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Surgical treatment of cavernous malformations involving medulla oblongata
Journal of Clinical Neuroscience xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Case study
Surgical treatment of cavernous malformations involving medulla oblongata Si Zhang 1, Sen Lin 1, Xuhui Hui, Hao Li, Chao You ⇑ Department of Neurosurgery, West China Hospital of Sichuan University, Chengdu, Sichuan, China
a r t i c l e
i n f o
Article history: Received 11 June 2016 Accepted 28 November 2016 Available online xxxx Keywords: Medulla oblongata Brainstem Cavernous malformation Microsurgery
a b s t r a c t Surgical treatment of cavernous malformations (CMs) involving medulla oblongata is more difficult than the CMs in other sites because of the surrounding vital structures. However, the distinctive features and treatment strategies have not been well illustrated. Therefore, we enrolled a total of 19 patients underwent surgical treatment of CMs involving medulla oblongata in our hospital from August 2008 to August 2014. The clinical features, surgical management and clinical outcome of these patients were retrospectively analyzed, while our institutional surgical indications, approaches and microsurgical techniques were discussed. In our study, gross total resection was achieved in 17 patients and subtotal resection in 2. Two patients underwent emergency surgeries due to severe and progressive neurological deficits. The postoperative new-onset or worsened neurological deficits occurred in 6 patients. After a mean follow-up of 45.8 ± 22.2 months, the neurological status was improved in 10 patients and remained stable in 7. The mean modified Rankin Scale (mRS) was 2.58 ± 1.26 preoperatively, 3.11 ± 0.99 postoperatively and 1.84 ± 1.42 at the recent follow-up, respectively. During the follow-up period, no rehemorrhage and recurrence occurred, and the residual lesions remained stable. We recommended surgical resection of symptomatic CMs involving medulla oblongata via optimal approaches, feasible entry zones and meticulous microsurgical techniques in attempting to achieve safe resection and favorable outcome. The clinical features, surgical indications, timing and microsurgical techniques of this special entity should be distinctive from the brainstem cavernous malformations in other sites. Ó 2016 Published by Elsevier Ltd.
1. Introduction Since brainstem cavernous malformations (CMs) are associated with higher hemorrhagic rates and poorer neurological outcome [1,2], microsurgical resection has been considered to be the optimal treatment [3,4]. In the last two decades, remarkable progress has been achieved in surgical treatment of brainstem CM and it is consensus that the primary goal of the surgery is to prevent further hemorrhage rather than neurological recovery [3–5]. Therefore, the surgical strategy of brainstem CMs has become how to balance the hemorrhagic morbidities and surgery-related morbidities. CMs involving medulla oblongata, as a more special entity of brainstem CMs, are of unique features comparing to the other sites. The CMs located in medulla oblongata and pontomedullary could be associated with potential life-threatening symptoms and the
⇑ Corresponding author at: Department of Neurosurgery, West China Hospital of Sichuan University, 37 Guo Xue Xiang, Wu Hou District, Chengdu 610041, China. Fax: +86 28 85164009. E-mail address: [email protected] (C. You). 1 Zhang and Lin contributed equally in this study as the co-first authors.
proximity to critical structures may pose a particular challenge to microsurgical resection. Therefore, we advocated that the surgery-related decision-making criteria, timing, surgical techniques and clinical outcome should be reconsidered. Based on our experience in surgical treatment of 19 patients harboring CMs involving medulla oblongata, we aim to evaluate the clinical features and neurofunctional outcome of these patients and summarize our institutional experience on surgical indications, timing and microsurgical techniques of this disease. 2. Methods 2.1. Clinical chart From August 2008 to August 2014, nineteen consecutive patients with CMs involving medulla oblongata underwent surgical treatment in our hospital. The clinical data including age, gender, symptoms and neurological signs at admission were retrospectively analyzed. The present study was approved by the West China Hospital Trials and Biomedical Ethics Committee. The mRS was used to evaluate the neurological status. Preoperatively,
http://dx.doi.org/10.1016/j.jocn.2016.11.014 0967-5868/Ó 2016 Published by Elsevier Ltd.
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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S. Zhang et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
cranial Computer Tomography (CT), Magnetic Resonance Imaging (MRI) with contrast enhancement and Diffusion Tensor Tractography (DTT) were performed as routine.
Table 1 Symptoms and signs on admission. Symptoms and signs
2.2. Surgery Our institutional surgical indication was CMs involving medulla oblongata which presented with symptomatic acute and subacute hemorrhage and were surgically accessible. We preferred performing the surgery during the subacute stage due to the favorable dissection plane. However, for patients with severe and progressive neurological deficits such as weakness of gag reflex and respiratory dysfunction, emergency surgery should be performed. Somatosensory evoked potentials, motor evoked potentials and brainstem auditory evoked potentials were monitored routinely. Recording needles were inserted into the orbicularis oris, orbicularis oculi muscles, the posterior pharyngeal wall and the tongue bilaterally. A stimulation probe was applied for cranial nerve nuclei and corticospinal tract mapping. The selection of the surgical approach was tailored individually. The safe entry zone was determined by the integration of anatomical landmarks, pial presentation, preoperative DTT, intraoperative neuronavigation and nuclei mapping. Standard microsurgical exposure and resection was performed including low-power bipolar coagulation and sharp dissection. Generally, an en bloc resection and elaborate exploration of the wall of hematoma cavity was attempted to improve the possibility of complete resection. However, if the hemodynamic instability occurred during separation of the lesion, piecemeal resection should be adopted. The developmental venous anomalies (DVAs) and the hemosiderin-stained gliotic tissues were preserved. 2.3. Follow-up and clinical outcome Postoperative complications and the new-onset or worsened neurological deficits were recorded, mRS was used to evaluate the neurological status postoperatively (3 days after the surgery). The follow-up was performed at 6 months after surgery and once a year thereafter. During the follow-up period, changes in neurological deficits (improved, stable or aggravated) and mRS were assessed in outpatient center. mRS scores of 1–2 was considered as favorable outcome. Experts of neuroimaging processed the cross analysis of the MRI to identify the recurrence and rehemorrhage. 3. Results There were 7 males and 12 females with a mean age of 39.74 ± 10.68 years (range from 15 to 58 years). All the patients presented with symptoms of one or more hemorrhagic episodes (10 patients presented with single episode of hemorrhage, 6 patients with two episodes and 2 patients with three or more episodes. one patient underwent the surgery for CM located in medulla oblongata 10 years ago, and suffered from rehemorrhage this time). The calculative annual hemorrhage rate was 4.24% (assuming that all CMs generated since birth) and the annual rehemorrhage rate was 54.17%. The most common symptom was sudden onset of cranial nerve dysfunction (n = 14) including dysphagia (n = 6), dysarthria (n = 4), facial (n = 3) and abducent paralysis (n = 3), cardiac instability (n = 2) and neck pain (n = 2). Other symptoms and neurological signs included hemiparesthesia (n = 11), hemiparesis (n = 9), ataxia (n = 5), headache (n = 2) and respiratory dysfunction (n = 3) (Table 1). The mean mRS score was 2.58 ± 1.26 preoperatively. According to the locations of these lesions, all the cases were divided into 3 groups: upper dorsal
Cranial nerve deficits Oculomotor paralysis Abducent paralysis Facial paralysis Dysphagia Dysarthria Cardiac instability Neck pain Hemiparesthesia and body numbness Hemiparesis Ataxia Headache Respiratory dysfunction
Lesion location, n Upper dorsal medulla involvement
Lower dorsal medulla involvement
Ventrolateral medulla involvement
4 0 1 2 1 1 2 0 2
4 0 0 0 2 1 0 1 1
10 1 2 1 3 2 0 1 8
1 1 2 2
0 0 0 0
8 4 0 1
medulla involvement (n = 6), lower dorsal medulla involvement (n = 3) and ventrolateral medulla involvement (n = 10). 3.1. Surgery Seventeen patients underwent surgical treatment in subacute phase after hemorrhage (Fig. 1), and two patients were taken for the emergency surgery (one for acute severe dysphagia combined with coma for 30 min, and one for progressive respiratory dysfunction) (Fig. 2). The following approaches were adopted: suboccipital approach (n = 9, including telovelar approach in 6 cases) (Fig. 3), retrosigmoid approach (n = 5) and far lateral approach (n = 5). Gross total resections were achieved in 17 cases, while subtotal resections were performed in 2 cases. These two lesions were observed involving the obex, and when we attempted to shrink the lesion away from eloquent hemosiderin-stained gliotic tissue, drastic cardiac instability occurred. Intraoperatively, the DVAs were observed in 4 cases (21.05%), and all the typical caput medusae structures were preserved carefully. The surrounding hemosiderin-stained gliotic tissues were preserved in all cases. 3.2. Complications and follow up Postoperative new-onset or worsened neurological deficits occurred in 6 patients including dysphagia (n = 1), dysarthria (n = 1), paresthesia (n = 2), ataxia (n = 2) and walking difficulty (n = 1). No surgical related hemiparesis occurred. The mean mRS 3 days after the surgery was 3.11 ± 0.99. One patient suffered from postoperative hydrocephalus, who was performed the VentriclePeritoneal shunt. Gastrostomy tube was placed in 6 patients who suffered from dysphagia preoperatively and two patients who presented with new onset of lower cranial nerves deficits. Tracheostomy was performed for the patients who suffered from respiratory dysfunction (n = 1) or severe aspiration pneumonia (n = 2). One patient required the ventilator due to preoperative respiratory failure despite an emergency surgery was performed, the patient died due to postoperative pneumonia eventually. Other complications included intracranial infection (n = 1) and aspiration pneumonia (n = 2). All the patients underwent routine follow-up. After a mean follow-up of 45.8 ± 22.2 months (range from 18 to 78 months), the preoperative neurological status was improved in 10 patients and remained stable in 7. The postoperative new-onset or worsened symptoms were improved in 5 patients and remained stable in 1. At the recent follow-up, the mean mRS was 1.84 ± 1.42 and 15
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
S. Zhang et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
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Fig. 1. Pre- and postoperative MRI of CM involving medulla oblongata. A 41-year-old female presented with four episodes of symptomatic hemorrhage in 3 years. Axial T1 (A), T2 (B) and contrast-enhanced (C) MRI revealed a CM involving upper dorsal medulla oblongata. The surgery was performed via telovelar approach. Postoperatively, she recovered with only mild ataxia. Postoperative axial T1 (E), T2 (F) and contrast-enhanced (G) MRI showed complete excision of the CM.
patients achieved favorable outcome (Table 2). All the patients with CMs involving the lower dorsal medulla (n = 3) in our series achieved favorable outcome with a mean mRS score of 1.00 ± 1.00. Seven patients (70%) with CMs involving ventrolateral medulla achieved favorable outcome with a mean mRS score of 2.10 ± 0.99. During the follow-up period, no rehemorrhage and recurrence occurred, and the residual lesions remained stable.
4. Discussion Rather than commonly located in the pontine, only approximately 10–20% of brainstem CMs were reported involving the medulla oblongata (Table 3) [3–7]. Due to the proximity to the critical neural structures, clinical presentations of hemorrhagic CMs involving medulla oblongata are more severe and lifethreatening. Moreover, the slightest damage to a vital structure caused by surgical intervention can result in fatal neurological deficits such as aspiration and respiratory dysfunction. Therefore, we considered that the hemorrhagic CMs involving medulla oblongata would be associated with distinctive features that the surgical indications, optimal timing, surgical techniques and clinical outcome should be emphasized separately.
4.1. Clinical features and outcome Generally, the symptoms of CMs involving medulla oblongata are correlated with the involvement of critical neural structures in different locations [8]. In our series, lower cranial nerve dysfunctions remained to be the most common pre- and postoperative symptoms. Tongue weakness and dysphagia caused by compression of the hypoglossal and ambiguus nuclei or surgical intervention were common neurological dysfunctions which might lead to life-threatening aspiration. Therefore, for patients with lower cranial nerve dysfunctions, routine placement of gastrostomy tube was recommended. According to the results of DTT, patients presented with hemiparesis in our series were more due to the compression from the lesions than destruction of the corticospinal tract. Hence, it would be reasonable to release the mass effect via surgical resection in aiming at achieving a favorable recovery. Moreover, three patients in our series presented with obex symptoms including one patient had sudden onset of severe respiratory failure. Obex involvement was considered as the most serious situation in this entity, thus the tracheostomy should be performed preoperatively and an emergency craniotomy be taken. The other symptoms such as hemiparesthesia and body numbness mostly occurred in patients with lesions located ventrolaterally, which
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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tomatic acute and subacute hemorrhage and are surgically accessible. The appropriate timing of surgery is still controversial [11]. Some authors have recommended operating during the subacute stage due to the better neurological status [12]. Whereas Bruneau et al. indicated that early surgery could promptly release the mass effect on brainstem nuclei and tracts, and thus improve the neurological outcome [13]. For CMs involving medulla oblongata in our series, we preferred performing the surgery during the subacute stage because of the favorable dissection plane. However, for patients suffered from severe and progressive neurological deficits such as weakness of gag reflex and respiratory dysfunction, an emergency surgery with routine electrophysiological monitoring should be considered. 4.3. Surgical approaches and techniques
Fig. 2. Intraoperative observation of a fatal CM in medulla obalongata. A 41-yearold male presented with progressive respiratory dysfunction for 1 day. Axial T2 (A) and sagittal contrast-enhanced (B) MRI showed a CM located in upper dorsal medulla. An emergency surgery was performed, and the surrounding hemosiderinstained gliotic tissues revealed potential repeated hemorrhage occurred (C). A gross total resection was considered to be achieved intraoperatively (D), however, the patient required ventilator postoperatively and MRI could not be performed, eventually, he died due to pneumonia.
could recover gradually after surgery. In our series, patients with CMs involving the lower dorsal medulla achieved best neurological outcome, which might be due to the consideration that preoperative neurological status in this group were mild and no one suffered from severe respiratory dysfunction. Although the more preoperative neurological dysfunctions led to the worse clinical outcome in patients with CMs involving ventrolateral medulla, none of them suffered from aggravated neurological functions postoperatively. However, it is difficult to conclude the relationship between locations and neurological outcome because of the small sample size in our study. In general, the clinical outcome of CMs involving medulla oblongata was equal or better than the overall condition in brainstem CMs (Table 3). Consistent with the previous studies, the long term neurological outcome in our series was favorable, however, in stark contrast with CMs in other sites, CMs involving medulla oblongata presented with severe preoperative neurological dysfunctions would be associated with catastrophic outcome.
4.2. Surgical indications and timing Numerous studies illustrated that the surgical indications for brainstem CMs should be repeated hemorrhages with progressive neurological deficits, and meanwhile, the lesion should be close to the pial surface [3,4,9]. However, given the high propensity of obex involvement and motor weakness of gag reflex, the attitude towards the hemorrhagic CMs involving medulla oblongata should be more aggressive [10]. Our institutional surgical indication is CMs involving medulla oblongata which present with symp-
The surgical approach and safe parenchymal entry zone should be tailored individually with integrating the results of preoperative DTT, neuronavigation, anatomical landmarks and intraoperative electrophysiological monitoring. (1) With the application of DTT, the relation of the CM to dislocated fiber tracts could be demonstrated in a 3-dimensional manner, which would be facilitate the preoperative planning of surgical approach[7,14]. (2) Electrophysiological monitoring and nuclei mapping can offer precise information intraoperatively in order to localize and avoid the direct damage of critical structures. Even for the lesions with significant pial presentation (hemosiderin or exophytic), these intraoperative measurements should be applied routinely to minimize the parenchymal incision. (3) It is critical to recognize the anatomy of the medulla oblongata, especially the landmarks and the spatial relation of the CMs to nuclei, tracts, cranial nerves, and vessels [8,9]. For the CMs involving the upper dorsal medulla, the lesions could be resected through the telovelar approach which provides a sufficient operative exposure without splitting the vermis. Even the minimal splitting of the inferior vermis may pose the underlying risk of postoperative truncal ataxia. Based on anatomical researches, the median sulcus above the facial colliculus, suprafacial and infrafacial triangles are safe entry zones on dorsal pontomedulla [8]. For the CMs involving the lower dorsal medulla, standard median suboccipital craniotomy was recommended. Despite the pial presentation would guide us to the lesion, landmarks of safe entry zones should also be identified including the posterior median fissure below the obex, the posterior intermediate sulcus between the gracile and cuneate fascicles and the posterior lateral sulcus medial to cuneate fascicle [8,15]. For the CMs involving ventrolateral medulla, retrosigmoid and far-lateral approach could offer anterolateral trajectory to achieve optimal exposure. The so-called ‘‘peri-trigeminal area” between the root of V and VII cranial nerves should be identified carefully [8,9,15– 17], utmost care should be given to preserve the corticospinal tract with the help of DTT and electrophysiological monitoring. Microsurgical techniques in treating with brainstem CMs have been mentioned in several studies [3,4,6,12,18–20]. It is consensus that gross total resection with minimal damage to the surrounding parenchyma is the main goal of surgery, and incomplete resection is the main risk of postoperative hemorrhage and recurrence. However, for CMs involving medulla oblongata, we consider that if the complete removal are associated with high risk of intraoperative morbidity or even fluctuated vital signs, partial resection is also acceptable and the outcome could be favorable. Moreover, for most cases, dissection plane should be decided early and preserved carefully during resection. However, for lesions involving the obex, piecemeal removal is recommended, especially when fluctuation of the vital signs occurred during en bloc resection. Two patients in our series underwent partial resection, because, during the surg-
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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Fig. 3. DTT guided surgical resection of a CM involving obex. A 36-year-old female presented with facial paralysis and tachycardia for 7 days. Axial T2 (A) and contrastenhanced (B) MRI showed a CM located in pontomedullary with obex involvement. DTT demonstrated the white matter was compressed anteriorly (C), and a telovelar approach was adopted. Postoperative axial T2 (D), axial (E) and sagittal (F) contrast-enhanced MRI showed the CM was resected with only mild hemosiderin left on T2weighted imaging (D). After 1 year of follow-up, the patient had mild facial paralysis with mRS 1.
Table 2 Clinical outcome based on lesion location. Location
Mean mRS score
Recent mRS Score, n (%)
Favorable outcome, n (%)
Preoperative
Postoperative
Recent
Improve
Stable
Worse/dead
Upper dorsal medulla involvement Lower dorsal medulla involvement Ventrolateral medulla involvement
2.83 ± 1.83 2.00 ± 1.00 2.60 ± 0.97
3.50 ± 1.38 2.33 ± 0.58 3.10 ± 0.74
1.83 ± 2.14 1.00 ± 1.00 2.10 ± 0.99
4 (66.7) 2 (66.7) 4 (40.0)
1 (16.7) 0 (0.0) 6 (60.0)
1 (16.7) 1 (33.3) 0 (0.0)
5 (83.3) 3 (100.0) 7 (70.0)
Total
2.58 ± 1.26
3.11 ± 0.99
1.84 ± 1.42
10 (52.6)
7 (36.8)
2 (10.5)
15 (78.9)
Table 3 Surgical series of cavernous malformation involving medulla oblongata. Study
Patients, n
*
Hauck et al. [18] Abla et al. [3] Chen et al. [12] Mai et al. [6] Li et al. [4] Pandey et al. [20]* Garcia et al. [19]* *
44 260 38 22 242 131 104
Total neurological outcome, n (%) Improve
Stable
Worse
13 (30.0) 174 (67.7) 21 (55.3) 12 (54.0) 147 (60.7) 80 (61.0) 57 (54.8)
26 (59.0) 83 (32.3) 15 (39.5) 7 (32.0) 70 (28.9) 34 (26.0) 36 (34.6)
5 (11.0) 2 (5.3) 3 (14.0) 25 (10.3) 7 (13.0) 11 (10.6)
CMs involving medulla oblongata, n (%)
8 (18.0) 69 (26.6) 6 (15.8) 4 (18.2) 40 (16.6) 12 (9.2) 20 (19.2)
Neurological outcome of CMs involving medulla oblongata, n (%) Improve
Stable
Worse
5 (63.0) 47 (68.1) 3 (50.0) 2 (50.0) 29 (72.5) 10 (83.3) 19 (95.0)
2 (25.0) 22 (31.9) 2 (33.3) 1 (25.0) 7 (17.5) 1 (8.3)
1 (13.0) 1 1 4 1 1
(16.7) (25.0) (10.0) (8.3) (5.0)
Patients in these studies were divided into three groups: midbrain, pontine and medulla oblongata. Lesions located in pontomedullary were not described separately.
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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eries, we found that our further manipulations induced significant fluctuation of vital signs including hypotension and bradycardia. These patients received conservative treatment and intensive follow-up. During the long-term follow-up, none of them suffered from recurrence and rehemorrhage. It is considered that the repeated congestive hemorrhage of CM is caused by the compression of draining veins of the CMs, evacuation of the hematoma and partial resection of the lesion would also reduce the risk of rehemorrhage [12]. In addition, we advocate that every attempt should be made to preserve the typical caput medusae as well as the surrounding hemosiderin-stained gliotic tissue. 4.4. Limitations This is an institutional long-term retrospective study concerning a special entity in brainstem CMs, and the small sample size as well as lacking of control group could not lead to conclusive evidence. Since most of the previous studies have focused on the brainstem CMs, details of these studies are difficult to extract and perform the further analysis. In any event, we considered that the CMs involving medulla oblongata should be treated with distinctive attitude comparing to the other sites of brainstem CMs, and further studies on this special entity would be expected.
5. Conclusion Surgical treatment of cavernous malformations involving medulla oblongata is particularly challenging. Safe resection and favorable outcome can be achieved by appropriate indications, optimal approaches, feasible entry zone and meticulous microsurgical techniques. The clinical features, surgical indications, timing and microsurgical techniques of this special entity should be distinctive from the brainstem cavernous malformations in other sites.
Statement None of the portions of the contents have been published or presented previously.
Sources of support This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflict of interests None. References [1] Gross BA, Lin N, Du R, et al. The natural history of intracranial cavernous malformations. Neurosurg Focus 2011;30:E24. [2] Washington CW, McCoy KE, Zipfel GJ. Update on the natural history of cavernous malformations and factors predicting aggressive clinical presentation. Neurosurg Focus 2010;29:E7. [3] Abla AA, Lekovic GP, Turner JD, et al. Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients. Neurosurgery 2011;68:403–14. ; discussion 14-5.. [4] Li D, Yang Y, Hao SY, et al. Hemorrhage risk, surgical management, and functional outcome of brainstem cavernous malformations. J Neurosurg 2013;119:996–1008. [5] Gross BA, Batjer HH, Awad IA, et al. Brainstem cavernous malformations: 1390 surgical cases from the literature. World Neurosurg 2013;80:89–93. [6] Mai JC, Ramanathan D, Kim LJ, et al. Surgical resection of cavernous malformations of the brainstem: evolution of a minimally invasive technique. World Neurosurg 2013;79:691–703. [7] Flores BC, Whittemore AR, Samson DS, et al. The utility of preoperative diffusion tensor imaging in the surgical management of brainstem cavernous malformations. J Neurosurg 2015;1–10. [8] Giliberto G, Lanzino DJ, Diehn FE, et al. Brainstem cavernous malformations: anatomical, clinical, and surgical considerations. Neurosurg Focus 2010;29:E9. [9] Petr O, Lanzino G. Brainstem cavernous malformations. J Neurosurg Sci 2015;59:271–82. [10] Wang CC, Liu A, Zhang JT, et al. Surgical management of brain-stem cavernous malformations: report of 137 cases. Surg Neurol 2003;59:444–54 [discussion 54]. [11] Chotai S, Qi S, Xu S. Prediction of outcomes for brainstem cavernous malformation. Clin Neurol Neurosurg 2013;115:2117–23. [12] Chen L, Zhao Y, Zhou L, et al. Surgical strategies in treating brainstem cavernous malformations. Neurosurgery 2011;68:609–20 [discussion 20-1]. [13] Bruneau M, Bijlenga P, Reverdin A, et al. Early surgery for brainstem cavernomas. Acta Neurochir 2006;148:405–14. [14] Chen X, Weigel D, Ganslandt O, et al. Diffusion tensor-based fiber tracking and intraoperative neuronavigation for the resection of a brainstem cavernous angioma. Surg Neurol 2007;68:285–91 [discussion 91]. [15] Cantore G, Missori P, Santoro A. Cavernous angiomas of the brain stem. Intraaxial anatomical pitfalls and surgical strategies. Surg Neurol 1999;52:84–93 [discussion -4]. [16] Asaad WF, Walcott BP, Nahed BV, et al. Operative management of brainstem cavernous malformations. Neurosurg Focus 2010;29:E10. [17] Recalde RJ, Figueiredo EG, de Oliveira E. Microsurgical anatomy of the safe entry zones on the anterolateral brainstem related to surgical approaches to cavernous malformations. Neurosurgery 2008;62:9–15 [discussion -7]. [18] Hauck EF, Barnett SL, White JA, et al. Symptomatic brainstem cavernomas. Neurosurgery 2009;64:61–70 [discussion -1]. [19] Garcia RM, Ivan ME, Lawton MT. Brainstem cavernous malformations: surgical results in 104 patients and a proposed grading system to predict neurological outcomes. Neurosurgery 2015. [20] Pandey P, Westbroek EM, Gooderham PA, Steinberg GK. Cavernous malformation of brainstem, thalamus, and basal ganglia: a series of 176 patients. Neurosurgery 2013;72:573–89 [discussion 88-9].
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Case study
Surgical treatment of cavernous malformations involving medulla oblongata Si Zhang 1, Sen Lin 1, Xuhui Hui, Hao Li, Chao You ⇑ Department of Neurosurgery, West China Hospital of Sichuan University, Chengdu, Sichuan, China
a r t i c l e
i n f o
Article history: Received 11 June 2016 Accepted 28 November 2016 Available online xxxx Keywords: Medulla oblongata Brainstem Cavernous malformation Microsurgery
a b s t r a c t Surgical treatment of cavernous malformations (CMs) involving medulla oblongata is more difficult than the CMs in other sites because of the surrounding vital structures. However, the distinctive features and treatment strategies have not been well illustrated. Therefore, we enrolled a total of 19 patients underwent surgical treatment of CMs involving medulla oblongata in our hospital from August 2008 to August 2014. The clinical features, surgical management and clinical outcome of these patients were retrospectively analyzed, while our institutional surgical indications, approaches and microsurgical techniques were discussed. In our study, gross total resection was achieved in 17 patients and subtotal resection in 2. Two patients underwent emergency surgeries due to severe and progressive neurological deficits. The postoperative new-onset or worsened neurological deficits occurred in 6 patients. After a mean follow-up of 45.8 ± 22.2 months, the neurological status was improved in 10 patients and remained stable in 7. The mean modified Rankin Scale (mRS) was 2.58 ± 1.26 preoperatively, 3.11 ± 0.99 postoperatively and 1.84 ± 1.42 at the recent follow-up, respectively. During the follow-up period, no rehemorrhage and recurrence occurred, and the residual lesions remained stable. We recommended surgical resection of symptomatic CMs involving medulla oblongata via optimal approaches, feasible entry zones and meticulous microsurgical techniques in attempting to achieve safe resection and favorable outcome. The clinical features, surgical indications, timing and microsurgical techniques of this special entity should be distinctive from the brainstem cavernous malformations in other sites. Ó 2016 Published by Elsevier Ltd.
1. Introduction Since brainstem cavernous malformations (CMs) are associated with higher hemorrhagic rates and poorer neurological outcome [1,2], microsurgical resection has been considered to be the optimal treatment [3,4]. In the last two decades, remarkable progress has been achieved in surgical treatment of brainstem CM and it is consensus that the primary goal of the surgery is to prevent further hemorrhage rather than neurological recovery [3–5]. Therefore, the surgical strategy of brainstem CMs has become how to balance the hemorrhagic morbidities and surgery-related morbidities. CMs involving medulla oblongata, as a more special entity of brainstem CMs, are of unique features comparing to the other sites. The CMs located in medulla oblongata and pontomedullary could be associated with potential life-threatening symptoms and the
⇑ Corresponding author at: Department of Neurosurgery, West China Hospital of Sichuan University, 37 Guo Xue Xiang, Wu Hou District, Chengdu 610041, China. Fax: +86 28 85164009. E-mail address: [email protected] (C. You). 1 Zhang and Lin contributed equally in this study as the co-first authors.
proximity to critical structures may pose a particular challenge to microsurgical resection. Therefore, we advocated that the surgery-related decision-making criteria, timing, surgical techniques and clinical outcome should be reconsidered. Based on our experience in surgical treatment of 19 patients harboring CMs involving medulla oblongata, we aim to evaluate the clinical features and neurofunctional outcome of these patients and summarize our institutional experience on surgical indications, timing and microsurgical techniques of this disease. 2. Methods 2.1. Clinical chart From August 2008 to August 2014, nineteen consecutive patients with CMs involving medulla oblongata underwent surgical treatment in our hospital. The clinical data including age, gender, symptoms and neurological signs at admission were retrospectively analyzed. The present study was approved by the West China Hospital Trials and Biomedical Ethics Committee. The mRS was used to evaluate the neurological status. Preoperatively,
http://dx.doi.org/10.1016/j.jocn.2016.11.014 0967-5868/Ó 2016 Published by Elsevier Ltd.
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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S. Zhang et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
cranial Computer Tomography (CT), Magnetic Resonance Imaging (MRI) with contrast enhancement and Diffusion Tensor Tractography (DTT) were performed as routine.
Table 1 Symptoms and signs on admission. Symptoms and signs
2.2. Surgery Our institutional surgical indication was CMs involving medulla oblongata which presented with symptomatic acute and subacute hemorrhage and were surgically accessible. We preferred performing the surgery during the subacute stage due to the favorable dissection plane. However, for patients with severe and progressive neurological deficits such as weakness of gag reflex and respiratory dysfunction, emergency surgery should be performed. Somatosensory evoked potentials, motor evoked potentials and brainstem auditory evoked potentials were monitored routinely. Recording needles were inserted into the orbicularis oris, orbicularis oculi muscles, the posterior pharyngeal wall and the tongue bilaterally. A stimulation probe was applied for cranial nerve nuclei and corticospinal tract mapping. The selection of the surgical approach was tailored individually. The safe entry zone was determined by the integration of anatomical landmarks, pial presentation, preoperative DTT, intraoperative neuronavigation and nuclei mapping. Standard microsurgical exposure and resection was performed including low-power bipolar coagulation and sharp dissection. Generally, an en bloc resection and elaborate exploration of the wall of hematoma cavity was attempted to improve the possibility of complete resection. However, if the hemodynamic instability occurred during separation of the lesion, piecemeal resection should be adopted. The developmental venous anomalies (DVAs) and the hemosiderin-stained gliotic tissues were preserved. 2.3. Follow-up and clinical outcome Postoperative complications and the new-onset or worsened neurological deficits were recorded, mRS was used to evaluate the neurological status postoperatively (3 days after the surgery). The follow-up was performed at 6 months after surgery and once a year thereafter. During the follow-up period, changes in neurological deficits (improved, stable or aggravated) and mRS were assessed in outpatient center. mRS scores of 1–2 was considered as favorable outcome. Experts of neuroimaging processed the cross analysis of the MRI to identify the recurrence and rehemorrhage. 3. Results There were 7 males and 12 females with a mean age of 39.74 ± 10.68 years (range from 15 to 58 years). All the patients presented with symptoms of one or more hemorrhagic episodes (10 patients presented with single episode of hemorrhage, 6 patients with two episodes and 2 patients with three or more episodes. one patient underwent the surgery for CM located in medulla oblongata 10 years ago, and suffered from rehemorrhage this time). The calculative annual hemorrhage rate was 4.24% (assuming that all CMs generated since birth) and the annual rehemorrhage rate was 54.17%. The most common symptom was sudden onset of cranial nerve dysfunction (n = 14) including dysphagia (n = 6), dysarthria (n = 4), facial (n = 3) and abducent paralysis (n = 3), cardiac instability (n = 2) and neck pain (n = 2). Other symptoms and neurological signs included hemiparesthesia (n = 11), hemiparesis (n = 9), ataxia (n = 5), headache (n = 2) and respiratory dysfunction (n = 3) (Table 1). The mean mRS score was 2.58 ± 1.26 preoperatively. According to the locations of these lesions, all the cases were divided into 3 groups: upper dorsal
Cranial nerve deficits Oculomotor paralysis Abducent paralysis Facial paralysis Dysphagia Dysarthria Cardiac instability Neck pain Hemiparesthesia and body numbness Hemiparesis Ataxia Headache Respiratory dysfunction
Lesion location, n Upper dorsal medulla involvement
Lower dorsal medulla involvement
Ventrolateral medulla involvement
4 0 1 2 1 1 2 0 2
4 0 0 0 2 1 0 1 1
10 1 2 1 3 2 0 1 8
1 1 2 2
0 0 0 0
8 4 0 1
medulla involvement (n = 6), lower dorsal medulla involvement (n = 3) and ventrolateral medulla involvement (n = 10). 3.1. Surgery Seventeen patients underwent surgical treatment in subacute phase after hemorrhage (Fig. 1), and two patients were taken for the emergency surgery (one for acute severe dysphagia combined with coma for 30 min, and one for progressive respiratory dysfunction) (Fig. 2). The following approaches were adopted: suboccipital approach (n = 9, including telovelar approach in 6 cases) (Fig. 3), retrosigmoid approach (n = 5) and far lateral approach (n = 5). Gross total resections were achieved in 17 cases, while subtotal resections were performed in 2 cases. These two lesions were observed involving the obex, and when we attempted to shrink the lesion away from eloquent hemosiderin-stained gliotic tissue, drastic cardiac instability occurred. Intraoperatively, the DVAs were observed in 4 cases (21.05%), and all the typical caput medusae structures were preserved carefully. The surrounding hemosiderin-stained gliotic tissues were preserved in all cases. 3.2. Complications and follow up Postoperative new-onset or worsened neurological deficits occurred in 6 patients including dysphagia (n = 1), dysarthria (n = 1), paresthesia (n = 2), ataxia (n = 2) and walking difficulty (n = 1). No surgical related hemiparesis occurred. The mean mRS 3 days after the surgery was 3.11 ± 0.99. One patient suffered from postoperative hydrocephalus, who was performed the VentriclePeritoneal shunt. Gastrostomy tube was placed in 6 patients who suffered from dysphagia preoperatively and two patients who presented with new onset of lower cranial nerves deficits. Tracheostomy was performed for the patients who suffered from respiratory dysfunction (n = 1) or severe aspiration pneumonia (n = 2). One patient required the ventilator due to preoperative respiratory failure despite an emergency surgery was performed, the patient died due to postoperative pneumonia eventually. Other complications included intracranial infection (n = 1) and aspiration pneumonia (n = 2). All the patients underwent routine follow-up. After a mean follow-up of 45.8 ± 22.2 months (range from 18 to 78 months), the preoperative neurological status was improved in 10 patients and remained stable in 7. The postoperative new-onset or worsened symptoms were improved in 5 patients and remained stable in 1. At the recent follow-up, the mean mRS was 1.84 ± 1.42 and 15
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Fig. 1. Pre- and postoperative MRI of CM involving medulla oblongata. A 41-year-old female presented with four episodes of symptomatic hemorrhage in 3 years. Axial T1 (A), T2 (B) and contrast-enhanced (C) MRI revealed a CM involving upper dorsal medulla oblongata. The surgery was performed via telovelar approach. Postoperatively, she recovered with only mild ataxia. Postoperative axial T1 (E), T2 (F) and contrast-enhanced (G) MRI showed complete excision of the CM.
patients achieved favorable outcome (Table 2). All the patients with CMs involving the lower dorsal medulla (n = 3) in our series achieved favorable outcome with a mean mRS score of 1.00 ± 1.00. Seven patients (70%) with CMs involving ventrolateral medulla achieved favorable outcome with a mean mRS score of 2.10 ± 0.99. During the follow-up period, no rehemorrhage and recurrence occurred, and the residual lesions remained stable.
4. Discussion Rather than commonly located in the pontine, only approximately 10–20% of brainstem CMs were reported involving the medulla oblongata (Table 3) [3–7]. Due to the proximity to the critical neural structures, clinical presentations of hemorrhagic CMs involving medulla oblongata are more severe and lifethreatening. Moreover, the slightest damage to a vital structure caused by surgical intervention can result in fatal neurological deficits such as aspiration and respiratory dysfunction. Therefore, we considered that the hemorrhagic CMs involving medulla oblongata would be associated with distinctive features that the surgical indications, optimal timing, surgical techniques and clinical outcome should be emphasized separately.
4.1. Clinical features and outcome Generally, the symptoms of CMs involving medulla oblongata are correlated with the involvement of critical neural structures in different locations [8]. In our series, lower cranial nerve dysfunctions remained to be the most common pre- and postoperative symptoms. Tongue weakness and dysphagia caused by compression of the hypoglossal and ambiguus nuclei or surgical intervention were common neurological dysfunctions which might lead to life-threatening aspiration. Therefore, for patients with lower cranial nerve dysfunctions, routine placement of gastrostomy tube was recommended. According to the results of DTT, patients presented with hemiparesis in our series were more due to the compression from the lesions than destruction of the corticospinal tract. Hence, it would be reasonable to release the mass effect via surgical resection in aiming at achieving a favorable recovery. Moreover, three patients in our series presented with obex symptoms including one patient had sudden onset of severe respiratory failure. Obex involvement was considered as the most serious situation in this entity, thus the tracheostomy should be performed preoperatively and an emergency craniotomy be taken. The other symptoms such as hemiparesthesia and body numbness mostly occurred in patients with lesions located ventrolaterally, which
Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014
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tomatic acute and subacute hemorrhage and are surgically accessible. The appropriate timing of surgery is still controversial [11]. Some authors have recommended operating during the subacute stage due to the better neurological status [12]. Whereas Bruneau et al. indicated that early surgery could promptly release the mass effect on brainstem nuclei and tracts, and thus improve the neurological outcome [13]. For CMs involving medulla oblongata in our series, we preferred performing the surgery during the subacute stage because of the favorable dissection plane. However, for patients suffered from severe and progressive neurological deficits such as weakness of gag reflex and respiratory dysfunction, an emergency surgery with routine electrophysiological monitoring should be considered. 4.3. Surgical approaches and techniques
Fig. 2. Intraoperative observation of a fatal CM in medulla obalongata. A 41-yearold male presented with progressive respiratory dysfunction for 1 day. Axial T2 (A) and sagittal contrast-enhanced (B) MRI showed a CM located in upper dorsal medulla. An emergency surgery was performed, and the surrounding hemosiderinstained gliotic tissues revealed potential repeated hemorrhage occurred (C). A gross total resection was considered to be achieved intraoperatively (D), however, the patient required ventilator postoperatively and MRI could not be performed, eventually, he died due to pneumonia.
could recover gradually after surgery. In our series, patients with CMs involving the lower dorsal medulla achieved best neurological outcome, which might be due to the consideration that preoperative neurological status in this group were mild and no one suffered from severe respiratory dysfunction. Although the more preoperative neurological dysfunctions led to the worse clinical outcome in patients with CMs involving ventrolateral medulla, none of them suffered from aggravated neurological functions postoperatively. However, it is difficult to conclude the relationship between locations and neurological outcome because of the small sample size in our study. In general, the clinical outcome of CMs involving medulla oblongata was equal or better than the overall condition in brainstem CMs (Table 3). Consistent with the previous studies, the long term neurological outcome in our series was favorable, however, in stark contrast with CMs in other sites, CMs involving medulla oblongata presented with severe preoperative neurological dysfunctions would be associated with catastrophic outcome.
4.2. Surgical indications and timing Numerous studies illustrated that the surgical indications for brainstem CMs should be repeated hemorrhages with progressive neurological deficits, and meanwhile, the lesion should be close to the pial surface [3,4,9]. However, given the high propensity of obex involvement and motor weakness of gag reflex, the attitude towards the hemorrhagic CMs involving medulla oblongata should be more aggressive [10]. Our institutional surgical indication is CMs involving medulla oblongata which present with symp-
The surgical approach and safe parenchymal entry zone should be tailored individually with integrating the results of preoperative DTT, neuronavigation, anatomical landmarks and intraoperative electrophysiological monitoring. (1) With the application of DTT, the relation of the CM to dislocated fiber tracts could be demonstrated in a 3-dimensional manner, which would be facilitate the preoperative planning of surgical approach[7,14]. (2) Electrophysiological monitoring and nuclei mapping can offer precise information intraoperatively in order to localize and avoid the direct damage of critical structures. Even for the lesions with significant pial presentation (hemosiderin or exophytic), these intraoperative measurements should be applied routinely to minimize the parenchymal incision. (3) It is critical to recognize the anatomy of the medulla oblongata, especially the landmarks and the spatial relation of the CMs to nuclei, tracts, cranial nerves, and vessels [8,9]. For the CMs involving the upper dorsal medulla, the lesions could be resected through the telovelar approach which provides a sufficient operative exposure without splitting the vermis. Even the minimal splitting of the inferior vermis may pose the underlying risk of postoperative truncal ataxia. Based on anatomical researches, the median sulcus above the facial colliculus, suprafacial and infrafacial triangles are safe entry zones on dorsal pontomedulla [8]. For the CMs involving the lower dorsal medulla, standard median suboccipital craniotomy was recommended. Despite the pial presentation would guide us to the lesion, landmarks of safe entry zones should also be identified including the posterior median fissure below the obex, the posterior intermediate sulcus between the gracile and cuneate fascicles and the posterior lateral sulcus medial to cuneate fascicle [8,15]. For the CMs involving ventrolateral medulla, retrosigmoid and far-lateral approach could offer anterolateral trajectory to achieve optimal exposure. The so-called ‘‘peri-trigeminal area” between the root of V and VII cranial nerves should be identified carefully [8,9,15– 17], utmost care should be given to preserve the corticospinal tract with the help of DTT and electrophysiological monitoring. Microsurgical techniques in treating with brainstem CMs have been mentioned in several studies [3,4,6,12,18–20]. It is consensus that gross total resection with minimal damage to the surrounding parenchyma is the main goal of surgery, and incomplete resection is the main risk of postoperative hemorrhage and recurrence. However, for CMs involving medulla oblongata, we consider that if the complete removal are associated with high risk of intraoperative morbidity or even fluctuated vital signs, partial resection is also acceptable and the outcome could be favorable. Moreover, for most cases, dissection plane should be decided early and preserved carefully during resection. However, for lesions involving the obex, piecemeal removal is recommended, especially when fluctuation of the vital signs occurred during en bloc resection. Two patients in our series underwent partial resection, because, during the surg-
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Fig. 3. DTT guided surgical resection of a CM involving obex. A 36-year-old female presented with facial paralysis and tachycardia for 7 days. Axial T2 (A) and contrastenhanced (B) MRI showed a CM located in pontomedullary with obex involvement. DTT demonstrated the white matter was compressed anteriorly (C), and a telovelar approach was adopted. Postoperative axial T2 (D), axial (E) and sagittal (F) contrast-enhanced MRI showed the CM was resected with only mild hemosiderin left on T2weighted imaging (D). After 1 year of follow-up, the patient had mild facial paralysis with mRS 1.
Table 2 Clinical outcome based on lesion location. Location
Mean mRS score
Recent mRS Score, n (%)
Favorable outcome, n (%)
Preoperative
Postoperative
Recent
Improve
Stable
Worse/dead
Upper dorsal medulla involvement Lower dorsal medulla involvement Ventrolateral medulla involvement
2.83 ± 1.83 2.00 ± 1.00 2.60 ± 0.97
3.50 ± 1.38 2.33 ± 0.58 3.10 ± 0.74
1.83 ± 2.14 1.00 ± 1.00 2.10 ± 0.99
4 (66.7) 2 (66.7) 4 (40.0)
1 (16.7) 0 (0.0) 6 (60.0)
1 (16.7) 1 (33.3) 0 (0.0)
5 (83.3) 3 (100.0) 7 (70.0)
Total
2.58 ± 1.26
3.11 ± 0.99
1.84 ± 1.42
10 (52.6)
7 (36.8)
2 (10.5)
15 (78.9)
Table 3 Surgical series of cavernous malformation involving medulla oblongata. Study
Patients, n
*
Hauck et al. [18] Abla et al. [3] Chen et al. [12] Mai et al. [6] Li et al. [4] Pandey et al. [20]* Garcia et al. [19]* *
44 260 38 22 242 131 104
Total neurological outcome, n (%) Improve
Stable
Worse
13 (30.0) 174 (67.7) 21 (55.3) 12 (54.0) 147 (60.7) 80 (61.0) 57 (54.8)
26 (59.0) 83 (32.3) 15 (39.5) 7 (32.0) 70 (28.9) 34 (26.0) 36 (34.6)
5 (11.0) 2 (5.3) 3 (14.0) 25 (10.3) 7 (13.0) 11 (10.6)
CMs involving medulla oblongata, n (%)
8 (18.0) 69 (26.6) 6 (15.8) 4 (18.2) 40 (16.6) 12 (9.2) 20 (19.2)
Neurological outcome of CMs involving medulla oblongata, n (%) Improve
Stable
Worse
5 (63.0) 47 (68.1) 3 (50.0) 2 (50.0) 29 (72.5) 10 (83.3) 19 (95.0)
2 (25.0) 22 (31.9) 2 (33.3) 1 (25.0) 7 (17.5) 1 (8.3)
1 (13.0) 1 1 4 1 1
(16.7) (25.0) (10.0) (8.3) (5.0)
Patients in these studies were divided into three groups: midbrain, pontine and medulla oblongata. Lesions located in pontomedullary were not described separately.
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eries, we found that our further manipulations induced significant fluctuation of vital signs including hypotension and bradycardia. These patients received conservative treatment and intensive follow-up. During the long-term follow-up, none of them suffered from recurrence and rehemorrhage. It is considered that the repeated congestive hemorrhage of CM is caused by the compression of draining veins of the CMs, evacuation of the hematoma and partial resection of the lesion would also reduce the risk of rehemorrhage [12]. In addition, we advocate that every attempt should be made to preserve the typical caput medusae as well as the surrounding hemosiderin-stained gliotic tissue. 4.4. Limitations This is an institutional long-term retrospective study concerning a special entity in brainstem CMs, and the small sample size as well as lacking of control group could not lead to conclusive evidence. Since most of the previous studies have focused on the brainstem CMs, details of these studies are difficult to extract and perform the further analysis. In any event, we considered that the CMs involving medulla oblongata should be treated with distinctive attitude comparing to the other sites of brainstem CMs, and further studies on this special entity would be expected.
5. Conclusion Surgical treatment of cavernous malformations involving medulla oblongata is particularly challenging. Safe resection and favorable outcome can be achieved by appropriate indications, optimal approaches, feasible entry zone and meticulous microsurgical techniques. The clinical features, surgical indications, timing and microsurgical techniques of this special entity should be distinctive from the brainstem cavernous malformations in other sites.
Statement None of the portions of the contents have been published or presented previously.
Sources of support This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Please cite this article in press as: Zhang S et al. Surgical treatment of cavernous malformations involving medulla oblongata. J Clin Neurosci (2016), http:// dx.doi.org/10.1016/j.jocn.2016.11.014