Journal of Pediatric Ophthalmology and Strabismus

Original Article 

Macular Thickness Following Strabismus Surgery as Determined by Optical Coherence Tomography

Hilla Reiss Mintz, MD; Michael Waisbourd, MD; Rivka Kessner, MD; Chaim Stolovitch, MD; Gad Dotan, MD; Meira Neudorfer, MD

Abstract

Purpose:

To investigate macular changes following strabismus surgery by using optical coherence tomography (OCT).

Methods:

The authors prospectively evaluated 60 eyes of 30 patients undergoing unilateral extraocular muscle surgery. OCT measurements employing the fast macular thickness mapping protocol were performed 1 day prior to surgery and 1 day postoperatively. Postoperative macular changes in the study eye that was operated on (n = 30) were compared with the fellow control eye (n = 30, controls).

Results:

There was an increase in mean ± standard deviation central foveal thickness (CFT) in the operated eyes, from 201.63 ± 18.36 µm at baseline to 206.03 ± 22.73 µm postoperatively (P = .024). Preoperative and postoperative perifoveal outer temporal quadrant thicknesses were 220.10 ± 16.23 and 225.80 ± 14.78 µm, respectively (P = .009). There were no differences between preoperative and postoperative retinal thickness measurements for all measured areas in the control eyes. Eyes that underwent surgery involving the rectus muscles showed a trend toward a greater CFT increase compared with eyes that had oblique muscle surgery (P = .070).

Conclusions:

The authors found subclinical increases in the foveal and perifoveal macular thicknesses following extraocular muscle surgery. These findings could be attributed to change in the mechanical forces caused by the new position of the extraocular muscles and transmitted via the sclera or, alternatively, to postoperative inflammation and alterations in the blood–retinal barrier. The clinical implications of these findings remain to be clarified.

[J Pediatr Ophthalmol Strabismus. 2016;53(1):11-15.]

Abstract

Purpose:

To investigate macular changes following strabismus surgery by using optical coherence tomography (OCT).

Methods:

The authors prospectively evaluated 60 eyes of 30 patients undergoing unilateral extraocular muscle surgery. OCT measurements employing the fast macular thickness mapping protocol were performed 1 day prior to surgery and 1 day postoperatively. Postoperative macular changes in the study eye that was operated on (n = 30) were compared with the fellow control eye (n = 30, controls).

Results:

There was an increase in mean ± standard deviation central foveal thickness (CFT) in the operated eyes, from 201.63 ± 18.36 µm at baseline to 206.03 ± 22.73 µm postoperatively (P = .024). Preoperative and postoperative perifoveal outer temporal quadrant thicknesses were 220.10 ± 16.23 and 225.80 ± 14.78 µm, respectively (P = .009). There were no differences between preoperative and postoperative retinal thickness measurements for all measured areas in the control eyes. Eyes that underwent surgery involving the rectus muscles showed a trend toward a greater CFT increase compared with eyes that had oblique muscle surgery (P = .070).

Conclusions:

The authors found subclinical increases in the foveal and perifoveal macular thicknesses following extraocular muscle surgery. These findings could be attributed to change in the mechanical forces caused by the new position of the extraocular muscles and transmitted via the sclera or, alternatively, to postoperative inflammation and alterations in the blood–retinal barrier. The clinical implications of these findings remain to be clarified.

[J Pediatr Ophthalmol Strabismus. 2016;53(1):11-15.]

Introduction

Strabismus surgery is associated with both structural and functional ocular alterations. It is well established that corneal curvature changes following surgery may affect refraction.1–6 Postoperative anterior chamber volume reduction,7–9 hemodynamic changes in the ophthalmic artery,10 and cystoid macular edema have also been described.11

Intraocular surgery (eg, cataract extraction or retinal detachment repair) and other pathologic conditions (eg, intraocular inflammation and retinal vascular occlusion) may result in changes in the macular structure.12–17 However, little is known about macular changes following strabismus surgery. Kasem and Sabry did not find significant macular changes after inferior oblique myectomy or anterior transposition.18 Turan-Vural et al. demonstrated an increase in macular thickness following inferior oblique muscle surgery, but there were no changes in macular measurements after horizontal muscle surgery alone.19

Optical coherence tomography (OCT) has the diagnostic capability of detecting subclinical postoperative macular changes.12–17 Its resolution is one to two orders of magnitude higher than that of other clinical imaging technologies, such as ultrasound, magnetic resonance imaging, or computed tomography.20

The aim of this study was to determine whether strabismus surgery is associated with changes in macular thickness as detected by OCT.

Patients and Methods

The Institutional Review Board of the Tel-Aviv Medical Center approved the study procedures. The study was conducted in accordance with the tenets of the Declaration of Helsinki and written informed consent was obtained from all participants or their surrogates. Consecutive patients scheduled for an elective unilateral extraocular muscle surgery (rectus or oblique) were enrolled. Exclusion criteria were: combined rectus and oblique surgery, bilateral surgery, any ocular pathology other than strabismus, and inability to complete a macular OCT examination 1 day preoperatively and 1 day postoperatively for any reason, including poor cooperation and cognitive impairment.

The patients underwent unilateral strabismus surgery (resection and/or recession) of the rectus or oblique muscles according to individual clinical indications. They were examined and operated on by one of the Department of Ophthalmology's two pediatric ophthalmologists (CS or GD).

A detailed medical and ocular history was obtained preoperatively. A comprehensive ophthalmological examination, including visual acuity, slit-lamp examination, and bilateral OCT macular imaging, was performed 1 day prior to the surgery and 1 day postoperatively. Both of the examinations were performed during the same time of the day (ie, between 09:00 and 11:00 hours). During baseline OCT examination, the examiner was masked to the type and laterality of the procedure to be performed.

The pupil of each eye was dilated with tropicamide 0.5% eye drops 30 minutes prior to the OCT scanning (Stratus OCT, software version 4.0; Carl Zeiss Meditec, Dublin, CA).

All scans were done using an internal fixation target of the OCT device. Fast macular thickness mapping protocol was used for retinal thickness assessment. This protocol is designed to map retinal thickness with six radial line scans, each 6 mm in length and centered on the fovea. Data were collected for 1.92 seconds.21,22 The fast macular thickness mapping protocol is much quicker than the standard macular thickness mapping protocol and therefore especially useful with patients who have difficulty maintaining fixation, such as younger children. The retinal map was divided into the nine areas of the Early Treatment Diabetic Retinopathy Study (ETDRS): minimal foveal thickness, a central 1-mm disc area, and two peripheral ring areas with diameters of 3 and 6 mm divided into four quadrants (superior, temporal, inferior, and nasal) centered on the fovea (Figure 1).23,24 The macular thickness volume was also measured.

The nine Early Treatment Diabetic Retinopathy Study (ETDRS) areas.

Figure 1.

The nine Early Treatment Diabetic Retinopathy Study (ETDRS) areas.

For statistical analyses, all measured parameters were generated automatically. We conducted two analyses, using the t test in both cases. One analysis was a comparison between the preoperative and postoperative macular thickness parameters of all operated and control eyes. The other analysis was a comparison between the change in macular thickness (calculated as the postoperative minus the preoperative macular thickness) of the patients who underwent rectus or oblique muscle surgeries. Possible confounders were assessed by a paired comparison between the study eye and its fellow control eye. The statistical analysis was performed using SPSS for Windows software (version 15.0; SPSS, Inc., Chicago, IL) A P value less than .05 was considered statistically significant.

Results

Sixty eyes of 30 patients (14 females and 16 males; mean age ± standard deviation: 28.9 ± 14.2 years; range: 6 to 62 years) were included in our analysis. All patients underwent unilateral, extraocular muscle surgery. The rectus muscles were operated on in 23 eyes (2 lateral rectus recession, 17 lateral rectus recession combined with medial rectus resection, 2 medial rectus recession combined with lateral rectus resection, 1 medial rectus resection combined with lateral rectus myotomy, 1 superior rectus recession) and the oblique muscles were operated on in 7 eyes (all inferior oblique recession). The demographic and clinical characteristics of the study patients are summarized in Table 1.

Demographic and Clinical Characteristics of the Patients (N = 30)

Table 1:

Demographic and Clinical Characteristics of the Patients (N = 30)

The mean ± standard deviation central foveal thickness (CFT) for the 30 study eyes increased from 201.63 ± 18.36 µm preoperatively to 206.03 ± 22.73 µm postoperatively (P = .024). The outer temporal thickness increased from 220.10 ± 16.23 µm preoperatively to 225.80 ± 14.78 µm postoperatively (P = .009). There were no significant differences in any of the other quadrants (Table 2), and no differences between the preoperative and postoperative retinal thickness measurements of the 30 control eyes.

Comparison Between Preoperative and Postoperative Macular Thickness and Volume

Table 2:

Comparison Between Preoperative and Postoperative Macular Thickness and Volume

Comparison of the two types of surgeries revealed a trend toward a significant increase in the mean CFT following rectus muscle surgery (5.82 ± 11.27 µm) compared with the oblique muscle surgery (0.50 ± 4.17 µm) (P = .07) (Figure 2). There were no differences between the two types of surgery in other macular areas of the study eyes (Table 3).

Postoperative changes in central foveal thickness (CFT): oblique (n = 7) versus rectus (n = 23) muscle surgeries.

Figure 2.

Postoperative changes in central foveal thickness (CFT): oblique (n = 7) versus rectus (n = 23) muscle surgeries.

Comparison Between Macular Thickness Changes in Rectus Versus Oblique Muscle Surgeries

Table 3:

Comparison Between Macular Thickness Changes in Rectus Versus Oblique Muscle Surgeries

There was a difference in the perifoveal inner inferior quadrant in the control eyes. Specifically, there was a minor thickening following oblique muscle surgery and a thinning after rectus muscle surgery (P = .043). No differences were found in the other macular areas.

Discussion

The results of this study demonstrated an asymptomatic increase in foveal and perifoveal thickness following extraocular muscle surgery. The pathogenesis of the macular changes we observed could be explained either mechanically or biomechanically. The change in the mechanical forces caused by the new position of the extraocular muscles and transmitted via the sclera has been reported to cause changes in refraction due to its effect on the cornea.1–7 The alterations can also be explained biomechanically as a transient, local inflammation secondary to the traumatic intervention, even though the retina was not directly involved. The inflammation might cause a breakdown in the blood–aqueous and blood–retinal barriers and increase vascular permeability. This is similar to the effects of inflammation caused by orbital trauma and intraocular surgery.25

OCT is an accurate tool for early diagnosis, analysis, and monitoring of retinopathy. Its high repeatability and resolution have been demonstrated in several studies.23,26 It allows for qualitative diagnosis of diabetic macular edema and for quantitative assessment of edema. OCT can detect retinal thickening in the absence of any abnormality found by slit-lamp examination and demonstrate the presence of diabetic macular edema even if it is not detected by angiography. The greatest sensitivity of OCT is in detecting subtle changes in retinal thickness, which is expected in the central area more than in the peripheral areas. This is due to the OCT mapping protocol, which consists of six radial tomograms performed in a spoke pattern centered on the fovea. This has the advantage of concentrating measurements in the central fovea. Loss of foveal depression attributed to diabetic macular edema has been previously demonstrated by OCT.23 Therefore, it is reasonable to assume that retinal changes following strabismus surgery are most likely to be detected in the foveal region, as shown in the current study.

There is a direct correlation between foveal thickening and loss of visual acuity.26–28 In the current study, patients underwent a complete ophthalmological examination including visual acuity testing, both preoperatively and postoperatively, but no clinical changes were detected. Therefore, we concluded that any changes that might have taken place were subclinical.

We also observed a trend toward a greater foveal thickening following rectus muscle surgery compared to oblique muscle surgery. This finding might be attributed to the different mechanical pressures during and after the two types of surgery. An additional and unexpected finding was the postoperative changes in the perifoveal inner inferior quadrant in the control eyes (ie, thickening after oblique muscle surgery and thinning after rectus muscle surgery). We believe that this was a random finding resulting from the small subgroups of patients.

There are currently only two reported investigations of the macular changes following strabismus surgery as seen on OCT. Kasem and Sabry emphasized the traction on the inferior oblique muscle insertion during surgery and the close anatomical relation to the macula, but they reported no significant macular changes after inferior oblique surgery.18 Turan-Vural et al. showed an increase in macular thickness following inferior oblique muscle recession surgery (with or without horizontal muscle surgery), but no change in macular thickness after horizontal muscle surgery alone.19 They attributed those changes mainly to the traumatic effect of the surgery.

Our study has several limitations, including the small sample size, the objectively difficult conditions for performing the examination (eg, 1 day postoperatively and young age of some of the patients), and the short follow-up period. Moreover, changes in macular thickness before and after rectus muscle surgery were relatively small (5 to 6 microns) and could have been influenced by OCT test–retest variability. Finally, the use of topical medications at the end of the surgery could have been a confounding factor.

OCT technology enabled us to detect subclinical macular thickening following strabismus surgery, mostly in the foveal region. Long-term follow-up studies are warranted to investigate the clinical implications of these findings and whether these macular changes are reversible.

References

  1. Snir M, Nissenkorn I, Buckman G, Cohen S, Ben-Sira I. Postoperative refractive changes in children with congenital esotropia: a preliminary study. Ophthalmic Surg. 1989;20:57–62.
  2. Denis D, Bardot J, Volot F, Saracco JB, Maumenee IH. Effects of strabismus surgery on refraction in children. Ophthalmologica. 1995;209:136–140. doi:10.1159/000310599 [CrossRef]
  3. Preslan MW, Cioffi G, Min YI. Refractive error changes following strabismus surgery. J Pediatr Ophthalmol Strabismus. 1992;29:300–304.
  4. Hainsworth DP, Bierly JR, Schmeisser ET, Baker RS. Corneal topographic changes after extraocular muscle surgery. J AAPOS. 1999;3:80–86. doi:10.1016/S1091-8531(99)70074-1 [CrossRef]
  5. Kwitko S, Feldon S, McDonnell PJ. Corneal topographic changes following strabismus surgery in Grave's disease. Cornea. 1992;11:36–40. doi:10.1097/00003226-199201000-00005 [CrossRef]
  6. Killer HE, Bähler A. Significant immediate and long-term reduction of astigmatism after lateral rectus recession in divergent Duane's syndrome. Ophthalmologica. 1999;213:209–210. doi:10.1159/000027422 [CrossRef]
  7. Emre S, Çankaya C, Demirel S, Doganay S. Comparison of preoperative and postoperative anterior segment measurements with Pentacam in horizontal muscle surgery. Eur J Ophthalmol. 2008;18:7–12.
  8. Jung JH, Choi HY. Comparison of preoperative and postoperative anterior segment measurements with Pentacam in strabismus surgery. J Pediatr Ophthalmol Strabismus. 2012;49:290–294. doi:10.3928/01913913-20120501-02 [CrossRef]
  9. Noh JH, Park KH, Lee JY, Jung MS, Kim SY. Changes in refractive error and anterior segment parameters after isolated lateral rectus muscle recession. J AAPOS. 2013;17:291–295. doi:10.1016/j.jaapos.2013.03.012 [CrossRef]
  10. Pelit A, Barutçu Ö, Oto S, Aydin P. Investigation of hemodynamic changes after strabismus surgery using color Doppler imaging. J AAPOS. 2002;6:224–227. doi:10.1067/mpa.2002.124901 [CrossRef]
  11. Mohney BG, Agarwal S. Cystoid macular edema following extraocular muscle surgery. J AAPOS. 2002;6:120–122. doi:10.1067/mpa.2002.121615 [CrossRef]
  12. von Jagow B, Ohrloff C, Kohnen T. Macular thickness after uneventful cataract surgery determined by optical coherence tomography. Graefes Arch Clin Exp Ophthalmol. 2007;254:1765–1771. doi:10.1007/s00417-007-0605-6 [CrossRef]
  13. Benson SE, Schlottmann PG, Bunce C, Xing W, Charteris DG. Optical coherence tomography analysis of the macula after scleral buckle surgery for retinal detachment. Ophthalmology. 2007;114:108–112. doi:10.1016/j.ophtha.2006.07.022 [CrossRef]
  14. Benson SE, Schlottmann PG, Bunce C, Xing W, Charteris DG. Optical coherence tomography analysis of the macula after vitrectomy surgery for retinal detachment. Ophthalmology. 2006;113:1179–1183. doi:10.1016/j.ophtha.2006.01.039 [CrossRef]
  15. Johansson M, Lundberg B, Behndig A. Optical coherence tomography evaluation of macular edema after phacoemulsification surgery with intracameral mydriatics. J Cataract Refract Surg. 2007;33:1436–1441. doi:10.1016/j.jcrs.2007.04.027 [CrossRef]
  16. Kim SJ, Equi R, Bressler NM. Analysis of macular edema after cataract surgery in patients with diabetes using optical coherence tomography. Ophthalmology. 2007;114:881–889. doi:10.1016/j.ophtha.2006.08.053 [CrossRef]
  17. Grewing R, Becker H. Retinal thickness immediately after cataract surgery measured by optical coherence tomography. Ophthalmic Surg Lasers. 2000;31:215–217.
  18. Kasem MA, Sabry D. Detection of macular changes by optical coherence tomography after inferior oblique muscle surgery. J AAPOS. 2011;15:334–337. doi:10.1016/j.jaapos.2011.07.003 [CrossRef]
  19. Turan-Vural E, Unlu C, Erdogan G, Aykut A, Bayramlar H, Atmaca F. Evaluation of macular thickness change after inferior oblique muscle recession surgery. Indian J Ophthalmol. 2014;62:715–718. doi:10.4103/0301-4738.136230 [CrossRef]
  20. Brezinski ME, Tearney GJ, Bouma BE, et al. Optical coherence tomography for optical biopsy properties and demonstration of vascular pathology. Circulation. 1996;93:1206–1213. doi:10.1161/01.CIR.93.6.1206 [CrossRef]
  21. Hajali M, Fishman GA, Anderson RJ. The prevalence of cystoid macular oedema in retinitis pigmentosa patients determined by optical coherence tomography. Br J Ophthalmol. 2008;92:1065–1068. doi:10.1136/bjo.2008.138560 [CrossRef]
  22. Hammer DX, Ferguson RD, Iftimia NV, Ustun T. Advanced scanning methods with tracking optical coherence tomography. Opt Express. 2005;13:7937–7947. doi:10.1364/OPEX.13.007937 [CrossRef]
  23. Massin P, Girach A, Erginay A, Gaudric A. Optical coherence tomography: a key to the future management of patients with diabetic macular oedema. Acta Ophthalmol Scand. 2006;84:466–474. doi:10.1111/j.1600-0420.2006.00694.x [CrossRef]
  24. Moura FC, Costa-Cunha LV, Malta RF, Monteiro ML. Relationship between visual field sensitivity loss and quadrantic macular thickness measured with Stratus-optical coherence tomography in patients with chiasmal syndrome. Arq Bras Oftalmol. 2010;73:409–413. doi:10.1590/S0004-27492010000500004 [CrossRef]
  25. Miyake K, Ibaraki N. Prostaglandins and cystoid macular edema. Surv Ophthalmol. 2002;47:203–216. doi:10.1016/S0039-6257(02)00294-1 [CrossRef]
  26. Sánchez-Tocino H, Alvarez-Vidal A, Maldonado MJ, Moreno-Montañés J, García-Layana A. Retinal thickness study with optical coherence tomography in patients with diabetes. Invest Ophthalmol Vis Sci. 2002;43:1588–1594.
  27. Neuringer M, Jeffrey BG. Visual development: neural basis and new assessment methods. J Pediatr. 2003;143:S87–S95. doi:10.1067/S0022-3476(03)00406-2 [CrossRef]
  28. Hee MR, Puliafito CA, Wong C, et al. Quantitative assessment of macular edema with optical coherence tomography. Arch Ophthalmol. 1995;113:1019–1029. doi:10.1001/archopht.1995.01100080071031 [CrossRef]

Demographic and Clinical Characteristics of the Patients (N = 30)

VariableValue
Age (y), mean ± SD (range)28.9 ± 14.2 (6 to 62)
Gender, n (%)
  Males > 18 years12 (40)
  Females > 18 years13 (32.5)
  Males < 18 years4 (13.3)
  Females < 18 years1 (3.3)
Type of surgery, n (%)
  Rectus muscle23 (76.6)
  Oblique muscle7 (23.3)

Comparison Between Preoperative and Postoperative Macular Thickness and Volume

VariablePreoperativePostoperativeP
Central foveal thickness (µm)a201.63 ± 18.36206.03 ± 22.73.024
Outer superior (µm)a238.70 ± 14.60239.73 ± 15.92.570
Outer temporal (µm)a220.10 ± 16.23225.80 ± 14.78.009
Outer inferior (µm)a223.40 ± 17.88234.47 ± 18.10.488
Outer nasal (µm)a257.13 ± 19.93257.90 ± 23.52.668
Inner superior (µm)a277.03 ± 17.04279.97 ± 19.70.114
Inner temporal (µm)a260.10 ± 15.19261.23 ± 16.60.581
Inner inferior (µm)a271.43 ± 16.88271.30 ± 16.63.942
Inner nasal (µm)a274.30 ± 16.96276.70 ± 20.40.203
Total macular volume (mm3)b6.91 ± 0.436.96 ± 0.45.130

Comparison Between Macular Thickness Changes in Rectus Versus Oblique Muscle Surgeries

ParameterRectus (n = 23)Oblique (n = 7)P
Central foveal thickness (µm)a5.82 ± 11.270.50 ± 4.17.070
Outer superior (µm)a0.27 ± 9.273.13 ± 11.68.492
Outer temporal (µm)a5.77 ± 11.015.50 ± 12.06.954
Outer inferior (µm)a−0.09 ± 8.304.25 ± 7.76.212
Outer nasal (µm)a0.59 ± 11.011.25 ± 5.06.873
Inner superior (µm)a1.68 ± 9.656.38 ± 10.23.256
Inner temporal (µm)a0.55 ± 11.182.75 ± 11.56.640
Inner inferior (µm)a−1.86 ± 8.894.63 ± 11.93.118
Inner nasal (µm)a1.50 ± 8.315.13 ± 15.08.407
Total macular volume (mm3)b0.04 ± 0.180.95 ± 0.25.534
Authors

From the Department of Ophthalmology, Tel-Aviv Medical Center, Tel Aviv, Israel, affiliated to the Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel.

The authors have no financial or proprietary interest in the materials presented herein.

Drs. Mintz and Waisbourd contributed equally to this work and should be considered as equal first authors.

Correspondence: Rivka Kessner, MD, 3 Kadima Street, Haifa 3438204, Israel. E-mail: rikikes@gmail.com

Received: May 28, 2015
Accepted: September 28, 2015

10.3928/01913913-20160113-07

Sign up to receive

Journal E-contents