Flexible Platform for In Situ Impedimetric Detection and Bioelectric Effect Treatment of Escherichia Coli Biofilms

Goal: This paper reports a platform for real-time monitoring and treatment of biofilm formation on three-dimensional biomedical device surfaces. Methods: We utilize a flexible platform consisting of gold interdigitated electrodes patterned on a polyimide substrate. The device was integrated onto the interior of a urinary catheter and characterization was performed in a custom-developed flow system. Biofilm growth was monitored via impedance change at 100 Hz ac with a 50 mV signal amplitude. Results: A 30% impedance decrease over 24 h corresponded to Escherichia coli biofilm formation. The platform also enabled removal of the biofilm through the bioelectric effect; a low concentration of antibiotic combined with the applied ac voltage signal led to a synergistic reduction in biofilm resulting in a 12% increase in impedance. Biomass characterization via crystal violet staining confirmed that the impedance detection results correlate with changes in the amount of biofilm biomass on the sensor. We also demonstrated integration with a chip-based impedance converter to enable miniaturization and allow in situ wireless implementation. A 5% impedance decrease measured with the impedance converter corresponded to biofilm growth, replicating the trend measured with the potentiostat. Conclusion: This platform represents a promising solution for biofilm infection management in diverse vulnerable environments. Significance: Biofilms are the dominant mode of growth for microorganisms, where bacterial cells colonize hydrated surfaces and lead to recurring infections. Due to the inaccessible nature of the environments where biofilms grow and their increased tolerance of antimicrobials, identification, and removal on medical devices poses a challenge.

[1]  Savita Khanna,et al.  Electric Field Based Dressing Disrupts Mixed-Species Bacterial Biofilm Infection and Restores Functional Wound Healing , 2017, Annals of surgery.

[2]  W. Bentley,et al.  An Integrated Microsystem for Real-Time Detection and Threshold-Activated Treatment of Bacterial Biofilms. , 2017, ACS applied materials & interfaces.

[3]  J. Aizenberg,et al.  An immobilized liquid interface prevents device associated bacterial infection in vivo. , 2017, Biomaterials.

[4]  W. Bentley,et al.  Autoinducer-2 analogs and electric fields - an antibiotic-free bacterial biofilm combination treatment , 2016, Biomedical microdevices.

[5]  S. Rice,et al.  Biofilms: an emergent form of bacterial life , 2016, Nature Reviews Microbiology.

[6]  U. Cvelbar,et al.  Atmospheric pressure plasma deposition of antimicrobial coatings on non-woven textiles , 2016 .

[7]  Melissa M. Reynolds,et al.  Plasma-modified nitric oxide-releasing polymer films exhibit time-delayed 8-log reduction in growth of bacteria. , 2016, Biointerphases.

[8]  Andrew Berkovich,et al.  A surface acoustic wave biofilm sensor integrated with a treatment method based on the bioelectric effect , 2016 .

[9]  H. Beyenal,et al.  Electrochemical biofilm control: a review , 2015, Biofouling.

[10]  D. Call,et al.  Electrochemical scaffold generates localized, low concentration of hydrogen peroxide that inhibits bacterial pathogens and biofilms , 2015, Scientific Reports.

[11]  W. Bentley,et al.  Effect of electrical energy on the efficacy of biofilm treatment using the bioelectric effect , 2015, npj Biofilms and Microbiomes.

[12]  Savita Khanna,et al.  Silver-Zinc Redox-Coupled Electroceutical Wound Dressing Disrupts Bacterial Biofilm , 2015, PloS one.

[13]  Joanna Aizenberg,et al.  Liquid-Infused Silicone As a Biofouling-Free Medical Material. , 2015, ACS biomaterials science & engineering.

[14]  S. Arana,et al.  Label-free interdigitated microelectrode based biosensors for bacterial biofilm growth monitoring using Petri dishes. , 2014, Journal of microbiological methods.

[15]  R. Lynfield,et al.  Multistate point-prevalence survey of health care-associated infections. , 2014, The New England journal of medicine.

[16]  F. Arizti,et al.  Interdigitated microelectrode biosensor for bacterial biofilm growth monitoring by impedance spectroscopy technique in 96-well microtiter plates , 2013 .

[17]  Reza Ghodssi,et al.  AI-2 analogs and antibiotics: a synergistic approach to reduce bacterial biofilms , 2012, Applied Microbiology and Biotechnology.

[18]  S Arana,et al.  Real time monitoring of the impedance characteristics of Staphylococcal bacterial biofilm cultures with a modified CDC reactor system. , 2012, Biosensors & bioelectronics.

[19]  Teodor Gotszalk,et al.  Evaluation of Pseudomonas aeruginosa biofilm formation using piezoelectric tuning fork mass sensors , 2012 .

[20]  W. Bentley,et al.  MICROFLUIDIC BIOFILM OBSERVATION, ANALYSIS AND TREATMENT (MICRO-BOAT) PLATFORM , 2012 .

[21]  Hsuan-Chen Wu,et al.  An ALD aluminum oxide passivated Surface Acoustic Wave sensor for early biofilm detection , 2012 .

[22]  W. Bentley,et al.  Development and validation of a microfluidic reactor for biofilm monitoring via optical methods , 2011 .

[23]  W. Bentley,et al.  Synthetic analogs tailor native AI-2 signaling across bacterial species. , 2010, Journal of the American Chemical Society.

[24]  Rashid Bashir,et al.  Electrical/electrochemical impedance for rapid detection of foodborne pathogenic bacteria. , 2008, Biotechnology advances.

[25]  H. Nelis,et al.  Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. , 2008, Journal of microbiological methods.

[26]  J. Mas,et al.  On-chip impedance measurements to monitor biofilm formation in the drinking water distribution network , 2006 .

[27]  A. Camper,et al.  Assessment of the Ability of the Bioelectric Effect To Eliminate Mixed-Species Biofilms , 2005, Applied and Environmental Microbiology.

[28]  Klaus Winzer,et al.  Making 'sense' of metabolism: autoinducer-2, LUXS and pathogenic bacteria , 2005, Nature Reviews Microbiology.

[29]  R. Darouiche,et al.  Treatment of infections associated with surgical implants. , 2004, The New England journal of medicine.

[30]  S. J. Kim,et al.  Biocompatibility of polyimide microelectrode array for retinal stimulation , 2004 .

[31]  K G Ong,et al.  Monitoring of bacteria growth using a wireless, remote query resonant-circuit sensor: application to environmental sensing. , 2001, Biosensors & bioelectronics.

[32]  G. Reid,et al.  Microbial Biofilms: Their Development and Significance for Medical Device—Related Infections , 1999, Journal of clinical pharmacology.

[33]  R J Palmer,et al.  Modern microscopy in biofilm research: confocal microscopy and other approaches. , 1999, Current opinion in biotechnology.

[34]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[35]  P. Stewart,et al.  Electrolytic Generation of Oxygen Partially Explains Electrical Enhancement of Tobramycin Efficacy againstPseudomonas aeruginosa Biofilm , 1999, Antimicrobial Agents and Chemotherapy.

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

[37]  J. Costerton,et al.  Electrical enhancement of biocide efficacy against Pseudomonas aeruginosa biofilms , 1992, Applied and environmental microbiology.

[38]  J. Costerton,et al.  Testing the susceptibility of bacteria in biofilms to antibacterial agents , 1990, Antimicrobial Agents and Chemotherapy.

[39]  D. Maki,et al.  A semiquantitative culture method for identifying intravenous-catheter-related infection. , 1977, The New England journal of medicine.

[40]  J W Warren,et al.  Catheter-associated urinary tract infections. , 2012, Critical care nurse.