Effects of recession versus tenotomy surgery without recession in adult rabbit extraocular muscle

Abstract

Purpose: Surgical recession of an extraocular muscle (EOM) posterior to its original insertion is a common form of strabismus surgery, weakening the rotational force exerted by the muscle on the globe and improving eye alignment. The purpose of this study was to assess myosin heavy chain (MyHC) isoform expression and satellite cell activity as defined by Pax7 expression in recessed EOMs of adult rabbits compared with that in muscles tenotomized but not recessed and with that in normal control muscles.

Methods: The scleral insertion of the superior rectus muscle was detached and sutured either 7 mm posterior to its original insertion site (recession surgery) or at the same site (tenotomy). One day before euthanization, the rabbits received bromodeoxyuridine (BrdU) injections. After 7 and 14 days, selected EOMs from both orbits were examined for changes in fast, slow, neonatal, and developmental MyHC isoform expression, Pax7 expression, and BrdU incorporation.

Results: Recession and tenotomy surgery resulted in similar changes in the surgical EOMs. These included a decreased proportion of fast MyHC myofibers, an increased proportion of slow MyHC myofibers, and increased BrdU-positive satellite cells. Similar changes were seen in the non-operated contralateral superior rectus muscles. The ipsilateral inferior rectus showed reciprocal changes to the surgical superior rectus muscles.

Conclusions: The EOMs are extremely adaptive to changes induced by recession and tenotomy surgery, responding with modulations in fiber remodeling and myosin expression. These adaptive responses could be manipulated to improve surgical success rates.

Figure 1.

(A) Control superior rectus muscle global layer immunostained for the fast MyHC isoform. (B) Superior rectus muscle global layer 2 weeks after recession surgery immunostained for the fast MyHC isoform. Bar, 50 μm. (C–F) Morphometric analysis of the effect of recession and tenotomy surgery on the MyHC isoform expression patterns 1 week after surgery compared with normal untreated control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 2.

Morphometric analysis of the effect of recession and tenotomy surgery on the MyHC isoform expression patterns 2 weeks after surgery compared with patterns in normal untreated control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 3.

Global layer of the superior rectus (A) 1 and (B) 2 weeks after surgical recession, immunostained for dystrophin. White arrows: myofibers in cross-section with only a thin rim of dystrophin immunostaining; black arrows: myofibers with a normal rim of dystrophin staining. Bar, 50 μm.

Figure 4.

Morphometric analysis of the effect of recession and tenotomy surgery on mean myofiber cross-sectional areas 1 and 2 weeks after surgery compared with normal untreated control superior rectus muscles. Red: tenotomized muscle; green: recessed muscles. *Significantly different from the control. #Significantly different from tenotomy. αSignificantly different compared with 1 week. Data are expressed as the mean ± SEM.

Figure 5.

Morphometric analysis of the frequency of Pax7-positive cells (A) 1 and (B) 2 weeks after recession and tenotomy surgery compared with normal control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 6.

(A) Recessed and (B) control superior rectus muscle immunostained for BrdU and dystrophin. Black arrow: a BrdU-positive myonucleus. White arrows: a BrdU-positive cell in the satellite cell position. Bar, 50 μm. Morphometric analysis of frequency of BrdU-positive cells 1 (C) and 2 (D) weeks after recession and tenotomy surgery compared with the number in normal control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 7.

Morphometric analysis of the MyHC isoform expression patterns in the layers of the antagonist inferior rectus muscle 1 and 2 weeks after surgical alteration of the ipsilateral superior rectus muscle compared with patterns in normal untreated control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 8.

Morphometric analysis of frequency of Pax7-positive cells at (A) 1 and (B) 2 weeks in the recessed SR, the antagonist IR, and the contralateral SR compared with the frequency in normal control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 9.

Morphometric analysis of frequency of BrdU-positive cells at (A) 1 and (B) 2 weeks in the recessed SR, the antagonist IR, and the contralateral SR compared with the frequency in normal control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.

Figure 10.

Morphometric analysis of the MyHC isoform expression patterns in the non-operated superior rectus muscle contralateral to a superior rectus muscle recession 1 and 2 weeks after surgery compared with the patterns in normal untreated control superior rectus muscles. *Significantly different from the control. Data are expressed as the mean ± SEM.