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Fibrotic superior oblique and superior rectus muscles with an accessory tissue band
Fibrotic superior oblique and superior rectus muscles with an accessory tissue band Seyhan B. Özkan, MD, Harun Çakmak, MD, and Volkan Dayanır, MD
Congenital fibrosis of extraocular muscles may rarely present by involvement of isolated extraocular muscles.1,2 We report a case with an unusual form of congenitally fibrotic superior oblique and superior rectus muscles with an accessory tissue band passing toward the limbus. Magnetic resonance imaging (MRI) findings as well as histopathological and surgical results were evaluated. To the best of our knowledge, there is only one partially similar case in the literature with coexistence of congenitally fibrotic superior rectus and superior oblique muscles, and the features of that case differ from those of our case.3
Case Report
A
7-year-old boy presented to the Adnan Menderes University Department of Ophthalmology, Aydın, Turkey, with the chief complaint of strabismus and abnormal eye movements since birth. The family history, pregnancy history, and the patient’s history were entirely unremarkable, with no consanguinity or maternal drug use. He was otherwise healthy on general physical examination. His ophthalmologic examination revealed a visual acuity of 20/20 in the right eye and 20/400 in the left eye. Cycloplegic refraction showed minimal refractive error in the right eye (⫹1.50) and marked astigmatism in the left eye (⫹4.00 ⫺9.50 ⫻ 90). He had 1 mm of ptosis of his left upper eyelid. He was orthophoric in the primary position with marked limitation of depression in the left eye. Elevation of the globe was severely restricted nasally, whereas elevation was relatively better temporally, as observed in Brown syndrome (Figure 1A). Slit-lamp examination revealed a tissue band passing toward the limbus at the 12 o’clock position and indenting the sclera on attempted downgaze (Figure 2A). Orbital MRI examination (Figure 3) revealed a slight nasal shift of the superior rectus muscle, placing it closer than normal to the superior oblique muscle. The space between the muscles was bridged with a tissue that appeared almost isointense. The trochlea appeared enlarged,
Author affiliations: Adnan Menderes University, Department of Ophthalmology, Aydın, Turkey Presented at the 30th Meeting of the European Strabismological Association, Killarney, Ireland, June 2005. The authors have no financial interest with any of the material used in this study. Submitted December 29, 2006. Revision accepted May 10, 2007. Reprint requests: Seyhan B. Özkan, MD, Professor of Ophthalmology, Adnan Menderes Universitesi, Tıp Fakültesi, Göz Hast. A.D., 09100, Aydın, Turkey (email: [email protected]). J AAPOS 2007;11:491-494. Copyright © 2007 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2007/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2007.05.005
Journal of AAPOS
irregularly shaped, and of intermediate signal intensity compared with the sound eye. The patient underwent surgery in an attempt to improve his binocular field and to decrease his astigmatism. Forced duction testing was positive in downward and upper nasal quadrant movements. The tissue band at the 12 o’clock position was dissected and found to be a separate structure from the superior rectus muscle (Figure 2B). The tissue band appeared to originate from the levator palpebrae superioris muscle and was excised. The superior rectus muscle appeared severely fibrotic and was recessed 5 mm. A superior oblique tenotomy was also performed from the nasal side of the superior rectus muscle. Although forced duction testing became negative in upper nasal quadrant, it was not totally free in downgaze, despite excision of the tissue band and even before the superior rectus muscle was resutured to the sclera. Histopathological evaluation of band tissue and superior rectus muscle revealed fibrosis and degenerated collagenized connective tissue (Figure 2C). The patient was orthophoric in the primary position postoperatively. A slight improvement in depression was obtained, whereas the improvement in other quadrants was poor (Figure 1B). The 1 mm of ptosis observed preoperatively had disappeared. No decrease of astigmatism was obtained (⫹4.00 ⫺9.00 ⫻ 180). With the use of glasses (⫹4.0 ⫺8.0 ⫻ 180) and patching, his visual acuity improved to 20/200.
Discussion Congenital fibrosis of the superior oblique and superior rectus muscles is a rare abnormality. Prakash et al,3 reporting a case with congenitally fibrotic superior rectus and superior oblique muscles, with marked limitation of elevation and slight restriction of depression, described a thick fibrous band including both superior rectus and superior oblique muscles and extending through the trochlea. The levator palpebrae superioris muscle was unaffected and there was no accessory tissue band in their case. The authors suggested that the development of the fibrous band including both superior rectus and superior oblique muscles might be the result of an intrauterine inflammatory disease. In our case the levator palpebrae superioris muscle was also affected, but in a different manner. The fibrous band was obviously a separate structure from the superior rectus muscle and seemed to be an extension of levator palpebrae superioris muscle. The supernumerary rectus muscles as well as the levator palpebrae superioris muscle have been reported previously in humans.4 The fibrous band may be
491
492
Özkan, Çakmak, and Dayanır
Volume 11 Number 5 / October 2007
FIG 1. (A) Preoperative motility pattern of the patient in nine positions of gaze. (B) Postoperative motility pattern following superior oblique tenotomy and superior rectus recession. Note the slight improvement in depression of the left eye.
a misdirected accessory part of the levator palpebrae superioris muscle. Recent evidence demonstrates that most of the developmental abnormalities of extraocular muscles with restricted eye movements are primarily a maldevelopment of specific cranial motoneurons and three subgroups of congenital fibrosis of extraocular muscles (CFEOM) are defined.5,6 Among those, the most recently described form is CFEOM3, which is autosomal-dominant and characterized by variable ptosis and restrictive ophthalmoplegia within a spectrum of severe to mild ocular motility restrictions. In our case there is no pertinent family history. While CFEOM1 and CFEOM3 are autosomal-dominant, new mutations occur regularly, and the lack of a family history does not rule out these conditions. However the unilateral presentation does make it less likely that this is a genetically determined condition. The presence of the accessory band makes CFEOM unlikely in our case. Extraocular muscles are demonstrated to develop from two mesodermal complexes.7 Superior rectus, superior oblique, and levator palpebrae superioris muscles derive
from superior mesodermal complex, whereas inferior rectus and inferior oblique muscles derive from inferior mesodermal complex. Lateral and medial rectus muscles derive from both mesodermal complexes. At the 28th day of embryogenesis, horizontal rectus muscles first appear. During the early stages of the 6th week, the superior oblique muscle begins to develop. At the 8th week of embryogenesis, the levator palpebrae superioris starts to develop as a separate structure from the superior rectus muscle. The trochlea also appears at this stage. It seems quite possible that any maldevelopment during that stage might have caused the problems in our case. The enlargement of the trochlea in MRI scans supports this view. superior rectus, superior oblique, and levator palpebrae superioris muscles are covered with a common epimysium early on in development until the embryo reaches 54 mm in size.7-9 Sevel7-9 demonstrated distinct extensions of condensed mesenchymal tissue that arise from this common epimysium and extend to attach to the trochlea. During this early stage of embryogenesis fibrosis may develop due to an abnormality of epimysium. MRI find-
Journal of AAPOS
Volume 11 Number 5 / October 2007
Özkan, Çakmak, and Dayanır
493
FIG 3. MRI examination was performed on a 1.5-Tesla superconducting magnet (Philips Gyroscan) with a surface coil. T1-weighted (678/16 ms TE/TE) contiguous 3-mm-thick multislice images were obtained in sagittal and axial planes. In coronal scans 2 mm thick multislice images were obtained (GE, 30/4.6 ms TR/TE). Note the close location of L SRM (left superior rectus muscle) and L SOM (left superior oblique muscle) bridged with a tissue almost isointense that caused a nasal shift of superior rectus muscle.
FIG 2. (A) Slit-lamp photograph of left eye illustrates the tissue band passing toward the limbus at the 12 o’clock position and indenting the sclera on attempted downgaze. (B) Intraoperative photograph (surgeon’s view from above). The tissue band (elevated with sutures) appears to be separate from the superior rectus muscle (SRM). (C) The histopathological specimen of tissue band is stained with hematoxylin-eosin. The tissue consists of collagenized fibrous connective tissue. Note the thickened eosinophilic collagen fibers.
Journal of AAPOS
ings—the close proximity of the superior rectus and superior oblique muscles and their relation with an isointense tissue—support a maldevelopment of epimysium. The ongoing restriction in downgaze despite excision of the tissue band and even after severing the superior rectus muscle suggest an abnormality in orbital fascial structures. The appearance of the trochlea in MRI scans was similar to our previously reported findings in Brown syndrome.10 The clinical features of our case may also be regarded as plus abnormalities with Brown syndrome. It has been demonstrated that ptosis and superior rectus underaction may be associated because of the close proximity of the embryological development of superior rectus and levator palpebrae superioris muscles.7 In our case, the question about the absence of marked ptosis arises despite our suggestion of the involvement of levator palpebrae superioris muscle. We postulate that the fibrous band represents a form of supernumerary levator palpebrae superioris muscle and only that portion of the muscle seems to be affected. In that case marked ptosis may not have developed since the other part of the levator palpebrae superioris muscle is relatively normal. We believe that an inflammatory etiology is unlikely to be responsible for the clinical picture in our case because the development of an accessory tissue band cannot be explained by an inflammatory origin. Since the limitation of ocular motility is not only related to the muscle tissue itself but also to the fascial structures among the extraocular muscles and the orbit, the results of surgery seem unsatisfactory. Only a subtle increase of depression could be obtained. Surgery could possibly have decreased the amount of astigmatism if the excision of the tissue band had been performed at an earlier age. References 1. Gillies EW. Congenital fibrosis of the vertically acting extraocular muscles. Ophthalmology 1995;102:607-12. 2. Harley RD. Congenital fibrosis of the extraocular muscles. Trans Am Ophthalmol Soc 1978;76:197-226.
494
Özkan, Çakmak, and Dayanır
3. Prakash P, Menon V, Ghost G. Congenital fibrosis of superior rectus and superior oblique: A case report. Br J Ophthalmol 1985;69:57-9. 4. Von Ludinghausen M. Bilateral supernumerary rectus muscles of the orbit. Clin Anat 1998;11:271-7. 5. Doherty EJ, Macy ME, Wang SM, Dykeman CP, Melanson MT, Engle EC. CFEOM3: A new extraocular congenital fibrosis syndrome that maps to 16q24.2-q24.3. Invest Ophthalmol Vis Sci 1999; 40:1687-94. 6. Engle EC. The genetic basis of complex strabismus. Pediatr Res 2006;59:342-8.
Volume 11 Number 5 / October 2007
7. Sevel D. A reappraisal of the origin of human extraocular muscles. Ophthalmology 1981;88:1330-8. 8. Sevel D. Ptosis and underaction of the superior rectus muscle. Ophthalmology 1984;91:1080-5. 9. Sevel D. Development of the connective tissue of the extraocular muscles and clinical significance. Graefes Arch Clin Exp Ophthalmol 1988;226:246-51. 10. S¸ener EC, Özkan SB, Arıbal ME, Sanac¸ AS¸, Aslan B. Evaluation of congenital Brown’s syndrome with magnetic resonance imaging. Eye 1996;10:492-6.
Journal of AAPOS
Congenital fibrosis of extraocular muscles may rarely present by involvement of isolated extraocular muscles.1,2 We report a case with an unusual form of congenitally fibrotic superior oblique and superior rectus muscles with an accessory tissue band passing toward the limbus. Magnetic resonance imaging (MRI) findings as well as histopathological and surgical results were evaluated. To the best of our knowledge, there is only one partially similar case in the literature with coexistence of congenitally fibrotic superior rectus and superior oblique muscles, and the features of that case differ from those of our case.3
Case Report
A
7-year-old boy presented to the Adnan Menderes University Department of Ophthalmology, Aydın, Turkey, with the chief complaint of strabismus and abnormal eye movements since birth. The family history, pregnancy history, and the patient’s history were entirely unremarkable, with no consanguinity or maternal drug use. He was otherwise healthy on general physical examination. His ophthalmologic examination revealed a visual acuity of 20/20 in the right eye and 20/400 in the left eye. Cycloplegic refraction showed minimal refractive error in the right eye (⫹1.50) and marked astigmatism in the left eye (⫹4.00 ⫺9.50 ⫻ 90). He had 1 mm of ptosis of his left upper eyelid. He was orthophoric in the primary position with marked limitation of depression in the left eye. Elevation of the globe was severely restricted nasally, whereas elevation was relatively better temporally, as observed in Brown syndrome (Figure 1A). Slit-lamp examination revealed a tissue band passing toward the limbus at the 12 o’clock position and indenting the sclera on attempted downgaze (Figure 2A). Orbital MRI examination (Figure 3) revealed a slight nasal shift of the superior rectus muscle, placing it closer than normal to the superior oblique muscle. The space between the muscles was bridged with a tissue that appeared almost isointense. The trochlea appeared enlarged,
Author affiliations: Adnan Menderes University, Department of Ophthalmology, Aydın, Turkey Presented at the 30th Meeting of the European Strabismological Association, Killarney, Ireland, June 2005. The authors have no financial interest with any of the material used in this study. Submitted December 29, 2006. Revision accepted May 10, 2007. Reprint requests: Seyhan B. Özkan, MD, Professor of Ophthalmology, Adnan Menderes Universitesi, Tıp Fakültesi, Göz Hast. A.D., 09100, Aydın, Turkey (email: [email protected]). J AAPOS 2007;11:491-494. Copyright © 2007 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2007/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2007.05.005
Journal of AAPOS
irregularly shaped, and of intermediate signal intensity compared with the sound eye. The patient underwent surgery in an attempt to improve his binocular field and to decrease his astigmatism. Forced duction testing was positive in downward and upper nasal quadrant movements. The tissue band at the 12 o’clock position was dissected and found to be a separate structure from the superior rectus muscle (Figure 2B). The tissue band appeared to originate from the levator palpebrae superioris muscle and was excised. The superior rectus muscle appeared severely fibrotic and was recessed 5 mm. A superior oblique tenotomy was also performed from the nasal side of the superior rectus muscle. Although forced duction testing became negative in upper nasal quadrant, it was not totally free in downgaze, despite excision of the tissue band and even before the superior rectus muscle was resutured to the sclera. Histopathological evaluation of band tissue and superior rectus muscle revealed fibrosis and degenerated collagenized connective tissue (Figure 2C). The patient was orthophoric in the primary position postoperatively. A slight improvement in depression was obtained, whereas the improvement in other quadrants was poor (Figure 1B). The 1 mm of ptosis observed preoperatively had disappeared. No decrease of astigmatism was obtained (⫹4.00 ⫺9.00 ⫻ 180). With the use of glasses (⫹4.0 ⫺8.0 ⫻ 180) and patching, his visual acuity improved to 20/200.
Discussion Congenital fibrosis of the superior oblique and superior rectus muscles is a rare abnormality. Prakash et al,3 reporting a case with congenitally fibrotic superior rectus and superior oblique muscles, with marked limitation of elevation and slight restriction of depression, described a thick fibrous band including both superior rectus and superior oblique muscles and extending through the trochlea. The levator palpebrae superioris muscle was unaffected and there was no accessory tissue band in their case. The authors suggested that the development of the fibrous band including both superior rectus and superior oblique muscles might be the result of an intrauterine inflammatory disease. In our case the levator palpebrae superioris muscle was also affected, but in a different manner. The fibrous band was obviously a separate structure from the superior rectus muscle and seemed to be an extension of levator palpebrae superioris muscle. The supernumerary rectus muscles as well as the levator palpebrae superioris muscle have been reported previously in humans.4 The fibrous band may be
491
492
Özkan, Çakmak, and Dayanır
Volume 11 Number 5 / October 2007
FIG 1. (A) Preoperative motility pattern of the patient in nine positions of gaze. (B) Postoperative motility pattern following superior oblique tenotomy and superior rectus recession. Note the slight improvement in depression of the left eye.
a misdirected accessory part of the levator palpebrae superioris muscle. Recent evidence demonstrates that most of the developmental abnormalities of extraocular muscles with restricted eye movements are primarily a maldevelopment of specific cranial motoneurons and three subgroups of congenital fibrosis of extraocular muscles (CFEOM) are defined.5,6 Among those, the most recently described form is CFEOM3, which is autosomal-dominant and characterized by variable ptosis and restrictive ophthalmoplegia within a spectrum of severe to mild ocular motility restrictions. In our case there is no pertinent family history. While CFEOM1 and CFEOM3 are autosomal-dominant, new mutations occur regularly, and the lack of a family history does not rule out these conditions. However the unilateral presentation does make it less likely that this is a genetically determined condition. The presence of the accessory band makes CFEOM unlikely in our case. Extraocular muscles are demonstrated to develop from two mesodermal complexes.7 Superior rectus, superior oblique, and levator palpebrae superioris muscles derive
from superior mesodermal complex, whereas inferior rectus and inferior oblique muscles derive from inferior mesodermal complex. Lateral and medial rectus muscles derive from both mesodermal complexes. At the 28th day of embryogenesis, horizontal rectus muscles first appear. During the early stages of the 6th week, the superior oblique muscle begins to develop. At the 8th week of embryogenesis, the levator palpebrae superioris starts to develop as a separate structure from the superior rectus muscle. The trochlea also appears at this stage. It seems quite possible that any maldevelopment during that stage might have caused the problems in our case. The enlargement of the trochlea in MRI scans supports this view. superior rectus, superior oblique, and levator palpebrae superioris muscles are covered with a common epimysium early on in development until the embryo reaches 54 mm in size.7-9 Sevel7-9 demonstrated distinct extensions of condensed mesenchymal tissue that arise from this common epimysium and extend to attach to the trochlea. During this early stage of embryogenesis fibrosis may develop due to an abnormality of epimysium. MRI find-
Journal of AAPOS
Volume 11 Number 5 / October 2007
Özkan, Çakmak, and Dayanır
493
FIG 3. MRI examination was performed on a 1.5-Tesla superconducting magnet (Philips Gyroscan) with a surface coil. T1-weighted (678/16 ms TE/TE) contiguous 3-mm-thick multislice images were obtained in sagittal and axial planes. In coronal scans 2 mm thick multislice images were obtained (GE, 30/4.6 ms TR/TE). Note the close location of L SRM (left superior rectus muscle) and L SOM (left superior oblique muscle) bridged with a tissue almost isointense that caused a nasal shift of superior rectus muscle.
FIG 2. (A) Slit-lamp photograph of left eye illustrates the tissue band passing toward the limbus at the 12 o’clock position and indenting the sclera on attempted downgaze. (B) Intraoperative photograph (surgeon’s view from above). The tissue band (elevated with sutures) appears to be separate from the superior rectus muscle (SRM). (C) The histopathological specimen of tissue band is stained with hematoxylin-eosin. The tissue consists of collagenized fibrous connective tissue. Note the thickened eosinophilic collagen fibers.
Journal of AAPOS
ings—the close proximity of the superior rectus and superior oblique muscles and their relation with an isointense tissue—support a maldevelopment of epimysium. The ongoing restriction in downgaze despite excision of the tissue band and even after severing the superior rectus muscle suggest an abnormality in orbital fascial structures. The appearance of the trochlea in MRI scans was similar to our previously reported findings in Brown syndrome.10 The clinical features of our case may also be regarded as plus abnormalities with Brown syndrome. It has been demonstrated that ptosis and superior rectus underaction may be associated because of the close proximity of the embryological development of superior rectus and levator palpebrae superioris muscles.7 In our case, the question about the absence of marked ptosis arises despite our suggestion of the involvement of levator palpebrae superioris muscle. We postulate that the fibrous band represents a form of supernumerary levator palpebrae superioris muscle and only that portion of the muscle seems to be affected. In that case marked ptosis may not have developed since the other part of the levator palpebrae superioris muscle is relatively normal. We believe that an inflammatory etiology is unlikely to be responsible for the clinical picture in our case because the development of an accessory tissue band cannot be explained by an inflammatory origin. Since the limitation of ocular motility is not only related to the muscle tissue itself but also to the fascial structures among the extraocular muscles and the orbit, the results of surgery seem unsatisfactory. Only a subtle increase of depression could be obtained. Surgery could possibly have decreased the amount of astigmatism if the excision of the tissue band had been performed at an earlier age. References 1. Gillies EW. Congenital fibrosis of the vertically acting extraocular muscles. Ophthalmology 1995;102:607-12. 2. Harley RD. Congenital fibrosis of the extraocular muscles. Trans Am Ophthalmol Soc 1978;76:197-226.
494
Özkan, Çakmak, and Dayanır
3. Prakash P, Menon V, Ghost G. Congenital fibrosis of superior rectus and superior oblique: A case report. Br J Ophthalmol 1985;69:57-9. 4. Von Ludinghausen M. Bilateral supernumerary rectus muscles of the orbit. Clin Anat 1998;11:271-7. 5. Doherty EJ, Macy ME, Wang SM, Dykeman CP, Melanson MT, Engle EC. CFEOM3: A new extraocular congenital fibrosis syndrome that maps to 16q24.2-q24.3. Invest Ophthalmol Vis Sci 1999; 40:1687-94. 6. Engle EC. The genetic basis of complex strabismus. Pediatr Res 2006;59:342-8.
Volume 11 Number 5 / October 2007
7. Sevel D. A reappraisal of the origin of human extraocular muscles. Ophthalmology 1981;88:1330-8. 8. Sevel D. Ptosis and underaction of the superior rectus muscle. Ophthalmology 1984;91:1080-5. 9. Sevel D. Development of the connective tissue of the extraocular muscles and clinical significance. Graefes Arch Clin Exp Ophthalmol 1988;226:246-51. 10. S¸ener EC, Özkan SB, Arıbal ME, Sanac¸ AS¸, Aslan B. Evaluation of congenital Brown’s syndrome with magnetic resonance imaging. Eye 1996;10:492-6.
Journal of AAPOS