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MRI of the eye muscles in a case of ophthalmoplegia caused by common carotid artery occlusion suggests ischemic myopathy
Journal of the Neurological Sciences 300 (2011) 176–178
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Short Communication
MRI of the eye muscles in a case of ophthalmoplegia caused by common carotid artery occlusion suggests ischemic myopathy☆ Thurid Sander a, Stefan Gottschalk b, Susanne Hertel a, Birte Neppert c, Christoph Helmchen a,⁎ a b c
Department of Neurology, University Luebeck, Ratzeburger Allee 160, 23538 Luebeck, Germany Department of Neuroradiology, University Luebeck, Germany Department of Ophthalmology, University Luebeck, Germany
a r t i c l e
i n f o
Article history: Received 10 May 2010 Received in revised form 4 August 2010 Accepted 16 September 2010 Available online 8 October 2010 Keywords: Ophthalmoplegia Carotid artery occlusion Muscle oedema
a b s t r a c t Ocular muscle palsies following carotid artery disease is thought to be caused by ischemia of the cranial oculomotor nerves but it may also be due to ischemia of the extraocular muscles (EOM). We studied a patient with common carotid artery occlusion syndrome (CCAOS) to elucidate the two competing hypotheses. MRI and sonography of the orbita showed oedematous swelling of all left EOM. MRI short-tau inversion recovery (STIR) sequences showed hyperintensities and a prolonged T2-relaxation time in EOM indicating muscle oedema. It decreased within two weeks as ophthalmoplegia improved. For several reasons ischemic EOM myopathy rather than ischemic neuropathy seems to be the morphological correlate of ophthalmoplegia after ipsilateral CCAOS in this patient. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Ocular muscle palsies are a rare but known finding following carotid artery disease. The pathomechanism of ophthalmoplegia, however, is not fully understood. It is usually thought to be caused by ischemia of the cranial oculomotor nerves [1–5] but it may also be due to ischemia of the extraocular muscles (EOM) [6,7]. We present a case study of ophthalmoplegia caused by common artery occlusion (CCAOS) based on clinical findings, muscle sonography and orbital MRI. The aim was to provide some evidence for either of the two competing hypotheses.
2. Case report A 48-year-old male patient was admitted with acute onset of diplopia with mild periorbital pain. Within the next hour he developed a right-sided weakness and aphasia, noticed a partial drop of the left eyelid and loss of vision in his left eye. On clinical examination he showed retinal arterial branch occlusion with complete amaurosis, Horner syndrome and complete ophthalmoplegia (3rd, 4th, and 6th cranial nerves) on the left side, partial aphasia and mild right-sided hemiparesis. Trigeminal nerve was not affected. Duplex-sonography (day of admission) and MR-angiography (2 days later) showed an Abbreviations: ACC, common carotid artery; MRI, magnetic resonance imaging; CCAOS, common carotid artery occlusion syndrome; EOM, extraocular muscles; STIR, short-tau inversion recovery. ☆ Dr. Sander is supported by a University Luebeck research grant (E 04-2009). ⁎ Corresponding author. Tel.: + 49 451 500 2927; fax: + 49 451 500 2489. E-mail address: [email protected] (C. Helmchen). 0022-510X/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2010.09.014
occlusion of the left common carotid artery (ACC) without signs of dissection (Fig. 1A, B). Cranial MRI revealed multiple small infarctions in the territory of the left middle cerebral artery. Fundus photography of the left eye one week after symptom onset revealed a cherry-red spot and milky-white oedema of the macula indicating retinal ischemia (Fig. 1C). MRI of the orbita showed oedematous swelling of the left EOM as compared to the healthy right side. Using MRI short-tau inversion recovery (STIR) sequences showed hyperintensities and a prolonged T2-relaxation time in EOM indicating muscle oedema (Fig. 1D, Table 1). The swelling was detected two days after symptom onset, and increased (9 days) and decreased (19 days) on follow up examinations. Orbital sonography 5 days after symptom onset revealed enlargement of the left medial rectus muscle compared to the right with a difference of 0.6 mm. Diagnostic workup was normal and showed no evidence for vasculitis or thyroid disease. ACC occlusion resolved incompletely within 3 days (Fig.1B). Ophthalmoplegia and Horner syndrome improved remarkably over the next 4 weeks while amaurosis persisted. Concomitant to the improvement of ophthalmoplegia oedema of the EOM decreased within two weeks. 3. Discussion Oedematous swelling of the EOM as assessed by MRI and muscle sonography seems to be the prominent morphological abnormality in this post hoc study of a patient with ophthalmoplegia after ipsilateral CCAOS. The vascular supply of the cranial oculomotor nerves largely arises from the inferolateral trunk of the internal carotid artery [4]. It also supplies the ophthalmic nerve (first division of the trigeminal nerve) which was not affected in our patient. Acute axonal block or denervation
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Fig. 1. A and B: Magnetic resonance angiography (2 days after symptom onset) shows occlusion (A) and recanalisation (B) of the left common carotid artery. (A) The carotid artery on the healthy right side (R) is shown on the left side of the angiogram. The lower arrow indicates the origin of the common carotid artery, the middle arrow the bifurcation, and the upper arrow the intracranial part of the internal carotid artery. In contrast, the course of the left carotid artery (L) is missing on the right side of the angiogram with the occluded vessel at its aortic origin. (B) Arrows indicate the course of the reperfused left common/internal carotid artery.C: Fundus photography of left eye one week after symptom onset showing a cherry-red spot and surrounding milky-white oedema in the macula indicating central retinal occlusion. Macula (M), optic disc (OD).D: Coronal STIR MRI of the orbita showing muscle oedema of the left extraocular muscles. Right superior rectus muscle (RSR), left superior rectus muscle (LSR), right medial rectus muscle (RMR), left medial rectus muscle (LMR), right lateral rectus muscle (RLR), left lateral rectus muscle (LLR), and optic nerve (ON).
of muscles can elicit mild muscle swelling which may be evident within one to two days after denervation by high signal intensities using STIR MRI. This enlargement of the intramuscular capillary bed is caused by an increase in the muscle blood volume [8,9] and an increase of extracellular fluid space [10–12]. In contrast, ischemia of the EOM [6,7] elicits depletion of adenosintriphosphate in the muscle cells leading to an intracellular influx of fluid with subsequent muscle swelling. The vascular supply of the EOM is variable as it is provided by branches of the external carotid artery and the ophthalmic artery arising from the internal carotid artery [13]. Thus, signal alterations and swelling of muscles can be recognized by MRI within only a few days after denervation and in muscle ischemia. However, several lines of evidence argue in favour of ischemic EOM myopathy as the morphological correlate of ophthalmoplegia. First, signal alterations in muscle ischemia are usually larger than those following denervation. This may be related to the mechanisms of muscle swelling (increased intracellular fluid vs. enlarged capillaries with increased interstitial fluid). Second, muscle oedema in ischemic myopathy can be partially or completely reversible within days depending on the interval to reperfusion. Accordingly, our patient showed rapid decrease of muscle swelling and signal alteration (T2relaxation time, hyperintensities in STIR) within 2 weeks along with
Table 1 Area (mm2) and circumference (mm) of the extraocular eye muscles cross sections as assessed by coronal MRI analysis. The difference by which the left extraocular eye muscles are larger than the corresponding right eye muscles is given in %.
Area
Circumference
T2-relaxation time
Lateral rectus muscle Medial rectus muscle Superior rectus muscle Lateral rectus muscle Medial rectus muscle Superior rectus muscle Lateral rectus muscle Medial rectus muscle Superior rectus muscle
Right
Left
Difference
38.9 mm2 25.1 mm2 18.1 mm2 23.6 mm 19.9 mm 20.6 mm 65 ± 7 ms 64 ± 9 ms 57 ± 6 ms
66.6 mm2 37.3 mm2 24.3 mm2 31.9 mm 23.1 mm 22.8 mm 90 ± 15 ms 90 ± 17 ms 84 ± 18 ms
71% 49% 34% 35% 16% 11% 38% 40% 47%
partial recovery of ocular motility. Vascular supply of the reperfused external carotid artery might have contributed to improvement of ischemic myopathy. In contrast, muscle oedema due to neuropathy usually increases over time to reach a maximum at about 1 to 4 months after denervation and may continue over 1–2 years [9,14]. Wallerian degeneration following an ischemic axonal block with subsequent nerve sprouting and functional recovery of muscles could not have developed within 2 weeks after denervation. Third, ischemia to the oculomotor nerves should have also affected the trigeminal nerve due to its common supply by the inferolateral trunk of the internal carotid artery. Unfortunately, nerve conduction studies and/or histopathology of both oculomotor nerves and EOM in CCAOS is not available but will be required to prove our hypothesis that ophthalmoplegia in our patient was caused by ischemic myopathy of EOM.
References [1] Lapresle J, Lasjaunias P. Cranial nerve ischaemic arterial syndromes. A review. Brain 1986;109(Pt 1):207–16. [2] Schievink WI, Mokri B, Garrity JA, Nichols DA, Piepgras DG. Ocular motor nerve palsies in spontaneous dissections of the cervical internal carotid artery. Neurology 1993;43(10):1938–41. [3] Serdaru M, Schaison M, Lhermitte F. Pupil sparing in oculomotor palsy and Claude Bernard Horner syndrome. Ann Neurol 1983;14(6):697–8. [4] Vargas ME, Desrouleaux JR, Kupersmith MJ. Ophthalmoplegia as a presenting manifestation of internal carotid artery dissection. J Clin Neuroophthalmol 1992;12(4):268–71. [5] Wessels T, Rottger C, Kaps M, Traupe H, Stolz E. Upper cranial nerve palsy resulting from spontaneous carotid dissection. J Neurol 2005;252(4):453–6. [6] Bogousslavsky J, Pedrazzi PL, Borruat FX, Regli F. Isolated complete orbital infarction: a common carotid artery occlusion syndrome. Eur Neurol 1991;31(2): 72–6. [7] Galetta SL, Leahey A, Nichols CW, Raps EC. Orbital ischemia, ophthalmoparesis, and carotid dissection. J Clin Neuroophthalmol 1991;11(4):284–7. [8] Koltzenburg M, Bendszus M. Imaging of peripheral nerve lesions. Curr Opin Neurol 2004;17(5):621–6. [9] Wessig C, Koltzenburg M, Reiners K, Solymosi L, Bendszus M. Muscle magnetic resonance imaging of denervation and reinnervation: correlation with electrophysiology and histology. Experimental Neurology 2004;185(2):254–61. [10] Holl N, Echaniz-Laguna A, Bierry G, Mohr M, Loeffler JP, Moser T, et al. Diffusionweighted MRI of denervated muscle: a clinical and experimental study. Skeletal Radiol 2008;37(12):1111–7.
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[11] Kikuchi Y, Nakamura T, Takayama S, Horiuchi Y, Toyama Y. MR imaging in the diagnosis of denervated and reinnervated skeletal muscles: experimental study in rats. Radiology 2003;229(3):861–7. [12] Polak JF, Jolesz FA, Adams DF. Magnetic resonance imaging of skeletal muscle. Prolongation of T1 and T2 subsequent to denervation. Invest Radiol 1988;23(5): 365–9.
[13] Hayreh SS. Orbital vascular anatomy. Eye (Lond) 2006;20(10):1130–44. [14] Filler AG, Maravilla KR, Tsuruda JS. MR neurography and muscle MR imaging for image diagnosis of disorders affecting the peripheral nerves and musculature. Neurol Clin 2004;22(3):643 vii.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Short Communication
MRI of the eye muscles in a case of ophthalmoplegia caused by common carotid artery occlusion suggests ischemic myopathy☆ Thurid Sander a, Stefan Gottschalk b, Susanne Hertel a, Birte Neppert c, Christoph Helmchen a,⁎ a b c
Department of Neurology, University Luebeck, Ratzeburger Allee 160, 23538 Luebeck, Germany Department of Neuroradiology, University Luebeck, Germany Department of Ophthalmology, University Luebeck, Germany
a r t i c l e
i n f o
Article history: Received 10 May 2010 Received in revised form 4 August 2010 Accepted 16 September 2010 Available online 8 October 2010 Keywords: Ophthalmoplegia Carotid artery occlusion Muscle oedema
a b s t r a c t Ocular muscle palsies following carotid artery disease is thought to be caused by ischemia of the cranial oculomotor nerves but it may also be due to ischemia of the extraocular muscles (EOM). We studied a patient with common carotid artery occlusion syndrome (CCAOS) to elucidate the two competing hypotheses. MRI and sonography of the orbita showed oedematous swelling of all left EOM. MRI short-tau inversion recovery (STIR) sequences showed hyperintensities and a prolonged T2-relaxation time in EOM indicating muscle oedema. It decreased within two weeks as ophthalmoplegia improved. For several reasons ischemic EOM myopathy rather than ischemic neuropathy seems to be the morphological correlate of ophthalmoplegia after ipsilateral CCAOS in this patient. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Ocular muscle palsies are a rare but known finding following carotid artery disease. The pathomechanism of ophthalmoplegia, however, is not fully understood. It is usually thought to be caused by ischemia of the cranial oculomotor nerves [1–5] but it may also be due to ischemia of the extraocular muscles (EOM) [6,7]. We present a case study of ophthalmoplegia caused by common artery occlusion (CCAOS) based on clinical findings, muscle sonography and orbital MRI. The aim was to provide some evidence for either of the two competing hypotheses.
2. Case report A 48-year-old male patient was admitted with acute onset of diplopia with mild periorbital pain. Within the next hour he developed a right-sided weakness and aphasia, noticed a partial drop of the left eyelid and loss of vision in his left eye. On clinical examination he showed retinal arterial branch occlusion with complete amaurosis, Horner syndrome and complete ophthalmoplegia (3rd, 4th, and 6th cranial nerves) on the left side, partial aphasia and mild right-sided hemiparesis. Trigeminal nerve was not affected. Duplex-sonography (day of admission) and MR-angiography (2 days later) showed an Abbreviations: ACC, common carotid artery; MRI, magnetic resonance imaging; CCAOS, common carotid artery occlusion syndrome; EOM, extraocular muscles; STIR, short-tau inversion recovery. ☆ Dr. Sander is supported by a University Luebeck research grant (E 04-2009). ⁎ Corresponding author. Tel.: + 49 451 500 2927; fax: + 49 451 500 2489. E-mail address: [email protected] (C. Helmchen). 0022-510X/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2010.09.014
occlusion of the left common carotid artery (ACC) without signs of dissection (Fig. 1A, B). Cranial MRI revealed multiple small infarctions in the territory of the left middle cerebral artery. Fundus photography of the left eye one week after symptom onset revealed a cherry-red spot and milky-white oedema of the macula indicating retinal ischemia (Fig. 1C). MRI of the orbita showed oedematous swelling of the left EOM as compared to the healthy right side. Using MRI short-tau inversion recovery (STIR) sequences showed hyperintensities and a prolonged T2-relaxation time in EOM indicating muscle oedema (Fig. 1D, Table 1). The swelling was detected two days after symptom onset, and increased (9 days) and decreased (19 days) on follow up examinations. Orbital sonography 5 days after symptom onset revealed enlargement of the left medial rectus muscle compared to the right with a difference of 0.6 mm. Diagnostic workup was normal and showed no evidence for vasculitis or thyroid disease. ACC occlusion resolved incompletely within 3 days (Fig.1B). Ophthalmoplegia and Horner syndrome improved remarkably over the next 4 weeks while amaurosis persisted. Concomitant to the improvement of ophthalmoplegia oedema of the EOM decreased within two weeks. 3. Discussion Oedematous swelling of the EOM as assessed by MRI and muscle sonography seems to be the prominent morphological abnormality in this post hoc study of a patient with ophthalmoplegia after ipsilateral CCAOS. The vascular supply of the cranial oculomotor nerves largely arises from the inferolateral trunk of the internal carotid artery [4]. It also supplies the ophthalmic nerve (first division of the trigeminal nerve) which was not affected in our patient. Acute axonal block or denervation
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177
Fig. 1. A and B: Magnetic resonance angiography (2 days after symptom onset) shows occlusion (A) and recanalisation (B) of the left common carotid artery. (A) The carotid artery on the healthy right side (R) is shown on the left side of the angiogram. The lower arrow indicates the origin of the common carotid artery, the middle arrow the bifurcation, and the upper arrow the intracranial part of the internal carotid artery. In contrast, the course of the left carotid artery (L) is missing on the right side of the angiogram with the occluded vessel at its aortic origin. (B) Arrows indicate the course of the reperfused left common/internal carotid artery.C: Fundus photography of left eye one week after symptom onset showing a cherry-red spot and surrounding milky-white oedema in the macula indicating central retinal occlusion. Macula (M), optic disc (OD).D: Coronal STIR MRI of the orbita showing muscle oedema of the left extraocular muscles. Right superior rectus muscle (RSR), left superior rectus muscle (LSR), right medial rectus muscle (RMR), left medial rectus muscle (LMR), right lateral rectus muscle (RLR), left lateral rectus muscle (LLR), and optic nerve (ON).
of muscles can elicit mild muscle swelling which may be evident within one to two days after denervation by high signal intensities using STIR MRI. This enlargement of the intramuscular capillary bed is caused by an increase in the muscle blood volume [8,9] and an increase of extracellular fluid space [10–12]. In contrast, ischemia of the EOM [6,7] elicits depletion of adenosintriphosphate in the muscle cells leading to an intracellular influx of fluid with subsequent muscle swelling. The vascular supply of the EOM is variable as it is provided by branches of the external carotid artery and the ophthalmic artery arising from the internal carotid artery [13]. Thus, signal alterations and swelling of muscles can be recognized by MRI within only a few days after denervation and in muscle ischemia. However, several lines of evidence argue in favour of ischemic EOM myopathy as the morphological correlate of ophthalmoplegia. First, signal alterations in muscle ischemia are usually larger than those following denervation. This may be related to the mechanisms of muscle swelling (increased intracellular fluid vs. enlarged capillaries with increased interstitial fluid). Second, muscle oedema in ischemic myopathy can be partially or completely reversible within days depending on the interval to reperfusion. Accordingly, our patient showed rapid decrease of muscle swelling and signal alteration (T2relaxation time, hyperintensities in STIR) within 2 weeks along with
Table 1 Area (mm2) and circumference (mm) of the extraocular eye muscles cross sections as assessed by coronal MRI analysis. The difference by which the left extraocular eye muscles are larger than the corresponding right eye muscles is given in %.
Area
Circumference
T2-relaxation time
Lateral rectus muscle Medial rectus muscle Superior rectus muscle Lateral rectus muscle Medial rectus muscle Superior rectus muscle Lateral rectus muscle Medial rectus muscle Superior rectus muscle
Right
Left
Difference
38.9 mm2 25.1 mm2 18.1 mm2 23.6 mm 19.9 mm 20.6 mm 65 ± 7 ms 64 ± 9 ms 57 ± 6 ms
66.6 mm2 37.3 mm2 24.3 mm2 31.9 mm 23.1 mm 22.8 mm 90 ± 15 ms 90 ± 17 ms 84 ± 18 ms
71% 49% 34% 35% 16% 11% 38% 40% 47%
partial recovery of ocular motility. Vascular supply of the reperfused external carotid artery might have contributed to improvement of ischemic myopathy. In contrast, muscle oedema due to neuropathy usually increases over time to reach a maximum at about 1 to 4 months after denervation and may continue over 1–2 years [9,14]. Wallerian degeneration following an ischemic axonal block with subsequent nerve sprouting and functional recovery of muscles could not have developed within 2 weeks after denervation. Third, ischemia to the oculomotor nerves should have also affected the trigeminal nerve due to its common supply by the inferolateral trunk of the internal carotid artery. Unfortunately, nerve conduction studies and/or histopathology of both oculomotor nerves and EOM in CCAOS is not available but will be required to prove our hypothesis that ophthalmoplegia in our patient was caused by ischemic myopathy of EOM.
References [1] Lapresle J, Lasjaunias P. Cranial nerve ischaemic arterial syndromes. A review. Brain 1986;109(Pt 1):207–16. [2] Schievink WI, Mokri B, Garrity JA, Nichols DA, Piepgras DG. Ocular motor nerve palsies in spontaneous dissections of the cervical internal carotid artery. Neurology 1993;43(10):1938–41. [3] Serdaru M, Schaison M, Lhermitte F. Pupil sparing in oculomotor palsy and Claude Bernard Horner syndrome. Ann Neurol 1983;14(6):697–8. [4] Vargas ME, Desrouleaux JR, Kupersmith MJ. Ophthalmoplegia as a presenting manifestation of internal carotid artery dissection. J Clin Neuroophthalmol 1992;12(4):268–71. [5] Wessels T, Rottger C, Kaps M, Traupe H, Stolz E. Upper cranial nerve palsy resulting from spontaneous carotid dissection. J Neurol 2005;252(4):453–6. [6] Bogousslavsky J, Pedrazzi PL, Borruat FX, Regli F. Isolated complete orbital infarction: a common carotid artery occlusion syndrome. Eur Neurol 1991;31(2): 72–6. [7] Galetta SL, Leahey A, Nichols CW, Raps EC. Orbital ischemia, ophthalmoparesis, and carotid dissection. J Clin Neuroophthalmol 1991;11(4):284–7. [8] Koltzenburg M, Bendszus M. Imaging of peripheral nerve lesions. Curr Opin Neurol 2004;17(5):621–6. [9] Wessig C, Koltzenburg M, Reiners K, Solymosi L, Bendszus M. Muscle magnetic resonance imaging of denervation and reinnervation: correlation with electrophysiology and histology. Experimental Neurology 2004;185(2):254–61. [10] Holl N, Echaniz-Laguna A, Bierry G, Mohr M, Loeffler JP, Moser T, et al. Diffusionweighted MRI of denervated muscle: a clinical and experimental study. Skeletal Radiol 2008;37(12):1111–7.
178
T. Sander et al. / Journal of the Neurological Sciences 300 (2011) 176–178
[11] Kikuchi Y, Nakamura T, Takayama S, Horiuchi Y, Toyama Y. MR imaging in the diagnosis of denervated and reinnervated skeletal muscles: experimental study in rats. Radiology 2003;229(3):861–7. [12] Polak JF, Jolesz FA, Adams DF. Magnetic resonance imaging of skeletal muscle. Prolongation of T1 and T2 subsequent to denervation. Invest Radiol 1988;23(5): 365–9.
[13] Hayreh SS. Orbital vascular anatomy. Eye (Lond) 2006;20(10):1130–44. [14] Filler AG, Maravilla KR, Tsuruda JS. MR neurography and muscle MR imaging for image diagnosis of disorders affecting the peripheral nerves and musculature. Neurol Clin 2004;22(3):643 vii.