Biofilm formation by the oral pioneer colonizer Streptococcus gordonii: an experimental and numerical study.

For decades, extensive research efforts have been conducted to improve the functionality and stability of implants. Especially in dentistry, implant treatment has become a standard medical practice. The treatment restores full dental functionality, helping patients to maintain high quality of life. However, about 10% of the patients suffer from early and late device failure due to peri-implantitis, an inflammatory disease of the tissues surrounding the implant. Peri-implantitis is caused by progressive microbial colonization of the device surface and the formation of microbial communities, so-called biofilms. This infection can ultimately lead to implant failure. The causative agents for the inflammatory disease, periodontal pathogenic biofilms, have already been extensively studied, but are still not completely understood. As numerical simulations will have the potential to predict oral biofilm formation precisely in the future, for the first time, this study aimed to analyze Streptococcus gordonii biofilms by combining experimental studies and numerical simulation. The study demonstrated that numerical simulation was able to precisely model the influence of different nutrient concentration and spatial distribution of active and inactive biomass of the biofilm in comparison with the experimental data. This model may provide a less time-consuming method for the future investigation of any bacterial biofilm.

[1]  D. Wildenschild,et al.  Biofilm growth in porous media: Experiments, computational modeling at the porescale, and upscaling , 2015, 1510.01218.

[2]  Zhibing Zhang,et al.  Characterisation of bacterial adhesion and removal in a flow chamber by micromanipulation measurements , 2008, Biotechnology Letters.

[3]  H. C. van der Mei,et al.  Initial microbial adhesion is a determinant for the strength of biofilm adhesion. , 1995, FEMS microbiology letters.

[4]  J W Wimpenny,et al.  Individual-based modelling of biofilms. , 2001, Microbiology.

[5]  J. A. Aas,et al.  Defining the Normal Bacterial Flora of the Oral Cavity , 2005, Journal of Clinical Microbiology.

[6]  P. Kolenbrander,et al.  Mutualistic Biofilm Communities Develop with Porphyromonas gingivalis and Initial, Early, and Late Colonizers of Enamel , 2009, Journal of bacteriology.

[7]  A. Sculean,et al.  Confusion over live/dead stainings for the detection of vital microorganisms in oral biofilms - which stain is suitable? , 2014, BMC oral health.

[8]  O. Petersen,et al.  Excretion of magnesium, calcium, and inorganic phosphate by the cat submandibular gland , 2004, Pflügers Archiv.

[9]  J. Barbeau,et al.  The buccale puzzle: The symbiotic nature of endogenous infections of the oral cavity. , 2002, The Canadian journal of infectious diseases = Journal canadien des maladies infectieuses.

[10]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[11]  G. J. Verkerke,et al.  Comparison of Velocity Profiles for Different Flow Chamber Designs Used in Studies of Microbial Adhesion to Surfaces , 2003, Applied and Environmental Microbiology.

[12]  Pascal Meier,et al.  Apoptosis in development , 2000, Nature.

[13]  P. Kolenbrander,et al.  Role of Streptococcus gordoniiAmylase-Binding Protein A in Adhesion to Hydroxyapatite, Starch Metabolism, and Biofilm Formation , 2001, Infection and Immunity.

[14]  M. Kilian,et al.  Taxonomic Study of Viridans Streptococci: Description of Streptococcus gordonii sp. nov. and Emended Descriptions of Streptococcus sanguis (White and Niven 1946), Streptococcus oralis (Bridge and Sneath 1982), and Streptococcus mitis (Andrewes and Horder 1906) , 1989 .

[15]  G. Ginsburg,et al.  The oral microbiome in health and disease and the potential impact on personalized dental medicine. , 2012, Oral diseases.

[16]  J. Costerton,et al.  Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms , 2002, Clinical Microbiology Reviews.

[17]  Mark R. Marten,et al.  Proteomic analysis of Staphylococcus aureus biofilm cells grown under physiologically relevant fluid shear stress conditions , 2014, Proteome Science.

[18]  L. Montanaro,et al.  Biofilm in Implant Infections: Its Production and Regulation , 2005, The International journal of artificial organs.

[19]  P. Stewart,et al.  Antimicrobial Penetration and Efficacy in an In Vitro Oral Biofilm Model , 2011, Antimicrobial Agents and Chemotherapy.

[20]  M. D. del Aguila,et al.  Analyses of Streptococcus mutans in saliva with species-specific monoclonal antibodies. , 2002, Hybridoma and hybridomics.

[21]  D. Hempel,et al.  Substrate utilization and mass transfer in an autotrophic biofilm system: Experimental results and numerical simulation. , 1997, Biotechnology and bioengineering.

[22]  M. Raff,et al.  Social controls on cell survival and cell death , 1992, Nature.

[23]  S. Kjelleberg,et al.  Cell Death in Pseudomonas aeruginosa Biofilm Development , 2003, Journal of bacteriology.

[24]  M. Wilson,et al.  Measuring the thickness of an outer layer of viable bacteria in an oral biofilm by viability mapping. , 2003, Journal of microbiological methods.

[25]  T. Beikler,et al.  Control of oral biofilms. , 2011, Periodontology 2000.

[26]  M. Jacques,et al.  Review: Microbial colonization of prosthetic devices , 1987, Microbial Ecology.

[27]  B. Nyvad,et al.  Transmission electron microscopy of early microbial colonization of human enamel and root surfaces in vivo. , 1987, Scandinavian journal of dental research.

[28]  K. Lewis,et al.  Programmed Death in Bacteria , 2000, Microbiology and Molecular Biology Reviews.

[29]  Mark Kittisopikul,et al.  Localized cell death focuses mechanical forces during 3D patterning in a biofilm , 2012, Proceedings of the National Academy of Sciences.

[30]  E. Greenberg,et al.  Sociomicrobiology: the connections between quorum sensing and biofilms. , 2005, Trends in microbiology.

[31]  H. Engelberg-Kulka,et al.  Addiction modules and programmed cell death and antideath in bacterial cultures. , 1999, Annual review of microbiology.

[32]  J. Costerton,et al.  Mechanism of electrical enhancement of efficacy of antibiotics in killing biofilm bacteria , 1994, Antimicrobial Agents and Chemotherapy.

[33]  H. Kuramitsu,et al.  Biofilm Formation by the Periodontopathic Bacteria Treponema denticola and Porphyromonas gingivalis. , 2005, Journal of periodontology.

[34]  J. Costerton,et al.  Optical sectioning of microbial biofilms , 1991, Journal of bacteriology.

[35]  J. Monod The Growth of Bacterial Cultures , 1949 .

[36]  L. Hancock,et al.  A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis , 2009, Molecular microbiology.

[37]  T. Attin,et al.  Impact of laminar flow velocity of different acids on enamel calcium loss , 2012, Clinical Oral Investigations.

[38]  J. Burgess,et al.  Life after death: the critical role of extracellular DNA in microbial biofilms , 2013, Letters in applied microbiology.

[39]  W. G. Characklis,et al.  Characterization of initial events in bacterial surface colonization by two Pseudomonas species using image analysis , 1992, Biotechnology and bioengineering.

[40]  H. Horvitz,et al.  Mechanisms and functions of cell death. , 1991, Annual review of cell biology.

[41]  D. Hempel,et al.  Behaviour of biofilm systems under varying hydrodynamic conditions. , 2004, Water science and technology : a journal of the International Association on Water Pollution Research.

[42]  H. C. van der Mei,et al.  Microbial Adhesion in Flow Displacement Systems , 2006, Clinical Microbiology Reviews.

[43]  R. Palmer,et al.  Molecular Characterization of Subject-Specific Oral Microflora during Initial Colonization of Enamel , 2006, Applied and Environmental Microbiology.

[44]  Yung-Hua Li,et al.  Quorum sensing and biofilm formation in Streptococcal infections. , 2003, The Journal of clinical investigation.

[45]  Xiaolin Tian,et al.  Quorum Sensing and Bacterial Social Interactions in Biofilms , 2012, Sensors.

[46]  T. Hughes,et al.  Space-time finite element methods for elastodynamics: formulations and error estimates , 1988 .

[47]  B. Rittmann,et al.  Development and experimental evaluation of a steady‐state, multispecies biofilm model , 1992, Biotechnology and bioengineering.

[48]  A Laupacis,et al.  The effect of elective total hip replacement on health-related quality of life. , 1993, The Journal of bone and joint surgery. American volume.

[49]  Gary C Armitage,et al.  Periodontal diagnoses and classification of periodontal diseases. , 2004, Periodontology 2000.

[50]  S. J. Caldwell,et al.  Multicellular Organization in a Degradative Biofilm Community , 1994, Applied and environmental microbiology.

[51]  L. Håvarstein,et al.  Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  C. Shun,et al.  Platelets enhance biofilm formation and resistance of endocarditis-inducing streptococci on the injured heart valve. , 2012, The Journal of infectious diseases.

[53]  S. Socransky,et al.  Identification of early microbial colonizers in human dental biofilm , 2004, Journal of applied microbiology.

[54]  Robert J. Palmer,et al.  Communication among Oral Bacteria , 2002, Microbiology and Molecular Biology Reviews.

[55]  E. Hellwig,et al.  Individual Vitality Pattern of in situ Dental Biofilms at Different Locations in the Oral Cavity , 2004, Caries Research.

[56]  James N. Petersen,et al.  Microbial growth and transport in porous media under denitrification conditions : experiments and simulations , 1997 .

[57]  J. Foster,et al.  Development of a Multispecies Oral Bacterial Community in a Saliva-Conditioned Flow Cell , 2004, Applied and Environmental Microbiology.

[58]  E. Decker The ability of direct fluorescence‐based, two‐colour assays to detect different physiological states of oral streptococci , 2001, Letters in applied microbiology.

[59]  K. Foster,et al.  The sociobiology of biofilms. , 2009, FEMS microbiology reviews.

[60]  Y. Tsai Impact of flow velocity on the dynamic behaviour of biofilm bacteria , 2005, Biofouling.

[61]  David L. Vaux,et al.  An evolutionary perspective on apoptosis , 1994, Cell.

[62]  Haluk Beyenal,et al.  Fundamentals of biofilm research , 2007 .

[63]  I. Klapper,et al.  A Multidimensional Multispecies Continuum Model for Heterogeneous Biofilm Development , 2007, Bulletin of mathematical biology.

[64]  U. Nackenhorst,et al.  A combined FIC‐TDG finite element approach for the numerical solution of coupled advection–diffusion–reaction equations with application to a bioregulatory model for bone fracture healing , 2012 .

[65]  C. Dawes,et al.  Estimation of the Velocity of the Salivary Film at Some Different Locations in the Mouth , 1989, Journal of dental research.

[66]  G H Dibdin,et al.  Mathematical Modeling of Biofilms , 1997, Advances in dental research.

[67]  J. Derks,et al.  Peri-implant health and disease. A systematic review of current epidemiology. , 2015, Journal of clinical periodontology.

[68]  H. Steller Mechanisms and genes of cellular suicide , 1995, Science.

[69]  Ling Li,et al.  An analytical solution for predicting the transient seepage from a subsurface drainage system , 2016 .

[70]  J. Bernimoulin Recent concepts in plaque formation. , 2003, Journal of clinical periodontology.

[71]  G. Bowden,et al.  Nutritional Influences on Biofilm Development , 1997, Advances in dental research.

[72]  J. Kreft,et al.  Biofilms promote altruism. , 2004, Microbiology.

[73]  J. Featherstone The caries balance: the basis for caries management by risk assessment. , 2004, Oral health & preventive dentistry.

[74]  E. Hellwig,et al.  Effect of two antimicrobial agents on early in situ biofilm formation. , 2005, Journal of clinical periodontology.

[75]  L. Hancock,et al.  Regulation of Autolysis-Dependent Extracellular DNA Release by Enterococcus faecalis Extracellular Proteases Influences Biofilm Development , 2008, Journal of bacteriology.

[76]  D. Cvitkovitch,et al.  Regulation of the Competence Pathway as a Novel Role Associated with a Streptococcal Bacteriocin , 2011, Journal of bacteriology.

[77]  Ravindra Duddu,et al.  A two‐dimensional continuum model of biofilm growth incorporating fluid flow and shear stress based detachment , 2009, Biotechnology and bioengineering.

[78]  杜昕,et al.  Infective endocarditis , 2007 .