Is Exercise Protective Against Influenza-Associated Mortality?
- Publication Date
- May 07, 2008
- Journal
- PLOS ONE
- Authors
- Chit Ming Wong, Hak Kan Lai, Chun Quan Ou, Sai Yin Ho, et al
- Volume
- 3
- Issue
- 5
- Pages
- e2108
- DOI
- https://dx.plos.org/10.1371/journal.pone.0002108
- Publisher URL
- http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0002108
- PubMed
- http://www.ncbi.nlm.nih.gov/pubmed/18461130
- PubMed Central
- http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2329855
- Europe PMC
- http://europepmc.org/abstract/MED/18461130
- Web of Science
- 000261642400030
- Scopus
- 47749126612
- Mendeley
- http://www.mendeley.com/research/exercise-protective-against-influenzaassociated-mortality
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Mendeley | Further Information
{"title"=>"Is exercise protective against influenza-associated mortality?", "type"=>"journal", "authors"=>[{"first_name"=>"Chit Ming", "last_name"=>"Wong", "scopus_author_id"=>"7404954904"}, {"first_name"=>"Hak Kan", "last_name"=>"Lai", "scopus_author_id"=>"11739685900"}, {"first_name"=>"Chun Quan", "last_name"=>"Ou", "scopus_author_id"=>"14070561800"}, {"first_name"=>"Sai Yin", "last_name"=>"Ho", "scopus_author_id"=>"7403716884"}, {"first_name"=>"King Pan", "last_name"=>"Chan", "scopus_author_id"=>"56939574800"}, {"first_name"=>"Thuan Quoc", "last_name"=>"Thach", "scopus_author_id"=>"6602850066"}, {"first_name"=>"Lin", "last_name"=>"Yang", "scopus_author_id"=>"55732928800"}, {"first_name"=>"Yuen Kwan", "last_name"=>"Chau", "scopus_author_id"=>"16300609300"}, {"first_name"=>"Tai Hing", "last_name"=>"Lam", "scopus_author_id"=>"7202522876"}, {"first_name"=>"Anthony Johnson", "last_name"=>"Hedley", "scopus_author_id"=>"7102584095"}, {"first_name"=>"Joseph Sriyal Malik", "last_name"=>"Peiris", "scopus_author_id"=>"7005486823"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"352025090", "pmid"=>"18461130", "doi"=>"10.1371/journal.pone.0002108", "scopus"=>"2-s2.0-47749126612", "isbn"=>"1932-6203 (Electronic)", "issn"=>"19326203", "sgr"=>"47749126612"}, "id"=>"fce39f49-3549-37a8-8815-b42784cb39dc", "abstract"=>"BACKGROUND: Little is known about the effect of physical exercise on influenza-associated mortality. METHODS AND FINDINGS: We collected information about exercise habits and other lifestyles, and socioeconomic and demographic status, the underlying cause of death of 24,656 adults (21% aged 30-64, 79% aged 65 or above) who died in 1998 in Hong Kong, and the weekly proportion of specimens positive for influenza A (H3N1 and H1N1) and B isolations during the same period. We assessed the excess risks (ER) of influenza-associated mortality due to all-natural causes, cardiovascular diseases, or respiratory disease among different levels of exercise: never/seldom (less than once per month), low/moderate (once per month to three times per week), and frequent (four times or more per week) by Poisson regression. We also assessed the differences in ER between exercise groups by case-only logistic regression. For all the mortality outcomes under study in relation to each 10% increase in weekly proportion of specimens positive for influenza A+B, never/seldom exercise (as reference) was associated with 5.8% to 8.5% excess risks (ER) of mortality (P<0.0001), while low/moderate exercise was associated with ER which were 4.2% to 6.4% lower than those of the reference (P<0.001 for all-natural causes; P = 0.001 for cardiovascular; and P = 0.07 for respiratory mortality). Frequent exercise was not different from the reference (change in ER -0.8% to 1.7%, P = 0.30 to 0.73). CONCLUSION: When compared with never or seldom exercise, exercising at low to moderate frequency is beneficial with lower influenza-associated mortality.", "link"=>"http://www.mendeley.com/research/exercise-protective-against-influenzaassociated-mortality", "reader_count"=>26, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>1, "Researcher"=>11, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>1, "Researcher"=>11, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Materials Science"=>1, "Mathematics"=>1, "Medicine and Dentistry"=>8, "Agricultural and Biological Sciences"=>8, "Neuroscience"=>1, "Sports and Recreations"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Neuroscience"=>{"Neuroscience"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Hong Kong"=>1, "United States"=>1, "Brazil"=>1, "Spain"=>1, "India"=>1, "French Polynesia"=>1}, "group_count"=>0}CrossRef
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Scopus | Further Information
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Journal Comments | Further Information
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/aae74948-1a2d-4401-af49-6b127e5fabaa", "title"=>"Referee Comments: Referee 3 (Eduardo Azziz-Baumgartner)", "body"=>"Referee 3's review (Eduardo Azziz-Baumgartner):\n\n**********\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.\n**********\n\nThe Wong et al manuscript is very interesting and would make a good addition to the literature with minor revisions. Below are a few suggestions to the authors:\n\n1. The abstract should be clearer and use parallel text to that of the main body of the manuscript. Authors should also attempt to change most sentences to active voice for clarity. There are several run-on sentences, colloquialisms, and dangling modifiers that could use editing to clarify findings.\n\n2. Authors should briefly provide details about the LIMOR study as readers will require this information to contextualize the data. Although the LIMOR study is referenced, I was distracted by the lack of information about the parent study.\n\n3. The authors indicated that questions about physical exercise date to a time period \"about ten years before their death.\" I did not understand if authors meant that informants were asked about decedents exercise habits during the ten years prior to their death (a ten year history) or about decedents exercise habits ten years prior to the death (as a cross-sectional view or snapshot ten years prior). I suspect from the data analysis that authors asked about exercise during the past ten years but they should state explicitly the actual language used during the interviews.\n\n4. I was unclear as to the exact variables that went into the logistic models as this is not the typical Boolean model of dead/alive = α + β1(E) + β2(smoking) + etc. Stating the explicit models used may clarify the analyses.\n\n5. I was distracted by the use of the terms \"risk\" during the odds ratio discussion and \"sensitivity\" during in the first paragraph of the section called \"Statistical Analysis\", subsection \"Influenza epidemic.\" I would suggest that authors use alternate terms for precision.\n\n6. I really liked the authors' attempts to account for a variety of potential interaction terms. Was there any data available on decedent's influenza vaccination status during the year of their death?\n\n7. I am concerned about the authors' suggestion that people older than 65 years may need to exercise less than frequently. While the findings are compelling, there are many potential confounders that have not been examined (e.g. vaccination status, etc.). I would more comfortable if the discussion section acknowledge the limitations of the analyses, the need for further studies, and the complexity of the risk/benefit of exercise as well as the need for increasing vaccination coverage. It would make more sense to me to see the authors recommend moderate exercise coupled with increase vaccination coverage.\n\n8. While it is interesting to see the authors first time use of population based data, I would encouraged them to explicitly state that the decedents are not linked to influenza sampling early in the manuscript. In addition, they should discuss the inherent limitations of mortality data de-linked from individual influenza sample data.\n\n9. I would recommend that authors consider deleting part 'a\" of table 1 as this data is also presented as figure 1. I am uncertain of the origin of the p values in section \"c\" of table 1 as it would seem that Chi squares would originate from bivariate analyses. Some of these comparisons would seem more appropriate for ANOVAs or something akin to them. Disaggregating the findings of E1 and E2 may also help. Clarifying what is being compared may help. It is also difficult to visualize the difference between E1 and E2 in Figure 2. I would also recommend deleting appendix 1 as it seems unnecessary.\n\n10. I do not understand why influenza intensity was presented \"as a percentage per 10% increase of influenza.\" It would seem that these regression models could use influenza intensity as a continuous independent variable.\n\n11. The first sentence of the second paragraph of the discussion section seems awkward.\n\n12. The third paragraph suggests that the interaction between exercise and immune function is clearly understood (i.e. \"can be explained...\"). I would suggest the use of more cautious language. While many in-roads have been made on this subject, there is much about causality that needs to be learned.\n\nGood work and good luck with the revisions.", "isRemoved"=>false, "created"=>"2008-05-12T17:56:27Z", "lastModified"=>"2008-05-12T17:56:27Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002108", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>1, "mostRecentActivity"=>"2008-05-19T02:47:48Z", "replies"=>[{"type"=>"REPLY", "parentID"=>15301, "annotationUri"=>"info:doi/10.1371/reply/9ad22cd3-dbde-4c55-9f57-94ac0d85db0e", "title"=>"RE: Referee Comments: Referee 3 (Eduardo Azziz-Baumgartner)", "body"=>"REPLY to 1: We have now modified the styles and used active voices in many sentences, and have revised the texts according to the reviewer’s suggestions.\r\n\r\nREPLY to 2: We have now included details about LIMOR study. (See Introduction 2nd paragraph, Method 1st and 5th paragraph)\r\n\r\nREPLY to 3: We were assessing the decedent’s exercise habits ten years before their death (i.e. around the year in 1988) by asking the decedents’ close relatives. This is a cross-sectional view ten years prior to death rather than a ten-year history of exercise habit. We chose to ask about the habit ten years before death to avoid any change in habits as a result of any disease development that eventually led to death. This is to minimize the possibility of reverse causation. We have now stated explicitly the actual language used during the interviews. (See Method 1st and 5th paragraph) \r\n\t\r\nREPLY to 4: In a stratified subset of data for assessment of excess mortality due to influenza intensity in exercise sub-groups, we used Poisson regression with daily number of deaths as the dependent variable and time varying covariates as independent variables to control for time trend and seasonality, and time varying confounding. As all the subjects were deceased persons, we did not use the model for dead/alive. But instead we modeled the variations of daily number of deaths with variations in influenza intensity. We then modeled the difference in excess mortality between exercise groups by means of case only logistic regression in the combined dataset. This was done by using logistic regression with logit function of exercise status as the dependent variable and influenza intensity variable together with confounding variables for individual subjects as the independent variables. The coefficient corresponding to the influenza intensity variable is used to assess interaction between effects of exercise and influenza (or interpreted as the difference in excess mortality between exercise groups). We have now stated the models explicitly. (See Method 6th and 7th paragraph).\r\n\r\nREPLY to 5: We have now modified the term “risk” to “odds” and deleted “sensitivity” in that sentence appropriately.\r\n\r\nREPLY to 6: We have looked at the availability of such data but it was not reported elsewhere in 1998 and before. Influenza vaccination became more available to the general public only after 2000 particularly after the SARS epidemic in Hong Kong. It was not a free vaccine available to the elderly before 1998. We have adjusted for most potential covariates (which are equivalent to interaction variables in case only logistic regression) available to use for the analysis.\r\n\r\nREPLY to 7: We have revised and explicitly stated clearly that our findings suggest that older people are recommended to do moderate exercise during influenza epidemics and do not suggest that they can ignore the potential benefit of vaccination. We clarified that doing more exercises under normal circumstances may be beneficial.\r\n\r\nREPLY to 8: We have now explicitly stated that the analysis was based on a database of a large case-control study of lifestyle and mortality (LIMOR study) in 1998 and ANOTHER database of influenza activity during the same period. (SEE Introduction 2nd paragraph)\r\n\r\n\r\nREPLY to 9: We have deleted ‘table 1a’ as suggested. We have also checked again our Chi-square tests that they were properly carried out. We have also made it clear that each p-value is resulted from the Chi-square test of a 2x3 table. We would use ANOVA if we were comparing continuous variables between two or more groups.\r\n\r\nREPLY to 10: Yes, influenza intensity is a continuous variable defined as the proportion of specimens positive for influenza isolates. In 1998, the mean influenza intensity was 10%, we therefore presented the excess risk of mortality per 10% increase. In our previous publications on the health impact of influenza we also presented the excess risk in term of per 10% increase. Thus presenting these results in the same way would enhance the readability of the estimates.\r\n\r\nREPLY to 11: We have now re-phrased it.\r\n\r\nREPLY to 12: We have now re-phrased it.\r\n\r\n\r\nThanks for reviewed our paper and provided your valuable comments.\r\n\r\nBest wishes,\r\nWong CM et al\r\n", "isRemoved"=>false, "created"=>"2008-05-19T02:47:48Z", "lastModified"=>"2008-05-19T02:47:48Z", "creator"=>{"userId"=>"162675"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002108", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-05-19T02:47:48Z", "replies"=>[]}]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/6a743428-8b92-4db9-99c3-0e4bf9bd1093", "title"=>"Referee Comments: Referee 4 (David Blazes)", "body"=>"Referee 4's review (David Blazes):\n\n**********\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.\n**********\n\nThis manuscript attempts to make a correlation between exercise and influenza associated mortality. While this is an interesting concept, there are serious methodologic flaws that limit the ability of this paper to address the issue at hand with scientific rigor.\nThe following issues limit the validity of the paper:\n\n(1) The hypothesis was not clearly stated and the paper at times does not agree with itself it terms of objectives - at times the authors state they will only examine the mortality in patients over 65 (pg.3), but then present data on over 30 year olds as well.\n\n(2) The underlying study from which the data was derived is not explained in detail, and almost certainly was not designed to look at mortality due to influenza - thus making suppositions based on this data is questionable - the results may have occured by chance.\n\n(3) Linking deaths to influenza just because they occur during an epidemic period is questionable logic - there are likely other confounding variables, even simply being exposed to more people during exercise.\n\n(4) The recall bias of proxies for something such as exercise is very limited, and likely invalid, especially after 10 years. Most people exercise individually.\n\n(5) The interpretation of exercise as immunomodulatory is overstated. Certainly, running a marathon affects the immune system, but 30 minutes of routine exercise as practiced by most of the population would not affect it in the same manner. The suggestion to limit exercise in populations at risk for coronary and other preventable diseases is dangerous.\n\nOverall, I think this manuscript includes many assumptions and suppositions that taken together limit the value of the conclusions that have been drawn from the data.", "isRemoved"=>false, "created"=>"2008-05-12T17:58:43Z", "lastModified"=>"2008-05-12T17:58:43Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002108", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>1, "mostRecentActivity"=>"2008-05-19T03:05:50Z", "replies"=>[{"type"=>"REPLY", "parentID"=>9823, "annotationUri"=>"info:doi/10.1371/reply/7401b5b1-ca48-401a-9d38-66c86a73ffa4", "title"=>"RE: Referee Comments: Referee 4 (David Blazes)", "body"=>"REPLY to (1): We have now stated the hypothesis as follows: “exercise frequency affects the susceptibility of an adult population (aged 30+) and its majority older subgroup (aged 65+, accounting for 79% of the total) to the activity of influenza viruses in terms of influenza-associated mortality” Thus we presented both 30+ and 65+ age groups.. (See Introduction 2nd paragraph)\r\n\r\n\r\nREPLY to (2): We have now included the details about the original study i.e. LIMOR study. (See Introduction 2nd paragraph, Method 1st and 5th paragraph). The reviewer is right to point out that the design of the original study (i.e. the LIMOR study) was not for assessing influenza-associated mortality. However, this is a population database with comprehensive data on personal lifestyles, and socio-economic and health status of the individuals. It is a unique and ideal database for assessment of effects of personal and environmental factors interactions. We have several publications on interaction between personal factors including exercise, smoking and socio-economic factor by air pollution interaction. We are now moving towards assessment for interaction between personal factors and influenza as a research area for individual susceptibility to environmental risk factors. We have the same concern on whether our results are just chance findings or not. We therefore performed the analysis with two measures of influenza (epidemic and intensity), different disease outcomes (all-cause mortality, and cardiovascular and respiratory mortality), and age groups (30+ and 65+). We also performed a series of sensitivity analyses with control for confounding factors. Our results are consistent throughout all of our analyses. We believe the results are unlikely to be due to chance alone.\r\n\r\n\r\nREPLY to (3): We agree with the reviewer that linking deaths to influenza just because they occur during an epidemic period with the lack of a direct diagnosis to confirm influenza as a cause of death would be subject to other confounding variables. During the influenza epidemic period there may be other factors which affect one’s susceptibility to death. However the method we used for this study assesses the mortality risk of the subjects after exposure to influenza viruses for short period of time. The results are therefore robust to the confounding factors of subjects as they do not change over short period of time. Nevertheless in this study we also controlled for all identified personal confounding factors. \r\n\r\nIn our study, influenza epidemic is one of two measures for influenza activity. We also used influenza intensity as the other measure. In analysis for influenza intensity we controlled for all possible time varying confounding factors including temperature and humidity. These would minimize the chance of obtaining confounded results. With regard to the situation the reviewer raised that a subject may be more exposed during exercise, then this would probably increase than reduce the influenza-associated mortality risk. As we found that moderate exercise is related to reduced risk of influenza-associated mortality, such situation would not have occurred.\r\n\r\nHowever it is necessary to conduct further study to confirm our results by means of alternative study design such as a cohort study. On the other hand our results obtained in this study would provide the evidence to generate hypotheses for further studies. (See Discussion last paragraph)\r\n\r\n\r\nREPLY to (4): We were assessing the decedents’ exercise habits ten years before their death (around the year in 1988) by asking a close relative of the decedents. We chose this to avoid any change in the habits during development of the disease that eventually caused death, to minimize reverse causation. (See Method 1st and 5th paragraph). We also confirmed that the recall error was within an acceptable level by means of a reliability check with repeated interviews which were conducted by telephone on a random sample of 235 cases about 3 weeks on average after the initial interview. The percentage agreement for exercise frequency categorization was satisfactory (73%) (See Discussion last paragraph). \r\n\r\n\r\nREPLY to (5): We have now revised the statements so as to be cautious, and have stated clearly and explicitly that our results may only apply particularly for older people during influenza epidemics. We clarify that we agree with a policy which encourages doing more exercise under normal circumstances. We have also recommended increasing vaccination coverage as well as doing moderate exercise during influenza epidemic periods. On the other hand doing exercise during influenza epidemics for more than three times per week, each lasts longer than 30 minutes may not be advisable for the older population. \r\n\r\n\r\nREVIEWER:\r\n”Overall, I think this manuscript includes many assumptions and suppositions that taken together limit the value of the conclusions that have been drawn from the data.”\r\n\r\nREPLY: We have extensively modified the manuscript after taking into account the reviewer’s comments. In addition we have revised our discussion, pointing out that the U-shaped relationships shown in this study is consistent with those found in our recently published paper on air pollution associated mortality and levels of exercise (Wong CM et al 2007;44:386-392). In the discussion we also point out that for relationships between mortality and exercise levels in Lam et al (2004;14:391-398) which did not put influenza and air pollution in the assessment, such U-shaped patterns were not found, supporting specificity for such U-shaped relationships. We are confident that this manuscript would provide an interesting and useful addition to the literature. \r\n\r\nThanks for reviewed our paper and provided valuable comments.\r\n\r\nBest wishes,\r\nWong CM et al\r\n", "isRemoved"=>false, "created"=>"2008-05-19T03:05:50Z", "lastModified"=>"2008-05-19T03:05:50Z", "creator"=>{"userId"=>"162675"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002108", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-05-19T03:05:50Z", "replies"=>[]}]}
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- {"month"=>"7", "year"=>"2008", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"53"}
- {"month"=>"8", "year"=>"2008", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"44"}
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- {"month"=>"2", "year"=>"2009", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"67"}
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- {"month"=>"4", "year"=>"2009", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"5", "year"=>"2009", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"36"}
- {"month"=>"6", "year"=>"2009", "pdf_views"=>"8", "xml_views"=>"1", "html_views"=>"40"}
- {"month"=>"7", "year"=>"2009", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"34"}
- {"month"=>"8", "year"=>"2009", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"53"}
- {"month"=>"9", "year"=>"2009", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"38"}
- {"month"=>"10", "year"=>"2009", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"51"}
- {"month"=>"11", "year"=>"2009", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"46"}
- {"month"=>"12", "year"=>"2009", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"24"}
- {"month"=>"1", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"49"}
- {"month"=>"2", "year"=>"2010", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"32"}
- {"month"=>"3", "year"=>"2010", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"33"}
- {"month"=>"4", "year"=>"2010", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"29"}
- {"month"=>"5", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"32"}
- {"month"=>"6", "year"=>"2010", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"7", "year"=>"2010", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"56"}
- {"month"=>"8", "year"=>"2010", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"194"}
- {"month"=>"9", "year"=>"2010", "pdf_views"=>"1", "xml_views"=>"1", "html_views"=>"16"}
- {"month"=>"10", "year"=>"2010", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"33"}
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- {"month"=>"12", "year"=>"2010", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"14"}
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- {"month"=>"3", "year"=>"2011", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"23"}
- {"month"=>"4", "year"=>"2011", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"22"}
- {"month"=>"5", "year"=>"2011", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"12"}
- {"month"=>"6", "year"=>"2011", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"7", "year"=>"2011", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"8", "year"=>"2011", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"19"}
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- {"month"=>"5", "year"=>"2012", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"6", "year"=>"2012", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"7", "year"=>"2012", "pdf_views"=>"1", "xml_views"=>"5", "html_views"=>"14"}
- {"month"=>"8", "year"=>"2012", "pdf_views"=>"9", "xml_views"=>"5", "html_views"=>"26"}
- {"month"=>"9", "year"=>"2012", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"15"}
- {"month"=>"10", "year"=>"2012", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"34"}
- {"month"=>"11", "year"=>"2012", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"22"}
- {"month"=>"12", "year"=>"2012", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"45"}
- {"month"=>"1", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"90"}
- {"month"=>"2", "year"=>"2013", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"35"}
- {"month"=>"3", "year"=>"2013", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"33"}
- {"month"=>"4", "year"=>"2013", "pdf_views"=>"2", "xml_views"=>"2", "html_views"=>"26"}
- {"month"=>"5", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"47"}
- {"month"=>"6", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"33"}
- {"month"=>"7", "year"=>"2013", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"32"}
- {"month"=>"8", "year"=>"2013", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"9", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"10", "year"=>"2013", "pdf_views"=>"1", "xml_views"=>"1", "html_views"=>"9"}
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- {"month"=>"3", "year"=>"2014", "pdf_views"=>"6", "xml_views"=>"2", "html_views"=>"23"}
- {"month"=>"4", "year"=>"2014", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"33"}
- {"month"=>"5", "year"=>"2014", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"6", "year"=>"2014", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"17"}
- {"month"=>"7", "year"=>"2014", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"8", "year"=>"2014", "pdf_views"=>"1", "xml_views"=>"2", "html_views"=>"11"}
- {"month"=>"9", "year"=>"2014", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"25"}
- {"month"=>"10", "year"=>"2014", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"29"}
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- {"month"=>"1", "year"=>"2015", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"20"}
- {"month"=>"2", "year"=>"2015", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"3", "year"=>"2015", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"15"}
- {"month"=>"4", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"1", "html_views"=>"9"}
- {"month"=>"5", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"12"}
- {"month"=>"6", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"9"}
- {"month"=>"7", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"8", "year"=>"2015", "pdf_views"=>"1", "xml_views"=>"2", "html_views"=>"11"}
- {"month"=>"9", "year"=>"2015", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"10", "year"=>"2015", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"11", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"12", "year"=>"2015", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"49"}
- {"month"=>"1", "year"=>"2016", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"16"}
- {"month"=>"2", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"16"}
- {"month"=>"3", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"22"}
- {"month"=>"4", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"5", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"15"}
- {"month"=>"6", "year"=>"2016", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"7", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"8", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"9", "year"=>"2016", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"25"}
- {"month"=>"10", "year"=>"2016", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"11", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"12", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"1", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"26"}
- {"month"=>"2", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"35"}
- {"month"=>"3", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"29"}
- {"month"=>"4", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"29"}
- {"month"=>"5", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"31"}
- {"month"=>"6", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"25"}
- {"month"=>"7", "year"=>"2017", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"12"}
- {"month"=>"8", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"20"}
- {"month"=>"9", "year"=>"2017", "pdf_views"=>"2", "xml_views"=>"1", "html_views"=>"12"}
- {"month"=>"10", "year"=>"2017", "pdf_views"=>"5", "xml_views"=>"3", "html_views"=>"18"}
- {"month"=>"11", "year"=>"2017", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"12", "year"=>"2017", "pdf_views"=>"7", "xml_views"=>"1", "html_views"=>"15"}
- {"month"=>"1", "year"=>"2018", "pdf_views"=>"9", "xml_views"=>"1", "html_views"=>"121"}
- {"month"=>"2", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"7"}
- {"month"=>"3", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"7"}
- {"month"=>"4", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"5"}
- {"month"=>"5", "year"=>"2018", "pdf_views"=>"2", "xml_views"=>"1", "html_views"=>"8"}
- {"month"=>"6", "year"=>"2018", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"11"}
- {"month"=>"7", "year"=>"2018", "pdf_views"=>"3", "xml_views"=>"3", "html_views"=>"2"}
- {"month"=>"8", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"1", "html_views"=>"2"}
- {"month"=>"9", "year"=>"2018", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"10", "year"=>"2018", "pdf_views"=>"2", "xml_views"=>"1", "html_views"=>"13"}
- {"month"=>"11", "year"=>"2018", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"12", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"3"}
- {"month"=>"1", "year"=>"2019", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"6"}
- {"month"=>"2", "year"=>"2019", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"3", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"5"}
- {"month"=>"4", "year"=>"2019", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"12"}
- {"month"=>"5", "year"=>"2019", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"6", "year"=>"2019", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"7", "year"=>"2019", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"8", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"3"}
- {"month"=>"9", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"2"}
- {"month"=>"10", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"6"}
- {"month"=>"11", "year"=>"2019", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"12", "year"=>"2019", "pdf_views"=>"10", "xml_views"=>"0", "html_views"=>"3"}
- {"month"=>"1", "year"=>"2020", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"2", "year"=>"2020", "pdf_views"=>"9", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"3", "year"=>"2020", "pdf_views"=>"106", "xml_views"=>"4", "html_views"=>"856"}
- {"month"=>"4", "year"=>"2020", "pdf_views"=>"127", "xml_views"=>"0", "html_views"=>"609"}
- {"month"=>"5", "year"=>"2020", "pdf_views"=>"73", "xml_views"=>"2", "html_views"=>"148"}
- {"month"=>"6", "year"=>"2020", "pdf_views"=>"23", "xml_views"=>"0", "html_views"=>"81"}
- {"month"=>"7", "year"=>"2020", "pdf_views"=>"12", "xml_views"=>"0", "html_views"=>"39"}
- {"month"=>"8", "year"=>"2020", "pdf_views"=>"14", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"9", "year"=>"2020", "pdf_views"=>"15", "xml_views"=>"0", "html_views"=>"31"}
- {"month"=>"10", "year"=>"2020", "pdf_views"=>"17", "xml_views"=>"1", "html_views"=>"59"}
- {"month"=>"11", "year"=>"2020", "pdf_views"=>"25", "xml_views"=>"0", "html_views"=>"77"}
- {"month"=>"12", "year"=>"2020", "pdf_views"=>"22", "xml_views"=>"3", "html_views"=>"26"}
- {"month"=>"1", "year"=>"2021", "pdf_views"=>"6", "xml_views"=>"1", "html_views"=>"28"}
- {"month"=>"2", "year"=>"2021", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"43"}
- {"month"=>"3", "year"=>"2021", "pdf_views"=>"14", "xml_views"=>"1", "html_views"=>"37"}
- {"month"=>"4", "year"=>"2021", "pdf_views"=>"3", "xml_views"=>"2", "html_views"=>"13"}
PMC Usage Stats | Further Information
- {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"15", "unique-ip"=>"17", "pdf"=>"10", "year"=>"2010", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"13", "year"=>"2010", "pdf"=>"10", "unique-ip"=>"18", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"14", "unique-ip"=>"15", "pdf"=>"10", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"7", "year"=>"2010", "pdf"=>"5", "unique-ip"=>"9", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"5", "pdf"=>"3", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"9", "year"=>"2010", "pdf"=>"1", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"6", "unique-ip"=>"10", "pdf"=>"12", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2010", "pdf"=>"4", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"2", "unique-ip"=>"7", "pdf"=>"2", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"1", "abstract"=>"3", "full-text"=>"4", "year"=>"2010", "pdf"=>"3", "unique-ip"=>"8", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"2", "year"=>"2010", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
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Relative Metric
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