Viruses Associated with Ovarian Degeneration in Apis mellifera L. Queens
Publication Date
January 25, 2011
Journal
PLOS ONE
Authors
Laurent Gauthier, Marc Ravallec, Magali Tournaire, François Cousserans, et al
Volume
6
Issue
1
Pages
e16217
DOI
https://dx.plos.org/10.1371/journal.pone.0016217
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0016217
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21283547
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3026828
Europe PMC
http://europepmc.org/abstract/MED/21283547
Web of Science
000286661400034
Scopus
79551546289
Mendeley
http://www.mendeley.com/research/viruses-associated-ovarian-degeneration-apis-mellifera-l-queens-1
Events
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Mendeley | Further Information

{"title"=>"Viruses associated with ovarian degeneration in Apis mellifera L. Queens", "type"=>"journal", "authors"=>[{"first_name"=>"Laurent", "last_name"=>"Gauthier", "scopus_author_id"=>"57196213533"}, {"first_name"=>"Marc", "last_name"=>"Ravallec", "scopus_author_id"=>"6602399552"}, {"first_name"=>"Magali", "last_name"=>"Tournaire", "scopus_author_id"=>"37662276200"}, {"first_name"=>"François", "last_name"=>"Cousserans", "scopus_author_id"=>"56321570100"}, {"first_name"=>"Max", "last_name"=>"Bergoin", "scopus_author_id"=>"7004318949"}, {"first_name"=>"Benjamin", "last_name"=>"Dainat", "scopus_author_id"=>"6508154270"}, {"first_name"=>"Joachim R.", "last_name"=>"de Miranda", "scopus_author_id"=>"7004471310"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"361204306", "doi"=>"10.1371/journal.pone.0016217", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"21283547", "issn"=>"19326203", "scopus"=>"2-s2.0-79551546289", "sgr"=>"79551546289"}, "id"=>"0e3cfe28-d273-34e7-b483-8c74b04c96e6", "abstract"=>"Queen fecundity is a critical issue for the health of honeybee (Apis mellifera L.) colonies, as she is the only reproductive female in the colony and responsible for the constant renewal of the worker bee population. Any factor affecting the queen's fecundity will stagnate colony development, increasing its susceptibility to opportunistic pathogens. We discovered a pathology affecting the ovaries, characterized by a yellow discoloration concentrated in the apex of the ovaries resulting from degenerative lesions in the follicles. In extreme cases, marked by intense discoloration, the majority of the ovarioles were affected and these cases were universally associated with egg-laying deficiencies in the queens. Microscopic examination of the degenerated follicles showed extensive paracrystal lattices of 30 nm icosahedral viral particles. A cDNA library from degenerated ovaries contained a high frequency of deformed wing virus (DWV) and Varroa destructor virus 1 (VDV-1) sequences, two common and closely related honeybee Iflaviruses. These could also be identified by in situ hybridization in various parts of the ovary. A large-scale survey for 10 distinct honeybee viruses showed that DWV and VDV-1 were by far the most prevalent honeybee viruses in queen populations, with distinctly higher prevalence in mated queens (100% and 67%, respectively for DWV and VDV-1) than in virgin queens (37% and 0%, respectively). Since very high viral titres could be recorded in the ovaries and abdomens of both functional and deficient queens, no significant correlation could be made between viral titre and ovarian degeneration or egg-laying deficiency among the wider population of queens. Although our data suggest that DWV and VDV-1 have a role in extreme cases of ovarian degeneration, infection of the ovaries by these viruses does not necessarily result in ovarian degeneration, even at high titres, and additional factors are likely to be involved in this pathology.", "link"=>"http://www.mendeley.com/research/viruses-associated-ovarian-degeneration-apis-mellifera-l-queens-1", "reader_count"=>66, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Student > Doctoral Student"=>8, "Researcher"=>13, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>3, "Student > Master"=>11, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>9}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Student > Doctoral Student"=>8, "Researcher"=>13, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>3, "Student > Master"=>11, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>9}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>51, "Medicine and Dentistry"=>2, "Veterinary Science and Veterinary Medicine"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>51}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>6}}, "reader_count_by_country"=>{"United States"=>1, "Poland"=>1, "Mexico"=>2, "United Kingdom"=>1, "France"=>1, "Australia"=>1, "Germany"=>1}, "group_count"=>2}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/804861"], "description"=>"<p>N: number of samples analysed.</p>", "links"=>[], "tags"=>["mated", "queens", "ages", "displaying", "coloration", "ovaries", "dissection", "egg-laying", "troubles"], "article_id"=>475213, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Percentages_of_mated_queens_sampling_A_of_different_ages_displaying_coloration_on_their_ovaries_ovary_coloration_upon_dissection_or_associated_with_egg_laying_troubles_fecundity_troubles_according_to_beekeeper_s_observations_/475213", "title"=>"Percentages of mated queens (sampling A) of different ages displaying coloration on their ovaries (ovary coloration) upon dissection or associated with egg-laying troubles (fecundity troubles) according to beekeeper's observations.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-01-25 01:26:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/804704"], "description"=>"<p>DWV and VDV-1 quantitative values are indicated as equivalent genome copies deduced from standard curves made of tenfold dilutions of PCR fragments.</p>", "links"=>[], "tags"=>["dwv", "vdv-1", "loads", "abdomen", "ovaries", "24", "queens", "samples"], "article_id"=>475061, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_DWV_and_VDV_1_loads_in_abdomen_and_ovaries_of_24_queens_samples_sampling_B_/475061", "title"=>"Distribution of DWV and VDV-1 loads in abdomen and ovaries of 24 queens samples (sampling B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-01-25 01:24:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/804806"], "description"=>"<p>Data were considered as significant if P<0.05.</p>", "links"=>[], "tags"=>["performed", "crossed", "variables"], "article_id"=>475174, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Records_of_the_different_statistical_tests_performed_from_four_different_crossed_variables_sampling_A_/475174", "title"=>"Records of the different statistical tests performed from four different crossed variables (sampling A).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-01-25 01:26:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/804245"], "description"=>"<p>A and B: Stereomicroscopic observation of ovaries displaying yellowish colorations in the ovarioles. C: Clumps in the terminal filament of ovarioles observed by phase contrast microscopy (Olympus MVX 10). D: Propidium iodide staining of an ovariole showing nuclear condensation in the terminal filament (×600). E: general view of the apex of an ovary double stained with propidium iodide (red) and DAPI (blue). F, G and H: Toluidin blue staining of 1 µm thick cuttings from the germinal region of two ovaries. F and H: ovarioles displaying degeneration process showing detail of the disorganization of follicles surrounded by several empty ovarioles; H: presence of crystalline arrays in the peritoneal epithelium (arrow). G, normal ovary: detail of three follicles at different developmental stages. The nurse cells chamber and the oocyte chamber differentiation appear on the follicle located on the right. fe: follicular epithelium; pe: periteoneal epithelium; bl: basal lamina. I–L: In situ hybridization assays performed from paraffin embedded tissues for the detection of DWV/VDV-1 RNA. I and J: staining performed from the terminal filament region of an ovary using either antisense (I) or sense (J) probe. K and L: <i>in situ</i> analysis performed from the vitellarium showing DWV/VDV-1 RNA staining in the periphery of an oocyte (Arrow) with the antisens probe (L); K: control sense probe. Slices were counterstained with eosin Y.</p>", "links"=>[], "tags"=>["Virology", "microbiology", "pathology"], "article_id"=>474612, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.g001", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histological_analysis_of_the_queen_ovary_/474612", "title"=>"Histological analysis of the queen ovary.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-01-25 01:16:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/804775"], "description"=>"<p>The respective age, fitness status (association with egg-laying troubles) and DWV titres recorded in each queen is indicated, as well as the presence of yellow colorations in the ovaries. nd: sample not dissected. HIGH: samples displaying a particular intense coloration in the ovary. ABPV: acute bee paralysis virus; VdMLV: <i>Varroa destructor</i> macula-like virus; BQCV: black queen cell virus; CBPV: chronic bee paralysis virus; DWV: deformed wing virus; IAPV: israeli acute bee paralysis virus; KBV: Kashmir bee virus; SBV: sacbrood virus; SBPV: slow paralysis virus; VDV-1: <i>Varroa destructor</i> virus-1.</p>", "links"=>[], "tags"=>["10", "viruses", "30", "mated", "queens", "regions", "france"], "article_id"=>475138, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.t003", "stats"=>{"downloads"=>3, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Presence_or_absence_of_10_different_bee_viruses_in_a_sample_of_30_mated_queens_collected_from_different_regions_of_France_sampling_A_/475138", "title"=>"Presence or absence of 10 different bee viruses in a sample of 30 mated queens collected from different regions of France (sampling A).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-01-25 01:25:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/401553", "https://ndownloader.figshare.com/files/401580", "https://ndownloader.figshare.com/files/401610", "https://ndownloader.figshare.com/files/401648"], "description"=>"<div><p>Queen fecundity is a critical issue for the health of honeybee (<em>Apis mellifera</em> L.) colonies, as she is the only reproductive female in the colony and responsible for the constant renewal of the worker bee population. Any factor affecting the queen's fecundity will stagnate colony development, increasing its susceptibility to opportunistic pathogens. We discovered a pathology affecting the ovaries, characterized by a yellow discoloration concentrated in the apex of the ovaries resulting from degenerative lesions in the follicles. In extreme cases, marked by intense discoloration, the majority of the ovarioles were affected and these cases were universally associated with egg-laying deficiencies in the queens. Microscopic examination of the degenerated follicles showed extensive paracrystal lattices of 30 nm icosahedral viral particles. A cDNA library from degenerated ovaries contained a high frequency of deformed wing virus (DWV) and <em>Varroa destructor</em> virus 1 (VDV-1) sequences, two common and closely related honeybee Iflaviruses. These could also be identified by <em>in situ</em> hybridization in various parts of the ovary. A large-scale survey for 10 distinct honeybee viruses showed that DWV and VDV-1 were by far the most prevalent honeybee viruses in queen populations, with distinctly higher prevalence in mated queens (100% and 67%, respectively for DWV and VDV-1) than in virgin queens (37% and 0%, respectively). Since very high viral titres could be recorded in the ovaries and abdomens of both functional and deficient queens, no significant correlation could be made between viral titre and ovarian degeneration or egg-laying deficiency among the wider population of queens. Although our data suggest that DWV and VDV-1 have a role in extreme cases of ovarian degeneration, infection of the ovaries by these viruses does not necessarily result in ovarian degeneration, even at high titres, and additional factors are likely to be involved in this pathology.</p> </div>", "links"=>[], "tags"=>["viruses", "ovarian", "degeneration", "queens"], "article_id"=>139344, "categories"=>["Cancer", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0016217.s001", "https://dx.doi.org/10.1371/journal.pone.0016217.s002", "https://dx.doi.org/10.1371/journal.pone.0016217.s003", "https://dx.doi.org/10.1371/journal.pone.0016217.s004"], "stats"=>{"downloads"=>17, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Viruses_Associated_with_Ovarian_Degeneration_in_Apis_mellifera_L_Queens/139344", "title"=>"Viruses Associated with Ovarian Degeneration in <em>Apis mellifera</em> L. Queens", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-01-25 02:35:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/804457"], "description"=>"<p>A: TEM analysis of a normal follicle showing nurse cells (nc), the thick basal lamina (bl) and the peritoneal epithelium (pe). B: TEM analysis of an empty ovariole with presence of viral particles (vp) and cellular debris lined by the peritoneal enveloppe (pe). C and D: TEM analysis showing cellular degeneration of follicular cells with myelin whorls (mw), lipid droplets (ld), viral particles (vp) and peritoneal envelope (pe). E: TEM observation of viral particles (vp) and the virogenic stroma (vs) near the plasma membrane (pm) of a follicular cell. F: detail of a crystalline matrix in a peritoneal epithelial cell. Bars in electron micrographs represent 5 µm, 3 µm, 2 µm, 2 µm, 250 nm and 3 µm in figures A, B, C, D, E and F, respectively.</p>", "links"=>[], "tags"=>["observations"], "article_id"=>474830, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ultrastructural_observations_in_the_germarium_/474830", "title"=>"Ultrastructural observations in the germarium.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-01-25 01:20:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/804636"], "description"=>"<p>Data are shown according to the presence of egg-laying troubles detected by beekeepers, the presence of yellow coloration in the upper ovary detected upon dissection and the queen age (Y = year). DWV quantitative values are indicated as equivalent genome copies deduced from a standard curve made of tenfold dilutions of a PCR fragment.</p>", "links"=>[], "tags"=>["dwv", "titres", "queens", "samples"], "article_id"=>475004, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.g004", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_DWV_titres_in_queens_samples_sampling_A_/475004", "title"=>"Distribution of DWV titres in queens samples (sampling A).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-01-25 01:23:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/804578"], "description"=>"<p>Mated queens were divided according to the 2 different samplings (A and B). Sampling A: sample made of 130 mated queens received from beekeepers. Sampling B: sample of 24 mated two year old queens displaying a high fitness. Virus abbreviations as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0016217#pone-0016217-t003\" target=\"_blank\">Table 3</a>.</p>", "links"=>[], "tags"=>["10", "viruses", "virgin", "mated"], "article_id"=>474943, "categories"=>["Virology", "Cell Biology", "Microbiology"], "users"=>["Laurent Gauthier", "Marc Ravallec", "Magali Tournaire", "François Cousserans", "Max Bergoin", "Benjamin Dainat", "Joachim R. de Miranda"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016217.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Detection_of_10_bee_viruses_in_virgin_and_mated_queens_/474943", "title"=>"Detection of 10 bee viruses in virgin and mated queens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-01-25 01:22:23"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
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  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
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  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
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  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"15", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"21", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"17", "full-text"=>"23", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
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Relative Metric

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