正常人及非共同性斜视病人眼外肌及眼球运动神经的MRI研究
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摘要
目的：用MRI研究正常人及非共同性斜视病人眼外肌、眼球运动神经眶内段及脑池段的影像特征。
对象与方法：正常受试者68例,非共同性斜视病人47例。MRI检查序列包括：眼眶部自旋回波T2WI冠状及斜冠状扫描；颅内神经行3D T2-SPACE和：3D-T1 MP RAGE序列扫描。在连续斜冠状MRI影像上追踪和分辨动眼、滑车和外展神经,直至分支进入相应的眼外肌。运用多平面重组技术分别在沿神经长轴的层面显示3对眼球运动神经的走行和毗邻结构。比较两种序列对3对眼球运动神经脑池段的显示情况,于眼外肌最大径线层面测量各条眼外肌的垂直径及水平径,于脑池段斜横断面测量动眼、展神经的直径。观察各型非共同性斜视病人眼外肌和相应眶内段及脑池段眼球运动神经的MRI特征。
结果：正常国人两侧眼外肌对称,且粗细有一定的规律,最大径线层面内各条眼外肌短径大小关系：下直肌>内直肌>上直肌>外直肌；长径大小关系：外直肌>内直肌>上直肌>下直肌。SPACE序列在显示神经及周围血管微细解剖方面优于MP RAGE(χ2=109.109,P=0.000).68例志愿者,动眼神经和外展神经脑池段100%显示,滑车神经87%显示；眶内段外展神经和动眼神经下支的分支完全显示,动眼神经上支65%显示,滑车神经47%显示。脑池段动眼神经、展神经直径平均分别为：2.2mm,1.3mm。眼球后退综合征Ⅰ型9例(13眼),MRI示眶内和脑干区展神经缺如,动眼神经正常,外直肌正常或轻微发育不良,于眶尖区CN3下干紧邻外直肌,外直肌受动眼神经错误的支配。上斜肌轻度发育不良；眼球后退综合征Ⅱ型9例(12眼),MRI示展神经正常,动眼神经正常或轻微发育不良,内直肌正常,外直肌肥大,于眶尖区CN3下干紧邻外直肌,外直肌受外展神经和动眼神经双重支配；先天性眼外肌纤维化病人6例(12眼),MRI示动眼神经严重发育不良,展神经正常或轻微发育不良,视神经中度发育不良,眼外肌广泛纤维化,尤其是上直肌、上睑提肌和外直肌；动眼神经麻痹4例(5眼),展神经麻痹2例(4眼),MRI示脑干区眼运动神经发育不良,相应的眼外肌也发育不良；滑车神经麻痹7例(11眼),MRI示上斜肌发育不良或萎缩；外斜V征7例(14眼),MRI示眼球运动神经正常,下斜肌增宽,上斜肌、上直肌萎缩；分离性垂直偏斜2例(4眼),MRI示眼球运动神经正常,下斜肌增宽；限制性斜视1例(1眼),MRI示眶下壁骨折,下直肌嵌顿。
结论：判断眼外肌大小是否正常可利用双侧眼外肌对称性及眼外肌粗细规律来判断。SPACE序列结合多平面重组技术可以清晰显示眼球运动神经脑池段及其毗邻关系。MRI能辅助临床对一些特殊性斜视做出诊断并提供鉴别诊断依据,从病理解剖学角度为该类斜视的产生机制提供客观依据。
Objective:To study the the structural basis and anatomic changes of extraocular muscles and ocular motor nerves in the orbits and brainstem in normal subjects and humans with noncomitant strabismus by high-resolution MRI.
Objects and methods:Sixty eight normal subjects and forty patients with noncomitant strabismus were performed high resolution MRI across the orbit and the brain-stem level. MR sequences included:EOMs and ocular motor nerves in the orbits were imaged with T2WI coronal and oblique-coronal planes. The ocular motor nerves at the brainstem were performed using 3D T2-SPACE and 3D-T1 MP RAGE. Ocular motor nerves in the orbits were distinguished to the EOMs in consistently oblique coronal planes and nerves in the brainstem were observed in oblique axial, oblique sagittal and coronal planes acquired with MPR. To compare the value of the two sequences in showing the 3 pairs ocular motor nerves in the brainstem. The vertical and horizontal diameters of EOMs in the maximum planes, CN3 and CN6 in the brainstem were measured on the oblique axial planes.
Results:The EOMs of normal Chinese were symmetrical on the two sides, and following a certain rule. The relationships of the short diameters of EOMs in the maximum planes were:IR>MR>SR>LR. That of the long diameters of EOMs were: LR>MR>SR>IR. SPACE sequence had more advantage in showing the ocular motor nerves and adjacent structures than MP RAGE(χ2=109.109, P=0.000). All of 136 CN3 and CN6 of the cisternal segment were well demonstrable in 68 normal subjects (100%). CN4 were depicted 87%. The larger inferior division of CN3 and branches to the target EOMs and CN6 were demonstrated well in all species. The superior division of CN3 was demonstrated 65%, CN4 was showed 47%. The diameters of CN3 and CN4 in the cistern were 2.2mm,1.3mm. Patients with type I DRS (9 cases. 13eyes) exhibited absence of CN6 in both orbit and brainstem regions, normal of CN3. there were no EOMs hypoplasia or LR and SO mild hypoplasia, Apparent branches to the LR were shown in the orbits, which was suggestive of aberrant innervation of LR by CN3. Patients with typeⅡDRS(9 cases,12eyes), CN6 in the affected side was normal, CN3 was normal or mild hypoplasia, the inferior branch of CN3 was close to the LR, the LR had dual-innervation of CN3 and CN6, there were MR normal, LR hypertrophy. Patients with CFEOM (6cases,12eyes), MRI demonstrated severe hypoplasia of CN3, normal or mild hypoplasia of CN6, moderate hypoplasia of the optic nerves, and all EOMs hypoplasia, particularly severe for the SR, LPS and LR. Patients with congenital or chronic CN3 (4 cases, 5eyes) and CN6 (7 cases,11 eyes) palsies had hypoplastic CN3s, CN6s in skull base, with hypoplasia of involved EOMs. Patients with CN4 (2 cases,4eyes) exhibited atrophy or hypoplasia of involved EOMs. Patients with V-exotropia (7 cases,14eyes) had normal ocular motor nerves, exhibited hypertrophy of 10 and atrophy of SO and SR. Patients with DVD (2 cases,4eyes) had normal ocular motor nerves, exhibited hypertrophy of 10. Patients with restrictive strabismus exhibited atrophy of IR, incarceration due to fracture of orbit inferior wall.
Conclusions:Sizes of EOMs can be assessed by the symmetry on the two sides and by observing the usual rule of EOMs. SPACE sequence combined with MPR could precisely show the ocular motor nerves, as well as the relationship with adjacent structures in the cistern. MRI can help to the diagnosis and differential diagnosis of noncomitant strabismus, the disinnervation or displasia of the ocular motor nerves is one of the possible mechanism of strabismus.
对象与方法：正常受试者68例,非共同性斜视病人47例。MRI检查序列包括：眼眶部自旋回波T2WI冠状及斜冠状扫描；颅内神经行3D T2-SPACE和：3D-T1 MP RAGE序列扫描。在连续斜冠状MRI影像上追踪和分辨动眼、滑车和外展神经,直至分支进入相应的眼外肌。运用多平面重组技术分别在沿神经长轴的层面显示3对眼球运动神经的走行和毗邻结构。比较两种序列对3对眼球运动神经脑池段的显示情况,于眼外肌最大径线层面测量各条眼外肌的垂直径及水平径,于脑池段斜横断面测量动眼、展神经的直径。观察各型非共同性斜视病人眼外肌和相应眶内段及脑池段眼球运动神经的MRI特征。
结果：正常国人两侧眼外肌对称,且粗细有一定的规律,最大径线层面内各条眼外肌短径大小关系：下直肌>内直肌>上直肌>外直肌；长径大小关系：外直肌>内直肌>上直肌>下直肌。SPACE序列在显示神经及周围血管微细解剖方面优于MP RAGE(χ2=109.109,P=0.000).68例志愿者,动眼神经和外展神经脑池段100%显示,滑车神经87%显示；眶内段外展神经和动眼神经下支的分支完全显示,动眼神经上支65%显示,滑车神经47%显示。脑池段动眼神经、展神经直径平均分别为：2.2mm,1.3mm。眼球后退综合征Ⅰ型9例(13眼),MRI示眶内和脑干区展神经缺如,动眼神经正常,外直肌正常或轻微发育不良,于眶尖区CN3下干紧邻外直肌,外直肌受动眼神经错误的支配。上斜肌轻度发育不良；眼球后退综合征Ⅱ型9例(12眼),MRI示展神经正常,动眼神经正常或轻微发育不良,内直肌正常,外直肌肥大,于眶尖区CN3下干紧邻外直肌,外直肌受外展神经和动眼神经双重支配；先天性眼外肌纤维化病人6例(12眼),MRI示动眼神经严重发育不良,展神经正常或轻微发育不良,视神经中度发育不良,眼外肌广泛纤维化,尤其是上直肌、上睑提肌和外直肌；动眼神经麻痹4例(5眼),展神经麻痹2例(4眼),MRI示脑干区眼运动神经发育不良,相应的眼外肌也发育不良；滑车神经麻痹7例(11眼),MRI示上斜肌发育不良或萎缩；外斜V征7例(14眼),MRI示眼球运动神经正常,下斜肌增宽,上斜肌、上直肌萎缩；分离性垂直偏斜2例(4眼),MRI示眼球运动神经正常,下斜肌增宽；限制性斜视1例(1眼),MRI示眶下壁骨折,下直肌嵌顿。
结论：判断眼外肌大小是否正常可利用双侧眼外肌对称性及眼外肌粗细规律来判断。SPACE序列结合多平面重组技术可以清晰显示眼球运动神经脑池段及其毗邻关系。MRI能辅助临床对一些特殊性斜视做出诊断并提供鉴别诊断依据,从病理解剖学角度为该类斜视的产生机制提供客观依据。
Objective:To study the the structural basis and anatomic changes of extraocular muscles and ocular motor nerves in the orbits and brainstem in normal subjects and humans with noncomitant strabismus by high-resolution MRI.
Objects and methods:Sixty eight normal subjects and forty patients with noncomitant strabismus were performed high resolution MRI across the orbit and the brain-stem level. MR sequences included:EOMs and ocular motor nerves in the orbits were imaged with T2WI coronal and oblique-coronal planes. The ocular motor nerves at the brainstem were performed using 3D T2-SPACE and 3D-T1 MP RAGE. Ocular motor nerves in the orbits were distinguished to the EOMs in consistently oblique coronal planes and nerves in the brainstem were observed in oblique axial, oblique sagittal and coronal planes acquired with MPR. To compare the value of the two sequences in showing the 3 pairs ocular motor nerves in the brainstem. The vertical and horizontal diameters of EOMs in the maximum planes, CN3 and CN6 in the brainstem were measured on the oblique axial planes.
Results:The EOMs of normal Chinese were symmetrical on the two sides, and following a certain rule. The relationships of the short diameters of EOMs in the maximum planes were:IR>MR>SR>LR. That of the long diameters of EOMs were: LR>MR>SR>IR. SPACE sequence had more advantage in showing the ocular motor nerves and adjacent structures than MP RAGE(χ2=109.109, P=0.000). All of 136 CN3 and CN6 of the cisternal segment were well demonstrable in 68 normal subjects (100%). CN4 were depicted 87%. The larger inferior division of CN3 and branches to the target EOMs and CN6 were demonstrated well in all species. The superior division of CN3 was demonstrated 65%, CN4 was showed 47%. The diameters of CN3 and CN4 in the cistern were 2.2mm,1.3mm. Patients with type I DRS (9 cases. 13eyes) exhibited absence of CN6 in both orbit and brainstem regions, normal of CN3. there were no EOMs hypoplasia or LR and SO mild hypoplasia, Apparent branches to the LR were shown in the orbits, which was suggestive of aberrant innervation of LR by CN3. Patients with typeⅡDRS(9 cases,12eyes), CN6 in the affected side was normal, CN3 was normal or mild hypoplasia, the inferior branch of CN3 was close to the LR, the LR had dual-innervation of CN3 and CN6, there were MR normal, LR hypertrophy. Patients with CFEOM (6cases,12eyes), MRI demonstrated severe hypoplasia of CN3, normal or mild hypoplasia of CN6, moderate hypoplasia of the optic nerves, and all EOMs hypoplasia, particularly severe for the SR, LPS and LR. Patients with congenital or chronic CN3 (4 cases, 5eyes) and CN6 (7 cases,11 eyes) palsies had hypoplastic CN3s, CN6s in skull base, with hypoplasia of involved EOMs. Patients with CN4 (2 cases,4eyes) exhibited atrophy or hypoplasia of involved EOMs. Patients with V-exotropia (7 cases,14eyes) had normal ocular motor nerves, exhibited hypertrophy of 10 and atrophy of SO and SR. Patients with DVD (2 cases,4eyes) had normal ocular motor nerves, exhibited hypertrophy of 10. Patients with restrictive strabismus exhibited atrophy of IR, incarceration due to fracture of orbit inferior wall.
Conclusions:Sizes of EOMs can be assessed by the symmetry on the two sides and by observing the usual rule of EOMs. SPACE sequence combined with MPR could precisely show the ocular motor nerves, as well as the relationship with adjacent structures in the cistern. MRI can help to the diagnosis and differential diagnosis of noncomitant strabismus, the disinnervation or displasia of the ocular motor nerves is one of the possible mechanism of strabismus.
引文
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[1]Jiao YH, Zhao KX, Wang ZC,et al.Detailed magnetic resonance imaging findings of the ocular motor nerves in Duane's retraction syndrome[J].J Pediatr Ophthalmol Strabismus,2009,46(5):278-285.
[2]Jiao YH, Zhao KX, Wang ZC,et al.Man FY. Magnetic resonance imaging of the ocular motor nerves in normal volunteers[J].Chin J Ophthalmol (Chin),2009,45 (3):219-224.
[3]Demer JL.Inflection in inactive lateral rectus muscle:evidence suggesting focal mechanical effects of connective tissues[J].Invest Ophthalmol Vis Sci,2008,49(11): 4858-4864.
[4]Kim JH, Hwang JM.Hypoplastic oculomotor nerve and absent abducens nerve in congenital fibrosis syndrome and synergistic divergence with magnetic resonance imaging [J].Ophthalmology 2005,112(4):728-732.
[5]Demer JL, Clark RA, Engle EC.Magnetic resonance imaging evidence for widespread orbital dysinnervation in congenital fibrosis of extraocular muscles due to mutations in KIF21 A[J].Invest Ophthalmol Vis Sci,2005,46(2):530-539.
[6]Demer JL, Clark RA, Lim KH,et al.Magnetic resonance imaging evidence for widespread orbital dysinnervation in dominant Duane's retraction syndrome linked to the DURS2 locus[J].Invest Ophthalmol Vis Sci,2007,48(1):194-202.
[7]Ouanounou S, Saigal G, Birchansky S.Mobius syndrome[J].AJNR Am J Neuroradiol,2005,26(2):430-432.
[8]Engle EC.The genetic basis of complex strabismus[J].Pediatr Res,2006,59(3): 343-348.
[9]Das VE, Mustari MJ.Correlation of cross-axis eye movements and motoneuron activity in non-human primates with "A" pattern strabismus[J].Invest Ophthalmol Vis Sci,2007,48(2):665-674.
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[11]Demer JL, Ortube MC, et al.High-resolution magnetic resonance imaging demonstrates abnormalities of motor nerves and extraocular muscles in patients with neuropathic strabismus[J].J AAPOS,2006,10(2):135-142.
[12]Naraslmban A,Tycbsen L,Poukens V,el al.Horizontal rectus muscle anatomy in naturally and artificially strabismic monkeys[J].Invest Ophthalmol Vis Sci,2007,48 (6):2576-2588.
[13]Joseph L. Demer,Maria Carolina Ortube,Elizabeth C. Engle,el al. High-Resolution Magnetic Resonance Imaging Demonstrates Abnormalities of Motor Nerves and Extraocular Muscles in Patients With Neuropathic Strabismus [J].J AAPOS,2006,10(2):135-142.
[14]Demer JL. A 12 year, prospective study of extraocular muscle imaging in complex strabismus[J].J AAPOS,2003,6(6):337-347.
[15]Demer, JL. Anatomy of strabismus. In:Taylor, D.; Hoyt, C., editors.Pediatric ophthalmology and strabismus.3.[M].London:Elsevier,2005:849-861.
[16]Demer JL, Kono R, Wright W. Magnetic resonance imaging of human extraocular muscles in convergence[J].J Neurophysiol,2003,89(4):2072-2085.
[17]Demer JL, Oh SY, Clark RA, et al.Evidence for a pulley of the inferior oblique muscle[J].Invest Ophthalmol Vis Sci,2003,44(9):3856-3865.
[18]Kono R, Demer JL.Magnetic resonance imaging of the functional anatomy of the inferior oblique muscle in superior oblique palsy[J].Ophthalmology,2003,110 (6):1219-1229.
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[20]Lane JI,Ward H,Witte RJ,et al.3-T imaging of the cochlear nerve and labyrinth in cochlear-implant candidates:3D fast recovery fast spin-echo versus 3D constructive interference in the steady state techniqnes[J].AJNR,2004,25(4):618-622.
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[22]Jun SB,Kim HJ,Yoo JY,et al.MR imaging of the internal auditory canal and inner ear at 3T:comparison between 3D driven equilibrium and 3D balanced fast field echo sequences [J].Korean J Radiol,2008,9(3):212-218.
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[25]Sujay Sheth,BA Barton F,Branstetter IV, et al.Appearance of Normal Cranial Nerves on Steady-State Free Precession MR Images[J].RadioGraphics,2009,29 (4):1045-1055
[26]Chavhan GB, Babyn PS, Jankharia BG,et al.Steady-state MR imaging sequences: physics, classification, and clinical applications[J].RadioGraphics,2008,28(4):1147-1160.
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[1]Jiao YH, Zhao KX, Wang ZC,et al.Detailed magnetic resonance imaging findings of the ocular motor nerves in Duane's retraction syndrome[J].J Pediatr Ophthalmol Strabismus,2009,46(5):278-285.
[2]Jiao YH, Zhao KX, Wang ZC,et al.Man FY. Magnetic resonance imaging of the ocular motor nerves in normal volunteers[J].Chin J Ophthalmol (Chin),2009,45 (3):219-224.
[3]Demer JL.Inflection in inactive lateral rectus muscle:evidence suggesting focal mechanical effects of connective tissues[J].Invest Ophthalmol Vis Sci,2008,49(11): 4858-4864.
[4]Kim JH, Hwang JM.Hypoplastic oculomotor nerve and absent abducens nerve in congenital fibrosis syndrome and synergistic divergence with magnetic resonance imaging [J].Ophthalmology 2005,112(4):728-732.
[5]Demer JL, Clark RA, Engle EC.Magnetic resonance imaging evidence for widespread orbital dysinnervation in congenital fibrosis of extraocular muscles due to mutations in KIF21 A[J].Invest Ophthalmol Vis Sci,2005,46(2):530-539.
[6]Demer JL, Clark RA, Lim KH,et al.Magnetic resonance imaging evidence for widespread orbital dysinnervation in dominant Duane's retraction syndrome linked to the DURS2 locus[J].Invest Ophthalmol Vis Sci,2007,48(1):194-202.
[7]Ouanounou S, Saigal G, Birchansky S.Mobius syndrome[J].AJNR Am J Neuroradiol,2005,26(2):430-432.
[8]Engle EC.The genetic basis of complex strabismus[J].Pediatr Res,2006,59(3): 343-348.
[9]Das VE, Mustari MJ.Correlation of cross-axis eye movements and motoneuron activity in non-human primates with "A" pattern strabismus[J].Invest Ophthalmol Vis Sci,2007,48(2):665-674.
[10]JIAO Yong-hong, ZHAO Kan-xing, WANG Zhen-chang,et al. Magnetic resonance imaging of the extraocular muscles and corresponding cranial nerves in patients with special forms of strabismus [J]. Chin Med J,2009,122(24):2998-3002.
[11]Demer JL, Ortube MC, et al.High-resolution magnetic resonance imaging demonstrates abnormalities of motor nerves and extraocular muscles in patients with neuropathic strabismus[J].J AAPOS,2006,10(2):135-142.
[12]Naraslmban A,Tycbsen L,Poukens V,el al.Horizontal rectus muscle anatomy in naturally and artificially strabismic monkeys[J].Invest Ophthalmol Vis Sci,2007,48 (6):2576-2588.
[13]Joseph L. Demer,Maria Carolina Ortube,Elizabeth C. Engle,el al. High-Resolution Magnetic Resonance Imaging Demonstrates Abnormalities of Motor Nerves and Extraocular Muscles in Patients With Neuropathic Strabismus [J].J AAPOS,2006,10(2):135-142.
[14]Demer JL. A 12 year, prospective study of extraocular muscle imaging in complex strabismus[J].J AAPOS,2003,6(6):337-347.
[15]Demer, JL. Anatomy of strabismus. In:Taylor, D.; Hoyt, C., editors.Pediatric ophthalmology and strabismus.3.[M].London:Elsevier,2005:849-861.
[16]Demer JL, Kono R, Wright W. Magnetic resonance imaging of human extraocular muscles in convergence[J].J Neurophysiol,2003,89(4):2072-2085.
[17]Demer JL, Oh SY, Clark RA, et al.Evidence for a pulley of the inferior oblique muscle[J].Invest Ophthalmol Vis Sci,2003,44(9):3856-3865.
[18]Kono R, Demer JL.Magnetic resonance imaging of the functional anatomy of the inferior oblique muscle in superior oblique palsy[J].Ophthalmology,2003,110 (6):1219-1229.
[19]Kono R,Clark RA,Demer JL. Active pulleys:Magnetic resonance imaging of rectus muscle paths in tertiary gazes [J]. In vest Ophthalmol Vis Sci,2002,43 (7):2179-2188.
[20]Lane JI,Ward H,Witte RJ,et al.3-T imaging of the cochlear nerve and labyrinth in cochlear-implant candidates:3D fast recovery fast spin-echo versus 3D constructive interference in the steady state techniqnes[J].AJNR,2004,25(4):618-622.
[21]Shinji N,Tokiko K,Hiroshi F,et al.MR cisternography of the cerebellopontine an-gle：comparison of three-dimensional fast asymmetrical spin-echo and three-dimensional constructive interference in the steady-state sequences [J]. AJNR, 2001,22(6):1179-1185.
[22]Jun SB,Kim HJ,Yoo JY,et al.MR imaging of the internal auditory canal and inner ear at 3T:comparison between 3D driven equilibrium and 3D balanced fast field echo sequences [J].Korean J Radiol,2008,9(3):212-218.
[23]Held P,Nitz W,Seitz J,et al.Comparison of 2D and 3D MRI of the optic and oculomotor nerve anatomy[J].Clin Imaging,2000,24(6):337-43.
[24]Yousry I,Moriggl B,Dieterich M,et al.MR anatomy of the proximal cisternal segment of the trochlear nerve:neurovascular relationships and landmarks[J]. Radiology,2002,223(1):31-38.
[25]Sujay Sheth,BA Barton F,Branstetter IV, et al.Appearance of Normal Cranial Nerves on Steady-State Free Precession MR Images[J].RadioGraphics,2009,29 (4):1045-1055
[26]Chavhan GB, Babyn PS, Jankharia BG,et al.Steady-state MR imaging sequences: physics, classification, and clinical applications[J].RadioGraphics,2008,28(4):1147-1160.
[27]Schmitz B, Hagen T, Reith W.Three-dimensional true FISP for high-resolution imaging of the whole brain[J].Eur Radiol,2003,13(7):1577-1582.
[28]Mikami T, Minamida Y, Yamaki T,et al.Cranial nerve assessment in posterior fossa tumors with fast imaging employing steady-state acquisition (FIESTA)[J]. Neurosurg Rev,2005,28(4):261-266.
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