Comparative In Vitro Study on Magnetic Iron Oxide Nanoparticles for MRI Tracking of Adipose Tissue-Derived Progenitor Cells
Publication Date
September 22, 2014
Journal
PLoS ONE
Authors
Annika Kasten, Cordula Grüttner, Jens-Peter Kühn, Rainer Bader, et al
Volume
9
Issue
9
Pages
e108055
DOI
https://dx.plos.org/10.1371/journal.pone.0108055
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0108055
Web of Science
000343679800064
Scopus
84907908975
Mendeley
http://www.mendeley.com/research/comparative-vitro-study-magnetic-iron-oxide-nanoparticles-mri-tracking-adipose-tissuederived-progeni
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Mendeley | Further Information

{"title"=>"Comparative In Vitro Study on Magnetic Iron Oxide Nanoparticles for MRI Tracking of Adipose Tissue-Derived Progenitor Cells", "type"=>"journal", "authors"=>[{"first_name"=>"Annika", "last_name"=>"Kasten"}, {"first_name"=>"Cordula", "last_name"=>"Grüttner"}, {"first_name"=>"Jens-Peter", "last_name"=>"Kühn"}, {"first_name"=>"Rainer", "last_name"=>"Bader"}, {"first_name"=>"Juliane", "last_name"=>"Pasold"}, {"first_name"=>"Bernhard", "last_name"=>"Frerich"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25244560", "doi"=>"10.1371/journal.pone.0108055", "issn"=>"1932-6203"}, "id"=>"5acb0507-6da5-3e05-9d69-98b95f256276", "abstract"=>"Magnetic resonance imaging (MRI) using measurement of the transverse relaxation time (R2*) is to be considered as a promising approach for cell tracking experiments to evaluate the fate of transplanted progenitor cells and develop successful cell therapies for tissue engineering. While the relationship between core composition of nanoparticles and their MRI properties is well studied, little is known about possible effects on progenitor cells. This in vitro study aims at comparing two magnetic iron oxide nanoparticle types, single vs. multi-core nanoparticles, regarding their physico-chemical characteristics, effects on cellular behavior of adipose tissue-derived stem cells (ASC) like differentiation and proliferation as well as their detection and quantification by means of MRI. Quantification of both nanoparticle types revealed a linear correlation between labeling concentration and R2* values. However, according to core composition, different levels of labeling concentrations were needed to achieve comparable R2* values. Cell viability was not altered for all labeling concentrations, whereas the proliferation rate increased with increasing labeling concentrations. Likewise, deposition of lipid droplets as well as matrix calcification revealed to be highly dose-dependent particularly regarding multi-core nanoparticle-labeled cells. Synthesis of cartilage matrix proteins and mRNA expression of collagen type II was also highly dependent on nanoparticle labeling. In general, the differentiation potential was decreased with increasing labeling concentrations. This in vitro study provides the proof of principle for further in vivo tracking experiments of progenitor cells using nanoparticles with different core compositions but also provides striking evidence that combined testing of biological and MRI properties is advisable as improved MRI properties of multi-core nanoparticles may result in altered cell functions.", "link"=>"http://www.mendeley.com/research/comparative-vitro-study-magnetic-iron-oxide-nanoparticles-mri-tracking-adipose-tissuederived-progeni", "reader_count"=>28, "reader_count_by_academic_status"=>{"Researcher"=>8, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>8, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Materials Science"=>2, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>3, "Physics and Astronomy"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Materials Science"=>{"Materials Science"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Republic of Singapore"=>1, "United States"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1685496"], "description"=>"<p>Cells were treated with (A) BNF starch nanoparticles and (B) nanomag-D-spio nanoparticles and cell numbers were determined up to 10 days after labeling. Cell treatment with both nanoparticle types resulted generally in a higher proliferation rate compared to control cells (n = 4; median, error bars represent 25<sup>th</sup> and 75<sup>th</sup> percentiles).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177708, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proliferation_of_nanoparticle_labeled_ASC_/1177708", "title"=>"Proliferation of nanoparticle-labeled ASC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685543"], "description"=>"<p>(A) Unlabeled, (B) BNF starch- and (C, E, F) nanomag-D-spio-labeled cells were chondrogenically stimulated for 21 d. Pellets were analyzed using Heidenhain's AZAN trichrome staining showing a reduced collagen type II-positive extracellular matrix (light blue) due to nanoparticle labeling. BNF-labeled cells (25 and 50 µg Fe/ml) failed to generate compact pellets (not shown) (Axio Imager M2, Carl Zeiss Microscopy GmbH, Jena, Germany; scale bars  = 100 µm). (D) Collagen type II was analyzed using Real-Time quantitative PCR revealing a diminished mRNA expression of collagen type II due to nanoparticle labeling (2∧ΔΔCT ± %CV; n = 2, normalized to β-actin).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177737, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g007", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_labeling_on_chondrogenic_differentiation_of_ASC_/1177737", "title"=>"Effect of labeling on chondrogenic differentiation of ASC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685574"], "description"=>"<p>Confocal laser scanning images of ASC labeled with red fluorescent variants of nanoparticles, BNF starch-redF (25 µg Fe/ml) or nanomag-CLD-redF (50 µg Fe/ml), and stained 24 h after labeling for mitochondria and lysosomes (LAMP-1) (both shown in green). Cell's nuclei were counterstained with Hoechst 33342 (blue). No co-localization between nanoparticles and mitochondria or nuclei was found. Both nanoparticle types appear to be associated with lysosomes 24 hours after labeling. In each case, overlay images are shown (LSM 780, Carl Zeiss Microscopy GmbH, Jena, Germany; scale bars  = 2 µm).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177768, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g008", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intracellular_localization_of_nanoparticles_/1177768", "title"=>"Intracellular localization of nanoparticles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685487"], "description"=>"<p>After treatment of ASC with BNF starch nanoparticles (10/25/50 µg Fe/ml) and nanomag-D-spio nanoparticles, a viability/cytotoxicity assay was performed up to 14 days following labeling. Viable cells and nuclei of apoptotic cells were stained with calcein AM (green) and ethidium homodimer (red), respectively. Cells were counterstained with Hoechst 33342 (blue). No cytotoxic effects were detected due to nanoparticle labeling (Axio Observer, Carl Zeiss Microscopy GmbH, Jena, Germany; scale bars  = 50 µm).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177699, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g002", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Viability_Cytotoxicity_test_after_nanoparticle_labeling_/1177699", "title"=>"Viability/Cytotoxicity test after nanoparticle labeling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685583"], "description"=>"<p>Uptake of nanoparticles was determined using a ferrozin assay and displayed as number of particles per cell. Shown is the maximal and minimal as well as mean ± SD number of particles per cell.</p>a,b<p>no significant difference between cellular uptake of BNF starch and nanomag-D-spio nanoparticles (Mann-Whitney U-test).</p><p>Nanoparticle uptake of labeled ASC.</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177777, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.t002", "stats"=>{"downloads"=>3, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nanoparticle_uptake_of_labeled_ASC_/1177777", "title"=>"Nanoparticle uptake of labeled ASC.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685581"], "description"=>"<p>R2* maps of cell phantoms are shown in (A). The (B) R2* values of cell phantoms as well as (C) iron load per cell are shown as a function of applied iron concentration for cell labeling. BNF starch and nanomag-D-spio labeled ASC were labeled with 0–50 µg Fe/ml and 0–200 µg Fe/ml, respectively. For cell phantoms, cells were embedded in 1.5% agarose and MRI was performed using a high-field 7.1 Tesla animal MR system (Clin Scan, Bruker Corp., Billerica, MA, USA). Pure agarose without cells served also as control. Iron load per cell was quantified using a ferrozine assay (n = 5, mean ± SD). For both nanoparticle types, the iron load per cell correlated with R2* values as a function of the applied iron concentration for cell labeling.</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177775, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g009", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_between_iron_content_per_cell_and_R2_values_/1177775", "title"=>"Correlation between iron content per cell and R2* values.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685582"], "description"=>"<p>Both nanoparticle types including their redF-labeled and PDL-coated variants were characterized by determination of hydrodynamic diameter, polydispersity index, and zeta potential.</p><p>Physico-chemical characterization of nanoparticles.</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177776, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.t001", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Physico_chemical_characterization_of_nanoparticles_/1177776", "title"=>"Physico-chemical characterization of nanoparticles.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685448"], "description"=>"<p>After incubation of ASC with BNF starch nanoparticles (10/25/50 µg Fe/ml) and nanomag-D-spio nanoparticles (25/50/100 µg Fe/ml), iron oxide of internalized particles was visualized by Prussian Blue staining (Zeiss Axiovert 40 CFL, Carl Zeiss Microscopy GmbH, Jena, Germany; scale bars  = 50 µm).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177669, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nanoparticle_internalization_verified_by_Prussian_Blue_staining_/1177669", "title"=>"Nanoparticle internalization verified by Prussian Blue staining.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685505"], "description"=>"<p>Cells were labeled with (A) BNF starch nanoparticles and (B) nanomag-D-spio nanoparticles. Osteogenic differentiation conditions were provided for 28 days following measurement of matrix calcification. BNF starch labeling of ASC resulted in a dose-dependent reduction of osteogenic differentiation potential whereas only nanomag-D-spio labeling at the highest concentration (100 µg Fe/ml) had a diminishing effect on the matrix calcification (n = 5; boxplots, Mann-Whitney U-test; *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177715, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g006", "stats"=>{"downloads"=>1, "page_views"=>56, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_labeling_on_osteogenic_differentiation_of_ASC_/1177715", "title"=>"Effect of labeling on osteogenic differentiation of ASC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685503"], "description"=>"<p>After cell labeling with (A) BNF starch nanoparticles and (B) nanomag-D-spio nanoparticles, adipogenic differentiation conditions were provided for 21 days and lipid droplet deposition was measured. BNF starch labeling of ASC resulted in a dose-dependent reduction of adipogenic differentiation potential (n = 4; boxplots, Mann-Whitney U-test; *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177713, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g005", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_labeling_on_adipogenic_differentiation_of_ASC_/1177713", "title"=>"Effect of labeling on adipogenic differentiation of ASC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685584", "https://ndownloader.figshare.com/files/1685585"], "description"=>"<div><p>Magnetic resonance imaging (MRI) using measurement of the transverse relaxation time (R2*) is to be considered as a promising approach for cell tracking experiments to evaluate the fate of transplanted progenitor cells and develop successful cell therapies for tissue engineering. While the relationship between core composition of nanoparticles and their MRI properties is well studied, little is known about possible effects on progenitor cells. This <i>in vitro</i> study aims at comparing two magnetic iron oxide nanoparticle types, single vs. multi-core nanoparticles, regarding their physico-chemical characteristics, effects on cellular behavior of adipose tissue-derived stem cells (ASC) like differentiation and proliferation as well as their detection and quantification by means of MRI. Quantification of both nanoparticle types revealed a linear correlation between labeling concentration and R2* values. However, according to core composition, different levels of labeling concentrations were needed to achieve comparable R2* values. Cell viability was not altered for all labeling concentrations, whereas the proliferation rate increased with increasing labeling concentrations. Likewise, deposition of lipid droplets as well as matrix calcification revealed to be highly dose-dependent particularly regarding multi-core nanoparticle-labeled cells. Synthesis of cartilage matrix proteins and mRNA expression of collagen type II was also highly dependent on nanoparticle labeling. In general, the differentiation potential was decreased with increasing labeling concentrations. This <i>in vitro</i> study provides the proof of principle for further <i>in vivo</i> tracking experiments of progenitor cells using nanoparticles with different core compositions but also provides striking evidence that combined testing of biological and MRI properties is advisable as improved MRI properties of multi-core nanoparticles may result in altered cell functions.</p></div>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177778, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108055.s001", "https://dx.doi.org/10.1371/journal.pone.0108055.s002"], "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Comparative_In_Vitro_Study_on_Magnetic_Iron_Oxide_Nanoparticles_for_MRI_Tracking_of_Adipose_Tissue_Derived_Progenitor_Cells/1177778", "title"=>"Comparative <i>In Vitro</i> Study on Magnetic Iron Oxide Nanoparticles for MRI Tracking of Adipose Tissue-Derived Progenitor Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-09-22 02:52:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1685493"], "description"=>"<p>Cells were treated with (A) BNF starch nanoparticles and (B) nanomag-D-spio nanoparticles. The activity of mitochondrial dehydrogenases was determined at day 7 after labeling. Only BNF starch labeling of ASC at the highest concentration of 50 µg Fe/ml diminished the activity of mitochondrial dehydrogenases significantly compared to control cells (n = 4; (A) mean ± SD, ANOVA/Tukey's-test; (B) boxplot, Mann-Whitney U-test; *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001).</p>", "links"=>[], "tags"=>["collagen type II", "MRI properties", "Magnetic Iron Oxide Nanoparticles", "asc", "concentration", "core composition", "iron oxide nanoparticle types", "progenitor cells", "cartilage matrix proteins"], "article_id"=>1177705, "categories"=>["Uncategorised"], "users"=>["Annika Kasten", "Cordula Grüttner", "Jens-Peter Kühn", "Rainer Bader", "Juliane Pasold", "Bernhard Frerich"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108055.g003", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activity_of_mitochondrial_dehydrogenases_/1177705", "title"=>"Activity of mitochondrial dehydrogenases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-22 02:52:19"}

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  • {"unique-ip"=>"23", "full-text"=>"21", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"16", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Engineering and technology", "average_usage"=>[282]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[271]}]}
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