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Multi-Channel Microfluidic Biosensor Platform Applied for Online Monitoring and Screening of Biofilm Formation and Activity

Publication Date: February 23, 2015
Journal: PLOS ONE
Authors: Julia Bruchmann, Kai Sachsenheimer, Bastian E. Rapp & Thomas Schwartz
Volume: 10
Issue: 2
Pages: e0117300
DOI: https://dx.plos.org/10.1371/journal.pone.0117300
Publisher URL: http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0117300
PubMed: http://www.ncbi.nlm.nih.gov/pubmed/25706987
PubMed Central: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4338023
Europe PMC: http://europepmc.org/abstract/MED/25706987
Web of Science: 000350662100074
Scopus: 84923816751
Mendeley: http://www.mendeley.com/research/multichannel-microfluidic-biosensor-platform-applied-online-monitoring-screening-biofilm-formation-a

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CiteULike03 May 03:19 UTC

CiteULike

Mendeley 4525 Apr 13:19 UTC

Mendeley | Further Information

{"title"=>"Multi-channel microfluidic biosensor platform applied for online monitoring and screening of biofilm formation and activity", "type"=>"journal", "authors"=>[{"first_name"=>"Julia", "last_name"=>"Bruchmann", "scopus_author_id"=>"55579508400"}, {"first_name"=>"Kai", "last_name"=>"Sachsenheimer", "scopus_author_id"=>"55654078000"}, {"first_name"=>"Bastian E.", "last_name"=>"Rapp", "scopus_author_id"=>"15770227400"}, {"first_name"=>"Thomas", "last_name"=>"Schwartz", "scopus_author_id"=>"35249228600"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"602523583", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0117300", "scopus"=>"2-s2.0-84923816751", "pmid"=>"25706987", "sgr"=>"84923816751"}, "id"=>"325f6559-6172-3be6-9b87-8c6232ee3ab8", "abstract"=>"Bacterial colonization of surfaces and interfaces has a major impact on various areas including biotechnology, medicine, food industries, and water technologies. In most of these areas biofilm development has a strong impact on hygiene situations, product quality, and process efficacies. In consequence, biofilm manipulation and prevention is a fundamental issue to avoid adverse impacts. For such scenario online, non-destructive biofilm monitoring systems become important in many technical and industrial applications. This study reports such a system in form of a microfluidic sensor platform based on the combination of electrical impedance spectroscopy and amperometric current measurement, which allows sensitive online measurement of biofilm formation and activity. A total number of 12 parallel fluidic channels enable real-time online screening of various biofilms formed by different Pseudomonas aeruginosa and Stenotrophomonas maltophilia strains and complex mixed population biofilms. Experiments using disinfectant and antibiofilm reagents demonstrate that the biofilm sensor is able to discriminate between inactivation/killing of bacteria and destabilization of biofilm structures. The impedance and amperometric sensor data demonstrated the high dynamics of biofilms as a consequence of distinct responses to chemical treatment strategies. Gene expression of flagellar and fimbrial genes of biofilms grown inside the microfluidic system supported the detected biofilm growth kinetics. Thus, the presented biosensor platform is a qualified tool for assessing biofilm formation in specific environments and for evaluating the effectiveness of antibiofilm treatment strategies.", "link"=>"http://www.mendeley.com/research/multichannel-microfluidic-biosensor-platform-applied-online-monitoring-screening-biofilm-formation-a", "reader_count"=>41, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>11, "Unspecified"=>4, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Materials Science"=>2, "Agricultural and Biological Sciences"=>14, "Chemical Engineering"=>2, "Physics and Astronomy"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>11}, "Materials Science"=>{"Materials Science"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>2}}, "reader_count_by_country"=>{"United States"=>2, "France"=>1}, "group_count"=>4}

ORCID28 Apr 19:15 UTC

Scopus | Further Information

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Web of Science®09 Feb 10:36 UTC

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Journal Comments25 Oct 16:08 UTC

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Figshare 15328 Apr 11:09 UTC

Figshare

{"files"=>["https://ndownloader.figshare.com/files/1920509"], "description"=>"The sensor system consists of a 12-flow channel module connectable to a custom-made electronics. The measurement electronics is designed with four ports for expandable connection of further 12-flow channel units (A). A 12-flow channel unit consists of an amperometric counter electrode and the fluidically independent microfluidic flow channels sealed by a substrate with planar gold-electrode structures (B). Different electrode designs were used depending on the application including circular electrodes with a gap of 500 μm and interdigitated electrodes with gaps of 15–100 μm (C).", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315172, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensor_system_/1315172", "title"=>"Sensor system.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920510"], "description"=>"The system operates in differential measurement mode using reference channels (bacteria-free) and measurement channels (probed with bacteria). The evaluated sensor signals are differential signals formed between two electrodes from either category. This differential measurement allows reducing sensor drift due to ambient influences (temperature, etc.). The schematic depicts one electrode in a reference channel (bacteria free) and an electrode in a measurement channel (with bacteria). Each channel has a total of two electrodes (each consisting of a measurement electrode and a counter electrode) for electrochemical impedance spectroscopy (EIS). Each microfluidic channel is additionally equipped with two amperometric electrodes, which consist of a chamber filled with electrolyte solution that is fluidically separated from the microfluidic channel by a proton exchange membrane (PEM). A carbon rod is inserted in this chamber and serves as the cathode, the EIS counter electrodes serve as the anode. The biofilm respiratory activity can be measured directly by measuring the current created during respiratory activity via the electrons collected by the cathode. The EIS electronic module is disconnected in amperometric measure mode and the amperometric electronic module is disconnected in EIS measure mode to avoid interferences.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315173, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g002", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_of_the_measurement_setup_/1315173", "title"=>"Schematic of the measurement setup.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920511"], "description"=>"Intensity of fluorescence images of the stained biofilm on the electrodes at different points in time (0.2 d = directly after seeding phase (S), 1 d, 2 d and 3 d) (B) were compared to the impedance signal (A). P. aeruginosa strain PA 49 in BHI 1:4 medium was used for the experiments. Values indicate means and standard deviations of 8 electrodes.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315174, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g003", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_of_impedance_signal_with_fluorescence_microscopy_/1315174", "title"=>"Correlation of impedance signal with fluorescence microscopy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920512"], "description"=>"Amperometric signal was compared to exoenzymatic activity (esterase activity in the supernatant) of the biofilm. P. aeruginosa was grown for 6 days in BHI 1:4 medium. Samples from the outflow of the microfluidic channels were collected at different points in time and analyzed in duplicates. Seeding phase is indicated (S). Standard deviations given for amperometric current are from 4 different electrodes. r = Pearson correlation coefficient; p = significance", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315175, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g004", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_of_amperometric_signal_with_exoenzymatic_activity_/1315175", "title"=>"Correlation of amperometric signal with exoenzymatic activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920513"], "description"=>"Sensitivity of the sensor system was tested over 4.5 days with inocula of 10, 102 and 104 bacteria/mL of P. aeruginosa strain PA 49 using 15 μm-gap interdigitated electrodes (A) and circular (B). Seeding phase is indicated (S).", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315176, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g005", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensor_sensitivity_/1315176", "title"=>"Sensor sensitivity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920520"], "description"=>"Biofilm destabilization and inactivation can be monitored using the sensor system. (A) Destabilization of a preformed biofilm (2 days old) of P. aeruginosa strain PA 49 which was exposed for 1.5 h to 1% Tergazyme. In comparison to an untreated biofilm a reduction of about 40% of the signal (and in correlation of the biomass) can be observed (left) in parallel also activity decreased (right). (B) Repeated destabilization on preformed biofilm (3 days old) of P. aeruginosa strain PA 14 which was exposed twice to Tergazyme for intervals of 1.5 h each. Iterated reduction in biomass can be observed. (C) Inactivation of a preformed biofilm (3 days old) of P. aeruginosa strain PA 14 which was exposed for 1 h to Sterillium. Signals of biomass (left) and activity (right) were compared between untreated and treated biofilms and are results of (at least) two independent electrodes.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315178, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g006", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensor_application_/1315178", "title"=>"Sensor application.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920521"], "description"=>"Impedance curves of 3 different isolates of P. aeruginosa and S. maltophilia are shown, which are categorized as strong, intermediate and weak biofilm formers according to their increase in biomass (ΔZ). Biofilms were grown for 3 days in BHI 1:4 medium in the sensor system.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315179, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g007", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Exemplary_biofilm_biomass_dynamics_/1315179", "title"=>"Exemplary biofilm biomass dynamics.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920522"], "description"=>"Probing of the biosensor system with outflow of a wastewater treatment plant which was used as inoculum for the system. After inoculation for 3 days the valves were switched to sterilized outflow of the sewage plant as further nutrient source. (A) Biofilm biomass was recorded by impedance and increased after an initiation phase after 6 days. Activity of the biofilm was monitored by changes in the produced amperometric current and stayed constant during the experiment. Seeding phase is not shown because of missing of an appropriate reference channel. (B) Live dead images of the electrodes were acquired after 1 d, 2 d, 3 d and at the end of the experiment.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315180, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g008", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Environmental_biofilm_/1315180", "title"=>"Environmental biofilm.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920523"], "description"=>"Biofilm biomass dynamics of P. aeruginosa strain PA 57 were recorded for 24 h in parallel to gene expression (A). Data results of at least two independent assays performed in duplicates. Flagellar and fimbrial genes flgE, flgD and cupA1 were analyzed for their expression in the planktonic state of P. aeruginosa strain PA 57, and in 1 h, 4 h and 24 h biofilms (B). Individual expressions were normalized to rpoD and scaled to the planktonic state. Replicates result from at least two independent experiments.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315181, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.g009", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_expression_analysis_/1315181", "title"=>"Gene expression analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920524"], "description"=>"* Pearson correlation coefficientPA = P. aeruginosaSM = S. maltophiliaClassification of isolates according to biofilm formation capacity.", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315182, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0117300.t001", "stats"=>{"downloads"=>9, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Classification_of_isolates_according_to_biofilm_formation_capacity_/1315182", "title"=>"Classification of isolates according to biofilm formation capacity.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-02-23 02:58:53"}
{"files"=>["https://ndownloader.figshare.com/files/1920526", "https://ndownloader.figshare.com/files/1920527", "https://ndownloader.figshare.com/files/1920528", "https://ndownloader.figshare.com/files/1920529", "https://ndownloader.figshare.com/files/1920530"], "description"=>"<div>Bacterial colonization of surfaces and interfaces has a major impact on various areas including biotechnology, medicine, food industries, and water technologies. In most of these areas biofilm development has a strong impact on hygiene situations, product quality, and process efficacies. In consequence, biofilm manipulation and prevention is a fundamental issue to avoid adverse impacts. For such scenario online, non-destructive biofilm monitoring systems become important in many technical and industrial applications. This study reports such a system in form of a microfluidic sensor platform based on the combination of electrical impedance spectroscopy and amperometric current measurement, which allows sensitive online measurement of biofilm formation and activity. A total number of 12 parallel fluidic channels enable real-time online screening of various biofilms formed by different Pseudomonas aeruginosa and Stenotrophomonas maltophilia strains and complex mixed population biofilms. Experiments using disinfectant and antibiofilm reagents demonstrate that the biofilm sensor is able to discriminate between inactivation/killing of bacteria and destabilization of biofilm structures. The impedance and amperometric sensor data demonstrated the high dynamics of biofilms as a consequence of distinct responses to chemical treatment strategies. Gene expression of flagellar and fimbrial genes of biofilms grown inside the microfluidic system supported the detected biofilm growth kinetics. Thus, the presented biosensor platform is a qualified tool for assessing biofilm formation in specific environments and for evaluating the effectiveness of antibiofilm treatment strategies.</div>", "links"=>[], "tags"=>["biofilm growth kinetics", "biofilm formation", "areas biofilm development", "Stenotrophomonas maltophilia strains", "microfluidic sensor platform", "amperometric sensor data", "antibiofilm treatment strategies", "chemical treatment strategies"], "article_id"=>1315184, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Julia Bruchmann", "Kai Sachsenheimer", "Bastian E. Rapp", "Thomas Schwartz"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0117300.s001", "https://dx.doi.org/10.1371/journal.pone.0117300.s002", "https://dx.doi.org/10.1371/journal.pone.0117300.s003", "https://dx.doi.org/10.1371/journal.pone.0117300.s004", "https://dx.doi.org/10.1371/journal.pone.0117300.s005"], "stats"=>{"downloads"=>13, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Multi_Channel_Microfluidic_Biosensor_Platform_Applied_for_Online_Monitoring_and_Screening_of_Biofilm_Formation_and_Activity_/1315184", "title"=>"Multi-Channel Microfluidic Biosensor Platform Applied for Online Monitoring and Screening of Biofilm Formation and Activity", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-02-23 02:58:53"}

PMC Usage Stats 110217 Feb 23:01 UTC

PMC Usage Stats | Further Information

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{"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
{"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}

Relative Metric10 May 17:59 UTC

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{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}

F1000Prime03 Mar 12:45 UTC

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