Direct measurement of ultrasonic activity on microbial metabolism and analysis of related uncertainty

The scope of this work is to identify the relation that exists between the alterations of the bacterial metabolism and the exposition to an ultrasonic field (O'Leary et al. 1997, Piyasena et al. 2003, Brujan2004). To made this relation quantifiable they will be used repeatable and reproducible metrological methods. To obtain this result the research will be centred on 3 specific goal: 1. To realise a measurement of the ultrasonic field, generated by an ultrasonic bath, using an hydrophone calibrated specifically with the wavelengths applied (Canney et al. 2008). 2. To choose a method, through uncertainty evaluation, to expose microbes to the ultrasonic field without an excessive alteration of the generated acoustic pressure. 3. To find a method to measure bacterial viability, represented by the planktonic growth and the biofilm development, after exposure to the ultrasounds. Studying the relationship between the bacteria metabolism and ultrasonic exposure it will be possible to identify novels and more precise methods to treat bacterial colonizations. This result will be in fact useful in various fields where the bacterial presence, and in particular biofilm development, is today an unresolved problem. At the same time this research will put the basis for many further studies that will be realized applying the same methods with different bacterial species, ultrasounds exposition conditions or ultrasonic devices

[1]  M. Wiedmann,et al.  Microtiter Plate Assay for Assessment of Listeria monocytogenes Biofilm Formation , 2002, Applied and Environmental Microbiology.

[2]  W. Nyborg Ultrasonic microstreaming and related phenomena. , 1982, The British journal of cancer. Supplement.

[3]  G. Orrù,et al.  Usefulness of real time PCR for the differentiation and quantification of 652 and JP2 Actinobacillus actinomycetemcomitans genotypes in dental plaque and saliva , 2006, BMC infectious diseases.

[4]  W. Pitt,et al.  Ultrasonic enhancement of antibiotic action on gram-negative bacteria , 1994, Antimicrobial Agents and Chemotherapy.

[5]  P. Stewart,et al.  Biofilm resistance to antimicrobial agents. , 2000, Microbiology.

[6]  T. D. de Kievit Quorum sensing in Pseudomonas aeruginosa biofilms. , 2009, Environmental microbiology.

[7]  J. Crump,et al.  Intravascular Catheter-Associated Infections , 2000, European Journal of Clinical Microbiology and Infectious Diseases.

[8]  S. Yadav,et al.  Biofilms: microbes and disease. , 2008, The Brazilian journal of infectious diseases : an official publication of the Brazilian Society of Infectious Diseases.

[9]  D. Wozniak,et al.  Role of polysaccharides in Pseudomonas aeruginosa biofilm development. , 2007, Current opinion in microbiology.

[10]  P. Sanderson Infection in orthopaedic implants. , 1991, The Journal of hospital infection.

[11]  Mark R Prausnitz,et al.  Bioeffects caused by changes in acoustic cavitation bubble density and cell concentration: a unified explanation based on cell-to-bubble ratio and blast radius. , 2003, Ultrasound in medicine & biology.

[12]  Diane Dalecki,et al.  Ultrasonic excitation of a bubble inside a deformable tube: implications for ultrasonically induced hemorrhage. , 2008, The Journal of the Acoustical Society of America.

[13]  N. Yakandawala,et al.  A microplate spectrofluorometric assay for bacterial biofilms , 2006, Journal of Industrial Microbiology & Biotechnology.

[14]  G. Pugliese,et al.  Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms , 2002, Infection Control & Hospital Epidemiology.

[15]  H. C. van der Mei,et al.  Physico-Chemical Interactions in Initial Microbial Adhesion and Relevance for Biofilm Formation , 1997, Advances in dental research.

[16]  M. Otto,et al.  Staphylococcal Biofilms , 2018, Microbiology spectrum.

[17]  Y. Zimmels,et al.  Removal of microbial biofilm on Water Hyacinth plants roots by ultrasonic treatment. , 2009, Ultrasonics.

[18]  Yukio Tomita,et al.  Transfection effect of microbubbles on cells in superposed ultrasound waves and behavior of cavitation bubble. , 2006, Ultrasound in medicine & biology.

[19]  Michael T. Wilson,et al.  Actinobacillus actinomycetemcomitans. , 2002, Journal of medical microbiology.

[20]  I. Sutherland Biofilm exopolysaccharides: a strong and sticky framework. , 2001, Microbiology.

[21]  J. Weiss,et al.  Inactivation of Escherichia coli O157:H7 by high-intensity ultrasonication in the presence of salts. , 2004, Foodborne pathogens and disease.

[22]  G. Orrù,et al.  In Vitro Evaluation of Enterococcus faecalis Adhesion on Various Endodontic Medicaments , 2009, The open dentistry journal.

[23]  P. Plésiat,et al.  Mechanisms of beta-lactam resistance in Pseudomonas aeruginosa: prevalence of OprM-overproducing strains in a French multicentre study (1997). , 2002, The Journal of antimicrobial chemotherapy.

[24]  W D O'Brien,et al.  Quantitative assessment of the germicidal efficacy of ultrasonic energy , 1991, Applied and environmental microbiology.

[25]  M. Kendall Statistical Methods for Research Workers , 1937, Nature.

[26]  J. M. Dow,et al.  Diffusible signals and interspecies communication in bacteria. , 2008, Microbiology.

[27]  E. Mohareb,et al.  Inactivation of microbes using ultrasound: a review. , 2003, International journal of food microbiology.

[28]  D. Dalecki,et al.  Ultrasonic excitation of a bubble near a rigid or deformable sphere: implications for ultrasonically induced hemolysis. , 2005, The Journal of the Acoustical Society of America.

[29]  K. Kogure,et al.  Bacterial motility: links to the environment and a driving force for microbial physics. , 2006, FEMS microbiology ecology.

[30]  P. Stewart,et al.  Analysis of biocide transport limitation in an artificial biofilm system , 1998, Journal of applied microbiology.

[31]  V. Robertson,et al.  A review of therapeutic ultrasound: effectiveness studies. , 2001, Physical therapy.

[32]  W R Laird,et al.  Dental plaque removal by cavitational activity during ultrasonic scaling. , 1988, Journal of clinical periodontology.

[33]  R. Genco,et al.  Position paper: sonic and ultrasonic scalers in periodontics. Research, Science and Therapy Committee of the American Academy of Periodontology. , 2000, Journal of periodontology.

[34]  A. Singer,et al.  The Effects of Low-Frequency Ultrasound on Staphylococcus epidermidis , 1999, Current Microbiology.

[35]  Katherine O'Riordan,et al.  Staphylococcus aureus Capsular Polysaccharides , 2004, Clinical Microbiology Reviews.

[36]  G. Greenstein Nonsurgical periodontal therapy in 2000: a literature review. , 2000, Journal of the American Dental Association.

[37]  W. Pitt,et al.  Ultrasound Increases the Rate of Bacterial Cell Growth , 2003, Biotechnology progress.

[38]  B. Finlay,et al.  Quorum sensing in bacterial virulence. , 2010, Microbiology.

[39]  P. Lambert,et al.  Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. , 2002, Journal of the Royal Society of Medicine.

[40]  T. Bigelow,et al.  Ultrasound histotripsy and the destruction of Escherichia coli biofilms , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[41]  J. Costerton,et al.  Eradication of biofilm cells of Staphylococcus aureus with tobramycin and cephalexin. , 1992, Canadian journal of microbiology.

[42]  J. Lopez-Ribot,et al.  Candida Biofilms: an Update , 2005, Eukaryotic Cell.

[43]  W. Pitt,et al.  Reducing bacterial resistance to antibiotics with ultrasound , 1999, Letters in applied microbiology.

[44]  Jean Kovalevsky,et al.  The development of modern metrology and its role today , 2005, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[45]  Y. Izumi,et al.  Current concepts and advances in manual and power-driven instrumentation. , 2004, Periodontology 2000.

[46]  H. Busscher,et al.  Effect of pulsed ultrasound in combination with gentamicin on bacterial viability in biofilms on bone cements in vivo , 2005, Journal of applied microbiology.

[47]  Gianfranco Genta Methods for Uncertainty Evaluation in Measurement , 2010 .

[48]  Ashlee M Earl,et al.  Ecology and genomics of Bacillus subtilis. , 2008, Trends in microbiology.

[49]  L. Blum,et al.  The development of an ultrasonic apparatus for the non‐invasive and repeatable removal of fouling in food processing equipment , 2000, Letters in applied microbiology.

[50]  G. B. Schaalje,et al.  Ultrasonic Enhancement of Antibiotic Action on Escherichia coli Biofilms: an In Vivo Model , 1999, Antimicrobial Agents and Chemotherapy.

[51]  J. Vila,et al.  Quorum-sensing regulator sdiA and marA overexpression is involved in in vitro-selected multidrug resistance of Escherichia coli. , 2010, The Journal of antimicrobial chemotherapy.

[52]  T J Mason,et al.  The development and evaluation of ultrasound in the biocidal treatment of water. , 1997, Ultrasonics sonochemistry.

[53]  R. Donlan,et al.  Biofilms: Microbial Life on Surfaces , 2002, Emerging infectious diseases.

[54]  William G. Pitt,et al.  The effect of frequency and power density on the ultrasonically-enhanced killing of biofilm-sequestered Escherichia coli , 2000 .

[55]  H. Ceri,et al.  Biofilm bacteria: formation and comparative susceptibility to antibiotics. , 2002, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[56]  P Stoodley,et al.  Effect of low-intensity ultrasound upon biofilm structure from confocal scanning laser microscopy observation. , 1996, Biomaterials.

[57]  Carsten Struve,et al.  Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation , 2010, BMC Microbiology.

[58]  J W Costerton,et al.  How bacteria stick. , 1978, Scientific American.

[59]  M. Tomich,et al.  Genetic Analysis of the Requirement for flp-2, tadV, and rcpB in Actinobacillus actinomycetemcomitans Biofilm Formation , 2006, Journal of bacteriology.

[60]  J. Seymour,et al.  Biopolymer and water dynamics in microbial biofilm extracellular polymeric substance. , 2008, Biomacromolecules.

[61]  L. Baddour,et al.  Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices , 1985, Journal of clinical microbiology.

[62]  W. Pitt,et al.  Ultrasonic enhancement of antibiotic action on several species of bacteria. , 1998, The Journal of general and applied microbiology.

[63]  T. Tolker-Nielsen,et al.  Quorum Sensing and Virulence of Pseudomonas aeruginosa during Lung Infection of Cystic Fibrosis Patients , 2010, PloS one.

[64]  J. Ghigo,et al.  Escherichia coli biofilms. , 2008, Current topics in microbiology and immunology.

[65]  D. de Beer,et al.  Liquid flow in heterogeneous biofilms , 1994, Biotechnology and bioengineering.

[66]  A. Walmsley,et al.  Ultrasonic dental scaler: associated hazards. , 2003, Journal of clinical periodontology.

[67]  Jun-Hyuk Choi,et al.  Development of Metrology for Modern Biology , 2012 .

[68]  R. Robison,et al.  Low-frequency ultrasound increases outer membrane permeability of Pseudomonas aeruginosa. , 2006, The Journal of general and applied microbiology.

[69]  T J Mason,et al.  The effect of sonication on microbial disinfection using hypochlorite. , 2004, Ultrasonics sonochemistry.

[70]  K. Jarrell,et al.  Prokaryotic motility structures. , 2003, Microbiology.

[71]  M. Hufnagel,et al.  A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. , 2004, The Journal of infectious diseases.

[72]  T. Wood,et al.  Motility influences biofilm architecture in Escherichia coli , 2006, Applied Microbiology and Biotechnology.

[73]  D. Sakellari,et al.  Hand instrumentation versus ultrasonic debridement in the treatment of chronic periodontitis: a randomized clinical and microbiological trial. , 2009, Journal of clinical periodontology.

[74]  J. Chapman,et al.  Bacteriostatic effect of sequential hydrodynamic and ultrasound‐induced stress , 2013, Journal of applied microbiology.

[75]  T. Bigelow,et al.  The destruction of Escherichia coli biofilms using high-intensity focused ultrasound. , 2009, Ultrasound in medicine & biology.

[76]  David B. Huang,et al.  Biofilm formation by enterococci. , 2007, Journal of medical microbiology.

[77]  H. Vlamakis,et al.  Biofilm development with an emphasis on Bacillus subtilis. , 2008, Current topics in microbiology and immunology.

[78]  C. Pameijer,et al.  Ultrasonics in endodontics: a review of the literature. , 2007, Journal of endodontics.

[79]  G. Orrù,et al.  Evaluation of Antimicrobial-Antibiofilm Activity of a Hydrogen Peroxide Decontaminating System Used in Dental Unit Water Lines , 2010, The open dentistry journal.

[80]  F. Scannapieco,et al.  Transcriptional and Translational Analysis of Biofilm Determinants of Aggregatibacter actinomycetemcomitans in Response to Environmental Perturbation , 2009, Infection and Immunity.

[81]  Thomas Bjarnsholt,et al.  Antibiotic resistance of bacterial biofilms. , 2010, International journal of antimicrobial agents.

[82]  A. Loomis XXXVIII. The physical and biological effects of high-frequency sound-waves of great intensity , 1927 .

[83]  M. Wilson,et al.  The bactericidal effects of dental ultrasound on Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. An in vitro investigation. , 1997, Journal of clinical periodontology.

[84]  O. Karatuna,et al.  Analysis of quorum sensing-dependent virulence factor production and its relationship with antimicrobial susceptibility in Pseudomonas aeruginosa respiratory isolates. , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[85]  S. Terzakis,et al.  Ultrasound-induced inactivation of gram-negative and gram-positive bacteria in secondary treated municipal wastewater. , 2009, Ultrasonics sonochemistry.

[86]  M. Widerström,et al.  In Vitro Effect of Ultrasound on Bacteria and Suggested Protocol for Sonication and Diagnosis of Prosthetic Infections , 2009, Journal of Clinical Microbiology.

[87]  Francis A. Duck,et al.  A Review of Therapeutic Ultrasound: Biophysical Effects , 2010 .

[88]  R. Darouiche,et al.  Candida Infections of Medical Devices , 2004, Clinical Microbiology Reviews.

[89]  Roberto Kolter,et al.  Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis , 1998, Molecular microbiology.

[90]  S. Molin,et al.  Spatial Organization of Microbial Biofilm Communities , 2000, Microbial Ecology.

[91]  N. Sforza,et al.  Hand and ultrasonic instrumentation in combination with root-coverage surgery: a comparative controlled randomized clinical trial. , 2009, Journal of periodontology.

[92]  T J Mason,et al.  The development and evaluation of ultrasound for the treatment of bacterial suspensions. A study of frequency, power and sonication time on cultured Bacillus species. , 2003, Ultrasonics sonochemistry.

[93]  E. Carr Everbach,et al.  Bacterial Stress Responses to 1-Megahertz Pulsed Ultrasound in the Presence of Microbubbles , 1998, Applied and Environmental Microbiology.

[94]  K. Krogfelt,et al.  Quorum-sensing-regulated virulence factors in Pseudomonas aeruginosa are toxic to Lucilia sericata maggots , 2010, Microbiology.

[95]  G. B. Schaalje,et al.  Ultrasonically Enhanced Vancomycin Activity Against Staphylococcus Epidermidis Biofilms in Vivo , 2004, Journal of biomaterials applications.

[96]  P. Bishop,et al.  Persistence of Klebsiella pneumoniae on simulated biofilm in a model drinking water system. , 2006, Environmental science & technology.

[97]  M. Fletcher The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene , 1977 .

[98]  T. Romeo,et al.  Biofilm Formation and Dispersal under the Influence of the Global Regulator CsrA of Escherichia coli , 2002, Journal of bacteriology.

[99]  Gail ter Haar Therapeutic ultrasound—An historical overview , 1999 .

[100]  G. B. Schaalje,et al.  Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. , 2005, American journal of infection control.