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Review Article

The 100 Most Cited Articles in Ophthalmology in Asia

Koh, Barry Moses Quan Ren BMedSc∗,†; Banu, Riswana DipSci; Sabanayagam, Charumathi PhD∗,‡

Author Information
Asia-Pacific Journal of Ophthalmology: September-October 2020 - Volume 9 - Issue 5 - p 379-397
doi: 10.1097/APO.0000000000000325

Abstract

Asia has seen a rise in ophthalmic diseases over the past decades, largely due to rapid population growths, ageing populations, and environmental risk factors.1 With 2 of the most populous countries in the world, China and India, still having the highest numbers of visually impaired people globally,2 Asia presents itself with a large data set to be studied. Beyond different prevalence of blindness between Asia and the rest of the world, prevalence of eye diseases also differs between races and regions within Asia (eg, myopia3 and angle-closure glaucoma4 are more common in Chinese compared to other Asian races). These unique epidemiological trends coupled with opportunities for ophthalmic research within Asia have led to the publication of highly cited ophthalmic research articles.

Much of the world's current understanding on Asian eye epidemiology has been elucidated from notable eye studies. Numerous well-characterized population studies (like the Taiwan Shihpai Eye Study,5 Japan Tajimi Study,6 Beijing Eye Study,7 Singapore Epidemiology of Eye Disease Study,8 and Andhra Pradesh Eye Study9) have allowed researchers to better understand the epidemiology and natural history of prevalent eye diseases within Asia. At the same time, there have been major advances into the science and practice of ophthalmology within Asia to meet the rising need of more efficient eye diagnosis and treatments elucidated by those studies. Numerous novel clinical studies [like Atropine for treatment of childhood myopia,10 and treatment of age-related macular degeneration (AMD) with embryonic stem cells11] were conceived in Asia to meet the challenges of high rates of myopia in Asian children8 and AMD in ageing Asian countries,12 respectively.

Today, Asia is facing a strategic test in catching up with the west in ophthalmic research, a development that presents both opportunities and challenges. With Asia's burgeoning middle class, its contributions to notable eye research has increased greatly at the turn of the century.13 A previous study identified that before 2000, only 3% of the 100 most cited articles on diabetic retinopathy (DR) came from Asia. After 2000, this number increased to 18%, marking an inflexion point for Asian eye research.14 Many of the problems Asia started facing 2 decades ago such as high myopia rates in children are now becoming problems for the West.15 Thus, there is a global imperative to understand the current landscape of Asian ophthalmology, as such, a review of the top 100 most-cited articles in ophthalmology and nonophthalmology journals was done.

METHODOLOGY

Search Strategy for Articles in Ophthalmology Journals

To generate the T100 list for Ophthalmology journals (T100-Eye), we searched the Scopus database by “source title,” using the relevant keywords and Boolean operators: “ophthalmology” OR “eye” OR “ocular” OR “ophthalmic” OR “retina” OR “cataract” OR “cornea” OR “vision research” OR “vision neuroscience” OR “retinopathy” OR “glaucoma.” The search was refined to “articles” OR “reviews,” limited to articles published in “English” and further refined by “country/territory” to include only countries in Asia. A list of ophthalmology journals was obtained from the 2018 Journal Citation Report (JCR, n = 57), which was used to further refine the search by “source title.” The articles from Scopus were sorted on highest number of citations by using “cited by (highest).” After limiting articles to between 1970 and 25 February 2020, the search result yielded 75,476 articles.

The top 200 articles were evaluated for their eligibility based on full-text reviews to ensure relevance to ophthalmology and Asia. This was done by excluding articles that had first or last author from countries outside Asia (such as non-Asian institutions) by 2 independent investigators (B.K. and R.B.) which were confirmed by a senior investigator (C.S.). The top 100 cited articles remaining were chosen.

Search Strategy for Articles in Nonophthalmology Journals

To generate the T100 list for general nonophthalmology journals (T100-General), we conducted a search by “article title” alone, based on keywords from most prevalent eye diseases which included: “ocular” OR “cataract” OR “retinopathy” OR “diabetic macular edema” OR “glaucoma” OR “macular degeneration” OR “maculopathy” OR “blindness” OR “keratoconus” OR “visual impairment” OR “visual acuity” OR “myopia” OR “microvascular.” After excluding articles published from ophthalmology journals, and by applying the same exclusion criteria as T100-Eye, 15,827 articles were found.

Characteristic and Statistical Analysis

Characteristics of these articles were analyzed according to the number of citations, journal, year of publication, impact factor (IF) based on the 2018 Thomson Reuters’ JCR, article type, country of origin, number of authors, and sex of authors. Articles from Asia represented those published from an Institution in Asia based on the first author's affiliation(s). The country of origin of each article was based on the affiliated institution of the first author as indicated on their publication. To identify the author's sex, name of authors was searched on institutional websites, finding their sex based on names and/or their photographs and/or their biographical paragraphs. Based on the objective of the research, articles were classified into 5 groups: epidemiological studies, that evaluated the prevalence or incidence of diseases or risk factor associations and health service research; clinical studies that included cases series, clinical observations, description of new management or investigative techniques, new diagnoses or classification, and genome-wide association studies; randomized controlled trials (RCTs) including data from RCTs that were observational in nature; basic science studies concerning histology, animal models, or molecular studies; reviews including narrative reviews, systematic reviews, and meta-analyses.

We compared the characteristics of articles using χ2 test (categorical variables), Kruskal–Wallis test, and Spearman correlation test. P values <0.05 were considered significant.

RESULTS

Citation Count and Publication Year

The T100-Eye articles were published between 1982 and 2015 (Table 1   ). The mean and median numbers of citations were 354 and 317, respectively (range: 249–1326). Six articles were cited >500 times of which only 1 was cited >1000 times. The most number of articles were published in the 5-year period between 2001 and 2005 (29%), followed by 1996 to 2000 (25%) and 2006 to 2010 (24%) (Fig. 1). Majority of reviews (11/12), epidemiological articles (25/30), and clinical studies (26/35) were published from 2000, whereas majority of RCTs (7/9) were published before 2000. Basic science articles had no discernible distribution patterns.

TABLE 1
TABLE 1:
The Top 100 Most Cited Articles From Asia in Ophthalmology Journals (T100-Eye) From 1960 to 2019
TABLE 1 (Continued)
TABLE 1 (Continued):
The Top 100 Most Cited Articles From Asia in Ophthalmology Journals (T100-Eye) From 1960 to 2019
TABLE 1 (Continued)
TABLE 1 (Continued):
The Top 100 Most Cited Articles From Asia in Ophthalmology Journals (T100-Eye) From 1960 to 2019
TABLE 1 (Continued)
TABLE 1 (Continued):
The Top 100 Most Cited Articles From Asia in Ophthalmology Journals (T100-Eye) From 1960 to 2019
FIGURE 1
FIGURE 1:
Number of T100 articles by publication period.

The T100-General articles were published between 1982 and 2017 (Table 2    ). For the full list refer to online supplementary tables, http://links.lww.com/APJO/A62. The mean and median citation counts were 265 and 158, respectively (range: 105–2628). Eight articles were cited >500 times of which 3 were cited >1000 times. The peak publication period occurred from 2001 to 2005 (31%), followed by 2006 to 2010 (23%), and 2011 to 2015 (20%) (Fig. 1). Seventy-eight percent of T100-General articles were published after 2000. Majority of reviews (15/16), epidemiological articles (9/13), clinical studies (33/37), and basic science articles (24/32) were published from 2000.

TABLE 2
TABLE 2:
The Top 100 Most Cited Articles From Asia in Non-Ophthalmology Journals (T100-General) From 1960 to 2019
TABLE 2 (Continued)
TABLE 2 (Continued):
The Top 100 Most Cited Articles From Asia in Non-Ophthalmology Journals (T100-General) From 1960 to 2019
TABLE 2 (Continued)
TABLE 2 (Continued):
The Top 100 Most Cited Articles From Asia in Non-Ophthalmology Journals (T100-General) From 1960 to 2019
TABLE 2 (Continued)
TABLE 2 (Continued):
The Top 100 Most Cited Articles From Asia in Non-Ophthalmology Journals (T100-General) From 1960 to 2019
TABLE 2 (Continued)
TABLE 2 (Continued):
The Top 100 Most Cited Articles From Asia in Non-Ophthalmology Journals (T100-General) From 1960 to 2019

Journal Title and IF

The T100-Eye articles collectively published in 22 ophthalmology journals. The journals with the most articles were Ophthalmology (n = 22, IF = 7.732), followed by Investigative Ophthalmology and Visual Science (IOVS, n = 17, IF = 3.812), and American Journal of Ophthalmology (AJO, n = 16, IF = 4.483) (Table 4). These 3 journals together represented 55 citation classics, and contributed to 6 of the top 7 most cited articles.

TABLE 3
TABLE 3:
Authors With ≥3 Total Number of T100 Publications.
TABLE 4
TABLE 4:
Journals That Contribute ≥3 Articles To The Top-100 Lists by IF

Two journals with relatively low IF in comparison to other journals, but had remarkably high number of publications, were: IOVS (IF = 3.812, ranked 8th in Journal IF) with 17 publications, and British Journal of Ophthalmology (BJO, IF = 3.615, ranked 9th in journal IF), with 5 articles. The median journal IF value was 4.4 (range: 1.6–11.8). There was no significant correlation between journal IF and number of citations (Pearson correlation coefficient = 0.07, P = 0.5). The article with the highest number of T100-eye citations (1326 citations) was a review and meta-analysis article on glaucoma by Tham et al from Singapore and was published in Ophthalmology in 2014.

The T100-General articles came from a wider source of journals, being published in 65 medical journals. Most articles came from Nature Genetics (n = 5, IF = 25.455), followed by Journal of Medical Systems (JMS, n = 4, IF = 2.415), Lancet (n = 4, IF = 59.102), New England Journal of Medicine (NEJM, n = 4, IF = 70.67), and Proceedings of the National Academy of Sciences of the United States of America (PNAS, n = 4, IF = 9.58). The article with the highest number of citations (2628 citations) was a RCT on diabetic microvascular complications and was published in Diabetes Research and Clinical Practice by Ohkubo et al from Japan in 1995. The second highly cited article (n = 1476) was a systematic review and meta-analysis article on DR by Yau et al published in Diabetes Care in 2012.

T100-General showed significant, but weak correlation between journal IF and number of citations (Pearson correlation coefficient = 0.25, P = 0.01). The median journal IF was 5.5 (range: 1.0–70.7). JMS and Annals of the Academy of Medicine Singapore (AAMS, n = 3, IF = 1.127) were 2 journals that had relatively high number of publications despite their low IFs.

Publication Patterns

Among the T100-Eye journals, Ophthalmology published from a wide diversity of Asian countries (Ophthalmology: 9 from Japan (41%), 4 from China, 4 from Singapore, 2 from Hong Kong, 1 from Taiwan, 1 from India and 1 from South Korea), compared with BJO (3/5 from Japan, 60%), AJO (10/16 from Japan, 63%), and Archives of Ophthalmology (6/8 from Japan, 75%).

Among the top general medical journals, Nature affiliated journals were journals that published more internationally (Nature research journals: 3 from Japan, 3 from Singapore, 2 from Israel, 1 from China and 1 from South Korea), compared to JAMA (2/3 from Singapore, 67%), NEJM (3/4 articles from Japan, 75%), and Lancet (4/4 from Singapore, 100%).

Type of Research

The number of articles by article type in the T100-Eye and T100-General were as follows: clinical studies (n = 35, n = 37), basic science (n = 14, n = 32), epidemiology (n = 30, n = 13), reviews (n = 12, n = 16), and RCTs (n = 9, n = 2) (Fig. 3). In T100-Eye, there was no significant association between article type and citation counts (P = 0.2), but there was a significant association between article type and journal IF (P = 0.002), with clinical studies publishing in journals with higher IF (median IF = 4.5) followed by epidemiology (median IF = 4.4), compared to review, RCT, and basic science (median IF = 4.0, 3.8, 3.8). For T100-General, although epidemiology articles had higher number of citations compared to other type of articles (median citations = 202 vs 151.5 for basic science, 160 for clinical studies and 142.5 for reviews), the differences were not statistically significant (P = 0.6). With regards to article type and IF, reviews were published in journals with higher IF (median IF = 9.3) while epidemiology in journals with lower IF (median = 4.5), but the difference was not statistically significant (P = 0.4).

FIGURE 3
FIGURE 3:
Number of T100 publications by research type.

Disease Category

Within the T100-Eye, the top 3 most prevalent diseases studied were myopia (n = 16), AMD (n = 15), and glaucoma (n = 10). Within the T100-General, the 3 most studied diseases were DR (n = 24), glaucoma (n = 16), and AMD (n = 12). (The full list of diseases is included in Table 5).

TABLE 5
TABLE 5:
Number of T100 Articles By Disease Categories

Authorship, Country of Origin, and Sex

The T100-Eye and General originated from 12 and 10 countries, respectively (Fig. 2). The country with the most T100-Eye and T100-General articles came from Japan (n = 42, n = 36), followed by Singapore (n = 17, n = 26), China (n = 9, n = 7), and India (n = 8, n = 10).

FIGURE 2
FIGURE 2:
Number of T100 publications by country of origin.

Overall, 82% and 84% of first authors were male for T100-Eye and T100-General, respectively, whereas 98% and 96% of last authors were male for T100-Eye and T100-General, respectively. There were no significant associations between sex of the first or last author with journal IF (P = 0.5, 0.1) or with number of citations (P = 0.9, 0.9) for the T100-Eye. Similarly, the T100-General had no significant associations for the same tests (P = 0.1, 0.2, 0.6, 0.8).

The countries with the most number of female first authors in the T100-Eye were Japan (n = 7), Singapore (n = 6), and Hong Kong (n = 2). For the T100-General, they were Japan (n = 5) and Singapore (n = 5), India (n = 3), and Thailand (n = 2). For female last authors in the T100-Eye there were only 2, one from Singapore and the other one from China. For female last authors in the T100-General, they were Singapore (n = 2) and India (n = 2).

A total of 8 first authors in the T100-Eye and 2 first authors in the T100-General had ≥3 T100 publications (Table 3). For the T100-Eye, 4 of the 8 authors were from Japan. For the T100-General, both authors were from Singapore. Wong had the most number of publications as first author (T100-Eye = 6, T100-General = 4). Tsubota had the highest number of last-author publications (n = 6) in T100-Eye, whereas Wong had the most in T100-General (n = 8).

Emerging Research Topics

The most recently studied topic in the T100-Eye was on the use of optical coherence tomography angiography (OCTA) to study the vascular clinical features of DR (n = 1) and glaucoma (n = 1). These 2 articles were published in 2015.

One of the most recent topics in the T100-General was on the use of artificial intelligence (AI) and automated detection systems to screen for DR (n = 10) and glaucoma (n = 4), using retinal and fundus images. Of the 14 articles on AI, 13 were published from 2008 to 2017. The 14 articles originated from 5 countries: Singapore (n = 8), Thailand (n = 2), India (n = 2), Pakistan (n = 1), and Japan (n = 1). Another recent topic is on the use of big data, specifically to complement AI and genomics meta-analysis studies. Big data were used in 3 articles in the T100-General published in 2011, 2012, and 2014 for genome-wide analysis studies on glaucoma and myopia.

DISCUSSION

The key findings of our analysis were the following. First, the peak publication period occurred from 2001 to 2005. Second, T100-Eye had higher number of citations than T100-General but published in journals with lower IF than T100-General. Third, observational studies including clinical and epidemiological studies were published in journals with higher IF than other type of studies. Fourth, the most-studied disease categories were myopia and AMD in T100-Eye, and DR and glaucoma in T100-General. Fifth, among top journals, Nature journals and Ophthalmology published more internationally. Sixth, majority of articles came from Japan and Singapore. Seventh, the author with higher number of first and last author was Wong from Singapore. Lastly, the most recent publication was OCT angiography in the T100-Eye, AI and big data in the T100-General.

Citation Count and Publication Year

The 2001 to 2005 Publication Peaks

The most number of publications came from 2001 to 2005, with 29 and 31 T100-Eye and T100-General articles, respectively. For the T100-General, 13 of these 31 articles belonged to the subcategory of basic science studies (8 from Japan). Likewise, 8 of the T100-Eye articles from 2001 to 2005 came from Japan. It becomes evident that Japan's contributions in basic science research from 2001 to 2005 were largely responsible for the peak in T100 publications. One reason to explain why Japan published such high numbers of basic science articles during that period may be due to policies like Japan's Science and Technology Basic Law (S&T), which emphasized research in basic science studies around the mid-1990s.16

Journal Title and IF

General Medical and Diabetes Journals Outperformed Ophthalmology Journals in IF

Publications from general medical journals, which included diabetes journals, had higher journal IFs compared to ophthalmology journals. They also produced more landmark articles, which are publications cited >1000 times, compared to ophthalmology journal. One such example includes the most cited article with 2628 citations, published in Diabetes Research and Clinical Practice, examining whether intensive insulin control could decrease diabetic microvasculature complications.17

These findings are in line with current literature. One study found that ophthalmology articles published in high-impact general medical journals have a lower risk of bias assessment compared to those published in high impact ophthalmology journals.18 Another article found that general medical journals had significantly lower self-citation rates compared to subspecialty journals within the field of ophthalmology.19 Thus, general medical journals remain the primary journal for landmark ophthalmology publications.

Ophthalmology Journals Had Higher Citations Than General Medical Journals

Despite general medical journals outperforming ophthalmology journals in IF, this did not translate into higher citation counts for general medical journals. This was unexpected as IFs are usually correlated with citation counts.20 This indicates that journal IFs alone do not entirely reflect the impact that articles can have over time, neither does it always influence which journals authors choose to publish in. Bibliometric analyses in other fields of medicine too found that IFs alone are not comprehensive indicators of the quality or impact that an article has over time.20

Type of Research

Clinical and Epidemiological Studies Were Published in Journals With Higher IF

From the results, observational studies including clinical and epidemiological studies were found to be published on average in higher IF journals compared to other types of studies. Current literature revealed that RCTs have been viewed as the highest quality studies for evidence based medicine.21 Surprisingly, observational studies outperformed RCTs both in number of articles and journal IF, which has challenged the notion that RCTs are the most commonly cited type of studies.

There are a few reasons that might explain this finding. First, observational studies could have complemented RCT findings in hypothesis generation and clinical testing.21 For example, in some situations, it may be difficult or unnecessary to perform a RCT; in these situations, well-designed observational studies may provide an alternative to obtain relevant data. A study suggested that observational studies advantages can be attributed to their applicability to patients.22 Another reason why observational studies were published in higher IF journals might be due to their history, as many well-accepted causal associations between vascular diseases and eyes have been based on observational studies.23 Lastly, observational studies also identify adverse reactions with the use/withdrawal of drugs that were not originally predicted based on research during the drug testing.24 These reasons might explain why observational studies were published on average in higher IF journals.

Disease Category

Myopia Was the Most Studied Eye Disease in T100-Eye

There are a few reasons that explain why myopia was ranked as the most studied disease in the T100-Eye. First, there is an inclination for Asia to focus on myopia research more than any other eye disease because the prevalence of myopia in East Asian countries are the highest worldwide.25 For example, myopia rates are estimated to be 40% in Japan,26 50% in Taiwan,27 and 70% in Singapore,3 which stand in stark contrast to 40% in the United States.15 As the prevalence of myopia is best studied through epidemiology articles,28 it was no surprise that in the T100-Eye, epidemiological studies were the most popular article type for myopia (16/24). One such example is the Tajimi Study from Japan which examined the prevalence of myopia in 3021 elderly Japanese people.6 The study found overall prevalence of myopia in the aged to be 41.8%, which was higher than what similar population studies previously reported. With increasing prevalence of myopia,3,15,25,29 new epidemiological studies on myopia will be needed to continually update older studies.

A second reason to explain why Asian myopia studies were cited highly is because many sociodemographic risk factors of myopia are more commonly found in Asian populations rather than Western ones.3 Consequently, this meant that many sociodemographic risk factors of myopia were discovered by population studies from Asia. One such sociodemographic risk factor is rapidly increasing education levels.30,31 One study in the T100-General investigated whether there was an association between myopia and educational attainment in Singapore.32 The study revealed that both prevalence and severity of myopia increased with higher levels of education. Singapore, Taiwan, and Hong Kong had periods of rapid educational growth33; hence, studies on education and myopia were best suited for them. Due to Asia's unique sociodemographic, many interesting risk factors of myopia are best elucidated from studies in Asia, explaining their popularity.

A third reason to explain myopia's popularity is that myopia can result in related eye problems.34,35 For example, cataracts developed sooner in highly myopic eyes.36 This can result in greater health care cost for Asian countries and increase pressure on ophthalmological and vision correction services.37 This conundrum has provided impetus for innovation. Large intervention studies from Taiwan38 and Singapore10 showed clinically significant results for the use of atropine to retard the progression of myopia. One T100-Eye article was on myopia treatment using a small incision lenticule extraction method for treating myopia.39 Thus, the economic burden of myopia and solutions to better treatment have helped myopia become the most studied disease in the T100-Eye.

DR Was the Most Studied Eye Disease in T100-General

There are a few reasons to explain why DR was the most studied disease in the T100-General. First, population demographics in Asian countries are progressing toward one that favors rising prevalence of DR, more rapidly than most other countries.40 As such many Asian countries have not only conducted epidemiological studies but also made use of them as evidence to start treatment studies.40 For example, one T100-General article showed that Simvastatin slows the progression of DR in patients with hypercholesterolemia.41 Pharmacological intervention study continues to be part of the T100-General indicating that current studies are citing such study for current treatment methods for DR. Hence, due to the sharp rise in DR prevalence, some Asian eye studies have been focused on DR treatment.

A second reason is because Asia is producing more notable publications on DR focused on better screening methods to pick up DR earlier.42-44 This is important because studies show that early screening for DR reduces vision loss by >90%, and is highly cost-effective.40 Certain Asian countries have consequently began developing better methods to screen for DR, identifying early risk factors of DR. For example, better screening methods for DR such as the use of AI systems to analyze retinal images have been published extensively in the T100-General.42-44 One country in particular, Singapore, has been a key driver of T100 AI articles. The country has published 5 of the 9 T100-General AI articles on DR. Genetic risk factor studies have also informed doctors on which populations are more at risk of developing DR. One such example includes a study on gene polymorphisms in vascular endothelial growth factors (VEGF), showing that a common VEGF polymorphic gene (commonly found in cardiovascular and Graves’ disease) predisposes type 2 diabetic patients to DR.45 The study ranked 10th in the T100-General. Thus, risk factors and screening articles have helped DR top the list.

Glaucoma and AMD Were Second and Third Most Studied Diseases

Glaucoma is the leading cause of irreversible blindness in Asia46; as such it was expected that glaucoma was within the top 3. The current health cost of glaucoma is one of the highest among eye diseases, primarily because damage by glaucoma is irreversible, unlike other eye diseases where blindness is reversible.46 It is likely that a series of factors such as cost,4 prevalence,9 the need for detection at an early stage,45,46 and many other factors are responsible for glaucoma's popularity in the T100.

For AMD, the disease is a major cause of blindness for elderly in Asia.47 The Shihpai Eye Study in Taiwan studied elderly Chinese population aged 65 years and older and showed the prevalence of early AMD was 9.2% and of late AMD to be 1.9%.5 In the Beijing Eye Study in China, the prevalence of early and late AMD in Chinese persons 40 years and older was reported to be 1.4% and 0.2%, respectively.7 Population studies on AMD have been instrumental in updating the public on the prevalence of AMD. Diseases such as polypoidal choroidal vasculopathy have also contributed to the severity of AMD and represented a few T100 articles. Lastly, treatment for exudative AMD in Asian populations such as the use of intravitreal Bevacizumab for the management of choroidal neovascularization in AMD48 are also popular.

International Publication Patterns

Nature and Ophthalmology Published More Internationally

Among the top journals, Nature and Ophthalmology were the 2 journals that had published from a large pool of international Asian countries. Top journals like NEJM (75% of articles from Japan), BJO (60% of articles from Japan), JAMA (67% of articles from Singapore), and Lancet (100% of articles from Singapore) showed larger percentages of articles originating from Japan and Singapore, compared to Nature (Japan, 30%) and Ophthalmology (Japan, 41%). Current literature showed that BJO and NEJM were the journals that published more internationally based on a global study.49 However, as this study is limited to top articles from Asia, it may not represent publication patterns outside of the field of ophthalmology or Asia.

Authorship, Country of Origin, and Sex

Over-Representation of Articles From Japan and Singapore

A jarring trend that was observed was the large number of articles and authors originating from Japan and Singapore. One reason might be because the spending on research and development (R&D) is higher in Japan and Singapore compared to other Asian countries. Japan and Singapore spent approximately 3.2% and 2.2%, respectively, of its gross domestic product (GDP) on R&D (data.worldbank.org), compared to countries like India (0.6%) and Hong Kong (0.9%). Positive national policies have also influenced the way Japan conducts health care research.50 The higher prevalence of eye diseases such as age-related maculopathy in Japanese populations,51 and higher prevalence of myopia and angle-closure glaucoma in Chinese residing in Singapore,4 thus result in these countries more intensively studying such eye issues. The history of these countries also contributed to some T100 publications. For example, a few articles from Japan studied the relationship between cataract cases among atomic bomb survivors and ionizing radiation doses.52,53 Many articles from Singapore studied the effects of economic development on myopia.

Overall Underrepresentation of Female Authors in Asia

The under-representation of women constituting first and last authors was apparent in this study. In the T100-Eye, 82% of first- and 98% of last authors were male. Similarly, in the T100-General, 84% of first- and 96% of last authors were male. The narrative of underrepresentation of females in top-cited publications has been found in many studies. One study in 2019 found that 18% of first authors in Asia were female, which was lower than other parts of the world like Europe which had 40% of articles first-authored by female.54 Another study in 2014 found that male principal investigators (PIs) in ophthalmology had higher total grant funding awarded to them compared to female PIs after controlling for publication experience.55 Fortunately, this trend has been changing with a significant increase in female first authors in ophthalmology articles to date.56

Japan and Singapore Had Highest Number of Female First Authors

In terms of number of female first authors, Japan and Singapore were top. One reason for this is that both countries are among the more developed nations in Asia which likely led to better sex distributions in authorship. A study on sex equality found that there was an association, albeit weak, still positive association between sex equality and economic growth.57 Our findings suggest that sex equality is not solely a function of socioeconomic change, but one that has implications on scientific publications as well. Second, women achieve parity with men in terms of enrolment rates in education in both Singapore and Japan.58 This has allowed women to have equal opportunities as men to contribute to scientific research. Thus, as women and men are converging with respects to educational attainment and literacy rates, more Asian countries will likely have better sex distributions in ophthalmic publications.

Authors With ≥3 T100 Ophthalmology Publications

Among the authors that published ≥3 T100 publications, Wong TY (n = 22) and Tsubota K (n = 8) are among the top contributors as first- and last authors to the T100 (Table 3). Wong contributed to 10 as first and 10 as last author, whereas Tsubota K contributed to 3 as first and 5 as last author. A study in 2019 conducted on research productivity on ophthalmic subspecialties explained that authors who published more articles tended to conduct research in multiple ophthalmology subspecialties. In the case of our study, we found this to be true. For example, Wong TY published in various subspecialties such as glaucoma, DR, and myopia. As these subspecialties complement other fields in medicine such as public health, they also open the way for more collaboration, hence providing wider opportunities for research.59 Another reason is related to the higher academic productivity of individuals and institutions. Countries like Japan, Hong Kong, and Singapore are known for higher work productivity,58 thus explaining the dominance of these countries in nurturing top authors in Asia ophthalmology.

AI in Asia

AI Was the Most Recent Topic in the T100-General

The most recent study topic in the T100-General in Asia was on the use of AI to diagnose DR and glaucoma. Thirteen of the 14 articles on AI were published from 2008 to 2017. Current literature supports our findings that AI is an upcoming topic in ophthalmology. A previous study in 2020 on T100 in DR14 showed that the only article published after 2016 in the T100-DR list, was a study on AI to screen for DR in a multiethnic and multicountry study.42 The large number of articles and their recent publication dates indicate that AI is gaining prominence in Asian ophthalmology.

The growth of AI to screen for eye diseases such as DR and glaucoma in Asia are driven by a few countries. Of the 13 articles on AI, only 5 countries namely, Singapore (n = 8), Thailand (n = 2), India (n = 2), Pakistan (n = 1), and Japan (n = 1), have contributed. Certain countries have health care systems that make implementation of AI very intentional. For example, programmes such as the Singapore National DR Screening Program have helped the country published highly cited AI articles.42 In Thailand, Google's Thailand diabetes programme has also produced notable AI articles. It becomes evident that many of these countries were early adopters of AI and were able to seize competitive advantages and maintained them over time. This was done by improving AI infrastructure through better algorithms and expanding data ecosystems through eye screening programmes. Thus, AI's growing prominence in Asia is primarily driven by a small number of countries but will likely expand, which will explain its emerging popularity.

Emerging Trends in the T100 Ophthalmology in Asia

OCTA in Asia

A recent study topic in the T100-Eye focused on the use of OCTA to study eye diseases. In fact, the only 2 articles that were published after 2014 in the T100-Eye were studies on the use of OCTA on retinal capillaries. The first study ranked 65th was a clinical observational study of OCTA to evaluate clinical fundus features of DR.60 The second article ranked 66th was on the use of OCTA to study parapapillary retinal perfusion in glaucoma.61 Before the use of OCTA, fluorescein angiography (FA) was commonly used to evaluate vascular abnormalities. However, because FA uses intravenous dye injections, this makes it dangerous and invasive to patients.62 One reason OCTA studies are becoming popular might be that OCTA is a noninvasive technique, which makes it less dangerous. Another reason might be because it provides better resolution images that are 3-dimensional. Lastly, it is also much quicker than conventional methods.63 Although OCTA might not be able to entirely replace FA, it remains a promising imaging technique for prevalent eye diseases like DR and glaucoma, which justifies its recent popularity.

One example of an upcoming OCTA study from Asia is a recently published article in 2016 by Akagi et al in AJO.64 The article studied microvascular density of the peripapillary retina and optic disc in eyes with primary open-angle glaucoma (POAG) and visual field (VF) defects, and found that microvascular reduction was associated with VF defects in a regional-specific manner. This was the first study to look at such an association and has 105 citations to date.

Big Data and Bioinformatics Used in T100 Asia Ophthalmology Studies

An emerging field in ophthalmology in Asia is the use of big data in ophthalmology. Due to the rapid adoption of electronic health records (EHRs) in ophthalmology, large volumes of stored data such as records of patients’ eye diseases, vascular diseases, and many other commodities, are now being increasingly analyzed.65 One branch of big data in ophthalmology is on the use of AI to analyze large quantities of data.66 An example of this is a T100 article published in JAMA in 2017 by Ting et al.42 The study used a novel AI deep learning system to screen for DR and VTDR in 8 data sets involving multiethnicities and countries, ranked 25th in the T100-General, receiving >250 citations in 2 years.

Another branch of big data involves its use in genomics meta-analysis studies.67 In ophthalmology, genetic data of exomes collected from patients over the years are analyzed to identify specific genes associated to eye diseases. For example, a T100 article ranked 89th in the T100-General, published in Nature Genetics in 2014 by Hysi et al, used data from 35,296 multiethnic participants to show that certain intraocular pressure loci are associated with POAG.68 Given that there is an increase in digitalization of health care in Asia and the rest of the world,66 stored medical data will only become larger and more useful.

Differences Between T100 Asia and T100 Global in Ophthalmology

T100-Asia Had Lower Citations Than Global

Comparing our data to a previous study, the T100 ophthalmology in Asia had overall lower citations in both journals compared to T100 in ophthalmology globally (Eye/General in T100 Asia: median citations = 317/158 compared to T100 global = 803/473).69 As the United States represented majority (80%) of the T100 global articles, it is possible that United States's scientific influence has driven the large citation gap between the T100 Asia and T100 Global in ophthalmology. Compared to Asia, the United States has larger funding for research and a long history of highly regarded publications and authors as well.70 There is also evidence that authors from the United States tend to cite US authors over non-US ones.71

T100-Asia Published More Recently Than Global

Articles from T100 in Asia were published more recently compared to global T100. In the T100-Eye and T100-General in Asia, 73% and 82% of articles were published from the year 2000, in comparison to 43% and 61% for T100 global.69 This suggests that much of Asia's top-cited ophthalmology publications have only been published within the past 2 decades. Increased government funding for research and growing research institutions have been instrumental for this inflexion point in Asia's research scene.72

Types of Research in Asia Versus Globally

In Asia, there were higher percentages of clinical studies, epidemiology, and basic science studies, compared to global. It is not known precisely why this is so, perhaps the higher prevalence of certain eye diseases like myopia have attributed to this.25 Sociodemographic risk factors like education and other diseases also make Asia ideal for epidemiology inquiries,26 whereas R&D-driven countries like Japan help boost basic science research.16

Myopia Was Studied More in Asia

Myopia in T100 Asia (n = 24) was also studied more than globally (n = 3). The earlier section on myopia highlighted 3 core reasons for this, namely, higher prevalence, predisposing social demographic risk factors, and health care cost.

Sex

There were more male first- and last authors in T100 Asia (Eye: 82%, 98% and General: 84%, 96%) than T100 global (Eye: 84%, 78% and General: 73%, 81%). This indicates that sex bias is more prevalent in some Asian societies compared to other countries.

Publication in Both T100 Asia and Global

Lastly, only 4 articles namely, Yau et al. 2012,73 Wong et al. 2004,74 Awata et al. 2002,45 and Tsubota et al.1999,75 were in T100 Asia and T100 global. This suggests that globally only a small portion of current ophthalmology citation classics come from Asia.

LIMITATIONS

First, the search was restricted to Scopus which inevitably led to omissions of highly-cited articles in other databases not yet recognized by Scopus. However, Scopus has been shown to have a broader coverage of scientific publications compared to other databases. Second, citation classic analysis usually favors articles that are older in its publication date.76 Third, this study did not exclude self-citations as the process was too complex for all 200 articles. However, studies show that self-citations have a minor impact on bibliometric studies, making up < 5% of total citations.77,78 Fourth, the search was restricted to articles that were published in “English” this meant notable citation classics published in other major languages might have been overlooked.

To conclude, the analysis of the T100 in ophthalmology in Asia showed that highly cited articles in Asian ophthalmology tended to be clinical and epidemiological studies. Myopia, DR, glaucoma, and AMD were the most studied eye diseases currently. Concurrently, the use of AI, OCT, and big data to study glaucoma and DR prevalence were recent topics that have been highly cited.

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Keywords:

100 most cited; Asia; bibliometric analysis; ophthalmology; review

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