Rectal Application of a Highly Osmolar Personal Lubricant in a Macaque Model Induces Acute Cytotoxicity but Does Not Increase Risk of SHIV Infection
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{"title"=>"Rectal application of a highly osmolar personal lubricant in a macaque model induces acute cytotoxicity but does not increase risk of SHIV infection", "type"=>"journal", "authors"=>[{"first_name"=>"Sundaram A.", "last_name"=>"Vishwanathan", "scopus_author_id"=>"13410918000"}, {"first_name"=>"Monica R.", "last_name"=>"Morris", "scopus_author_id"=>"55975092000"}, {"first_name"=>"Richard J.", "last_name"=>"Wolitski", "scopus_author_id"=>"7003288439"}, {"first_name"=>"Wei", "last_name"=>"Luo", "scopus_author_id"=>"55334103600"}, {"first_name"=>"Charles E.", "last_name"=>"Rose", "scopus_author_id"=>"15521036500"}, {"first_name"=>"Dianna M.", "last_name"=>"Blau", "scopus_author_id"=>"15729433700"}, {"first_name"=>"Theodros", "last_name"=>"Tsegaye", "scopus_author_id"=>"26423988000"}, {"first_name"=>"Sherif R.", "last_name"=>"Zaki", "scopus_author_id"=>"7101848151"}, {"first_name"=>"David A.", "last_name"=>"Garber", "scopus_author_id"=>"36973693000"}, {"first_name"=>"Leecresia T.", "last_name"=>"Jenkins", "scopus_author_id"=>"55975268100"}, {"first_name"=>"Tara C.", "last_name"=>"Henning", "scopus_author_id"=>"57196564140"}, {"first_name"=>"Dorothy L.", "last_name"=>"Patton", "scopus_author_id"=>"7101646532"}, {"first_name"=>"R. Michael", "last_name"=>"Hendry", "scopus_author_id"=>"7005267536"}, {"first_name"=>"Janet M.", "last_name"=>"Mcnicholl", "scopus_author_id"=>"7004421758"}, {"first_name"=>"Ellen N.", "last_name"=>"Kersh", "scopus_author_id"=>"36893402600"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0120021", "pmid"=>"25853710", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\r1932-6203 (Linking)", "sgr"=>"84928905459", "scopus"=>"2-s2.0-84928905459", "pui"=>"604108614"}, "id"=>"81459beb-dc09-3b10-befe-fb05b7e1ed30", "abstract"=>"<sec id=\"sec001\"> <title>Background</title> <p>Personal lubricant use is common during anal intercourse. Some water-based products with high osmolality and low pH can damage genital and rectal tissues, and the polymer polyquaternium 15 (PQ15) can enhance HIV replication <italic>in vitro</italic>. This has raised concerns that lubricants with such properties may increase STD/HIV infection risk, although <italic>in vivo</italic> evidence is scarce. We use a macaque model to evaluate rectal cytotoxicity and SHIV infection risk after use of a highly osmolar (&gt;8,000 mOsm/kg) water-based lubricant with pH of 4.4, and containing PQ15.</p> </sec> <sec id=\"sec002\"> <title>Methods</title> <p>Cytotoxicity was documented by measuring inflammatory cytokines and epithelial tissue sloughing during six weeks of repeated, non-traumatic lubricant or control buffer applications to rectum and anus. We measured susceptibility to SHIV<sub>SF162P3</sub> infection by comparing virus doses needed for rectal infection in twenty-one macaques treated with lubricant or control buffer 30 minutes prior to virus exposure.</p> </sec> <sec id=\"sec003\"> <title>Results</title> <p>Lubricant increased pro-inflammatory cytokines and tissue sloughing while control buffer (phosphate buffered saline; PBS) did not. However, the estimated AID<sub>50</sub> (50% animal infectious dose) was not different in lubricant- and control buffer-treated macaques (p = 0.4467; logistic regression models).</p> </sec> <sec id=\"sec004\"> <title>Conclusions</title> <p>Although the test lubricant caused acute cytotoxicity in rectal tissues, it did not increase susceptibility to infection in this macaque model. Thus neither the lubricant-induced type/extent of inflammation nor the presence of PQ15 affected infection risk. This study constitutes a first step in the <italic>in vivo</italic> evaluation of lubricants with regards to HIV transmission.</p> </sec>", "link"=>"http://www.mendeley.com/research/rectal-application-highly-osmolar-personal-lubricant-macaque-model-induces-acute-cytotoxicity-not-in", "reader_count"=>7, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Medicine and Dentistry"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Spain"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2010911"], "description"=>"<p>Study design showing the cytotoxicity phase of the study (A); black rectangles = lubricant application; grey triangles = sample collections immediately prior to each product application (longitudinal time points); black triangles = samples taken 15 minutes to 48 hours after product application (acute time points); open hexagons = rectal biopsies, taken from one animal at 30 minutes post lubricant-application, and from one animal a week after last lubricant application; m = minutes; h = hours; B. Induction of pro-inflammatory cytokine TNF-α at acute time points (15 or 30 m, and 2, 4, 24, or 48 h post-product application); circles represent individual macaques; C. Induction of pro-inflammatory cytokine TNF-α at all time points during 6 weeks of product application; medians and ranges are graphed.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372053, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.g001", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cytotoxicity_study_design_Phase_I_and_induction_of_pro_inflammatory_cytokines_/1372053", "title"=>"Cytotoxicity study design (Phase I) and induction of pro-inflammatory cytokines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010930", "https://ndownloader.figshare.com/files/2010931", "https://ndownloader.figshare.com/files/2010932", "https://ndownloader.figshare.com/files/2010933", "https://ndownloader.figshare.com/files/2010934", "https://ndownloader.figshare.com/files/2010935"], "description"=>"<div><p>Background</p><p>Personal lubricant use is common during anal intercourse. Some water-based products with high osmolality and low pH can damage genital and rectal tissues, and the polymer polyquaternium 15 (PQ15) can enhance HIV replication <i>in vitro</i>. This has raised concerns that lubricants with such properties may increase STD/HIV infection risk, although <i>in vivo</i> evidence is scarce. We use a macaque model to evaluate rectal cytotoxicity and SHIV infection risk after use of a highly osmolar (>8,000 mOsm/kg) water-based lubricant with pH of 4.4, and containing PQ15.</p><p>Methods</p><p>Cytotoxicity was documented by measuring inflammatory cytokines and epithelial tissue sloughing during six weeks of repeated, non-traumatic lubricant or control buffer applications to rectum and anus. We measured susceptibility to SHIV<sub>SF162P3</sub> infection by comparing virus doses needed for rectal infection in twenty-one macaques treated with lubricant or control buffer 30 minutes prior to virus exposure.</p><p>Results</p><p>Lubricant increased pro-inflammatory cytokines and tissue sloughing while control buffer (phosphate buffered saline; PBS) did not. However, the estimated AID<sub>50</sub> (50% animal infectious dose) was not different in lubricant- and control buffer-treated macaques (p = 0.4467; logistic regression models).</p><p>Conclusions</p><p>Although the test lubricant caused acute cytotoxicity in rectal tissues, it did not increase susceptibility to infection in this macaque model. Thus neither the lubricant-induced type/extent of inflammation nor the presence of PQ15 affected infection risk. This study constitutes a first step in the <i>in vivo</i> evaluation of lubricants with regards to HIV transmission.</p></div>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372070, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0120021.s001", "https://dx.doi.org/10.1371/journal.pone.0120021.s002", "https://dx.doi.org/10.1371/journal.pone.0120021.s003", "https://dx.doi.org/10.1371/journal.pone.0120021.s004", "https://dx.doi.org/10.1371/journal.pone.0120021.s005", "https://dx.doi.org/10.1371/journal.pone.0120021.s006"], "stats"=>{"downloads"=>2, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rectal_Application_of_a_Highly_Osmolar_Personal_Lubricant_in_a_Macaque_Model_Induces_Acute_Cytotoxicity_but_Does_Not_Increase_Risk_of_SHIV_Infection_/1372070", "title"=>"Rectal Application of a Highly Osmolar Personal Lubricant in a Macaque Model Induces Acute Cytotoxicity but Does Not Increase Risk of SHIV Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010927"], "description"=>"<p>The p-values were calculated using unpaired t-tests (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0120021#sec006\" target=\"_blank\">Materials & Methods</a> for details); the statistically significant ones are indicated in bold; CI = confidence interval.</p><p><sup>1</sup>We calculated the geometric means (GMs) of cytokines concentrations as shown, combining the measurements at 15m, 30m, 2- and 4-h acute time points. Levels of eight other cytokines were determined (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0120021#sec006\" target=\"_blank\">Methods</a>) but many of the data points were below the assay limit of detection, and not suitable for accurate statistical analyses</p><p>Cytokine concentration in rectal lavages at acute time points post lubricant/control buffer application.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372067, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.t001", "stats"=>{"downloads"=>7, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cytokine_concentration_in_rectal_lavages_at_acute_time_points_post_lubricant_control_buffer_application_/1372067", "title"=>"Cytokine concentration in rectal lavages at acute time points post lubricant/control buffer application.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010919"], "description"=>"<p>Showing biopsies from one animal (ID: 604962) collected before lubricant application (A) and 30 minutes after (B) product application; B shows focal infiltrates of inflammatory cells (square box), predominately mononuclear, seen in the lamina propria; there is no disruption of architecture. C is a magnified section (30x) of the square box with the green arrows showing mononuclear cells.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372061, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.g003", "stats"=>{"downloads"=>5, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hematoxylin_and_eosin_stain_20x_of_rectal_biopsies_/1372061", "title"=>"Hematoxylin and eosin stain (20x) of rectal biopsies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010915"], "description"=>"<p>A. Lubricant induces rectal shedding of epithelial cells. Examples of epithelial sloughing in a control- (top left) and lubricant-treated animal (top right). The lower panel shows a representative H&E stain of sloughed rectal epithelial cells (20x); B. Blood associated with rectal washes; photographs of microfuges containing rectal lavages; C,D. Epithelial sloughing measured at acute time points collected after the 2nd weekly lubricant application (C), and those measured over the entire study (D). The panel D in this figure shows three collections per week (day 1, pre-lubricant; day 2 pre-lubricant; day 2 post-lubricant), as indicated in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0120021#pone.0120021.g001\" target=\"_blank\">Fig. 1</a>.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372057, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.g002", "stats"=>{"downloads"=>6, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Epithelial_sloughing_and_blood_/1372057", "title"=>"Epithelial sloughing and blood.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010928"], "description"=>"<p>‘+’ = animal infected at the indicated dose;</p><p>‘0’ = animal not infected;</p><p>PBS = phosphate buffered saline; TCID<sub>50</sub> = tissue culture 50% infectious dose. The challenges were performed in six sets of macaques; sets1 and 2 were phosphate buffered saline (PBS)-treated controls; sets 3, 4, 5 and 6 were lubricant-treated.</p><p><sup>1</sup>Historical data from 5 uninfected and 1 infected animals were included at 250 TCID<sub>50</sub>, and 4 uninfected and 1 infected animals at 50 TCID<sub>50</sub>; these animals were non-PBS-treated</p><p>SHIV162p3 challenge doses and infection.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372068, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.t002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SHIV162p3_challenge_doses_and_infection_/1372068", "title"=>"SHIV162p3 challenge doses and infection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010923"], "description"=>"<p>A. Plasma SHIV RNA levels measured in control buffer-treated (black symbols; solid lines) and lubricant-treated (grey symbols; broken lines) animals. B. SHIV RNA levels measured in rectal secretions, in control buffer-treated (open symbols) and lubricant-treated (closed symbols) animals; 0 = time of peak plasma viremia.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372065, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.g005", "stats"=>{"downloads"=>1, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plasma_and_rectal_SHIV_RNA_/1372065", "title"=>"Plasma and rectal SHIV RNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-08 04:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/2010921"], "description"=>"<p>Lubricant was applied non-traumatically for three weeks, on two consecutive days per week. The animal was challenged with SHIV<sub>SF162p3</sub> 30 minutes after the sixth lubricant application (open triangle). To check for plasma viremia and virus shedding, samples were collected for at least 2 weeks post-peak viremia. Not shown are baseline blood draws that were performed before the first lubricant application to ensure that the animal is not infected.</p>", "links"=>[], "tags"=>["SHIVSF 162P infection", "Macaque Model Induces Acute Cytotoxicity", "epithelial tissue sloughing", "SHIV Infection BackgroundPersonal lubricant use", "std", "pq", "SHIV infection risk", "pbs", "rectal tissues", "polymer polyquaternium 15", "aid", "control buffer applications", "control buffer 30 minutes", "model"], "article_id"=>1372063, "categories"=>["Uncategorised"], "users"=>["Sundaram A. Vishwanathan", "Monica R. Morris", "Richard J. Wolitski", "Wei Luo", "Charles E. Rose", "Dianna M. Blau", "Theodros Tsegaye", "Sherif R. Zaki", "David A. Garber", "Leecresia T. Jenkins", "Tara C. Henning", "Dorothy L. Patton", "R. Michael Hendry", "Janet M. McNicholl", "Ellen N. Kersh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120021.g004", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Challenge_study_design_Phase_II_/1372063", "title"=>"Challenge study design (Phase II).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-08 04:12:14"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"65", "full-text"=>"87", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"58", "full-text"=>"65", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"70", "full-text"=>"74", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"136", "full-text"=>"150", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}

Relative Metric

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