SPECIAL ARTICLE The 101 Most Frequently Cited Articles in Journals From 1850 to 1949

Norio Ohba, MD; Kumiko Nakao, MD

e screened 32 ophthalmology journals that had published articles during the period from 1850 through 1949 to identify top-cited articles in the field of ophthalmology (hereafter referred to as citation classics) using the online data- base Science Citation Index Expanded (Thompson Reuters, Chicago, Illinois). TheW 101 most frequently cited articles were published in 16 journals. Archives of Ophthalmology had the most top-cited articles (n=31), followed by American Journal of Ophthalmology (n=24) and Albrecht von Graefe’s Archiv für Ophthalmologie (n=9). These articles originated from 14 coun- tries, with the United States publishing the majority (n=58). Most of the citation classics are clini- cal studies on topics such as rubella , of prematurity, sicca, sympathetic ophthalmia, and the first report of eponymous diseases (eg, Leber hereditary , Duane retraction syndrome, and ). A considerable number of these articles were ignored initially and for several decades after publication, but, like the classic fairy tale Sleeping Beauty, they have been rediscovered. Our study provides a historical perspective on the classic papers in the literature that are still influential in ophthalmology. Arch Ophthalmol. 2010;128(12):1610-1617

The citation of published articles provides METHODS an indication of the relevance of the cited work to later literature. The number of ci- tations an article receives after its publica- In September 2009, we accessed the online da- tion reflects its influence on the scientific tabase Science Citation Index Expanded community. Analysis of the number of (Thompson Reuters, Chicago, Illinois),2 which times an article is cited may allow for the provides citation data for its source journals, and identification of a seminal advance in a spe- searched for articles that were published in oph- cialty and may provide a historical perspec- thalmology journals between 1850 and 1949, tive on the field’s scientific progress. Cita- using the Cited Reference Search option of the tion classics in a given specialty are defined database. In the query box for the year of pub- lication, we entered “1850-1949” to limit pub- as those articles that have been most fre- lication during the century. In the query box for quently cited in journals dedicated to the the journal source, we used a Boolean “OR” logic specialty and related fields. An earlier study search strategy with a set of suffix terms, in- identified and described citation classics in cluding ophth*, ophthal*, ophthalmol*, ophtal*, ophthalmology from 1975 to 2006.1 We re- oftal*, auge*, ocul*, ottal*, eye*, and physi- port herein an analysis of classic articles that ological optics. In this way, we identified 7316 were published in ophthalmology jour- articles that were published in a total of 32 oph- nals during the century from 1850 to 1949 thalmology journals between 1850 and 1949 and and have received the most frequent cita- that received at least 1 citation (Table 1). With tions up to the recent decades. the use of this search strategy, we retrieved data on the number of times each article was cited, the first author’s last name and first-name ini- Author Affiliations: Orthoptics and Visual Science, Faculty of Medical Welfare, tials, the abbreviated journal title, and the ar- Aichishukutoku University, Aichi (Dr Ohba), and Department of Ophthalmology, ticle publication year, volume, and first page Kagoshima University Graduate School of Medicine, Kagoshima-shi (Dr Nakao), number. Citation format errors in the retrieved Japan. information were not rare, and they included

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 thalmologie, British Journal of Oph- Table 1. List of Screened Ophthalmology Journals thalmology, and Transactions of the Ophthalmological Society of the United No. of Articles Cited Year of Kingdom. These journals also had a Publication 1 or More 50 or More larger number of articles that were Journal Title Screened Citations Citations cited 50 times or more (Table 1). The Annales d’Oculistique (Paris, France) 1838-1949 201 4 number of articles receiving at least Albrecht von Graefe’s Archiv für Ophthalmologiea 1854-1949 799 24 1 citation increased steadily from Royal London Ophthalmic Hospital Reports 1857-1917 61 2 1850 to 1948 (ie, from 82 articles in Klinische Monastsblätter für Augenheilkunde 1863-1949 892 11 the 1850s to 2070 articles in the Transactions of the American Ophthalmological Society 1864-1949 256 2 1940s). Archives of Ophthalmology and Otology (New York, NY) 1869-1878 13 0 Archiv für Augenheilkunde 1871-1937 242 4 With regard to number of times Berichite der Deutsch Ophthalmologischen Gesellschaft 1875-1922 79 2 cited, the top-cited article was the one 3 Centralblatt für praktische Augenheilkunde 1877-1919 62 0 by Gregg, whose first report of ru- Archives of Ophthalmology (New York, NY) 1879-1928 194 5 bella cataract was published in 1941 Archives d’Ophtalmologie (Paris, France) 1880-1949 201 2 in the Transactions of the Ophthalmo- Transactions of the Ophthalmological Society of the 1880-1949 442 15 logical Society of Australia and has United Kingdom Ophthalmic Review 1882-1916 43 1 since been cited 1160 times; this American Journal of Ophthalmology (second series) 1884-1917 47 0 number is greater than that of the top- Beiträge zur Augenheilkund (Hamburg, Germany) 1890-1915 15 0 cited article in the previous study Ophthalmic Record 1891-1917 46 0 from 1975 to 2006.1 As shown in Annals of Ophthalmology (Chicago, IL) 1892-1917 35 0 Table 2, the remaining 4 of the top Nippon Ganka Gakkai Zasshi (Tokyo, Japan) 1897-1849 73 2 5 articles cited are as follows: Oster- Zeitschrift für Augenheilkunde 1899-1938 250 3 berg4 in 1935 on the human retinal Ophthalmoscope 1903-1916 52 1 Transactions of American Academy of Ophthalmology 1903-1949 267 5 photoreceptor cell topography (cited 5 and Otolaryngology 417 times); Takayasu in 1908 (cited Ophthalmology 1904-1917 52 0 372 times), which was the first to de- British Journal of Ophthalmology 1917-1949 499 20 scribe Takayasu arteritis; Talbot and American Journal of Ophthalmology (third series) 1918-1949 1025 50 Marshall6 in 1941 on the neural Acta Ophthalmologica 1923-1949 218 11 mechanisms of visual localization and Klinica Oczna (Poland) 1923-1949 8 0 Archives of Ophthalmology (Chicago, IL) 1929-1949 1003 80 discrimination (cited 366 times); and 7 Vestnik Oftalmologii (Russia) 1937-1949 20 0 Michaelson and Campbell in 1948 Ophthalmologica 1938-1949 179 2 on the development of retinal vascu- Documenta Ophthalmologica 1938-1946 17 2 lar system (cited 365 times). With re- Transactions of the Ophthalmological Society of Australia 1939-1949 16 2 gard to citation rank, the article that British Journal of Physiological Optics 1940-1949 9 0 received 100 citations ranked 59th, Total 7316 250 the article that received 75 citations a Inclusive of Archiv für Ophthalmologie 1854-1870. ranked 121st, the article that re- ceived 50 citations ranked 241st, and the article that received 25 citations simple page number inversions, incor- RESULTS rect volume number but correct page ranked 734th. The top 101 were de- number and year, and partial misspell- fined as citation classics3-103 because ing of author’s last name, but we were gen- Table 1 provides a summary of the there were 4 joint positions at the erous in our citation tallies, including journal titles and publication years 98th rank with 80 citations. these relatively accurate citations as long that we screened. Of 32 journals, 19 Table 3 provides data on the jour- as there was only 1 minor error per cit- started publication in the second half nals in which the citation classics were ing string. of the 19th century, with the oldest published. The citation classics were The records were compiled in an Ex- cel spreadsheet (Microsoft 2003, Micro- one in 1838 (Annales d’Oculistique), published in 16 journals. Archives of soft, Redmond, Washington). The 101 and 13 started publication in the first Ophthalmology had the most top- most-cited articles were identified, and half of the 20th century. The articles cited articles (n=31), followed by their original texts were reviewed to char- were written in 6 different languages: American Journal of Ophthalmology acterize the article title, authors, affilia- English (n=20), German (n=7). (n=24), Albrecht von Graefe’s Archiv tion and country, journal source, publi- French (n=2), Japanese (n=1), Pol- für Ophthalmologie (n=9), British Jour- cation year, language, type of research ish (n=1), and Russian (n=1). nal of Ophthalmology (n=8), and Acta methodology, study topic, and ocular tis- We identified a total of 7316 ar- Ophthalmologica (n=7). Up to the mid sue studied. Furthermore, information ticles that have received at least 1 ci- 1910s, before the founding of British about the publications that cited each clas- tation. The number of articles cited Journal of Ophthalmology, American sic article was obtained to investigate the subject category of the articles that cited was led by American Journal of Oph- Journal of Ophthalmology (third se- the relevant classics and the year-by- thalmology (third series), followed by ries), and Acta Ophthalmologica, Eu- year citation history to define the rela- Archives of Ophthalmology, Klinische ropean journals (including Albrecht tionship between year since publication Monatsblätter für Augenheilkunde, Al- von Graefe’s Archiv für Ophthalmolo- and citations per year. brecht von Graefe’s Archiv für Oph- gie and Transactions of the Ophthal-

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Ocular Tissues Times Top-Cited Article Topic Studied Percentage of Subject Categories Cited Gregg3 Rubella cataract Pediatrics 67%; public, environmental, and occupational health 56% 1160 Osterberg4 Topography of visual cells Ophthalmology 53.2%; neuroscience 38.8% 417 Takayasu5 Takayasu arteritis Retina Medicine 25.5%; cardiac and cardiovascular systems 24.3% 372 Talbot and Marshall6 Visual acuity Visual function Neuroscience 61.6%; physiology 18.2% 366 Michaelson and Campbell7 Retinal vascular development Retina Ophthalmology 65.6% 365 Sjogren8 Keratoconjunctivitis sicca Medicine 27.9%; ophthalmology 19.9% 307 Terry9 Retinopathy of prematurity Retina Ophthalmology 46.0%; pediatrics 28.3% 299 Bourne et al10 pigmentosa (rat) Retina Ophthalmology 57.4%; neuroscience 19.3% 280 Stiles11 Color vision Visual function Neuroscience 49.3%; ophthalmology 44.1% 263 Holmes12 Disturbance of visual orientation Neuroscience 50.0%; clinical neurology 31.7% 261 Holmes13 Visual defect and cerebral lesions Optic nerve Neuroscience 45.0%; clinical neurology 32.8% 251 Friedenwald14 Tonometry Ophthalmology 88.1% 250 Schirmer15 Schirmer test Adnexa Ophthalmology 57.1% 227 Callender16 Uveal melanoma Ophthalmology 63.4%; oncology 14.7% 215 Cogan17 Nonsyphilitic interstitial Cornea Ophthalmology 20.1%; otolaryngology 19.6% 204 Franceschetti and Klein18 Franceschetti-Klein syndrome Adnexa Ophthalmology 21.9%; dentistry 15.7% 193 Davis19 anatomy (rabbit) Adnexa Ophthalmology 30.7%; neuroscience 24.1% 167 Warkany and Schraffenberger20 Vitamin A deficiency (rat) Eyeball Developmental biology 19.3%; nutrition 10.6% 162 Hale21 Vitamin A deficiency (pig) Eyeball Medicine 12.7%; nutrition 11.4% 156 Laurence and Moon22 Laurence-Bardet-Biedl syndrome Retina Ophthalmology 17.8%; medicine 17.1% 155 Owens and Owens23 Retinopathy of prematurity Retina Pediatrics 33.6%; ophthalmology 27.0%; medicine 16.5% 148 Usher24 Usher syndrome Retina Ophthalmology 26.5%; genetics and heredity 25.2% 148 Wald25 Photochemistry of vision Retina Ophthalmology 27.6%; physiology 22.8% 147 Heerfordt26 Uveoparotid fever Uvea Medicine 43.7%; ophthalmology 11.2% 144 Duane27 Duane syndrome Ocular muscles Ophthalmology 67.7%; clinical neurology 12.8% 143 Leber28 Leber hereditary optic Optic nerve Ophthalmology 33.8%; medicine 16.8% 142 neuropathy Karpe29 Clinical electroretinography Retina Ophthalmology 72.8% 140 Stargardt30 Stargardt disease Retina Ophthalmology 68.9%; genetics and heredity 14.0% 140 Ashton31 Retina Ophthalmology 43.6%; medicine 31.4% 137 Forrest32 Orbital tumors Adnexa Ophthalmology 72.1%; surgery 12.5% 137 von Hippel33 von Hippel–Lindau disease Retina Ophthalmology 29.2%; medicine 16.8% 136 Fincham34 Visual function Ophthalmology 79.0%; neuroscience 10.9% 135 Davis35 Optic nerve tumor Optic nerve Ophthalmology 50.4%; clinical neurology 26.5%; psychology 22.4% 134 Naffziger36 Adnexa Ophthalmology 28.2%; medicine 22.9% 130 Holmes37 Visual orientation Optic nerve Neuroscience 53.1%; clinical neurology 26.5%; 128 psychology (experimental) 22.4% Sorsbyetal38 Sorsby fundus dystrophy Retina Ophthalmology 67.9%; genetics and heredity 12.2% 126 Carpenter and Smyth39 Chemical burn of cornea (rabbit) Cornea Toxicology 55.2%; pharmacology 27.2% 124 Friedenwald40 Retinal vascular disease Retina Ophthalmology 54.5%; medicine 227% 123 Krause41 Krause syndrome Brain Ophthalmology 41.3%; medicine 20.7% 123 Smelser42 Exophthalmos Adnexa Endocrinology 24.4%; ophthalmology 22.8% 123 Martin43 Optic nerve glioma Optic nerve Ophthalmology 38.1%; clinical neurology 28.8% 122 Tay44 Tay-Sachs disease Retina Clinical neurology 18.6%; medicine 11.8% 118 Walls and Judd45 Color vision Visual function Ophthalmology 34.9%; neuroscience 27.9% 118 Callender et al46 Uveal melanoma Uvea Ophthalmology 68.4% 116 de Rötth47 Fetal membrane transplantation Ophthalmology 76.8% 116 Wagner48 Wagner syndrome Retina Ophthalmology 81.2% 116 Adamantiades49 Behc¸et-Adamantiades disease Uvea Medicine 23.2%; ophthalmology 19.6% 112 Coats50 Coats disease Retina Ophthalmology 78.8% 111 Grönblad51 Grönblad-Strandberg syndrome Retina Medicine 36.0%; ophthalmology 26.7% 111 Best52 Best disease Retina Ophthalmology 73.2%; genetics and heredity 21.4% 110 Leber53 Amaurosis congenita of Leber Retina Ophthalmology 64.5%; genetics and heredity 17.3% 110 Mandelbaum and Sloan54 Peripheral visual acuity Visual function Ophthalmology 48.5%; neuroscience 33.9% 110 Cogan55 Accommodation Visual function Ophthalmology 55.9%; psychology 27.3% 106 Ludvigh and McCarthy56 Ocular media light transmission Visual function Ophthalmology 31.3%; neuroscience 20.5% 106 Pfeiffer57 Traumatic enophthalmus Adnexa Surgery 58.3%; ophthalmology 27.1% 106 Verhoeff and Grossman58 Age-related macular Retina Ophthalmology 92.5% 104 degeneration Duane59 Accommodation Visual function Ophthalmology 70.9%; neuroscience 12.1% 100 van der Hoeve60 Phacomatosis Eyeball Ophthalmology 39.8%; clinical neurology 16.7% 100 Lindau61 Retinal angiomatosis Retina Ophthalmology 31.9%; medicine 17.5% 97 Rothmund62 Atopic cataract Lens Medicine 20.3%; dermatology 19.5% 97 Cogan63 Corneal neovascularization Cornea Ophthalmology 59.8%; pathology 18.6% 96 Collins64 Sympathetic ophthalmia Uvea Ophthalmology 57.4%; immunology 12.8% 96 Davis65 Optic nerve tumor Optic nerve Ophthalmology 50.4%; clinical neurology 18.0% 95 Craig and Gogela66 Orbital meningioma Adnexa Ophthalmology 36.2%; clinical neurology 34.8% 94 Edgerton67 Herpes zoster ophthalmicus Cornea Ophthalmology 71.2%; clinical neurology 13.9% 94 Knapp68 Cocaine anesthesia Cornea Ophthalmology 81.0%; surgery 23.2% 94 Walsh and King69 Intracranial aneurysm Brain Clinical neurology 44.8%; ophthalmology 33% 94 Wolff70 Anatomy of the lid Adnexa Ophthalmology 70.9% 94 Howard71 Judgment of distance Visual function Ophthalmology 46.2%; neuroscience 17.9% 93

(continued)

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Ocular Tissues Times Top-Cited Article Topic Studied Percentage of Subject Categories Cited Kinsey72 Ocular transmission of UV Visual function Ophthalmology 71.1% 93 Treacher Collins73 anomaly Adnexa Genetics and heredity 24.2%; dentistry, oral surgery, and medicine 93 21.2%; otorhinolaryngology 18.2%; surgery 18.2%; ophthalmology 15.2% Ferree et al74 Peripheral visual field Visual function Ophthalmology 70.2%; neuroscience 18.0% 92 Rados75 Marfan syndrome Lens Medicine 26.5%; ophthalmology 18.4% 92 Friedenwald76 Intraocular fluid Glaucoma Ophthalmology 59.8%; pharmacology and pharmacotherapy 11.9% 90 Magoun and Ranson77 Pupillary light reflex Visual function Neuroscience 56.0%; zoology 18.7% 90 Sugar and Barbour78 Pigmentary glaucoma Glaucoma Ophthalmology 95.5% 90 Adler79 Visual acuity Visual function Ophthalmology 40.4%; physics 12.3% 89 Cogan et al80 Hypercalcemic keratopathy Cornea Ophthalmology 61.1%; medicine 26.7% 89 Fuchs81 Heterochromic cyclitis Uvea Ophthalmology 98.9% 89 Koyanagi82 Vogt-Koyanagi-Harada syndrome Uvea Ophthalmology 60.7%; medicine 10.1% 89 Ogle83 Visual function Ophthalmology 60.5%; neuroscience 47.4% 89 Batten84 Batten-Mayou syndrome Retina Clinical neurology 32.6%; ophthalmology 15.6% 88 Norrie85 Norrie disease Retina Ophthalmology 51.1%; genetics and heredity 24.4% 88 Ascher86 Aqueous vein Glaucoma Ophthalmology 88.0% 87 Day et al87 Intraocular vitamin C Lens Nutrition 31.0%; ophthalmology 31% 87 Guerry and Kendig88 Impatency of nasolacrimal duct Adnexa Ophthalmology 62.4%; pediatrics 24.4% 85 Gundersen89 Herpetic keratitis Cornea Ophthalmology 80.5% 85 Kinsey90 Blood aqueous barrier Glaucoma Ophthalmology 78.9% 85 Vogt91 Vogt-Koyanagi-Harada syndrome Uvea Ophthalmology 60.7%; medicine 10.1% 85 Barkan92 Glaucoma Glaucoma Ophthalmology 90.7% 84 Owens93 Retinopathy of prematurity Retina Ophthalmology 40.0%; medicine 20.0%; obstetrics and gynecology 84 20.0%; pediatrics 20.0%; public, environmental, and occupational health 20.0% Cogan and Kinsey94 Ultraviolet keratitis Cornea Ophthalmology 62.4% 83 Cushing and Eisenhardt95 Chiasmal meningioma Brain Surgery 40.7%; clinical neurology 39.8% 83 Mandelbaum96 Dark adaptation Visual function Ophthalmology 77.8%; neurosciences 33.3%; clinical neurology 83 11.1%; multidisciplinary sciences 11.1% Swan97 Corneal permeability Cornea Ophthalmology 69.2%; pharmacology 21.9%; chemistry 12.3% 82 Weinberger98 Visual hallucination Brain Clinical neurology 38.0%; psychiatry 26.3% 82 Cogan and Kinsey99 Corneal physiology Cornea Ophthalmology 59.1%; public, environmental, and occupational 81 health 13.6% Bailliart100 Retinal arterial pressure Retina Ophthalmology 48.5%; clinical neurology 25.7% 80 Elschnig101 Sympathetic ophthalmia Uvea Ophthalmology 77.9% 80 Maummenee102 Lupus erythematosus Retina Ophthalmology 40%; medicine 32% 80 Rieger103 Rieger syndrome Uvea Ophthalmology 62.6%; genetics and heredity 11.1% 80

mological Society of the United King- Table 3. Journals in Which the Top-Cited Articles Were Published dom) contributed predominantly to From 1850 to 1949 the citation classics. Table 4 shows the countries of Articles, No. origin of the citation classics. More Journal 1850-1916 1917-1949 than half of the citation classics origi- Archives of Ophthalmologya 229nated in the United States, followed American Journal of Ophthalmology (third series) 0 24 by the United Kingdom, Germany, Albrecht von Graefe’s Archiv für Ophthalmologieb 81Sweden, and Switzerland. These ar- British Journal of Ophthalmology 08ticles were written in English (n=84), Acta Ophthalmologica 07German (n=14), French (n=2), and Transactions of the Ophthalmological Society of the United 33 Kingdom Japanese (n=1). Klinische Monatsblätter für Augenheilkund 12 Of the 101 citation classics, 77 Documenta Ophthalmologica 02were written by a single author, 18 Annales d’Oculistique 02by 2 authors, and 6 by 3 authors Royal London Ophthalmic Hospital Reports 20(Table 2). Ten authors contributed Zeitschrift für Augenheilkunde 20to 2 or more articles as the first au- Transactions of the American Academy of Ophthalmology 01 Transactions of American Ophthalmological Society 01thor. Cogan authored 6 ar- 17,55,63,80,94,99 19,35,65 Transactions of the Ophthalmological Society of Australia 01ticles, Davis, Frieden- 14,40,76 12,13,37 Nippon Ganka Gakkai Zasshi 10wald, and Holmes each Ophthalmic Review 10authored 3 articles, and Callen- Total 20 81 der,16,46 Duane,27,59 Kinsey,72,90 Leber,28,53 Mandelbaum,54,96 and W. a Of the 101 top-cited articles, 3 were published in Archives of Ophthalmology (New York, 1879-1928) C. Owens23,93 each authored 2 ar- and 28 were published in Archives of Ophthalmology (Chicago, 1929-1949). We treated the 2 journals as 1 journal and arbitrarily divided the years of publication into 1850-1916 and 1917-1949. ticles (Table 2). None of the cita- b Inclusive of Archiv für Ophthalmologie. tion classics were the product of a

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 mentary glaucoma,78 aqueous veins,86 ten’s case reports of cerebral degen- Table 4. Country of Origin herpetic keratitis,89 and gonios- eration with macular changes,84 of Citation Classics in copy.92 The remaining 28 articles were Bailliart’s assessment of retinal ar- Ophthalmology From 1850 to 1949 cited most frequently in other medi- tery blood pressure,100 and Elsch- cal journals besides ophthalmology, nig’s work on sympathetic ophthal- Top-Cited 101 Country Articles, No. including clinical neurology or neu- mia. A type 3 life-cycle curve means roscience (n=10), general medicine that an article takes several decades United States 58 United Kingdom 16 (n=8), pediatrics (n=2), and sur- after publication to get started in the Germany 7 gery (n=2). Fifteen articles* have citation history, followed by a marked Sweden 5 received citations primarily in speci- increase in the latest decades (Figure, Switzerland 3 ality journals other than ophthalmol- I-N); the type 3 life-cycle curve is Austria 2 ogy. For instance, the article by Gregg3 identified in 30 articles. It is remark- Denmark 2 on rubella cataract has received the able that 15 of the 30 articles with the Japan 2 Australia 1 most citations in pediatrics, public type 3 life-cycle curve were pub- Czechoslovakia 1 health, environmental health, occu- lished before 1920, including Le- France 1 pational health, and obstetrics jour- ber’s description of hereditary optic Greece 1 nals; the 2 articles by Holmes12,13 on neuropathy,53 Treacher Collins’ de- Netherlands 1 the visual disturbances due to perfo- scription of eyelid anomaly,73 Schir- Poland 1 rating gunshot head injuries have re- mer’s study of tear production and se- Total 101 ceived many citations in neuro- cretion,15 von Hippel’s description of science, clinical neurology, and retinal angioma,33 Tay’s description behavioral science journals; the ar- of familial infantile idiocy,44 Duane’s multi-institutional or international ticle by Warkany and Schraffen- retraction syndrome,27 de Rötth’s in- collaboration. berger20 on the experimental ocular troduction of amniotic membrane The specialty categories of the 101 malformations due to maternal vita- transplantation for conjunctival re- citation classics (Table 2) were min A deficiency has received most pair,47 and Sorsby et al’s description anatomy/physiology/biochemistry citations in articles concerning devel- of fundus dystrophy characterized by (n=25), / opmental biology, nutrition, and gen- late-onset progressive macular de- genetic ophthalmology (n=25), pa- eral medicine; and the article by Tay44 generation.38 The type 4 life-cycle thology/microbiology/pharmacol- on the cherry red spot in the macula curve has a nearly constant citation ogy (n=14), general medical and has been cited primarily in journals rate from publication up to the pres- surgical ophthalmology (n=14), dedicated to clinical neurology, medi- ent, and this type was identified in 10 neuro-ophthalmology (n=10), ocu- cine, and pediatrics. articles (Figure, O); the type 4 life- lar oncology (n=7), and systemic The Science Citation Index Ex- cycle curve is seen in Takayasu’s case ophthalmology (n=6). Seventy-one panded online database provided the report5 of unique retinal vascular dis- citation classics were observational data on the annual citations that each ease called Takayasu retinitis, and studies of new clinical disease, diag- article has received since publica- Heerfordt’s uveoparotid fever.26 The nostic and therapeutic innovations, or tion. Analysis of 10-year cumulative type 5 life-cycle curve has marked ci- histopathologic studies. Thirty articles citation data revealed that the rela- tations in the early decades after pub- reported results of basic research, of tionship between the decade since lication, followed by a trough of few which 22 were on the physiological publication and citations per decade or no citations, which is followed by optics or visual psychophysics in hu- is fitted by 1 of 5 types of life-cycle a revival in citations (Figure, P); this mans and 8 were on the ocular curve (Figure). Type 1 is character- type was identified in 7 articles, in- anatomy and physiology in animals. ized by a rapid increase in citations cluding reports of retinopathy of pre- The main topics included studies on to a peak in the first or second de- maturity by Terry9 and Owens and retina, , and vitreous tissue cade after publication, followed by a Owens,23 and Lindau’s description of (n=28), visual function (n=15), ocu- decrease in citations in the subse- a syndrome characterized by angio- lar adnexa (n=11), the cornea quent decades (Figure, A-E), and this matosis of the retina and hemangio- (n=11), the uvea (n=10), and the op- type was identified in 17 citation clas- blastoma of the cerebellum.61 tic nerve (n=7). sics. Type 2 is characterized by a The subject categories of journals gradual increase in citations to a peak that cited the citation classics ranged in the 3 or more decades after pub- COMMENT from ophthalmology to many other lication, followed by a gradual de- specialties (Table 2). Of the 101 ci- crease in citations in the subsequent These citation classics provide a his- tation classics, 74 were cited most by decades, revealing an inverted u- torical perspective of the progress in articles in ophthalmology journals; shape relationship (Figure, F-H); the ophthalmology from 1850 to 1949. It these articles with predominant cita- type 2 life-cycle curve was identified is remarkable that the majority of these tions by ophthalmology journals dealt in 36 articles, 11 of which were pub- old articles are still cited and con- with a diverse range of clinical top- lished before 1930, including Bat- tinue to have an influence in the field ics, such as tonometry,14 age-related of ophthalmology. Clinical observa- ,58 use of co- *References 3, 5, 6, 12, 13, 20, 21, 37, 39, tions were predominant with case re- caine in ophthalmic surgery,68 pig- 44, 62, 73, 75, 93, 98. ports of new disease, innovations of

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 A Day et al 193187 B Krause 194641 C Cogan and Kinsey 194299 30 60 40 30 20 40 20 10 20 10 0 0 0

D Friedenwald 194976 E Smelser 193742 F Gregg 19413 60 40 300

40 200 20 20 100

0 0 0

G Bailliart 1917100 H Bourne et al 193810 I Leber 187128 30 80 40

20 40 20 10

0 0 0

J Treacher Collins 193373 K Best 190552 L Duane 190527 10-year Cumulative Citation Scores 10-year Cumulative Citation Scores 10-year Cumulative Citation Scores 30 30 40

20 20 20 10 10

0 0 0

M Stargardt 190930 N de Rötth 194047 O Takayasu 19085 60 100 100

40 50 50 20

0 0 0

1908 1918 1928 1938 1948 1958 1968 1978 1988 1998 2008 1908 1918 1928 1938 1948 1958 1968 1978 1988 1998 2008 P Terry 19429 80

40

0

1908 1918 1928 1938 1948 1958 1968 1978 1988 1998 2008

Figure. Different types of life cycles with regard to citation history of top-cited articles in ophthalmology. The abscissa (x axis) shows the years by decade, and the ordinate (y axis) shows the number of times that an article was cited for 10-year cumulative data. The open circles illustrate the year of publication of the cited article with the reference number. A-E, Type 1 life cycle. F-H, Type 2 life cycle. I-N, Type 3 life cycle. O, Type 4 life cycle. P, Type 5 life cycle.

visual functional examinations, and described a genetic disease, such as fined epidemiology, molecular biol- improvement of medical and surgi- Usher syndrome,24 Stargardt dis- ogy, immunology, laser technology, cal management of ophthalmic dis- ease,30 and Leber hereditary optic neu- intraocular lens implantation, vitreo- ease. Basic studies consisted of clas- ropathy,28 were a remarkably high retinal surgery, randomized con- sical physiology, biochemistry, and proportion of the citation classics, trolled trial–based research, and trans- pharmacology as well as light micro- which may be attributed to the de- lational research. Concerning scopic anatomy and histopathology. velopment of molecular genetics in the authorship, 77 of the 101 current ci- Notably, simple methodologies have 1990s and 2000s. tation classics were by a single au- made a profound impact on a wide A comparison of the current cita- thor, whereas 14 of the 100 articles range of clinical topics, including ru- tion classics with the previously in the modern citation classics1 were bella cataract,3 keratoconjunctivitis reported citation classics in ophthal- product of multicenter studies with sicca,8 retinopathy of prematu- mology from 1975 to 20061 demon- as many as 50 or more authors, and rity,9,23,93 visual disturbances associ- strates that there was a shift of the the remaining 86 articles were by a ated with cerebral damage,12,13,37 dia- main contribution from European mean of 3 authors. The changing betic retinopathy,31 senile disciform countries to the United States and trend in authorship may be attrib- macular degeneration,58 and pigmen- points to the outstanding progress in uted to the advancement of technolo- tary glaucoma.78 The articles that first research technologies, including re- gies that have necessitated the col-

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 laboration of researchers of different ria of the current citation classics. Fur- 11. Stiles WS. Increment thresholds and the mecha- nisms of colour vision. Doc Ophthalmol. 1949; background. thermore, herein, we have been 3:138-165. The precise tempo of the aging concerned only with articles in oph- 12. Holmes G. Disturbances of visual orientation. Br process of the citation history of pub- thalmology journals. It is likely that J Ophthalmol. 1918;2(9):449-468. 13. Holmes G. Disturbances of vision caused by ce- lication may vary with the category we have overlooked influential ar- rebral lesions. Br J Ophthalmol. 1918;2(7): of journals and the study topic. ticles that were published in other 353-384. Among the 5 types of citation life medical journals and received fre- 14. Friedenwald JS. Contribution to the theory and practice of tonometry. Am J Ophthalmol. 1937; cycles that we identified herein, the quent citations (eg, Behc¸et’s 1937 20:985-1024. type 3, characterized by many de- article on Behc¸et disease that was pub- 15. Schirmer O. Studien zur physiologie und patholo- gie der Tränenabsonderung und Tränenabfuhr. Al- cades’ latency after publication fol- lished in Dermatologische Wochen- brecht von Graef Arch Ophthalmol. 1903;56: 112 lowed by marked citations in recent schrift and has received more than 197-291. years, provides an intriguing story 850 citations in a wide range of spe- 16. Callender GR. Malignant melanotic tumors of the eye: a study of histologic types in all cases. Trans that reminds us of the classic fairy tale cialty journals). Despite these limi- Am Acad Ophthalmol Otolaryngol. 1931;36: Sleeping Beauty: an article that goes tations, the current citation classics 131-142. unnoticed (sleeps) for a long time and provide a historical perspective of the 17. Cogan DG. Syndrome of nonsyphilitic intersti- tial keratitis and vestibuloauditory symptoms. then, almost suddenly, attracts a lot scientific advances of ophthalmol- Arch Ophthalmol. 1945;33(3):144-149. of attention (is awaked by a prince). ogy from 1850 to 1949 that are still 18. Franceschetti A, Klein D. The mandibulofacial dys- ostosis; a new hereditary syndrome. Acta Oph- A representative instance is the re- influential in the 21st century, and thalmol (Copenh). 1949;27(2):143-224. port in 1940 of amniotic membrane they offer researchers hints about how 19. Davis FA. The anatomy and histology of the eye transplantation for ocular surface dis- to produce an article that can be cited and orbit of the rabbit. Trans Am Ophthalmol Soc. 47 1929;27:401-441. orders by de Rötth, which was frequently over several decades. 20. Warkany J, Schraffenberger E. Congenital malfor- barely recognized until the late 1990s mations induced in rats by maternal vitamin A de- (Figure). It is notable that related ar- ficiency, 1: defects of the eye. Arch Ophthalmol. Submitted for Publication: Octo- 1946;35:150-169. ticles by contemporaries Sorsby et ber 21, 2009; final revision re- 21. Hale F. The relation of vitamin A to anophthalmos al104 and Lavery105 had a similar ci- ceived February 14, 2010; ac- in pigs. Am J Ophthalmol. 1935;18:1087-1092. 22. Laurence JZ, Moon RC. Four cases of “retinitis pig- tation life cycle, although with fewer cepted February 16, 2010. mentosa” occurring in the same family and ac- citations. To the best of our knowl- Correspondence: Norio Ohba, MD, companied by general imperfections of edge, this is the first paper to use the Orthoptics and Visual Science, Fac- development. Ophthalmic Rev. 1866;2:32-41. 23. Owens WC, Owens EU. Retrolental fibroplasia in metaphor of Sleeping Beauty to ana- ulty of Medical Welfare, Aichishuku- premature infants; studies on the prophylaxis of lyze citation patterns in the medi- toku University, Asahigaoka 109-3, the disease; the use of alpha tocopheryl acetate. cal literature. The sleeping beauties Am J Ophthalmol. 1949;32(12):1631-1637. Minami-sakaemachi Owariasahi- 24. Usher CH. On the inheritance of retinitis pigmen- are not just an exotic whim in phys- shi, Aichi 488-0046, Japan. tosa, with notes of cases. Roy Lond Ophthal- ics and psychology.106,107 Financial Disclosure: None reported. mol Hosp Rep. 1914;19:130-236. 25. Wald G. The photochemistry of vision. Doc There are limitations in the cur- Ophthalmol. 1949;3:94-137. rent citation classics. The online da- REFERENCES 26. Heerfordt CF. 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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 and a review of the literature. Arch Ophthalmol. einer eigentümlichen Hautdegeneration. Archiv 89. Gundersen T. Herpes corneae with special refer- 1940;23(5):957-1022. Ophthalmologie (Berlin). 1868;14:159-182. ence to its treatment with strong solution of iodine. 36. Naffziger HC. Pathologic changes in the orbit in 63. Cogan DG. Vascularization of the cornea: its ex- Arch Ophthalmol. 1936;15(2):225-249. progressive exophthalmos. Arch Ophthalmol. perimental induction by small lesions and a new 90. Kinsey VE. Transfer of ascorbic acid and re- 1933;9:1-12. theory of its pathogenesis. Arch Ophthal. 1949; lated compounds across the blood-aqueous 37. Holmes G. Disturbances of visual orientation. Br 41(4):406-416. barrier. Am J Ophthalmol. 1947;30(10):1262- J Ophthalmol. 1918;2(10):506-516. 64. Collins RC. Experimental studies on sympathetic 1266. 38. Sorsby A, Mason MEJ, Gardener N. A fundus dys- ophthalmia. Am J Ophthalmol. 1949;32(12): 91. Vogt A. Frühzeitiges Ergrauen der Zilien und Be- trophy with unusual features. Br J Ophthalmol. 1687-1699, illust. merkungen über den sogennanten plötzlichen 1949;33(2):67-97. 65. Davis FA. Primary tumors of the optic nerve (a phe- Eintritt dieser Veränderung. Klin Monatsbl 39. Carpenter CP, Smyth HF Jr. Chemical burns of the nomenon of Recklinghausen’s disease): a clini- Augenheilkd. 1906;44:228-242. rabbit cornea. Am J Ophthalmol. 1946;29(11): cal and pathologic study with a report of five cases 92. Barkan O. Glaucoma: classification, causes, and 1363-1372. and a review of the literature. Arch Ophthalmol. surgical control: results of microgonioscopic 1940;23:735-821. 40. Friedenwald JS. A new approach to some prob- research. Am J Ophthalmol. 1938;21:1099- 66. Craig WM, Gogela LJ. Intraorbital meningio- lems of retinal vascular disease. Am J Ophthalmol. 1117. mas: a clinicopathologic study. Am J Ophthalmol. 1949;32(4):487-498. 93. Owens WC, Owens EU. Retrolental fibroplasia in 1949;32(12):1663-1680, illust. 41. Krause AC. Congenital encephalo-ophthalmic premature infants. Am J Ophthalmol. 1949; dysplasia. Arch Ophthalmol. 1946;36:387- 67. Edgerton AE. Herpes zoster ophthalmicus: report of cases and review of literature. Arch Ophthalmol. 32(1):1-21. 444. 94. Cogan DG, Kinsey VE. Action spectrum of kera- 42. Smelser GK. A comparative study of experimen- 1945;34(2):114-153. 68. Knapp H. On cocaine and its use in ophthalmic titis produced by ultraviolet radiation. Arch tal and clinical exophthalmos. Am J Ophthalmol. and general surgery. Arch Ophthalmol. 1884; Ophthalmol. 1946;35(6):670-677. 1937;20:1189-1203. 13:402-448. 95. Cushing H, Eisenhardt L. Meningiomas arising from 43. Martin P. Primary gliomas of the chiasm and op- 69. Walsh FB, King AB. Ocular signs of intracranial the tuberculum sellae: with the syndrome of pri- tic nerves in their intracranial portion. Arch Oph- saccular aneurysms: experimental work on col- mary optic atrophy and bitemporal field defects thalmol. 1923;52:209-241. lateral circulation through the ophthalmic artery. combined with a normal sella turcica in a middle- 44. Tay W. Symmetrical changes in the region of the Arch Ophthalmol. 1942;27(1):1-33. aged person. Arch Ophthalmol. 1929;1:1-41. yellow spot in each eye of an infant. Trans Oph- 70. Wolff E. The muco-cutaneous junction of the lid- 96. Mandelbaum J. Dark adaptation: some physi- thalmol Soc U K. 1881;1:55-57. margin and the distribution of the tear fluid. Trans ologic and clinical considerations. Am J Ophthalmol. 45. Walls GL, Judd HD. The intra-ocular colour filters Ophthalmol Soc U K. 1946;66:291-308. 1941;26(2):203-239. of vertebrates. Br J Ophthalmol. 1933;17(11): 71. Howard HJ. A test for the judgment of distance. 97. Swan KC. Corneal permeability, I: factors affect- 641-675. Am J Ophthalmol. 1919;2:656-675. ing penetration of drugs into the cornea. 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