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Interdisciplinary Neurosurgery: Advanced Techniques and
Case Management
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Case report
Two cases of ventral midbrain cavernous malformations successfully removed through orbitozygomatic interpeduncular approach
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Keiichi Tsuji *, Naoki Nitta, Kenji Takagi, Toshihiro Yokoi, Kazuhiko Nozaki
Department of Neurosurgery, Shiga University of Medical Science, Seta Tsukinowa-cho, Otsu, Shiga 520-2192, Japan
ARTICLE INFO
Article history: Received 18 February 2016 Revised 22 April 2016 Accepted 7 May 2016 Available online xxxx
Keywords:
Ventral midbrain cavernous malformation Cerebral peduncle
Orbitozygomatic interpeduncular approach
ABSTRACT
Ventral midbrain cavernous malformations are rare, and annual bleeding rate is higher than supratentorial lesions. Rebleeding rate is also high if surgical resection is incomplete. The ventral midbrain is deeply located and surrounded by many perforators, which make the approach to this region difficult.
We experienced two cases of ventral midbrain cavernous malformations successfully removed via orbitozygomatic interpeduncular approach. In these cases, most parts of the lesions exist behind the cerebral peduncle extending interpeduncular fossa. In the first case involving a 15-year-old girl, we removed the lesion completely through an ipsilateral orbitozygomatic interpeduncular approach with minimum sacrifice of the right cerebral peduncle. However, in the second case involving a 43-year-old man, the same approach did not reach the lesion behind the ipsilateral cerebral peduncle. At the second operation, a contralateral orbitozygomatic interpeduncular approach was used to remove the residual lesion completely.
Ipsilateral and contralateral orbitozygomatic interpeduncular approaches with minimum destruction of the cerebral peduncle are options for the lesions which exist in the interpeduncular fossa and behind the cerebral peduncle. © 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Cavernous malformations are low flow vascular malformations. Brainstem cavernous malformations account for approximately 1830% of cerebral cavernous malformations [11,24] and 14.2%-25% of them occur at the midbrain [13,31]. The annual bleeding rate of cerebral cavernous malformations is 0.39%-1.3%, however the annual rebleeding rate increases up to 4.5%-22.9% [2,16]. Brainstem cavernous malformations are unique in their higher annual hemorrhagic risk of 21-60% and higher surgical risk than other lesions [1,9,10,14,23,31]. Rehemorrhagic events from residual lesions are also high if surgical resection is incomplete [1,6,12]. Therefore, brainstem cavernous malformations with repeated hemorrhage should be treated aiming complete cure without delay.
The midbrain is composed of a dense concentration of nuclei and fibers which makes it difficult to reach the lesion inside it. However, the ventral lesion between the cerebral peduncles can be approached via the interpeduncular cistern with the orbitozygomatic approach [1], and the transpeduncular approach through the inner one-fifth of the cerebral peduncle is also reported [22]. We experienced two cases of
Abbreviations: MRI, Magnetic resonance imaging.
* Corresponding author. E-mail addresses: tsujikei@belle.shiga-med.ac.jp (K. Tsuji), nnitta@belle.shiga-med.ac.jp (N. Nitta), gitty@belle.shiga-med.ac.jp (K. Takagi), tyokoi@belle.shiga-med.ac.jp (T. Yokoi), noz@belle.shiga-med.ac.jp (K. Nozaki).
ventral midbrain cavernous malformations which were removed successfully with only an ipsilateral orbitozygomatic approach via the interpeduncular cistern in the first case involving a 15-year-old girl, and with ipsi- and contralateral orbitozygomatic approaches by two steps in the second case involving a 43-year-old man both with minimum damage to the cerebral peduncle.
2. Case report
2.1. Case 1
A 15-year-old girl was admitted to our institute to undergo operation for a cavernous malformation in the ventral midbrain. She had been well until 4 months before admission, when occipital headache, diplopia, and ptosis of the right eye developed. On admission to our hospital, neurological examination revealed a moderate degree of right oculomotor nerve palsy. MRI showed that a cavernous malformation was located behind the medial part of the right cerebral peduncle extending into the interpeduncular fossa (Fig.1). She underwent surgical resection via a right orbitozygomatic interpeduncular approach (Fig.2). The sylvian fissure was opened widely and the right oculomotor nerve, right posterior cerebral artery, right superior cerebellar artery, and basilar artery were confirmed. A longitudinal incision of about 5 mm was made on the discolored medial surface of the right cerebral peduncle immediately inferior to the exiting right oculomotor nerve through between the right posterior cerebral artery and the right superior
http://dx.doi.org/10.1016/j.inat.2016.05.003
2214-7519/© 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Fig. 1. MR images and intraoperative findings in case 1. Preoperative T1-weighted image (A),andT2-weightedimage (B) showing a cavernous malformation located in the medial border of the right cerebral peduncle. Intraoperative findings (C, D): the region of incision (asterisk) on the medial surface of the right cerebral peduncle at the lower border of the exit zone of the right oculomotor nerve (arrow) (C) and an exposed mulberry-like lesion (D). ★ indicates right posterior cerebral artery. Postoperative axial T1-weighted (E) at 2 years after surgery showing a complete resection of the lesion.
cerebellar artery, and then the lesion was resected completely (Fig.1). After the operation, her right oculomotor palsy had worsened temporarily, and improved completely at one year after the surgery. The MR1 every 6 months after the surgery has revealed no recurrence for four years until now (Fig.1).
22. Case2
A 43-year-old man who had been diagnosed with an asymptomatic cavernous malformation in the midbrain suffered from a sudden onset of diplopia and right eye ptosis while he was playing golf, and MRI at another hospital showed intralesional hemorrhage and enlargement of the lesion. He was referred to our hospital for operation.
Neurological examination at admission revealed a mild degree of right oculomotor palsy with diplopia and ptosis. MRI at admission showed that the lesion was located behind the medial and lateral part of the right cerebral peduncle extending into interpeduncular fossa (Fig.3). He underwent surgical resection via a right orbitozygomatic interpeduncular approach through the medial surface of the right cerebral peduncle in the same manner of case 1. However, we could not reach the lateral part of the lesion hidden by the right cerebral peduncle (Fig.3). We followed up the patient with serial MRI at an outpatient clinic, and at two years after the first surgery, the right oculomotor palsy worsened and MRI at the time revealed an enlargement of the lesion (Fig.4). After obtaining informed consent, we selected the contralateral
orbitozygomatic interpeduncular approach through the same incision corridor used in the first operation, and the lesion was resected completely (Fig.4). A temporary deterioration of the right oculomotor nerve palsy occurred and left hemianopsia due to compression of the left optic tract was observed after the surgery. The symptoms improved gradually and he only had mild ptosis of the right eye and mild diplopia. Follow-up MRI two years after the second operation showed no recurrence (Fig.4).
3. Discussion
Brainstem cavernous malformations are not frequent in cerebral cavernous malformation [13,31]. Both annual hemorrhage rate and rehemorrhage rate of brainstem cavernous malformations are higher than other cerebral lesions [1,2,9,10,14,16,23,31]. The surgical approach for brainstem cavernous malformations is dictated by the two point method described by Brown et al. [4]. Although the rate of early postoperative morbidity is relatively high, most symptoms improve gradually after the surgery, and microsurgical outcome of brainstem cavernous malformations seems acceptable in cases with complete resection (Table 1). Recently, a transclival approach using endoscopic techniques has also been reported particularly for middle to lower brainstem cavernous malformations [28]. For ventral midbrain lesions transsylvian approaches with some modifications have been used (Table 2). An orbitozygomatic transsylvian approach has been recommended by
Fig. 2. Skin incision and craniotomy of case 1. The head is rotated 30° contralaterally to the surgical side and a semicircular skin incision was made from the inferior edge of the zygoma to the forehead beyond the midline (*). The scalp flap is mobilized anteriorly and at 2-3 cm posterior to the lateral orbital rim, subfascial dissection was made and the deep layer of the temporalis fascia is separated subperiosteally to expose the superior orbital rim, zygomatic process, malar eminence inferior to the zygomaticofacial foramen. After normal frontotemporal craniotomy, the root of the zygomatic arch and the zygomatic bone just above the level of the malar eminence were cut. Periorbita and dura mater of frontal and temporal regions were separated to expose the upper and lateral wall of the orbita. The superior orbital rim was cut at the supraorbital foramen preserving the supraorbital nerve, and the superior and lateral orbital bone was cut down to the inferior orbital fissure to make a free orbitozygomatic piece (★).
several authors to make the operative field shallower and wider [1,27], and the rate of complete resection is high (Table 2). However, a contralateral transsylvian approach to ventral midbrain cavernous malformations has been reported only in one case to our knowledge [1].
The ventral midbrain area delimited above by the posterior cerebral artery, below by the superior cerebellar artery, medially by the oculomotor nerve and basilar artery, and laterally by the pyramidal tract is a fairly safe entry zone [3,5,33], and the lesion of the ventral midbrain is resected from this narrow space. Abla et al. reported 260 cases of brainstem cavernous malformations treated surgically including 48 cases of midbrain lesions [1]. They recommended the orbitozygomatic approach to a lesion at the cerebral peduncle, and presented one case of a ventral midbrain lesion which was successfully removed through the contralateral orbitozygomatic approach. Two other papers reported successful resection through a transpeduncular approach by splitting the medial part of the cerebral peduncle without further neurological deficits [18,22,33]. Our two cases had hemorrhagic lesions causing neurologic deficits and an abutting pial surface and fitted the criteria of surgical resection as Abla and their colleagues described [1,8]. 1n case 1, an ipsilateral approach was enough to remove the lesion with minimal retraction of the cerebral peduncle. However, in case 2, most parts of the lesion located behind the cerebral peduncle and complete resection of the lesion with the ipsilateral orbitozygomatic interpeduncular approach would cause an injury to the right cerebral peduncle, and result in left hemiparesis. Since the patient had deterioration of the symptoms due to an enlargement of the residual lesion, we planned to remove it through a contralateral orbitozygomatic interpeduncular approach to reach the lesion behind the right cerebral peduncle to avoid damage to the right cerebral peduncle. The contralateral approach made it possible to reach the most lateral border of the lesion with successful total resection. However, a deeper operative field and the risk of injuries of perforators from the basilar artery should be considered.
The association of developmental venous anomalies (DVA) must be noted and should be preserved because they drain normal tissues. Fritschi et al. reported that the association of cavernous malformation and venous anomaly in the brainstem was 8% (11 out of 139 cases), and Zimmerman et al. described that the association was 16.6% (4 out of 24 cases). Porter et al. reported a 100% correlation in 86 brainstem cavernous malformations by intraoperative findings [10,25,32]. These reports indicate the importance of not only preoperative imaging studies but also intraoperative inspection, and surgical approach should be selected considering the location of not only cavernous malformations but also DVA to avoid injury of DVA. 1n our cases, preoperative MR images indicated a DVA at the dorsal midbrain in case 1 and no apparent DVA in case 2, and no apparent DVA was observed around the lesions. The transsylvian interpeduncular fossa approach is a reasonable option without making further injury to normal neuronal tissues.
4. Conclusion
This case report indicates that the contralateral orbitozygomatic interpeduncular approach is an option for cavernous malformations of the ventral midbrain. 1f the lesion locates behind the cerebral peduncle facing interpeduncular fossa and extends to the lateral side, the contralateral orbitozygomatic approach may be considered.
Conflicts of interest
References
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Fig. 3. Radiologic images and intraoperative finding of case 2. Preoperative computed tomographic image (A), Tl-weighted image (B), and T2-weighted image (C) showing a cavernous malformation with hemorrhage behind the right cerebral peduncle facing the interpeduncular fossa. Intraoperative finding at first operation (D): the surgical corridor (asterisk) is on the medial surface of the right cerebral peduncle between the right posterior artery and the superior cerebellar artery, inside the right oculomotor nerve (arrow) and outside the basilar artery (★).
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Fig. 4. MR images and intraoperative finding of the second surgery of case 2. Tl-weighted image 6 months after surgery (A) and before the second surgery (B) showing enlargement of the cavernous malformation. Intraoperative findings of the second surgery (C): the surgical corridor is behind the basilar artery (★) between the left posterior cerebral artery and superior cerebellar artery (arrow). Postoperative Tl-weighted image at 2 years after the second surgery showing complete resection and no recurrence (D).
Table 1
Major series of brainstem cavernous malformations in the past 10 years.
Study (authors) Patients Total resection Rebleeds Early morbidity Early mortality Outcome
Ferroli, 2005 [9] 52 cases 92.3% (48/52) NA 44.2% (23/52) 1.9% (1/52) 80.7% improved or same
Cenzato, 2008 [6] 30 cases 90.0% (27/30) 33.3% (1/3) 26.7% (8/30) 0% 96.7% improved or same
Hauck 2009 [13] 44 cases 95.5% (42/44) 100% (2/2) NA 0% 88.6% improved or same
LiH, 2009 [17] 37 cases 100% (37/37) 0% 21.6% (8/37) 0% 94.6% improved or same
Huang, 2010 [14] 22 cases 90.9% (20/22) 50% (1/2) 27.3% (6/22) 0% 86.4% improved or same
Ichinose, 2010 [15] 10 cases 90% (9/10) 100% (1/1) NA 0% 100% improved or same
Ohue, 2010 [23] 36 cases 91.6% (33/36) 33.3% (1/3) 50% (18/36) 0% 91.6% improved or same
de Oliveira, 2010 [8] 45 cases 100% (45/45) 0% 44% (20/45) 0% 88% improved or same
Ramina, 2011 [27] 43 cases 97% (42/43) 0% 14.0% (6/43) 0% 32% improved
Abla, 2011 [1] 260 cases 88.8% (231/260) 62.0% (18/29) 52.7% (137/260) 1.2% (3/260) 68% improved
Takagi, 2013 [29] 18 cases 92.8% (13/14) 33.3% (1/3) 21.4%(3/14) 0% 79% improved or same
MaiJC, 2013 [19] 22 cases 91% (20/22) 0% NA 0% 86% improved or same
Chen, 2014 [7] 38 cases 97.4% (37/38) 0% 34.2% (13/38) 0% 94.7% improved or same
[21] H. Nakase, H. Ohnishi, H. Touho, S. Miyamoto, Y. Watabe, T. Itoh, K. Yamada, K. Shibamoto, J. Karasawa, Surgical excision of a cavernous angioma of the cerebral peduncle by orbito-fronto-malar approach, No Shinkei Geka 21 (1993) 163-166.
[22] T. Ohmura, K. Hirakawa, M. Ohta, H. Utsunomiya, T. Fukushima, Cavernous malformation of the ventral midbrain successfully removed via a transsylvian-transpeduncular approach: case report, Neurol. Med. Chir. (Tokyo) 48 (2008) 569-572.
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[27] R Ramina, T.A. Mattei, P.H. de Aguiar, M.S. Meneses, V.R Ferraz, R Aires, D.F. Kirchhoff, K.D. de Carvalho, Surgical management of brainstem cavernous malformations, Neurol. Sci. 32 (2011) 1013-1028.
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Table 2
Characteristic, location, surgical approach, and outcome of reported cases with ventral midbrain or cerebral peduncle cavernous malformations.
Authors Pt age Location Clinical symptoms Surgical approach Resectability Outcome
Zimmerman RS, 1991 44 Cerebral peduncle Left face/hand numbness, diplopia Subtemporal N/A Improved
[32] [32] Nakase H, 1993 [21] 36 Cerebral peduncle Right hemiparesis, right facial palsy, right Orbitozygomatic(Orbitofrontomalar) Total Improved
cheiro-oral syndrome
Morimoto M, 1996 57 Cerebral peduncle Diplopia, right opthalmalgia Subtemporal Subtotal Rebleeding
[20] [20] Headache, diplopia, nausea, left hemiparesis Peritoneal Total Improved
Takami T, 2003 [30] 67 Mesencephalon Right oculomotor palsy, left facial nerve palsy, Extradural orbitozygomatic Total Improved
left hemiparesis
Quiñones-Hinojosa A, 20 Cerebral peduncle Left oculomotor palsy, right hemiparesis Orbitozygomatic transsylvian Total Improved
2005[26]
Li ST, 2007 [18] 42 Ventral midbrain Left upper extremity tremor, headache, diplopia Transsylvian Total Improved
Ohmura T, 2008 [22] 37 Cerebral peduncle Right dysesthesia, hypesthesia, mild Transsylvian-transpeduncular Total Improved
hemiparesis, left oculomotor palsy
IchinoseT, 2010 [15] 62 Ventral midbrain Diplopia, hemiparesis Orbitozygomatic Total Improved
(mRS 4 ^ 2)
1 Ventral midbrain Hemiparesis Orbitozygomatic, transchoroidal Total Not
fissure determined
Abla AA, 2011 [1] 67 Ventral midbrain Altered consciousness level, dizziness, ataxia (all Orbitozygomatic (contralateral) Total No
improved) deterioration
MaiJC, 2013 [19] 23 Mesencephalothalamic Hemiparesis, hyperreflexia Orbitozygomatic Total Improved
(mRS4 ^ 2)
37 Mesencephalic Mild left limb numbness, partial right CNIII and Orbitozygomatic Total Unchanged
IV palsy (mRS1)
60 Mesencephalic Diplopia, gait ataxia, headache, right Orbitozygomatic Total Unchanged
hemiparesis (mRS2)
57 Mesencephalic Headache, dizziness, impaired tandem gait Orbitozygomatic Total Improves
(mRS2 ^ 1)
38 Mesencephalic Severe headache, tremors, dysphagia Orbitozygomatic Total Improved
(mRS1)
