Is
Quality and Completeness of Reporting of Systematic Reviews and
Meta-Analyses Published in High Impact Radiology Journals Associated
with Citation Rates?
- Published: March 16, 2015
- DOI: 10.1371/journal.pone.0119892
Abstract
Purpose
Thepurpose of this study is to determine whether study quality and
completeness of reporting of systematic reviews (SR) and meta-analyses
(MA) published in high impact factor (IF) radiology journals is
associated with citation rates.
Methods
AllSR and MA published in English between Jan 2007–Dec 2011, in radiology
journals with an IF >2.75, were identified on Ovid MEDLINE. The
Assessing the Methodologic Quality of Systematic Reviews (AMSTAR)
checklist for study quality, and the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA) checklist for study
completeness, was applied to each SR & MA. Each SR & MA was then
searched in Google Scholar to yield a citation rate. Spearman
correlation coefficients were used to assess the relationship between
AMSTAR and PRISMA results with citation rate. Multivariate analyses were
performed to account for the effect of journal IF and journal 5-year IF
on correlation with citation rate. Values were reported as medians with
interquartile range (IQR) provided.
Results
129studies from 11 journals were included (50 SR and 79 MA). Median AMSTAR
result was 8.0/11 (IQR: 5–9) and median PRISMA result was 23.0/27 (IQR:
21–25). The median citation rate for SR & MA was 0.73
citations/month post-publication (IQR: 0.40–1.17). There was a positive
correlation between both AMSTAR and PRISMA results and SR & MA
citation rate; ρ=0.323 (P=0.0002) and ρ=0.327 (P=0.0002)
respectively. Positive correlation persisted for AMSTAR and PRISMA
results after journal IF was partialed out; ρ=0.243 (P=0.006) and ρ=0.256 (P=0.004), and after journal 5-year IF was partialed out; ρ=0.235 (P=0.008) and ρ=0.243 (P=0.006) respectively.
Conclusion
Thereis a positive correlation between the quality and the completeness of a
reported SR or MA with citation rate which persists when adjusted for
journal IF and journal 5-year IF.
Figures
Citation: van der Pol
CB, McInnes MDF, Petrcich W, Tunis AS, Hanna R (2015) Is Quality and
Completeness of Reporting of Systematic Reviews and Meta-Analyses
Published in High Impact Radiology Journals Associated with Citation
Rates? PLoS ONE 10(3):
e0119892.
doi:10.1371/journal.pone.0119892
Academic Editor: Terence J. Quinn, University of Glasgow, UNITED KINGDOM
Received: July 15, 2014; Accepted: January 20, 2015; Published: March 16, 2015
Copyright: © 2015 van der Pol et al. This is an open access article distributed under the terms of the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Financial support from the University of Ottawa Department of Radiology for statistical analysis.
Competing interests: The authors have declared that no competing interests exist.
CB, McInnes MDF, Petrcich W, Tunis AS, Hanna R (2015) Is Quality and
Completeness of Reporting of Systematic Reviews and Meta-Analyses
Published in High Impact Radiology Journals Associated with Citation
Rates? PLoS ONE 10(3):
e0119892.
doi:10.1371/journal.pone.0119892
Academic Editor: Terence J. Quinn, University of Glasgow, UNITED KINGDOM
Received: July 15, 2014; Accepted: January 20, 2015; Published: March 16, 2015
Copyright: © 2015 van der Pol et al. This is an open access article distributed under the terms of the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Financial support from the University of Ottawa Department of Radiology for statistical analysis.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Impact factor (IF) is a metric that attempts to quantify the overall citation rate of a journal [1].It is widely considered a measure of journal prestige, and is often
used to measure the research performance of investigators and
institutions [2–4].
As a journal’s IF depends on the number of times a journal’s articles
are cited, there has been interest across a variety of medical
specialties to determine factors which are associated with citation [5–9]. More recently, there has been increased reference to journal IF in radiology publications [10–13].
A
journal’s IF is calculated by determining the number of times the
articles published in a journal over a preceding period of time are
cited by indexed journals within a year, divided by the total number of
“citable items” published in the journal during the same preceding
period of time [14].
This calculation is often skewed by outlying articles, specifically
articles that receive a high number of post-publication citations [10,15].
A journal’s IF therefore does not represent the number of citations for
each individual article, but rather the sum of all citations of all
published articles. The impact of any single article cannot be assumed
based on the IF of the journal it was published in [16,17].
As
one of the highest levels of evidence available in the diagnostic
imaging literature, systematic reviews (SR) and meta-analyses (MA) are
conducted in attempt to produce high impact findings [18].
These pool existing data to eliminate bias, increase sample size and
ultimately provide stronger answers to clinical questions than can be
achieved from any individual component study [19–21].
Yet factors associated with post-publication citations of diagnostic
imaging related SR & MA have not been well characterized. In
particular, it is unclear if the quality or completeness of SR & MA
affects how often they are cited.
Several tools have been developed to quantify the quality and completeness of SR & MA [22–24]. These include “The Assessing the Methodologic Quality of Systematic Reviews” (AMSTAR) [22]
to assess quality, and the “Preferred Reporting Items for Systematic
Reviews and Meta-Analyses” (PRISMA) statement to assess completeness of
reporting [24].
The purpose of this study is to determine whether study quality and
completeness of reporting of SR & MA published in high IF radiology
journals are associated with individual article citation rates.
Materials and Methods
Study selection and data extraction
Asearch was performed in MEDLINE to identify SR & MA published in
radiology journals with an impact factor >2.75 based on the Thomson
ISI ranking. A radiology journal was defined as any journal included on
the Thomson ISI ranking that primarily published articles related to any
aspect of medical imaging. This included any radiology subspecialty
specific journals. Medical imaging related SR & MA published in
non-radiology journals were excluded. A threshold of 2.75 was chosen to
include studies in the most frequently cited radiology journals while
limiting the total number of studies to a manageable amount. The search
was limited to English language articles published between Jan 2007–Dec
2011. Two investigators independently retrieved and reviewed all
included articles, with discrepancies resolved by consensus (A.S.T., a
third year radiology resident and M.D.F.M., a staff radiologist with
more than 3 years of experience in the performance and review of SR
& MA).
Data
extraction was performed independently on included articles by two
investigators (A.S.T. and R.H., both third year radiology residents) and
assessed using AMSTAR & PRISMA checklists (S1 Fig. and S1 Table).
The first ten articles were reviewed in consensus to become familiar
with application of the AMSTAR and PRISMA checklists. Following this,
all remaining articles were reviewed independently. Discrepancies were
resolved through consensus or, if there was persistent disagreement,
discussed with a third investigator (M.D.F.M.). The detailed methods can
be found in the previously published paper titled “Association of study
quality with completeness of reporting: have completeness of reporting
and quality of systematic reviews and meta-analyses in major radiology
journals changed since publication of the PRISMA statement?” [25].
Outcome measure assessment
Thenumber of citations for each individual SR & MA was documented
based on the number of citations indexed through Google Scholar [26] as of April 5, 2014. A post-publication citation rate
was then calculated by dividing the total number of citations for each
article by the total number of months since the earliest date of
publication (e.g. epub ahead of print date) [27,28].
The purpose of using a citation rate rather than absolute
post-publication citation counts was to eliminate the effect of varying
amounts of time since publication, since studies published earlier have
had more time to accumulate citations.
Statistical analysis
MedianAMSTAR and PRISMA results were reported, along with the interobserver
agreement as calculated using the kappa coefficient (κ) for all SR &
MA except the first ten, which were reviewed in consensus. Spearman
correlation coefficients (ρ) were used to assess for correlation between
AMSTAR result and citation rate, PRISMA result and citation rate,
journal IF and citation rate, and journal 5-year IF and citation rate. A
multivariate analysis was performed: Spearman partial correlations were
performed to assess the associations between AMSTAR or PRISMA results
and post-publication citation rate while controlling for the effect of
journal IF and journal 5-year IF. Scatter plots were created to
demonstrate the distribution of citation rates relative to AMSTAR and
PRISMA results with polynomial lines fitted to data using LOESS (local
polynomial regression fitting) [29].
All statistical analysis was performed using SAS version 9.2 (SAS
Institute Inc. Cary, NC, USA). Values are reported as medians with
interquartile range (IQR).
Results
129 studies from 11 journals were identified that met our inclusion criteria [30–158] (S2 Table). A meta-regression analysis [159] included by Tunis et al. [25]was excluded from our study since it was not a systematic review. The
median AMSTAR result was 8.0/11 (IQR: 5–9) and median PRISMA result was
23.0/27 (IQR: 21–25). The overall inter-observer agreement was moderate
for the PRISMA results with κ = 0.57, and higher for the AMSTAR results
with κ = 0.69. The median citation rate for SR & MA was 0.73
citations/month post-publication (IQR: 0.40–1.17). Scatter plots show
the distribution of citation rates relative to AMSTAR result (Fig. 1) and PRISMA result (Fig. 2).
Fig 1. Scatter plot demonstrating the distribution of citations rates for each AMSTAR result.
Solid line: polynomials fitted to all data using LOESS [29]. Dashed line: polynomials linking subsets of data. Double dot-and-dash line: straight lines fitted to subsets of data.doi:10.1371/journal.pone.0119892.g001
Fig 2. Scatter plot demonstrating the distribution of citations rates for each PRISMA result.
Solid line: polynomials fitted to all data using LOESS [29]. Dashed line: polynomials linking subsets of data. Double dot-and-dash line: straight lines fitted to subsets of data.doi:10.1371/journal.pone.0119892.g002
After
multivariate analysis, a positive correlation persisted for AMSTAR and
PRISMA results after journal IF was partialed out; ρ = 0.243 (P = 0.006) and ρ = 0.256 (P = 0.004) respectively. Similarly, a positive correlation persisted after journal 5-year IF was partialed out; ρ = 0.235 (P = 0.008) and ρ = 0.243 (P = 0.006) respectively.
Discussion
Ourresults suggest that the quality and completeness of SR & MA
reported in high impact radiology journals is associated with
post-publication citation rates. This association persisted on
multivariate analysis. Although nearly the same study population was
used as in a study by Tunis et al. [25], the purpose of our study was entirely different. Thus we felt an independent publication was warranted.
Radiology
journals with an IF >2.75 may be more likely to publish SR & MA.
Even though we limited our assessment to journals with a high IF, our
use of multivariate analysis to partial out the effect of journal IF and
5-year IF should help correct for the fact that these journals are more
frequently cited. Despite including only “high impact” journals, at the
time of our analysis, none of the journals required submission of a
PRISMA checklist along with a submitted manuscript. Radiology
was the only journal that had endorsed the PRISMA statement. It is our
hope that our findings encourage editors to endorse and authors to
adhere to the PRISMA checklist in the future.
Comparison to other studies
Priorstudies have investigated factors associated with post-publication
citation counts. Several factors shown to correlate with more citations
include: study design and study topic in the urology literature [5];
high levels of evidence, large sample size, multi-institutional studies
and conflict of interest disclosure in the orthopedic surgery
literature [6]; extended description of statistical analysis [7]; statistically significant papers in the psychiatry literature [8]; being indexed in numerous databases, number of authors, clinical relevance scores and number of cited references [9]; and article length in the general medicine literature [160].
We are unaware of any prior work assessing the effect of SR & MA
study quality and completeness on post-publication citation rates.
A study by Royle et al. investigated factors associated with higher citation counts of SR [16].
They found that the number of authors, first author from the United
States, an ICD-10 chapter heading of Neoplasms, type of intervention
classified as Investigation, Diagnostics or Screening, and having an
international collaboration all correlated with increased citation
counts. Similar to our study, they found that journal IF was a stronger
predictor of citations.
A
prior investigation of studies that were originally submitted to an
emergency medicine specialty meeting found study design and quality did
not correlate with post-publication citation rates [161].
Unlike in our study, they did not exclusively evaluate SR & MA, did
not apply the AMSTAR and PRISMA checklists, and did not specifically
look at the diagnostic imaging literature. Similar to our study and the
study by Royle et al., they found that journal IF was more important
than any other variable for post-publication counts.
It
is interesting to note that our results confirm previous
findings—namely that higher quality studies are cited more frequently.
It is also interesting to note that the median number of citations/month
was 0.73 (8.7 citations/year); this is considerably higher than the
number of citations typically seen in our included cohort of radiology
journals whose 2011 impact factors range from 2.75–6.07 [162]. This supports prior findings that studies of higher levels of evidence are cited more often [5,6,163].
Limitations
Thereare several limitations to this study. Cross-referencing Google Scholar
citation counts with other known citation databases such as Scopus [164] or the Thomson Reuters Web of Science [165] may have been beneficial since absolute citation counts have been shown to vary between databases [166].
However we were comparing relative citation counts between articles,
and several studies have shown a strong correlation between Google
Scholar citations counts and the Thomson Reuters Web of Science citation
counts [167–169]. Furthermore, Google Scholar is arguably more comprehensive than other citation databases in certain fields [170,171].
Another limitation was that our calculation of citation rate, by
dividing the total number of citations by time since publication,
assumes that the citation frequency is independent of the time since
publication. Given the difficulty in predicting the time course of
citations, which can vary considerably over time between articles and
depend on multiple factors including the article topic and the journal
of publication, this could introduce a source of bias in our analysis [172–174].
However we felt that our calculated citation rate based on the number
of citations over a three to seven year period following publication was
adequate and that any bias is likely to apply evenly over all studies,
thus minimizing the impact on our study conclusions. Furthermore, the
interface of Google Scholar and other citation indexes do not allow for
practical extraction of monthly citation information.
Several additional limitations outlined and addressed by Tunis et al. [25]
are applicable to our study: the assessment of journals was not blinded
to the journal or time of publication, our search was limited to
radiology journals with high IF and thus does not represent the totality
of the radiology literature, the selection of impact factor threshold
was somewhat arbitrary (and was chosen as a practical means to result in
a reasonable number of articles to review), and finally our
interobserver agreement was only moderate. We believe that our moderate
interobserver agreement was due to many items being flagged as unclear
by one reviewer to be discussed with the other.
Conclusion
Inconclusion, there is positive correlation between the quality and the
completeness of SR & MA published in high impact radiology journals
with citation rate, which persists when adjusted for journal IF and
journal 5-year IF. Although citation counts took on a wide range of
values for a particular AMSTAR and PRISMA score, this study provides
statistical evidence against there being “no relationship” with study
quality and completeness and post-publication citations. This reinforces
the importance of complete reporting and following publishing
guidelines for authors of SR and MA, and might encourage more journals
to endorse these guidelines.
Supporting Information
S2 Table. List of included articles with total PRISMA and AMSTAR results.
doi:10.1371/journal.pone.0119892.s003
(DOC)
Author Contributions
Conceivedand designed the experiments: MM CvdP WP AT RH. Performed the
experiments: CvdP WP AT RH. Analyzed the data: MM CvdP WP. Contributed
reagents/materials/analysis tools: CvdP AT RH. Wrote the paper: MM CvdP
WP AT RH.
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PLOS ONE: Is Quality and Completeness of Reporting of Systematic Reviews and Meta-Analyses Published in High Impact Radiology Journals Associated with Citation Rates?
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