CHOROIDAL THICKNESS IN CLINICALLY SIGNIFICANT PSEUDOPHAKIC CYSTOID MACULAR EDEMA DOMINIK ODROBINA, MD, PHD, IWONA LAUDANSKA-OLSZEWSKA, MD, PHD Purpose: To study the choroidal thickness with an enhanced depth imaging spectral domain optical coherence tomography in clinically significant pseudophakic cystoid macular edema (CME). Methods: Twenty patients with CME after uneventful cataract surgery were included. Choroidal thickness was analyzed and measured at various points: subfoveal and 1.5 mm nasal, 1.5 mm temporal, 1.5 mm inferior, and 1.5 mm superior from the center of the fovea. We compare choroidal thickness between affected and fellow eyes. Results: The mean subfoveal choroidal thickness measured in 28 eyes with CME was 229.14 ± 62.61 mm and 280.82 ± 79.09 mm in fellow eyes. At any point (subfoveal, 1,500 mm; nasal, 1,500 mm; temporal, 1,500 mm; inferior, 1,500 mm; 1,500 mm superior from the center of the fovea), the choroidal thickness of the affected eye was significantly (P , 0.01) thinner than that of the fellow eye. Conclusion: The thinner choroid in eyes with CME than in fellow eyes may suggest that the reduced choroidal blood flow in the choriocapillaris is also a possible factor of CME. RETINA 35:136–140, 2015
P
seudophakic cystoid macular edema (CME) can occur after cataract surgery and is the main reason of decreased visual acuity.1–4 The incidence of acute clinically significant CME after uncomplicated cataract surgery was reported by authors as 1% to 2%.5,6 There are many risk factors of macular edema, but the pathogenesis are still uncertain. Many authors postulated that inflammation mediators, especially prostaglandins and cytokines, cause the breakdown of the blood–retinal barrier (BRB).1,3,6 The breakdown of the BRB is directly associated with CME development.7 The mechanical factor, which is vitreoretinal traction, can also cause macular edema.8 However, it seems that there may be other factors that may cause damages to the BRB and macular edema formation. The development in recent years of new imaging methods, namely enhanced depth imaging optical coherence tomography, allows us to more accurately and better illustrate the choroid in vivo.9 As a result, it
was noted that it may play a role in the pathogenesis of many chorioretinal diseases.10–12 Because of a lack of retinal vasculature in the fovea area, changes in the choroid, especially in choriocapillaris, may cause damage to the retinal layers. Properly functioning and normal choroid construction plays a very important role in the proper functioning of the retina. The purpose of this study was to investigate the subfoveal choroidal thickness in the acute symptomatic CME after uncomplicated cataract surgery using enhanced depth imaging optical coherence tomography.
Materials and Methods This is a retrospective observational study of 28 patients with clinically significant pseudophakic CME after uneventful cataract surgery (phacoemulsification and implantation of a foldable intraocular lens). Inclusion criteria were decreased visual acuity or disturbing metamorphopsia after uneventful phacoemulsification because of CME and fellow eye without any ocular surgeries. Patients were excluded if had undergone previous ocular surgery other than uncomplicated cataract surgery in eye with CME and any
From the Ophthalmology Clinic Boni Frates Lodziensis, Łódź, Poland. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Dominik Odrobina, MD, PhD, Ophthalmology Clinic Boni Frates Lodziensis, Al. Hippiczna 36 m.2, Lodz 94-049, Poland; e-mail: [email protected]
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CHOROIDAL THICKNESS IN PSEUDOPHAKIC CME ODROBINA AND LAUDANSKA-OLSZEWSKA
ocular surgeries in the fellow eye or had glaucoma, retinal vascular disorders, diabetes mellitus, macular degeneration, uveitis, and other ocular disorders, myopic refractive error exceeding −6.0 diopters (D), axial length .25 mm, and difference in axial length between the operated eye and the fellow eye in any of the studied patient did not exceed 0.4 mm. We also excluded patients with difference in refractive error .1.0 D between the operated and fellow eye. The patients underwent ophthalmologic examinations, including visual acuity and refraction, intraocular pressure, anterior segment and fundus examination with Volk 78 and 90 lenses (Volk Optical Inc, Mentor, OH), and fluorescein angiography (Spectralis; Heidelberg Engineering, Heidelberg, Germany). Choroidal thickness was measured using enhanced depth imaging optical coherence tomography imaging (Spectralis; Heidelberg Engineering). The choroidal thickness was measured from the outer portion of the hyperreflective line corresponding to the base of retinal pigment epithelium to the margin or hyperreflective line corresponding to chorioscleral interface. In each patient, we performed two horizontal and vertical line scans through the fovea. Choroidal thickness was measured in a horizontal and vertical section beneath the fovea and 1.5 mm nasal, 1.5 mm temporal, 1.5 mm inferior, and 1.5 mm superior from the center of the fovea. The images were taken by one experienced ophthalmologist (D.O.), and the images were measured and analyzed by 2 ophthalmologists (D.O. and I.L.-O.). The results did not differ more than 5 mm and were repeatable (Lin’s concordance correlation coefficient for agreement; P , 0.001 in each investigated area of the choroid, respectively). We have taken an average of these two measurements. Choroidal thickness was measured manually using manual calipers. Enhanced depth imaging optical coherence tomography was performed and analyzed in all patients (28 eyes) with clinically significant
137
pseudophakic CME and in the fellow eyes (28 eyes) without any previous ocular surgery and any diseases. Statistical analyses were performed using the Pearson’s product–moment correlation coefficient and the Wilcoxon’s test. All the statistical procedures were performed by means of Stata 12.1 Special Edition (StataCorp LP, College Station, TX). The significance level was set to be P , 0.05. Results Twenty-eight eyes of 28 patients diagnosed as having clinically significant CME after uneventful phacoemulsification (16 women and 12 men; mean age ± SD, 72.46 ± 9.07 years) were included in this study. The mean logMAR visual acuity in examination data was 1.07 ± 0.77. The mean duration between the cataract surgery and the onset of clinically significant CME was 8.29 ± 2.87 weeks. There were observed statistically significant differences concerning the choroidal thickness (in micrometers) in the examined patients’ operated eyes versus their unaffected fellow eyes (Figure 1). The mean subfoveal choroidal thickness measured in 28 eyes with CME was 229.14 ± 62.61 mm and 280.82 ± 79.09 mm in fellow eyes. At either point (subfoveal, 1,500 mm; nasal, 1,500 mm; temporal, 1,500 mm; inferior, 1,500 mm superior from the center of the fovea), the choroidal thickness of the affected eye was significantly (P , 0.01) thinner than that of the fellow eye. Relevant details are displayed in Table 1. The mean central retinal thickness in the studied patients’ operated eyes amounted to 453.50 mm (SD = 142.79, Q1 = 354.50, median = 413.00, Q3 = 506.00, interquartile range = 151.50 mm) and in their fellow eyes it came to 209.96 mm (SD = 25.63; Q1 = 195.50; median = 205.00; Q3 = 214.00; interquartile range = 18.50 mm).
Fig. 1. Representative case of CME compared with the fellow eye (yellow markings indicate choroidal thickness in each measured area). Enhanced depth imaging optical coherence tomography image of a vertical scan (A) and of a horizontal scan (B) of the eye with CME after uncomplicated cataract surgery. Enhanced depth imaging optical coherence tomography image of a vertical scan (C) and of a horizontal scan (D) of the fellow eye.
138
Patients’ age (years) Duration between cataract surgery and onset of CME (weeks) Visual acuity in the affected eye LogMAR in the affected eye Subfoveal choroidal thickness (mm) Affected eye Fellow eye Choroidal thickness (mm) in a nasal area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in a temporal area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in a superior area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in an inferior area at 1,500 mm from the center of the fovea Affected eye Fellow eye
M
Q1; Me; Q3
IQR
SD
SE
72.46 8.29
64.00; 73.00; 79.00 6.00; 8.00; 10.00
15.00 4.00
9.07 2.87
1.71 0.54
68.95–75.98 7.17–9.40
12.51 34.58
58–92 4–14
0.22 0.7786
0.04 0.34–0.51 0.1471 0.7691–1.3729
52.56 72.70
0.05–0.80 0.2231–2.9957
0.425 0.25; 0.45; 0.60 1.0710 0.5108; 0.8047; 1.4067
0.35 0.8959
95% CI
CV, %
Min.–Max.
229.14 280.82
195.00; 226.00; 262.00 67.00 225.00; 282.00; 326.00 101.00
62.61 79.09
11.83 14.95
204.86–253.42 250.15–311.49
27.32 28.17
124–367 155–459
194.64 232.68
159.50; 196.50; 225.00 190.50; 231.00; 271.00
54.48 71.03
10.30 13.42
173.52–215.77 205.14–260.22
27.99 30.53
93–316 104–398
65.50 80.50
P*
,0.001 ,0.001
0.003 239.93 271.62
206.50; 233.50; 269.50 232.50; 284.50; 309.00
63.00 76.50
57.04 78.28
10.78 14.79
217.81–262.05 241.61–302.32
23.77 28.78
130–361 120–485
230.57 266.18
195.50; 230.50; 288.00 92.50 216.00; 264.50; 335.00 119.00
64.39 80.59
12.17 15.23
205.60–255.54 234.93–297.43
27.93 30.28
121–341 128–408
,0.001
0.009 215.54 242.61
193.00; 211.50; 242.00 49.00 195.00; 240.00; 299.50 104.50
65.44 70.36
12.37 13.30
190.16–240.91 215.33–269.89
30.36 29.00
98–382 124–382
*The Wilcoxon test was performed. CI, 95% confidence interval; CV, coefficient of variation; IQR, interquartile range; M, mean value; Min. minimum; Max., maximum; SD, standard deviation; SE, standard error; Q1; Me; Q3, 25th percentile; 50th percentile (median); and 75th percentile values.
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2015 VOLUME 35 NUMBER 1
Table 1. Descriptive Statistics for Age, Time Between Uneventful Cataract Surgery and Onset of CME, Visual Acuity, LogMAR, and Choroidal Thickness Measurements (mm) in 28 Patients Having Undergone Phacoemulsification in Their Operated Eyes Versus Fellow Eyes
CHOROIDAL THICKNESS IN PSEUDOPHAKIC CME ODROBINA AND LAUDANSKA-OLSZEWSKA
The analyzed duration between the cataract surgery and the onset of CME (weeks) significantly correlated only with visual acuity: r = −0.78 (P = 0.006) and logMAR: r = 0.76 (P , 0.001). Discussion To the best of our knowledge, this is the first study that investigates the choroidal thickness in clinically significant pseudophakic CME. The pathogenesis of the formation of macular edema after uncomplicated cataract surgery is still unclear. It is known that the inflammatory process after cataract surgery is a risk factor and has a significant impact on the formation of the CME. It is also known that inflammatory mediators cause the breakdown of the BRB.1,6,7 It seems, however, that the inflammatory process is not the only factor that causes macular edema after uncomplicated cataract surgery. In this study, the subfoveal choroidal thickness of eyes with CME was significantly thinner (P , 0.001) than that in fellow eyes. The mean subfoveal choroidal thickness measured in eyes with CME was 229.14 ± 62.61 mm compared with 280.82 ± 79.09 mm in fellow eyes. Some authors showed that in patients with diabetic retinopathy, the choroid is also thinner.12,13 We speculated that there are some mechanisms similar to those in diabetic retinopathy. Taking into consideration that decreased blood flow in the choriocapillaris may reduce the transportation of oxygen and nutrients to the retinal pigment epithelium and to the outer nuclear layer, it may also cause retinal hypoxia.14 This may cause the increase of the level of vascular endothelial growth factor (VEGF). The higher level of VEGF also causes the breakdown of the BRB and increased vascular permeability, which contributes to the formation of macular edema. The fact that some authors describe the efficacy of intravitreal anti-VEGF drugs for the treatment of pseudophakic CME may support our hypothesis.15 However, some authors show that anti-VEGF therapy is not effective.16 The mechanism of this entity is composite and for the present moment is not well known. That is why the higher level of VEGF may not be the only factor. Querques et al12 suggested that a decrease of choroidal thickness was due to atrophy and dropout of the choriocapillaris. They have also shown that eyes with nonproliferative diabetic retinopathy and clinically significant macular edema have a thinner choroid compared with eyes without macular edema and diabetic retinopathy. This may suggest that in eyes without macular edema, there is only decreased
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choroidal blood flow without damage of the choriocapillaris. Other authors have also shown that the subfoveal choroid is thinner in diabetic retinopathy and in diabetic macular edema.13,17,18 In the literature, the authors also describe different results. Kim et al19 concluded in their study that choroidal thickness increased significantly with the severity of diabetes retinopathy and decreased in PRP-treated eyes. Similar to these findings, in the article of the Beijing Eye Study, the choroid was thicker in patients with diabetes.20 In our opinion, the differences in the results between the authors can be caused by different methodology and the composite mechanism of diabetic retinopathy. It is also stated that in patients with diabetes, the incidence of CME is more frequent.21 Therefore, reduced choroidal thickness in patients with diabetes and the increased likelihood of CME in these patients may suggest that choroidal blood flow may have an effect on the occurrence of pseudophakic macular edema. In our study, we also found that at either point (subfoveal, 1,500 mm nasal; 1,500 mm temporal; 1,500 mm inferior; 1,500 mm superior from the center of the fovea), the choroidal thickness of the affected eye was significantly (P , 0.01) thinner than that of the fellow eye, and this may also have importance in the pathogenesis of the edema formation. In the majority of patients, CME resolves spontaneously.22 This could mean that the mechanism causing CME is temporary. In our opinion, most cases of pseudophakic CME may be explained by a short-term decrease in choroidal blood flow without atrophy or dropout of the choriocapillaris. There are several limitations to this study. Our study has a small sample size and a lack of data before surgery. Therefore, we cannot definitively determine whether the choroidal thickness decreased after cataract surgery or whether the choroid was thinner before surgery and may affect edema. This data could give us information about choroidal thickness before cataract surgery. Another factor is that it is difficult to identify the choriocapillaris layer, middle layer, and large vascular layer of the choroid by this system. This would help us to determine the thickness of which layer of the choroid has been reduced. In conclusion, our results demonstrated that eyes with clinically significant pseudophakic CME have a thinner choroid compared with the fellow eyes. It is probable that the inflammatory process and mediators play the main role in the development of pseudophakic CME, but the choroidal blood flow in the choriocapillaris is also possible factor of CME.
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Key words: enhanced depth imaging spectral domain optical coherence tomography, choroidal thickness, pseudophakic cystoid macular edema. References 1. Loewenstein A, Zur D. Postsurgical cystoid macular edema. Dev Ophthalmol 2010;47:148–159. 2. Yilmaz T, Cordero-Coma M, Gallagher MJ. Ketorolac therapy for the prevention of acute pseudophakic cystoid macular edema: a systematic review. Eye (Lond) 2012;26:252–258. 3. Rossetti L, Chaudhuri J, Dickersin K. Medical prophylaxis and treatment of cystoid macular edema after cataract surgery. The results of a meta-analysis. Ophthalmology 1998; 105:397–405. 4. Ursell PG, Spalton DJ, Whitcup SM, Nussenblatt RB. Cystoid macular edema after phacoemulsification: relationship to blood-aqueous barrier damage and visual acuity. J Cataract Refract Surg 1999;25:1492–1497. 5. Ray S, D’Amico DJ. Pseudophakic cystoid macular edema. Semin Ophthalmol 2002;17:167–180. 6. Wolf EJ, Braunstein A, Shih C, Braunstein RE. Incidence of visually significant pseudophakic macular edema after uneventful phacoemulsification in patients treated with nepafenac. J Cataract Refract Surg 2007;33:1546–1549. 7. Cunha-Vaz JG, Travassos A. Breakdown of the blood-retinal barriers and cystoid macular edema. Surv Ophthalmol 1984; 28:485–492. 8. Schepens CL, Avila MP, Jalkh AE, et al. The role of vitreous in cystoid macular edema. Surv Ophthalmol 1984;28:499–504. 9. Spaide RF, Koizumi H, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008;146:496–500. 10. Kim SW, Oh J, Kwon SS, et al. Comparison of choroidal thickness among patients with healthy eyes, early age-related maculopathy, neovascular age-related macular degeneration, central serous chorioretinopathy, and polypoidal choroidal vasculopathy. Retina 2011;31:1904–1911. 11. Dhoot DS, Huo S, Yuan A, et al. Evaluation of choroidal thickness in retinitis pigmentosa using enhanced depth
12.
13.
14. 15.
16.
17.
18.
19.
20.
21.
22.
imaging optical coherence tomography. Br J Ophthalmol 2013;97:66–69. Querques G, Lattanzio R, Querques L, et al. Enhanced depth imaging optical coherence tomography in type 2 diabetes. Invest Ophthalmol Vis Sci 2012;53:6017–6024. Esmaeelpour M, Povazay B, Hermann B, et al. Mapping choroidal and retinal thickness variation in type 2 diabetes using three-dimensional 1060-nm optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:5311– 5316. Alm A. Ocular circulation. In: Hart WM, ed. Adler’s Physiol Eye. 9th ed. St. Louis, MO: CV Mosby; 1992:198–227. Barone A, Russo V, Prascina F, Delle Noci N. Short term safety and efficacy of intravitreal bevacizumab for pseudophakic cystoid edema. Retina 2009;29:33–37. Spitzer MS, Ziemssen F, Yoeruek E, et al. Efficacy of intravitreal bevacizumab in treating postoperative pseudophakic cystoid macular edema. J Cataract Refract Surg 2008;34: 70–75. Regatieri CV, Branchini L, Carmody J, et al. Choroidal thickness in patients with diabetic retinopathy analyzed by spectraldomain optical coherence tomography. Retina 2012;32: 563–568. Adhi M, Brewer E, Waheed NK, Duker JS. Analysis of morphological features and vascular layers of choroid in diabetic retinopathy using spectral-domain optical coherence tomography. JAMA Ophthalmol 2013;131:1267–1274. Kim JT, Lee DH, Joe SG, et al Changes in choroidal thickness in relation to the severity of retinopathy and macular edema in type 2 diabetic patients. Invest Ophthalmol Vis Sci 2013;54: 3378–3384. Xu J, Xu L, Du KF, et al. Subfoveal choroidal thickness in diabetes and diabetic retinopathy. Ophthalmology 2013;120: 2023–2028. Pollack A, Leiba H, Bukelman A, Oliver M. Cystoid macular edema following cataract extraction in patients with diabetes. Br J Ophthalmol 1992;76:221–224. Perente I, Utine CA, Ozturker C, et al. Evaluation of macular changes after uncomplicated phacoemulsification surgery by optical coherence tomography. Curr Eye Res 2007;32: 241–247.
P
seudophakic cystoid macular edema (CME) can occur after cataract surgery and is the main reason of decreased visual acuity.1–4 The incidence of acute clinically significant CME after uncomplicated cataract surgery was reported by authors as 1% to 2%.5,6 There are many risk factors of macular edema, but the pathogenesis are still uncertain. Many authors postulated that inflammation mediators, especially prostaglandins and cytokines, cause the breakdown of the blood–retinal barrier (BRB).1,3,6 The breakdown of the BRB is directly associated with CME development.7 The mechanical factor, which is vitreoretinal traction, can also cause macular edema.8 However, it seems that there may be other factors that may cause damages to the BRB and macular edema formation. The development in recent years of new imaging methods, namely enhanced depth imaging optical coherence tomography, allows us to more accurately and better illustrate the choroid in vivo.9 As a result, it
was noted that it may play a role in the pathogenesis of many chorioretinal diseases.10–12 Because of a lack of retinal vasculature in the fovea area, changes in the choroid, especially in choriocapillaris, may cause damage to the retinal layers. Properly functioning and normal choroid construction plays a very important role in the proper functioning of the retina. The purpose of this study was to investigate the subfoveal choroidal thickness in the acute symptomatic CME after uncomplicated cataract surgery using enhanced depth imaging optical coherence tomography.
Materials and Methods This is a retrospective observational study of 28 patients with clinically significant pseudophakic CME after uneventful cataract surgery (phacoemulsification and implantation of a foldable intraocular lens). Inclusion criteria were decreased visual acuity or disturbing metamorphopsia after uneventful phacoemulsification because of CME and fellow eye without any ocular surgeries. Patients were excluded if had undergone previous ocular surgery other than uncomplicated cataract surgery in eye with CME and any
From the Ophthalmology Clinic Boni Frates Lodziensis, Łódź, Poland. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Dominik Odrobina, MD, PhD, Ophthalmology Clinic Boni Frates Lodziensis, Al. Hippiczna 36 m.2, Lodz 94-049, Poland; e-mail: [email protected]
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CHOROIDAL THICKNESS IN PSEUDOPHAKIC CME ODROBINA AND LAUDANSKA-OLSZEWSKA
ocular surgeries in the fellow eye or had glaucoma, retinal vascular disorders, diabetes mellitus, macular degeneration, uveitis, and other ocular disorders, myopic refractive error exceeding −6.0 diopters (D), axial length .25 mm, and difference in axial length between the operated eye and the fellow eye in any of the studied patient did not exceed 0.4 mm. We also excluded patients with difference in refractive error .1.0 D between the operated and fellow eye. The patients underwent ophthalmologic examinations, including visual acuity and refraction, intraocular pressure, anterior segment and fundus examination with Volk 78 and 90 lenses (Volk Optical Inc, Mentor, OH), and fluorescein angiography (Spectralis; Heidelberg Engineering, Heidelberg, Germany). Choroidal thickness was measured using enhanced depth imaging optical coherence tomography imaging (Spectralis; Heidelberg Engineering). The choroidal thickness was measured from the outer portion of the hyperreflective line corresponding to the base of retinal pigment epithelium to the margin or hyperreflective line corresponding to chorioscleral interface. In each patient, we performed two horizontal and vertical line scans through the fovea. Choroidal thickness was measured in a horizontal and vertical section beneath the fovea and 1.5 mm nasal, 1.5 mm temporal, 1.5 mm inferior, and 1.5 mm superior from the center of the fovea. The images were taken by one experienced ophthalmologist (D.O.), and the images were measured and analyzed by 2 ophthalmologists (D.O. and I.L.-O.). The results did not differ more than 5 mm and were repeatable (Lin’s concordance correlation coefficient for agreement; P , 0.001 in each investigated area of the choroid, respectively). We have taken an average of these two measurements. Choroidal thickness was measured manually using manual calipers. Enhanced depth imaging optical coherence tomography was performed and analyzed in all patients (28 eyes) with clinically significant
137
pseudophakic CME and in the fellow eyes (28 eyes) without any previous ocular surgery and any diseases. Statistical analyses were performed using the Pearson’s product–moment correlation coefficient and the Wilcoxon’s test. All the statistical procedures were performed by means of Stata 12.1 Special Edition (StataCorp LP, College Station, TX). The significance level was set to be P , 0.05. Results Twenty-eight eyes of 28 patients diagnosed as having clinically significant CME after uneventful phacoemulsification (16 women and 12 men; mean age ± SD, 72.46 ± 9.07 years) were included in this study. The mean logMAR visual acuity in examination data was 1.07 ± 0.77. The mean duration between the cataract surgery and the onset of clinically significant CME was 8.29 ± 2.87 weeks. There were observed statistically significant differences concerning the choroidal thickness (in micrometers) in the examined patients’ operated eyes versus their unaffected fellow eyes (Figure 1). The mean subfoveal choroidal thickness measured in 28 eyes with CME was 229.14 ± 62.61 mm and 280.82 ± 79.09 mm in fellow eyes. At either point (subfoveal, 1,500 mm; nasal, 1,500 mm; temporal, 1,500 mm; inferior, 1,500 mm superior from the center of the fovea), the choroidal thickness of the affected eye was significantly (P , 0.01) thinner than that of the fellow eye. Relevant details are displayed in Table 1. The mean central retinal thickness in the studied patients’ operated eyes amounted to 453.50 mm (SD = 142.79, Q1 = 354.50, median = 413.00, Q3 = 506.00, interquartile range = 151.50 mm) and in their fellow eyes it came to 209.96 mm (SD = 25.63; Q1 = 195.50; median = 205.00; Q3 = 214.00; interquartile range = 18.50 mm).
Fig. 1. Representative case of CME compared with the fellow eye (yellow markings indicate choroidal thickness in each measured area). Enhanced depth imaging optical coherence tomography image of a vertical scan (A) and of a horizontal scan (B) of the eye with CME after uncomplicated cataract surgery. Enhanced depth imaging optical coherence tomography image of a vertical scan (C) and of a horizontal scan (D) of the fellow eye.
138
Patients’ age (years) Duration between cataract surgery and onset of CME (weeks) Visual acuity in the affected eye LogMAR in the affected eye Subfoveal choroidal thickness (mm) Affected eye Fellow eye Choroidal thickness (mm) in a nasal area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in a temporal area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in a superior area at 1,500 mm from the center of the fovea Affected eye Fellow eye Choroidal thickness (mm) in an inferior area at 1,500 mm from the center of the fovea Affected eye Fellow eye
M
Q1; Me; Q3
IQR
SD
SE
72.46 8.29
64.00; 73.00; 79.00 6.00; 8.00; 10.00
15.00 4.00
9.07 2.87
1.71 0.54
68.95–75.98 7.17–9.40
12.51 34.58
58–92 4–14
0.22 0.7786
0.04 0.34–0.51 0.1471 0.7691–1.3729
52.56 72.70
0.05–0.80 0.2231–2.9957
0.425 0.25; 0.45; 0.60 1.0710 0.5108; 0.8047; 1.4067
0.35 0.8959
95% CI
CV, %
Min.–Max.
229.14 280.82
195.00; 226.00; 262.00 67.00 225.00; 282.00; 326.00 101.00
62.61 79.09
11.83 14.95
204.86–253.42 250.15–311.49
27.32 28.17
124–367 155–459
194.64 232.68
159.50; 196.50; 225.00 190.50; 231.00; 271.00
54.48 71.03
10.30 13.42
173.52–215.77 205.14–260.22
27.99 30.53
93–316 104–398
65.50 80.50
P*
,0.001 ,0.001
0.003 239.93 271.62
206.50; 233.50; 269.50 232.50; 284.50; 309.00
63.00 76.50
57.04 78.28
10.78 14.79
217.81–262.05 241.61–302.32
23.77 28.78
130–361 120–485
230.57 266.18
195.50; 230.50; 288.00 92.50 216.00; 264.50; 335.00 119.00
64.39 80.59
12.17 15.23
205.60–255.54 234.93–297.43
27.93 30.28
121–341 128–408
,0.001
0.009 215.54 242.61
193.00; 211.50; 242.00 49.00 195.00; 240.00; 299.50 104.50
65.44 70.36
12.37 13.30
190.16–240.91 215.33–269.89
30.36 29.00
98–382 124–382
*The Wilcoxon test was performed. CI, 95% confidence interval; CV, coefficient of variation; IQR, interquartile range; M, mean value; Min. minimum; Max., maximum; SD, standard deviation; SE, standard error; Q1; Me; Q3, 25th percentile; 50th percentile (median); and 75th percentile values.
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2015 VOLUME 35 NUMBER 1
Table 1. Descriptive Statistics for Age, Time Between Uneventful Cataract Surgery and Onset of CME, Visual Acuity, LogMAR, and Choroidal Thickness Measurements (mm) in 28 Patients Having Undergone Phacoemulsification in Their Operated Eyes Versus Fellow Eyes
CHOROIDAL THICKNESS IN PSEUDOPHAKIC CME ODROBINA AND LAUDANSKA-OLSZEWSKA
The analyzed duration between the cataract surgery and the onset of CME (weeks) significantly correlated only with visual acuity: r = −0.78 (P = 0.006) and logMAR: r = 0.76 (P , 0.001). Discussion To the best of our knowledge, this is the first study that investigates the choroidal thickness in clinically significant pseudophakic CME. The pathogenesis of the formation of macular edema after uncomplicated cataract surgery is still unclear. It is known that the inflammatory process after cataract surgery is a risk factor and has a significant impact on the formation of the CME. It is also known that inflammatory mediators cause the breakdown of the BRB.1,6,7 It seems, however, that the inflammatory process is not the only factor that causes macular edema after uncomplicated cataract surgery. In this study, the subfoveal choroidal thickness of eyes with CME was significantly thinner (P , 0.001) than that in fellow eyes. The mean subfoveal choroidal thickness measured in eyes with CME was 229.14 ± 62.61 mm compared with 280.82 ± 79.09 mm in fellow eyes. Some authors showed that in patients with diabetic retinopathy, the choroid is also thinner.12,13 We speculated that there are some mechanisms similar to those in diabetic retinopathy. Taking into consideration that decreased blood flow in the choriocapillaris may reduce the transportation of oxygen and nutrients to the retinal pigment epithelium and to the outer nuclear layer, it may also cause retinal hypoxia.14 This may cause the increase of the level of vascular endothelial growth factor (VEGF). The higher level of VEGF also causes the breakdown of the BRB and increased vascular permeability, which contributes to the formation of macular edema. The fact that some authors describe the efficacy of intravitreal anti-VEGF drugs for the treatment of pseudophakic CME may support our hypothesis.15 However, some authors show that anti-VEGF therapy is not effective.16 The mechanism of this entity is composite and for the present moment is not well known. That is why the higher level of VEGF may not be the only factor. Querques et al12 suggested that a decrease of choroidal thickness was due to atrophy and dropout of the choriocapillaris. They have also shown that eyes with nonproliferative diabetic retinopathy and clinically significant macular edema have a thinner choroid compared with eyes without macular edema and diabetic retinopathy. This may suggest that in eyes without macular edema, there is only decreased
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choroidal blood flow without damage of the choriocapillaris. Other authors have also shown that the subfoveal choroid is thinner in diabetic retinopathy and in diabetic macular edema.13,17,18 In the literature, the authors also describe different results. Kim et al19 concluded in their study that choroidal thickness increased significantly with the severity of diabetes retinopathy and decreased in PRP-treated eyes. Similar to these findings, in the article of the Beijing Eye Study, the choroid was thicker in patients with diabetes.20 In our opinion, the differences in the results between the authors can be caused by different methodology and the composite mechanism of diabetic retinopathy. It is also stated that in patients with diabetes, the incidence of CME is more frequent.21 Therefore, reduced choroidal thickness in patients with diabetes and the increased likelihood of CME in these patients may suggest that choroidal blood flow may have an effect on the occurrence of pseudophakic macular edema. In our study, we also found that at either point (subfoveal, 1,500 mm nasal; 1,500 mm temporal; 1,500 mm inferior; 1,500 mm superior from the center of the fovea), the choroidal thickness of the affected eye was significantly (P , 0.01) thinner than that of the fellow eye, and this may also have importance in the pathogenesis of the edema formation. In the majority of patients, CME resolves spontaneously.22 This could mean that the mechanism causing CME is temporary. In our opinion, most cases of pseudophakic CME may be explained by a short-term decrease in choroidal blood flow without atrophy or dropout of the choriocapillaris. There are several limitations to this study. Our study has a small sample size and a lack of data before surgery. Therefore, we cannot definitively determine whether the choroidal thickness decreased after cataract surgery or whether the choroid was thinner before surgery and may affect edema. This data could give us information about choroidal thickness before cataract surgery. Another factor is that it is difficult to identify the choriocapillaris layer, middle layer, and large vascular layer of the choroid by this system. This would help us to determine the thickness of which layer of the choroid has been reduced. In conclusion, our results demonstrated that eyes with clinically significant pseudophakic CME have a thinner choroid compared with the fellow eyes. It is probable that the inflammatory process and mediators play the main role in the development of pseudophakic CME, but the choroidal blood flow in the choriocapillaris is also possible factor of CME.
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