Article

The uterine fibroid/myoma tumour: analysis of the global

research architecture using density-equalizing mapping

Dörthe Brüggmann a,b,c,*, Frank Louwen a, Tatjana Braun b, Doris Klingelhöfer b,

Jan Bauer b, Michael H Bendels b, Matthias Bundschuh b, David Quarcoo b,
Jenny Jaque c, Eileen M Wanke b,1, David A Groneberg b,1
a
Department of Gynecology and Obstetrics, Goethe-University, Frankfurt, Germany
b
Division of Social Medicine and Epidemiology, Institute of Occupational Medicine, Social Medicine and Environmental Medicine,
Goethe-University, Frankfurt, Germany
c
Department of Obstetrics and Gynecology, Keck School of Medicine of USC, Los Angeles, California, USA

Dörthe Brüggmann is a board-certified gynaecologist at the OB/GYN Department, Goethe-University, Frankfurt,

Germany, and holds a joint position in the Division of Female Health/Prevention at the Institute of Occupational,
Social and Environmental Medicine. Additionally, she serves as an Adjunct Professor in the OB/GYN Depart-
ment at the USC Keck School of Medicine in Los Angeles.

KEY MESSAGE
This study represents the first global description of the uterine fibroid research landscape over the past century.
The multitude of quantitative and semi-qualitative dimensions that were presently assessed demonstrates
that this field of OB/GYN clearly differs from other fields and is closely related to surgical and diagnostic issues.

A B S T R A C T

Uterine fibroids can severely impact a woman’s quality of life, result in significant morbidity and are a leading indication for hysterectomy. Many aspects
of the disease remain largely obscure. Despite these knowledge gaps, no detailed maps of the global fibroid research architecture have yet been gen-
erated. This study used the NewQIS approach to assess worldwide research productivity, encompassing numerous aspects of the scientific output, quality
and socioeconomic features. Regression analysis indicated an increase in fibroid research activity in the investigated time periods. Global research
output was dominated by leading Western countries, with the USA at the forefront, but also by East Asian countries. Socioeconomic benchmarking
revealed that Taiwan had the highest fibroid research activity per GDP, with a calculated average of 279.46 fibroid-related publications per 1000 billion
USD GDP. Finland was the most active country with respect to research activity per population size. Subject area analyses revealed major differences
in research focuses, for example ‘Radiology, Nuclear Medicine and Medical Imaging’ was assigned to 29.92% of South Korean and to only 10.38% of
US-American publications. In conclusion, this analysis of global fibroid research activity illustrates a multitude of important features ranging from quan-
titative and semi-qualitative fibroid research aspects to socioeconomic benchmarking.
© 2017 Published by Elsevier Ltd on behalf of Reproductive Healthcare Ltd.

* Corresponding author.
E-mail address: brueggmann@med.uni-frankfurt.de (D Brüggmann).
1
These authors contributed equally to this work.
https://doi.org/10.1016/j.rbmo.2017.10.112
1472-6483/© 2017 Published by Elsevier Ltd on behalf of Reproductive Healthcare Ltd.
228 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238
Introduction
Uterine fibroids or leiomyomas represent the most common benign
tumour of the female genital tract (Downes et al., 2010; Lumsden et al.,
2015; Sparic et al., 2016). Matthew Baille first described these mono-
clonal tumours originating from uterine myometrium, in 1793 (Sparic
et al., 2016). A woman over 45 years of age has a fibroid lifetime risk
of more than 60% as estimated in longitudinal studies (Okolo, 2008).
However, the accurate prevalence of fibroids is largely unknown
because the majority remain asymptomatic and undiagnosed. In a
population-based study conducted in the USA, 51% of randomly se-
lected premenopausal women with no previous history of myomas
received an ultrasound-based diagnosis of uterine fibroids (Baird et al.,
2003). The incidence of leiomyomas is up to three-fold greater in black
women, who develop these tumours at earlier ages than white females
(Baird et al., 2003). Uterine fibroids become clinically apparent in only
up to 40% of women aged 40 years and over (Okolo, 2008). Also, their
incidence based on histology is more than twice the clinical inci-
dence (Okolo, 2008; Sparic et al., 2016). Leiomyomas cause significant
morbidity due to abnormal uterine bleeding and pelvic pressure symp-
toms. Hence, they have great impact on the quality of life of many
women and the healthcare system in general (Okolo, 2008; Sparic et al.,
2016).
Recently published reviews concluded that more research is
necessary to determine the risk factors associated with fibroid onset
and growth (Commandeur et al., 2015; Drayer and Catherino, 2015).
Also, no clear insight into uterine fibroid epidemiology has yet been
achieved. Future research into the genetic background and modifi-
able risk factors may shed light on fibroid prevention and provide
new approaches to non-surgical and surgical fibroid treatment
(Sparic et al., 2016; Yang et al., 2016). It is for these reasons, as well
as the high myoma prevalence, that further multidisciplinary, trans-
lational and clinical research is needed. To plan new research
strategies and to supply decision-makers with information concern-
ing funding strategies, scientometric approaches may be of help for
uterine fibroid research. It is therefore the objective of the present
study to assess scientific performance in the field of uterine fibroid
research over the past century using the tools of the ‘New Quality
and Quantity Indices in Science’ (NewQIS) platform (Groneberg-Kloft
et al., 2009a, 2009b). The project combines scientometric tools and
advanced density-equalizing mapping procedures (Gastner and
Newman, 2004) to assess the global uterine fibroid research
architecture.
Materials and methods
NewQIS protocol
The present study was facilitated by the NewQIS platform
(Groneberg-Kloft et al., 2009a, 2009b). We established this comput-
ing platform in 2009 as an international, multidisciplinary project, and
it has been used to assess more than 50 different biomedical enti-
ties to date. The NewQIS platform approach encompasses advanced
visualization algorithms such as Gastner and Newman’s density-
equalizing calculations, indices modified for country-specific
contributions to the current body of literature based on the concept
of the Hirsch index (h-index) (Hirsch, 2005, 2007) and other
scientometric tools in order to evaluate and visualize uterine
fibroid-specific research activity (Groneberg-Kloft et al., 2013; Kusma
et al., 2009; Vitzthum et al., 2010).
Data source and search algorithms
The Web of Science database (WoS, Thomson Scientific) was em-
ployed for data collection as described in previous NewQIS studies
(Gerber et al., 2014; Koster et al., 2016). The following search strat-
egy was used to identify fibroid-related research data: fibroid* OR
fibroma* OR fibromyoma* OR leiomyoma* OR myoma* [Title] and
uteri* OR uterus OR myometr* OR myomectom* OR hysterectomy OR
GnRH OR emboli*ation OR *fertil* OR reproduct* OR pregnan* OR
abort* OR miscarriage* OR pelvi* OR gynecolog* OR obstetric*
OR menorrhagia OR bleeding OR anemia OR oestrogen OR steroid*
OR *menopaus* OR black OR afroamerica* OR nullipar* OR submu-
cous OR intramural OR subsero* OR intracavitar* OR cervi* [Topic]
NOT cutan* OR skin OR *esophag* OR gastr* OR gallbladder OR liver
OR spine [Title] NOT ‘gastrointestinal bleed*’ OR ‘GI bleed*’ OR ‘rectal
bleed*’ OR ‘vaginal leiomyoma*’ OR *nasal OR ‘*vascular leiomyoma*’
OR ‘jejunal leiomyoma*’ OR ‘duodenal leiomyoma*’ OR ‘leiomyoma*
of the duodenum’ OR ‘leiomyoma* of the jejunum’ OR appendiceal
leiomyoma OR ‘intestinal leiomyoma*’ OR ‘Leiomyoma* of the urinary
bladder’ OR ‘bladder leiomyoma*’ OR urethral leiomyoma OR ‘cardi*
leiomyoma*’ OR ‘cardi* fibroma*’ OR chondromyxoid OR fibromato-
sis OR ‘leiomyoma of the breast’ OR ‘skin leiomyoma*’ OR ‘*esophag*
leiomyoma*’ OR ‘gastr* leiomyoma*’ OR ‘colon* leiomyoma*’ OR
‘benign metastasizing leiomyoma*’ OR ‘mesosalphinx leiomyoma*’
OR ‘fibroma* of the jaw*’ OR odontogenic OR ‘Collagenous Fibroma*’
OR ‘Nuchal Fibroma*’ OR ‘leiomyoma of the vulva’ OR ‘soft tissue leio-
myoma’ OR male OR ‘black bear’ OR ‘Colon* Polyp’ OR ‘endocardial
fibroma*’ OR ‘*pharyngeal fibroma*’ OR ‘ventricular fibroma’ OR ‘pul-
monary emboli*ation’ OR ‘ovar* leiomyoma*’ OR ‘ovar* fibroma*’ OR
bone [Topic].
The search covered the time period between 1900 and 2015. This
search term was entered in the WoS as described previously for other
areas of medicine (Groneberg et al., 2016; Quarcoo et al., 2015; Scutaru
et al., 2010). All document types were included in the analysis.
Data analysis and categorization
As previously described, retrieval of the metadata with exact biblio-
graphic details of all uterine fibroid-related publications was followed
by numerous sorting and analysing steps (Groneberg et al., 2015;
Ohlendorf et al., 2015; Scutaru et al., 2010). These steps included analy-
sis for originating countries, languages, document types, citations,
cited references, year published and subject categories. Then, amongst
other things, research-specific, country-specific h-indices were con-
structed. The h-index was developed by Jorge Hirsch in 2005 in order
to gauge the quality attributed to the scientific achievement of single
authors (Hirsch, 2005, 2007). The concept was used here particu-
larly to assess country-specific uterine fibroid research, as described
previously for other diseases (Groneberg-Kloft et al., 2009a, 2009b;
Hirsch, 2005).
Economic analysis
In order to assess the relative contributions of highly active nations
in uterine fibroid research with regard to their socioeconomic status
and financial resources, the national gross domestic product (GDP)
 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238
was related to the country-specific uterine fibroid research activities.
Economic facts and the classification of countries according to their
income were obtained from the World Factbook (CIA, 2015).
Density-equalizing mapping procedures
The core technique of the NewQIS program consists of an algo-
rithm that generates world maps visualizing quantitative and qualitative
assessments in a specific research area (Groneberg-Kloft et al., 2008a,
2008b; Kusma et al., 2009; Vitzthum et al., 2010). In the present study,
fibroid research-specific world maps were generated using density-
equalizing mapping procedures (DEMP): after transfer of the metadata
to Excel charts and parameter analysis, uterine fibroid-specific DEMPs
were created based on methods previously published by Gastner and
Newman (2004). The territories of the different fibroid research-
publishing countries were separated from each other and resized in
proportion to the selected fibroid research-specific variable of inter-
est (i.e. country-specific h-indices).
Analysis of uterine fibroid research collaborations
To analyse national and international research collaborations, all af-
filiations of authors that published fibroid-specific publications were
collected and investigated as previously described for other dis-
eases (Carl et al., 2014). A relationship of two authors was identified
as a collaboration if they worked in different countries and contrib-
uted to the same publication. A chart diagram was constructed with
vectors representing the quantity of the collaborative work by their
width and shade of grey.
Results
Density-equalizing mapping
Between 1900 and 2015 a total of 6176 documents related to uterine
fibroids were identified. The first 20 publications were authored in 1900.
From the 1990s to the new millennium, around 100 publications were
published each year. After 2002 this number increased to more than
200 articles per year, and from 2013 onwards more than 300 ar-
ticles per year were authored (Figure 1A). Regression analysis from
1970 to 2015 identified an r2 value of 0.91. In the country-specific analy-
sis, authors from 95 countries participated in uterine fibroid research
with scientists from the USA displaying the highest fibroid research
activity (n = 2185 fibroid-related publications). They were followed by
the UK with n = 411 publications, Japan (n = 407), Germany (n = 310),
Italy (n = 309), China (n = 243), France (n = 207), Canada (n = 152),
Taiwan (n = 148) and South Korea (n = 137) (Figure 1B). DEMP analy-
sis visualized the research activity of individual countries by the
distortion of the global map with a focus on North America, Europe
and Far East Asia including Japan, China, Taiwan and South Korea
(Figure 1B).
The total citation analysis indicated a leading position of the USA
with a total of n = 41,524 citations related to fibroid-specific publi-
cations. This was followed by the UK (n = 6984) and Japan (n = 5974)
(Figure 2A). Fibroid-specific h-index analysis for each country also
showed a leading position of the USA with an h-index of 92, meaning
that 92 fibroid-related publications authored by US-American scien-
tists were being cited at least 92 times. The USA was followed by
229
the UK (h-index = 44), Japan and Italy (h-index = 40 each) (Figure 2B).
The average citation number per fibroid publication attributed to
every country investigated was analysed. This number was
termed the citation rate (cr). Countries that published fewer than 30
myoma publications were excluded from this particular analysis. In
the cr ranking, Sweden was leading the field with a cr of 22.78,
followed by Finland (cr = 21.95). The USA had a cr of 19.00 and
articles from the UK received 16.99 average citations per publica-
tion (Figure 2C).
Socioeconomic analysis of uterine fibroid research
In order to assess uterine fibroid research activities with regard to
the socioeconomic status of a country, the GDP of each country in
1000 billion (bn) USD was used, serving as a proxy measure for
total economic strength and resources that can be dedicated to
research. Among high-income countries, Taiwan was ranked first
with 148 uterine fibroid-related research papers and a calculated
average of 279.46 fibroid-related publications per 1000 bn USD
GDP (RGDP). It was followed by Israel (RGDP = 266.62), and Finland
(RGDP = 243.36) (Table 1). The UK had an RGDP = 139.56, and the USA
reached an RGDP of 125.43. Turkey was identified as the upper middle-
income country with the highest RGDP (169.95) whereas China had a
RGDP value of 23.41.
Also, the country-specific uterine fibroid publications were related
to the population size. Here, Finland was the most active high-
income country with 12.55 publications per million inhabitants (Rpop),
followed by Israel (Rpop = 10.36), Sweden (Rpop = 7.92), Belgium (Rpop
= 6.90) and the USA (Rpop = 6.85) (Figure 3A). In the upper middle-
income country ranking, Turkey was ranked in first position with an
Rpop of 1.68, followed by South Africa (0.66). China had an Rpop of 0.18
(Table 1). When the economic strength of a country was analysed using
the GDP in bn USD per capita (Rpc), the USA was ranked as the first
high-income country with an index of Rpc = 39.87, followed by the UK
(Rpc = 10.90) and Japan (Rpc = 10.77) (Figure 3B, Table 1).
Fibroid research subject area analysis
In the past two decades, the leading subject categories of uterine fibroid
research included ‘Obstetrics and Gynecology’, ‘Reproductive Biology’
and ‘Radiology, Nuclear Medicine and Medical Imaging’. Between 1966
and 2015, the chronological development of the subject areas was
analysed in greater detail: we noted a prominent increase in the pub-
lication number in the field of ‘Reproductive Biology’, with a growth
of 17.1% between 1986 and 1990 and of 23.4% between 2011 and 2015.
It was striking that ‘Public Health’ did not belong to the most active
subject areas in myoma research (Figure 4A). When subject area
analysis was conducted for highly active uterine fibroid research coun-
tries, major differences were found for the field of ‘Radiology, Nuclear
Medicine and Medical Imaging’. Here, South Korea’s proportion to-
talled 29.92% while only 10.38% of publications dedicated to this area
were attributed to the USA (Figure 4B).
International uterine fibroid collaborations
In total, 476 international collaborations (n) contributed to the 6176
overall publications. The USA was the most active country, partici-
pating in 268 collaborative relationships representing 56.3% of all
international collaborations. The USA was followed by the UK, with
n = 91 collaborations, Italy (n = 73) and Germany (n = 72), respectively.
230 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238

Figure 1 – Density-equalizing map of global uterine fibroid research activity. (A) Number of publications. (B) Number of published items
per year.

The most common bilateral collaborations were found between US- France (155 institutions). In China, 142 institutions were working on
American scientists and their Italian, Canadian and German uterine fibroid research (Figure 6).
counterparts (Figure 5).

Number of institutions per country Discussion

The number of institutions per country devoted to uterine fibroid re-
search was also analysed using DEMP techniques. Figure 6 illustrates
that 720 different US-American institutions participated in fibroid re-
search. The USA was followed by Japan (224 institutions), the UK (211
institutions), Germany (165 institutions), Italy (161 institutions) and
Uterine fibroids represent the most common benign tumours of the
female reproductive system. They cause significant morbidity and de-
terioration in the quality of life of many women worldwide (Downes
et al., 2010; Sparic et al., 2016). It has been estimated that about 40–
60% of all hysterectomies are due to the presence of uterine fibroids
 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238 231

Figure 2 – Density-equalizing maps of global uterine fibroid research quality. (A) Total number of fibroid-specific citations per country.
(B) Fibroid-specific h-indices. (C) Fibroid-specific citation rates (threshold of 30 publications per country).

(Fleischer et al., 2008; Sparic et al., 2016). The pathophysiology of
myomas is still largely obscure, with altered smooth muscle cell pro-
liferation and disordered angiogenesis playing prominent roles
(Fleischer et al., 2008). Because the cause of uterine fibroids remains
unclear and their biology is poorly understood (Okolo, 2008), new re-
search efforts are needed. Therefore, this analysis was performed
to present preliminary data on the global background of fibroid re-
search over the past century. In contrast to the numerous studies
already existing for OB/GYN entities such as endometriosis
(Brüggmann et al., 2016a, 2016b), Caesarean section (Brüggmann et al.,
2015), gestational diabetes (Brüggmann et al., 2016a, 2016b), breast
cancer (Glynn et al., 2010; Healy et al., 2011) or polycystic ovary
232 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238

Table 1 – Socioeconomic analysis of fibroid research of the most active countries.

Country No. of GDP in GDP per Population Articles/GDP Ranking 1 Articles/ Ranking 2 Articles/ Ranking 3
articles 1000 bn capita total in mill. in 1000 bn GDP per population
USD USD capita in mill.
Finland 66 0.2712 40.5 5.26 243.36 HI3 1.63 HI19 12.55 HI1
Israel 81 0.3038 33.4 7.82 266.62 HI2 2.43 HI12 10.36 HI2
Sweden 77 0.5701 44.7 9.72 135.06 HI8 1.72 HI18 7.92 HI3
Belgium 72 0.5347 41.7 10.44 134.65 HI9 1.73 HI17 6.90 HI4
USA 2185 17.42 54.8 318.9 125.43 HI10 39.87 HI1 6.85 HI5
UK 411 2.945 37.7 63.74 139.56 HI7 10.90 HI2 6.45 HI6
Taiwan 148 0.5296 43.6 23.35 279.46 HI1 3.39 HI10 6.34 HI7
Switzerland 48 0.7121 55.2 8.06 67.41 HI20 0.87 HI21 5.96 HI8
Netherlands 100 0.8664 47.4 16.87 115.42 HI12 2.11 HI14 5.93 HI9
Italy 309 2.148 34.5 61.68 143.85 HI6 8.96 HI4 5.01 HI10
Australia 106 1.444 46.6 22.5 73.41 HI18 2.27 HI13 4.71 HI11
Denmark 26 0.3408 44.3 5.56 76.29 HI17 0.59 HI23 4.68 HI12
Greece 49 0.238 25.8 10.77 205.88 HI4 1.90 HI16 4.55 HI13
Canada 152 1.789 44.5 34.83 84.96 HI15 3.42 HI8 4.36 HI14
Germany 310 3.86 44.7 80.99 80.31 HI16 6.94 HI5 3.83 HI15
Austria 29 0.4371 45.4 8.22 66.35 HI21 0.64 HI22 3.53 HI16
Japan 407 4.616 37.8 127.1 88.17 HI14 10.77 HI3 3.20 HI17
France 207 2.847 40.4 66.25 72.71 HI19 5.12 HI6 3.12 HI18
South Korea 137 1.41 35.4 49.03 97.16 HI13 3.87 HI7 2.79 HI19
Czech Republic 25 0.2057 28.4 10.62 121.54 HI11 0.88 HI20 2.35 HI20
Poland 83 0.5466 24.4 38.34 151.85 HI5 3.40 HI9 2.16 HI20
Spain 93 1.407 33 47.73 66.10 HI22 2.82 HI11 1.95 HI21
Turkey 137 0.8061 19.6 81.61 169.95 UMI1 6.99 UMI2 1.68 UMI1
South Africa 32 0.3501 12.7 48.37 91.40 UMI2 2.52 UMI4 0.66 UMI2
Brazil 86 2.353 15.2 202.6 36.55 UMI4 5.66 UMI3 0.42 UMI3
Russia 48 1.857 24.8 142.47 25.85 HI23 1.94 HI15 0.34 HI22
Egypt 27 0.2864 11.1 86.89 94.27 LMI1 2.43 LMI2 0.31 LMI1
Iran 25 0.4041 16.5 80.84 61.87 UMI3 1.52 UMI5 0.31 UMI4
China 243 10.38 12.9 1355.7 23.41 UMI5 18.84 UMI1 0.18 UMI5
India 98 2.05 5.8 1236.3 47.80 LMI2 16.90 LMI1 0.08 LMI2
Sources for GDP (current prices in 1000 bn US dollars) and GDP per capita (current prices in 1000 US dollars): International Monetary Fund.
HI = high-income country; LMI = lower middle-income country; UMI = upper middle-income country.
Threshold 25 fibroid-related publications.

syndrome (Brüggmann et al., 2017a, 2017b, 2017c), detailed
density-equalizing maps do not yet exist for the field of uterine fibroid
research.
We want to address some limitations before discussing the main
findings of the study: as previously stated, one limitation of this study
is based upon the fact that the WoS includes predominantly jour-
nals published in the English language (Brüggmann et al., 2017a,
2017b, 2017c). Therefore, non-English articles may be under-
represented in our search. However, scientists usually publish their
high-quality research in English journals, which limits this particu-
lar bias. Another bias is linked to our investigated parameters based
on citation counts. High citation numbers are believed to reflect high
scientific quality. However, this relationship is biased by the so-
called Matthew effect (Merton, 1968): publications by renowned
scientists will be cited more than works by lesser known scientists.
Boosted mainly by the author’s popularity in the field, the citation count
of these papers increases exponentially right after publication (Merton,
1968).
From a historical perspective, general uterine fibroid research ac-
tivity over the past decades develops similarly to other areas of science.
We identified only minimal scientific activity until the 1970s. During
the following two decades, a strong increase in research productiv-
ity was noted. Publication numbers in the field have increased
dramatically since the late 1990s and reached the striking output of
300 annual publications after 2013. Interestingly, the nature of uterine
fibroid research differs from other gynaecological disorders. This can
be concluded from the subject area analysis, in which a large per-
centage of publications was attributed to subject areas such as
‘radiology’, whereas public health issues were of limited interest. By
contrast, researchers in ‘gestational diabetes’ or ‘caesarean section’
also dedicated their scientific activity to the important field of ‘Public
Health’ (Brüggmann et al., 2015, 2016a, 2016b). However, uterine fi-
broids are reported to be the most common indication for hysterectomy
in the USA and Australia (Fleischer et al., 2008; Sparic et al., 2016)
and burden many women around the globe by affecting their quality
of life. Hence, we underline the imminent need to target this tumour
by interventions in the field of public health. Funding agencies may
pay specific attention to grant proposals in this area focusing on or-
ganized efforts raising awareness and implementing interventions
within the society, organizations or the community.
From a country-specific viewpoint, the pattern of uterine fibroid
research productivity largely parallels research activity in other areas
of biomedical sciences (Groneberg-Kloft et al., 2008a, 2008b). High-
income countries – the USA in particular – are leaders in the field
of uterine fibroid research. This finding is not surprising due to the
surgical (i.e. novel approaches) and technical (i.e. diagnostic) equip-
ment required for the medical care of leiomyoma patients and related
research, which is dependent on a high level of industrialization (‘high
 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238 233

Figure 3 – Density-equalizing maps of global uterine fibroid research socioeconomic figures. (A) Publications/population in mill.
(B) Publications/GDP in 1000 billion (bn) USD, threshold: ≥ 30 specific publications.

tech’). Within our study, a particularly outstanding position was oc-
cupied by the USA. Besides its dominance regarding the overall
research activity related to myomas, the USA was also found in the
leading position when analyses of the total citation count or the
country-specific h-indices were performed. We attribute this promi-
nent role of the USA to the outstanding overall resources this country
attributes to research and development in general, e.g. 2.7%
of its GDP in 2013 (http://databank.worldbank.org/data/reports
.aspx?source=2&series=GB.XPD.RSDV.GD.ZS&country) supporting the
highest number of institutions working on fibroids within the com-
munity. Apart from this dominant role of US-American institutions,
the UK, Japan and Germany are the most active countries in fibroid
research. A similar pattern was revealed in a global research output
study that analysed a total of 5,527,558 publications in diverse fields
of medicine (Groneberg-Kloft et al., 2008a, 2008b). The USA was found
to be the most productive country with an impressive number of
1,893,800 publications. Japan ranked second with 573,473 items fol-
lowed by Germany ( n = 444,775) and the UK ( n = 415,499)
(Groneberg-Kloft et al., 2008a, 2008b). Interestingly, many East Asian
countries play an important role in the international uterine fibroid
research community. These nations are represented by Japan, China,
Taiwan and South Korea, which belong to the top ten most productive
countries. It should be pointed out that this finding is in striking con-
trast to other gynaecological disorders, i.e. Caesarean section
(Brüggmann et al., 2015).
Overall research activity is a benchmark, which is heavily depen-
dent on different socioeconomic features and resources. To assess
the role of single countries in fibroid research in relation to their
population sizes and economic welfare, NewQIS recently intro-
duced a set of socioeconomic parameters into the analysis panel
(Brüggmann et al., 2017a, 2017b, 2017c). We reviewed international
uterine fibroid research activity in context with the GDP of single
countries, which was used as a proxy for the nation’s capacity to
invest in research. Here, Taiwan appeared to be the country with
the highest fibroid research activity per 1000 bn USD, followed by
Israel and Finland. Based on these results, we acknowledge a po-
tential bias in relating the country-specific publication numbers to
the current GDP but not the average GDP over the past century.
However, because most of the articles were published in the past
20 years and the GDP ranking of countries had not changed signifi-
cantly over time, we feel it appropriate to use the current GDP to
examine our data in the context of socioeconomic resources of the
investigated countries. This approach was also supported and used
by numerous other authors working in the bibliometric field
234 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238

Figure 4 – Subject area analysis of uterine fibroid research. (A) Relative proportions of the most assigned subject areas in five-year
intervals between 1965 and 2014. (B) Proportions of the most assigned subject areas in most active countries.

(Badenhorst et al., 2016; Phillips et al., 2013; Sweileh et al., 2017;
Zyoud, 2015).
When the scientific productivity of a single nation was related to
its population size, Finland, Israel and Sweden were found to occupy
the top positions. This pattern of Scandinavian countries in promi-
nent positions was also replicated in the analysis of (semi)-qualitative
aspects of fibroid research, e.g. the citation rate (cr, the average ci-
tations per fibroid publication). Here, Sweden was leading with 22.78
citations per article, followed by Finland (cr = 21.95). Altogether, this
finding indicates that the relatively small Scandinavian nations have
established effective and efficient research structures that produce
high-quality science. This not only applies to Sweden, the traditional
 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238 235

Figure 5 – Uterine fibroid research collaborations between countries. Numbers in brackets (publication numbers/number of collaborative
publications), threshold: ≥ 20 collaborations of a single country.

Figure 6 – Density-equalizing mapping of institutions. Total number of fibroid research-performing institutions per country.
236 REPRODUCTIVE BIOMEDICINE ONLINE 36 (2018) 227–238
host of the Nobel prizes (Pernow, 1997), but also to Finland and
Denmark.
When the network of international collaborations was analysed,
it was apparent that 7.7% of collaborative articles out of all re-
search publications on myomas (n = 476 out of 6176 fibroid-specific
publications) is a rather low rate compared with other fields in
gynaecology. We postulate that this finding can be explained by the
benign nature of the tumour and the abundance of patients and avail-
able specimens, which do not require the performance of complex
multinational studies with a focus on chemotherapy, genetic back-
grounds, etc. or to establish research networks to share resources.
In other fields such as ovarian carcinoma, there are many large in-
ternational multicentre studies and multinational networks, e.g. the
Ovarian Cancer Association Consortium, which translate into prolific,
collaborative and high-quality research activities connecting scien-
tists around the globe (Pearce et al., 2012; Shen et al., 2013).
Besides scientific databases such as the WoS, popular search
engines like Google may provide useful information on uterine fi-
broids and related awareness in the general population. In this respect,
a recent study by Brito et al. (2014) analysed global search trends
for uterine fibroids on the internet using the Google Trends Search
Application. The authors reported that the mean annual global search
activity on fibroids decreased significantly between 2004 and 2012 (Brito
et al., 2014). In 2004, the mean annual search activity was 77.25% of
the overall peak search activity and decreased to 64.41% in 2012. The
countries with highest search volume were the USA, Canada, Aus-
tralia, India and the UK. By contrast, the number of uterine fibroid-
related websites grew during this period, from 5680 to almost 70,600
(Brito et al., 2014). The authors concluded that a decreased relative
search activity does not necessarily represent a trend towards de-
clining popularity of the subject. Therefore, it should be noted that
the overall popularity, measured by the absolute number of Google
searches, actually increased from 2004 to 2012. The authors also stated
that the increased number of uterine fibroid-related websites may
represent the growing number of people who are burdened by the
condition and therefore interested in raising awareness (Brito et al.,
2014). In our study, we see this increasing interest among the general
population paralleled by a growing scientific productivity related to
uterine fibroids. This is an encouraging development that needs to
be further facilitated. Therefore, more resources should be dedi-
cated to research and public health endeavours with a focus on this
condition to meet the interest this disease evokes in the general public.
Conclusions
This study represents the first concise analysis of global uterine fibroid
research activity. We assessed scientific productivity worldwide with
respect to both quantitative (overall research output) and semi-
qualitative aspects (citation parameters), and in context with
socioeconomic features. By using these metrics, we present the first
global picture of the research architecture associated with uterine
fibroids and highlight potential shortcomings in the scientific landscape.
Acknowledgements
We thank G Volante for helpful comments. This study is part of a PhD
thesis project (TB).
A R T I C L E I N F O
Article history:
Received 21 March 2017
Received in revised form 11 October 2017
Accepted 20 October 2017
Declaration: The authors report no
financial or commercial conflicts of
interest.
Keywords:
Density-equalizing mapping
Diagnosis
Female health
Fibroid
Myoma
Socioeconomic analysis
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