Bibliometric analysis of peer-reviewed literature in transgender health (1900 – 2017)

Background Transgender community is marginalized and under-researched. Analysis of peer-reviewed literature in transgender health is needed to better understand health needs and human rights of transgender people. Therefore, the aim of this study was to analyze global research activity in transgender health published in peer-reviewed journals. Methods Peer-reviewed documents in transgender health were retrieved using Scopus database. VOSviewer was used to map frequently encountered author keywords while ArcGIS 10.1 was used to map the geographical distribution of the retrieved documents. Most active countries, institutions, and authors were presented. The study period was set from 1900 to 2017. Results In total, 5772 peer-reviewed documents were obtained. English (5008; 86.8%) was the most frequently encountered language. A dramatic increase in the number of publications was seen in the last decade. The retrieved documents had an average of 12.1 citations per document and h-index of 92. Most frequently encountered author keywords were Human immunodeficiency virus infection and acquired immune deficiency syndrome (HIV/AIDS), mental health, and discrimination. Authors from 80 different countries contributed to publishing the retrieved documents. Publications originated mainly from Northern America, certain European countries, Australia, and Brazil. Professor Gooren, L.J.G. was the most active author in this field with 104 (1.88%) publications. Top active authors were in the fields of endocrinology, plastic surgery, psychiatry/psychology, public health, and sexology. Five of the top ten active authors were from the USA, three were from the Netherlands, and two were from Belgium. The most active institution was the VU University Medical Center (Netherlands) (184; 3.2%) followed by the University of California, San Francisco (USA) (157; 2.7%). The International Journal of Transgenderism was most active (284; 4.9%) in publishing articles in transgender health. However, documents published in the American Journal of Public Health had the highest impact with 53.5 citations per article. Conclusion There was a noticeable growth of research in transgender health in the last decade. Researchers from different world regions need to get involved in health and human rights research of transgender community. Electronic supplementary material The online version of this article (10.1186/s12914-018-0155-5) contains supplementary material, which is available to authorized users.


Background
The term "transgender" describes a wide range of persons who are present across different cultures and countries [1]. The opposite term to transgender is "cisgender" which is a description for people whose gender identity matches the sex that they were assigned at birth [2]. Unfortunately, no global and updated data on the number of transgender persons are available, but there are approximately 1 million transgender adults living in the United States of America (USA) [3,4] and approximately 9.0 million living in Asia and the Pacific regions [5,6]. Estimates from different world regions indicate that the prevalence of transgender identity varies between 0.1% and 1.1% of reproductive age adults [7].
Transgender people face several social and health challenges such as violence, stigma, discrimination, social rejection, and inadequate specialized healthcare facilities [8,9]. There are tremendous efforts in many developed countries to recognize the human rights of transgender persons [10][11][12]. Part of the action plan to endorse transgender community was to get researchers and academics engaged in research activity pertaining to health needs and challenges facing transgender persons. The scientific community can endorse the transgender community in several ways. For example, The Lancet had issued a series of comments and reports on transgender health that aimed to increase awareness and to promote better health services for the transgender community [8,9,[13][14][15][16][17][18]. Several specific journals have been launched to endorse health and human rights of lesbian, gay, bisexual, and transgender people (LGBTQ). The letter "Q" in the LGBTQ refers to those who identify as queer or are questioning their sexual identity [19].
The Institute of Medicine considers transgender persons as neglected, marginalized, understudied, and in critical and urgent need of research regarding their health status and health needs [1,8]. Transgender individuals are usually researched within LGBTQ community. However, transgender people are different from lesbians, gays, and bisexuals and might have different health and life experiences than gay and lesbians [20]. In light of the large numbers of transgender persons and the international efforts to endorse and strengthen human rights of neglected and marginalized groups, analysis of global research activity in transgender health becomes important [21][22][23][24][25][26][27][28][29]. Therefore, the aim of this study was to assess peer-reviewed literature in transgender health and present the results in bibliometric tables and maps. Research in transgender health is an essential component in recognition of this community and its health needs and health rights. The community of transgender individuals is seeking social support from all communities including those in academia and research scientist. Findings of the current bibliometric analysis could be used to advocate the human and health rights of transgender people particularly in countries with limited research activity in this field. Furthermore, bibliometric data obtained from the current study could be used by international health organizations and health activists to encourage politicians and health policymakers to adopt issues related to transgender health and include these issues in their political agendas and campaigns.

Database
In bibliometric studies, a large database is used to retrieve relevant documents for subsequent analysis. This study was conducted using SciVerse Scopus which has been used in several previously published bibliometric studies [30][31][32][33][34][35][36][37]. The choice of Scopus was based on the advantages it has over Web of Science and Pubmed [38]. The duration of this study was set from 1900 to 2017. Furthermore, no language restriction was made in retrieving the relevant documents. Articles indexed in Scopus must have an English abstract, and therefore, the relevancy of any retrieved document could be confirmed by reading the English abstract regardless of the original language of the document.

Search strategy and inclusion criteria
Search strategy and keywords used were illustrated in (Additional file 1). Keywords used were partially obtained from published systematic reviews in transgender health [9,39,40]. The search strategy was based on both title search and journal search. In the title search, all documents with the following keywords in the title were retrieved: Title(enby or queer or transfeminine or genderqueer or bigender or pangender or genderfluid or agender or "transgender*" or "transsexual*" or "trans men" or "trans women" or "gender dysphoria" or "gender nonconform*" or "sex* reaassig*" or "gender reassign*" or transvest* or travesty or "koti" or "hijra" or "mahuvahine" or "mahu" or "waria" or katoey or "cross dresser" or "bantut" or "nadleehi" or "berdache" or "xanith" or "gender dysphori*" or "gender incongruen*" or "gender non-conform*" or "gender affirm* surg*" or "gender variant" "FTM individ*" or "MTF individ*" or transgender* or "trans men" or transmen or transman or "trans man" or"trans male" or transmale or "trans women" or transwomen or transwoman or "trans woman" or "trans female" or transfemale or "trans masculine" or transmasculine or transsex* or transvest* or "sex reassignment" or "gender reassignment" or "gender change" or "sex change")) or((Title("gender minorit*") and title-abstract-key(transgender* or transsex*))) or ((Title("female to male" OR "male to Female" or M2F or F2M) and title-abstract-key(transgender or transsex*))) or ((Title("two spirits" or "non binary" or cisgender) and title-abstract-key (transgender or transsexual*))) In journal search, all documents published in journals having the keyword "transgender" were retrieved under the condition that the document has the term transgender or transsexual in the title and/or abstract. The search looked like this: (Journal name (transgender*) and titleabstract-key (transgender or transsex* OR M2F or F2M)).
The results obtained from the strategies stated above were combined.

Exclusion criteria
1. Documents published in non-health related journals such as "English teaching" or "English lite*" or Estudios or literature or geography were excluded. 2. Documents within the subject areas of computer, mathematics, physics, chemistry engineering, material science, agriculture, and veterinary were also excluded. 3. Documents with keywords pertaining to plants or animals or birds such as plant or flower or animal or fly or birds or vet* or butterf* were also excluded. 4. Only documents published in peer-reviewed journals were retrieved and analyzed. Conference abstracts/papers published in peer-reviewed journals were included in the analysis while conference abstract not published in peer-reviewed journals were not included in the study. Books and book chapters were excluded.
The asterisk is used in the search strategy as a wildcard to retrieve any possible related keyword while the quotation marks were used to retrieve the exact phrase written within the quotation.

The validity of search strategy
In this study, the validity of the search strategy was confirmed by two methods. In the first method, the author manually reviewed the top 200 cited articles to make sure that all these articles were relevant to the theme of the study. In the second method, the number of articles for each of the top ten active authors was retrieved manually and compared with the number obtained through the search strategy. The results of the comparison showed strong and significant correlation (r = 0.96; p < 0.01) indicative of the high validity of research method.

Bibliometric indicators
Retrieved documents were analyzed and results were presented as top ten active countries, authors, institutions, and journals. Data pertaining to active countries, journals, authors, and institutions are exported from Scopus to Excel program for tabulation. It should be noted here that Scopus counts the number of publications for each country based on author affiliation regardless of the position of the author in the author list. Therefore, there is a potential overlap in the number of publications assigned for each country. For example, a document with two authors from two different countries is counted once for each country. Same applies to data pertaining to most active authors and institutions.

Bibliometric mapping
Author keywords were visualized using VOSviewer program [41] which is available for free download [42] along with its technical manual [43]. In VOSviewer, author keywords are mapped based on a minimum number of occurrences. The size of the node for each keyword in the map represents its frequency of occurrence in the retrieved documents. Larger node size indicated a high frequency of occurrence. VOSviewer can also be used to do overlay visualization in which keywords with yellow color represent the most recently used author keywords. The geographical distribution of publications was mapped using ArcGIS 10.1 software [44]. This software is available at the Faculty of Engineering at An-Najah National University and available for staff use. In ArcGIS, different colors are given to various world regions. Map regions with white color represent countries with missing data or no research contribution to the field being investigated. In the current study, the impact of publications was measured using Hirschindex (h-index) which depends on the number of citations of the publication with higher h-index indicating higher impact [45].

Ethical consideration
No human subjects were involved in this study and, therefore, no approval from institutional review board was required.

Growth of publications
The oldest published article in transgender health appeared in "Zeitschrift für die gesamte Neurologie und Psychiatrie" journal in 1913 [46]. This article discussed the neurological and psychiatric background of transvestism. The number of publications continued to grow slowly from 1913 to 2004 (Fig. 1

Citation analysis
The retrieved documents received 69910 citations, an average of 12.1 citations per document. The h-index of the retrieved documents was 92. The range of citations obtained was from 0 to 524. The article that received the highest citations was published in International Journal of Transgenderism in 2012. This article provided clinical guidance for health professionals on how to assist transgender, transsexual, and gender non-conforming people in a safe and effective way [47]. Table 1 shows the list of highly cited articles. The list included seven research articles and three review articles. Three of the highly cited articles were published in Journal of Homosexuality. The list included articles that discussed aspects in the field of mental health, infectious diseases, endocrinology, neurology, and public health of the transgender community.

Mapping author keywords
Health-related author keywords with minimum occurrences of 10 were visualized and presented in network visualization map (Fig. 2 a). The most frequently encountered author keywords were grouped into seven different clusters shown in different colors. The most prominent clusters were those pertaining to HIV and other sexually transmitted diseases (STD), mental health, social acceptance and human rights, psychotherapy, and counseling. Overlay visualization, which shows the time of appearance of most frequently author keywords, indicated that keywords such as stigma, health disparities, health services, resilience, HIV prevention, and social support were the most recently used author keywords (Fig. 2 b).

Geographical distribution of retrieved documents
Authors from 80 different countries contributed to publishing the retrieved documents. Geographical distribution of the retrieved documents was based on the country affiliation of all authors participating in publishing the retrieved articles. Retrieved documents originated mainly from Northern America, certain European countries, Australia, and Brazil (Fig. 3). The African region, Middle East, and

Highly active countries
The top ten active countries were shown in Table 2 along with the impact of their publications measured as the number of citations per article. Documents with authors from the Netherlands had the highest impact with an average number of citations of 35 per document followed by those from Belgium (17.1), and those from the USA (15.6). Authors in top ten active countries contributed to 4377 (75.1%) documents. Authors from the USA participated in publishing 2494 (43.2%) documents. The most active countries included one country from Latin America; Brazil (114; 2.0%). None of the countries in top ten list were from South -East Asia or Africa or the Middle East or Eastern Europe.

Authorship analysis and active institutions/organizations
Approximately 10,000 authors participated in publishing the retrieved documents, an average of 2.4 authors per document. Table 3 shows top ten active authors Professor Gooren, L.J.G. was the most active with 104 (2.4%) publications. The most active authors were in the fields of endocrinology, plastic surgery, psychiatry/psychology, sexology, and public health. Five of the top ten active authors were from the USA, three were from the Netherlands, and two were from Belgium. When retrieved data were analyzed for most active institutions/organizations, the VU University Medical Center in the Netherlands ranked first with 184 (3.2%) publications followed by the University of California, San Francisco (USA) with 157 (2.7%) publications. Seven institutions of the top ten list were in the USA, one was in Canada, one was in Belgium, and one was in the Netherlands (Table 4).

Most active journals
Retrieved documents were published in journals with different scopes. The top ten list included journals in the field of transgender /sexual medicine, public health, endocrinology, plastic surgery, and psychiatry (Table 5).   (27). The majority of top 10 active journals were in the field of sexual medicine. One journal was in the field of public health, one was in plastic surgery, and one in the field of AIDS. Eight of most active journals were based in the USA while two were based in Europe.

Discussion
In this study, we aimed to assess and analyze growth and research trends of peer-reviewed publications in transgender health. Publications in transgender health showed a sharp rise after 2005. Several factors could be cited to explain the sharp rise in the number of publications. Of particular importance is the appearance of publications in transgender health in highly prestigious journals such as The Lancet and the American Journal of Public Health which encouraged researchers in various disciplines to get involved in this research topic. A potentially second reason is the findings that the number of transgender people is larger than expected even in epidemiological studies and surveys in non-western countries [48,49]. A third possible reason is the active role of human rights and transgender groups which argued against stigma and discrimination faced by the transgender community [10,[50][51][52][53][54]. Furthermore, transphobia led many researchers and health organizations to address this issue in international forums in order to support the health and human rights of the transgender community [55][56][57][58][59].
The current study showed that mental health research dominated the field of transgender health. Most mental health issues faced by transgender people are due to cultural intolerance, social stigma, discrimination, violence, and victimization [60][61][62][63][64]. The social stress and stigma created higher prevalence of depression and suicidal ideation in transgender individuals compared with cisgender people [65,66]. Transgender individuals are subject to psychological stress [67] due to discrimination and social rejection. It should be emphasized that mental health issues in transgender persons are not due to transgender identity [9]. Studies indicated that a major cause of depression and suicidal ideation among transgender individuals is the stigma, trans-phobia, sexual assault, violence, and social de-evaluation [68,69]. The World Health Organization (WHO) is considering declassification of transgender and sexual orientation from mental health disease classification [70]. Such move by WHO was supported by the scientific community [71,72]. A key element in overcoming mental problems such as depression, anxiety, and stress in transgender persons is social support and acceptance [73,   [66].
The current study showed that global contribution to transgender health research was limited to the regions of Americas, Europe, South-East Asia, and Western Pacific. It was not surprising that countries such as USA, Brazil, Philippines, and Thailand showed relatively high research activity. Unofficial reports indicated large numbers of transgender people in these countries. The number of publications from African and Mediterranean regions was limited. This could be attributed to the limited number of transgender people in both regions or due to limited research capacity in these regions. African region is considered the highest in terms of numbers of people with AIDS [75,76] which could be due to the presence of infected female sex workers, lack of healthcare, and preventive measures but not due to transgender identity [77][78][79]. For the Mediterranean region, the cultural and religious background does not allow for sexual freedom and, therefore, data regarding transgender people, HIV, gay, lesbians, and bisexuals are relatively limited and might be inaccurate in that region [80][81][82][83][84].
The current study indicated that literature in transgender health discussed several aspects of STD including HIV/AIDS. A study carried out in the USA found that 28% of transgender individuals had HIV and 21% had other sexually transmitted diseases [40,85]. Lack of preventive health practices and lack of screening are potential causes for the high prevalence of STD among transgender individuals [86][87][88][89].
Transgender health is a global issue and publications in this field is growing as a separate field or as part of research in LGBTQ community as an overall. The author did his best to collect all peer-reviewed documents in transgender health to endorse research and encourage other researchers and clinicians to get engaged in this field. However, the author acknowledges the fact that not all publications and health journals are indexed in Scopus and therefore, some publications in this field might be missed. This is a common limitation in bibliometric studies [31,36,[90][91][92][93].

Conclusion
The results of the current study showed (1) dramatic increase in the number of publications in transgender health in the last decade; (2) the bulk of literature in transgender health focused on HIV/AIDS, mental health, and discrimination; (3) regions of Africa, Middle East, and East Europe had the least research contribution to transgender health; (4) most active and leading authors and institutions in transgender health were restricted to northern America and Europe; and (5) h-index of peer reviewed documents in transgender health was less than 100 but relatively higher than that recorded for other subjects [34,94].

Funding
None.

Availability of data and materials
All data present in this article can be retrieved from Scopus using keywords listed in the methodology.
Authors' contributions WS: concept, data extraction, analysis and presentation, manuscript preparation, and manuscript submission and follow up. The author read and approved the final manuscript.
Ethics approval and consent to participate Not applicable.

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Competing interests
The author declares that he has no competing interests.

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