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Long-term increase in subfoveal choroidal thickness after surgery for senile cataracts
PII: S0002-9394(14)00287-6
DOI: 10.1016/j.ajo.2014.05.016
Reference: AJOPHT 8922
Please cite this article as: Noda, Y, Ogawa, A, Toyama, T, Ueta T, Long-term increase in subfoveal
choroidal thickness after surgery for senile cataracts, American Journal of Ophthalmology (2014), doi:
10.1016/j.ajo.2014.05.016.
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Yasuo Noda,1 Asako Ogawa,1 Taku Toyama,1 Takashi Ueta1
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Department of Ophthalmology, University of Tokyo School of Medicine, 7-3-1
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Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
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Ophthalmology, University of Tokyo School of Medicine, 7-3-1 Hongo,
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Bunkyo-ku, Tokyo, 113-8655, Japan. Fax; +81-3-3817-0798. Tel:
+81-3-3815-5411. E-mail address: ueta-tky@umin.ac.jp
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ABSTRACT
PURPOSE: To evaluate the impact of cataract surgery on subfoveal choroidal
thickness and central retinal thickness in the elderly.
DESIGN: Prospective observational case series.
METHODS: This cohort study included 29 eyes of 29 patients with senile
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cataract, but no previous ocular surgery or other ocular abnormality. All 29 eyes
received standard surgery by phacoemulsification and intraocular lens
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implantation. Subfoveal choroidal thickness and central retinal thickness were
measured at baseline, and 1, 3, and 6 months postoperatively by spectral
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domain optical coherence tomography. Multiple regression analysis was
conducted to identify predictors of larger changes in subfoveal choroidal
thickness, including gender, age, baseline choroidal thickness, axial length,
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refractive status before surgery, and duration of surgery.
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RESULTS: The 29 patients with senile cataract received cataract surgery without
complication. Mean subfoveal choroidal thickness was 193.8, 208.9, 210.2, and
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6 months after surgery. Multiple regression analysis revealed that male gender
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cataract surgery.
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INTRODUCTION
Recent advances of enhanced depth imaging (EDI) using a spectral domain
optical coherence tomography (SD-OCT) enables the observation of the
choroid1,2 with sufficient intra- and inter-observer agreement.3,4 SD-OCT has
revealed the importance of the change in choroidal thickness in numerous retinal
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and choroidal disorders including central serous chorioretinopahthy,5,6
age-related macular degeneration (AMD)7,8 and diabetic retinopathy,9,10 but also
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physiological conditions including age,11 gender,11 axial length,11 refractive
status11 and circadian change.12,13
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Surgery for senile cataract is one of the most commonly performed ophthalmic
surgeries with significant importance for quality of vision in the elderly.
Pseudophakic macular edema or Irvine-Gass syndrome is the well-know
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influence of cataract surgery on the retina though its pathogenesis has not been
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fully understood. Recently, retinal thickening after cataract surgery has been
reported even in the healthy eyes without definite morphologic change on
SD-OCT.14 Considering the close relationship between the retina and the
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imaging, 29 eyes of 29 consecutive patients were entered in this study. If both
eyes were operated for their cataract during the study period, the first eyes were
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included for analysis. Exclusion criteria were eyes with histories of ocular
diseases including diabetic retinopathy, early or late AMD, retinal vein occlusion,
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uveitis or other vascular and inflammatory retinal disorders. The evaluated eyes
of the included patients should not have a history of prior ocular surgery for the
entry to this study.
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All examinations were conducted at the Department of Ophthalmology,
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University of Tokyo Hospital. BCVA and Spectralis SD-OCT (Heidelberg
Engineering Inc, Dossenheim, Germany) examinations and biomicroscopy were
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Cataract surgery
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surgeries were performed using INFINITI Vision System (Alcon Inc, Fort Worth,
US). After the phacoemulsification, the blue light-filtering IOL was implanted in
the bag. Complications including posterior capsule rupture, vitreous loss, and
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prolapse through the wound or iris trauma were exclusion criteria although no
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the choroidal thickness shows circadian change,12,13 the patients were
scheduled to be examined at the same time at each visit (within 1 o’clock hour
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difference). In the Spectralis SD-OCT, a previously tracked image could be used
as a reference to obtain new images at the same point of the fundus at each visit.
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6 mm horizontal section running through the center of the fovea with a quality
score ≥ 25 was selected. The subfoveal choroidal thickness was measured
manually using the Heidelberg Eye Explorer software (version 5.4; Heidelberg
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Engineering Co.). Two masked independent observers measured subfoveal
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choroidal thickness perpendicularly from the outer edge of the hyper-reflective
retinal pigment epithelium (RPE) to the inner sclera at the fovea by using
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Statistics
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Changes in the subfoveal choroidal thickness and central retinal thickness after
cataract surgery were analyzed by repeated measures ANOVA and Bonferroni’s
post-test. Peak postoperative values were compared to the baseline by paired
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t-test. The magnitude of the change from baseline to the peak was analyzed with
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RESULTS
29 eyes of the 29 patients with senile cataract were included. Mean ± SD age of
the patients was 73.0 ± 7.2 years old and 14 patients were male. Mean ± SD
axial length was 23.6 ± 1.35 mm, and axial length in 5 eyes was more than 25
mm. All patients fulfilled the evaluation visits at baseline and after surgery.
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There was no complication in the post-operative course of all the patients. By
1 month postoperatively the inflammation indicated by cells or flare in the
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anterior chamber on slit-lamp microscopy disappeared in all the patients. No
cystoid macular edema or subretinal fluid developed which was evaluated by
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SD-OCT. We also confirmed a favorable interobserver agreement to measure
subfoveal choroidal thickness on the OCT at baseline (Pearson correlation =
0.948, P < 0.0001).
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The mean central retinal thickness of the 29 eyes at baseline, and
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postoperative1, 3, and 6 months were 222.7, 230.8, 225.9, and 224.7 µm,
respectively (Figure 1). Repeated measures ANOVA did not indicate a statistical
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significance (P = 0.468). Bonferroni’s post test also did not show statistical
significance for the tendency of the increased central retinal thickness at 1
month (P = 0.165), 3 months (P = 0.569), and 6 months (P = 0.659)
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postoperatively.
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not reveal a problem (P = 0.862), and consistent with this, sphericity adjustments
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comprised age, gender, baseline choroidal thickness, axial length, refractive
status before surgery, and the duration of surgery. The multiple regression
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analysis revealed that thicker baseline choroid (P = 0.0048) and male gender (P
= 0.014) were significantly associated with larger amplitude of the increase in
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subfoveal choroidal thickness after cataract surgery.
Lastly, we evaluated when the increased subfoveal choroidal thickness could
return to the baseline thickness. If “returning to the baseline thickness” is defined
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as within ± 3µm thickness of the baseline, 3 (10.3%) and 6 (20.7%) eyes
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returned to the baseline at 3 and 6 months, respectively. In the other 20 (69.0%)
eyes, their subfoveal choroidal thickness was still thicker than the baseline at 6
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months.
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DICUSSION
The results of the present study indicate that cataract surgery could increase the
choroidal thickness in the elderly population. Our results support a recent report
by Ohsugi et al.21 that reported a significant increase in choroidal thickness after
cataract surgery. In contrast, the other report evaluating 14 patients up to 1
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month did not found significant change in choroidal thickness after surgery.22
Both of the previous studies21,22 as well as this study used EDI mode of
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Spectralis SD-OCT for evaluating choroidal thickness. In the present study, we
carefully evaluated the change in choroidal thickness by conducting OCT at the
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same timing of the day and evaluating the change in both central retinal
thickness and subfoveal choroidal thickness.
We observed a tendency of the increased central retinal thickness at 1 month
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postoperatively, although it did not reach statistical significance. In contrast, we
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observed an increase in subfoveal choroidal thickness for longer period of time,
and even at 6 months postoperatively subfoveal choroidal thickness did not
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status before surgery did not influence the magnitude of change in the subfoveal
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choroidal thickness. The specific role of gender for the change in the subfoveal
choroidal thickness needs to be studied.
The mechanism for the increase in the choroidal thickness after cataract
surgery has not been clear. A speculation is that it may be related to the
postoperative inflammation because pro-inflammatory prostaglandins and
cytokines are considered to explain the macular edema after cataract
surgery,23,24 and inflammatory disorders are also known to increase the
choroidal thickness.25,26 However, inflammation might not be able to explain why
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Our results that surgery for senile cataract affects the choroidal vasculature
could be of interest from the viewpoint of the potential association between
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cataract surgery and late AMD that has been in debate.15–20 In Beaver Dam and
Blue Mountains eye studies, cataract surgery was associated with the increased
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incidence of late AMD, especially neovascular AMD.17–19 In contrast, in
Age-Related Eye Disease Study (AREDS)20 there was no significant increase in
the incidence of late AMD after cataract surgery. As for the influence of cataract
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surgery on pre-existing AMD, recent review of literature showed that there has
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not been sufficient evidence to obtain a conclusion,16 although cataract surgery
improves visual acuity of patients with late AMD in general.29,30 The present
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study revealed that cataract surgery influences the choroid after surgery and it
persists as long as 6 months postoperatively, however, whether the influence
has pathogenic role or not needs further research in the future.
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An important limitation of this study is that we could not confirm whether and
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when the increased subfoveal choroidal thickness can return to the baseline.
Although we observed subfoveal choroidal thickness for 6 months
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ACKNOWLEDGMENT
Funding/Support; none
Financial disclosures; none
Contribution of authors; Concept and design (YN,TU), data acquisition (YN, AO,
TU, TT), analysis and interpretation of data (YN, AO, TU), drafting of manuscript
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(YN, TT), critical revision for important intellectual content (TU).
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REFERENCES
1. Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging
spectral-domain optical coherence tomography. Am J Ophthalmol
2008;146(4):496–500.
2. Margolis R, Spaide RF. A pilot study of enhanced depth imaging optical
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coherence tomography of the choroid in normal eyes. Am J Ophthalmol
2009;147(5):811–815.
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3. Branchini L, Regatieri CV, Flores-Moreno I, Baumann B, Fujimoto JG, Duker
JS. Reproducibility of choroidal thickness measurements across three spectral
SC
domain optical coherence tomography systems. Ophthalmology
2012;119(1):119–123.
4. Shao L, Xu L, Chen CX, et al. Reproducibility of subfoveal choroidal thickness
U
measurements with enhanced depth imaging by spectral-domain optical
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coherence tomography. Invest Ophthalmol Vis Sci 2013;54(1):230–233.
5. Maruko I, Iida T, Sugano Y, Ojima A, Ogasawara M, Spaide RF. Subfoveal
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Retina 2009;29(10):1469–73.
7. Chung SE, Kang SW, Lee JH, Kim YT. Choroidal thickness in polypoidal
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12. Tan CS, Ouyang Y, Ruiz H, Sadda SR. Diurnal variation of choroidal
thickness in normal, healthy subjects measured by spectral domain optical
coherence tomography.
Invest Ophthalmol Vis Sci 2012;53(1):261–266.
13. Usui S, Ikuno Y, Akiba M, et al. Circadian changes in subfoveal choroidal
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thickness and the relationship with circulatory factors in healthy subjects. Invest
Ophthalmol Vis Sci 2012;53(4):2300–2307.
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14. Mylonas G, Sacu S, Deák G, et al; Macula Study Group Vienna. Macular
edema following cataract surgery in eyes with previous 23-gauge vitrectomy and
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peeling of the internal limiting membrane. Am J Ophthalmol
2013;155(2):253–259.e2.
15. Wang JJ, Fong CS, Rochtchina E, et al. Risk of age-related macular
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degeneration 3 years after cataract surgery: paired eye comparisons.
AN
Ophthalmology 2012;119(11):2298–2303.
16. Casparis H, Lindsley K, Kuo IC, Sikder S, Bressler NB. Surgery for cataracts
M
18. Cugati S, Mitchell P, Rochtchina E, Tan AG, Smith W, Wang JJ. Cataract
surgery and the 10-year incidence of age-related maculopathy: the Blue
Mountains Eye Study. Ophthalmology 2006;113(11):2020–2025.
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19. Wang JJ, Klein R, Smith W, Klein BE, Tomany S, Mitchell P. Cataract surgery
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nonsteroidal anti-inflammatory agent. Expert Opin Pharmacother.
2009;10(14):2379–2385.
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24. Xu H, Chen M, Forrester JV, Lois N. Cataract surgery induces retinal
pro-inflammatory gene expression and protein secretion. Invest Ophthalmol Vis
SC
Sci 2011;52(1):249–255.
25. Nakayama M, Keino H, Okada AA, et al. Enhanced depth imaging optical
coherence tomography of the choroid in Vogt-Koyanagi-Harada disease. Retina
2012;32(10):2061–2069.
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26. Aoyagi R, Hayashi T, Masai A, et al. Subfoveal choroidal thickness in
multiple evanescent white dot syndrome. Clin Exp Optom 2012;95(2):212–217.
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27. Arany Z1, Foo SY, Ma Y, et al. HIF-independent regulation of VEGF and
angiogenesis by the transcriptional coactivator PGC-1alpha. Nature
2008;451(7181):1008–1012.
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age-related macular degeneration: age-related eye disease study report no. 27.
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Ophthalmology 2009;116(11):2093–2100.
30. Rosenfeld PJ, Shapiro H, Ehrlich JS, Wong P; MARINA and ANCHOR Study
Groups. Cataract surgery in ranibizumab-treated patients with neovascular
age-related macular degeneration from the phase 3 ANCHOR and MARINA
trials. Am J Ophthalmol 2011;152(5):793–798.
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FIGURE LEGENDS
Figure 1. Time course of subfoveal retinal (left) and choroidal (right) thickness
before (i.e., baseline) and after cataract surgery. Repeated measures ANOVA for
retinal change was not significant (P = 0.468). In contrast, repeated measures
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ANOVA for choroidal change indicated a statistical significance (P < 0.0001).
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Figure 2. An example case of the increased choroidal thickness after surgery for
senile cataract.
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Table 1. Results of multiple regression analysis for the increase in choroidal thickness
after cataract surgery.
Estimated coefficient (95% CI) P value
Male 6.75 (1.50–12.0)* 0.014
Age (years old) 0.24 (-0.54–1.02) 0.53
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Refractive status (diopter) 0.43 (-1.49–2.35) 0.88
Axial length (mm) -1.99 (-7.20–3.21) 0.25
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Baseline choroidal thickness (µm) 0.094 (0.032–0.16) 0.0048
The duration of surgery (min) -0.13 (-0.55–0.29) 0.53
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*The value is odds ratio vs. female
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Dr. Yasuo Noda, M.D. graduated from The University of Tokyo School of
Medicine in 1997. Dr. Noda is currently serving as a director of vitreoretinal
surgery in the Department of Opthalmology, The University of Tokyo
Hospital.
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