in a peer-reviewed journal or able to be accessed through a search of PubMed as of August 2013, I was unaware of his work until provided with this correspondence. However, in a search of the literature subsequent to receiving this notification, I was able to identify one article published in German by Remky and Amalric in 1990 that confirmed Jose Moro´n’s work in 1946, prior to the first publications by Gerd MeyerSchwickerath in 1949.1,2 In their history of photosurgery of the eye, Drs Remky and Amalric also allude to the use of photocoagulation on a human eye in 1817 by Hieronymous Hess of Basel for therapeutic coagulation in 1835. Reaching further back into history, it has been suggested that Plato either used or was aware of photocoagulation by the sun to treat the eye, in a translation by Benjamin Jowet in 2006.3 It would seem, as stated in my Jackson Lecture: ‘‘Finally, in keeping with the adage that, while failure is an orphan, success has many fathers, the history of the laser, which has had so many positive disruptive impacts in every facet of modern-day life, continues to be written and rewritten.’’4 The author again thanks Drs Grzybowski and Ascaso for their thoughtful and well-documented information indicating that attempts had been made to perform photocoagulation in humans in the modern era even prior to Meyer-Schwickerath’s first documented approach in 1949.2,4 MARK S. BLUMENKRANZ
Palo Alto, California CONFLICT OF INTEREST DISCLOSURES: SEE THE ORIGINAL article for any disclosures of the authors.
REFERENCES
1. Remky H, Amalric P. History of photosurgery in the eye. Gesnerus 1990;47(Pt 1):67–81 [in German]. 2. Meyer-Schwickerath G. Ber 55 Vers. Deutsch Opht Ges Heidelberg 1949:256. 3. Palanker DV, Blumenkranz MS, Marmor MF. Fifty years of ophthalmic laser therapy. Arch Ophthalmol 2011;129(12): 1613–1619. 4. Blumenkranz MS. The evolution of laser therapy in ophthalmology: a perspective on the interactions between photons, patients, physicians, and physicists: the LXX Edward Jackson memorial lecture. Am J Ophthalmol 2014;158(1):12–25.
Choroidal Thickness in Non-Arteritic Anterior Ischemic Optic Neuropathy
the affected eyes and in the unaffected contralateral eyes had a significantly thinner macular choroid after adjusting for age, optic disc diameter, sex, and refractive error in comparison to the individuals of a control group without fundus or optic nerve disorders. The authors suggest that a thin choroid may be added to the diagnostic features of nonarteritic AION. We congratulate and applaud their interesting and important work on this topic; however, some important issues need to be addressed. As the choroid is a highly vascular tissue, choroidal thicknesses are known to vary with intraocular pressure, blood pressure, smoking, and the use of certain drugs, such as phosphodiesterase inhibitors.2 The choroid also suffers from microvascular changes and dyslipidemia.3 However, the authors did not exclude the subjects having systemic diseases such as diabetes, hypertension, hypercholesterolemia, and obstructive sleep apnea. Also, the authors did not indicate whether they had any smokers or subjects with vascular medications, although both of them were shown to affect choroidal thickness. As systemic diseases are often comorbid with nonarteritic AION, expecting diabetes mellitus, obstructive sleep apnea, or hypertension more in the non-arteritic AION group is reasonable.4 Inclusion of these kinds of patients obviously affect the choroid and may change the results. Therefore, it should be kept in mind that choroid thinning seen in Schuster and associates’ study might be attributable to the underlying systemic diseases and concomitant interventions in patients. The authors stated that age and refractive error were corrected before comparing choroidal thickness between the groups. However, they did not adjust the axial length, which is known to be among the most important confounding factors for the interpretation of the choroidal thickness. Although refractive error is associated with axial length, it is not stable throughout life. Myopic shifts can occur, especially in elderly patients, because of nuclear cataract progression. In this study, non-arteritic AION patients tended to be older than controls, although not significantly (66.9 vs 71.9, P ¼ .07). Therefore, adjusting axial length instead of refractive error would be more accurate, particularly in this older population. In contrast to this study, a very recent study demonstrated an increase in choroidal thickness in eyes with chronic non-arteritic AION.5 Moreover, further large-scale, high-quality studies to confirm these preliminary results would be worthwhile. We congratulate the authors on their informative article and hope our remarks will contribute to more accurate elaboration of the results. MIAO HE WENYONG HUANG
EDITOR: WE READ THE ARTICLE ENTITLED ‘‘CHOROIDAL THICKNESS IN
Non-Arteritic Anterior Ischemic Optic Neuropathy’’ by Schuster and associates,1 and would like to offer our comments. The authors, in this hospital-based case-control study, demonstrated that patients with non-arteritic anterior ischemic optic neuropathy (non-arteritic AION) in VOL. 159, NO. 1
Guangzhou, China THE AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported. The authors indicate no funding support.
CORRESPONDENCE
207
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in non-arteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014; 158(6):1342–1347. 2. Mrejen S, Spaide RF. Optical coherence tomography: imaging of the choroid and beyond. Surv Ophthalmol 2013;58(5): 387–429. 3. Wong IY, Wong RL, Zhao P, Lai WW. Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography. Retina 2013;33(2):423–428. 4. Hayreh SS. Ischemic optic neuropathy. Prog Retin Eye Res 2009;28(1):34–62. 5. Dias-Santos A, Ferreira J, Pinto LA, et al. Choroidal thickness in nonarteritic anterior ischaemic optic neuropathy: a study with optical coherence tomography. Neuro-Ophthalmology 2014;38(4):173–179.
REPLY
hypercholesterolemia, diabetes mellitus, and use of some dyslipidemia. Since we did not adjust for these parameters in our study, Drs He and Huang discuss that the thin subfoveal choroid detected in the patients of our study might have been attributable to underlying systemic diseases and might not have primarily been associated with the acute nonarteritic anterior ischemic optic neuropathy. In contrast to the remark by Drs He and Huang, large population-based studies such as the Beijing Eye Study did not detect strong associations between subfoveal choroidal thickness and the parameters mentioned. One may therefore assume that the marked difference in subfoveal choroidal thickness between patients with acute non-ischemic optic neuropathy and normal individuals may not have been markedly influenced, if at all, by underlying diseases. We completely agree with Drs He and Huang in that it had been better to use axial length instead of refractive error to adjust the measurements of subfoveal choroidal thickness. ALEXANDER K. SCHUSTER
WE THANK DRS HE AND HUANG FOR THEIR INTEREST IN OUR
PHILIPPE STEINMETZ
study.1 In their letter, Dres He and Huang point out that a previous study in contrast to our investigation showed that subfoveal choroidal thickness was significantly thicker in eyes (n ¼ 18) at 57.2 6 26.9 months after an acute nonischemic anterior ischemic optic neuropathy than in eyes of a control group (n ¼ 28).2 In the same study, subfoveal choroidal thickness increased with longer follow-up after the event (P ¼ .047; correlation coefficient r ¼ 0.46). Taking into account the mean follow-up of 57.2 months and extrapolating the regression line of the association between subfoveal choroidal thickness and follow-up time as shown on Figure 3 in the article, one arrives at a subfoveal choroidal thickness of about 190 mm at the time when the nonischemic anterior ischemic optic neuropathy occurred.2 That is approximately the same value or even thinner than the value we found in our study on patients with an acute nonischemic anterior ischemic optic neuropathy (subfoveal choroidal thickness: 207 6 55 mm). Both values of subfoveal choroidal thickness, the one of the previous study (approximately 190 mm) and the one of our study (207 6 55 mm), are thinner than the mean value of subfoveal choroidal thickness (254 6 107 mm) found in a population-based study on 3233 Chinese individuals after adjustment for age and refractive error.3 Similar measurements of subfoveal choroidal thickness as in the study on Chinese subjects were found in investigations on individuals of other ethnicity.4–6 One may therefore infer that the previous study and our study both agree in that eyes with an acute non-arteritic anterior ischemic optic neuropathy have a thinner subfoveal choroid as compared to normal eyes. Drs He and Huang additionally mention that choroidal thickness may depend on ocular systemic parameters such as intraocular pressure, blood pressure, smoking,
TESSA M. FORSTER FRANK C. SCHLICHTENBREDE ¨ RN C. HARDER BJO
208
JOST B. JONAS
Heidelberg, Germany CONFLICT OF INTEREST DISCLOSURES: SEE THE ORIGINAL article for any disclosures of the authors.
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in non-arteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014; 158(6):1342–1347. 2. Dias-Santos A, Ferreira J, Pinto LA, et al. Choroidal thickness in nonarteritic anterior ischaemic optic neuropathy: a study with optical coherence tomography. Neuro-Ophthalmology 2014;38(4):173–179. 3. Wei WB, Xu L, Jonas JB, et al. Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology 2013;120(1):175–180. 4. Spaide RF, Koizumi H, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008;146(4):496–500. 5. Ikuno Y, Maruko I, Yasuno Y, et al. Reproducibility of retinal and choroidal thickness measurements in enhanced depth imaging and high-penetration optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52(8):5536–5540. 6. Rahman W, Chen FK, Yeoh J, Patel P, Tufail A, Da Cruz L. Repeatability of manual subfoveal choroidal thickness measurements in healthy subjects using the technique of enhanced depth imaging optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52(5):2267–2271.
AMERICAN JOURNAL OF OPHTHALMOLOGY
JANUARY 2015
Palo Alto, California CONFLICT OF INTEREST DISCLOSURES: SEE THE ORIGINAL article for any disclosures of the authors.
REFERENCES
1. Remky H, Amalric P. History of photosurgery in the eye. Gesnerus 1990;47(Pt 1):67–81 [in German]. 2. Meyer-Schwickerath G. Ber 55 Vers. Deutsch Opht Ges Heidelberg 1949:256. 3. Palanker DV, Blumenkranz MS, Marmor MF. Fifty years of ophthalmic laser therapy. Arch Ophthalmol 2011;129(12): 1613–1619. 4. Blumenkranz MS. The evolution of laser therapy in ophthalmology: a perspective on the interactions between photons, patients, physicians, and physicists: the LXX Edward Jackson memorial lecture. Am J Ophthalmol 2014;158(1):12–25.
Choroidal Thickness in Non-Arteritic Anterior Ischemic Optic Neuropathy
the affected eyes and in the unaffected contralateral eyes had a significantly thinner macular choroid after adjusting for age, optic disc diameter, sex, and refractive error in comparison to the individuals of a control group without fundus or optic nerve disorders. The authors suggest that a thin choroid may be added to the diagnostic features of nonarteritic AION. We congratulate and applaud their interesting and important work on this topic; however, some important issues need to be addressed. As the choroid is a highly vascular tissue, choroidal thicknesses are known to vary with intraocular pressure, blood pressure, smoking, and the use of certain drugs, such as phosphodiesterase inhibitors.2 The choroid also suffers from microvascular changes and dyslipidemia.3 However, the authors did not exclude the subjects having systemic diseases such as diabetes, hypertension, hypercholesterolemia, and obstructive sleep apnea. Also, the authors did not indicate whether they had any smokers or subjects with vascular medications, although both of them were shown to affect choroidal thickness. As systemic diseases are often comorbid with nonarteritic AION, expecting diabetes mellitus, obstructive sleep apnea, or hypertension more in the non-arteritic AION group is reasonable.4 Inclusion of these kinds of patients obviously affect the choroid and may change the results. Therefore, it should be kept in mind that choroid thinning seen in Schuster and associates’ study might be attributable to the underlying systemic diseases and concomitant interventions in patients. The authors stated that age and refractive error were corrected before comparing choroidal thickness between the groups. However, they did not adjust the axial length, which is known to be among the most important confounding factors for the interpretation of the choroidal thickness. Although refractive error is associated with axial length, it is not stable throughout life. Myopic shifts can occur, especially in elderly patients, because of nuclear cataract progression. In this study, non-arteritic AION patients tended to be older than controls, although not significantly (66.9 vs 71.9, P ¼ .07). Therefore, adjusting axial length instead of refractive error would be more accurate, particularly in this older population. In contrast to this study, a very recent study demonstrated an increase in choroidal thickness in eyes with chronic non-arteritic AION.5 Moreover, further large-scale, high-quality studies to confirm these preliminary results would be worthwhile. We congratulate the authors on their informative article and hope our remarks will contribute to more accurate elaboration of the results. MIAO HE WENYONG HUANG
EDITOR: WE READ THE ARTICLE ENTITLED ‘‘CHOROIDAL THICKNESS IN
Non-Arteritic Anterior Ischemic Optic Neuropathy’’ by Schuster and associates,1 and would like to offer our comments. The authors, in this hospital-based case-control study, demonstrated that patients with non-arteritic anterior ischemic optic neuropathy (non-arteritic AION) in VOL. 159, NO. 1
Guangzhou, China THE AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported. The authors indicate no funding support.
CORRESPONDENCE
207
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in non-arteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014; 158(6):1342–1347. 2. Mrejen S, Spaide RF. Optical coherence tomography: imaging of the choroid and beyond. Surv Ophthalmol 2013;58(5): 387–429. 3. Wong IY, Wong RL, Zhao P, Lai WW. Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography. Retina 2013;33(2):423–428. 4. Hayreh SS. Ischemic optic neuropathy. Prog Retin Eye Res 2009;28(1):34–62. 5. Dias-Santos A, Ferreira J, Pinto LA, et al. Choroidal thickness in nonarteritic anterior ischaemic optic neuropathy: a study with optical coherence tomography. Neuro-Ophthalmology 2014;38(4):173–179.
REPLY
hypercholesterolemia, diabetes mellitus, and use of some dyslipidemia. Since we did not adjust for these parameters in our study, Drs He and Huang discuss that the thin subfoveal choroid detected in the patients of our study might have been attributable to underlying systemic diseases and might not have primarily been associated with the acute nonarteritic anterior ischemic optic neuropathy. In contrast to the remark by Drs He and Huang, large population-based studies such as the Beijing Eye Study did not detect strong associations between subfoveal choroidal thickness and the parameters mentioned. One may therefore assume that the marked difference in subfoveal choroidal thickness between patients with acute non-ischemic optic neuropathy and normal individuals may not have been markedly influenced, if at all, by underlying diseases. We completely agree with Drs He and Huang in that it had been better to use axial length instead of refractive error to adjust the measurements of subfoveal choroidal thickness. ALEXANDER K. SCHUSTER
WE THANK DRS HE AND HUANG FOR THEIR INTEREST IN OUR
PHILIPPE STEINMETZ
study.1 In their letter, Dres He and Huang point out that a previous study in contrast to our investigation showed that subfoveal choroidal thickness was significantly thicker in eyes (n ¼ 18) at 57.2 6 26.9 months after an acute nonischemic anterior ischemic optic neuropathy than in eyes of a control group (n ¼ 28).2 In the same study, subfoveal choroidal thickness increased with longer follow-up after the event (P ¼ .047; correlation coefficient r ¼ 0.46). Taking into account the mean follow-up of 57.2 months and extrapolating the regression line of the association between subfoveal choroidal thickness and follow-up time as shown on Figure 3 in the article, one arrives at a subfoveal choroidal thickness of about 190 mm at the time when the nonischemic anterior ischemic optic neuropathy occurred.2 That is approximately the same value or even thinner than the value we found in our study on patients with an acute nonischemic anterior ischemic optic neuropathy (subfoveal choroidal thickness: 207 6 55 mm). Both values of subfoveal choroidal thickness, the one of the previous study (approximately 190 mm) and the one of our study (207 6 55 mm), are thinner than the mean value of subfoveal choroidal thickness (254 6 107 mm) found in a population-based study on 3233 Chinese individuals after adjustment for age and refractive error.3 Similar measurements of subfoveal choroidal thickness as in the study on Chinese subjects were found in investigations on individuals of other ethnicity.4–6 One may therefore infer that the previous study and our study both agree in that eyes with an acute non-arteritic anterior ischemic optic neuropathy have a thinner subfoveal choroid as compared to normal eyes. Drs He and Huang additionally mention that choroidal thickness may depend on ocular systemic parameters such as intraocular pressure, blood pressure, smoking,
TESSA M. FORSTER FRANK C. SCHLICHTENBREDE ¨ RN C. HARDER BJO
208
JOST B. JONAS
Heidelberg, Germany CONFLICT OF INTEREST DISCLOSURES: SEE THE ORIGINAL article for any disclosures of the authors.
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in non-arteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014; 158(6):1342–1347. 2. Dias-Santos A, Ferreira J, Pinto LA, et al. Choroidal thickness in nonarteritic anterior ischaemic optic neuropathy: a study with optical coherence tomography. Neuro-Ophthalmology 2014;38(4):173–179. 3. Wei WB, Xu L, Jonas JB, et al. Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology 2013;120(1):175–180. 4. Spaide RF, Koizumi H, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008;146(4):496–500. 5. Ikuno Y, Maruko I, Yasuno Y, et al. Reproducibility of retinal and choroidal thickness measurements in enhanced depth imaging and high-penetration optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52(8):5536–5540. 6. Rahman W, Chen FK, Yeoh J, Patel P, Tufail A, Da Cruz L. Repeatability of manual subfoveal choroidal thickness measurements in healthy subjects using the technique of enhanced depth imaging optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52(5):2267–2271.
AMERICAN JOURNAL OF OPHTHALMOLOGY
JANUARY 2015
