Submicron-Bubble-Enhanced Focused Ultrasound for Blood–Brain Barrier Disruption and Improved CNS Drug Delivery
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Mendeley | Further Information

{"title"=>"Submicron-Bubble-Enhanced Focused Ultrasound for Blood–Brain Barrier Disruption and Improved CNS Drug Delivery", "type"=>"journal", "authors"=>[{"first_name"=>"Ching-Hsiang", "last_name"=>"Fan"}, {"first_name"=>"Hao-Li", "last_name"=>"Liu"}, {"first_name"=>"Chien-Yu", "last_name"=>"Ting"}, {"first_name"=>"Ya-Hsuan", "last_name"=>"Lee"}, {"first_name"=>"Chih-Ying", "last_name"=>"Huang"}, {"first_name"=>"Yan-Jung", "last_name"=>"Ma"}, {"first_name"=>"Kuo-Chen", "last_name"=>"Wei"}, {"first_name"=>"Tzu-Chen", "last_name"=>"Yen"}, {"first_name"=>"Chih-Kuang", "last_name"=>"Yeh"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24788566", "doi"=>"10.1371/journal.pone.0096327", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"1932-6203"}, "id"=>"2e16fba0-d3b4-3146-a1a9-f622853eb6b5", "abstract"=>"The use of focused ultrasound (FUS) with microbubbles has been proven to induce transient blood-brain barrier opening (BBB-opening). However, FUS-induced inertial cavitation of microbubbles can also result in erythrocyte extravasations. Here we investigated whether induction of submicron bubbles to oscillate at their resonant frequency would reduce inertial cavitation during BBB-opening and thereby eliminate erythrocyte extravasations in a rat brain model. FUS was delivered with acoustic pressures of 0.1-4.5 MPa using either in-house manufactured submicron bubbles or standard SonoVue microbubbles. Wideband and subharmonic emissions from bubbles were used to quantify inertial and stable cavitation, respectively. Erythrocyte extravasations were evaluated by in vivo post-treatment magnetic resonance susceptibility-weighted imaging, and finally by histological confirmation. We found that excitation of submicron bubbles with resonant frequency-matched FUS (10 MHz) can greatly limit inertial cavitation while enhancing stable cavitation. The BBB-opening was mainly caused by stable cavitation, whereas the erythrocyte extravasation was closely correlated with inertial cavitation. Our technique allows extensive reduction of inertial cavitation to induce safe BBB-opening. Furthermore, the safety issue of BBB-opening was not compromised by prolonging FUS exposure time, and the local drug concentrations in the brain tissues were significantly improved to 60 times (BCNU; 18.6 µg versus 0.3 µg) by using chemotherapeutic agent-loaded submicron bubbles with FUS. This study provides important information towards the goal of successfully translating FUS brain drug delivery into clinical use.", "link"=>"http://www.mendeley.com/research/submicronbubbleenhanced-focused-ultrasound-bloodbrain-barrier-disruption-improved-cns-drug-delivery-3", "reader_count"=>37, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>5}, "reader_count_by_subject_area"=>{"Engineering"=>9, "Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>3, "Nursing and Health Professions"=>1, "Medicine and Dentistry"=>5, "Agricultural and Biological Sciences"=>5, "Neuroscience"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>2, "Chemistry"=>3, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>9}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>3}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "China"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1482818"], "description"=>"<p>Group 1  =  in-house submicron bubbles with 10-MHz FUS sonication; Group 2  =  SonoVue with 10-MHz FUS sonication; Group 3  =  in-house submicron bubbles with 1-MHz FUS sonication; Group 4  =  SonoVue with 1-MHz FUS sonication.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models"], "article_id"=>1014494, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.t001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sonication_parameters_of_the_four_experimental_groups_/1014494", "title"=>"Sonication parameters of the four experimental groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482796"], "description"=>"<p>A: Size distributions of in-house submicron bubbles and commercial SonoVue bubbles. Left diagram was measured by DLS and right one was determined by Coulter counter, which could provide both size distribution and concentration information. B: Experimental setup. C: Timeline of the <i>in vivo</i> experiment.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "settings"], "article_id"=>1014476, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g001", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_settings_and_procedures_/1014476", "title"=>"Experimental settings and procedures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482814"], "description"=>"<p>Grade 0 indicates no detectable damage, whereas grade 1 denotes erythrocyte extravasations that are considered to be safe. Grades 2 or 3 show hemorrhage regarded as severe. <sup>Δ</sup>Detected cell apoptosis as assessed by the TUNEL assay.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "hemorrhage", "sonication", "acoustic"], "article_id"=>1014490, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Occurrence_of_brain_hemorrhage_according_to_sonication_at_different_acoustic_pressures_/1014490", "title"=>"Occurrence of brain hemorrhage according to sonication at different acoustic pressures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482805"], "description"=>"<p>A: In-house submicron bubbles with 10-MHz FUS sonication. B: SonoVue with 10-MHz FUS sonication. C: In-house submicron bubbles with 1-MHz FUS sonication. D: SonoVue with 1-MHz FUS sonication. (white arrows: the BBB-opening region; red arrows: areas of erythrocyte extravasations; blue arrows: brain edema).</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "fus"], "article_id"=>1014485, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g005", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MRI_results_after_FUS_sonication_/1014485", "title"=>"MRI results after FUS sonication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482800"], "description"=>"<p>A: EB extravasation into brain tissue. (white arrows: the BBB-opening region; red arrows: areas of erythrocyte extravasations). B: Acoustic-emission change ratio (red line: in-house submicron bubbles with 10-MHz FUS sonication; blue line: SonoVue with 10-MHz FUS sonication; solid line: subharmonic-frequency signal; dotted line: ICD. C: Correlation between acoustic-emission signals and amount of EB extravasation for in-house submicron bubbles with 10-MHz FUS sonication.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "bbb-opening", "acoustic-emission", "signals", "10-mhz"], "article_id"=>1014480, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relations_between_levels_of_BBB_opening_and_acoustic_emission_signals_under_10_MHz_sonication_/1014480", "title"=>"Relations between levels of BBB-opening and acoustic-emission signals under 10-MHz sonication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482817"], "description"=>"<p>Summary of 10-MHz FUS with BCNU-bubbles for enhanced BCNU delivery.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "10-mhz", "fus", "bcnu-bubbles", "enhanced", "bcnu"], "article_id"=>1014493, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.t002", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_10_MHz_FUS_with_BCNU_bubbles_for_enhanced_BCNU_delivery_/1014493", "title"=>"Summary of 10-MHz FUS with BCNU-bubbles for enhanced BCNU delivery.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482798"], "description"=>"<p>A: Frequency spectra acquired from PCD during 10-MHz FUS sonication with (red) or without (blue) in-house submicron bubbles. Top: 0.5 MPa, only the fundamental frequency (10 MHz). Middle: 1.5 MPa, the additional peak appeared at about subharmonic frequency (5 MHz). Bottom: 4.5 MPa, the spectrum was accompanied by wideband acoustic emission, indicated by a bump at approximately 2.2–6.8 MHz. B: Frequency spectra acquired from PCD during 1-MHz FUS sonication with (red) or without (blue) SonoVue. Top: 0.5 MPa. With injecting bubbles, both the fundamental frequency (1 MHz) and subharmonic signal (0.5 MHz) could be measured. Bottom: 1.5 MPa, with injecting bubbles, the frequency spectrum was accompanied by wideband acoustic emission, indicated by a bump at approximately 0.5–8 MHz.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models"], "article_id"=>1014478, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acoustic_emission_signal_spectra_/1014478", "title"=>"Acoustic-emission signal spectra.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482816"], "description"=>"<p>A: Quantitative evaluation of BCNU release into brain tissue associated with transcranial FUS-triggered destruction of BCNU-bubbles (Single asterisk, <i>P</i><0.05). The corresponding brain sections: B: 2.5 MPa; 1 site; 1 min/site, and C: 4.5 MPa; 1 site; 4 min/site. The treated hemisphere brain was the left brain.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "transcranial", "fus", "enhancing", "encapsulated"], "article_id"=>1014492, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Repetitive_and_transcranial_FUS_treatment_for_enhancing_delivery_of_encapsulated_drugs_/1014492", "title"=>"Repetitive and transcranial FUS treatment for enhancing delivery of encapsulated drugs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482813"], "description"=>"<p>A: H&E-stained and B: TUNEL-stained sections after application of in-house submicron bubbles with 10-MHz FUS sonication. The dotted rectangles indicate the BBB-opening region confirmed by EB extravasation. Positive control: hemorrhage and apoptotic cells (group 4, 1.5 MPa). Scale bars: 1 mm, 1 mm, and 50 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "evaluations"], "article_id"=>1014489, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histological_evaluations_after_BBB_opening_/1014489", "title"=>"Histological evaluations after BBB-opening.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482802"], "description"=>"<p>A: EB extravasation into brain tissue. (white arrows: the BBB-opening region; red arrows: areas of erythrocyte extravasations). B: Acoustic-emission change ratio (red line: in-house submicron bubbles with 1-MHz FUS sonication; blue line: SonoVue with 1-MHz FUS sonication; solid line: subharmonic-frequency signal; dotted line: ICD.</p>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "bbb-opening", "acoustic-emission", "signals", "1-mhz"], "article_id"=>1014482, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327.g004", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relations_between_levels_of_BBB_opening_and_acoustic_emission_signals_under_1_MHz_sonication_/1014482", "title"=>"Relations between levels of BBB-opening and acoustic-emission signals under 1-MHz sonication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-02 02:53:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/1482819"], "description"=>"<div><p>The use of focused ultrasound (FUS) with microbubbles has been proven to induce transient blood–brain barrier opening (BBB-opening). However, FUS-induced inertial cavitation of microbubbles can also result in erythrocyte extravasations. Here we investigated whether induction of submicron bubbles to oscillate at their resonant frequency would reduce inertial cavitation during BBB-opening and thereby eliminate erythrocyte extravasations in a rat brain model. FUS was delivered with acoustic pressures of 0.1–4.5 MPa using either in-house manufactured submicron bubbles or standard SonoVue microbubbles. Wideband and subharmonic emissions from bubbles were used to quantify inertial and stable cavitation, respectively. Erythrocyte extravasations were evaluated by <i>in vivo</i> post-treatment magnetic resonance susceptibility-weighted imaging, and finally by histological confirmation. We found that excitation of submicron bubbles with resonant frequency-matched FUS (10 MHz) can greatly limit inertial cavitation while enhancing stable cavitation. The BBB-opening was mainly caused by stable cavitation, whereas the erythrocyte extravasation was closely correlated with inertial cavitation. Our technique allows extensive reduction of inertial cavitation to induce safe BBB-opening. Furthermore, the safety issue of BBB-opening was not compromised by prolonging FUS exposure time, and the local drug concentrations in the brain tissues were significantly improved to 60 times (BCNU; 18.6 µg versus 0.3 µg) by using chemotherapeutic agent-loaded submicron bubbles with FUS. This study provides important information towards the goal of successfully translating FUS brain drug delivery into clinical use.</p></div>", "links"=>[], "tags"=>["anatomy", "histology", "nervous system", "biotechnology", "Bioengineering", "Biomedical Engineering", "organisms", "animals", "vertebrates", "mammals", "rodents", "rats", "Clinical medicine", "Diagnostic medicine", "Diagnostic radiology", "Magnetic resonance imaging", "pharmacology", "pharmacokinetics", "Drug distribution", "Radiology and imaging", "Model organisms", "Animal models", "focused", "ultrasound", "disruption", "cns"], "article_id"=>1014495, "categories"=>["Biological Sciences"], "users"=>["Ching-Hsiang Fan", "Hao-Li Liu", "Chien-Yu Ting", "Ya-Hsuan Lee", "Chih-Ying Huang", "Yan-Jung Ma", "Kuo-Chen Wei", "Tzu-Chen Yen", "Chih-Kuang Yeh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096327", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Submicron_Bubble_Enhanced_Focused_Ultrasound_for_Blood_8211_Brain_Barrier_Disruption_and_Improved_CNS_Drug_Delivery_/1014495", "title"=>"Submicron-Bubble-Enhanced Focused Ultrasound for Blood–Brain Barrier Disruption and Improved CNS Drug Delivery", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-02 02:53:02"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Medicine and health sciences", "average_usage"=>[285]}, {"subject_area"=>"/Medicine and health sciences/Pharmaceutics", "average_usage"=>[299, 467]}, {"subject_area"=>"/Physical sciences/Physics", "average_usage"=>[266]}]}
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