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PII: S0090-4295(19)31088-X
DOI: https://doi.org/10.1016/j.urology.2019.11.033
Reference: URL 21885
Please cite this article as: Alan Paniagua Cruz BS , Kevin Y. Zhu , Chad Ellimoottil MD, MS ,
Casey A. Dauw MD , Aruna Sarma PhD , Ted A. Skolarus MD, MPH , Characterizing the
benign prostatic hyperplasia literature: a bibliometric analysis, Urology (2019), doi:
https://doi.org/10.1016/j.urology.2019.11.033
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Alan Paniagua Cruz, BSa, Kevin Y. Zhub, Chad Ellimoottil, MD, MSc,
Casey A. Dauw, MDc, Aruna Sarma, PhDc, Ted A. Skolarus, MD, MPHd
a
University of Michigan Medical School, Ann Arbor, MI, bUniversity of Michigan, Ann
Arbor, MI, cMichigan Medicine Department of Urology, Dow Division of Health Services
Research, Ann Arbor, MI, dVeterans Affairs Ann Arbor Healthcare System,
Ann Arbor, MI
Disclosures: This work was accepted as a moderated poster for the 2019 Annual
Meeting of the American Urological Association in Chicago, Illinois.
Corresponding Author:
Ted A. Skolarus, MD, MPH, FACS
Associate Professor of Urology University of Michigan
Urology Section Chief
VA Ann Arbor Healthcare System
Research Investigator
VA HSR&D Center for Clinical Management Research
Phone: (734) 647-9712
Fax: (734) 232-2400
tskolar@med.umich.edu
ABSTRACT
examining the impact of academic literature. We used the following search terms and
Boolean logic “(“benign prostat*”) AND (hyperplasia OR enlarg*)” and characterized the
100 most-cited BPH articles through 2018 including citations, journal, author, year, and
country.
RESULTS: The top 100 BPH articles were published between 1978 and 2012. Citations
journals. The Journal of Urology was the most published journal (n=25), followed by
European Urology (n=17), and Urology (n=15). In general, the oldest 10 articles focused
was the most productive decade with nearly half of the top 100 articles (n=44). Twenty-
six different countries contributed to the top 100 articles, with the US (n= 74), Italy
CONCLUSIONS: This study represents the first bibliometric analysis of the leading BPH
articles impacting the academic literature. The focus has evolved from BPH
These findings may guide research priorities for this increasingly common condition.
ABBREVIATION KEY
INTRODUCTION
that affects older men.1 The prevalence of BPH and its associated disability, ranging
make this disease a public health priority. Indeed, decades of research have provided
While the current academic BPH literature is extensive, its current state has not
and research gaps, as well as to guide future funding priorities. For example, assessing
the scientific literature has been used to guide research and practice priorities ranging
investments.4 Despite the increasing relevance of BPH to our aging male population,
there are no empirical studies characterizing the most influential BPH articles currently
impacting the field. One increasingly common approach to assess the impact of
network analysis, citation indices, and impact factors, bibliometrics can be used to
objectively evaluate the impact of articles, researchers, and journals for a given field.
This approach is increasingly applied to urology (e.g., hypospadias, ureteral reflux,
prostate cancer), though it has yet to be applied to BPH where its population-based
landscape of academic BPH literature. We examined the most commonly cited articles,
authors, institutions, countries, journals, and content areas impacting the field over time.
Not only do our novel findings highlight the most influential BPH literature to date, they
may also help guide research and funding priorities to advance the translation of BPH
research to practice.
METHODS
created by the Institute of Scientific Information and now owned by Clarivate Analytics. 10
Through its platform, the Web of Science Core Collection™ connects to regional citation
indexes, patent data, and specialized citation indexes, covering book series, conference
proceedings, and over 33,000 journals.11 Similarly, Scopus™ and Google Scholar™ can
also be used for citation indexing. Although Scopus™ is believed to offer broader
content coverage, it only covers articles published after 1960. Furthermore, journals
present in Scopus™ and not Web of Science™ have been shown to have lower citation
impact, although it is unclear if this holds true for BPH literature. 10 Google Scholar™,
on the other hand, offers the most literary coverage, but “suffers from a lack of quality
control” resulting in numerous inaccuracies.10 For these reasons, we conducted our
Search methodology
To identify the top cited articles in the BPH literature, we performed our search
through the Web of Science™ Database (v.5.31) on December 12th, 2018. A Boolean
search was conducted using the terms “(“benign prostat*”) AND (hyperplasia OR
enlarg*)” with the largest timespan allowed through the Web of ScienceTM (“all years
(1864 – 2019)”). In order to reduce English publication bias, we conducted our search
under the “all databases” option; which included the Web of Science™ Core Collection,
KCI Korean Journal Database, MEDLINE®, Russian Science Citation Index, ScIELO
Citation Index, and Zoological Record. We limited our results to articles and reviews and
Literature review
Two authors (APC and KYZ) independently assessed the content of our search
results. They reviewed the titles of all identified articles and the abstracts of articles
requiring further content validation confirming that the article indeed included BPH
Bibliometric analysis
institution, country, category, and journal of publication. We further provided the h-index
and e-index for authors with multiple publications in the top 100 to highlight their overall
complement the h-index and represents the square root of excess citations not
incorporated into the h-index calculation. 12,13 Moreover, we retrieved the median
citation per article (MCA) and median citation per review (MCR) from Clarivate
Analytics’ Journal Citation Reports for journals that published the top 100. Unlike the
journal impact factor, which has become a misused and gameable metric, the median
citation per article/review is a more helpful representation of the total number of citations
14
a typical paper is expected to receive when published in a specific journal.
Citation indices
For the top 100 BPH articles, we then calculated an Adjusted Citation Index (ACI)
publication age.9,15 As shown previously, this is one way to account for the higher
number of citations seen in older articles resulting from greater “exposure time.” For
instance, in 2019, an article published in 1969 with 100 citations would have an ACI of
2.0, while an article published 2009 with 35 citations would have an ACI of 3.5. Altmetric
Attention Scores (AAS) were also provided to offer insight into an article’s online
dissemination. AAS are weighted scores that reflect online attention an article has
better understand the relationships between the ACI and publication characteristics, we
also studied the associations between ACI and number of authors, cited references,
MCA, MCR, AAS, and years since publication using non-parametric (Spearman’s)
correlation.17
All analyses were conducted between December 2018 and October 2019. This
study was deemed exempt from the Institutional Review Board at the University of
Michigan.
RESULTS
Our initial search yielded 12,576 publications. After limiting our results to articles
and reviews, 7,932 publications remained. Next, we rank ordered each article according
to its number of citations and selected the first 100 as our top 100 BPH articles. All of
these articles were written in English and published between 1978 and 2012. As
illustrated in the Figure, nearly half (44%) of articles were published in the 1990’s,
followed closely by the 2000’s with 39%. Taken together, over 80% of the most
We found total citation counts ranged from 153 to 2,171, with a median and
mean of 206.5 and 282 citations per article, respectively. Over 50% of total citations
were from the top 28 articles, with the three leading articles having over 1,000 citations
each. As shown in Table 1, the most cited article was published in 1992 by Barry et al.
and described the development and validation of the American Urological Association
symptom index for BPH. The second most cited article was from Berry et al. in 1984
and characterized the prevalence and development of BPH with age. The third most
cited article from McConnell et al. in 2003 presented randomized controlled trial results
from the Medical Therapy of Prostatic Symptoms Study (MTOPS) evaluating the long-
term effects of doxazosin, finasteride, and combination therapy, on the clinical
progression of BPH. In general, the oldest 10 articles in the top 100 focused on the
etiology and pathogenesis of BPH, while the newest 10 tended to examine BPH
After calculating the ACI in order to adjust for publication date, “The American
Urological Association symptom index for benign prostatic hyperplasia” by Barry et al.
remained the most frequently cited publication with an average of 83.1 citations per year
(Table 1). Calculating the ACI resulted in significant changes in citation ranks, with one
article moving up 71 positions in ranking and another article dropping 60. Only three
publications did not change positions, remaining in positions 1, 9, and 87. Seven of the
10 most cited articles remained in the top 10 after adjusting for publication year.
Furthermore, we found significant correlations between the ACI and years since
publication (rho= -0.62, p <0.001), number of authors (rho= 0.28, p = 0.005), MCA (rho=
0.48, p <0.001), and AAS (rho= 0.45, p <0.001). However, we did not find a correlation
was the most published journal with 25 top 100 BPH articles, followed by European
Urology (MCA: 9, MCR: 14) with 17, and Urology (MCA: 1, MCR:2) with 15. The New
England Journal of Medicine (MCA: 36, MCR: 26) was the most published general
medical journal with 9 articles, five of which were in our top 10 most cited list. The Web
of Science classified the majority of the articles under the Urology Nephrology category
(n=69).
In terms of authorship, 7 authors had two or more first author publications, and
23 institutions had five or more BPH articles in the top 100 (Table 3 and Supplementary
Table 1, respectively). The most published author, C.G. Roehrborn (h-index: 78, e-
index: 99.2), had 9 first-authorships and 15 total articles in the top 100 BPH articles.
The success of C.G. Roehrborn coincided with The University of Texas System being
the most accomplished institution. Lastly, the United States had the most articles in the
top 100 (n=74), followed by Italy (n=19), and Canada (n=12) (Supplementary Table 2).
DISCUSSION
We characterized the top 100 most-cited articles in the BPH literature to date.
We found nearly a quarter of the articles were responsible for half of the total citations,
and that higher journal MCA, article AAS, and more co-authors were associated with an
increasing adjusted citation index. Ten urology-specific journals accounted for 69% of
the articles, with a few authors having more than a single publication in the top 100. All
of the publications in the top 100 were written in English, and the majority originated
from the United States and its institutions. In general, the oldest 10 articles in the top
100 focused on the etiology and pathogenesis of BPH, while the newest 10 tended to
examine BPH treatment and outcomes. Collectively, these findings suggest the most
cited BPH literature originates from a small subset of journals, authors, and countries
We discovered an interesting shift during the last few decades from attempts to
better understand the pathophysiology and characterize the evolving impact of BPH on
functional outcomes through a period of randomized medical therapy trials to the most
recent high-impact literature focused on efficacy of medical and surgical BPH
treatments. This could be due to the recent expansion of the BPH drug and surgical
therapy armamentarium. Indeed, there are over a dozen BPH treatment options ranging
from monotherapy with alpha-blocker drugs (e.g., tamsulosin) and combination therapy
techniques. This could also be reflective of research funding trends to study BPH. For
example, the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK)
funded the “Minimally Invasive Surgical Therapy Consortium for Benign Prostatic
Hyperplasia” in 2003.18 This clinical trial looked to compare the efficacy and safety of
therapy (TUMT), and medical therapy with alfuzosin and finasteride. Furthermore, in
July 2015, the NIDDK provided a research update on two independent studies
evaluating the role of fibrosis in BPH and its potential for development of future
therapies.19 Going forward, policy decisions regarding the best use of research funds to
advance prostate health for our aging population will need to consider these findings
and where the best value for the research investment may come from.
Our study adds to the growing characterization of the most cited literature in
urology and urologic diseases.6 Previous investigators have used bibliometric analyses
studies, our study indicates a minority of articles are responsible for the majority of
Garfield, the creator of the impact factor.20 At times, 20% of the articles can account for
were from the United States. Previous bibliometric analyses have shown similar
and those investing more in research and development tend to have higher biomedical
research output.22 These factors help explain the international distribution of our leading
BPH literature.
Our results showing a significant shift in article ranking when calculating the ACI
are also consistent with other investigators.9,15 Such large shifts can be due to older
articles with a high total citation count, but a diminishing citation rate, or to younger
articles with a high early citation count. By using the ACI, we attempted to account for
the influence of time on total citations. The use of total citations and ACI can both be
used to characterize articles as in this study. Interestingly, articles with a high total
citation count and low ACI are more likely to represent “historical interest, and may not
reflect current knowledge, controversy, and clinical applications of the topic.”15 This is
the case in our study with the 1978 article by McNeal et al. describing the origin and
evolution of benign prostate enlargement. While in the top 10 for total citations, after
adjustment, this article fell to 58 indicating its historical nature. Ideally, we would be able
between ACI, years since publication, and number of authors, but adds to the literature
by also showing associations with MCA, and AAS.17 The negative association between
ACI and years since publication in this study indicates a majority of our top 100 articles
were composed of older articles with decreasing citation rates. This is in line with
citation dynamics where a scientific article reaches its maximum citation rate 3 to 10
years after publication, and slowly declines afterward.23 Our findings also show that a
journal’s MCA positively correlates with ACI, underscoring the notion that article
interestingly found a positive association between ACI and AAS, meaning that articles
with higher average citation counts, tended to receive more online attention as
Huang et al., but this involved total citation counts.24 Further research is needed to see
Our study should be considered in the context of several limitations. First, there
is no known association between citation count and study quality. An article may be
both positively and negatively cited by other articles. Citations are also only capable of
measuring the impact of papers to authors of other papers, and do not measure the
authors may inflate their citation counts via self-citations. Although this is a possibility,
the broad author distribution in our top 100 articles indicates this would be unlikely to
impact our findings. Third, we only utilized one database when conducting our search.
publications when compared to other databases like Scopus™. Although none of our
top 100 articles were published before 1960, we believed it was important to not limit
our initial search. Furthermore, Web of Science™ provides greater transparency with
regard to coverage than do other resources, like Google Scholar™.10 Therefore, the
benefits of using Web of Science™ in this study outweigh potential limitations. Finally, it
is possible that our search did not provide an exhaustive review of the BPH literature.
However, the breadth of databases available through the Web of Science™, our study
time frame (1864 – 2019), and face-validity of our findings minimizes the risk our study
leading BPH literature to date. We found the most cited BPH articles originate from a
small subset of journals, authors, and countries. These findings may be used to guide
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FIGURE LEGEND
The 1990’s were the most prolific decade with almost 50% (n=44) of the publications for
the top 100 articles. Furthermore, greater than 80% of the publications occurred in the