Evolution of Telepathology: A Comprehensive Analysis of Global Telepathology Literature Between 1986 and 2017

Objective: Telepathology is an application of telemedicine providing remote evaluation and consultation of digital pathology images and can be used for educational or experimental purposes. Bibliometrics is a statistical discipline investigating publication patterns and trends in a certain academic field. Although bibliometric and scientometric studies are becoming increasingly popular, the relevant literature contains only one limited article related to telepathology. The aim of our study was to perform a holistic bibliometric analysis of the telepathology literature. Material and Method: Since the first article on telepathology was published in 1986, we included all indexed articles retrieved from Web of Science databases between 1986 and 2017. Results: We found that the USA covering 43.01% of all literature was the leading country in the telepathology field and was followed by Germany, Italy and the UK (n=120, 90 and 83, respectively). The countries with the most contributions were located in the continents of Europe and North America. The most productive source titles were Human Pathology, Journal of Telemedicine and Telecare, and Modern Pathology. Harvard University ranked first with 59 articles. The most commonly used keywords of the telepathology literature were “telepathology”, “telemedicine”, “digital pathology”, “virtual microscopy” and “telecytology”. We noted that all of the ten countries with the most contributions were in the developed category of UN classification and all twenty of the most productive institutions were from developed countries. Conclusion: We suggest that researchers from developing and least developed countries should be encouraged to carry out novel studies since telemedicine is a required and promising technology for rural developing or least developed areas in which access to health care is difficult.


INTRODUCTION
Telemedicine is the process of transmitting medical information and the application of medical services using communication technologies (1).The World Health Organization (WHO) defines telemedicine as "..the delivery of healthcare services, where distance is a critical factor, by all healthcare professionals using information and communication technologies for the exchange of valid information for diagnosis, treatment and prevention of disease and injuries, research and evaluation, and for the continuing education of healthcare providers, all in the interests of advancing the health of individuals and their communities…" (2).Telepathology is a relatively novel practice of telemedicine providing remote evaluation of digital pathology images.Telepathology is defined by the American Telemedicine Association as "the electronic multimedia communication across a network of pathologyrelated information, between two or more locations for use between pathologists and/or qualified laboratory personnel, and may include involvement by clinicians and/or patients" (3).Telepathology can be used for educational or experimental purposes, primary diagnosis and secondary consultation in all divisions of pathology including histocytopathology, autopsy, and surgical and anatomical pathology (4).
Bibliometrics provides holistic data on publication trends and patterns and is described as "science of science" (5).Although scientometric and bibliometric studies have been popular recently, only one study relevant to telepathology has been reported so far to the best of our knowledge.To fully utilize the advantages of telepathology, individual feasibility studies are necessary, as data analysis, organizations, societies and infrastructures (6).Our study aims to present a comprehensive bibliometric analysis of the literature of telepathology.

MATERIAL and METHOD
All data of our study was retrieved from four databases of Web of Science (WOS, Thomson Reuters, New York, NY, USA) titled Web of Science Core Collection, Korean Journal Database, SciELO Citation Index and Russian Science Citation Index.We used the keywords of "telepathology" and "telecytology" to search the WoS database.All documents produced between 1986 and 2017 were included.Since the first article of telepathology literature was published in 1986, we chose 1986 as the starting year.We used GunnMap to generate a global productivity map (7).VOSviewer was the freeware tool used for creating scientometric networks in our study (8).We used the United Nations (UN) system for country classification (9).

General Feature of the Literature
Our search yielded 1109 articles in the telepathology literature between 1986 and 2017.Only 237 documents (21.37%) were open access.The peak year for number of publications was 2012 with 83 articles.No pattern was detected in the progress of the total number of publications by year.No items were produced in the years of 1988, 1990 and 1992 (Figure 1).English is the main language of the literature (94.91%) followed by German and French (2.43 and 2.08%, respectively).The most studied research areas were found to be health care sciences, telecommunications, pathology, computer science and oncology (68.89, 63.12, 55.45, 42.38 and 39.58%, respectively; Table I).The most common document types in the literature were original article, meeting abstract and review (72.77, 28.40 and 18.12%, respectively; Table II).

Productivity of Countries, Authors, Journals and Institutions
The USA, covering 43.01% of the literature, was detected to rank first among countries with 477 articles, followed by Germany, Italy and the UK (n=120, 90 and 83, respectively;

Citations, Keywords and Bibliometric Network Analyses
The h-index is a calculated metric value to measure productivity and citation impact in a certain area.The h-index of telepathology literature was 52.The total number of citations was 14,911 (8,997 without self-citations) and the average number of citations per item were 13.45.The most common keywords of the telepathology literature were "telepathology", "telemedicine", "digital pathology", "virtual microscopy" and "telecytology" (Table VIII).Bibliometric network analysis of the keywords revealed a "starburst pattern" in which keywords of "telepathology", "digital pathology" and "internet" were centered (Figure 4).As we analyzed the co-authorship among countries, it was found that the most collaborative countries were the USA with 377 documents and 6286 citations (total link strength, TLS=127) followed by Italy, the UK and Germany (TLS=79, 73 and 71, respectively; Figure 5).

DISCUSSION
The earliest telemedicine applications date back to the eighteenth and nineteenth centuries.In these centuries, patients wrote detailed letters containing medical histories and symptoms and sent them to specialist doctors by couriers, and doctors responded with the diagnosis, treatment plan and prescription (12).Willem Einthoven (1860-1927), a Dutch doctor and physiologist who invented the first electrocardiogram (ECG) transmitted ECGs of the patients from the hospital to an off-site laboratory by means of telegraph (13).The first remote assessment of medical images, reported in 1950, was performed between the Chester County Hospital and Philadelphia over a distance of twenty-eight miles via commercial telephone wires or radio and described as "telognosis" (14).In the late 1950s, National Aeronautics and Space Administration (NASA) initiated the Space Technology Applied to Rural Papago Advanced Health Care (STARPAHC) Project for telemedical consultation of people living in remote locations of Arizona's Papago Indian Reservation with little or no medical services.In 1964, a closed circuit television system was introduced between the Nebraska Psychiatric Institute and the Norfolk State Hospital 112 miles away to use telemedicine for neurologic and psychiatric evaluation of the patients (15).The first recorded telepathology procedure was performed in the late 1960s between Massachusetts General Hospital and Logan Airport Medical Station in Boston via a realtime "television microscopy" service (16).Since this onset, the research area of telepathology has been growing into subfields.The first paper in the telepathology field was an editorial published in 1986 and titled "Prospects for Telepathology" by Ronald Weinstein.The author defined telepathology as "the practice of pathology by visualizing an indirect image on a television screen rather than viewing a specimen directly through a microscope…".Interestingly, there was no study on telepathology in the  Bibliometrics is a popular statistical application providing quantitative and qualitative analysis of a certain academic field (19).The term was coined by Alan Pritchard in the late 1960s as ''an application of mathematics and statistical methods to books and other media of communication" although Siyali Ramamrita Ranganathana, who was a librarian and mathematician from India, created the principal ideas behind bibliometrics and scientometrics in the 1940s (19,20).Bibliometric studies have become increasingly popular in the academic literature in the last decades, and a total of 8806 reports have been published in the time period of our study according to the WoS databases.Although the term of telepathology has been included in MeSH terminology since 1996, the scientific literature contained only one bibliometric study of telepathology.Della Mea reported the first and only bibliometric study in the telepathology literature in 2011 (21).The data of this study was extracted from PubMed and only 967 papers medical literature prior to this definition.Weinstein predicted the future of computer technology perfectly and defined the level of development of telepathology at that time as "an embryonic stage of development" (16).Over the last 30 years, the generation of telepathology systems has improved rapidly with the evolution of digital microscopy: video-microscopy, robotic microscopy and the upgrade to virtual slide processing systems.This change is a revolution in the traditional pathology practice in today's computer age (17).Increased workload, case complexity, financial constraints, and staffing shortages justify wider implementations of digital pathology (6).The possibility to consult expert colleagues using telepathology, particularly for cases not requiring molecular investigations in external laboratories, may also permit significant financial savings, reduce the turnaround time, facilitate the international change of information, and support the sharing of even more cases (18).

Figure 2 :
Figure 2: Top ten countries publishing telepathology articles between 1986 and 2017.

Figure 3 :
Figure 3: Publication density of world countries in the telepathology field.

Figure 4 :
Figure 4: Bibliometric network of the most used keywords in the telepathology literature.

Figure 5 :
Figure 5: The most collaborative countries in the telepathology literature.

Table I :
The most studied research areas of the telepathology literature between 1986 and 2017.
Figure 1: Number of telepathology publications by year.

Table II :
Document types published in the telepathology literature.Table III).The source titles with the most contributions were Human Pathology, Journal of Telemedicine and Telecare and Modern Pathology (n= 80, 69 and 56 articles, respectively; Table IV).The most productive meeting in this field was the 10 th European Congress on Telepathology and the 4 th International Congress on Virtual Microscopy with 20 proceedings (Table V).Harvard University was the leading institution with 59 documents followed by the University of Arizona, Pennsylvania Commonwealth System of Higher Education, and the University of Pittsburgh (n= 52, 50 and 48 items, respectively; Table VI).

Table III :
The 20 most prolific authors of the telepathology literature between 1986 and 2017.

Table IV :
The journals with the most contributions to the telepathology literature.

Table VII :
The most cited articles in telepathology literature by decades.

Table VIII :
The 20 most used keywords in the telepathology literature.