Vaccination Targeting a Surface Sialidase of P. acnes: Implication for New Treatment of Acne Vulgaris
- Publication Date
- February 06, 2008
- Journal
- PLOS ONE
- Authors
- Teruaki Nakatsuji, Yu Tsueng Liu, Cheng Po Huang, Richard L. Gallo, et al
- Volume
- 3
- Issue
- 2
- Pages
- e1551
- DOI
- https://dx.plos.org/10.1371/journal.pone.0001551
- Publisher URL
- http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0001551
- PubMed
- http://www.ncbi.nlm.nih.gov/pubmed/18253498
- PubMed Central
- http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2212713
- Europe PMC
- http://europepmc.org/abstract/MED/18253498
- Web of Science
- 000260535700022
- Scopus
- 45249113958
- Mendeley
- http://www.mendeley.com/research/vaccination-targeting-surface-sialidase-p-acnes-implication-new-treatment-acne-vulgaris
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Mendeley | Further Information
{"title"=>"Vaccination targeting a surface sialidase of P. acnes: Implication for new treatment of acne vulgaris", "type"=>"journal", "authors"=>[{"first_name"=>"Teruaki", "last_name"=>"Nakatsuji", "scopus_author_id"=>"23101032800"}, {"first_name"=>"Yu Tsueng", "last_name"=>"Liu", "scopus_author_id"=>"36071758200"}, {"first_name"=>"Cheng Po", "last_name"=>"Huang", "scopus_author_id"=>"35083564200"}, {"first_name"=>"Richard L.", "last_name"=>"Gallo", "scopus_author_id"=>"7201433211"}, {"first_name"=>"Chun Ming", "last_name"=>"Huang", "scopus_author_id"=>"55731250300"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-45249113958", "sgr"=>"45249113958", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0001551", "pmid"=>"18253498", "isbn"=>"1932-6203", "pui"=>"351836836"}, "id"=>"a8d5f4fb-431e-318f-9870-fd90035dc629", "abstract"=>"BackgroundAcne vulgaris afflicts more than fifty million people in the United State and the severity of this disorder is associated with the immune response to Propionibacterium acnes (P. acnes). Systemic therapies for acne target P. acnes using antibiotics, or target the follicle with retinoids such as isotretinoin. The latter systemic treatment is highly effective but also carries a risk of side effects including immune imbalance, hyperlipidemia, and teratogenicity. Despite substantial research into potential new therapies for this common disease, vaccines against acne vulgaris are not yet available.Methods and FindingsHere we create an acne vaccine targeting a cell wall-anchored sialidase of P. acnes. The importance of sialidase to disease pathogenesis is shown by treatment of a human sebocyte cell line with recombinant sialidase that increased susceptibility to P. acnes cytotoxicity and adhesion. Mice immunized with sialidase elicit a detectable antibody; the anti-sialidase serum effectively neutralized the cytotoxicity of P. acnes in vitro and P. acnes-induced interleukin-8 (IL-8) production in human sebocytes. Furthermore, the sialidase-immunized mice provided protective immunity against P. acnes in vivo as this treatment blocked an increase in ear thickness and release of pro-inflammatory macrophage inflammatory protein (MIP-2) cytokine.ConclusionsResults indicated that acne vaccines open novel therapeutic avenues for acne vulgaris and other P. acnes-associated diseases.", "link"=>"http://www.mendeley.com/research/vaccination-targeting-surface-sialidase-p-acnes-implication-new-treatment-acne-vulgaris", "reader_count"=>41, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Librarian"=>2, "Researcher"=>14, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>3, "Other"=>5, "Student > Master"=>5, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Librarian"=>2, "Researcher"=>14, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>3, "Other"=>5, "Student > Master"=>5, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>19, "Medicine and Dentistry"=>9, "Chemistry"=>2, "Social Sciences"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Colombia"=>2, "United States"=>1, "United Kingdom"=>1}, "group_count"=>1}CrossRef
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Scopus | Further Information
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Journal Comments | Further Information
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/c50d5f84-34be-459f-9af7-32fb0910fc01", "title"=>"Academic Editor comments: Holger Bruggemann", "body"=>"Academic editor's comments:\r\n\r\nReview of the original version of the manuscript:\r\nThe manuscript of Nakatsuji et al describes investigations on a sialidase of Propionibacterium acnes, and addresses its possible use as a vaccine for treatment of acne vulgaris. \r\n\r\nThe message of this work is clear and significant: anti-sialidase serum can attenuate P. acnes virulence, and sialidase-immunized mice can suppress P. acnes induced inflammation. I think that these results have the potential to open a new avenue of research against acne as well as against other P. acnes-associated diseases. As such, the paper and its results are of interest for a broad readership. \r\n\r\nAlthough the authors did a solid job and adhered to the standards for research conduct and the presentation of results, some concerns exist which have to be addressed: \r\n\r\n1. The mouse is a poor model for dermatologists, which was also mentioned in the manuscript (p22). P. acnes is usually not a resident of mice. Thus, special care has to be taken when drawing conclusions and conferring them to the human host. The authors examined ear swelling in mice. It was not clear from reading the manuscript why the authors chose that specific area in that animal model to observe effects of P. acnes and its sialidase. The mouse ear has certainly a cell type composition which cannot be compared to the situation of human hair follicles. \r\n\r\n2. Anti-sialidase serum was shown to have a significant effect in inhibiting P. acnes pathogenesis. But little information was given in the manuscript concerning the P. acnes sialidase protein or gene: for instance, it was not shown that the sialidase gene is expressed in vitro and /or in vivo. A simple Real-Time-PCR experiment could confirm the expression pattern, which would be of importance when evaluating the sialidase as a virulence factor of P. acnes. \r\n\r\n3. I found it not surprising that the authors could not detect any antibodies against sialidase in P. acnes-treated mice (p16, 2nd paragraph; p20, last paragraph): mice were vaccinated with heat-killed P. acnes. Thus, proteins of P. acnes were denatured during the heat treatment. The more important question is: what about acne patients? Do they produce antibodies against sialidase? It has been show that the serum of acne patients (as well as of healthy individuals) contains specific antibodies against P. acnes components. In this respect: what happens if mice are vaccinated with live or attenuated P. acnes? \r\n\r\n4. Two other genes can be found in the genome of P. acnes with similarities to sialidases (PPA0685, PPA0684). Did the authors check their functions as well? \r\n\r\n5. No experiments with a P. acnes sialidase negative mutant were performed. Such experiments would certainly be valuable and of benefit for the message of the paper. A sialidase negative P. acnes mutant should have a different virulence potential compared to the wild-type. Furthermore, a sialidase-overexpressing P. acnes strain could be created, which should have similar effects on sebocytes compared to effects on pre-treated sebocytes with recombinant sialidase. Please comment. \r\n\r\nMinor points: \r\n- p17, 2nd paragraph: special care should be taken when choosing appropriate controls. For instance, did the authors work with heat-killed P. acnes, with respect to the results as presented in figure 4? \r\n\r\n- p22: results are mixed with the discussion. The discussion section should be reorganized in order to clearly separate results and discussion.\r\n\r\nReview of the first revised manuscript:\r\nThe authors answered in detail to the comments of the reviewers. Additional experiments have been carried out which improved the manuscript significantly. \r\nA comment on the real-time PCR experiment: the level of siliadase gene expression seems very low, which has not been mentioned in the text. \r\nI did not understand why the authors performed \"serial dilutions of a pGEM-T Easy Vector containing the \r\nPCR product inserts to estimate the number of expressed genes.\" \r\nI thought that the sialidase transcript was compared to 16srRNA transcription.\r\n\r\n**********\r\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.", "isRemoved"=>false, "created"=>"2008-02-08T22:17:01Z", "lastModified"=>"2008-02-08T22:17:01Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001551", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-02-08T22:17:01Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/7681a583-dd66-41fd-a0b6-65c40617deae", "title"=>"Academic Editor comments: Holger Bruggemann", "body"=>"Academic editor's comments:\r\n\r\nReview of the original version of the manuscript:\r\n\r\nThe manuscript of Nakatsuji et al describes investigations on a sialidase of Propionibacterium acnes, and addresses its possible use as a vaccine for treatment of acne vulgaris. \r\n\r\nThe message of this work is clear and significant: anti-sialidase serum can attenuate P. acnes virulence, and sialidase-immunized mice can suppress P. acnes induced inflammation. I think that these results have the potential to open a new avenue of research against acne as well as against other P. acnes-associated diseases. As such, the paper and its results are of interest for a broad readership.\r\n\r\nAlthough the authors did a solid job and adhered to the standards for research conduct and the presentation of results, some concerns exist which have to be addressed: \r\n\r\n1. The mouse is a poor model for dermatologists, which was also mentioned in the manuscript (p22). P. acnes is usually not a resident of mice. Thus, special care has to be taken when drawing conclusions and conferring them to the human host. The authors examined ear swelling in mice. It was not clear from reading the manuscript why the authors chose that specific area in that animal model to observe effects of P. acnes and its sialidase. The mouse ear has certainly a cell type composition which cannot be compared to the situation of human hair follicles. \r\n\r\n2. Anti-sialidase serum was shown to have a significant effect in inhibiting P. acnes pathogenesis. But little information was given in the manuscript concerning the P. acnes sialidase protein or gene: for instance, it was not shown that the sialidase gene is expressed in vitro and /or in vivo. A simple Real-Time-PCR experiment could confirm the expression pattern, which would be of importance when evaluating the sialidase as a virulence factor of P. acnes. \r\n\r\n3. I found it not surprising that the authors could not detect any antibodies against sialidase in P. acnes-treated mice (p16, 2nd paragraph; p20, last paragraph): mice were vaccinated with heat-killed P. acnes. Thus, proteins of P. acnes were denatured during the heat treatment. The more important question is: what about acne patients? Do they produce antibodies against sialidase? It has been show that the serum of acne patients (as well as of healthy individuals) contains specific antibodies against P. acnes components. In this respect: what happens if mice are vaccinated with live or attenuated P. acnes? \r\n\r\n4. Two other genes can be found in the genome of P. acnes with similarities to sialidases (PPA0685, PPA0684). Did the authors check their functions as well? \r\n\r\n5. No experiments with a P. acnes sialidase negative mutant were performed. Such experiments would certainly be valuable and of benefit for the message of the paper. A sialidase negative P. acnes mutant should have a different virulence potential compared to the wild-type. Furthermore, a sialidase-overexpressing P. acnes strain could be created, which should have similar effects on sebocytes compared to effects on pre-treated sebocytes with recombinant sialidase. Please comment. \r\n\r\nMinor points: \r\n- p17, 2nd paragraph: special care should be taken when choosing appropriate controls. For instance, did the authors work with heat-killed P. acnes, with respect to the results as presented in figure 4? \r\n\r\n- p22: results are mixed with the discussion. The discussion section should be reorganized in order to clearly separate results and discussion.\r\n\r\nReview of the first revised manuscript:\r\n\r\nThe authors answered in detail to the comments of the reviewers. Additional experiments have been carried out which improved the manuscript significantly. \r\nA comment on the real-time PCR experiment: the level of siliadase gene expression seems very low, which has not been mentioned in the text. \r\nI did not understand why the authors performed \"serial dilutions of a pGEM-T Easy Vector containing the \r\nPCR product inserts to estimate the number of expressed genes.\" \r\nI thought that the sialidase transcript was compared to 16srRNA transcription.\r\n\r\n**********\r\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.", "isRemoved"=>false, "created"=>"2008-02-08T22:26:15Z", "lastModified"=>"2008-02-08T22:26:15Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001551", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-02-08T22:26:15Z", "replies"=>[]}
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- {"month"=>"2", "year"=>"2012", "pdf_views"=>"14", "xml_views"=>"1", "html_views"=>"84"}
- {"month"=>"3", "year"=>"2012", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"4", "year"=>"2012", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"74"}
- {"month"=>"5", "year"=>"2012", "pdf_views"=>"17", "xml_views"=>"0", "html_views"=>"81"}
- {"month"=>"6", "year"=>"2012", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"44"}
- {"month"=>"7", "year"=>"2012", "pdf_views"=>"11", "xml_views"=>"1", "html_views"=>"70"}
- {"month"=>"8", "year"=>"2012", "pdf_views"=>"11", "xml_views"=>"5", "html_views"=>"37"}
- {"month"=>"9", "year"=>"2012", "pdf_views"=>"29", "xml_views"=>"0", "html_views"=>"91"}
- {"month"=>"10", "year"=>"2012", "pdf_views"=>"15", "xml_views"=>"0", "html_views"=>"73"}
- {"month"=>"11", "year"=>"2012", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"74"}
- {"month"=>"12", "year"=>"2012", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"65"}
- {"month"=>"1", "year"=>"2013", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"2", "year"=>"2013", "pdf_views"=>"10", "xml_views"=>"3", "html_views"=>"54"}
- {"month"=>"3", "year"=>"2013", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"56"}
- {"month"=>"4", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"32"}
- {"month"=>"5", "year"=>"2013", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"67"}
- {"month"=>"6", "year"=>"2013", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"57"}
- {"month"=>"7", "year"=>"2013", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"8", "year"=>"2013", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"42"}
- {"month"=>"9", "year"=>"2013", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"44"}
- {"month"=>"10", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"109"}
- {"month"=>"11", "year"=>"2013", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"41"}
- {"month"=>"12", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"71"}
- {"month"=>"1", "year"=>"2014", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"49"}
- {"month"=>"2", "year"=>"2014", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"62"}
- {"month"=>"3", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"95"}
- {"month"=>"4", "year"=>"2014", "pdf_views"=>"10", "xml_views"=>"1", "html_views"=>"102"}
- {"month"=>"5", "year"=>"2014", "pdf_views"=>"14", "xml_views"=>"1", "html_views"=>"95"}
- {"month"=>"6", "year"=>"2014", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"90"}
- {"month"=>"7", "year"=>"2014", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"104"}
- {"month"=>"8", "year"=>"2014", "pdf_views"=>"3", "xml_views"=>"2", "html_views"=>"50"}
- {"month"=>"9", "year"=>"2014", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"82"}
- {"month"=>"10", "year"=>"2014", "pdf_views"=>"10", "xml_views"=>"2", "html_views"=>"126"}
- {"month"=>"11", "year"=>"2014", "pdf_views"=>"14", "xml_views"=>"1", "html_views"=>"87"}
- {"month"=>"12", "year"=>"2014", "pdf_views"=>"10", "xml_views"=>"2", "html_views"=>"67"}
- {"month"=>"1", "year"=>"2015", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"38"}
- {"month"=>"2", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"58"}
- {"month"=>"3", "year"=>"2015", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"4", "year"=>"2015", "pdf_views"=>"10", "xml_views"=>"1", "html_views"=>"47"}
- {"month"=>"5", "year"=>"2015", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"36"}
- {"month"=>"6", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"36"}
- {"month"=>"7", "year"=>"2015", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"48"}
- {"month"=>"8", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"46"}
- {"month"=>"9", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"67"}
- {"month"=>"10", "year"=>"2015", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"65"}
- {"month"=>"11", "year"=>"2015", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"53"}
- {"month"=>"12", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"75"}
- {"month"=>"1", "year"=>"2016", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"63"}
- {"month"=>"2", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"3", "year"=>"2016", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"69"}
- {"month"=>"4", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"45"}
- {"month"=>"5", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"27"}
- {"month"=>"6", "year"=>"2016", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"7", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"30"}
- {"month"=>"8", "year"=>"2016", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"43"}
- {"month"=>"9", "year"=>"2016", "pdf_views"=>"20", "xml_views"=>"0", "html_views"=>"53"}
- {"month"=>"10", "year"=>"2016", "pdf_views"=>"19", "xml_views"=>"0", "html_views"=>"56"}
- {"month"=>"11", "year"=>"2016", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"41"}
- {"month"=>"12", "year"=>"2016", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"39"}
- {"month"=>"1", "year"=>"2017", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"44"}
- {"month"=>"2", "year"=>"2017", "pdf_views"=>"9", "xml_views"=>"1", "html_views"=>"54"}
- {"month"=>"3", "year"=>"2017", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"55"}
- {"month"=>"4", "year"=>"2017", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"204"}
- {"month"=>"5", "year"=>"2017", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"276"}
- {"month"=>"6", "year"=>"2017", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"250"}
- {"month"=>"7", "year"=>"2017", "pdf_views"=>"10", "xml_views"=>"2", "html_views"=>"288"}
- {"month"=>"8", "year"=>"2017", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"185"}
- {"month"=>"9", "year"=>"2017", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"164"}
- {"month"=>"10", "year"=>"2017", "pdf_views"=>"11", "xml_views"=>"2", "html_views"=>"150"}
- {"month"=>"11", "year"=>"2017", "pdf_views"=>"14", "xml_views"=>"2", "html_views"=>"137"}
- {"month"=>"12", "year"=>"2017", "pdf_views"=>"4", "xml_views"=>"3", "html_views"=>"108"}
- {"month"=>"1", "year"=>"2018", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"77"}
- {"month"=>"2", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"3", "year"=>"2018", "pdf_views"=>"11", "xml_views"=>"4", "html_views"=>"40"}
- {"month"=>"4", "year"=>"2018", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"26"}
- {"month"=>"5", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"14"}
- {"month"=>"6", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"15"}
- {"month"=>"7", "year"=>"2018", "pdf_views"=>"13", "xml_views"=>"3", "html_views"=>"22"}
- {"month"=>"8", "year"=>"2018", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"21"}
- {"month"=>"9", "year"=>"2018", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"10", "year"=>"2018", "pdf_views"=>"10", "xml_views"=>"1", "html_views"=>"59"}
- {"month"=>"11", "year"=>"2018", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"33"}
- {"month"=>"12", "year"=>"2018", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"1", "year"=>"2019", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"2", "year"=>"2019", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"3", "year"=>"2019", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"4", "year"=>"2019", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"5", "year"=>"2019", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"15"}
- {"month"=>"6", "year"=>"2019", "pdf_views"=>"27", "xml_views"=>"1", "html_views"=>"11"}
- {"month"=>"7", "year"=>"2019", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"18"}
- {"month"=>"8", "year"=>"2019", "pdf_views"=>"9", "xml_views"=>"1", "html_views"=>"18"}
- {"month"=>"9", "year"=>"2019", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"10", "year"=>"2019", "pdf_views"=>"15", "xml_views"=>"0", "html_views"=>"9"}
- {"month"=>"11", "year"=>"2019", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"9"}
- {"month"=>"12", "year"=>"2019", "pdf_views"=>"13", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"1", "year"=>"2020", "pdf_views"=>"12", "xml_views"=>"2", "html_views"=>"15"}
- {"month"=>"2", "year"=>"2020", "pdf_views"=>"16", "xml_views"=>"1", "html_views"=>"14"}
- {"month"=>"3", "year"=>"2020", "pdf_views"=>"61", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"4", "year"=>"2020", "pdf_views"=>"21", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"5", "year"=>"2020", "pdf_views"=>"21", "xml_views"=>"1", "html_views"=>"9"}
- {"month"=>"6", "year"=>"2020", "pdf_views"=>"17", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"7", "year"=>"2020", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"22"}
- {"month"=>"8", "year"=>"2020", "pdf_views"=>"11", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"9", "year"=>"2020", "pdf_views"=>"11", "xml_views"=>"1", "html_views"=>"19"}
- {"month"=>"10", "year"=>"2020", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"11", "year"=>"2020", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"12", "year"=>"2020", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"12"}
- {"month"=>"1", "year"=>"2021", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"13"}
PMC Usage Stats | Further Information
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"43", "year"=>"2010", "pdf"=>"15", "unique-ip"=>"35", "figure"=>"6", "scanned-summary"=>"0", "supp-data"=>"1"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"39", "unique-ip"=>"42", "pdf"=>"20", "year"=>"2010", "figure"=>"44", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"35", "year"=>"2010", "pdf"=>"27", "unique-ip"=>"40", "figure"=>"35", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"25", "unique-ip"=>"28", "pdf"=>"15", "year"=>"2010", "figure"=>"58", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"5", "full-text"=>"34", "year"=>"2010", "pdf"=>"16", "unique-ip"=>"29", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"25", "unique-ip"=>"20", "pdf"=>"7", "year"=>"2010", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"1"}
- {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"18", "year"=>"2010", "pdf"=>"17", "unique-ip"=>"27", "figure"=>"15", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"8", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"19", "unique-ip"=>"20", "pdf"=>"16", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"2"}
- {"month"=>"9", "scanned-page-browse"=>"0", "cited-by"=>"2", "abstract"=>"8", "full-text"=>"22", "year"=>"2010", "pdf"=>"10", "unique-ip"=>"36", "figure"=>"22", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"10", "cited-by"=>"1", "abstract"=>"9", "full-text"=>"20", "unique-ip"=>"46", "pdf"=>"8", "year"=>"2010", "figure"=>"41", "scanned-summary"=>"0", "supp-data"=>"1"}
- {"month"=>"11", "scanned-page-browse"=>"0", "cited-by"=>"2", "abstract"=>"1", "full-text"=>"20", "year"=>"2010", "pdf"=>"13", "unique-ip"=>"21", "figure"=>"10", "scanned-summary"=>"0", "supp-data"=>"2"}
- {"scanned-page-browse"=>"0", "month"=>"12", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"15", "unique-ip"=>"20", "pdf"=>"15", "year"=>"2010", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"20", "year"=>"2011", "pdf"=>"16", "unique-ip"=>"26", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"1", "abstract"=>"2", "full-text"=>"15", "unique-ip"=>"23", "pdf"=>"8", "year"=>"2011", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"23", "year"=>"2011", "pdf"=>"13", "unique-ip"=>"26", "figure"=>"8", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"14", "unique-ip"=>"29", "pdf"=>"9", "year"=>"2011", "figure"=>"27", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"6", "full-text"=>"14", "year"=>"2011", "pdf"=>"11", "unique-ip"=>"24", "figure"=>"9", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"12", "unique-ip"=>"14", "pdf"=>"7", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"14", "year"=>"2011", "pdf"=>"6", "unique-ip"=>"15", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"8", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"6", "unique-ip"=>"14", "pdf"=>"1", "year"=>"2011", "figure"=>"8", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"9", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"28", "year"=>"2011", "pdf"=>"13", "unique-ip"=>"27", "figure"=>"6", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"10", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"17", "unique-ip"=>"22", "pdf"=>"6", "year"=>"2011", "figure"=>"6", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"11", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"28", "year"=>"2011", "pdf"=>"11", "unique-ip"=>"23", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"12", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "unique-ip"=>"14", "pdf"=>"7", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "year"=>"2012", "pdf"=>"2", "unique-ip"=>"11", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"14", "unique-ip"=>"16", "pdf"=>"8", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"25", "year"=>"2012", "pdf"=>"10", "unique-ip"=>"25", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "unique-ip"=>"7", "pdf"=>"3", "year"=>"2012", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"21", "year"=>"2012", "pdf"=>"10", "unique-ip"=>"15", "figure"=>"8", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"90", "month"=>"2", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"11", "unique-ip"=>"10", "pdf"=>"5", "year"=>"2008", "figure"=>"268", "scanned-summary"=>"152", "supp-data"=>"146"}
- {"month"=>"3", "scanned-page-browse"=>"59", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"1", "year"=>"2008", "pdf"=>"10", "unique-ip"=>"30", "figure"=>"243", "scanned-summary"=>"143", "supp-data"=>"116"}
- {"scanned-page-browse"=>"51", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"7", "unique-ip"=>"4", "pdf"=>"0", "year"=>"2008", "figure"=>"148", "scanned-summary"=>"86", "supp-data"=>"92"}
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Relative Metric
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