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Hypoplastic inferior rectus muscle in association with accessory extraocular muscle and globe retraction
Short Reports Hypoplastic inferior rectus muscle in association with accessory extraocular muscle and globe retraction Seyhan B. Özkan, MD,a Yelda Özsunar Dayanır, MD,a and Yelda Gökçe Balcı, MDb
Ocular motility problems related to congenital abnormalities of extraocular muscles are rare conditions. Such congenital abnormalities may present in a spectrum from accessory additional rectus muscles to absence of extraocular muscles. Absence of one or more extraocular muscles is a rare condition usually seen in association with craniofacial syndromes and only rarely in isolation.1-8 None of the cases with the absence of an extraocular muscle were reported to be in association with an accessory extraocular muscle or paradoxical contraction of an extraocular muscle. We present a case with bilateral hypoplasia of the inferior rectus muscle with an accessory extraocular muscle in association with globe retraction and -pattern exodeviation.
Kinematic magnetic resonance imaging (MRI) examination was performed to demonstrate the possible paradoxical contraction of extraocular muscles and sagittal, coronal, and axial MRI scans were obtained on a 1.5-Tesla signa unit. MRI examination revealed bilateral hypoplastic inferior rectus muscles with retrobulbar accessory muscle tissue lying below the optic nerve. On kinematic MRI, the accessory muscle tissue was found to contract in downgaze (Figure 2 and Video 1, available at jaapos.org). That muscle tissue appeared to be in anatomical relation with both lateral and medial rectus muscles behind the globe (Figure 3).
Case Reports
A
12-year-old girl presented to the Adnan Menderes University Department of Ophthalmology, Aydın, Turkey, with abnormal eye movements from birth. She was otherwise healthy. On examination, best-corrected visual acuity was 20/25 ( plano ⫹0.75 ⫻ 90) in the right eye and 20/50 ( plano ⫹0.75 ⫻ 90) in the left eye. No abnormal head position or chin depression was observed. There was 1 mm of ptosis in her left eye with 16 mm of levator function. Cover testing was performed and she was orthophoric in the primary position at both near and distance. Although she was orthophoric in upgaze, she had a -pattern exodeviation of 45⌬ in downgaze. She had a marked underaction of bilateral inferior rectus and overaction of bilateral superior oblique muscles with a slight limitation of adduction in her left eye. There was also globe retraction on attempted adduction with some downshoot and also slight upshoot on adduction in the left eye (Figure 1). Fusion was present with Bagolini glasses testing at both near and distance in primary position and upgaze, whereas there was suppression of the left eye in downgaze. The TNO test was negative for stereopsis.
Author affiliations: aDepartment of Ophthalmology, bDepartment of Radiology, Adnan Menderes University, Aydın, Turkey Presented at the 30th Annual Meeting of the European Strabismological Association, Killarney, Ireland, June 2005. Submitted January 12, 2007. Revision accepted April 30, 2007. ¨ niversitesi, Tıp Reprint requests: Dr. Seyhan B. Özkan, Adnan Menderes U Fakültesi, Göz Hast. A.D. 09100, Aydın (email: [email protected]). J AAPOS 2007;11:488-490. Copyright © 2007 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2007/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2007.04.016
488
Discussion Congenital absence of inferior rectus is rare and it is even more unusual for it to occur bilaterally and in the absence of a craniofacial abnormality.1-3 To the best of our knowledge, bilateral hypoplasia of the inferior rectus muscle in association with paradoxical contraction of extraocular muscle and an accessory extraocular muscle has not been reported before. Embryologically, inferior rectus, inferior oblique, and inferior portions of the lateral rectus muscles originate from inferior mesodermal complex.9 Any problem that affects the development of the inferior mesodermal complex might lead to the clinical and radiological findings in our patient. The accessory muscle lying in close proximity with the rectus muscle was shown to contract on downgaze, suggesting that it consisted of muscular tissue rather than fibrotic tissue (Figure 2). The maximal cross-sectional area of an extraocular muscle has been shown to move toward the origin during contraction.10,11 The same finding was observed in both the lateral rectus and the accessory muscles on downgaze on sagittal scans in our patient. Both lateral rectus and the accessory muscles must have received branches of oculomotor nerve. The clues about the possible miswiring in our case are the globe retraction in adduction and the paradoxical contraction of lateral rectus muscle and the accessory rectus muscle on downgaze; these suggested that the presented case has some features of an atypical Duane syndrome. The accessory muscle may represent an atavistic musculus retractor bulbi muscle. The musculus retractor bulbi originates near the optic foramen and runs rostrally, forming a muscular cone that is covered by the rectus muscles. It consists of four separate flat muscular funiculi: the dor-
Journal of AAPOS
Volume 11 Number 5 / October 2007
Özkan, Dayanır and Balcı
489
FIG 1. Ocular motility photographs of the patient in nine positions of gaze. Note the globe retraction in adduction.
FIG 2. The accessory muscle (AcM) in sagittal kinematic MRI scans from upgaze to downgaze of the right eye. Note the contraction of accessory muscle in downgaze. (See also Video 1, available at jaapos.org.)
Journal of AAPOS
490
Özkan, Dayanır and Balcı
Volume 11 Number 5 / October 2007
In our case, the contraction of the accessory muscle in downgaze suggests oculomotor nerve innervation. We suggest that the retrobulbar accessory extraocular muscle may be an atavistic extraocular muscle similar to the musculus retractor bulbi. The unusual findings in the presented case suggested that developmental abnormalities of extraocular muscles must be considered in differential diagnosis for A- or -pattern exotropia. Literature Search Medline (1967-2006) and Exerpta Medica/Embase (19802006), were searched, using the following terms: hypoplastic inferior rectus, inferior rectus hypoplasia, inferior rectus aplasia, musculus retractor bulbi, accessory extraocular muscle, kinematic MRI, and cine MRI. References
FIG 3. Coronal MRI scans of the right (A, C) and left (B, D) eyes. A, B: Posterior orbital area. HIR, hypoplastic inferior rectus muscle. C, D: Coronal scans just posterior to the globe. AcM, Accessory muscle, shown below the optic nerve. Note the relation of accessory muscle with the lateral rectus and medial rectus muscles.
solateral and dorsomedial sections, and the ventrolateral and ventromedial sections. The four muscular funiculi insert at the caudal part of the globe and are mainly innervated by the abducens nerve and occasionally may receive branches from the oculomotor nerve.12 This muscle is found in dogs, cats, rabbits, and avian species but not in humans.13 Valmaggia et al14 reported a patient with an elevation deficit caused by an accessory extraocular muscle under the optic nerve that they attributed to a retractor bulbi muscle. In contrast with our case, the inferior rectus muscle was normal and no globe retraction was observed, whereas the accessory muscle appeared to cause a mechanical restriction on elevation in their case. We suggest that the association of the accessory muscle under the optic nerve with inferior rectus hypoplasia counterbalanced each other and no apparent elevation problem was observed. In a cadaver study, Ludinghausen15 described supernumerary rectus muscles lying sagittally in between the optic nerve and the lateral rectus muscle and joining the terminal part of inferior rectus muscle. Since that muscle was innervated by oculomotor nerve and had muscular bridges to the superior rectus muscle, the author postulated that it was an aberration of the rectus muscle rather than a remnant of musculus retractor bulbi.
1. Lin PY, Yen MY. Congenital absence of bilateral inferior rectus muscles: a case report. J Pediatr Ophthalmol Strabismus 1997;34: 382-4. 2. Pimenides D, Young S, Minty I, Spratt J, Tiffin PA. Familial aplasia of the inferior rectus muscles. J Pediatr Ophthalmol Strabismus 2005;42:222-7. 3. Astle WF, Hill VE, Ells AL, Chi NT, Martinovic E. Congenital absence of the inferior rectus muscle diagnosis and management. J AAPOS 2003;7:339-44. 4. Cooper EL, Greenspan JA. Congenital absence of the inferior rectus muscle. Arch Ophthalmol 1971;86:451-4. 5. Ingham PN, McGovern ST, Crompton JL. Congenital absence of the inferior rectus muscle. Aust NZ J Ophthalmol 1986;14:355-8. 6. Munoz M. Congenital absence of the inferior rectus muscle. Am J Ophthalmol 1996;121:327-9. 7. Majid MA, Ah-Fat FG, Wilson R, Marsh IB. Congenital absence of the inferior rectus muscle in a patient with neurofibromatosis. Eye 2001;15:795-6. 8. Taylor RH, Kraft SP. Aplasia of the inferior rectus muscle. Ophthalmology 1997;104:415-8. 9. Sevel D. Ptosis and underaction of the superior rectus muscle. Ophthalmology 1984;91:1080-5. 10. Demer JL, Miller JM. Magnetic resonance imaging of the functional anatomy of the superior oblique muscle. Invest Ophthalmol Vis Sci 1995;36:906-13. 11. Özkan SB, Arıbal EM, Can D, Karaman ZC. Kinematic magnetic resonance imaging in Y pattern exodeviations. J Pediatr Ophthalmol Strabismus 2003;40:39-43. 12. Shimokawa T, Akita K, Sato T, Ru F, Yi SQ, Tanaka S. Comparative anatomical study of the m. retractor bulbi with special reference to the nerve innervations in rabbits and dogs. Okajimas Folia Anat Jpn 2002;78:235-43. 13. Kleckowska J, Pospieszny N. Morphological examination of the intraorbital muscles (musculi bulbi) in Persian cats in the perinatal period. Anat Histol Embryol 2005;34:15-9. 14. Valmaggia C, Zaunbauer W, Gottlob I. Elevation deficit caused by accessory extraocular muscle. Am J Ophthalmol 1996;121:444-5. 15. Ludinghausen M. Bilateral supernumerary rectus muscles of the orbit. Clin Anat 1998;11:271-7.
Journal of AAPOS
Ocular motility problems related to congenital abnormalities of extraocular muscles are rare conditions. Such congenital abnormalities may present in a spectrum from accessory additional rectus muscles to absence of extraocular muscles. Absence of one or more extraocular muscles is a rare condition usually seen in association with craniofacial syndromes and only rarely in isolation.1-8 None of the cases with the absence of an extraocular muscle were reported to be in association with an accessory extraocular muscle or paradoxical contraction of an extraocular muscle. We present a case with bilateral hypoplasia of the inferior rectus muscle with an accessory extraocular muscle in association with globe retraction and -pattern exodeviation.
Kinematic magnetic resonance imaging (MRI) examination was performed to demonstrate the possible paradoxical contraction of extraocular muscles and sagittal, coronal, and axial MRI scans were obtained on a 1.5-Tesla signa unit. MRI examination revealed bilateral hypoplastic inferior rectus muscles with retrobulbar accessory muscle tissue lying below the optic nerve. On kinematic MRI, the accessory muscle tissue was found to contract in downgaze (Figure 2 and Video 1, available at jaapos.org). That muscle tissue appeared to be in anatomical relation with both lateral and medial rectus muscles behind the globe (Figure 3).
Case Reports
A
12-year-old girl presented to the Adnan Menderes University Department of Ophthalmology, Aydın, Turkey, with abnormal eye movements from birth. She was otherwise healthy. On examination, best-corrected visual acuity was 20/25 ( plano ⫹0.75 ⫻ 90) in the right eye and 20/50 ( plano ⫹0.75 ⫻ 90) in the left eye. No abnormal head position or chin depression was observed. There was 1 mm of ptosis in her left eye with 16 mm of levator function. Cover testing was performed and she was orthophoric in the primary position at both near and distance. Although she was orthophoric in upgaze, she had a -pattern exodeviation of 45⌬ in downgaze. She had a marked underaction of bilateral inferior rectus and overaction of bilateral superior oblique muscles with a slight limitation of adduction in her left eye. There was also globe retraction on attempted adduction with some downshoot and also slight upshoot on adduction in the left eye (Figure 1). Fusion was present with Bagolini glasses testing at both near and distance in primary position and upgaze, whereas there was suppression of the left eye in downgaze. The TNO test was negative for stereopsis.
Author affiliations: aDepartment of Ophthalmology, bDepartment of Radiology, Adnan Menderes University, Aydın, Turkey Presented at the 30th Annual Meeting of the European Strabismological Association, Killarney, Ireland, June 2005. Submitted January 12, 2007. Revision accepted April 30, 2007. ¨ niversitesi, Tıp Reprint requests: Dr. Seyhan B. Özkan, Adnan Menderes U Fakültesi, Göz Hast. A.D. 09100, Aydın (email: [email protected]). J AAPOS 2007;11:488-490. Copyright © 2007 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2007/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2007.04.016
488
Discussion Congenital absence of inferior rectus is rare and it is even more unusual for it to occur bilaterally and in the absence of a craniofacial abnormality.1-3 To the best of our knowledge, bilateral hypoplasia of the inferior rectus muscle in association with paradoxical contraction of extraocular muscle and an accessory extraocular muscle has not been reported before. Embryologically, inferior rectus, inferior oblique, and inferior portions of the lateral rectus muscles originate from inferior mesodermal complex.9 Any problem that affects the development of the inferior mesodermal complex might lead to the clinical and radiological findings in our patient. The accessory muscle lying in close proximity with the rectus muscle was shown to contract on downgaze, suggesting that it consisted of muscular tissue rather than fibrotic tissue (Figure 2). The maximal cross-sectional area of an extraocular muscle has been shown to move toward the origin during contraction.10,11 The same finding was observed in both the lateral rectus and the accessory muscles on downgaze on sagittal scans in our patient. Both lateral rectus and the accessory muscles must have received branches of oculomotor nerve. The clues about the possible miswiring in our case are the globe retraction in adduction and the paradoxical contraction of lateral rectus muscle and the accessory rectus muscle on downgaze; these suggested that the presented case has some features of an atypical Duane syndrome. The accessory muscle may represent an atavistic musculus retractor bulbi muscle. The musculus retractor bulbi originates near the optic foramen and runs rostrally, forming a muscular cone that is covered by the rectus muscles. It consists of four separate flat muscular funiculi: the dor-
Journal of AAPOS
Volume 11 Number 5 / October 2007
Özkan, Dayanır and Balcı
489
FIG 1. Ocular motility photographs of the patient in nine positions of gaze. Note the globe retraction in adduction.
FIG 2. The accessory muscle (AcM) in sagittal kinematic MRI scans from upgaze to downgaze of the right eye. Note the contraction of accessory muscle in downgaze. (See also Video 1, available at jaapos.org.)
Journal of AAPOS
490
Özkan, Dayanır and Balcı
Volume 11 Number 5 / October 2007
In our case, the contraction of the accessory muscle in downgaze suggests oculomotor nerve innervation. We suggest that the retrobulbar accessory extraocular muscle may be an atavistic extraocular muscle similar to the musculus retractor bulbi. The unusual findings in the presented case suggested that developmental abnormalities of extraocular muscles must be considered in differential diagnosis for A- or -pattern exotropia. Literature Search Medline (1967-2006) and Exerpta Medica/Embase (19802006), were searched, using the following terms: hypoplastic inferior rectus, inferior rectus hypoplasia, inferior rectus aplasia, musculus retractor bulbi, accessory extraocular muscle, kinematic MRI, and cine MRI. References
FIG 3. Coronal MRI scans of the right (A, C) and left (B, D) eyes. A, B: Posterior orbital area. HIR, hypoplastic inferior rectus muscle. C, D: Coronal scans just posterior to the globe. AcM, Accessory muscle, shown below the optic nerve. Note the relation of accessory muscle with the lateral rectus and medial rectus muscles.
solateral and dorsomedial sections, and the ventrolateral and ventromedial sections. The four muscular funiculi insert at the caudal part of the globe and are mainly innervated by the abducens nerve and occasionally may receive branches from the oculomotor nerve.12 This muscle is found in dogs, cats, rabbits, and avian species but not in humans.13 Valmaggia et al14 reported a patient with an elevation deficit caused by an accessory extraocular muscle under the optic nerve that they attributed to a retractor bulbi muscle. In contrast with our case, the inferior rectus muscle was normal and no globe retraction was observed, whereas the accessory muscle appeared to cause a mechanical restriction on elevation in their case. We suggest that the association of the accessory muscle under the optic nerve with inferior rectus hypoplasia counterbalanced each other and no apparent elevation problem was observed. In a cadaver study, Ludinghausen15 described supernumerary rectus muscles lying sagittally in between the optic nerve and the lateral rectus muscle and joining the terminal part of inferior rectus muscle. Since that muscle was innervated by oculomotor nerve and had muscular bridges to the superior rectus muscle, the author postulated that it was an aberration of the rectus muscle rather than a remnant of musculus retractor bulbi.
1. Lin PY, Yen MY. Congenital absence of bilateral inferior rectus muscles: a case report. J Pediatr Ophthalmol Strabismus 1997;34: 382-4. 2. Pimenides D, Young S, Minty I, Spratt J, Tiffin PA. Familial aplasia of the inferior rectus muscles. J Pediatr Ophthalmol Strabismus 2005;42:222-7. 3. Astle WF, Hill VE, Ells AL, Chi NT, Martinovic E. Congenital absence of the inferior rectus muscle diagnosis and management. J AAPOS 2003;7:339-44. 4. Cooper EL, Greenspan JA. Congenital absence of the inferior rectus muscle. Arch Ophthalmol 1971;86:451-4. 5. Ingham PN, McGovern ST, Crompton JL. Congenital absence of the inferior rectus muscle. Aust NZ J Ophthalmol 1986;14:355-8. 6. Munoz M. Congenital absence of the inferior rectus muscle. Am J Ophthalmol 1996;121:327-9. 7. Majid MA, Ah-Fat FG, Wilson R, Marsh IB. Congenital absence of the inferior rectus muscle in a patient with neurofibromatosis. Eye 2001;15:795-6. 8. Taylor RH, Kraft SP. Aplasia of the inferior rectus muscle. Ophthalmology 1997;104:415-8. 9. Sevel D. Ptosis and underaction of the superior rectus muscle. Ophthalmology 1984;91:1080-5. 10. Demer JL, Miller JM. Magnetic resonance imaging of the functional anatomy of the superior oblique muscle. Invest Ophthalmol Vis Sci 1995;36:906-13. 11. Özkan SB, Arıbal EM, Can D, Karaman ZC. Kinematic magnetic resonance imaging in Y pattern exodeviations. J Pediatr Ophthalmol Strabismus 2003;40:39-43. 12. Shimokawa T, Akita K, Sato T, Ru F, Yi SQ, Tanaka S. Comparative anatomical study of the m. retractor bulbi with special reference to the nerve innervations in rabbits and dogs. Okajimas Folia Anat Jpn 2002;78:235-43. 13. Kleckowska J, Pospieszny N. Morphological examination of the intraorbital muscles (musculi bulbi) in Persian cats in the perinatal period. Anat Histol Embryol 2005;34:15-9. 14. Valmaggia C, Zaunbauer W, Gottlob I. Elevation deficit caused by accessory extraocular muscle. Am J Ophthalmol 1996;121:444-5. 15. Ludinghausen M. Bilateral supernumerary rectus muscles of the orbit. Clin Anat 1998;11:271-7.
Journal of AAPOS