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Abstracts of Randomized Controlled Trials Presented at the Society for Pediatric Research Meeting
An Example of Publication Bias
Terry P. Klassen, MD;
Natasha Wiebe, MMath;
Kelly Russell, BSc;
Kelly Stevens, BSc;
Lisa Hartling, MSc;
William R. Craig, MD;
David Moher, MSc
Arch Pediatr Adolesc Med. 2002;156:474-479.
ABSTRACT
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Background Publication bias toward studies that favor new therapies has been known
to occur for the past 40 years, yet its implications are not well studied
in child health. The increased interest in meta-analyses has highlighted the
need to identify the totality of evidence when addressing treatment questions.
Objectives To measure the percentage of randomized controlled trials (RCTs) presented
at a major pediatric scientific meeting that were subsequently published as
full-length articles, to investigate factors associated with publication,
and to describe the variables that change from abstract to manuscript form.
Design The scientific proceedings from the Society for Pediatric Research were
hand searched for RCTs (1992-1995). Subsequent publication was ascertained
through a search of various electronic databases. Quality of abstracts and
manuscripts was measured, and data were extracted using a structured form.
Results A total of 264 (59.1%) of 447 abstracts were subsequently published.
Almost 64% of RCTs that were subsequently published favored new therapy compared
with 43.5% of studies that were never published (P<.001).
Mean effect size for published vs unpublished RCTs was 0.74 vs 0.05 (P<.001). Median sample size was larger in published
(n = 45) vs unpublished (n = 34) RCTs (P = .02).
Quality was significantly lower for abstracts vs published RCTs (P<.001). For 5% of abstracts that were subsequently published, the
conclusion regarding treatment efficacy changed.
Conclusions Publication bias is a serious threat to assessing the effectiveness
of interventions in child health, as little more than half of RCTs presented
at a major scientific meeting are subsequently published. There is a need
to institute an international registry of RCTs in children so that the totality
of evidence can be accessed when assessing treatment effectiveness.
INTRODUCTION
PUBLICATION BIAS, or the selective publication of studies that favor
new therapies, poses a serious threat to validly assessing the effectiveness
of new therapies.1 To practice evidence-based
medicine, the totality of evidence for and against a new therapy needs to
be considered. The selective publication or submission of only those manuscripts
that show a beneficial effect of therapy has important implications on the
pool of evidence available on which to base decisions. This has implications
for the individual clinician and for researchers who aim to synthesize existing
evidence in the form of a systematic review.
In a recent meta-analysis evaluating the effectiveness of glucocorticoids
for children with croup, Ausejo et al2 demonstrated
the challenge of selective publication. Formal statistical testing showed
that studies with smaller sample sizes tended to show larger positive effects
of an intervention. One plausible explanation for this observation is publication
bias.3 This finding casts uncertainty on the
degree of benefit conferred on patients with croup from glucocorticoids compared
with placebo. McAuley and colleagues4 showed
that excluding the gray literature (ie, literature that is difficult to identify
or retrieve, of which abstracts form the largest proportion at 61%) may yield
larger estimates in meta-analyses by 15%.
Scientific meetings are often the first forum in which new research
is shared with one's peers; hence, they represent a unique opportunity to
examine the nature and existence of selective publication.5-6
We undertook this study to (1) measure the percentage of randomized trials
presented at a major pediatric scientific meeting that were subsequently published,
(2) investigate factors associated with publication, and (3) describe the
variables that changed from abstract to manuscript form.
MATERIALS AND METHODS
SELECTION OF ABSTRACTS AND MANUSCRIPTS
Abstracts of randomized controlled trials (RCTs) were identified by
hand-searching the proceedings from the Society for Pediatric Research (1992-1995).
To determine whether an abstract was later published in manuscript form, the
following databases were searched between February 1 and July 31, 2000: PubMed,
EMBASE, Cochrane Library, CINAHL, Web of Science, Current Contents, and HEALTHSTAR.
The databases were searched with the assistance of a medical librarian using
the name of the primary author and key words found in the title. At least
one common outcome must have been found in the abstract and the manuscript
to be considered as the corresponding manuscript. If a relevant citation was
not found in any of the databases, we assumed that the study had not been
published in manuscript form.
Abstracts and manuscripts were included if they reported phase III RCTs
with pediatric outcomes (studies reporting outcomes on pregnant women were
excluded). Studies were excluded if they reported outcomes of nonrandomized
treatment arms only.
ASSESSMENT OF METHODOLOGICAL QUALITY
The quality, or internal validity, of the abstracts and manuscripts
was assessed in 3 ways. First, study quality was scored according to a validated
5-point scale developed by Jadad et al.7 This
scale is composed of 5 questions to determine whether (1) the study was described
as randomized, (2) an appropriate method of randomization was used (eg, table
of random numbers), (3) the study was described as double blinded, (4) blinding
was appropriate (eg, identical placebo), and (5) there was an adequate description
of withdrawals and dropouts. A score of 5 indicates a high-quality study.7 Second, concealment of allocation, or the method used
to prevent foreknowledge of group assignment by the patients and the investigators,
was assessed. Allocation concealment was rated as adequate (eg, centralized
or pharmacy-controlled randomization), inadequate (ie, any procedure that
is transparent before allocation, such as an open list of random numbers),
or unclear or not reported.8 Third, funding
source was recorded as pharmaceutical, government, private, other, or unclear
or not reported.
DATA EXTRACTION
The following information was recorded for abstracts and manuscripts:
journal citation, year of publication, diagnostic category (as designated
in the proceedings of the Society for Pediatric Research), trial design (ie,
parallel or crossover), study type (ie, efficacy vs equivalency), stage of
study (ie, preliminary or completed), pilot study vs full trial, number of
withdrawals, and results.
The overall study conclusions (ie, favored the intervention or not)
were determined by the authors' statements in their concluding remarks. If
the study favored an intervention, the efficacious treatment was noted. Primary
outcomes were determined in 1 of 3 ways: stated by the authors (19.9%), inferred
by the extractors through the title or concluding remarks (32.2%), or randomly
selected from probable primary outcomes using a computer-generated table of
random numbers (47.9%).
Study type was defined according to the authors' statements with respect
to the primary hypothesis. If the authors intended to demonstrate a significant
difference between treatments, the study type was recorded as efficacy. Equivalence
was deemed the study type when authors intended to show that there was no
significant difference between treatments.
STATISTICAL ANALYSIS
Data were entered into a database program (Access; Microsoft Corp, Redmond,
Wash) and were analyzed using a statistical package (S-PLUS 2000; MathSoft
Inc, Cambridge, Mass). Medians and interquartile ranges were used to describe
nonparametric data, means and SDs were used for normal continuous data, and
percentages and 95% confidence intervals (CIs) were used for dichotomous and
categorical data. Odds ratios were converted into effect sizes using a method
devised by Hasselblad and Hedges.9 Percentages
and their associated 95% CIs were also calculated for descriptive purposes
and to quantify the change in variables from abstract to manuscript. To measure
the association between different variables and publication status, the following
tests were used: Pearson  2 tests for dichotomous and other
categorical data, t tests (Welch modified for unequal
variances) for normal continuous data, and Wilcoxon rank sum tests for otherwise
nonparametric data. Logistic regression was used to evaluate predictors of
publication while controlling for possible confounders such as overall study
conclusions and study type. We expected that overall study conclusions would
interact with study type. Thus, without the interaction term, study type might
reduce the benefit attributed to the overall study conclusions. Log-rank tests
were used to assess time to publication. Funnel plots (sample size vs effect
size), the rank correlation test,10 and weighted
regression3 were used to determine publication
bias.
RESULTS
SAMPLE
A total of 447 abstracts were identified; 264 (59.1%; 95% CI, 54.4%-63.7%)
were found as published manuscripts. Table
1 gives the number of abstracts identified and the percentage published
in manuscript form, by year.
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Table 1. Abstracts Published in Manuscript Form, by Year*
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Sixteen manuscripts were excluded for the following reasons: not being
RCTs (n = 10, although their abstracts claimed randomization), cluster designs
(n = 2), data authenticity questioned by the journal editors (n = 2), unavailable
methods (n = 1), and study presented as a brief communication (n = 1). The
additional information gained by reading the manuscripts was not used to exclude
abstracts because further information was not available for abstracts not
subsequently published. The included manuscripts (n = 248) were used exclusively
in the change in variables (from abstract to manuscript form) analysis. The
other analyses were based entirely on abstract data.
Abstracts were classified into 26 diagnostic categories. The most common
categories were neonatology-general (24.6% of abstracts that remained unpublished
and 23.1% of those that were subsequently published), neonatal pulmonology
(14.8% of those unpublished and 12.9% of those published), neonatal nutrition
and metabolism (12.6% of those unpublished and 11.4% of those published),
and infectious diseases (7.1% of those unpublished and 10.6% of those published).
The remaining categories were used for less than 10% of either type of abstract.
Manuscripts were published in 62 journals: 24.2% in Journal of Pediatrics, 20.6% in Pediatrics,
and the remaining 55.2% in a variety of journals (with  4.0% in any one
journal).
There were few abstracts on pilot studies (3.3% of unpublished abstracts
and 2.3% of published abstracts) or studies in their preliminary stages (8.2%
of unpublished abstracts and 7.6% of published abstracts). The number of withdrawals
was reported in only 6.0% and 3.4% of unpublished and published abstracts,
respectively. These variables were not considered in the logistic regression
analysis.
QUALITY OF ABSTRACTS AND MANUSCRIPTS
Table 2 summarizes study
quality by document type. There were no differences in quality measures between
abstracts that were subsequently published and those that remained unpublished.
Scores on the quality variables were significantly different for all abstracts
compared with published manuscripts. Quality variables were not associated
with overall study conclusions favoring the new therapy (Jadad score, P = .85; funding source, P = .81).
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Table 2. Quality Variables by Document Type*
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PREDICTORS OF PUBLICATION
Table 3 provides the results
of univariate analyses assessing predictors of publication. Variables associated
with publication were study conclusions favoring treatment (63.5% vs 43.7%; P<.001), sample size (n = 45 vs 34; P = .02), and measures of treatment effect. Measures of treatment effect
were evaluated in 3 ways: odds ratios for dichotomous outcomes (P = .009), standardized mean differences for continuous outcomes (P = .01), and overall effect sizes (odds ratios and standardized
mean differences combined) (P<.001).
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Table 3. Predictors of Publication: Univariate Results*
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Table 4 gives the results
of logistic regression analysis of predictors of publication. The interaction
between study type and overall study conclusions was significant. Successful
equivalency studies, that is, studies in which the statistical results were
nonsignificant, thereby agreeing with the study hypothesis, had the greatest
odds of being published. Sample size was also significant, with the chances
of publication increasing with larger sample size. Because the distribution
of sample size was strongly skewed to the right, greater and greater increases
are demanded to produce an equivalent predicting effect. This diminishing
return is captured by a log-log transformation of the sample size variable.
Effect size was not put into the model because its properties were closely
associated with overall study conclusions.
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Table 4. Predictors of Publication: Results From Logistic Regression
(n = 343)*
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VARIABLES THAT CHANGE FROM THE ABSTRACT TO THE PUBLISHED MANUSCRIPT
Two hundred forty-eight abstracts were paired with their subsequent
manuscripts. Of these, 239 had conclusions favoring treatment; 2.1% changed
from favoring treatment in the abstract to not favoring treatment in the manuscript,
whereas 2.9% changed from not favoring treatment in the abstract to favoring
treatment in the manuscript.
Most measures of treatment effect changed slightly from the abstract
to the manuscript. Thirty-eight percent and 45.1% decreased in log odds ratios
and standardized mean differences, respectively, whereas 44.0% and 37.3% increased.
Overall significance in effect size was also evaluated (P.05). In 4.0% of the cases, abstract outcomes were significant
but changed to nonsignificant in manuscript form; 8.9% changed from nonsignificant
to significant. In 10.8% of studies, the sample size decreased from the abstract
to the manuscript, whereas in 48.3% the sample size increased.
TIME TO PUBLICATION
Figure 1 shows the time to
publication by overall study conclusions. The probability of publication plateaued
after approximately 60 months. After 5 years, 34.2% of studies with significant
findings remained unpublished compared with 55.7% of studies with nonsignificant
results.
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Figure 1. Time to publication by significant
and nonsignificant findings.
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Of studies that were subsequently published, abstracts with Jadad scores
of 1 or less were published on average 24.7 months after the abstract appeared
in the proceedings of the Society for Pediatric Research compared with 21.3
months for those with scores greater than 1 (P =
.11). There was a significant difference between abstracts that did not report
a funding source (25.1 months) and those that did (20.9 months) (P = .049). Favoring the new therapy was not associated with time to
publication (P = .74).
PUBLICATION BIAS
Figure 2 and Figure 3 show funnel plots for published and unpublished studies.
In the absence of publication bias, the funnel plot should resemble an inverted
funnel. Smaller studies naturally (or statistically) give a wide range of
effect sizes; they are less stable because they contain less information.
Thus, at the base of the inverted funnel, one would expect to see the widest
spread. At the top of the plot, the effect sizes should converge at a point,
if there exists a trial that is sufficiently large to be relatively stable.
The funnel plot of published studies (Figure
2) and statistical tests for publication bias show that small unsuccessful
studies are less likely to be published (rank correlation test, P = .03; weighted regression, P = .02); the
base of the inverted funnel is not balanced, resulting in funnel plot asymmetry.
No asymmetry was observed in the sample of studies that were not subsequently
published (rank correlation test, P = .43; weighted
regression, P = .62) (Figure 3). All studies combined (Figure 3) suggest evidence of publication bias that predates submission
to the pediatric meeting (rank correlation test, P
= .07; weighted regression, P = .02). Missing studies
favoring the control groups are indicated by the asymmetry of the plot. Publication
bias may include nonsubmission of studies to the meetings or to journals (submission
bias) and rejection of submissions by editorial staff (publication bias).
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Figure 2. Funnel plot of published studies.
Outliers: -9.4, 25; -5.1, 14; -1.4, 6794; -0.6, 2342; -0.2,
5699; and 0.1, 2416.
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Figure 3. Funnel plot of all studies. Outliers: -9.4,
25; -5.1, 14; -1.4, 6794; -0.6, 2342; -0.2, 5699;
0.1, 2416; and 10.8, 7.
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COMMENT
The results of this study demonstrate that a major factor predicting
publication after presentation of an RCT at a scientific meeting is a positive
outcome favoring the new therapy. The larger the treatment effect, the more
likely that a study will be published. This is the first time to our knowledge
that this has been shown in the area of child health but is consistent with
results of studies in other areas.1, 11-12
One implication of this finding is that by using only the published literature
to examine the effectiveness of a new therapy, one could get an inflated view
of the benefit of a new therapy. Even more worrisome is to conclude that a
treatment is effective when if the totality of evidence had been identified
(published and unpublished) it may indeed not be better than existing treatments.
It is not known how many RCTs performed in children are never submitted
to a scientific meeting. Although the collection of RCTs presented at scientific
meetings does not capture the entire universe of RCTs performed in children,
it does provide a useful filter to examine the question of publication bias.
The funnel plot of all studies submitted to the Society for Pediatric Research
meeting indicates that submission bias exists (Figure 3), albeit this bias is less pronounced than in studies that
are published as full manuscripts (Figure
2).
The results of our analyses indicate that studies with negative findings
are less likely to be published. Stern and Simes13
examined clinical trials approved by a research ethics board for 10 years
and found that the hazard ratio for studies with positive vs negative findings
being published was 3.13 (P<.001). Scherer and
colleagues14 conducted a meta-analysis on studies
that documented the proportion of studies published after presentation at
a scientific meeting and found an overall estimate of 51%, which is similar
to our estimate of 59.1%. Two of these studies, in the areas of ophthalmology
and perinatology, were confined to RCTs, and reported publication rates were
61% and 36%, respectively.
Several options have been proposed to minimize publication bias. An
international registry of RCTs has been suggested1, 15-16
whereby all trials would be registered at their inception. A standard method
of identifying trials for registration would be through ethics review boards,
as all trials require ethics approval before beginning. Recently, an amnesty
for authors of unpublished trials was initiated. One hundred medical journals
solicited information on unpublished research by requesting authors to complete
an unreported trial registration form.17 This
initiative had modest results, with 165 trials involving 32 000 participants
being registered within the first year.18
Until publication bias can be fully prevented, there is a need to quantify
its existence and to interpret study findings accordingly. Methods have been
developed for the detection of publication bias, but they lack sufficient
statistical power in meta-analyses with fewer than 10 trials.19
In addition, their performance varies with factors such as sample size, number
of trials, and size of treatment effect.20-21
Publication bias may be more frequent in child health as sample sizes
are smaller than those in the general literature. Smaller sample sizes mean
more statistical fluctuation, hence the probability that small studies may
show large treatment effects. Small studies with large treatment effects that
favor new therapies are more likely to be published than those that do not
favor new therapies. It would be prudent for researchers in child health to
move toward larger multicenter trials whenever possible to avoid this "small
study effect."
In a survey of editors, 30% of them said they would not publish a meta-analysis
that included unpublished research.22 The meta-analyst
is caught in a dilemma, as excluding abstracts or other unpublished RCTs means
the meta-analysis may be biased toward favoring treatment. McAuley et al4 demonstrated that the average quality of abstracts
was lower than full manuscript reports of RCTs. They could not determine whether
this was because lower-quality RCTs were not published or whether, as we demonstrate,
the lower-quality assessments are because of limited information contained
in an abstract. In our study, most abstracts (76%) had a Jadad score of 1.
We know that with published manuscripts, RCTs that score less than 2 may have
treatment effects 30% larger than high-quality studies (score >2).23 The lack of complete reporting holds true for allocation
concealment, as 100% of the abstracts had unclear allocation concealment.
A structured reporting system for abstracts of RCTs that would require the
author to document these key areas would help solve this problem without greatly
increasing the length requirements of abstracts. This has worked well for
reporting of RCTs in journals, and the adoption of these guidelines by journals
has improved their quality of reporting.22, 24
Another solution would be an international registry of trials that would allow
meta-analysts to access longer and more detailed versions of the RCT study
report in a database.
Despite what has been known about publication bias for 40 years,25 it remains a threat to assessing the validity of
therapy in child health. It is urgent that funding agencies, governmental
bodies, health administrators, researchers, and clinicians join together to
eliminate this important and serious bias.
| What This Study Adds
What Is Already Known and Why This Study Needed to Be Done
- Publication bias is a serious threat to assessing
new therapies
- The probability of bias increases if the study
demonstrates greater benefit for the new therapy, hence seriously undermining
our confidence in the published record of evidence as a true estimate of benefit
What This Study Adds to Medical Information and Its Implications
- This study demonstrates that publication bias is
also a significant issue in child health as 40% of trials presented at a scientific
meeting are not published
- When synthesizing therapy evidence, it is critical
to assess for the possibility of publication bias
- Prevention of publication bias could occur if all
randomized trials performed in children were mandated to undergo international
registration at the time of ethics approval
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AUTHOR INFORMATION
Accepted for publication January 10, 2002.
Corresponding author and reprints: Terry P. Klassen, MD, Department
of Pediatrics, University of Alberta, 2C3.67 Walter C. Mackenzie Centre, Edmonton,
Alberta, Canada T6G 2B7 (e-mail: terry.klassen{at}ualberta.ca).
From the Department of Pediatrics, University of Alberta, and the Alberta
Research Centre for Child Health Evidence, Edmonton (Drs Klassen and Craig
and Mss Wiebe, Russell, Stevens, and Hartling); and the Thomas C. Chalmers
Centre for Systematic Reviews, Children's Hospital of Eastern Ontario, University
of Ottawa (Mr Moher).
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