Cardiovascular Research 2004 61(2):201-203; doi:10.1016/j.cardiores.2003.11.023
© 2004 by European Society of Cardiology
Copyright © 2004, European Society of Cardiology
Impact factors: no totum pro parte by skewness of citation
Tobias Opthofa,*,
Ruben Coronelb and
Hans Michael Piperc
aDepartment of Medical Physiology, University Medical Center Utrecht, PO Box 85060, 3508 AB Utrecht, The Netherlands
bMolecular and Experimental Cardiology Group, Academic Medical Center, Amsterdam, The Netherlands
cInsitute of Physiology, Justus Liebig University, Giessen, Germany
* Corresponding author. Tel.: +31-30-2538900; fax: +31-30-2539036. t.opthof{at}med.uu.nl
Received 10 October 2003; revised 15 November 2003; accepted 21 November 2003
Citation of the various papers published in one and the same journal is highly skewed. Journals with a high impact factor obtain this high value by frequent citation of only a limited number of their papers and, on the other hand, journals with low impact factors publish many papers that remain uncited [1]. Thus, mere publication of a paper in a given journal cannot be regarded as a quality marker of that particular paper [2], it just means that the authors have succeeded in surviving the review process of that journal. Seglen [3] has analyzed that 50% of the obtained citations are accumulated by only 15% of the contents of a journal. In addition, the most frequently cited 50% of the contents obtain almost all citations (90%). These numbers were based on an analysis of three biochemical journals (Biochimica Biophysica Acta, Biochemical Journal and Journal of Biochemical Chemistry) and have later been confirmed for two cardiovascular journals (Circulation Research and Cardiovascular Research) [4]. Both analyses applied to recently published papers [3,4]. It is not known whether these data vary over time and whether or not they depend on impact itself.
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1. Skewness of citation
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We have analyzed the original research papers of
Cardiovascular Research published between 1992 and 2000 (
n = 1886). We have
taken advantage from the fact that the impact factor of
Cardiovascular Research increased from 1.47 in 1991 to 4.69 in 2002. This allowed
us to relate the skewness of citations both to the time since
publication and to impact. Thus, for year 1 (the calendar year
of publication itself), we had nine sets of data (contents of
1992 as cited in 1992 through contents of 2000 as cited in 2000).
For year 2 (the calendar year following the year of publication),
we also had nine sets of data (contents of 1992 as cited in
1993 through contents of 2000 as cited in 2001). The same applied
to year 3. Starting with year 4 the sets of data decreased by
one per year for obvious reasons. In year 11 we only had one
set of data (contents of 1992 as cited in 2002). In total we
analyzed 63 sets of data.
Fig. 1 shows that for all 63 sets of data (varying with respect to years since publication and impact), 50% of citations are obtained by 14.0±4.8% (S.D.) of papers (triangle). The most frequently cited half of the papers obtains 90.3±6.1% (S.D.) of all citations (Fig. 1, circle). Finally, only 65.7%±19.5 (S.D.) of the papers is cited in a particular year and thus 34.3% of papers remains uncited (Fig. 1, square). The solid line of identity has been included in Fig. 1 as an aid to appreciate the skewness of citation of individual papers. If all papers would be cited in line with the impact factor, this line would give the relationship between the percentage of papers and the percentage of obtained citations.

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Fig. 1 The contents of Cardiovascular Research as published between 1992 and 2000 (1886 original papers only) were analyzed concerning citation from 1992 till 2002. This led to 63 sets of data. For each set, the percentage of papers needed to accumulate 50% of the citations was scored (triangles). Also, the percentage of citations obtained by the most frequently cited 50% of the papers was calculated (circles). Finally, the percentage of papers accounting for all citations in a given year was determined (squares). The error bars indicate standard deviations. The solid line of identity depicts equal citation of all published papers.
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2. Skewness of citation and years since publication
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Fig. 2 shows the relationship of the parameters described in
Fig. 1 with the years since publication. Thus, the most frequently
cited 50% of the papers (open circles) accumulate on average
90.3% of the citations (as shown in
Fig. 1). Also, 50% of the
citations are obtained by only 14.0% of the papers (triangles).
About two thirds of the papers (67.3%) are less frequently cited
than the average paper (data not shown). These parameters did
not show a substantial dependence on time since publication.
In contrast, there was a significant relationship between the
years since publication and the percentage of uncited papers
(squares). This figure is about 20% during years 3 and 4 since
publication but is substantially higher during earlier and later
years
(Fig. 2).

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Fig. 2 Within the same 63 data sets as described in Fig. 1, we analyzed whether the percentage of papers required to accumulate 50% of the citations (triangles), the percentage of citations obtained by the most frequently cited 50% of the papers (circles), and the percentage of uncited papers (squares) were correlated with the years since publication. The latter parameter varied substantially over the years, whereas the first two did not. Polynomial curve fits are shown. Error bars indicate standard error of the mean.
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3. Skewness of citation and impact
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Fig. 3 shows that the same parameters as tested in
Fig. 2 have
a significant correlation with the impact of the underlying
scientific material. Impact was simply defined as the number
of citations obtained in all years since publication divided
by the number of published papers and was based on original
papers only. Impact is thus not the same as impact
factor. The number of uncited papers decreases substantially
when the impact is higher, which would be expected, although
higher impact might also result from more frequent citation
of a limited number of papers. The amount of citations obtained
by the best 50% of the papers is also negatively
correlated with impact. In contrast, the percentage of papers
that accumulates 50% of the citations is positively correlated
with impact. This suggests that for journals with a higher impact
factor, (i) the square in
Fig. 1 (indicating the percentage
of cited vs. uncited papers) tends to shift to the right, (ii)
the circle in
Fig. 1 (indicating the percentage of citations
obtained by the best cited 50% of papers) shifts to a lower
value along a vertical line, and (iii) the triangle in
Fig. 1 (indicating the percentage of papers receiving half of all citations)
tends to shift to the right. Thus, although skewness of citation
is substantial for journals with a high impact factor (such
as
Cardiovascular Research or
Circulation Research [4]), it
will probably be even more skewed for journals with a low impact
factor. This is also suggested by comparison of the citations
obtained in 1994 by the papers of
Cardiovascular Research and
Circulation Research published in 1992 and 1993. The percentage
of papers receiving half of all citations was 16% for
Circulation Research and 12% for
Cardiovascular Research [4]. Indeed, the
difference between the impact factors of those two journals
was larger in 1994 (6.97 vs. 2.89) than at present. The large
majority of scientific papers is published in journals with
impact factors well below 2.00, at least in the field of cardiovascular
science, underscoring the significance of the title of this
editorial.

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Fig. 3 Within the same 63 data sets as described in Fig. 1, we analyzed whether the percentage of papers required to accumulate 50% of the citations (triangles), the percentage of citations obtained by the most frequently cited 50% of the papers (circles), and the percentage of uncited papers (squares) were correlated with impact. This was the case for all linear regression lines. Correlation coefficients were 0.654, –0.697, –0.471 and –0.932, respectively. All fulfilled P<0.0005. Error bars indicate standard error of the mean.
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4. Uncited papers
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In 1996 De Jong and Schaper
[5] reported that in the field of
clinical cardiology, 46% of a total of 137,019 papers published
between 1981 and 1992 remained uncited during that same period.
Papers published in 1981 scored in this category if they remained
uncited during the full 12-year period between 1981 and 1992.
Papers published in 1992 scored in this category if uncited
in 1992. Thus, by and large, half of papers remained uncited
for a period of 6 years after publication. We analyzed our 63
data sets, published between 1992 and 2000 and cited between
1992 and 2002, in the same way.
Fig. 4 shows the results and
focuses on the percentage of uncited papers
per year (see also
Fig. 2) and
per all years. Although the percentage of uncited
papers is between 30% and 50% between years 7 and 10 since publication
(open squares), the percentage of papers that remains uncited
during all
consecutive years (filled squares) declines to below
4% after year 5 and below 2% during year 8 since publication.
In order to qualify for the papers depicted with
the filled squares, a paper should—at any year along the
abscissa—have been uncited during
all preceding years
as well. The observation of De Jong and Schaper
[5] with respect
to 46% of uncited papers over a period of 12 years since publication
in the field of clinical cardiology, therefore, probably results
from the inclusion of many journals with a low impact factor.
Despite the fact that many papers remain uncited per year (see
(Figs. 1, 2 and 4)

), the number of papers that remains uncited
during a sustained period is very low for a journal with a higher
impact factor such as
Cardiovascular Research (Fig. 4).

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Fig. 4 The percentage of uncited papers as a function of the years since publication. Open squares: data per year. A paper qualified for this group if it remained uncited during that particular year, irrespective of its citations in all other years. Filled squares: Cumulative data per year, including all preceding years. A paper qualified for this group if it remained uncited during that particular year and all preceding years. Error bars indicate standard error of the mean.
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5. Conclusion
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In conclusion, skewness of citation of papers is substantial.
On the average, the 50% most frequently cited papers obtain
about 90% of the citations. This percentage is relatively constant
over the years after publication, but may be higher (almost
100%) for journals with a low impact factor and may be lower
(but still 80%) for journals with a high impact factor. The
percentage of papers that accumulate 50% of the citations is
about 14%, but it may be below 10% for journals with a low impact
factor and around 20% for journals with a high impact factor.
Despite this correlation with impact, it is obvious that the
impact factor of a scientific journal is not a
totum pro parte for its individual papers
[1–4]. Obviously, for the assessment
of the quality of scientific papers there is no alternative
to reading... as pointed out previously by Sidney Brenner (see
Ref. [3] for source).
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References
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- Anonymous. Deciphering impact factors. Nat. Neurosci. (2003) 8:783.
- Opthof T. Sense and nonsense about the impact factor. Cardiovasc. Res. (1997) 33:1–7.[Abstract/Free Full Text]
- Seglen P.O. Why the impact factor of journals should not be used for evaluating research. BMJ (1997) 314:498–502.[Free Full Text]
- Opthof T., Coronel R. The impact factor of leading cardiovascular journals: where is your paper best cited? Neth. Heart J. (2002) 10:198–202.
- De Jong J.W., Schaper W. The international rank order of clinical cardiology. Eur. Heart J. (1996) 17:35–42.[Abstract/Free Full Text]

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