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A bibliometric analysis of the global research on biosimilars

  • Akram Hernández-Vásquez
  • Christoper A. Alarcon-Ruiz
  • Guido Bendezu-Quispe
  • Daniel Comandé
  • Diego Rosselli
Open Access
Research

Abstract

Background

Biosimilars could be a promising option to help decrease healthcare costs and expand access to treatment. There is no previous evidence of a global bibliometric analysis on biosimilars. Therefore, we aimed to assess the quantity and quality of worldwide biosimilars research.

Methods

We performed a bibliometric analysis using documents about biosimilars published until December 2016 in journals indexed in Scopus. We extracted the annual research, languages, countries, journals, authors, institutions, citation frequency, and the metrics of journals. The data were quantitatively and qualitatively analyzed using Microsoft Excel 2013. Additional information about authors' participation was obtained using the R-package Bibliometrix. Publication activity was adjusted for the countries by population size. Also, author co-citation analysis and a term co-occurrence analysis with the terms included in the title and abstract of publications was presented as network visualization maps using VOSviewer.

Results

A total of 2330 biosimilar-related documents identified in the Scopus database, most of them were articles (1452; 62.32%). The number of documents published had an exponential increased between 2004 and 2016 (p < 0.001). The United States was the country with the highest production with 685 (29.40%) documents followed by Germany and UK with 293 (12.58%) and 248 (10.64%), respectively. Switzerland (11.05), Netherlands (5.85) and UK (3.83) showed the highest per capita ratio. The highest citation/article ratio were for the Netherlands (28.06), Spain (24.23), and France (20.11). Gabi Journal published 73 (3.13%) documents; both Biopharm International and Pharmaceutical Technology and Mabs, 41 (1.76%). Three out of top ten journals were Trade publications. Amgen Incorporated from the USA was the most prolific institution with 51 documents followed by Pfizer Inc. with 48. Terms about specific diseases and drugs were found in recent years, compared with terms such as legislation, structure, protein, dose and generic in the early years.

Conclusions

Research production and publication of documents on biosimilars are increasing. The majority of publications came from high-income countries. The trends in terminology use are according to state of the art in the topic, and reflects the interest in the utilization of biosimilars in diseases who are expected to obtain benefits of its use.

Keywords

Biosimilar pharmaceuticals Bibliometrics Biomedical research (source: MeSH NLM) 

Abbreviations

MeSH

Medical subject heading

SNIP

SCImago journal rank

SRJ

Source normalised impact per paper

UK

United Kingdom

USA

United States of America

Background

A biosimilar, or “similar biological product”, is a highly similar product to an already approved biological product regarding structure, function, potency, quality, clinical efficacy and safety [1]. Currently, there are already 5 and 39 biosimilars products approved in the United States [2] and Europe [3], respectively. The number of approved biosimilars might increase in the next year due to manifest interest from different healthcare systems and international organizations [4].

The development of biological products represented a significant advance in the therapy of many diseases that did not have effective treatments. Nonetheless, these products require a vast expenditure of money and resources to develop, leading to an increase in the cost of these therapies for both patients and the health sector [5, 6]. The field of biosimilars could be a promising option to help decrease healthcare costs and expand access to treatment [7] particularly when many patents have already expired or will do so soon [8].

Few studies had evaluated the clinical evidence in support of different biosimilars: there are only three cancer related-biosimilars products whose safety/efficacy have been published [9], while five biosimilars for chronic inflammatory diseases have six clinical trials comparing them with their reference drug [10]. This situation of scarce evidence may lead physicians [11], pharmacists [12] and patients to have low confidence their safety and efficacy [13].

Bibliometric analysis is a useful method to objectively measure current research of a certain subject and its international scientific influence as an aspect of scientific quality [14]. However, to our knowledge, there is no previous evidence of a global bibliometric analysis on biosimilars. Our study aimed to assess the quantity and quality of worldwide biosimilars research.

Methods

Study design

We performed a bibliometric analysis using documents published until December 2016 in journals indexed in Scopus (https://www.scopus.com/). While there are a variety of document types, only articles, reviews, editorials and letters were included.

Source of information

Scopus (Elsevier BV Company, USA) is the largest abstract and citation database of scientific peer-review literature including more than 22,000 titles from international publishers. We decided to use this database because it includes all MEDLINE documents and includes further characteristics such as country of all the authors and citations per document, information that is relevant for this study [15, 16, 17].

Search strategy

A literature search was conducted by a research librarian in Scopus for publications on a single day, October 18, 2017, and used the following MeSH and free terms in the title and abstract field: biosimilar pharmaceutical OR biosimilar*. The validity of the search strategy was tested by manually reviewing retrieved articles.

Data analysis

All data were collected by two authors and downloaded in csv format (Additional file 1: Dataset). The data were imported to Microsoft Excel 2013 and quantitatively and qualitatively analyzed. The Scopus database presents some disadvantages for bibliometric applications [17]. For this reason, it was necessary to standardize the data. We detected documents mistakenly attributed to the domain of author name and affiliation. Therefore, a standardization was carried out manually by the authors.

Bibliometric indicators were extracted from the data and with the option “Analyze Results” in Scopus, including annual research, languages, countries, journals, authors, institutions, and citation frequency. Scopus Journal Metrics was used to extract the metrics of journals. The contributions of countries were evaluated based on paper and citation numbers, and the research output of each country was adjusted according to population size (https://www.cia.gov/library/publications/the-world-factbook/geos/ag.html). To describe more information about author participation in research production about biosimilars, we use the open-source Bibliometrix R-package (http://www.bibliometrix.org/) to obtain the mean of articles per author, the mean of authors per article, the mean of articles’ citation and the number of articles with only one or more than one author.

Author co-citation analysis (ACA) to analyze the relations among highly cited references and productive authors, and a term co-occurrence analysis with the terms included in the title and abstract of publications was presented as network visualization maps using VOSviewer version 1.6.6 (Leiden University, Leiden, Netherlands) techniques [18].

Research ethics

The data were downloaded from Scopus and as secondary data, did not involve any interactions with human subjects. There were no ethical questions about the data. Approval of an ethics committee was not necessary.

Results

A total number of 2330 documents indexed on Scopus were retrieved from 2004 to 2016. The majority of papers were articles (1452; 62.32%) followed by reviews (642; 27.55%), editorials (138; 5.92%), and letters (98; 4.21%). In 2004, three publications were identified compared to 521 in 2016 (Fig. 1); this increase in the amount of papers was statistically significant (p < 0.001). In general, 83 countries contributed to research articles about biosimilars. Table 1 listed the top ten countries, which represented 84.12% of the total. Seven of the top ten publishing countries are European. United States was the country with the highest production with 685 (29.40%) documents followed by Germany and UK with 293 (12.58%) and 248 (10.64%), respectively. European countries such as Switzerland (11.05), Netherlands (5.85) and UK (3.83) showed the highest per capita ratio. The highest citation/article ratio were for the Netherlands (28.06), Spain (24.23), and France (20.11).
Fig. 1

Annual scientific documents of biosimilar research, Scopus 2004–2016

Table 1

Top ten countries with more publications on biosimilars, and there average citation rate. Scopus 2004–2016

Rank

Country

Number of documents

% of articles

Number of articles per million inhabitants

Citations (up 2016)

Citations/Article

1

United States

685

29.40

2.10

6768

9.88

2

Germany

293

12.58

3.64

4373

14.92

3

United Kingdom

248

10.64

3.83

3824

15.42

4

Italy

149

6.39

2.40

2097

14.07

5

France

132

5.67

2.10

2654

20.11

6

Netherlands

100

4.29

5.85

2806

28.06

7

Spain

91

3.91

1.86

2205

24.23

8

Switzerland

91

3.91

11.05

1783

19.59

9

India

86

3.69

0.07

338

3.93

10

Canada

85

3.65

2.39

794

9.34

The analysis of the subject area, Table 2 shows that most documents were included in the broad category “Medicine” with 1453, followed by “Pharmacology, toxicology and pharmaceutics” with 946 and “Biochemistry, Genetics and Molecular biology” with 607.
Table 2

Subject areas for documents published on biosimilars, Scopus, 2004–2016

Rank

Subject area

Documents published

% of documents

1

Medicine

1453

37.92

2

Pharmacology, Toxicology and Pharmaceutics

946

24.69

3

Biochemistry, Genetics and Molecular Biology

607

15.84

4

Immunology and Microbiology

219

5.72

5

Health Professions

165

4.31

6

Chemistry

137

3.58

7

Chemical Engineering

136

3.55

8

Business, Management and Accounting

68

1.77

9

Engineering

62

1.62

10

Mathematics

39

1.02

Table 3

Top ten journals publishing on biosimilars (N = 2330). Scopus 2004–2016

Rank

Source title

Publication type

Documents published

% of articles

CiteScore 2016

SJR 2016

SNIP 2016

1

Gabi Journal

Journal

73

3.13

0.28

0.23

0.08

2

Biopharm International

Trade Publication

41

1.76

0.17

0.16

0.08

3

Mabs

Journal

41

1.76

4.66

1.62

1.25

4

Biodrugs

Journal

40

1.72

2.98

1.01

1.13

5

Bioprocess International

Trade Publication

39

1.67

0.26

0.23

0.25

6

Pharmaceutical Technology

Journal

39

1.67

0.09

0.14

0.16

7

Biologicals

Journal

34

1.46

1.65

0.62

0.74

8

Contract Pharma

Trade Publication

30

1.29

0.02

0.12

0

9

Journal of Generic Medicines

Journal

28

1.20

0.12

0.14

0.39

10

Expert Opinion on Biological Therapy

Journal

27

1.16

3.14

1.14

0.75

The total of documents retrieved were published in 803 journals, but top ten journals account for 18.82% of the total (Table 3). The top journals included in first place Gabi Journal with 73 (3.13%) documents, followed by Biopharm International and Pharmaceutical Technology and Mabs both with 41 (1.76%). Three out of ten titles were Trade publications. Mabs journal had the greatest SJR 2016 (1.62).

Table 4 presents a ranking of the Top ten institutions that published in biosimilars. Amgen Incorporated from the USA was the most prolific institution with 51 documents followed by Pfizer Inc. with 48. Seven of this top 10 list are European institutions, the others from USA. Four institutions were pharmaceutical companies. Based on the citations, academic institutions obtained higher positions compared to pharmaceutical companies being Medizinische Universitat Wien the institution with the highest number of citations and citations per articles ratio.
Table 4

Top ten institutions publishing on biosimilars, and their citations. Scopus 2004–2016

Rank

Institution Name

Country

Number of papers

Citations

Citations/Article

1

Amgen Incorporated

United States

51

394

7.73

2

Pfizer Inc.

United States

48

201

4.19

3

Utrecht University

Netherlands

44

898

20.41

4

Duke University

United States

37

763

20.62

5

Sandoz International GmbH

Germany

33

460

13.94

6

Medizinische Universitat Wien

Austria

23

1538

66.87

7

KU Leuven

Belgium

22

227

10.32

8

Erasmus University Medical Center

Netherlands

20

929

46.45

9

Universita degli Studi di Milano

Italy

20

152

7.6

10

Novartis International AG

Switzerland

19

174

9.

There were 6344 authors in the documents on biosimilars. The mean of articles per author was 0.4 and there were 420 documents with only one author. A co-authorship analysis that included authors with at least five publications is shown in Fig. 2. There were 143 authors; each circle represents one author, the closer the circles the closer the collaboration.
Fig. 2

Author co-authorship analysis with VOSviewer for biosimilars publications. Minimum of five documents per author, 143 authors were included. Weighted by citations and scores by average of citations

We show the top 10 cited articles in biosimilars in Table 5. The article “EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update” published in 2014 received the highest citation (962) within the retrieved documents. The top 10 include five articles and five reviews. All of the top ten cited articles were published in scientific journals. In general, the mean of citations per article was 9.6.
Table 5

Top 10 cited documents of biosimilars research. Scopus 2004–2016

Rank

Title

Year

Journal name

Cited by

Type of document

1

EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update

2014

Annals of the Rheumatic Diseases

962

Article

2

2010 update of EORTC guidelines for the use of granulocyte-colony stimulating factor to reduce the incidence of chemotherapy-induced febrile neutropenia in adult patients with lymphoproliferative disorders and solid tumours

2011

European Journal of Cancer

498

Article

3

Biopharmaceutical benchmarks 2014

2014

Nature Biotechnology

275

Article

4

A randomised, double-blind, parallel-group study to demonstrate equivalence in efficacy and safety of CT-P13 compared with innovator infliximab when coadministered with methotrexate in patients with active rheumatoid arthritis: The PLANETRA study

2013

Annals of the Rheumatic Diseases

269

Article

5

A randomised, double-blind, multicentre, parallel-group, prospective study comparing the pharmacokinetics, safety, and efficacy of CT-P13 and innovator infliximab in patients with ankylosing spondylitis: The PLANETAS study

2013

Annals of the Rheumatic Diseases

250

Article

6

Analytical tools for characterizing biopharmaceuticals and the implications for biosimilars

2012

Nature Reviews Drug Discovery

215

Review

7

PEG-modified biopharmaceuticals

2009

Expert Opinion on Drug Delivery

201

Review

8

The challenge of biosimilars

2008

Annals of Oncology

178

Review

9

Sublingual immunotherapy: World Allergy Organization position paper 2013 update

2014

World Allergy Organization Journal

172

Review

10

Biosimilars: What clinicians should know

2012

Blood

158

Review

In the analysis of terms co-occurrence (Fig. 3), we used words in the titles and abstracts related to specific diseases and drugs. Rheumatoid arthritis, ulcerative colitis, rheumatism, infliximab, etanercept, and tofacitinib were found in recent years, compared with terms such as legislation, structure, protein, dose and generic in the early years.
Fig. 3

Terms co-occurrence analysis of tittles and abstracts (overlay visualization) and their temporal evolution with VOSviewer for biosimilars publications. Binary counting method, choose threshold (10 terms). Term “conclusion” was excluded

Discussion

Biosimilars’ cost-saving potential is their best attribute, making them an attractive option in the close future [19]. Also, the mandatory research that they have to do prior of their approval, and their large utility in diverse diseases, such as cancer, hemophilia, autoimmune diseases, and rare genetic conditions, make biosimilars an interesting field to make research. This explains the growing interest by many groups, including patients, health insurers, and providers, as well as the pharmaceutical industry. This interest is evidenced in the exponential increased of documents published on biosimilars between 2004 and 2016. High-income countries seem to dominate research in the field of biosimilars where the United States and Western European countries contributed to most of the world’s research on biosimilars, and receive the most of the citations.

Authors from the United States published the highest number of scientific publications and received more citation compared to other countries. This result is not surprising, since the US leads the rankings in worldwide research, including medicine [20, 21, 22]. Majority of top-ranking countries were European. Although Switzerland, Netherlands, and United Kingdom do not have as many papers but go to the top of the list when we adjust by population. On the other hand, Netherlands, Spain, and France have the greatest citation per article. Those situations are similar in other biomedical fields: Rheumatology [20], arthroscopy [23], foot and ankle [24], and probiotics in pediatrics [25], but it differs from endocrinology and metabolism field [26] and research on tramadol [27]. It would perhaps be better to adjust by the number of researchers, instead of inhabitants, but this information is not easily accessible [26].

“Gabi Journal” and “Mabs” were the most productive peer-review journals in the topic of biosimilars. Besides, “Biopharm International”, a trade publication journal, occupied the second most productive journal on biosimilars. It is remarkable that three trade publication journals, perhaps showing the industry’s interest in promoting their products, were in the top 10 most productive journals, but they do not receive that many citations. This may reflect the fact that they might be considered less trustful, or that they are not necessarily targeted at researchers [28]. Both “Mabs” and “Expert Opinion on Biological Therapy” are rated much higher in CiteScore 2017, SJR 2016, and SNIP 2016, despite having less publications. These suggest that at least in the field of biosimilars quantity is not necessarily correlated with quality. This situation differs from other biomedical fields like spine surgery [29].

Only three of the top 10 institutions were from America, the other seven were from Europe. This reflects the fact that biosimilars are a subject of interest in many different countries. Additionally, institutions with most citations and mean citation rate were from universities, which might indicate its better quality. Also, there is less risk that universities have conflicts of interest in developing research papers in biosimilars, so their results might be more trustful.

The top five most cited papers were original articles. The top two were guidelines for management of clinical conditions (rheumatoid arthritis and febrile neutropenia). This could be explained because three biosimilars are available to treat rheumatoid arthritis and others are in the way to approval [30], and the recent approval process of granulocyte-colony stimulating factor biosimilars, a useful drug to treat febrile neutropenia [31]. Moreover, clinical practice guidelines from any field generally have a lot of cites. The fourth and fifth most cited articles were randomized controlled clinical trials of the infliximab biosimilar CT-P13. This is the first biosimilar monoclonal antibody approved by the European Medicines Agency [32]. Overall, those two clinical trials help to understand and accept their interchangeability with infliximab as a feasible and safe strategy to be applied in real-life clinical practice [33]. On the other side, there were five reviews in the top 10. Mostly, they try to better explain biosimilars to health professionals, especially clinician [34], that could have some reluctance about the use of biosimilars [35]. These reviews focus on improving the uptake of biosimilars, educating the physicians, and motivating to adopt them in routine clinical practice [36].

Words included in the title and abstracts of biosimilars research papers and their main year when they were published were: Legislation (2011), enzyme (2012), structure, protein, dose, antibody, interchangeability (2013), glycosylation, receptor, phase, adverse event (2014), and rheumatoid arthritis, ulcerative colitis, extrapolation, rituximab, etanercept (2015). This suggests that the emphasis of biosimilars research responds to a subject that is very new to researchers and should follow the law of the development of a new discipline. This find is similar to a report in a previous bibliometric analysis on exomes [37]. In the field of biosimilars, there are requirements for their approval, including to demonstrate similarity, safety, and effectiveness [38]. These terms were more frequently found in the early.

The present research shows an overall view about biosimilars research and their distribution mostly in high-income countries where they have policies to their approval. Although markets like BRICS (Brazil, Russia, India, China, and South Africa), MIST (Mexico, Indonesia, South Korea, and Turkey) [39], and Latin America [40] provides an emerging future to biosimilars, they do not represent an important influence in biosimilars research. Also, the present study like previous bibliometric analyses has some limitations. First, our study did not include articles published in non-Scopus databases. However, Scopus is a reliable and significant source for bibliometric studies in general. Second, it is difficult to distinguish articles that focus on biosimilars from those that only mention the term or tangentially address it. However, using correct keywords and given its original subject, this study still provides a comprehensive picture of biosimilar research productivity, which could be used to track overall trends and identify topics of interest.

Conclusions

In summary, the results of the present study showed that documents published in journals about biosimilars are increasing. The majority of publications came from high-income countries, being the US the most productive country in biosimilars followed by European countries. To the best of our knowledge, this is the first study conducted in the analysis of research production and citations in biosimilars. The trends in terminology use are according to state of the art in the topic that comes from issues of safety and efficacy to the study of new biosimilar products in specific diseases.

Notes

Funding

This research received no specific grant from any funding agency.

Availability of data and materials

All data analyzed in this study is included in Dataset 1: Data obtained from Scopus, a. CSV that contain list of studies included.

Authors’ contributions

AHV conceived the idea for the study; AHV and DC collected the data; AHV and GBQ did the statistical analysis; AHV, GBQ, CAAR and DR drafted the manuscript; all authors contributed in the writing and preparation of the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

This study did not require the approval of an ethics committee as it is a secondary analysis of a database of a public domain and of free access.

Consent for publication

This study did not require consent for publication.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary material

40545_2018_133_MOESM1_ESM.csv (6.2 mb)
Additional file 1: Dataset 1: Data obtained from Scopus, a .CSV that contain list of studies included. (CSV 6323 kb)

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© The Author(s). 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  1. 1.Universidad Privada del NorteLimaPeru
  2. 2.Facultad de MedicinaUniversidad Ricardo PalmaLimaPeru
  3. 3.Universidad Peruana Cayetano HerediaLimaPeru
  4. 4.Institute for Clinical Effectiveness and Health Policy (IECS)Buenos AiresArgentina
  5. 5.Departamento de Epidemiología Clínica y Bioestadística, Facultad de MedicinaPontificia Universidad JaverianaBogotáColombia

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