Graefes Arch Clin Exp Ophthalmol (2011) 249:1373–1377 DOI 10.1007/s00417-011-1647-3

NEURO-OPHTHALMOLOGY

The change of the extraocular muscle insertion after a slanted recession in rabbit eyes Minwook Chang & Joong-Hoon Kim & Seung-Hyun Kim

Received: 9 November 2010 / Revised: 21 January 2011 / Accepted: 1 February 2011 / Published online: 9 April 2011 # Springer-Verlag 2011

Abstract Purpose To evaluate the change of slanting degree after slanted recession using a rabbit model. Methods A prospective, controlled study was performed in ten eyes of five rabbits with anatomically normal eyes. These eyes were divided into two groups according to the amount of slanted recession. In right eyes, slanted superior recti (SR) muscle recession was performed with 6 mm of nasal margin and 2 mm of temporal margin (4-mm slanting group), and in fellow eyes, slanted SR muscle recession was performed with 6 mm and 4 mm, respectively (2-mm slanting group). We measured both margins of superior recti from insertion, and calculated the amount of anterior creeping movement of both margins at 30, 60, and 90 postoperative days, and also compared the change of slanting degree of the SR muscle between the two groups. Results Slanting degrees showed a gradual decrease in all rabbit eyes. In the 4-mm slanting group, each margin of anterior movement was 2.4.mm (nasal) and 0.9 mm (temporal) and slanting degrees decreased in 50-75%. In the 2-mm slanting group, the margins of anterior movement were 2.9 mm and 1.8 mm respectively, and slanting degrees decreased in 25∼50%. The amount of slanting degree showed a greater decrease in the 4-mm group than in the 2-mm group at postoperative 3 months (p=0.045). Electronic supplementary material The online version of this article (doi:10.1007/s00417-011-1647-3) contains supplementary material, which is available to authorized users. M. Chang : J.-H. Kim : S.-H. Kim Department of Ophthalmology, Korea University College of Medicine, Seoul, Korea S.-H. Kim (*) Department of Ophthalmology, Korea University Ansan Hospital, 516, Gojan-dong, Ansan, Gyunggi-do 425-707, South Korea e-mail: [email protected]

Conclusion Both margins of extraocular muscle in slanted recession showed anterior movement at postoperative 3 months; therefore, the effectiveness of slanted recession might be decreased postoperatively. Keywords Slanted recession . Insertion . Convergence excess

Introduction Slanted recession on the medial rectus (MR) muscle was introduced as an effective surgical treatment, especially for convergence excess esotropia [1–4] and AV pattern esotropia [5, 6]. The physiologic and rational basis of the slanted recession of the lateral rectus (LR) muscle was based on Scott’s investigation [7]. During primary gaze, fibers of the upper and lower margin of the LR are of equal length. However, in downgaze, upper muscle fibers are extended and lower muscle fibers are shortened. Consequently, at near vision and downgaze, lower fibers of the LR muscles are shorter than upper fibers. Thus, by recessing the lower muscle fibers more than the upper fibers, exotropia (XT) at near fixation is reduced and the muscle tension of upper and lower fibers is balanced at the new insertion, which results in a similar alignment of the eye for near and distance. Biedner and Rothkoff [2] reported that all seven patients treated by slanting muscle insertion had their A or V pattern eliminated, with six achieving good alignment in all positions of gaze. Nemet et al. [10] recommended the slanted procedure for MR recession or resection in patients with convergence excess esotropia and for convergence insufficiency exotropia. Gharabaghi and Zanjani [6] reported that slanted MR muscle recession was an easy, non-invasive approach without any additional complications for use in treatment of high AC/A esotropia, and that

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Fig. 1 The new insertion was created in an oblique fashon in comparison with the original insertion, the amount of recession were 6 mm at nasal margin and 2 mm at temporal margin in right eye (4-mm slanting group) and 4 mm at temporal margin in left eye (2-mm slanting group). R : right eye ; L : left eye, T : temporal ; N : nasal, SR : superior rectus

mean distant-near disparity had been reduced by about 11PD (67.5%) after the surgery. However, Choi and Hwang [8] reported that bilateral slanted MR resections in patients with exotropia of the convergence insufficiency type resulted in undercorrection in all patients. Few studies have reported on anatomical change of the slanted muscle over time, and controversy still exists with regard to a satisfactory explanation of the mechanism of correction of eyeball misalignment after performance of the slanting technique. The aim of this study was to elucidate the change of the new insertion of extraocular muscle after slanted recession over time, to suggest a clue for the correction mechanism of the slanted recession.

Methods All procedures were performed according to guidelines for the use of animals in research prepared by the Korea National Institute of Health and the ARVO Statement for the Use of Table 1 Postoperative anterior advancement of SR muscles that underwent recession surgery in rabbit models. All of the SR muscles in rabbits showed movement anteriorly at 3 months from surgery

Rabbit

Eye

Surgerya (N/T)

One monthb (N/T)

Two monthsb (N/T)

Three monthsb (N/T)

1

Right Left Right Left Right Left Right Left Right Left

6 6 6 6 6 6 6 6 6 6

2.5 / 1 4 / 2.5 3.5 / 1.5 3/2 2.5 / 1.5 3.5 / 3 4/1 4 / 2.5 3.5 / 1.5 4 / 2.5

2/1 3/2 3/ 1.5 3/2 2.5 / 1 3/2 4/1 3/2 2.5 / 1 3.5 / 2

2 / 0.5 3/2 2.5 / 1 2.5 / 1.5 2.5 / 1 3/2 3/1 3/2 2/1 3 / 1.5

3 4 N/T: nasal/temporal immediately after surgery.

b

postoperative days.

Animals in Ophthalmic and Vision Research. The protocol was approved by the Institutional Animal Care and Use Committee of Korea University Medical Center. Slanted recession surgery of the superior rectus (SR) muscle was performed on both eyes of five New Zealand white rabbits (weight, 2.5–3.0 kg), which had anatomically normal eyes. Rabbits were anesthetized with an intramuscular injection of ketamine (10 mg/kg) and xylazine (2 mg/kg), and topical anesthesia was administered using propacaine hydrochloride. The limbal conjunctiva and anterior Tenon’s capsule were opened, the superior rectus muscle was exposed, and the intermuscular membrane and check ligaments were dissected. The reason for use of superior rectus muscles in our study was that it is the thickest extraocular muscle in rabbits, making it easy to observe [9]. The SR muscle was then placed on a double-armed 6–0 prolene suture close to the insertion and disinserted from the globe. Prolene was used for better postoperative visualization of the new insertion than that provided by absorbable suture material [9]. Ten SR muscles were divided into two groups according to the amount of slanted recession as follows: the 4-mm slanting group (five SR muscles of right eyes), and 2-mm slanting group (five SR muscles of left eyes). The new insertion was created in

Amount of recession (mm)

2

a

Fig. 2 Anterior movement of the recessed superior rectus muscle occurred abruptly at postoperative 1 month and then progressed gradually in 4-mm and 2-mm slanting groups

5

/ / / / / / / / / /

2 4 2 4 2 4 2 4 2 4

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test and Wilcoxon signed-rank test. Statistical significance was defined as a p-value of<0.05.

Results

Fig. 3 Slanting degree in both groups decreased abruptly from postoperative 1 month, and then changed gradually to postoperative 3 months

an oblique fashion in comparison with the original insertion; the amount of recession was 6 mm at the nasal margin and 2 mm at the temporal margin in the right eye (4-mm slanting group) and 4 mm at the temporal margin in the left eye (2-mm slanting group) (Fig. 1). After reinsertion, the amount of recession was measured again using a caliper. Ofloxacin eye ointment was applied topically at the end of the procedure. Rabbits were examined at 30, 60, and 90 postoperative days under anesthesia. The amount of anterior movement was calculated by subtracting the distance of postoperative new insertion from the distance of initial, new insertion, and measured using a caliper from the corneal limbus for comparison of the change of the slanting degrees between the two groups. Slanting degree was defined as the difference of the amount of recession between nasal and temporal areas of the SR muscle. At the last examination, rabbits were humanely euthanized by inhalation of CO2 gas under general anesthesia. Statistical analysis was performed using SPSS 12.0 for Windows (SPSS Inc., Chicago, IL, USA: 2004). Changes of muscle recession were compared using the Mann–Whitney Table 2 Change of slanting degrees (SD) of SR muscles in two groups at 3 months from surgery. In the 4 mm slanting group, the decrease in slanting degree was greater than in the 2 mm slanting group (p=0.045)

immediately after surgery.

b

postoperative days.

c [SD( at immediate after surgery) − SD( at 3 postoperative months)] * 100 / SD( at immediate after surgery) d

Mann–Whitney test on the slanting degree between the two groups

Discussion Slanted recession of the horizontal extraocular muscle was originally described by Boyd et al. for patients with a significant A–V pattern of strabismus [6]. And there have been many reports on the effectiveness of these procedures. Nemet et al. [4] reported a 77% reduction in distance–near

Slanting Degrees (mm) Rabbit

Eye

Surgerya

Three monthsb

Decrease in SDc(%)

P-valued

1

Right Left Right Left Right Left Right Left Right Left

4 2 4 2 4 2 4 2 4 2

2 1 1.5 1 1.5 1 2 1 1 1.5

50% 50% 62.5% 50% 62.5% 50% 50% 50% 75% 25%

0.045d

2 a

In this study, all SR muscles that had undergone slanted recession showed gradual movement anteriorly from the initial insertion during each examination (Table 1) (Figs. 2, 4 and 5). The change of slanting degrees in these two groups is shown in Table 2. Without exception, slanting degrees decreased in all SR muscles of both the 4-mm and 2-mm groups. The anterior movement and decrease of slanting degree of the recessed superior rectus muscle occurred abruptly from postoperative 1 month, and then progressed gradually (Figs. 2 and 3) The average amount of decrease in slanting degrees at 3 postoperative months was 1.75 mm in ten SR muscles of rabbits. In the 2-mm slanting group, a decrease in slanting degree of 0.9 mm was observed at 3 months after surgery; that is a 25–50% decrease compared to initial slanting degrees. In the 4-mm slanting group, the average amount of decrease in slanting degrees at 3 postoperative months was 2.4 mm, that is a 50–75% decrease, compared to initial slanting degrees. The amount of decrease in slanting degrees was greater in the 4-mm slanting group than in the 2-mm slanting group (p=0.045).(Tables 1 and 2).

3 4 5

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Fig. 4 The nasal edge of the SR muscle in 4-mm slanting group, which shows the right eye of the number 2 rabbit (left), moved 3 mm anteriorly at 2 postoperative months (right)

esotropia after bilateral symmetric slanting recession of the medial rectus (MR) muscles. Ahadzadegan [1] showed that slanted recession of the MR muscles reduced distance–near disparity by 69%, with a satisfactory outcome in 80% of cases. Gharabaghi and Zanjani [2] demonstrated that in treatment of high accommodative convergence/accommodation (AC/A) ratio esotropia, satisfactory results occurred in 70% of patients who underwent slanted recession. And a majority of studies of slanted recession, regardless of good results, were not able to provide a satisfactory explanation of the mechanism of correction after performance of this surgery. We began this study from this point, and attempted to find the mechanism of correction of the specific eyeball misalignment from the modification of the unstable insertion of slanted recession. As a result, we found that SR muscles that had undergone slanted recession had moved anteriorly. And slanting degrees were decreased after 3 months from immediate surgery in both the 2-mm and 4-mm slanting groups. The amount of decrease in slanting degree ranged from 0.5 mm to 3 mm, which means a decrease of 25∼75% compared with the amount of immediate surgery. Comparison of the amount of decrease in slanting degree between the two study groups showed a greater decrease of slanting degree in the 4-mm slanting group than in the 2-mm group. To the best of our knowledge, there has been no report on extraocular muscle Fig. 5 The temporal edge of the SR muscle in 2-mm slanting group, which shows left eye of the number 1 rabbit (left), moved 2 mm anteriorly at 3 postoperative months (right)

migration after slanted recession, and we are not sure why the new insertion of slanted recession moved forward. Mazow [10, 11] found that muscle had moved anterior to sutured recession sites, and he suggested that indeed what may have happened was a “creeping forward of the retroplaced muscle”. He explained the phenomenon as the role of conjunctiva and Tenon’s capsule with the muscle and its fascial envelope. If the envelope is disturbed, then raw muscle surface is opposing raw scleral surface, and an inflammatory reaction takes place resulting in adhesions and advancement. However , controversy continues over the mechanism of slanted recession to decrease a distant–near disparity; contrary to the previous reports [1–4], the initial effect of slanting surgery could be large, but the effect can show a gradual decrease. So our results may not explain this mechanism for correction of distance–near disparity with this slanted recession fully because the patient series who underwent the slanted recession show decreased AC/A ratio in the long-term follow-up. Further clinical study would be necessary in order to compare our results for clinical correlation. This study had some limitations. First, the sample size of the study was small; therefore, the statistical power was weak. Second, the observation period was not long enough for evaluation of the long-term effect of slanted recession

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surgery. Third, these results were acquired from SR muscle in a rabbit model; therefore, it was difficult to apply directly to the result of slanted medial rectus muscle recession in human beings, because functional aspects of extraocular muscles are very different between lateral-eyed animals (rabbit) and frontal-eyed animals (human, cat) [12, 13]. Rabbits need little ocular movement in their everyday life. Furthermore, the superior rectus muscle of rabbit may not act in response to accommodation. If more ocular movements occur, the effect of slanted recession may be maintained. Therefore, the experimental strabismus study conducted in rabbits has a restrictive value, but the findings in our study will suggest a modification of the current procedure. Further research which includes a larger recession or larger degree of slanting surgery to compensate for the long-term movement of the muscles is warranted to validate the clinical significance of the present data. In conclusion, the slanting degrees of SR muscles with slanted recession in a rabbit model showed a greater decrease at 3 months from surgery, and the amount of decrease in slanting degree was larger in the 4-mm slanting group than in the 2-mm group. This result might suggest that the effectiveness of slanting could be decreased with time.

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1377 2. Gharabaghi D, Zanjani LK (2006) Comparison of results medial rectus muscle recession using augmentation, Faden procedure, and slanted recession in the treatment of high accommodative convergence / accommodation ratio esotropia. J Pediatr Ophthalmol Strabismus 43:91–94 3. Lee SY (1998) Treatment for convergence excess esotropia by slanted medial rectus muscle recession. J Korean Ophthalmol Soc 39:3045–3052 4. Nemet P, Stolovitch C, Loewenstein A (1993) A new operation: slanted (reinsertion) medial rectus muscle recession surgery for convergence excess esotropia: results in 12 cases. Binocul Vision Strab Q 8:241–246 5. Biedner B, Rothkoff L (1995) Treatment for ‘A’ or ‘V’ pattern esotropia by slanting muscle recession. Br J Ophthalmol 79:807–885 6. Boyd TAS, Leitch GT, Budd GE (1971) A new treatment for “A” and “V” patterns in strabismus by slanting muscle insertions. Can J Ophthalmol 6:170–177 7. Scott AB (1975) Strabismus muscle forces and innervation. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications, 1st edn. Pergamon Press, Oxford 8. Choi MY, Hwang JM (2006) The long-term result of slanted medial rectus resection in exotropia of the convergence insufficiency type. Eye 20:1279–1283 9. Yang SM, Kim SH, Cho YA (2008) The difference in muscle slippage according to scleral suture techniques in rectus muscle resection of rabbit eyes. Eye 22:564–568 10. Mazow ML (1973) Conjunctiva and the creeping muscle. J Pediatr Ophthalmol 10:267–270 11. Mazow ML, Leal V (1976) Experimental creeping muscle. J Pediatr Ophthalmol 13:168–170 12. Ezure K, Graf W (1984) A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral- and frontaleyed animals I. Orientation of semicircular canals and extraocular muscles. Neuroscience 12:85–93 13. Simpson JI, Graf W (1981) Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann NY Acad Sci 374:20–30