Mother-to-Infant Transmission of Intestinal Bifidobacterial Strains Has an Impact on the Early Development of Vaginally Delivered Infant's Microbiota
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{"title"=>"Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota", "type"=>"journal", "authors"=>[{"first_name"=>"Hiroshi", "last_name"=>"Makino", "scopus_author_id"=>"37861524900"}, {"first_name"=>"Akira", "last_name"=>"Kushiro", "scopus_author_id"=>"6603104058"}, {"first_name"=>"Eiji", "last_name"=>"Ishikawa", "scopus_author_id"=>"47661345000"}, {"first_name"=>"Hiroyuki", "last_name"=>"Kubota", "scopus_author_id"=>"36637567100"}, {"first_name"=>"Agata", "last_name"=>"Gawad", "scopus_author_id"=>"56030391700"}, {"first_name"=>"Takafumi", "last_name"=>"Sakai", "scopus_author_id"=>"7404831057"}, {"first_name"=>"Kenji", "last_name"=>"Oishi", "scopus_author_id"=>"24402137800"}, {"first_name"=>"Rocio", "last_name"=>"Martin", "scopus_author_id"=>"16069052600"}, {"first_name"=>"Kaouther", "last_name"=>"Ben-Amor", "scopus_author_id"=>"7801496176"}, {"first_name"=>"Jan", "last_name"=>"Knol", "scopus_author_id"=>"7005797980"}, {"first_name"=>"Ryuichiro", "last_name"=>"Tanaka", "scopus_author_id"=>"7402347763"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203", "pui"=>"372334619", "sgr"=>"84893685421", "doi"=>"10.1371/journal.pone.0078331", "scopus"=>"2-s2.0-84893685421", "pmid"=>"24244304"}, "id"=>"09d57753-884f-35aa-ae39-50763f24c2f4", "abstract"=>"OBJECTIVES: Bifidobacterium species are one of the major components of the infant's intestine microbiota. Colonization with bifidobacteria in early infancy is suggested to be important for health in later life. However, information remains limited regarding the source of these microbes. Here, we investigated whether specific strains of bifidobacteria in the maternal intestinal flora are transmitted to their infant's intestine.\\n\\nMATERIALS AND METHODS: Fecal samples were collected from healthy 17 mother and infant pairs (Vaginal delivery: 12; Cesarean section delivery: 5). Mother's feces were collected twice before delivery. Infant's feces were collected at 0 (meconium), 3, 7, 30, 90 days after birth. Bifidobacteria isolated from feces were genotyped by multilocus sequencing typing, and the transitions of bifidobacteria counts in infant's feces were analyzed by quantitative real-time PCR.\\n\\nRESULTS: Stains belonging to Bifidobacterium adolescentis, Bifidobacterium bifidum, Bifidobacterium catenulatum, Bifidobacterium longum subsp. longum, and Bifidobacterium pseudocatenulatum, were identified to be monophyletic between mother's and infant's intestine. Eleven out of 12 vaginal delivered infants carried at least one monophyletic strain. The bifidobacterial counts of the species to which the monophyletic strains belong, increased predominantly in the infant's intestine within 3 days after birth. Among infants delivered by C-section, monophyletic strains were not observed. Moreover, the bifidobacterial counts were significantly lower than the vaginal delivered infants until 7 days of age.\\n\\nCONCLUSIONS: Among infants born vaginally, several Bifidobacterium strains transmit from the mother and colonize the infant's intestine shortly after birth. Our data suggest that the mother's intestine is an important source for the vaginal delivered infant's intestinal microbiota.", "link"=>"http://www.mendeley.com/research/mothertoinfant-transmission-intestinal-bifidobacterial-strains-impact-early-development-vaginally-de", "reader_count"=>170, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>8, "Researcher"=>37, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>35, "Other"=>9, "Student > Bachelor"=>27, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>8, "Researcher"=>37, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>7, "Student > Master"=>35, "Other"=>9, "Student > Bachelor"=>27, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Agricultural and Biological Sciences"=>75, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>3, "Environmental Science"=>2, "Nursing and Health Professions"=>8, "Biochemistry, Genetics and Molecular Biology"=>13, "Medicine and Dentistry"=>41, "Neuroscience"=>1, "Sports and Recreations"=>1, "Psychology"=>6, "Social Sciences"=>2, "Immunology and Microbiology"=>12}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>41}, "Social Sciences"=>{"Social Sciences"=>2}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Psychology"=>{"Psychology"=>6}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>2}, "Chemistry"=>{"Chemistry"=>3}, "Neuroscience"=>{"Neuroscience"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>12}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>75}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>8}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>4, "Japan"=>1, "Brazil"=>1, "Italy"=>1, "France"=>1, "Switzerland"=>1}, "group_count"=>10}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1281074", "https://ndownloader.figshare.com/files/1281075", "https://ndownloader.figshare.com/files/1281076", "https://ndownloader.figshare.com/files/1281077", "https://ndownloader.figshare.com/files/1281078"], "description"=>"<div><p>Objectives</p><p><i>Bifidobacterium</i> species are one of the major components of the infant's intestine microbiota. Colonization with bifidobacteria in early infancy is suggested to be important for health in later life. However, information remains limited regarding the source of these microbes. Here, we investigated whether specific strains of bifidobacteria in the maternal intestinal flora are transmitted to their infant's intestine.</p><p>Materials and Methods</p><p>Fecal samples were collected from healthy 17 mother and infant pairs (Vaginal delivery: 12; Cesarean section delivery: 5). Mother's feces were collected twice before delivery. Infant's feces were collected at 0 (meconium), 3, 7, 30, 90 days after birth. Bifidobacteria isolated from feces were genotyped by multilocus sequencing typing, and the transitions of bifidobacteria counts in infant's feces were analyzed by quantitative real-time PCR.</p><p>Results</p><p>Stains belonging to Bifidobacterium adolescentis, Bifidobacterium bifidum, Bifidobacterium catenulatum, Bifidobacterium longum subsp. longum, and Bifidobacterium pseudocatenulatum, were identified to be monophyletic between mother's and infant's intestine. Eleven out of 12 vaginal delivered infants carried at least one monophyletic strain. The bifidobacterial counts of the species to which the monophyletic strains belong, increased predominantly in the infant's intestine within 3 days after birth. Among infants delivered by C-section, monophyletic strains were not observed. Moreover, the bifidobacterial counts were significantly lower than the vaginal delivered infants until 7 days of age.</p><p>Conclusions</p><p>Among infants born vaginally, several Bifidobacterium strains transmit from the mother and colonize the infant's intestine shortly after birth. Our data suggest that the mother's intestine is an important source for the vaginal delivered infant's intestinal microbiota.</p></div>", "links"=>[], "tags"=>["intestinal", "bifidobacterial", "strains", "vaginally", "delivered"], "article_id"=>850900, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0078331.s001", "https://dx.doi.org/10.1371/journal.pone.0078331.s002", "https://dx.doi.org/10.1371/journal.pone.0078331.s003", "https://dx.doi.org/10.1371/journal.pone.0078331.s004", "https://dx.doi.org/10.1371/journal.pone.0078331.s005"], "stats"=>{"downloads"=>13, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mother_to_Infant_Transmission_of_Intestinal_Bifidobacterial_Strains_Has_an_Impact_on_the_Early_Development_of_Vaginally_Delivered_Infant_s_Microbiota_/850900", "title"=>"Mother-to-Infant Transmission of Intestinal Bifidobacterial Strains Has an Impact on the Early Development of Vaginally Delivered Infant's Microbiota", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281071"], "description"=>"<p>Primers targeting species belonging to <i>B. adolescentis</i>, <i>B. bifidum</i>, <i>B. catenulatum</i>, <i>B. pseudocatenulatum</i> were designed by Delétoile <i>et al.</i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0078331#pone.0078331-Deltoile1\" target=\"_blank\">[30]</a>, and <i>B. longum</i> subsp. <i>longum</i> primers were designed by Makino <i>et al.</i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0078331#pone.0078331-Makino1\" target=\"_blank\">[21]</a>.</p>", "links"=>[], "tags"=>["sets", "mlst"], "article_id"=>850897, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.t001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sets_for_MLST_analysis_/850897", "title"=>"Primer sets for MLST analysis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281069"], "description"=>"<p>Numbers of vaginal delivered (VD) infants were 12, infants delivered by C-section (CS) were 5. Bars represent the median values respectively. For values less than the qPCR detection limit (10<sup>6</sup> cells/g of feces), “detection limit/√2” <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0078331#pone.0078331-Chen1\" target=\"_blank\">[34]</a> was used as a complement value. Stars indicate significant differences between VD infants and CD infants (*<i>P</i><0.05; **<i>P</i><0.01).</p>", "links"=>[], "tags"=>["bifidobacteria", "17", "feces", "days"], "article_id"=>850895, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.g003", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_total_bifidobacteria_detected_in_17_infant_s_feces_from_0_to_7_days_of_age_/850895", "title"=>"The total bifidobacteria detected in 17 infant's feces from 0 to 7 days of age.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281070"], "description"=>"<p>Infant no.<sup>a</sup> The <i>B. adolescentis</i> group consists of <i>B. adolescentis</i> genotypes A and B. <sup>b</sup> The <i>B. catenulatum</i> group consists of <i>B. catenulatum</i> and <i>B. pseudocatenulatum</i>.</p>", "links"=>[], "tags"=>["numbers", "bifidobacteria", "infants", "days"], "article_id"=>850896, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.g004", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_numbers_of_bifidobacteria_in_infants_from_0_day_to_7_days_after_birth_/850896", "title"=>"The numbers of bifidobacteria in infants from 0 day to 7 days after birth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281068"], "description"=>"<p>All dendrogram were generated by a multi-scale setting for comparison and UPGMA for clustering.</p>", "links"=>[], "tags"=>["22", "isolates", "cesarean", "delivered", "mother-infant"], "article_id"=>850894, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.g002", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dendrogram_of_22_individual_B_longum_subsp_longum_isolates_from_5_cesarean_delivered_mother_infant_pairs_/850894", "title"=>"Dendrogram of 22 individual <i>B. longum</i> subsp. <i>longum</i> isolates from 5 cesarean delivered mother-infant pairs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281065"], "description"=>"<p>Dendrogram of (A) 15 individual strains of <i>B. adolescentis</i> (ADO), (B) 25 individual <i>B. bifidum</i> strains (BIF), (C) 7 individual <i>B. catenulatum</i> strains (CAT), (D) 28 individual <i>B. longum</i> subsp. <i>longum</i> strains (LON), (E) 6 individual <i>B. pseudocatenulatum</i> strains (PSE) were all generated by a multi-scale setting for comparison and UPGMA for clustering. <sup>*</sup> Isolates from both members of a mother–infant pair and showing the same MLST profile within a given cluster.</p>", "links"=>[], "tags"=>["mlst", "profiles", "strains", "12", "vaginal", "delivered", "mother-infant"], "article_id"=>850891, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.g001", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_MLST_profiles_of_strains_obtained_from_12_vaginal_delivered_mother_infant_pairs_/850891", "title"=>"Comparison of MLST profiles of strains obtained from 12 vaginal delivered mother-infant pairs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281073"], "description"=>"<p>“•” represents that at least one mother-infant monophyletic <i>Bifidobacterium</i> strain was isolated from the indicated family. Mother no. 5 gave birth to twins (A, B).</p>", "links"=>[], "tags"=>["mother-infant", "monophyletic", "strains", "16"], "article_id"=>850899, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.t003", "stats"=>{"downloads"=>4, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Detection_of_mother_infant_monophyletic_Bifidobacterium_strains_among_16_families_/850899", "title"=>"Detection of mother-infant monophyletic <i>Bifidobacterium</i> strains among 16 families.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-14 03:38:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1281072"], "description"=>"a<p>The <i>B. adolescentis</i> group consists of <i>B. adolescentis</i> genotypes A and B.</p>b<p>The B. catenulatum group consists of B. catenulatum and B. pseudocatenulatum.</p>", "links"=>[], "tags"=>["rrna", "targeted", "primer", "sets"], "article_id"=>850898, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Hiroshi Makino", "Akira Kushiro", "Eiji Ishikawa", "Hiroyuki Kubota", "Agata Gawad", "Takafumi Sakai", "Kenji Oishi", "Rocío Martín", "Kaouther Ben-Amor", "Jan Knol", "Ryuichiro Tanaka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078331.t002", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_16S_rRNA_gene_targeted_primer_sets_used_for_qPCR_/850898", "title"=>"16S rRNA gene targeted primer sets used for qPCR.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-14 03:38:21"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"16", "full-text"=>"20", "pdf"=>"14", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
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  • {"unique-ip"=>"50", "full-text"=>"58", "pdf"=>"25", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"31", "full-text"=>"23", "pdf"=>"17", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
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  • {"unique-ip"=>"54", "full-text"=>"61", "pdf"=>"32", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
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  • {"unique-ip"=>"32", "full-text"=>"36", "pdf"=>"22", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"18", "full-text"=>"24", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"unique-ip"=>"35", "full-text"=>"36", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"21", "full-text"=>"20", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"30", "full-text"=>"29", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"26", "full-text"=>"23", "pdf"=>"16", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"24", "full-text"=>"29", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"35", "full-text"=>"43", "pdf"=>"19", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"30", "full-text"=>"20", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"2", "cited-by"=>"1", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"19", "full-text"=>"26", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"15", "full-text"=>"19", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
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  • {"unique-ip"=>"39", "full-text"=>"38", "pdf"=>"16", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"29", "full-text"=>"35", "pdf"=>"15", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
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  • {"unique-ip"=>"28", "full-text"=>"30", "pdf"=>"16", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"33", "full-text"=>"35", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"6", "cited-by"=>"1", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"37", "full-text"=>"34", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Ecology and environmental sciences", "average_usage"=>[284, 475, 603, 722, 826, 928, 1026, 1129, 1225, 1310, 1390, 1468, 1549]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Surgical and invasive medical procedures", "average_usage"=>[223, 396, 511, 599, 690, 775, 859, 936, 1012, 1090, 1168, 1237, 1299]}, {"subject_area"=>"/People and places", "average_usage"=>[270, 456, 573, 676, 773, 867, 955, 1037, 1120, 1205, 1286, 1363, 1436]}, {"subject_area"=>"/People and places/Population groupings", "average_usage"=>[265, 456, 578, 682, 782, 881, 965, 1053, 1133, 1223, 1310, 1391, 1457]}]}

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