- Email: [email protected]
Indocyanine green-assisted peeling of the internal limiting membrane in macular hole surgery affects visual outcome
back when the suspension containing the triamcinolone acetonide crystals and the (diluted) solvent agent are pressed through the filter and removed from the syringe. At the end of the filtering process, approximately 0.2 ml suspension are left over consisting of the triamcinolone acetonide crystals and the rest of Ringer⬘s solution, with more than 99% of the solvent agent removed. Because the millipore filter will not keep back all of the triamcinolone acetonide crystals, recent measurements have suggested that approximately 90% to 95% of the original dosage of 25 mg triamcinolone will be available for intravitreal injection.
patients with type 2 diabetes and also in individuals with normal and impaired glucose metabolism. This suggests that, in addition to lowering of serum glucose and blood pressure in diabetic patients, adequate treatment of (abdominal) obesity by lifestyle intervention might contribute to the prevention of retinopathy in diabetic (and nondiabetic) individuals. BETTINE C. P. POLAK, MD, PHD JACQUELINE M. DEKKER, PHD ANNETTE C. MOLL, MD, PHD HENDRIK A. VAN LEIDEN, MD
Amsterdam, The Netherlands
JOST B. JONAS, MD INGRID KREISSIG, MD
REFERENCES
ROBERT F. DEGENRING, MD
Heidelberg, Germany
REFERENCE
1. Jonas JB, Kreissig I, Degenring RF. Intravitreal triamcinolone acetonide for pseudophakic cystoid macular edema. Am J Ophthalmol 2003;136:384 –386.
1. Chaturvedi N, Sjoelie AK, Porta M, et al. Markers of insulin resistance are strong risk factors for retinopathy incidence in type 1 diabetes. Diabetes Care 2001;24:284 –289. 2. van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids and obesity are associated with retinopathy: The Hoorn study. Diabetes Care 2002;25:1320 –1325. 3. van Leiden HA, Dekker JM, Moll AC, et al. Risk factors for incident retinopathy in a diabetic and nondiabetic population: The Hoorn study. Arch Ophthalmol 2003;121:245–251.
Perspectives on Diabetic Retinopathy
AUTHOR REPLY
EDITOR:
AS CITED BY DR. BETTINE CECILE POLAK AND ASSOCIATES
THE ARTICLE BY L. M. AIELLO (AM J OPHTHALMOL 2003;136:
in their letter to the editor, abdominal obesity in type 1 and type 2 diabetes is an important systemic risk factor for progression of diabetic retinopathy and should have been discussed and listed in Table 10 (Am J Ophthalmol 2003;136:130) and their references included. I greatly appreciate that the authors of this letter have brought to our attention the importance of appropriate treatment of obesity.
122–135) gives an excellent review of the current understanding of diabetic retinopathy with recommendations for preventing and curing diabetic retinopathy now and in the future. The suggestions for evidence-based diabetic patient care can be extended from daily diabetic (eye) care, patient education, and instruction of medical and nonmedical care providers to the development, updating, and implementation of guidelines on screening for diabetic retinopathy. A number of tables summarize recommendations for ocular examination schedules, management of diabetic retinopathy, and systemic risk factors for (progression of) diabetic retinopathy: hypertension, dyslipidemia, gastroparesis, poor glucose control, renal insufficiency, anemia, pregnancy, and eating disorders. We would like to stress the importance of treatment of abdominal obesity in diabetic, both type 1 and type 2, and even in nondiabetic individuals. In the Eurodiab study,1 a high waist-to-hip ratio was found to be an independent risk factor in diabetes type 1 patients. In the Hoorn study,2,3 a population-based cohort study on glucose metabolism in The Netherlands, an increased body mass index and a high waist-hip ratio were found to be independent determinants for the prevalence and incidence of retinopathy, respectively. This was observed in VOL. 136, NO. 6
LLOYD M. AIELLO, MD
Boston, Massachusetts
Indocyanine Green-assisted Peeling of the Internal Limiting Membrane in Macular Hole Surgery Affects Visual Outcome EDITOR: THE ARTICLE BY HARITOGLOU AND ASSOCIATES (AM J
Ophthalmol 2002;134:836 – 841) on indocyanine green (ICG)-assisted peeling of the internal limiting membrane (ILM) in macular hole surgery,1 was most interesting, although we are concerned about some of the authors’ observations and conclusions. First, they questioned our conclusion regarding postmortem artifact of cellular elements in our initial study.2 Indeed, cellular elements have been reported in epiretinal
CORRESPONDENCE
1193
or ILM specimens, whether ICG dye or not is used.3 Because this was a cadaver study, determining causation is problematic. Although they claim the finding of retinal elements on the retinal side of the ILM was “. . . in contrast to our experience and observations in former investigations.” We could not find supportive histopatholologic data in two of their references.4,5 In another reference,3 the ultrastuctural studies actually revealed cellular elements, including astrocytes and glial cells with “microvilli resembling ‘fiber baskets’ of Mu¨ ller cells” in eyes that underwent membrane peeling without ICG. Therefore, their assertion that ICG alters the cleavage plane does not appear to be valid. Second, they report no obvious differences in surgical approach between our second study6 and theirs. We respectfully submit that there are substantial differences. In the current study, Haritoglou and associates1 report using 0.2 cc to 0.5 cc of ICG for 1 minute. Although we initially used a similar technique, we have modified our approach.6 We currently use 0.05 cc to 0.1 cc and begin evacuation within 30 seconds. Also, their method of dilution differs from ours. Moreover, we never purposefully evacuate fluid from the macular hole itself. And we avoid prolonged suction of the posterior hyaloid with the vitrectomy probe, as they describe in their methods section. Finally, their ICG dye originates from a different manufacturer (Pulsion Medical) than ours (Akorn). Third, we are concerned about the validity of comparisons between the 20 patients involving a single surgeon in the current paper and their earlier work in 105 patients involving four surgeons undergoing ILM peeling without the use of ICG.4 In the current study,1 Goldmann visual fields were done on all patients, whereas in their earlier study4 scanning laser ophthalmoscope static microperimetry was done to evaluate small paracentral scotomas. In the earlier study4 the methods section does not describe doing more peripheral (Goldmann) visual fields. Although they have separately reported Goldmann visual fields in patients undergoing ILM peeling without ICG,7 it is not clear that this is the same patient population because the period of time differed slightly between the two papers. There are also critical differences in histopathologic evaluation of the two groups. All ILM specimens from the 20 patients in the ICG group were evaluated by light and electron microscopy, whereas none of the patients in their earlier work were evaluated histopathologically.4 Thus, it is not known that the tissue removed in their earlier (non-ICG) group was ILM. Several factors have been implicated in visual field defects following macular hole surgery before the use of ICG. It is difficult to follow their logic regarding the role of ICG use in the macular region as a cause of peripheral visual field defects. Although it is possible ICG is toxic to the optic nerve, this seems unlikely in the absence of a new relative afferent pupillary defect or optic atrophy. In summary, we do not believe that the conclusion of Haritoglou and associates that “ICG type used in our 1194
AMERICAN JOURNAL
patients may affect visual outcome and contribute to the occurrence of postoperative visual field defects” is valid for the reasons discussed herein. We are also not convinced that there are in fact differences between stained and unstained ILM, as they have asserted, or that the cleavage plane is altered. Although they acknowledge that the limitations of their study include the fact that it is a noncomparative study, Haritoglou and coworkers persist in comparing study groups that are not comparable because of the issues enumerated above. ROBERT E. FOSTER, MD CHRISTOPHER D. RIEMANN, MD ANDREA P. DA MATA, MD SCOTT E. BURK, MD, PHD MICHAEL R. PETERSEN, MD, PHD
Cincinnati, Ohio ROBERT H. ROSA, JR., MD
Temple, Texas REFERENCES
1. Haritoglou C, Gandorfer A, Gass CA, et al. Indocyanine green-assisted peeling of the internal limiting membrane in macular hole surgery affects visual outcome: a clinicopathologic correlation. Am J Ophthalmol 2002;134:836 –841. 2. Burk SE, Da Mata AP, Snyder ME, Foster RE. Indocyanine green assisted peeling of the retinal internal-limiting membrane. Ophthalmology 2000;107:2010 –2014. 3. Messmer EM, Heidenkummer HP, Kampik A. Ultrastructure of epiretinal membranes associated with macular holes. Graefes Arch Clin Exp Ophthalmol 1998;236:248 –254. 4. Haritoglou C, Gass CA, Schaumberger M, et al. Macular changes after peeling of the internal limiting membrane in macular hole surgery. Am J Ophthalmol 2001;132:363–368. 5. Liesenhoff O, Messmer EM, Pulur A, Kampik A. Treatment of full-thickness idiopathic macular holes. Der Ophthalmologe 1996;93:655–659. 6. Da Mata AP, Burk SE, Riemann CD, Snyder ME, et al. ICG-assisted peeling of the retinal ILM [Letter]. Ophthalmology 2002;109:1040 –1041. 7. Gass CA, Haritoglou C, Messmer EM, et al. Peripheral visual field defects after macular hole surgery: a complication with decreasing incidence. Br J Ophthalmol 2001;85:549 –551.
AUTHOR REPLY WE THANK DR. FOSTER AND COWORKERS FOR THEIR CRIT-
ical statement concerning our article. We can not agree with their major concerns, however, upon which we comment as follows: First, in their letter they refer to an article from our institution describing ultrastructural findings in epiretinal membranes associated with macular holes.1 Indeed, cellular epiretinal elements were identified as glial cells with characteristics of Mu¨ ller cells. These cells are definitely situated at the vitreal surface of the ILM. On the retinal side of the ILM some tiny cellular elements are present. That corresponds well with a recent report on the presence of such elements in specimens of epiretinal membranes OF
OPHTHALMOLOGY
DECEMBER 2003
patients with type 2 diabetes and also in individuals with normal and impaired glucose metabolism. This suggests that, in addition to lowering of serum glucose and blood pressure in diabetic patients, adequate treatment of (abdominal) obesity by lifestyle intervention might contribute to the prevention of retinopathy in diabetic (and nondiabetic) individuals. BETTINE C. P. POLAK, MD, PHD JACQUELINE M. DEKKER, PHD ANNETTE C. MOLL, MD, PHD HENDRIK A. VAN LEIDEN, MD
Amsterdam, The Netherlands
JOST B. JONAS, MD INGRID KREISSIG, MD
REFERENCES
ROBERT F. DEGENRING, MD
Heidelberg, Germany
REFERENCE
1. Jonas JB, Kreissig I, Degenring RF. Intravitreal triamcinolone acetonide for pseudophakic cystoid macular edema. Am J Ophthalmol 2003;136:384 –386.
1. Chaturvedi N, Sjoelie AK, Porta M, et al. Markers of insulin resistance are strong risk factors for retinopathy incidence in type 1 diabetes. Diabetes Care 2001;24:284 –289. 2. van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids and obesity are associated with retinopathy: The Hoorn study. Diabetes Care 2002;25:1320 –1325. 3. van Leiden HA, Dekker JM, Moll AC, et al. Risk factors for incident retinopathy in a diabetic and nondiabetic population: The Hoorn study. Arch Ophthalmol 2003;121:245–251.
Perspectives on Diabetic Retinopathy
AUTHOR REPLY
EDITOR:
AS CITED BY DR. BETTINE CECILE POLAK AND ASSOCIATES
THE ARTICLE BY L. M. AIELLO (AM J OPHTHALMOL 2003;136:
in their letter to the editor, abdominal obesity in type 1 and type 2 diabetes is an important systemic risk factor for progression of diabetic retinopathy and should have been discussed and listed in Table 10 (Am J Ophthalmol 2003;136:130) and their references included. I greatly appreciate that the authors of this letter have brought to our attention the importance of appropriate treatment of obesity.
122–135) gives an excellent review of the current understanding of diabetic retinopathy with recommendations for preventing and curing diabetic retinopathy now and in the future. The suggestions for evidence-based diabetic patient care can be extended from daily diabetic (eye) care, patient education, and instruction of medical and nonmedical care providers to the development, updating, and implementation of guidelines on screening for diabetic retinopathy. A number of tables summarize recommendations for ocular examination schedules, management of diabetic retinopathy, and systemic risk factors for (progression of) diabetic retinopathy: hypertension, dyslipidemia, gastroparesis, poor glucose control, renal insufficiency, anemia, pregnancy, and eating disorders. We would like to stress the importance of treatment of abdominal obesity in diabetic, both type 1 and type 2, and even in nondiabetic individuals. In the Eurodiab study,1 a high waist-to-hip ratio was found to be an independent risk factor in diabetes type 1 patients. In the Hoorn study,2,3 a population-based cohort study on glucose metabolism in The Netherlands, an increased body mass index and a high waist-hip ratio were found to be independent determinants for the prevalence and incidence of retinopathy, respectively. This was observed in VOL. 136, NO. 6
LLOYD M. AIELLO, MD
Boston, Massachusetts
Indocyanine Green-assisted Peeling of the Internal Limiting Membrane in Macular Hole Surgery Affects Visual Outcome EDITOR: THE ARTICLE BY HARITOGLOU AND ASSOCIATES (AM J
Ophthalmol 2002;134:836 – 841) on indocyanine green (ICG)-assisted peeling of the internal limiting membrane (ILM) in macular hole surgery,1 was most interesting, although we are concerned about some of the authors’ observations and conclusions. First, they questioned our conclusion regarding postmortem artifact of cellular elements in our initial study.2 Indeed, cellular elements have been reported in epiretinal
CORRESPONDENCE
1193
or ILM specimens, whether ICG dye or not is used.3 Because this was a cadaver study, determining causation is problematic. Although they claim the finding of retinal elements on the retinal side of the ILM was “. . . in contrast to our experience and observations in former investigations.” We could not find supportive histopatholologic data in two of their references.4,5 In another reference,3 the ultrastuctural studies actually revealed cellular elements, including astrocytes and glial cells with “microvilli resembling ‘fiber baskets’ of Mu¨ ller cells” in eyes that underwent membrane peeling without ICG. Therefore, their assertion that ICG alters the cleavage plane does not appear to be valid. Second, they report no obvious differences in surgical approach between our second study6 and theirs. We respectfully submit that there are substantial differences. In the current study, Haritoglou and associates1 report using 0.2 cc to 0.5 cc of ICG for 1 minute. Although we initially used a similar technique, we have modified our approach.6 We currently use 0.05 cc to 0.1 cc and begin evacuation within 30 seconds. Also, their method of dilution differs from ours. Moreover, we never purposefully evacuate fluid from the macular hole itself. And we avoid prolonged suction of the posterior hyaloid with the vitrectomy probe, as they describe in their methods section. Finally, their ICG dye originates from a different manufacturer (Pulsion Medical) than ours (Akorn). Third, we are concerned about the validity of comparisons between the 20 patients involving a single surgeon in the current paper and their earlier work in 105 patients involving four surgeons undergoing ILM peeling without the use of ICG.4 In the current study,1 Goldmann visual fields were done on all patients, whereas in their earlier study4 scanning laser ophthalmoscope static microperimetry was done to evaluate small paracentral scotomas. In the earlier study4 the methods section does not describe doing more peripheral (Goldmann) visual fields. Although they have separately reported Goldmann visual fields in patients undergoing ILM peeling without ICG,7 it is not clear that this is the same patient population because the period of time differed slightly between the two papers. There are also critical differences in histopathologic evaluation of the two groups. All ILM specimens from the 20 patients in the ICG group were evaluated by light and electron microscopy, whereas none of the patients in their earlier work were evaluated histopathologically.4 Thus, it is not known that the tissue removed in their earlier (non-ICG) group was ILM. Several factors have been implicated in visual field defects following macular hole surgery before the use of ICG. It is difficult to follow their logic regarding the role of ICG use in the macular region as a cause of peripheral visual field defects. Although it is possible ICG is toxic to the optic nerve, this seems unlikely in the absence of a new relative afferent pupillary defect or optic atrophy. In summary, we do not believe that the conclusion of Haritoglou and associates that “ICG type used in our 1194
AMERICAN JOURNAL
patients may affect visual outcome and contribute to the occurrence of postoperative visual field defects” is valid for the reasons discussed herein. We are also not convinced that there are in fact differences between stained and unstained ILM, as they have asserted, or that the cleavage plane is altered. Although they acknowledge that the limitations of their study include the fact that it is a noncomparative study, Haritoglou and coworkers persist in comparing study groups that are not comparable because of the issues enumerated above. ROBERT E. FOSTER, MD CHRISTOPHER D. RIEMANN, MD ANDREA P. DA MATA, MD SCOTT E. BURK, MD, PHD MICHAEL R. PETERSEN, MD, PHD
Cincinnati, Ohio ROBERT H. ROSA, JR., MD
Temple, Texas REFERENCES
1. Haritoglou C, Gandorfer A, Gass CA, et al. Indocyanine green-assisted peeling of the internal limiting membrane in macular hole surgery affects visual outcome: a clinicopathologic correlation. Am J Ophthalmol 2002;134:836 –841. 2. Burk SE, Da Mata AP, Snyder ME, Foster RE. Indocyanine green assisted peeling of the retinal internal-limiting membrane. Ophthalmology 2000;107:2010 –2014. 3. Messmer EM, Heidenkummer HP, Kampik A. Ultrastructure of epiretinal membranes associated with macular holes. Graefes Arch Clin Exp Ophthalmol 1998;236:248 –254. 4. Haritoglou C, Gass CA, Schaumberger M, et al. Macular changes after peeling of the internal limiting membrane in macular hole surgery. Am J Ophthalmol 2001;132:363–368. 5. Liesenhoff O, Messmer EM, Pulur A, Kampik A. Treatment of full-thickness idiopathic macular holes. Der Ophthalmologe 1996;93:655–659. 6. Da Mata AP, Burk SE, Riemann CD, Snyder ME, et al. ICG-assisted peeling of the retinal ILM [Letter]. Ophthalmology 2002;109:1040 –1041. 7. Gass CA, Haritoglou C, Messmer EM, et al. Peripheral visual field defects after macular hole surgery: a complication with decreasing incidence. Br J Ophthalmol 2001;85:549 –551.
AUTHOR REPLY WE THANK DR. FOSTER AND COWORKERS FOR THEIR CRIT-
ical statement concerning our article. We can not agree with their major concerns, however, upon which we comment as follows: First, in their letter they refer to an article from our institution describing ultrastructural findings in epiretinal membranes associated with macular holes.1 Indeed, cellular epiretinal elements were identified as glial cells with characteristics of Mu¨ ller cells. These cells are definitely situated at the vitreal surface of the ILM. On the retinal side of the ILM some tiny cellular elements are present. That corresponds well with a recent report on the presence of such elements in specimens of epiretinal membranes OF
OPHTHALMOLOGY
DECEMBER 2003