Ocular motility problems caused by thyroid eye disease may present in the acute or chronic phase. Patients may complain of diplopia and eye movement discomfort and associated limitations.1 Strabismus surgery is necessary to restore binocular vision at primary gaze. Previous reports on various methods assessing extraocular muscle involvement and surgical dosing and technique have indicated the various surgical techniques and their outcomes.1–3
The inflammatory changes result in alterations to muscle anatomy and physiology and iatrogenic alterations preceding surgical intervention. Therefore, responses to conventional surgical doses in strabismus with thyroid eye disease are not predictable.4 This unpredictability persists to be a major concern in surgical correction of strabismus in patients with thyroid eye disease. To our knowledge, there is no published report on whether postoperative initial alignments can affect the surgical outcome of strabismus surgery in patients with thyroid eye disease. It may be difficult to predict the long-term surgical outcomes according to initial postoperative deviations. The purpose of this study was to investigate the surgical outcome according to the initial postoperative angle of deviation after strabismus surgery in patients with hypotropia and esotropia who had thyroid eye disease.
Patients and Methods
The study was conducted according to the principles outlined in the Declaration of Helsinki and approved by the institutional review board with an understanding on exemption of informed consent for retrospective collection of the clinical data. The data were accessed anonymously. The local ethics committee of the Institutional Review Board at Korea University Medical Center approved the study protocol. Patients who were diagnosed as having thyroid eye disease and underwent strabismus surgery between 2012 and 2016 were retrospectively analyzed.
All patients were euthyroid at the time of surgery. History of orbital decompression and presence of diplopia at primary gaze were evaluated. The prism and alternate cover tests (prism diopters [PD]) were performed at a distance of 6 m and 33 cm at primary gaze with full correction of refractive error. All measurements of the strabismus were stable for at least 12 months prior to surgery.5 Patients were excluded if they had combined strabismus, A- or V-patterned strabismus, oblique dysfunction, or other orbital diseases, or if they had previously undergone a strabismus surgery.
All surgeries were performed by one experienced surgeon (S-HK). The intraoperative forced duction test was performed prior to surgery under general anesthesia. All patients underwent affected muscle recession surgery using a fixed suture technique with polyglactin 910. Additionally, combined surgery with contralateral antagonist rectus muscle recession using fixed suture was performed according to the preoperative angle of deviation. For instance, ipsilateral inferior rectus muscle recession alone or in combination with contralateral superior rectus muscle recession was performed in patients with hypotropia. We used the standard surgical dose table, but we also attempted to correct the restriction for the surgery.6
Ocular assessment was performed on postoperative day 1 and month 1, 3, 6, and 12. After 12 months postoperatively, patients were followed up at 6-month intervals. The postoperative ocular assessment included angle of deviation and presence of diplopia at primary gaze. All patients were followed up for at least 12 months after surgery.
The patients were divided into two groups according to the type of strabismus: hypotropia and esotropia. The angle of deviation on postoperative day 1 was measured and classified into three groups: undercorrection (greater than 5 PD), full correction, and overcorrection (greater than 5 PD), compared with preoperative angle of deviation.
The surgical outcomes were evaluated at the final visit. A successful outcome was defined as an absence of diplopia and maintenance of vertical (less than 5 PD) or horizontal (less than 10 PD) stable alignment at primary gaze. Subjective diplopia within successful motor alignment at the final visit was defined as failure in this study.
Statistical analysis was performed using SPSS software for Windows (version 21.0; IBM-SPSS, Inc). The aforementioned variables were compared between the two groups using the Mann–Whitney test and Fisher's exact test. Statistical significance was set a P value of less than .05.
Seventy-eight patients were included in this study. The mean age was 53.4 ± 9.5 years (range: 37 to 72 years). Forty-three patients (55.1%) were female. Fifty-one patients were diagnosed as having hypotropia and 27 as having esotropia. Orbital decompression was performed in 11 patients (14.1%) before strabismus surgery. The mean postoperative follow-up period was 17.4 ± 8.7 months (range: 12 to 36 months).
In subgroup analysis, undercorrection, full correction, and overcorrection on postoperative day 1 in the hypotropia group occurred in 25 (49.0%), 12 (23.5%), and 14 (27.5%) patients, respectively. Undercorrection, full correction, and overcorrection occurred on postoperative day 1 in the esotropia group in 13 (48.2%), 6 (22.2%), and 8 (29.6%) patients, respectively. The mean success rate was 65.4% at the final visit. There was no significant difference in the success rate between the hypotropia and esotropia groups (P = .53). The detailed pre-operative and postoperative angles of deviation and final success rates are shown in Table 1.
Comparison of Surgical Results in Patients With Hypotropia and Esotropia
Twelve patients (23.5%) underwent reoperation for overcorrected deviation of hypotropia and 3 patients (5.9%) required reoperation for residual hypotropia during the follow-up period. Three patients (5.9%) in the hypotropia group required prism glasses for diplopia at primary gaze during the follow-up period. Six patients (22.2%) underwent reoperation for overcorrected deviation of esotropia. One patient (3.7%) in the esotropia group underwent reoperation for residual esotropia during the follow-up period. Two patients (7.4%) in the esotropia group required prism glasses at primary gaze during the follow-up period.
The success rates according to the angle of deviation on postoperative day 1 were compared between the hypotropia and esotropia groups (Figure 1). The final success for undercorrection and full correction of hypotropia on postoperative day 1 was achieved in 20 (80.0%) and 8 (66.7%) patients, respectively. However, the final success for overcorrection of hypotropia on postoperative day 1 was achieved in only 5 patients (35.7%). The success rate was significantly higher for undercorrection and full correction than for overcorrection in the hypotropia group (P = .02). The final success for undercorrection and full correction of esotropia on postoperative day 1 was achieved in 11 (84.6%) and 5 patients (83.3%), respectively, in the esotropia group. The final success for overcorrection of esotropia on postoperative day 1 was observed in 3 patients (37.5%), which was significantly lower than that for undercorrection and full correction in the esotropia group (P = .03).
Final success rates according to the angle of deviation on postoperative day 1.
Successful surgical treatment for strabismus in patients with thyroid eye disease results in realignment of visual axes and stabilization of the field of single binocular vision. However, strabismus surgery in patients with thyroid eye disease remains challenging for surgeons because the strabismus in thyroid eye disease is unpredictable and incomitant. There is no gold standard surgical method or general consensus regarding when surgical treatment should be considered. The surgical results in patients with thyroid eye disease can be highly unpredictable, with reoperation rates reported between 17% and 45%.7,8 The overall success rate of strabismus surgery in patients with thyroid eye disease at the final visit was 65.4% and the reoperation rate for residual or overcorrected deviations in this study was 29.5%, including both hypotropia and esotropia, which was comparable with that in previous studies.
Several surgical techniques can be applied to improve the results of strabismus surgery in patients with thyroid eye disease, such as modification of the surgery or implementation of new techniques. Conventionally, recession of the affected muscles is strongly recommended and resection in restrictive strabismus should be avoided due to the risk of limitation of movement and globe retraction with worsening diplopia due to the progression of incomitance.9 Recently, variable techniques including adjustable sutures of affected muscles,10 intraoperative relaxed muscle positioning,11 and resection of vertical or horizontal rectus muscles12,13 have been reported to treat strabismus effectively in patients with thyroid eye disease. In this study, we performed recession of the affected muscles alone or combined with the recession of contralateral antagonist muscles with fixed sutures.
To the best of our knowledge, there has been no study on the initial target angle after strabismus surgery in patients with thyroid eye disease during the early postoperative period. Volpe et al14 reported that undercorrection of hypotropia in patients with thyroid eye disease as the initial goal using an adjustable suture technique showed 65% excellent surgical results during the mean follow-up period of 38 weeks. Buckley et al15 stated that the postoperative goal of strabismus surgery in thyroid eye disease should be a slight undercorrection for hypotropia, as there is typically a late drift toward overcorrection. In this study, we did not intend to achieve initial undercorrection of deviation after surgery; however, surgical success rates of undercorrection and full correction of strabismus on postoperative day 1 were significantly higher than that of overcorrection of strabismus (P < .05 for all). Additionally, these results were observed in patients with hypotropia and those with esotropia.
Several authors have described late overcorrection after strabismus surgery in patients with thyroid eye disease. Altered muscle dynamics and the presence of asymmetric muscle involvement in patients with thyroid eye disease could result in late overcorrection after strabismus surgery. Hudson and Feldon16 reported that 41% of patients with thyroid eye disease have marked overcorrection within weeks to months after strabismus surgery. Other studies have described that strabismus surgery in patients with preoperative hypotropia could result in mostly late overcorrections.17,18 Late overcorrection after surgery for vertical strabismus is a common phenomenon. However, 9 (64.3%) and 4 (50%) patients with overcorrection greater than 5 PD on postoperative day 1 for hypotropia and esotropia, respectively, required reoperation for late overcorrection during the follow-up period. We could not explain these results exactly and speculated that asymmetrical horizontal muscle involvement, fibrotic changes, or multifactorial reasons in thyroid eye disease could have been the causes of late overcorrection after strabismus surgery. Buckley et al15 demonstrated that late drift toward overcorrection could also occur after correction of esotropia in patients with thyroid eye disease.15 The cause of late overcorrection is most likely multifactorial, and it would be difficult to minimize this problem with a specific surgical technique.
There is no surgical nomogram especially based on the deviation in thyroid eye disease. The surgical doses were decided based on the surgeon's experience, preferred techniques, standard nomogram in concomitant strabismus, and results on the intra-operative forced duction test. Previous studies stated that the dose response in thyroid eye disease is greater than that in non-thyroid eye disease surgery, which may account for some of the unpredictability, particularly if fixed sutures are used.19,20
It is challenging to predict the surgical effect of strabismus surgery using fixed sutures. In the current study, we did not intend to achieve specific surgical goals on postoperative day 1 after strabismus surgery. We used the standard surgical nomogram that has been used widely.6
There are some limitations to this study. First, the design of this study was retrospective and a small number of patients were enrolled. Second, patients who underwent surgeries for combined strabismus or torsional diplopia were not enrolled in this study. Thus, we could not apply our results to the surgery for these types of strabismus in thyroid eye disease. Third, ocular alignment on postoperative day 1 was divided into three groups, based on vertical and horizontal deviations of 5 PD. Additionally, accurate initial target angle or ranges after surgery could not be suggested in this study, although there were successful outcomes in patients who showed undercorrection or full correction after strabismus surgery. Finally, the mean follow-up period after surgery was relatively short, so further long-term follow-up is needed to determine the definite postoperative results.
Intended minimal undercorrection or full correction of strabismus after hypotropia and esotropia surgery during early postoperative periods could improve surgical success rates in patients with thyroid eye disease.
- Coats DK, Paysse EA, Plager DA, Wallace DK. Early strabismus surgery for thyroid ophthalmopathy. Ophthalmology. 1999;106(2):324–329. doi:10.1016/S0161-6420(99)90071-4 [CrossRef]
- Mourits MP, Koorneef L, van Mourik-Noordenbos AM, et al. Extraocular muscle surgery for Graves' ophthalmopathy: does prior treatment influence surgical outcome?Br J Ophthalmol. 1990;74(8):481–483. doi:10.1136/bjo.74.8.481 [CrossRef]
- Yang ML, Hsu HN, Ma L, Kao LY. Surgical management of strabismus for dysthyroid ophthalmopathy. Chang Gung Med J. 2004;27(11):787–793.
- Wallang BS, Kekunnaya R, Granet D. Strabismus surgery in thyroid-related eye disease: strategic decision making. Curr Ophthalmol Rep. 2013;1(4):218–228. doi:10.1007/s40135-013-0027-z [CrossRef]
- Evans D, Kennerdell JS. Extraocular muscle surgery for dysthyroid myopathy. Am J Ophthalmol. 1983;95(6):767–771. doi:10.1016/0002-9394(83)90062-4 [CrossRef]
- Rosenbaum AL, Santiago AP. Clinical Strabismus Management: Principles and Surgical Techniques. WB Saunders; 1999.
- Bartley G, Fatourechi V, Kadrmas E, et al. Clinical features of Graves' ophthalmopathy in an incidence cohort. J Neuroophthalmol. 1997;17(1):73. doi:10.1097/00041327-199703000-00018 [CrossRef]
- Lee H, Roh HS, Yoon JS, Lee SY. Assessment of quality of life and depression in Korean patients with Graves' ophthalmopathy. Korean J Ophthalmol. 2010;24(2):65–72. doi:10.3341/kjo.2010.24.2.65 [CrossRef]
- Kraus DJ, Bullock JD. Treatment of thyroid ocular myopathy with adjustable and nonadjustable suture strabismus surgery. Trans Am Ophthalmol Soc. 1993;91:67–79.
- Zhang MS, Hutchinson AK, Drack AV, Cleveland J, Lambert SR. Improved ocular alignment with adjustable sutures in adults undergoing strabismus surgery. Ophthalmology. 2012;119(2):396–402. doi:10.1016/j.ophtha.2011.07.044 [CrossRef]
- Dal Canto AJ, Crowe S, Perry JD, Traboulsi EI. Intraoperative relaxed muscle positioning technique for strabismus repair in thyroid eye disease. Ophthalmology. 2006;113(12):2324–2330. doi:10.1016/j.ophtha.2006.04.036 [CrossRef]
- Lee JY, Park KA, Woo KI, Kim YD, Oh SY. Surgical outcomes of unilateral recession-resection for vertical strabismus in patients with thyroid eye disease. J AAPOS. 2017;21(1):19–22. doi:10.1016/j.jaapos.2016.11.019 [CrossRef]
- Yoo SH, Pineles SL, Goldberg RA, Velez FG. Rectus muscle resection in Graves' ophthalmopathy. J AAPOS. 2013;17(1):9–15. doi:10.1016/j.jaapos.2012.09.018 [CrossRef]
- Volpe NJ, Mirza-George N, Binenbaum G. Surgical management of vertical ocular misalignment in thyroid eye disease using an adjustable suture technique. J AAPOS. 2012;16(6):518–522. doi:10.1016/j.jaapos.2012.08.010 [CrossRef]
- Buckley EG, Plager DA, Repka MX, Wilson ME, Plager DA. In: Plager DA, ed. Strabismus Surgery: Basic and Advanced Strategies. Ophthalmology Monographs, vol 17. Oxford University Press; 2004.
- Hudson HL, Feldon SE. Late overcorrection of hypotropia in Graves ophthalmopathy. Predictive factors. Ophthalmology. 1992;99(3):356–360. doi:10.1016/S0161-6420(92)31965-7 [CrossRef]
- De Hoog J, Stravers S, Kalmann R. Recession of the inferior rectus muscle in Graves' orbitopathy. Eye (Lond). 2010;24(6):1011–1017. doi:10.1038/eye.2009.267 [CrossRef]
- Wright KW. Late overcorrection after inferior rectus recession. Ophthalmology. 1996;103(9):1503–1507. doi:10.1016/S0161-6420(96)30476-4 [CrossRef]
- Peragallo JH, Velez FG, Demer JL, Pineles SL. Postoperative drift in patients with thyroid ophthalmopathy undergoing unilateral inferior rectus muscle recession. Strabismus. 2013;21(1):23–28. doi:10.3109/09273972.2012.762533 [CrossRef]
- Schotthoefer EO, Wallace DK. Strabismus associated with thyroid eye disease. Curr Opin Ophthalmol. 2007;18(5):361–365. doi:10.1097/ICU.0b013e32827038f2 [CrossRef]
Comparison of Surgical Results in Patients With Hypotropia and Esotropia
|Value||Hypotropia (n = 51)||Esotropia (n = 27)||P|
|Age (y), mean ± SD (range)||52.4 ± 8.8 (37 to 55)||55.2 ± 6.7 (38 to 72)||.56a|
|Female, no. (%)||28 (54.9)||15 (55.5)||.29b|
|Preoperative angle of deviation (PD), mean ± SD (range)||26.4 ± 10.3 (10 to 40)||37.4 ± 12.3 (16 to 55)||.03a|
|Angle of deviation at postoperative day 1 (PD), mean ± SD (range)||1.0 ± 5.7 (−10 to 6)c||1.8 ± 6.4 (−8 to 10)c||.24a|
|Ocular alignment at postoperative day 1||.18b|
| Undercorrection, no. (%)||25 (49.0)||13 (48.2)|
| Fullcorrection, no. (%)||12 (23.5)||6 (22.2)|
| Overcorrection, no. (%)||14 (27.5)||8 (29.6)|
|Reoperation, no. (%)||15 (29.4)||7 (25.9)||.55b|
|Subjective diplopia, no. (%)||3 (5.9)||2 (7.4)||.75b|
|Mean follow-up period, mean ± SD (range)||15.9 ± 7.8 (12 to 30)||19.1 ± 5.8 (18 to 36)||.14a|
|Final success rate, no. (%)||33 (64.7)||18 (66.7)||.53b|