CORRESPONDENCE Choroidal Thickness in _ Nonarteritic Anterior Ischemic Optic Neuropathy EDITOR: WE
READ
WITH
INTEREST
THE
ARTICLE
ENTITLED
‘‘Choroidal Thickness in Nonarteritic Anterior Ischemic Optic Neuropathy,’’ by Schuster and associates.1 The authors have investigated the choroidal thicknesses (CT) in patients who had nonarteritic anterior ischemic optic neuropathy (NAION) at the acute stage and reported that the affected eyes of patients who had acute NAION and their contralateral, unaffected eyes showed significantly thinner macular CTs than the eyes of healthy subjects. Therefore, the authors have proposed that a thin choroid might be a diagnostic feature of NAION. We thank the authors for their intriguing study and would like to make some contributions with respect to 2 points for further CT studies in NAION. First, for the choroidal thickness measurements, they used 1 horizontal section passing through the center of the fovea, which was evaluated on this section at 7 points, and separately compared these measurements between the patient and the control groups. However, taking optical coherence tomography (OCT) measurements at 1 selected point and comparing these to each other is not the most precise method for determining CTs, since these measurements, which are performed manually, could be affected by local irregularities of the choroidscleral boundary.2,3 Therefore, several points in the same horizontal sections of the macula could be measured to reduce the risk of mistakes. The average of these measurements could then be compared. However, in future, the development of automatic software for CT measurements will help to improve the accuracy of these measurements. In addition, CT measurements could be affected by a number of factors such as age, sex, spherical equivalent, axial length, diurnal variation, smoking, coffee addiction, and some conditions such as diabetes mellitus and age-related macular degeneration.4–6 To eliminate these potentially confusing factors, the authors have statistically adjusted some of them for comparisons; however, these adjustments did not include all the factors mentioned above. Also, in their study, although there was a significant difference in terms of the CTs between the acute NAION patients and the healthy subjects, there were no significant differences between the CT measurements of the affected and
994
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2015 BY
unaffected eyes in patients with acute NAION and between their affected and previously affected eyes. This might support the assertion that the study by Schuster and associates1 could have been influenced by these confusing factors. In contrast to this study, Dias-Santos and associates2 have reported that the mean CT is significantly higher in patients with chronic NAION than in healthy subjects and that this might be a marker of the local dysfunction of the vascular autoregulation mechanisms of the choroid. These authors also reported that there is a statistical association between CT and the amount of time after the ischemic attack. However, Schuster and associates1 have reported that, in terms of the CTs, the affected eyes of patients who had acute NAION did not differ significantly from their contralateral eyes that had previously been affected by NAION. Because of these conflicting casecontrol studies, further prospective studies with larger sample sizes as well as follow-up studies are needed to validate these results. SABAN GONUL SULEYMAN OKUDAN
Konya, Turkey 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.
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in nonarteritic 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. Gonul S, Ozturk BT, Okudan S. Measurement of choroid thickness in pregnant women using enhanced depth imaging optical coherence tomography. Arq Bras Oftalmol. http://dx. doi.org/10.5935/0004-2749.201400XX. 4. Li XQ, Larsen M, Munch IC. Subfoveal choroidal thickness in relation to sex and axial length in 93 Danish university students. Invest Ophthalmol Vis Sci 2011;52(11): 8438–8441. 5. Vural AD, Kara N, Sayin N, Pirhan D, Ersan HB. Choroidal thickness changes after a single administration of coffee in healthy subjects. Retina 2014;34(6):1223–1228.
ELSEVIER INC. ALL
RIGHTS RESERVED.
0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2015.01.036
6. Sizmaz S, Kuc¸ukerdonmez C, Pinarci EY, Karalezli A, Canan H, Yilmaz G. The effect of smoking on choroidal thickness measured by optical coherence tomography. Br J Ophthalmol 2013;97(5):601–604.
REPLY WE THANK DRS GONUL AND OKUDAN FOR THEIR INTEREST
in our study.1 In their letter, they mention the inaccuracy of manually performed measurements of choroidal thickness and suggest to average several manual measurements taken at different locations in the same horizontal section of the macula. One may argue against this suggestion, since the choroidal thickness markedly gets thinner the more distant from the foveola. Interestingly, we found that the eyes with acute nonarteritic anterior ischemic optic neuropathy had thinner choroidal thickness measurements in the foveola and in all other measurement locations except for the nasal location.1 We agree with Drs Gonul and Okudan that an automatic delineation of the choroidal borders may be helpful for choroidal thickness measurements.2 Drs Gonul and Okudan state, and we fully agree, that choroidal thickness depends on a variety of ocular and systemic parameters such as age, spherical equivalent, and axial length. Since we did not adjust for all of these parameters in our study, Drs Gonul and Okudan discussed 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. We would like to bring forward the argument that in large population-based studies such as the Beijing Eye Study, systemic diseases including arterial hypertension and diabetes mellitus did not have a major influence on subfoveal choroidal thickness.3 Since the choroidal thickness measurements had been adjusted for the main factors (ie, age and refractive error) influencing choroidal thickness, one may infer that the marked difference in subfoveal choroidal thickness between patients with acute nonischemic optic neuropathy and normal individuals in our study may not have been markedly influenced by differences between both groups in the prevalence of underlying systemic diseases. Drs Gonul and Okudan cited a previous study by Dias-Santos and associates in which subfoveal choroidal thickness was significantly thicker in eyes at 57.2 6 26.9 months after an acute nonischemic anterior ischemic optic neuropathy than in the control group.4 This appears to be in contrast to our investigation. In the study by Dias-Santos, however, subfoveal choroidal thickness increased with longer follow-up
VOL. 159, NO. 5
after the event (P ¼ .047; correlation coefficient r ¼ 0.46). Taking into account the mean follow-up and extrapolating the regression line of the association between subfoveal choroidal thickness and follow-up time, one arrives at a subfoveal choroidal thickness of about 190 mm at the time when the nonischemic anterior ischemic optic neuropathy occurred.4,5 That is approximately the same value we found in our study on patients with an acute nonischemic anterior ischemic optic neuropathy. Both values of subfoveal choroidal thickness, as determined by extrapolation in the study by Dias-Santos and as measured in our study, are thinner than the mean value of subfoveal choroidal thickness (254 6 107 mm) measured in a populationbased study on 3233 Chinese individuals after adjustment for age and refractive error. In investigations on individuals of other ethnicity, similar measurements of subfoveal choroidal thickness were found as in the Beijing Eye Study.6,7 In conclusion, the previous study by Dias-Santos and associates and our study both support that eyes with an acute nonischemic anterior ischemic optic neuropathy have a thinner subfoveal choroid as compared to normal eyes. ALEXANDER K. SCHUSTER PHILIPPE STEINMETZ TESSA M. FORSTER FRANK C. SCHLICHTENBREDE ¨ RN C. HARDER BJO 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 nonarteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014;158(6): 1342–1347. 2. Zhang L, Lee K, Niemeijer M, Mullins RF, Sonka M, Abra`moff MD. Automated segmentation of the choroid from clinical SD-OCT. Invest Ophthalmol Vis Sci 2012;53(12): 7510–7519. 3. Wei WB, Xu L, Jonas JB, et al. Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology 2013;120(1): 175–180. 4. 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. 5. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Reply. Am J Ophthalmol 2015;159(1): 208 [Reply to PMID 25217855].
CORRESPONDENCE
995
READ
WITH
INTEREST
THE
ARTICLE
ENTITLED
‘‘Choroidal Thickness in Nonarteritic Anterior Ischemic Optic Neuropathy,’’ by Schuster and associates.1 The authors have investigated the choroidal thicknesses (CT) in patients who had nonarteritic anterior ischemic optic neuropathy (NAION) at the acute stage and reported that the affected eyes of patients who had acute NAION and their contralateral, unaffected eyes showed significantly thinner macular CTs than the eyes of healthy subjects. Therefore, the authors have proposed that a thin choroid might be a diagnostic feature of NAION. We thank the authors for their intriguing study and would like to make some contributions with respect to 2 points for further CT studies in NAION. First, for the choroidal thickness measurements, they used 1 horizontal section passing through the center of the fovea, which was evaluated on this section at 7 points, and separately compared these measurements between the patient and the control groups. However, taking optical coherence tomography (OCT) measurements at 1 selected point and comparing these to each other is not the most precise method for determining CTs, since these measurements, which are performed manually, could be affected by local irregularities of the choroidscleral boundary.2,3 Therefore, several points in the same horizontal sections of the macula could be measured to reduce the risk of mistakes. The average of these measurements could then be compared. However, in future, the development of automatic software for CT measurements will help to improve the accuracy of these measurements. In addition, CT measurements could be affected by a number of factors such as age, sex, spherical equivalent, axial length, diurnal variation, smoking, coffee addiction, and some conditions such as diabetes mellitus and age-related macular degeneration.4–6 To eliminate these potentially confusing factors, the authors have statistically adjusted some of them for comparisons; however, these adjustments did not include all the factors mentioned above. Also, in their study, although there was a significant difference in terms of the CTs between the acute NAION patients and the healthy subjects, there were no significant differences between the CT measurements of the affected and
994
Ó
2015 BY
unaffected eyes in patients with acute NAION and between their affected and previously affected eyes. This might support the assertion that the study by Schuster and associates1 could have been influenced by these confusing factors. In contrast to this study, Dias-Santos and associates2 have reported that the mean CT is significantly higher in patients with chronic NAION than in healthy subjects and that this might be a marker of the local dysfunction of the vascular autoregulation mechanisms of the choroid. These authors also reported that there is a statistical association between CT and the amount of time after the ischemic attack. However, Schuster and associates1 have reported that, in terms of the CTs, the affected eyes of patients who had acute NAION did not differ significantly from their contralateral eyes that had previously been affected by NAION. Because of these conflicting casecontrol studies, further prospective studies with larger sample sizes as well as follow-up studies are needed to validate these results. SABAN GONUL SULEYMAN OKUDAN
Konya, Turkey 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.
REFERENCES
1. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Choroidal thickness in nonarteritic 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. Gonul S, Ozturk BT, Okudan S. Measurement of choroid thickness in pregnant women using enhanced depth imaging optical coherence tomography. Arq Bras Oftalmol. http://dx. doi.org/10.5935/0004-2749.201400XX. 4. Li XQ, Larsen M, Munch IC. Subfoveal choroidal thickness in relation to sex and axial length in 93 Danish university students. Invest Ophthalmol Vis Sci 2011;52(11): 8438–8441. 5. Vural AD, Kara N, Sayin N, Pirhan D, Ersan HB. Choroidal thickness changes after a single administration of coffee in healthy subjects. Retina 2014;34(6):1223–1228.
ELSEVIER INC. ALL
RIGHTS RESERVED.
0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2015.01.036
6. Sizmaz S, Kuc¸ukerdonmez C, Pinarci EY, Karalezli A, Canan H, Yilmaz G. The effect of smoking on choroidal thickness measured by optical coherence tomography. Br J Ophthalmol 2013;97(5):601–604.
REPLY WE THANK DRS GONUL AND OKUDAN FOR THEIR INTEREST
in our study.1 In their letter, they mention the inaccuracy of manually performed measurements of choroidal thickness and suggest to average several manual measurements taken at different locations in the same horizontal section of the macula. One may argue against this suggestion, since the choroidal thickness markedly gets thinner the more distant from the foveola. Interestingly, we found that the eyes with acute nonarteritic anterior ischemic optic neuropathy had thinner choroidal thickness measurements in the foveola and in all other measurement locations except for the nasal location.1 We agree with Drs Gonul and Okudan that an automatic delineation of the choroidal borders may be helpful for choroidal thickness measurements.2 Drs Gonul and Okudan state, and we fully agree, that choroidal thickness depends on a variety of ocular and systemic parameters such as age, spherical equivalent, and axial length. Since we did not adjust for all of these parameters in our study, Drs Gonul and Okudan discussed 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. We would like to bring forward the argument that in large population-based studies such as the Beijing Eye Study, systemic diseases including arterial hypertension and diabetes mellitus did not have a major influence on subfoveal choroidal thickness.3 Since the choroidal thickness measurements had been adjusted for the main factors (ie, age and refractive error) influencing choroidal thickness, one may infer that the marked difference in subfoveal choroidal thickness between patients with acute nonischemic optic neuropathy and normal individuals in our study may not have been markedly influenced by differences between both groups in the prevalence of underlying systemic diseases. Drs Gonul and Okudan cited a previous study by Dias-Santos and associates in which subfoveal choroidal thickness was significantly thicker in eyes at 57.2 6 26.9 months after an acute nonischemic anterior ischemic optic neuropathy than in the control group.4 This appears to be in contrast to our investigation. In the study by Dias-Santos, however, subfoveal choroidal thickness increased with longer follow-up
VOL. 159, NO. 5
after the event (P ¼ .047; correlation coefficient r ¼ 0.46). Taking into account the mean follow-up and extrapolating the regression line of the association between subfoveal choroidal thickness and follow-up time, one arrives at a subfoveal choroidal thickness of about 190 mm at the time when the nonischemic anterior ischemic optic neuropathy occurred.4,5 That is approximately the same value we found in our study on patients with an acute nonischemic anterior ischemic optic neuropathy. Both values of subfoveal choroidal thickness, as determined by extrapolation in the study by Dias-Santos and as measured in our study, are thinner than the mean value of subfoveal choroidal thickness (254 6 107 mm) measured in a populationbased study on 3233 Chinese individuals after adjustment for age and refractive error. In investigations on individuals of other ethnicity, similar measurements of subfoveal choroidal thickness were found as in the Beijing Eye Study.6,7 In conclusion, the previous study by Dias-Santos and associates and our study both support that eyes with an acute nonischemic anterior ischemic optic neuropathy have a thinner subfoveal choroid as compared to normal eyes. ALEXANDER K. SCHUSTER PHILIPPE STEINMETZ TESSA M. FORSTER FRANK C. SCHLICHTENBREDE ¨ RN C. HARDER BJO 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 nonarteritic anterior ischemic optic neuropathy. Am J Ophthalmol 2014;158(6): 1342–1347. 2. Zhang L, Lee K, Niemeijer M, Mullins RF, Sonka M, Abra`moff MD. Automated segmentation of the choroid from clinical SD-OCT. Invest Ophthalmol Vis Sci 2012;53(12): 7510–7519. 3. Wei WB, Xu L, Jonas JB, et al. Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology 2013;120(1): 175–180. 4. 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. 5. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB. Reply. Am J Ophthalmol 2015;159(1): 208 [Reply to PMID 25217855].
CORRESPONDENCE
995
