Milestones, Rivalries and Controversy:
The Origins of Photography and Ophthalmic Photography
Part III, The First Human Fundus Photograph
From the earliest days of photography, several investigators sought to use the camera to document the condition of the eye. Due to the technical limitations of available photosensitive materials and the difficulty in illuminating the interior of the eye, fundus photography became the holy grail of medical imaging.
In the decades immediately following the introduction of photography in 1839, there were incremental advances toward the elusive goal of photographing the ocular fundus. In 1851, Helmholtz introduced the ophthalmoscope. That same year, Frederick Scott Archer described the collodion photographic process, a significant improvement over the calotype and daguerrotype. A decade later, Clerk-Maxwell demonstrated a color photography method in 1861.
In the early 1860’s Henry Noyes of New York, and A.M. Rosebrugh of Toronto, both constructed fundus cameras and attempted fundus photography on animals. Although this news was encouraging, Hermann Helmholtz was skeptical and commented on Rosebrugh’s technique in the correspondence column of The Ophthalmic Review, “I must confess I cannot yet believe that it (photographing the fundus oculi) will succeed in the human subject; the chief difficulty is evidently the use of sufficiently powerful sun-light, which would only be admissible with a completely blind eye.”
He was right. Early results were severely compromised by insufficient light, long exposures, eye movement, and prominent corneal reflexes that obscured detail. Spectral sensitivity of available photographic emulsions had very little red sensitivity, adding to the difficulty of adequate exposure. It would be several decades before these problems could be conquered. Even as advances were made, results were often disappointing. Lucien Howe, one of the early pioneers in fundus photography stated in 1894, “It is so easy, in theory, to photograph the interior of the eye, that it has undoubtedly been attempted many times. It is so difficult, however, in fact to accomplish this, that no satisfactory results have been obtained, in spite of the great value of this method of recording observations if it could be brought to perfection.”
The First Human Fundus Photograph
When it comes to the first successful human fundus photo, different historical accounts assign priority to different investigators. Lucien Howe, Jackman & Webster, and E Barr have all been mentioned in texts and historical reviews as being the first to photograph the fundus of a living human being. Most accounts list Jackman and Webster since they published their technique along with a reproduction of a fundus image in two photography periodicals in 1886:
Photographing the Eye of the Living Human Retina.
Photographic News, England May 7, 1886
Jackman T, Webster JD
On Photographing the Eye of the Living Human Retina.
Philadelphia Photographer, June 5, 1886
Jackman T, Webster JD
The article from the June 1886 Philadelphia Photographer described a 2 ½ minute exposure resulting in an image with a prominent corneal reflex, but a faintly visible optic disc. The Philadelphia Photographer at that time was sparsely illustrated, mostly with line drawings, along with a few low quality engravings and woodblock prints. Photogravure was too expensive a process for a periodical like this and halftone reproduction had not yet been widely adopted (First use was in 1880). The reproduction of the fundus photograph in the Philadelphia Photographer was an engraving which only simulated the original photograph. There is no doubt however that Jackman and Webster were the first to publish a fundus “image” of a living human subject.
Howe, Starr, and “Barr”
Three other names played a prominent role in early fundus photography. According to some historical accounts, Elmer Barr and Lucien Howe may have been first to photograph the human retina. In the Textbook of Ophthalmic Photography, Don Wong stated, “In the following year, 1887, E. Barr of Buffalo, N.Y., also obtained results… During that same time, still a third physician, Dr. Lucien Howe of N.Y. claimed to have made the first photographs of the human fundus. This was reported at the American Ophthalmological Society in 1887.”
A literature search for these authors turned up two articles with similar sounding titles. I was able to access them online and interestingly they are both from researchers in Buffalo NY and were released the same month.
Photography of the Interior of the Eye.
Trans Amer Ophth Soc. 23:568-71 July 1887
Lucien Howe, MD of Buffalo, N.Y.
On Photographing the Interior of the Human Eyeball
Amer J Ophth 4:181-3 July, 1887
Elmer Barr, MD of Buffalo, N.Y
Howe’s 1887 report to the American Ophthalmological Society credited the work as that of his assistant, “Dr Elmer Starr of Buffalo, N.Y.”, while the name on the American Journal of Ophthalmology article was Elmer Barr. What’s the likelihood that there was an Elmer Barr and Elmer Starr, both of Buffalo, working independently to photograph the living human retina? An odd coincidence? Starr’s name didn’t turn up in a traditional literature search of the medical journals. I was convinced that either the name Barr or Starr had to be a typographical error. Since corrections aren’t indexed in journal search databases, it was a challenge to turn up any evidence of a typographic error using a search engine, but during a manual search of the next issue of the AJO, I was able to turn up this correction:
“The name of the author of the paper on ‘Photographing the Interior of the Human Eyeball,’ published in our last number is not, as printed, Dr. E Barr, but Dr. Elmer Starr. Am. J. Ophthalmol. 4:240, 1887.”
Sure enough, it really was Elmer Starr, not Elmer Barr! I was also able to find another correction for an article in the Scientific American of the following year that had also been mislabeled as Elmer Barr: “In our Supplement 650, June 16, 1888, we published a paper on the Photography of the Human Eye, in which, by a typographical error, the author’s name appeared as Barr, Instead of Starr. The paper was written by Dr. Elmer Starr, of Buffalo, N.Y”.
After finding the corrections of Barr/Starr, a further search of the science and photography periodicals from the late 1800’s turned up another paper by Elmer Starr: “Photographing the human eye.” in the Philadelphia Photographer 1887. It was essentially the same content and technique as the Howe and Barr papers. Indeed they all came from the same lab and described the same image. At least the Philadelphia Photographer got Starr’s name right! An early historical review from the turn of the century misspelled Starr’s first name as Elemer multiple times, while another review mentioned the work of “Lowe in 1887” (they were referring to Howe).
Lucien Howe is a well-known name in ophthalmology. Howe was educated in the United States and abroad, having spent time studying and conducting research with Lister in Edinburgh, von Helmholtz in Heidelberg and others, before returning to the United States and establishing the Buffalo Eye and Ear Infirmary. He was a Professor of Ophthalmology at the University of Buffalo, served as President of the American Ophthalmological Society, established the Howe Laboratory of Ophthalmology at Harvard University, and has had several prestigious awards and medals established in his name.
Starr was one of Howe’s assistants and they collaborated on the fundus photography project in 1886-88. Howe described their results as the first “recognizable” fundus photograph, apparently a nod to Jackman & Webster being the first to “publish” a fundus photograph. Based on the written accounts, Howe and Starr’s image was more “recognizable” as a fundus, but it’s difficult to tell from the published illustrations which were woodcut reproductions. Interestingly, Howe’s account was delivered as a third-person report, while both the “Barr” and Starr papers are written in the first person. All of this suggests that Starr was the principle investigator and actually took the photographs. I haven’t been able to find a single historical account that credits Starr as being among the first to obtain a recognizable photograph of the living human retina. Starr seems to have missed his place in history simply because of a typo.
Another “publication” that has been included in historical reference lists is: “Barr E. Dr.s Jackman & Webster. Philadelphia Photographer. June 5, 1986.” As listed, it appears as if the (non-existent) Barr might have written an article describing Jackman and Webster’s results. No such reference turned up in a literature search and as we now know, “Barr” was really Starr. After a thorough search, I believe the reference doesn’t exist at all. It appears to be a fragment of text from the Barr article (Barr E. On photographing the interior of the human eyeball. Amer J Ophth 1887; 4:181-183), where he mentions publication of the Jackman and Webster photograph in his introduction. My guess is the listing was a historian’s note-to-self to search for the Jackman & Webster reference after seeing it mentioned in Barr. Unfortunately this phantom reference was repeated by at least one additional author in a historical review, which only served to perpetuate the “Barr” mistake.
After publication in 1887, Howe didn’t pursue fundus photography any further, but did present on the topic to the Ophthalmological Society of the UK in 1893. It was essentially a repeat of the same material he presented six years earlier. He was no longer investigating fundus photography but hoped to “incite others to do better work…” In reviewing the limited progress to date, he listed Rosebrugh, Fick, and Gerloff as “the only three other attempts which as far as I can ascertain, have thus far been published.” He conspicuously left out any mention of Jackman and Webster, which is curious because all of the previous Howe/Barr/Starr papers referred to the published Jackman and Webster photograph. Was this omission a mistake or done on purpose? He again thanked Starr for his assistance, but fell short of thoroughly crediting him as he had in the past. In an 1895 address to the American Otological Society Howe reported on his attempts to photograph the eardrum. In it, he again took credit for having “showed the first photographs made of the human fundus oculi.” It seems as if Howe asserted a claim of priority for being the first to photograph the living human fundus and chose to ignore the prior work of Jackman and Webster.
Howe was later embroiled in a different priority dispute with George T. Stevens during meetings of the AOS in 1909-1910. He publicly challenged Stevens’ design for a tropometer, claiming it was based on a previous design by Nicati in 1876. Howe did his best to prove his point, “It occurred to me that some question might arise concerning this point of priority, and therefore I brought in the references.”
Howe and Stevens had previously authored competing books on ocular motility and the dispute may have arisen from this separate rivalry. In a final observation in his priority debate with Stevens, Howe stated, “it has occurred to us all probably, to think we have some new idea and afterward that we discover that it is old.” Howe’s conclusion could easily apply to several of the priority disputes in this historical review.
Thorner vs. Dimmer
By the turn of the century there were improvements in both film and instrumentation that significantly improved photographic results. Bagneris, Guilloz, Gerloff, Wolff, Thorner, and Dimmer all made improvements in photographing the fundus oculi around this time. Tactics such as water bath immersion, corneal cover plates, and polarized light were used to reduce unwanted corneal reflexes but these techniques were ultimately deemed impractical.
In 1898 Walter Thorner of Berlin designed the first reflex-free ophthalmoscope based on the simple principle of transmitting the illuminating beam through one half of the dilated pupil and viewing the light reflected through the other half. The following year Friedrich Dimmer of Vienna showed reflex-free photographs at the Ninth International Congress of Ophthalmology that caused quite a stir, and another rivalry was born.
Dimmer continued to refine his technique and collaborated with Zeiss Jena to design and build a complex reflex-free fundus camera. It was so large and expensive that only one was ever built by Zeiss.
Thorner used a camera of his own design, but his images were smaller, had a limited field of view, and were unevenly illuminated compared with Dimmer’s.
A report from the Tenth International Congress of Ophthalmology in The Ophthalmoscope from 1904 compared their images, “Professor Dimmer, of Gratz, showed twenty beautiful photographs of the fundus oculi, normal and abnormal. The photographs were so good as to allow one to recognize, literally at a glance, the conditions they depicted. The apparatus by which these extraordinary photographs were taken was also on view. It is, unfortunately, almost as big as a grand piano, and is stated to be correspondingly expensive. Dr. Walter Thorner, of Berlin, also showed photographs of the fundus oculi, but for beauty and detail they could not be compared with those of Professor Dimmer.”
Dimmer’s instrument incorporated the principles introduced by Thorner, but Thorner was skeptical of the Dimmer’s results and accused him of retouching the photographs to remove the central corneal reflex. This resulted in another bitter feud that lasted several years.
Keeler and co-authors recently summarized the rivalry, “By 1908 Dimmer had produced exceptional black and white images which were published in an atlas. Thorner was so impressed that he wrongly accused Dimmer, of “touching up” the results. Thorner however took comfort in the knowledge that only one instrument, the size of a small car, could take these photographs and the instrument could not be commercialised.”
Thorner later designed a stereoscopic camera and published the first stereo fundus photographs in 1909. Dimmer went on to publish an atlas of retinal images with Pillat in 1927 that is considered an important landmark in retinal imaging.
Milestones, Rivalries and Controversy
From that point on there were several milestones in the evolution of both photography and ophthalmic photography, but they are decidedly less controversial that the ones chosen for this series. It seems that the most important milestones in photography, fundus photography and stereo imaging occurred during the Victorian Era’s great enthusiasm for science and invention. Several of the principles were competitive, bitter men, who craved recognition for their contributions and a place in history.
History has certainly smiled on some of them and been unkind to others.
“The camera exists because men were intrigued by the function of the eye and wished to be able to reproduce on a permanent record that which the eye enabled the brain to record. How appropriate then that ophthalmology has turned the camera into a valuable tool for recording the structures of the eye.”
Evolution of Ophthalmic Photography. International Ophthalmology Clinics. 1976; 16(2):1-22
Wong D. Textbook of Ophthalmic Photography. Inter-Optics Publications, New York, 1982
Meyer-Schwickerath, G. Ophthalmology and photography. Am J. Ophthalmol 1968; 66:1011
Hurtes R. Evolution of ophthalmic photography. International Ophthalmology Clinics. 1976; 16(2):1-22
Bedell AJ. 1935. Stereoscopic fundus photography. JAMA 105:1502-1505.
Van Cader, TC. History of ophthalmic photography. J Ophthalmic Photography 1978; 1:7-9
Saine PJ. Landmarks in the development of fluorescein angiography. JOP 1993; 15:17
Rosebrugh AM. A new ophthalmoscope for photographing the fundus oculi. Canada Medical Journal and Monthly Record of Medical and Surgical Science. Vol 1, 1865; 163-169.
Rosebrugh AM. On a new ophthalmoscope for photographing the fundus oculi. The Ophthalmic Review: A Quarterly Journal of Ophthalmic Surgery & Science Vol 1, 1865; 119-125 http://books.google.com/books?id=v_MEAAAAQAAJ&pg=PA119
Helmholtz H. Correspondence. The Ophthalmic Review: A Quarterly Journal of Ophthalmic Surgery & Science Vol 1, 1865; 312
Noyes HD. A modification of the ophthalmoscope. Trans Am Ophthalmol Soc.1869;1(6):51-4.
Jackman WT, Webster JD. On photographing the retina of the living eye. Philadelphia Photographer 1886;23:340-341
Barr E. On photographing the interior of the human eyeball. Amer J Ophth 1887; 4:181-183
Howe L. Photography of the interior of the eye. Trans Amer Ophth Soc. 1887; 23:568-571
Starr E. Photographing the human eye. Philadelphia Photographer 1887; 24:714-716
Howe L. Orthochromatic plates for photographing the interior of the human eye. Trans Ophthalmol Soc UK. 1894; 14:251-255
Thorner W. A new stationary ophthalmoscope without reflexes. Amer J Ophth. 1899; 16:330-345.
Dimmer F. Die Photographie des Augenhintergrundes. 1907 Weisbaden: Bergmann 1907
Ballantyne AJ. Book Review: Die Photographie des Augenhintergrundes. The Ophthalmoscope. 1907 Jul: 140-143
Parsons HJ. The photography of the fundus oculi. Nature 1906; 74:104
Stephenson S, Oliver CA, Eds. The Ophthalmoscope. A Monthly Review of Current Ophthalmology. Tenth international congress of ophthalmology. 510-515
Keeler R, Singh AD, Dua HS. “Empowering eyes”: the Thorner Optometer. Br J Ophthalmol 2011 95:925
Keeler R, Singh AD, Dua HS. Battling with reflections: the Busch stereoscopic reflexless binocular ophthalmoscope. Br J Ophthalmol 2013 97:119-120
Vail D. Lucien Howe: the laboratory and experimental ophthalmology. Am J Ophthalmol 1963; 55: 261-279.
Ravin JG, Stern AM. Lucien Howe, hereditary blindness, and the eugenics movement. Arch Ophthalmol.2010 Jul;128(7):924-30
Cyber-Sight. Historical review of stereoscopic imaging. Project ORBIS International, 2003.