a Novel R-phycoerythrin from an Antarctic Red Alga
MacColl, R., Eisele, L. E., Williams, E. C., & Bowser, S. S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.29.17157 · Cited by 52
Fractal structure of biofilms: new tools for investigation of morphology
(1995) · Water Science & Technology · doi:10.1016/0273-1223(96)00013-3 · Cited by 50
Diffusion of Radio tracers in Human Dental Plaque
Tatevossian, A. (2009) · Caries Research · doi:10.1159/000260396 · Cited by 39
Removal and recovery of lead fixed-bed biosorption with immobilized bacterial biomass
(1998) · Water Science & Technology · doi:10.1016/s0273-1223(98)00526-5 · Cited by 35
Glucan Inhibition of Diffusion in Plaque
Hojo, S., Higuchi, M., & Araya, S. (1976) · Journal of Dental Research · doi:10.1177/00220345760550011501 · Cited by 35
Hereditary fructose intolerance. Dental status of eight patients.
Tm, M., & Froesch, E. R. (1967) · PubMed · Cited by 33
Multidimensional Modeling of Biofilm Structure
Picioreanu, C. (1999) · Research Repository (Delft University of Technology) · Cited by 31
Diffusion and binding measurements within oral biofilms using fluorescence photobleaching recovery methods
Birmingham, J. J., Hughes, N. P., & Treloar, R. (1995) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1995.0168 · Cited by 27
Effect of extracellular polysaccharides on diffusion of NaF and [14C]-sucrose in human dental plaque and in sediments of the bacterium Streptococcus sanguis 804 (NCTC 10904)
McNee, S. G., Geddes, D. A. M., Weetman, D. A., Sweeney, D., & BEELEY, J. A. (1982) · Archives of Oral Biology · doi:10.1016/0003-9969(82)90107-8 · Cited by 27
Time-resolved study of biofilm architecture and transport processes using experimental and simulation techniques: the role of EPS
Kuehn, M., Mehl, M., Hausner, M., Bungartz, H., & Wuertz, S. (2001) · Water Science & Technology · doi:10.2166/wst.2001.0361 · Cited by 27
Fractal structure of biofilms: new tools for investigation of morphology
Hermanowicz, S. W., Schindler, U., & Wilderer, P. A. (1995) · Water Science & Technology · doi:10.2166/wst.1995.0273 · Cited by 27
A Brief Survey of Recent in vitro Work on Diffusion of Small Ions and Molecules in Dental Plaque
Dibdin, G. H. (2015) · KARGER eBooks · doi:10.1159/000408738 · Cited by 23
Effect of SDS Micelles on Rhodamine-B Diffusion in Hydrogels
Häglund, B. O., Sundelöf, L., Upadrashta, S. M., & Wurster, D. E. (1996) · Journal of Chemical Education · doi:10.1021/ed073p889 · Cited by 19
Uptake of phenylacetic acid by two strains ofPenicillium chrysogenum
Eriksen, S. H., Søderblom, T. B., Jensen, B., & Olsen, J. (1998) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19981105)60:3 · Cited by 17
Characterization of monoclonal antibodies for rapid identification of in clinical samples
Thurnheer, T., Guggenheim, B., & Gmür, R. (1997) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(97)00125-0 · Cited by 15
Self-citation
Characterization of monoclonal antibodies for rapid identification of Actinomyces naeslundii in clinical samples
Thurnheer, T., Guggenheim, B., & Gmür, R. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1997.tb10378.x · Cited by 15
Self-citation
Fiber-optic microsensors to measure backscattered light intensity in biofilms
Beyenal, H., Lewandowski, Z., Yakymyshyn, C. P., Lemley, B., & Wehri, J. (2000) · Applied Optics · doi:10.1364/ao.39.003408 · Cited by 14
Application of mineral support on cephamycin C production in culture using soybean oil as the sole carbon source
Ichida, M., Park, Y., 小堺, 裕., & Okabe, M. (1997) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19970120)53:2 · Cited by 11
Competition between nitrogen-fixing cyanobacteria during phosphorus-limited growth
Nobel, W. T. D., Staats, N., & Mur, L. R. (1995) · Water Science & Technology · doi:10.1016/0273-1223(95)00685-0 · Cited by 10
Local Mass Transfer Coefficients in Bacterial Biofilms Using Fluorescence Recovery After Photobleaching (FRAP)
Bryers, J. D., & Drummond, F. (1996) · Progress in biotechnology · doi:10.1016/s0921-0423(96)80028-1 · Cited by 6
Water law and human rights - roles and responsibilities
de Lange, M. (2001) · Water Science & Technology · doi:10.2166/wst.2001.0204 · Cited by 6
Biofilm structure and behaviour: influence of hydrodynamics and nutrients
Stoodley, P., Boyle, J. D., & Lappin-Scott, H. M. (1999) · ePrints Soton (University of Southampton) · Cited by 5

Research works printed but not linked: 3

10.1562/0031-8655(2002)075<0570:HODIMB>2.0.CO;2 · DOI
Hermanowicz S. W. 2003. Biofilm structure: an interplay of models and experiments p. 32-47. In S. Wuertz P. L. Bishop and P. A. Wilderer (ed.) Biofilms in wastewater treatment—an interdisciplinary approach in press. International Water Association Publishing London United Kingdom.
von Smoluchowski, M. 1906. Zur kinetischen Theorie der Brownschen Molekularbegegung und der Suspension. Ann. Phys.21:756-780.

Sorted by citations

Biology of Streptococcus mutans-Derived Glucosyltransferases: Role in Extracellular Matrix Formation of Cariogenic Biofilms
Bowen, W. H., & Koo, H. (2011) · Caries Research · doi:10.1159/000324598 · Cited by 1,085
The biofilm matrix: multitasking in a shared space
Flemming, H., van Hullebusch, E. D., Neu, T. R., Nielsen, P. H., Seviour, T. W., Stoodley, P., Wingender, J., & Wuertz, S. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00791-0 · Cited by 1,062
Resistance of bacterial biofilms to disinfectants: a review
Bridier, A., Briandet, R., Thomas, V., & Dubois‐Brissonnet, F. (2011) · Biofouling · doi:10.1080/08927014.2011.626899 · Cited by 997
Dental Plaque as a Microbial Biofilm
Marsh, P. D. (2004) · Caries Research · doi:10.1159/000077756 · Cited by 763
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 all 145

Authors: Thurnheer, T., Gmür, R., Shapiro, S., & Guggenheim, B.
Affiliations: University of Zurich (CH)
Institute for Oral Microbiology and General Immunology, University of Zürich, CH-8028 Zürich, Switzerland
ORCID: Thurnheer, Thomas
Shapiro, Stuart
Venue: Applied and Environmental Microbiology
Publisher: American Society for Microbiology
Published: 2003-03
Volume: 69
Issue: 3
Pages: 1702-1709
ISSN: 0099-2240 (ISSN-L)
1098-5336
DOI: 10.1128/aem.69.3.1702-1709.2003
PMC: PMC150054
OpenAlex: W2166083475
Cited by: 145
References: 62
Citations by year: 2026: 1 · 2025: 2 · 2024: 3 · 2023: 7 · 2022: 5 · 2021: 10 · 2020: 5 · 2019: 4 · 2018: 8 · 2017: 3 · 2016: 6 · 2015: 11 · 2014: 6 · 2013: 11 · 2012: 6
FWCI: 9.97
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Applied and Environmental Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich)
Funders: Universität Konstanz
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 › General Dentistry › Dental Health and Care Utilization
Keywords: supragingival plaque, dental plaque, macromolecular diffusion, diffusion coefficient, molecular weight dependence, tortuosity, fluorescent probes, immunoglobulin M, Actinomyces naeslundii, Fusobacterium nucleatum, Streptococcus sobrinus, Streptococcus oralis, Veillonella dispar, Candida albicans, hydroxyapatite, caries development, oral health
MeSH terms: Actinomyces, Albumins, Candida albicans, Dental Plaque, Dextrans, Diffusion, Fluorescent Dyes, Gingiva, Models, Biological, Veillonella, Fusobacterium nucleatum, Streptococcus sobrinus, Biofilms, Streptococcus oralis, Macromolecular Substances

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

Mass Transport of Macromolecules within an In Vitro Model of Supragingival Plaque

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks