Recombinant Monovalent Llama-Derived Antibody Fragments (VHH) to Rotavirus VP6 Protect Neonatal Gnotobiotic Piglets against Human Rotavirus-Induced Diarrhea
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{"title"=>"Recombinant Monovalent Llama-Derived Antibody Fragments (VHH) to Rotavirus VP6 Protect Neonatal Gnotobiotic Piglets against Human Rotavirus-Induced Diarrhea", "type"=>"journal", "authors"=>[{"first_name"=>"Celina G.", "last_name"=>"Vega", "scopus_author_id"=>"55326777000"}, {"first_name"=>"Marina", "last_name"=>"Bok", "scopus_author_id"=>"44761047800"}, {"first_name"=>"Anastasia N.", "last_name"=>"Vlasova", "scopus_author_id"=>"16246782500"}, {"first_name"=>"Kuldeep S.", "last_name"=>"Chattha", "scopus_author_id"=>"26030260100"}, {"first_name"=>"Silvia", "last_name"=>"Gómez-Sebastián", "scopus_author_id"=>"6507533554"}, {"first_name"=>"Carmen", "last_name"=>"Nuñez", "scopus_author_id"=>"56002966800"}, {"first_name"=>"Carmen", "last_name"=>"Alvarado", "scopus_author_id"=>"55351960400"}, {"first_name"=>"Rodrigo", "last_name"=>"Lasa", "scopus_author_id"=>"57200265661"}, {"first_name"=>"José M.", "last_name"=>"Escribano", "scopus_author_id"=>"55402647000"}, {"first_name"=>"Lorena L.", "last_name"=>"Garaicoechea", "scopus_author_id"=>"15062650300"}, {"first_name"=>"Fernando", "last_name"=>"Fernandez", "scopus_author_id"=>"57197112469"}, {"first_name"=>"Karin", "last_name"=>"Bok", "scopus_author_id"=>"57194045150"}, {"first_name"=>"Andrés", "last_name"=>"Wigdorovitz", "scopus_author_id"=>"6602679344"}, {"first_name"=>"Linda J.", "last_name"=>"Saif", "scopus_author_id"=>"7102226747"}, {"first_name"=>"Viviana", "last_name"=>"Parreño", "scopus_author_id"=>"6603502038"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-84878499313", "doi"=>"10.1371/journal.ppat.1003334", "sgr"=>"84878499313", "isbn"=>"1553-7374 (Electronic)\\n1553-7366 (Linking)", "pmid"=>"23658521", "issn"=>"15537366", "pui"=>"369039706"}, "id"=>"66dd8821-cadb-3ae4-ba54-2a3ba1a287c1", "abstract"=>"Group A Rotavirus (RVA) is the leading cause of severe diarrhea in children. The aims of the present study were to determine the neutralizing activity of VP6-specific llama-derived single domain nanoantibodies (VHH nanoAbs) against different RVA strains in vitro and to evaluate the ability of G6P[1] VP6-specific llama-derived single domain nanoantibodies (VHH) to protect against human rotavirus in gnotobiotic (Gn) piglets experimentally inoculated with virulent Wa G1P[8] rotavirus. Supplementation of the daily milk diet with 3B2 VHH clone produced using a baculovirus vector expression system (final ELISA antibody -Ab- titer of 4096; virus neutralization -VN- titer of 256) for 9 days conferred full protection against rotavirus associated diarrhea and significantly reduced virus shedding. The administration of comparable levels of porcine IgG Abs only protected 4 out of 6 of the animals from human RVA diarrhea but significantly reduced virus shedding. In contrast, G6P[1]-VP6 rotavirus-specific IgY Abs purified from eggs of hyperimmunized hens failed to protect piglets against human RVA-induced diarrhea or virus shedding when administering similar quantities of Abs. The oral administration of VHH nanoAb neither interfered with the host's isotype profiles of the Ab secreting cell responses to rotavirus, nor induced detectable host Ab responses to the treatment in serum or intestinal contents. This study shows that the oral administration of rotavirus VP6-VHH nanoAb is a broadly reactive and effective treatment against rotavirus-induced diarrhea in neonatal pigs. Our findings highlight the potential value of a broad neutralizing VP6-specific VHH nanoAb as a treatment that can complement or be used as an alternative to the current strain-specific RVA vaccines. Nanobodies could also be scaled-up to develop pediatric medication or functional food like infant milk formulas that might help treat RVA diarrhea.", "link"=>"http://www.mendeley.com/research/recombinant-monovalent-llamaderived-antibody-fragments-vhh-rotavirus-vp6-protect-neonatal-gnotobioti", "reader_count"=>63, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>7, "Researcher"=>17, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>3, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>7, "Researcher"=>17, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>3, "Student > Bachelor"=>7, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>39, "Medicine and Dentistry"=>3, "Veterinary Science and Veterinary Medicine"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Business, Management and Accounting"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>39}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "South Africa"=>1, "Kenya"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1052187"], "description"=>"a<p>Determined by fluorescence focus forming unit reduction assay. A 10 ml (4.8 percent) aliquot of each Ab pool (VHH/IgY/Control larvae/IgG) was added to 210 ml of sterile commercial bovine milk to obtain the indicated final Ab titer to Wa HRV. Neg = negative.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "elisa", "isotype-specific", "ab", "titers", "wa", "hrv", "supplemented", "bovine", "gn"], "article_id"=>696684, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.t001", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VN_and_ELISA_isotype_specific_Ab_titers_to_Wa_HRV_in_the_supplemented_bovine_milk_used_to_feed_Gn_piglets_/696684", "title"=>"VN and ELISA isotype-specific Ab titers to Wa HRV in the supplemented bovine milk used to feed Gn piglets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-02 01:51:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052184"], "description"=>"<p>Continuous lines represent geometric mean of porcine IgG Ab titers (GMT) to the corresponding treatment administered (VHH, IgY or IgG Abs) in serum samples per group every 7 days. Dashed lines represent ELISA Ab titer of passive Abs to Wa HRV (VHH, IgY or IgG Abs) in rectal swabs every 7 days. The bars at PID 21 represent porcine IgG and IgA Abs to passive treatment in SIC: small intestinal contents and LIC: large intestinal contents collected after euthanasia. All animals were orally inoculated at 72 h of age [0 post inoculation day (0 PID)], and euthanized at PID 21±3. The arrow at PID 0 indicates the inoculation day. Different letters indicate significant differences between groups (p<0.05). In the case of groups CL, IgG and NT the results represent porcine IgG Ab titers to chicken IgY in serum but a similar response was observed against VHH nanoAbs (data not shown).</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "responses", "passive", "treatments", "sera", "intestinal", "contents", "treated"], "article_id"=>696681, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immune_responses_to_the_passive_treatments_were_determined_in_sera_and_intestinal_contents_of_treated_piglets_/696681", "title"=>"Immune responses to the passive treatments were determined in sera and intestinal contents of treated piglets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052182"], "description"=>"<p>When comparing ASC numbers of the same isotype among treatment groups, different letters indicate a significant difference (Kruskal-Wallis rank sum test, p<0.05). n = number of piglets in each group. The IgM ASC response was not included as no IgM ASC were detected in most of the groups of pigs.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "wa", "hrv-specific", "asc", "mnc", "gut-associated", "lymphoid", "tissues", "21"], "article_id"=>696679, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g005", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Numbers_of_Wa_HRV_specific_ASC_per_5_10_5_MNC_obtained_from_gut_associated_lymphoid_tissues_Duodenum_Jejunum_Ileum_21_PID_/696679", "title"=>"Numbers of Wa HRV-specific ASC per 5×10<sup>5</sup> MNC obtained from gut-associated lymphoid tissues (Duodenum, Jejunum, Ileum) 21 PID.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052178"], "description"=>"<p>All animals were orally inoculated at 72 h of age [0 post inoculation day (0 PID)], and euthanized at 21±3 PID. SIC: small intestinal contents; and LIC: large intestinal contents, were collected after euthanasia. The arrow at 0 PID indicates the inoculation day.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "isotype-specific", "ab", "titers", "wa", "hrv", "elisa", "rectal", "swab", "fluids", "groups"], "article_id"=>696675, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Geometric_mean_isotype_specific_Ab_titers_GMT_to_Wa_HRV_per_group_per_day_from_ELISA_assay_detected_in_rectal_swab_fluids_of_the_experimental_groups_of_piglets_/696675", "title"=>"Geometric mean isotype-specific Ab titers (GMT) to Wa HRV per group per day (from ELISA assay) detected in rectal swab fluids of the experimental groups of piglets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052176"], "description"=>"<p>All animals were orally inoculated at 72 h of age [0 post inoculation day (0 PID)], and euthanized at 21±3 PID. SIC: small intestinal contents; and LIC: large intestinal contents, were collected after euthanasia. Horizontal bars represent the mean days of diarrhea duration for each group. The arrow at 0 PID indicates the inoculation day. The thin line indicates the duration of the passive treatments.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "titer", "ccif", "rectal", "swab", "fluids", "groups"], "article_id"=>696674, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g001", "stats"=>{"downloads"=>2, "page_views"=>38, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_titer_of_virus_shed_per_day_per_pig_from_CCIF_assay_detected_daily_in_rectal_swab_fluids_of_the_experimental_groups_of_piglets_/696674", "title"=>"Mean titer of virus shed per day per pig (from CCIF assay) detected daily in rectal swab fluids of the experimental groups of piglets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052186"], "description"=>"<p>Treatment Group abbreviations as well as passive treatments administered to each group of pigs are clarified in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003334#ppat-1003334-t001\" target=\"_blank\">Table 1</a>. VHH = piglets treated with VHH nanoAbs to VP6 at a final Wa HRV ELISA Ab titer of 4096; IgY = piglets treated with IgY Abs to VP6 at a final Wa HRV ELISA Ab titer of 4096; CL = piglets treated with control larvae; IgG = piglets treated with porcine IgG Abs to Wa HRV at a final Wa HRV ELISA Ab titer of 4096; NT = not treated piglets; n = number of animals per group; AUC = area under the curve. ND = not detected. PID = post inoculation day.</p>a<p>Determined by ELISA and CCIF.</p>b<p>Diarrhea duration was defined as the number of days with fecal score ≥2. Stool consistency was scored daily (0 = normal; 1 = pasty; 2 = semi-liquid; 3 = liquid).</p>c<p>Mean cumulative score was Σ(faecal scores ≥2)/number of animals. For statistical analysis, ND was considered as zero.</p>d<p>Proportions in the same column with different superscript upper case letters (A, B, C) differs significantly (Fisher's exact test, p<0.05).</p>e<p>Means in the same column with different superscript upper case letters differ significantly (Kruskall-Wallis rank sum test; p<0.05). Piglets were fed with 210 ml of sterile milk, twice a day, for 9 days with or without the addition of the corresponding volume of VP6 VHH pool, VP6 IgY pool, control larvae pool or Wa HRV porcine IgG pool, according to the experimental group.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "shedding", "gn", "piglets", "inoculation", "virhrv", "wa"], "article_id"=>696683, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.t002", "stats"=>{"downloads"=>2, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diarrhea_and_virus_shedding_in_Gn_piglets_after_oral_inoculation_with_VirHRV_Wa_P_8_G1_/696683", "title"=>"Diarrhea and virus shedding in Gn piglets after oral inoculation with VirHRV Wa (P[8]G1).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-02 01:51:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052185"], "description"=>"<p>A fourfold dilution of each VHH clone (3B2 VHH, derived from llamas vaccinated with VP6 from RVA strain C486 -G6P[1]I?-,or non-related VHH nanoAb) was mixed with an equal volume of RVA containing 100 focus forming units (FFU) of each strain. The numbers represent the minimum VHH concentration that reduced >80% of the number of fluorescent focus forming units (FFU) of each RVA strain. Neg = no neutralizing activity was observed at the highest concentration tested (62.50 µg VHH/ml). The G-type, P-type and I-type of RVA strains is clarified in brackets next to each strain name (according to <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003334#ppat.1003334-Matthijnssens4\" target=\"_blank\">[91]</a>).</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "rva", "fluorescent", "assay", "vhh"], "article_id"=>696682, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.t003", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_RVA_fluorescent_focus_reduction_assay_using_VHH_antibodies_/696682", "title"=>"<i>In vitro</i> RVA fluorescent focus reduction assay using VHH antibodies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-02 01:51:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052180"], "description"=>"<p>When comparing ASC numbers of the same isotype among treatment groups, different letters indicate a significant difference (Kruskal-Wallis rank sum test, p<0.05). n = number of piglets in each group. The IgM ASC response was not included as no IgM ASC were detected in most of the groups of pigs.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "wa", "hrv-specific", "asc", "mnc", "systemic", "lymphoid", "tissues", "mln", "draining", "intestine", "21"], "article_id"=>696677, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g004", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Numbers_of_Wa_HRV_specific_ASC_per_5_10_5_MNC_obtained_from_systemic_lymphoid_tissues_blood_and_spleen_and_MLN_draining_the_small_and_large_intestine_at_21_PID_/696677", "title"=>"Numbers of Wa HRV-specific ASC per 5×10<sup>5</sup> MNC obtained from systemic lymphoid tissues (blood and spleen) and MLN draining the small and large intestine at 21 PID.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/1052179"], "description"=>"<p>The isotype-specific and VN Abs to Wa HRV in serum samples were determined weekly by ELISA and VN assay. The arrow indicates the experimental inoculation with Wa HRV (0 PID). PID: post inoculation days.</p>", "links"=>[], "tags"=>["Infectious diseases", "Viral diseases", "Rotavirus infection", "hrv-specific", "porcine", "abs"], "article_id"=>696676, "categories"=>["Medicine"], "users"=>["Celina G. Vega", "Marina Bok", "Anastasia N. Vlasova", "Kuldeep S. Chattha", "Silvia Gómez-Sebastián", "Carmen Nuñez", "Carmen Alvarado", "Rodrigo Lasa", "José M. Escribano", "Lorena L. Garaicoechea", "Fernando Fernandez", "Karin Bok", "Andrés Wigdorovitz", "Linda J. Saif", "Viviana Parreño"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003334.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wa_HRV_specific_porcine_Abs_in_piglet_s_sera_/696676", "title"=>"Wa HRV-specific porcine Abs in piglet's sera.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-02 01:51:16"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"18", "full-text"=>"23", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"8"}
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  • {"unique-ip"=>"28", "full-text"=>"38", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"20", "full-text"=>"25", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
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  • {"unique-ip"=>"19", "full-text"=>"21", "pdf"=>"6", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
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  • {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"27", "full-text"=>"20", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
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Relative Metric

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