
==== Front
Infect Dis Clin Microbiol
Infect Dis Clin Microbiol
10.36519
Infect Dis Clin Microbiol
Infectious Diseases & Clinical Microbiology
2667-646X
DOC Design and Informatics Co. Ltd.

10.36519/idcm.2023.250
Original Article
Bibliometric Analysis
Virology
Bibliometric Analysis of Human Metapneumovirus Studies
https://orcid.org/0000-0002-4740-1579
Alıravcı Işıl Deniz isildeniz.aliravci@comu.edu.tr
1*
https://orcid.org/0000-0002-7568-035X
Çelik Taylan 2
https://orcid.org/0000-0002-6264-1685
Çelik-Ekinci Semiha 3
https://orcid.org/0000-0003-4108-0847
Hamidi Aziz Ahmad 3
1 Department of Infectious Diseases and Clinical Microbiology, Çanakkale 18 Mart University Hospital, Çanakkale, Türkiye
2 Department of Pediatri, Çanakkale 18 Mart University Hospital, Çanakkale, Türkiye
3 University of Health Sciences, Fatih Sultan Mehmet Training and Research Hospital, Istanbul, Türkiye
* Corresponding author at: Department of Infectious Diseases and Clinical Microbiology, Çanakkale 18 Mart University Hospital, Çanakkale, Türkiye
12 2023
29 12 2023
5 4 311322
05 6 2023
06 9 2023
Copyright © 2024 Infectious Diseases and Clinical Microbiology
2024
https://creativecommons.org/licenses/by-nc/4.0/ This work is licensed under a Creative Commons Attribution-Non Commercial 4.0 International License.
Objective

This study aimed to estimate research productivity and general characteristics of research in different regions of the world in the field of human metapneumovirus (hMPV).

Materials and Methods

We used the Web of Science (WoS) electronic database to retrieve articles on “human metapneumovirus,” published up to March 31, 2023. Parameters such as research productivity, the total number of publications, average citation counts of all articles, research productivity by top publishing countries and affiliated organizations, links between countries/organizations, and top keywords were assessed.

Results

We found 826 articles in the WoS database. The first article on hMPV was published in 2002, and 2008 was the year that the most articles on hMPV were published, with 70 articles. The articles were cited 26,797 times (14,498 times without self-citations) and 32.25 times on average per article. Hirsch (H)-index was 80. The year 2008 also had the highest number of citations, with more than 1800. The United States was the most productive country, producing 295 documents (35.714%), one-third of all publications in this field worldwide. Canada (6.5%) and Japan (6.5%) followed the United States regarding total hMPV publications worldwide. The leading funding agencies for hMPV research were from the United States, Europe, China, and Japan.

Conclusion

Our findings imply that developed countries should assist developing countries in enhancing their research infrastructures.

Keywords

bibliometric analysis
publication
hMPV
human metapneumovirus
==== Body
pmcHighlights

The first article on hMPV was published in 2002.

2008 was the year that the most articles on hMPV were published, with 70 articles.

Authors from 69 countries and 1083 organizations/institutions contributed to the literature on hMPV.

The United States had the largest number of publications on hMPV, with one-third of all publications worldwide.

Introduction

Human metapneumovirus (hMPV) is an enveloped, single-stranded ribonucleic acid (RNA) virus in the genus Metapneumovirus (1). In 2016, the Pneumoviridae family replaced Paramyxoviridae as a new classification for this virus (2).

It was first identified as a lower respiratory tract infection etiological agent in the Netherlands in 2001 (3, 4), and in recent years it has been detected all over the world (2). According to studies, hMPV has been present in human populations for more than 50 years (5). Transmission to humans occurs through direct or close contact with the infected person's secretions (4). Signs and symptoms of hMPV infection have been reported in primates other than humans, such as macaque monkeys (4). It has been reported that hMPV causes infection mostly in late winter and spring, but the seasonal distribution is not known for certain and can cause co-infection with other respiratory viruses (3). The signs and symptoms are frequently severe and resemble infections with respiratory syncytial viruses (5).

It is a common cause of respiratory tract infections, mainly in childhood, but immunocompromised patients and adults can also become infected with this virus (4). Seniors who have hMPV may acquire severe respiratory conditions (5). Previous studies conducted in different countries reported that the virus is especially active in pediatric patients and is detected in 5-20% of lower respiratory tract infections (2). Seroprevalence studies demonstrated that humans become infected for the first time before the age of five and continue to become infected for the rest of their lives (6). Human metapneumovirus is divided into two main, separate genetic groups, A and B, which exhibit antigenic differences but share the same clinical signs of infection (5) and also further divided into subclasses that include A1, A2, and B1, B2 with seasonal variation (2).

Direct antigen tests, cell cultures, molecular methods, and serologic methods are currently used in the diagnosis of hMPV infection (3). The current situation regarding the treatment of hMPV infections is supportive. Ribavirin, monoclonal antibodies, inhibitory peptides, and small interfering ribonucleic acids have been used in human/animal in vivo models, and several vaccine studies are being conducted to control hMPV infection in non-human primate models (7-10).

Numerous bibliometric analyses have been conducted on respiratory pathogenic viruses (11-14). “Bibliometric study” is a methodological technique from the library sciences based on reviewing scientific literature about specific topics by using statistical analysis to estimate the impact and productivity of authors, articles, papers, and other journals, including citing numbers. This study aimed to provide a detailed analysis of scientific research articles on hMPV. We explored annual trends of publications and core journals showing current status and future research trends by representing highly productive authors, institutions, countries, or regions and co-cited references. Our bibliometric study provides a systematic and comprehensive analysis of the scientific research on hMPV, which may inform future research directions and facilitate the development of effective prevention and treatment strategies for this virus.

Materials and Methods

We conducted a bibliometric study to analyze scientific research articles related to hMPV+. We retrieved scientific research articles on hMPV from the Web of Science (WoS) electronic bibliometric database. We selected this bibliographic database because it covers comprehensive and relevant scientific literature from various disciplines.

First, we typed human metapneumovirus OR hMPV OR HMPV in the title section of the search engine and retrieved all relevant literature published until March 31, 2023. We performed a literature search in one day (April 1, 2023), as the database was updated every day.

To accomplish this, we searched for all types of documents containing original research data, such as articles, letters, reviews, and conference proceedings. The data extracted in the bibliometric analysis were the title, author name, year of publication, journal name, publication type, country of origin for each article, number of articles published per country, and citation count.

The search was not restricted to a specific language, and we examined the number of article citations and the dominant countries according to the year period. The data are presented as percentages and decimals in the tables and graphs.

We used descriptive statistics to calculate the total number of articles, average citation count per article, and percentage of articles published per country. We also used a network analysis tool (VOSviewer software) to visualize the co-authorship and co-citation patterns among the institutions and countries involved in the research on hMPV and to broadcast network links between countries/institutions and the most preferred keywords.

Results

In our initial search using the selected keywords, we obtained 1120 results, of which 826 were articles. We focused our analysis on articles and excluded other document types. According to the WoS database, the first publication on hMPV was in 2002. 2008 was the year that the most articles on hMPV were published, with 70 articles (Figure 1), and the year 2008 also had the highest number of citations (>1800) (Figure 1). The majority of research on hMPV was published between 2002-2012. Figure 1 shows the number of publications on hMPV and their citations from 2002 to March 2023; the graph was obtained from the WoS database. Most hMPV-related articles (n=775; 93.826%) were published in journals indexed in the Science Citation Index Expanded of the WoS Core Collection and English (n=800; 96.852%), Spanish (0.969%), Turkish (0.969%), French (0.726%), and Korean (0.484%) were the preferred publishing languages.

Authors from 69 countries and 1083 organizations/institutions have contributed to the literature on hMPV. The United States had the largest number of publications on hMPV (n=295, 35.714%). According to our findings, Canada (n=72), Japan (n=66), China (n=66), the Netherlands (n=48), France (n=44), England (n=37), Australia (n=32), Spain (n=29), and Germany (n=26) were also listed among the top publishing countries for hMPV (Table 1).

Figure 1 Citations and publications over time.

Table 1

Top publishing countries on hMPV.

Countries/Regions

	n (%) of 826

	
USA

	295 (35.714)

	
Canada

	72 (8.717)

	
Japan

	66 (7.990)

	
China

	66 (7.990)

	
Netherlands

	48 (5.811)

	
France

	44 (5.327)

	
England

	37 (4.479)

	
Australia

	32 (3.874)

	
Spain

	29 (3.511)

	
Germany

	26 (3.148)

	
Italy

	24 (2.906)

	
South Korea

	22 (2.663)

	
Turkey

	17 (2.058)

	
Brazil

	16 (1.937)

	
Chile

	14 (1.695)

	
India

	14 (1.695)

	
Israel

	12 1.453)

	
South Africa

	11 (1.332)

	
Argentina

	10 (1.211)

	
Iran

	10 (1.211)

	
Norway

	10 (1.211)

	
Taiwan

	10 (1.211)

	
Thailand

	10 (1.211)

	

Vanderbilt University (the United States), Laval University (Canada), Erasmus University Rotterdam (the Netherlands), and Erasmus University Medical Center (the Netherlands) were among the top publishing organizations/institutions on hMPV. In addition, AstraZeneca Pharmaceutical Company was among these organizations (Table 2).

Table 2

The top publishing organizations/institutions on hMPV.

Publishing organizations/Institutions

	n (%)

	
Vanderbilt University

	53 (6.416)

	
Laval University

	49 (5.932)

	
Erasmus University

	39 (4.722)

	
Erasmus University Medical Center

	38 (4.60)

	
The University of Texas System

	35 (4.237)

	
The National Institutes of Health

	31 (3.753)

	
The University of Texas Medical Branch

	29 (3.511)

	
The National Institute of Allergy and Infectious Diseases

	27 (3.269)

	
Centers for Disease Control and Prevention

	24 (2.906)

	
AstraZeneca

	19 (2.300)

	

The 826 articles included in our study were published in 235 journals. The Journal of Virology' published 61 publications on hMPV and ranked first among journals with the highest number of publications on hMPV (Table 3).

Table 3

The top publishing journals and citation numbers on hMPV.

	Number of articles

	Total citations

	Average citations

	
Journal of Virology

	61

	1189

	19.49

	
Journal of Medical Virology

	49

	652

	13.31

	
Journal of Clinical Virology

	39

	427

	10.95

	
Journal of Infectious Diseases

	37

	2015

	54.46

	
Journal of Clinical Microbiology

	33

	1097

	33.24

	
Emerging Infectious Diseases

	27

	1437

	53.22

	
Pediatric Infectious Disease Journal

	26

	638

	24.54

	
Plos One

	25

	421

	16.84

	
Journal of General Virology

	24

	638

	26.5

	
Japanese Journal of Infectious Diseases

	20

	322

	16.1

	

The top funding agency was the United States Department of Health and Human Services, which supported 158 articles, followed by the United States National Institutes of Health (153 articles) and the United States National Institute of Allergy Infectious Diseases (85 articles). The leading funding agencies for hMPV research were from the United States, Europe, China, and Japan (Table 4).

Table 4

The leading funding organizations of hMPV research.

Funding organizations

	n

	% of 826

	
United States Department of Health and Human Services (USA)

	158

	19.128

	
National Institutes of Health (USA)

	153

	18.523

	
National Institute of Allergy Infectious Diseases (USA)

	85

	10.291

	
European Commission (Europe)

	24

	2.906

	
National Natural Science Foundation of China (China)

	23

	2.785

	
Ministry of Education Culture Sports Science And Technology Japan (Japan)

	19

	2.300

	
Nih National Center For Research Resources (USA)

	18

	2.179

	
Canadian Institutes of Health Research (Canada)

	17

	2.058

	
Japan Society for the Promotion of Science (Japan)

	14

	1.695

	
AstraZeneca (England)

	13

	1.574

	

The total number of citations for articles was 26,797, with an average of 32.25 citations per article. According to the WoS database results, the highest number of citations for a single article was 316, and the Hirsch (H)-index of 826 articles was 80. A summary of the most cited 25 articles is shown in Table 5. Williams, JV, was the most productive author with 47 articles.

Table 5

Summary of most cited 25 articles.

Journal

	Title

	First author

	Author gender

	Publication year

	Total citations

	
New England Journal of Medicine

	Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children

	Williams, JV.

	Male

	2004

	646

	
Journal of Infectious Diseases

	Virological features and clinical manifestations associated with human metapneumovirus: A new paramyxovirus responsible for acute respiratory-tract infections in all age groups

	Boivin, G.

	Male

	2002

	426

	
Journal of Infectious Diseases

	Human metapneumovirus infections in young and elderly adults

	Falsey, AR.

	Female

	2003

	409

	
Virology

	Analysis of the genomic sequence of a human metapneumovirus

	van den Hoogen, BG.

	Female

	2002

	328

	
Emerging Infectious Diseases

	Human metapneumovirus infections in hospitalized children

	Boivin, G.

	Male

	2003

	317

	
Journal of Infectious Diseases

	Prevalence and clinical symptoms of human metapneumovirus infection in hospitalized patients

	van den Hoogen, BG.

	Female

	2003

	313

	
Journal of Infectious Diseases

	Characterization of human metapneumoviruses isolated from patients in North America

	Peret, TCT.

	Female

	2002

	300

	
Emerging Infectious Diseases

	Antigenic and genetic variability of human metapneumoviruses

	van den Hoogen, BG.

	Female

	2004

	286

	
Journal of Infectious Diseases

	Dual infection of infants by human metapneumovirus and human respiratory syncytial virus is strongly associated with severe bronchiolitis

	Semple, MG.

	Male

	2005

	279

	
Emerging Infectious Diseases

	Human metapneumovirus in severe respiratory syncytial virus bronchiolitis

	Greensill, J.

	Female

	2003

	249

	
Journal of Clinical Microbiology

	Real-time reverse transcriptase PCR assay for detection of human metapneumoviruses from all known genetic lineages

	Maertzdorf, J.

	Male

	2004

	243

	
Emerging Infectious Diseases

	Human metapneumovirus as a cause of community-acquired respiratory illness

	Stockton, J.

	Female

	2002

	226

	
Pediatric Infectious Disease Journal

	Clinical impact and diagnosis of human metapneumovirus infection

	Van den Hoogen, BG.

	Female

	2004

	209

	
New England Journal of Medicine

	Burden of human metapneumovirus infection in young children

	Edwards, Kathryn M.

	Female

	2013

	202

	
Journal of Infectious Diseases

	Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults

	Widmer, K.

	Female

	2012

	202

	
Pediatrics

	Human metapneumovirus infection in the United States: Clinical manifestations associated with a newly emerging respiratory infection in children

	Esper, F.

	Male

	2003

	200

	
Emerging Infectious Diseases

	Human metapneumovirus infection among children hospitalized with acute respiratory illness

	Mullins, JA.

	Male

	2004

	190

	
Virology

	Genetic diversity between human metapneumovirus subgroups

	Biacchesi, S.

	Male

	2003

	190

	
Journal of Infectious Diseases

	The role of human metapneumovirus in upper respiratory tract infections in children: A 20-year experience

	Williams, JV.

	Male

	2006

	183

	
Annals of Internal Medicine

	Brief communication: Fatal human metapneumovirus infection in stem-cell transplant recipients

	Englund, JA.

	Female

	2006

	178

	
Pediatric Infectious Disease Journal

	Presence of the new human metapneumovirus in French children with bronchiolitis

	Freymuth, F.

	Male

	2003

	178

	
Emerging Infectious Diseases

	Respiratory tract reinfections by the new human Metapneumovirus in an immunocompromised child

	Pelletier, G.

	Male

	2002

	178

	
Journal of Clinical Microbiology

	Human metapneumovirus associated with respiratory tract infections in a 3-year study of nasal swabs from infants in Italy

	Maggi, F.

	Male

	2003

	176

	
Journal of Infectious Diseases

	A 1-year experience with human Metapneumovirus in children aged < 5 years

	Esper, F.

	Male

	2004

	171

	
Journal of Virology

	Recombinant human metapneumovirus lacking the small hydrophobic SH and/or attachment G glycoprotein: Deletion of G yields a promising vaccine candidate

	Biacchesi, S.

	Male

	2004

	164

	

We examined publication trends by dividing the publication years into two 10-year periods. When we compared the first period, 2002-2012, with the second period, 2013-2023, we observed that the number of publications decreased from 462 to 364 in the second period. The citation number was higher in the 2002-2012 period than in the 2013-2023 period (22,483 and 4192, respectively). The United States had the most publications in both periods. However, while Canada ranked second regarding the number of publications in the first period, it dropped to fifth place in the second period, and there was an increase in Chinese publications in the second period (Table 6).

Table 6

The comparison of time periods.

Publication period

	Number of articles

	Times cited

	H index

	Top five publishing countries

	
2002-2012

	462

	22,483

	80

	USA (188) Canada (54) Japan (36) Netherlands (36) England (22)

	
2013-2023

	364

	4192

	31

	USA (127) China (44) Japan (30) France (23) Canada (18)

	

We used the VOSviewer software to visualize the co-authorship and co-citation patterns among the institutions and countries involved in the research on hMPV and obtain network links between countries/institutions and the most preferred keywords. In Figure 2a, we created citation mapping of articles with a minimum of 10 citations. The larger circles indicate a higher total link strength. The top 28 articles are shown in Figure 2. Figure 2b shows author citation mapping. In the figure, the larger the circle size, the greater the document and citation strength of the author. The lines represent citation relationships.

Figure 2a Citation mapping of the articles with minimum 10 citations.

Figure 2b Author citation mapping.

Figure 3 shows the citation relations by country. The bigger the circle, the more document and citation strength of the country.

Figure 3 Citation relations by countries.

Figures 4a and 4b show the co-authorship mapping using. Figure 4a shows authors with co-authorship relations out of 254, according to the total link strength. Thirty had a relationship, while others did not. The lines represent the relationship.

Figure 4a The co-authorship mapping between authors.

Figure 4b The co-authorship mapping between authors.

Figure 4b shows the co-authorship relations between institutions and publishing times. Clusters are filtered by document and citation number, and the most active ones in the clusters are shown. The legend shows the publication dates of the articles.

Discussion

Numerous new and re-emerging infections, some affecting both humans and animals, are caused by viruses, significantly threatening public health (15). This study focused on hMPV, which has been reported worldwide since its discovery by Dutch researchers in 2002. It causes an increasing number of cases, especially in children and immunosuppressants, owing to respiratory tract infections (3, 4). Although bibliometric studies, a popular method today, have been conducted for many popular or traditional infectious etiologic agents and viruses (14, 16-19), our study is the first to evaluate hMPV in the literature.

This study comprehensively analyzes the hMPV-related literature based on the WoS database, which presents global hMPV research regarding the number of reports and their distribution of countries, institutions, and journals. A comprehensive assessment of the state of hMPV research is necessary to guide future research goals, primarily through collaboration among numerous academic researchers in various fields. Our findings may have an impact on future theoretical research because a good indicator of production and advancement may be the number of publications over time (20).

We preferred the WoS database for bibliometric analysis of hMPV-related literature because the WoS database indexes quality publications and covers journal abstracts and citations (21, 22).

This report provides a national-level overview of how hMPV research has progressed over the past 21 years in many countries. The results showed that American articles predominate over those from other countries in scientific journals. We identified countries that contributed to research on hMPV and found the United States to be the leading contributor, followed by Canada and Japan. English was the leading publishing language. The most productive institutions were from the United States, Canada, and the Netherlands. In addition, the leading funding agencies for hMPV research were from the United States, Europe, China, and Japan. All the mentioned countries are economically developed. Similar to our findings, previous studies on scientific productivity have shown that economically developed countries are more productive regarding scientific studies (16-20).

The top three journals were the Journal of Virology (with 61 records), Journal of Medical Virology (with 49 records), and Journal of Clinical Virology (with 39 records). These journals have high impact factors and are indexed in the WoS Core Collection Science Citation Index Expanded. They mainly publish documents that explore the structure and basic functions of viruses, how they interact with their hosts and environments, and how they change over time, as well as cutting-edge methodologies and therapeutic and diagnostic approaches.

Using VOS Viewer, we identified the most preferred keywords in research articles. We also analyzed the co-authorship and co-citation patterns among the institutions, authors, and countries involved in research on hMPV. Keywords were analyzed as we described before to understand better the researchers' current concerns and anticipated research trends. A paper's keywords can be considered the most crucial core details that reflect the main research objectives of the paper (21, 22). Therefore, we gathered and examined keywords issued by the authors. Keywords related to topics such as the relationship between hMPV and other respiratory viruses (influenza, bocavirus, etc.), pathophysiology, clinical presentations, and risk groups (children and the elderly) were the most frequent keywords.

In conclusion, our bibliometric analysis provides a comprehensive overview of research on hMPV, highlighting the most active countries, institutions, and research topics. Our findings imply that developed countries should assist developing countries in enhancing their research infrastructures. These findings may inform future research and guide the development of effective prevention and treatment strategies for hMPV.

Additional Information

Ethical Approval

N.A.

Informed Consent

N.A.

Peer-review

Externally peer-reviewed

Author Contributions

Concept – I.D.A., T.Ç.; Design – I.D.A., S.Ç.E.; Supervision – I.D.A., A.A.H.; Funding – I.D.A.; Materials – S.Ç.E., I.D.A.; Data Collection and/or Processing – T.Ç., I.D.A.; Analysis and/or Interpretation – T.Ç., S.Ç.E., I.D.A.; Literature Review – A.A.H.; Writer – I.D.A., S.Ç.E., A.A.H.; Critical Reviews – A.A.H.

Conflict of Interest

The authors declare no conflict of interest.

Financial Disclosure

The authors declared that this study has received no financial support.
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