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Brainstem Cavernous Malformations: 1390 Surgical Cases from the Literature
Brainstem Cavernous Malformations: 1390 Surgical Cases from the Literature Bradley A. Gross1, H. Hunt Batjer2, Issam A. Awad3, Bernard R. Bendok2, Rose Du1
Key words Angioma - Brainstem - Cavernoma - Cavernous - Surgery -
Abbreviations and Acronyms CM: Cavernous malformation SRS: Stereotactic radiosurgery From the 1Department of Neurological Surgery, Brigham and Womens Hospital and Harvard Medical School, Boston, Massachusetts; 2Department of Neurological Surgery, The Feinberg School of Medicine and McGaw Medical Center, Northwestern University, Chicago, Illinois; and 3Section of Neurosurgery, The Pritzker School of Medicine, The University of Chicago, Chicago, Illinois, USA To whom correspondence should be addressed: Rose Du, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2013) 80, 1/2:89-93. http://dx.doi.org/10.1016/j.wneu.2012.04.002 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
INTRODUCTION Among the variety of lesions faced by vascular neurosurgeons, brainstem cavernous malformations (CMs) present a considerable microsurgical challenge and were once the subject of rare case reports (13, 45, 51). After large series were reported by the Barrow Neurological Institute in 1999 (40) and the Beijing Neurosurgical Institute in 2003 (53), an explosion of studies surfaced in the literature detailing the results of surgical resection (9, 16, 18, 50). Amidst this, we previously amassed results from 52 surgical series with 821 patients and found a 92% complete excision rate with 85% of patients being improved or the same at long-term follow-up (18). Impressively, since this initial report, a litany of series with nearly as many patients have been reported (1, 2, 6, 10-12, 15, 17, 20, 22, 23, 30, 32, 36, 42, 44, 49, 50), prompting us to amass their results, compare them, and combine them with those of our previous report.
- OBJECTIVE:
Although surgical resection of brainstem cavernous malformations (CM) has been reviewed, numerous large surgical series have been recently reported.
- METHODS:
Eighteen new surgical series with 710 patients were found via a PubMed search, in addition to our previous meta-analysis. Complete excision, complications, and long-term outcome results were compiled across these series. They were then compared and subsequently combined with those of our previous report.
- RESULTS:
We combined results of 68 surgical series with 1390 patients, incorporating results from our previous meta-analysis. Across 61 series, 1178 of 1291 (91%) CMs were completely excised. Of 105 partially resected CMs with ample follow-up, 65 rebled (62%). Across 46 series providing information on early neurologic morbidity, the overall rate was 45%. Specifically, 12% of patients required tracheostomy and/or gastrostomy procedures. Overall longterm condition was improved in 62% of patients across 51 series. Across 60 series, overall long-term condition was improved or the same in 84% of patients, with worsening in the remaining 16%. The overall surgical and/or cavernoma related mortality rate for all 1390 patients was 1.5%. Notably, these results did not differ significantly between our initial review and the combined data from the subsequent 18 surgical series recently reported in the literature.
- CONCLUSION:
Surgical resection of brainstem CM continues to present a considerable challenge with resultant morbidity akin to another CM hemorrhage. We therefore prefer to offer surgery only to patients with at least one previous hemorrhage with CM pial representation. Appropriate patient counseling about expected early morbidity and the potential for long-term worsening is crucial.
METHODS The PubMed database was queried with the search terms “cavernoma,” “cavernous malformation,” “cavernous angioma,” “brainstem,” and “surgery” from May 2008 to January 2012. As per our previous selection criteria, any series containing at least three patients with brainstem CMs undergoing surgery was included. This resulted in 18 reports (1, 2, 6, 10-12, 15, 17, 20, 22, 23, 30, 32, 36, 42, 44, 49, 50), two of which were inclusive, larger updates of previous series in the literature (2, 5, 15, 40). We first compiled these results and compared them with those of our previous review (18). We then combined results from both analyses to synthesize overall complete excision rates, early morbidity, tracheostomy and/or
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gastrostomy rates, and long-term follow-up condition. Patients that were reported in multiple reports, namely those in larger updates of prior reports (2, 5, 15, 40), were counted once.
RESULTS During the last 3.5 years, 18 surgical series containing at least three patients with brainstem CMs were reported, including the largest study of 260 patients reported by Abla et al. (2). These 18 series included a total of 710 patients (median: 26.5 patients), a similar total to the 821 patients presented across 52 surgical series over the prior 21 years. Results are summarized in Table 1.
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Table 1. Surgical Series of Brainstem Cavernous Malformations, 2008 to 2011 Study
Patients
Obliteration Rate
Postop Rebleeds*
Abla et al., 2010 (1)
40
34/40 (85%)
5/6 (83%)
Abla et al., 2011 (2)
260
231/260 (89%)
18/29 (62%)
Bhardwaj et al., 2009 (6)
7
5/7 (71%)
Cenzato et al., 2008 (10)
30
27/30 (90%)
Chen et al., 2011 (11)
55
Consales et al., 2010 (12)
Early Morbidity 19/40 (48%)
Trach/PEG 4/40 (10%)
Improved 16/36 (44%)
137/260 (53%) 27/260 (10%) 174/257 (68%)
Same
Worse
Death
9/36 (25%) 10/36 (28%)
1/40 (2.5%)
83 same or worse
3/260 (1.2%)
5/7 (71%)
1/7 (14%)
3/7 (43%)
8/30 (27%)
21/30 (70%)
8/30 (27%)
1/30 (3%)
0
55/55 (100%)
14/55 (25%)
38/52 (73%)
6/52 (12%)
8/52 (15%)
0
4/4 (100%)
1/4 (25%)
2/4 (50%)
2/4 (50%)
4
Dukatz et al., 2011 (15)
71
69/71 (97%)
Francois et al., 2010 (17)
9
7/9 (78%)
1/3 (33%)
44/71 (62%) 19/71 (27%) 2/2 (100%)
Hauck et al., 2009 (20)
44
42/44 (95%)
2/2 (100%)
Huang et al., 2010 (22)
22
20/22 (91%)
1/2 (50%) 1/1 (100%)
Ichinose et al., 2010 (23)
10
9/10 (90%)
Li et al., 2010 (30)
37
37/37 (100%)
Menon et al., 2011 (32)
23
0
4/9 (44%)
7/9 (78%) 5/44 (11%)
6/22 (27%)
8/37 (22%)
5/37 (14%)
12/23 (52%)
5/23 (22%)
0
3/7 (43%)
0
0
0
8/71 (11%)
0
2/9 (22%)
0
13/44 (30%)
26 (59%)
5 (11%)
0
10/22 (45%)
9/22 (41%)
3/22 (14%)
0
7/10 (70%)
3/10 (30%)
20/37 (54%) 15/37 (41%) 9/23 (39%)
Ohue et al., 2010 (36)
36
33/36 (92%)
1/3 (33%)
18/36 (50%)
16/36 (44%)
Ramina et al., 2011 (42)
43
42/43 (98%)
0/1 (0%)
6/43 (14%)
14/43 (33%)
Sanai et al., 2010 (44)
4
4/4 (100%)
Steno et al., 2011 (49)
9
7/9 (78%)
1/2 (50%)
3/9 (33%)
1/4 (25%)
7/9 (78%)
Tarnaris et al., 2008 (50)
6
4/6 (67%)
3/3 (100%)
2/6 (33%)
1/5 (20%)
0 17 (47%)
0
0
2/37 (5%)
0
12/23 (52%)
2/23 (9%)
3 (8%)
0 0
4 improved/same 0 1/5 (20%)
0 0 3/5 (60%)
0 2/9 (22%) 0
CM, cavernous malformation; Trach, tracheostomy; PEG, percutaneous endoscopic gastrostomy. *For incompletely resected CM.
Comparing these new series to those amassed in our previous report (Table 2), we found the same 92% complete excision rate. Complication rates were also remarkably similar—a 42% early neurologic morbidity rate with 58% of patients improved, 84% improved or the same, and 16% worse or dead at long-term follow-up. Overall, excluding overlapping studies, we had data for 1390 patients across 68 surgical series. Across 61 series with 1291 patients, there was an overall 91% complete excision rate. Importantly, of 105 partially resected CMs with ample followup, 65 rebled (62%). The mortality rate from hemorrhage of a residual CM was 6% (4/65 cases). Across 46 series with 944 patients, there was a 45% early neurologic morbidity rate. Twelve percent of patients across 10 series required an early tracheostomy and/or gastrostomy. One-half of these reports provided follow-up of these patients, and only 4 of 26 (15%) tracheostomies and/or gastrostomies were permanent. Long term condition was improved in 62% of patients across 51
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series. Across 60 reports, long-term condition was improved or the same in 84% of patients while 14% of patients were worse. Surgical and/or cavernomarelated mortality was 1.5% across all studies. DISCUSSION Previously confused with demyelinating disease (3, 7, 52), brainstem gliomas (47, 55), and even strokes (25, 27), brainstem CMs are now recognized as a curable cause of morbid brainstem injury. Concomitant with advances in magnetic resonance imaging techniques, small surgical series detailing the resection of brainstem CMs began to surface in the late 1980s (29, 55) with a subsequent explosion of studies undertaken during the past decade (2, 9, 15, 16, 18, 50, 53). Although the results provided by this comprehensive review may serve as a guide, contemplation of resecting these challenging lesions requires an understanding of their natural history weighed against, most importantly, the
surgeon’s own surgical outcomes and experience. Natural History In a recent review of natural history studies of CMs incorporating a total of 837 patients, 18% had brainstem CM (19). Combining data from 3 prospective studies (26, 33, 39), the overall hemorrhage rate of all CM was 2.4% per patientyear (19). Female sex (33) and hemorrhage (26, 39) were risk factors for subsequent bleeding (19). Although brainstem location was generally not a risk factor for hemorrhage per se, it clearly correlated with a more malignant clinical course, with the study of Porter et al. (39) citing an annual clinical event rate as high as 10.6% for these lesions. It is clear however that a subset of brainstem CM may have a relatively benign natural history (28), whereas others may rebleed several times in one year (4, 20). This is underscored by surgical series reporting annual rebleed rates ranging from 18% to 60% (9, 16, 20, 40, 53). Furthermore, in the recent study
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Table 2. Summary of Results from Our Initial, Current, and Combined Review of 68 Surgical Series with at Least 3 Brainstem Cavernous Malformations in the Literature Initial Report
Current Report
Total
Total patients Number of series
821 52
710 18
1390 68
Resection rate Number of series
684/745 (92%) 46
631/687 (92%) 17
1178/1291 (91%) 61
Postop rebleeds Number of series
30/51 11
35/54 11
65/105 22
Early morbidity Number of series
236/500 (47%) 33
244/585 (42%) 15
425/944 (45%) 46
Trach/PEG Number of series
18/161 (11%) 5
46/390 (12%) 6
52/434 (12%) 10
Overall condition Improved Number of series
224/316 (71%) 35
400/695 (58%) 17
Improved/same Number of series
577/683 (85%) 45
334/399 (84%) 16
889/1058 (84%) 60
Worse Number of series
93/683 (14%) 45
60/399 (15%) 16
151/1058 (14%) 60
Died Number of series
16/821 (1.8%) 52
8/710 (1.1%) 17
21/1390 (1.5%) 68
609/987 (62%) 51
PEG, percutaneous endoscopic gastrostomy.
of Hauck et al. (20), after a second neurological event, the subsequent monthly event rate was 8%. This reinforces the validity of intervention after at least one CM hemorrhage.
Surgical Approach Given that brainstem CM may follow a relatively benevolent natural course, we do not operate on incidental or asymptomatic lesions. In fact, we often await a second hemorrhage before offering surgery, defining the lesion as one within the aggressive subset of brainstem CM, requiring treatment to avoid impending further deterioration. In preparation for surgery, like other groups (2), we counsel patients that the early postoperative outcome may mimic an additional hemorrhagic event, underscored by the 45% perioperative neurologic morbidity rate and 12% rate of early tracheostomy and/or gastrostomy from our review. In the largest series reported to date, the rates of postoperative cerebrospinal fluid leak and postoperative wound infection or meningitis were 5% each (2). Across the
experienced hands of surgeons included in our review, a worse condition at follow-up was observed in 14% of cases, with a 1.5% chance of death. It is also noteworthy that the rate of complete excision and outcome results did not significantly differ in recent surgical series compared with those in our original review. From a number of potential options (Table 3), surgical approach can often be
dictated by the two-point method advocated by Brown et al. (8). Since our previous report, several small series detailing approaches to the dorsal midbrain and ventral pons have surfaced. Five variants to the supracerebellar infratentorial approach to the dorsal midbrain have been demonstrated across two recent studies (14, 44). De Oliveira et al. (14) describe three medialto-lateral variants used in 45 patients with brainstem CM, presenting the traditional median and paramedian supracerebellar infratentorial trajectories as well as the extreme lateral supracerebellar infratentorial approach. The latter, used in 23 of 45 cases in this series, is performed with the patient in the park-bench position. A retrosigmoid craniotomy is performed with skeletonization of the transverse sinus and extension of the craniotomy above it, with the surgeon removing bone that would otherwise obstruct an extreme lateral approach above the cerebellum. Sanai et al. (44) describe two superior to inferior variants of the supracerebellar infratentorial approach, naturally created by widening the supracerebellar infratentorial plane via the sitting position. One trajectory along the superior cerebellum (supracerebellar supratrochlear) affords access as high as the thalamus, whereas the other along the tentorium (infratentorial infratrochlear) affords access as low as the fourth cranial nerve. These approaches were used in four cases of brainstem CM, resulting in complete resection in all cases without any patients suffering long-term worsening. Approaches to ventral pontine lesions have varied from the standard retrosigmoid craniotomy to the extensive transcochlear
Table 3. Surgical Approaches to Brainstem Cavernous Malformation Location
Approach
Posterior midbrain
Supracerebellar infratentorial Occipital transtentorial
Anterior midbrain/upper pons
Pterional/orbitozygomatic transsylvian Subtemporal
Anterior pons
Retrosigmoid Anterior transpetrosal (Kawase) Presigmoid/retrolabyrinthine
Anterior medulla
Far lateral Transoral
Floor of fourth ventricle
Telovelar Transvermian
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approach in the literature (40). Overall, patients with CM of the ventral pons have generally fared better than their counterparts with dorsal lesions requiring approaches via the floor of the fourth ventricle (16, 18, 40). This may be in part attributable to “safer” entry zones in the ventrolateral pons (16, 18, 43) as well as the generally low morbidity of the oft-used retrosigmoid approach. Nevertheless, this approach is limited in true ventral exposure because it requires ample retraction of the cerebellum. To overcome this, a recent report by Ohue et al. (37) presented the retrosigmoid suprafloccular transhorizontal fissure approach. The horizontal fissure of the cerebellum is dissected between the superior semilunar lobule and flocculus, affording far easier access to the root entry zone of the fifth nerve and limiting requisite cerebellar retraction. The authors used this approach for 10 pontine CM, with complete resection in nine cases and only one patient experiencing long-term worsening of condition (37). At times, a more direct ventral approach is still required, necessitating either an anterior transpetrosal (Kawase) (24, 48) or presigmoid (retrolabyrinthine) approach (21, 46). Hauck et al. (21) recently demonstrated the added ventral exposure afforded by the latter in nine patients. All CM were completely resected, and only one patient experienced long-term morbidity (hearing loss). Regardless of the selected approach, care must be taken to identify and preserve associated developmental venous anomalies (2, 16, 18). After drainage of the hematoma and definition of a peripheral cleavage plane, the lesion is often removed piecemeal to avoid undue traction on the brainstem, with subsequent meticulous hemostasis and inspection for residual lesion. As we demonstrate, 62% of residual lesions will bleed postoperatively (often early), emphasizing the importance of complete resection. Radiosurgery As acknowledged by Lunsford et al. (31), stereotactic radiosurgery (SRS) is a potential alternative to observation of aggressive CM, not to microsurgery. Two of the largest series of CM SRS have recently been reported (31, 34). Both were primarily comprised of brainstem CM, and rates of post-SRS hemorrhage ranged from 11% to 15% per year
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in the first 2 years after SRS, decreasing to 1% to 2.4% thereafter. Adverse radiation events occurred in approximately 15% of patients in each series. The pre-SRS hemorrhage rates are inflated by selection bias implicit in these studies. In addition, several patients, intuitively with high-risk CM, are selected to undergo surgery after SRS, deflating postSRS hemorrhage rates with time. One must also question whether post-SRS hemorrhage rates in these studies differ from the natural history of these lesions. One natural history study has already demonstrated inherent clustering of CM hemorrhages (4). The lack of impact of CM size on postSRS bleed rate is also notable. Given the fact that CM size has been repeatedly shown not to impact natural hemorrhage rate (19, 26, 33), by extrapolation from the literature on arteriovenous malformation SRS (38, 41), one would expect small CM to have significantly lower post-SRS hemorrhage rates than larger ones. This has not yet been reported (34), reinforcing uncertainty about the actual effects of SRS on CM. Indeed, as is well known, SRS can in fact induce de novo CM development (35), ironically even after SRS for other CM (54). CONCLUSION Brainstem CMs continue to present a considerable microsurgical challenge, with high early postoperative morbidity rates (45%) and long-term worsening in approximately 15% of patients after surgery. Complete excision, achieved in 91% of cases overall, should be the goal, as 62% of partially resected CMs rebled postoperatively. Even as an alternative only to observation, CM SRS is still reviewed with skepticism.
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45. Scott BB, Seeger JF, Schneider RC: Successful evacuation of a pontine hematoma secondary to rupture of a pathologically diagnosed ”cryptic” vascular malformation: Case report. J Neurosurg 39:104-108, 1973.
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46. Seifert V, Raabe A, Zimmermann M: Conservative (labyrinth-preserving) transpetrosal approach to the clivus and petroclival region—indications, complications, results and lessons learned. Acta Neurochir (Wien) 145:631-642, 2003. 47. Simard JM, Garcia-Bengochea F, Ballinger WE Jr, Mickle JP, Quisling RG: Cavernous angioma: A review of 126 collected and 12 new clinical cases. Neurosurgery 18:162-172, 1986. 48. Steiger HJ, Hanggi D, Stummer W, Winkler PA: Custom-tailored transdural anterior transpetrosal approach to ventral pons and retroclival regions. J Neurosurg 104:38-46, 2006. 49. Steno J, Bizik I, Stenova J, Timarova G: Subtemporal transtentorial resection of cavernous malformations involving the pyramidal tract in the upper pons and mesencephalon. Acta Neurochir (Wien) 153:1955-1962, 2011. 50. Tarnaris A, Fernandes RP, Kitchen ND: D1oes conservative management for brain stem cavernomas have better long-term outcome? Br J Neurosurg 22:748-757, 2008. 51. Terao H, Hori T, Matsutani M, Okeda R: Detection of cryptic vascular malformations by computerized tomography: Report of two cases. J Neurosurg 51:546-551, 1979. 52. Vrethem M, Thuomas KA, Hillman J: Cavernous angioma of the brain stem mimicking multiple sclerosis. N Engl J Med 336:875-876, 1997. 53. Wang CC, Liu A, Zhang JT, Sun B, Zhao YL: Surgical management of brain-stem cavernous malformations: report of 137 cases. Surg Neurol 59:444-454, 2003. 54. Yeon JY, Suh YL, Kim JH, Lee JI: Development of de novo cavernous hemangioma after radiosurgery for cavernous hemangioma. J Korean Neurosurg Soc 48:532-533, 2010. 55. Yoshimoto T, Suzuki J: Radical surgery on cavernous angioma of the brainstem. Surg Neurol 26:72-78, 1986.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 13 January 2012; accepted 3 April 2012; published online 5 April 2012 Citation: World Neurosurg. (2013) 80, 1/2:89-93. http://dx.doi.org/10.1016/j.wneu.2012.04.002 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
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Key words Angioma - Brainstem - Cavernoma - Cavernous - Surgery -
Abbreviations and Acronyms CM: Cavernous malformation SRS: Stereotactic radiosurgery From the 1Department of Neurological Surgery, Brigham and Womens Hospital and Harvard Medical School, Boston, Massachusetts; 2Department of Neurological Surgery, The Feinberg School of Medicine and McGaw Medical Center, Northwestern University, Chicago, Illinois; and 3Section of Neurosurgery, The Pritzker School of Medicine, The University of Chicago, Chicago, Illinois, USA To whom correspondence should be addressed: Rose Du, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2013) 80, 1/2:89-93. http://dx.doi.org/10.1016/j.wneu.2012.04.002 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
INTRODUCTION Among the variety of lesions faced by vascular neurosurgeons, brainstem cavernous malformations (CMs) present a considerable microsurgical challenge and were once the subject of rare case reports (13, 45, 51). After large series were reported by the Barrow Neurological Institute in 1999 (40) and the Beijing Neurosurgical Institute in 2003 (53), an explosion of studies surfaced in the literature detailing the results of surgical resection (9, 16, 18, 50). Amidst this, we previously amassed results from 52 surgical series with 821 patients and found a 92% complete excision rate with 85% of patients being improved or the same at long-term follow-up (18). Impressively, since this initial report, a litany of series with nearly as many patients have been reported (1, 2, 6, 10-12, 15, 17, 20, 22, 23, 30, 32, 36, 42, 44, 49, 50), prompting us to amass their results, compare them, and combine them with those of our previous report.
- OBJECTIVE:
Although surgical resection of brainstem cavernous malformations (CM) has been reviewed, numerous large surgical series have been recently reported.
- METHODS:
Eighteen new surgical series with 710 patients were found via a PubMed search, in addition to our previous meta-analysis. Complete excision, complications, and long-term outcome results were compiled across these series. They were then compared and subsequently combined with those of our previous report.
- RESULTS:
We combined results of 68 surgical series with 1390 patients, incorporating results from our previous meta-analysis. Across 61 series, 1178 of 1291 (91%) CMs were completely excised. Of 105 partially resected CMs with ample follow-up, 65 rebled (62%). Across 46 series providing information on early neurologic morbidity, the overall rate was 45%. Specifically, 12% of patients required tracheostomy and/or gastrostomy procedures. Overall longterm condition was improved in 62% of patients across 51 series. Across 60 series, overall long-term condition was improved or the same in 84% of patients, with worsening in the remaining 16%. The overall surgical and/or cavernoma related mortality rate for all 1390 patients was 1.5%. Notably, these results did not differ significantly between our initial review and the combined data from the subsequent 18 surgical series recently reported in the literature.
- CONCLUSION:
Surgical resection of brainstem CM continues to present a considerable challenge with resultant morbidity akin to another CM hemorrhage. We therefore prefer to offer surgery only to patients with at least one previous hemorrhage with CM pial representation. Appropriate patient counseling about expected early morbidity and the potential for long-term worsening is crucial.
METHODS The PubMed database was queried with the search terms “cavernoma,” “cavernous malformation,” “cavernous angioma,” “brainstem,” and “surgery” from May 2008 to January 2012. As per our previous selection criteria, any series containing at least three patients with brainstem CMs undergoing surgery was included. This resulted in 18 reports (1, 2, 6, 10-12, 15, 17, 20, 22, 23, 30, 32, 36, 42, 44, 49, 50), two of which were inclusive, larger updates of previous series in the literature (2, 5, 15, 40). We first compiled these results and compared them with those of our previous review (18). We then combined results from both analyses to synthesize overall complete excision rates, early morbidity, tracheostomy and/or
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gastrostomy rates, and long-term follow-up condition. Patients that were reported in multiple reports, namely those in larger updates of prior reports (2, 5, 15, 40), were counted once.
RESULTS During the last 3.5 years, 18 surgical series containing at least three patients with brainstem CMs were reported, including the largest study of 260 patients reported by Abla et al. (2). These 18 series included a total of 710 patients (median: 26.5 patients), a similar total to the 821 patients presented across 52 surgical series over the prior 21 years. Results are summarized in Table 1.
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Table 1. Surgical Series of Brainstem Cavernous Malformations, 2008 to 2011 Study
Patients
Obliteration Rate
Postop Rebleeds*
Abla et al., 2010 (1)
40
34/40 (85%)
5/6 (83%)
Abla et al., 2011 (2)
260
231/260 (89%)
18/29 (62%)
Bhardwaj et al., 2009 (6)
7
5/7 (71%)
Cenzato et al., 2008 (10)
30
27/30 (90%)
Chen et al., 2011 (11)
55
Consales et al., 2010 (12)
Early Morbidity 19/40 (48%)
Trach/PEG 4/40 (10%)
Improved 16/36 (44%)
137/260 (53%) 27/260 (10%) 174/257 (68%)
Same
Worse
Death
9/36 (25%) 10/36 (28%)
1/40 (2.5%)
83 same or worse
3/260 (1.2%)
5/7 (71%)
1/7 (14%)
3/7 (43%)
8/30 (27%)
21/30 (70%)
8/30 (27%)
1/30 (3%)
0
55/55 (100%)
14/55 (25%)
38/52 (73%)
6/52 (12%)
8/52 (15%)
0
4/4 (100%)
1/4 (25%)
2/4 (50%)
2/4 (50%)
4
Dukatz et al., 2011 (15)
71
69/71 (97%)
Francois et al., 2010 (17)
9
7/9 (78%)
1/3 (33%)
44/71 (62%) 19/71 (27%) 2/2 (100%)
Hauck et al., 2009 (20)
44
42/44 (95%)
2/2 (100%)
Huang et al., 2010 (22)
22
20/22 (91%)
1/2 (50%) 1/1 (100%)
Ichinose et al., 2010 (23)
10
9/10 (90%)
Li et al., 2010 (30)
37
37/37 (100%)
Menon et al., 2011 (32)
23
0
4/9 (44%)
7/9 (78%) 5/44 (11%)
6/22 (27%)
8/37 (22%)
5/37 (14%)
12/23 (52%)
5/23 (22%)
0
3/7 (43%)
0
0
0
8/71 (11%)
0
2/9 (22%)
0
13/44 (30%)
26 (59%)
5 (11%)
0
10/22 (45%)
9/22 (41%)
3/22 (14%)
0
7/10 (70%)
3/10 (30%)
20/37 (54%) 15/37 (41%) 9/23 (39%)
Ohue et al., 2010 (36)
36
33/36 (92%)
1/3 (33%)
18/36 (50%)
16/36 (44%)
Ramina et al., 2011 (42)
43
42/43 (98%)
0/1 (0%)
6/43 (14%)
14/43 (33%)
Sanai et al., 2010 (44)
4
4/4 (100%)
Steno et al., 2011 (49)
9
7/9 (78%)
1/2 (50%)
3/9 (33%)
1/4 (25%)
7/9 (78%)
Tarnaris et al., 2008 (50)
6
4/6 (67%)
3/3 (100%)
2/6 (33%)
1/5 (20%)
0 17 (47%)
0
0
2/37 (5%)
0
12/23 (52%)
2/23 (9%)
3 (8%)
0 0
4 improved/same 0 1/5 (20%)
0 0 3/5 (60%)
0 2/9 (22%) 0
CM, cavernous malformation; Trach, tracheostomy; PEG, percutaneous endoscopic gastrostomy. *For incompletely resected CM.
Comparing these new series to those amassed in our previous report (Table 2), we found the same 92% complete excision rate. Complication rates were also remarkably similar—a 42% early neurologic morbidity rate with 58% of patients improved, 84% improved or the same, and 16% worse or dead at long-term follow-up. Overall, excluding overlapping studies, we had data for 1390 patients across 68 surgical series. Across 61 series with 1291 patients, there was an overall 91% complete excision rate. Importantly, of 105 partially resected CMs with ample followup, 65 rebled (62%). The mortality rate from hemorrhage of a residual CM was 6% (4/65 cases). Across 46 series with 944 patients, there was a 45% early neurologic morbidity rate. Twelve percent of patients across 10 series required an early tracheostomy and/or gastrostomy. One-half of these reports provided follow-up of these patients, and only 4 of 26 (15%) tracheostomies and/or gastrostomies were permanent. Long term condition was improved in 62% of patients across 51
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series. Across 60 reports, long-term condition was improved or the same in 84% of patients while 14% of patients were worse. Surgical and/or cavernomarelated mortality was 1.5% across all studies. DISCUSSION Previously confused with demyelinating disease (3, 7, 52), brainstem gliomas (47, 55), and even strokes (25, 27), brainstem CMs are now recognized as a curable cause of morbid brainstem injury. Concomitant with advances in magnetic resonance imaging techniques, small surgical series detailing the resection of brainstem CMs began to surface in the late 1980s (29, 55) with a subsequent explosion of studies undertaken during the past decade (2, 9, 15, 16, 18, 50, 53). Although the results provided by this comprehensive review may serve as a guide, contemplation of resecting these challenging lesions requires an understanding of their natural history weighed against, most importantly, the
surgeon’s own surgical outcomes and experience. Natural History In a recent review of natural history studies of CMs incorporating a total of 837 patients, 18% had brainstem CM (19). Combining data from 3 prospective studies (26, 33, 39), the overall hemorrhage rate of all CM was 2.4% per patientyear (19). Female sex (33) and hemorrhage (26, 39) were risk factors for subsequent bleeding (19). Although brainstem location was generally not a risk factor for hemorrhage per se, it clearly correlated with a more malignant clinical course, with the study of Porter et al. (39) citing an annual clinical event rate as high as 10.6% for these lesions. It is clear however that a subset of brainstem CM may have a relatively benign natural history (28), whereas others may rebleed several times in one year (4, 20). This is underscored by surgical series reporting annual rebleed rates ranging from 18% to 60% (9, 16, 20, 40, 53). Furthermore, in the recent study
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Table 2. Summary of Results from Our Initial, Current, and Combined Review of 68 Surgical Series with at Least 3 Brainstem Cavernous Malformations in the Literature Initial Report
Current Report
Total
Total patients Number of series
821 52
710 18
1390 68
Resection rate Number of series
684/745 (92%) 46
631/687 (92%) 17
1178/1291 (91%) 61
Postop rebleeds Number of series
30/51 11
35/54 11
65/105 22
Early morbidity Number of series
236/500 (47%) 33
244/585 (42%) 15
425/944 (45%) 46
Trach/PEG Number of series
18/161 (11%) 5
46/390 (12%) 6
52/434 (12%) 10
Overall condition Improved Number of series
224/316 (71%) 35
400/695 (58%) 17
Improved/same Number of series
577/683 (85%) 45
334/399 (84%) 16
889/1058 (84%) 60
Worse Number of series
93/683 (14%) 45
60/399 (15%) 16
151/1058 (14%) 60
Died Number of series
16/821 (1.8%) 52
8/710 (1.1%) 17
21/1390 (1.5%) 68
609/987 (62%) 51
PEG, percutaneous endoscopic gastrostomy.
of Hauck et al. (20), after a second neurological event, the subsequent monthly event rate was 8%. This reinforces the validity of intervention after at least one CM hemorrhage.
Surgical Approach Given that brainstem CM may follow a relatively benevolent natural course, we do not operate on incidental or asymptomatic lesions. In fact, we often await a second hemorrhage before offering surgery, defining the lesion as one within the aggressive subset of brainstem CM, requiring treatment to avoid impending further deterioration. In preparation for surgery, like other groups (2), we counsel patients that the early postoperative outcome may mimic an additional hemorrhagic event, underscored by the 45% perioperative neurologic morbidity rate and 12% rate of early tracheostomy and/or gastrostomy from our review. In the largest series reported to date, the rates of postoperative cerebrospinal fluid leak and postoperative wound infection or meningitis were 5% each (2). Across the
experienced hands of surgeons included in our review, a worse condition at follow-up was observed in 14% of cases, with a 1.5% chance of death. It is also noteworthy that the rate of complete excision and outcome results did not significantly differ in recent surgical series compared with those in our original review. From a number of potential options (Table 3), surgical approach can often be
dictated by the two-point method advocated by Brown et al. (8). Since our previous report, several small series detailing approaches to the dorsal midbrain and ventral pons have surfaced. Five variants to the supracerebellar infratentorial approach to the dorsal midbrain have been demonstrated across two recent studies (14, 44). De Oliveira et al. (14) describe three medialto-lateral variants used in 45 patients with brainstem CM, presenting the traditional median and paramedian supracerebellar infratentorial trajectories as well as the extreme lateral supracerebellar infratentorial approach. The latter, used in 23 of 45 cases in this series, is performed with the patient in the park-bench position. A retrosigmoid craniotomy is performed with skeletonization of the transverse sinus and extension of the craniotomy above it, with the surgeon removing bone that would otherwise obstruct an extreme lateral approach above the cerebellum. Sanai et al. (44) describe two superior to inferior variants of the supracerebellar infratentorial approach, naturally created by widening the supracerebellar infratentorial plane via the sitting position. One trajectory along the superior cerebellum (supracerebellar supratrochlear) affords access as high as the thalamus, whereas the other along the tentorium (infratentorial infratrochlear) affords access as low as the fourth cranial nerve. These approaches were used in four cases of brainstem CM, resulting in complete resection in all cases without any patients suffering long-term worsening. Approaches to ventral pontine lesions have varied from the standard retrosigmoid craniotomy to the extensive transcochlear
Table 3. Surgical Approaches to Brainstem Cavernous Malformation Location
Approach
Posterior midbrain
Supracerebellar infratentorial Occipital transtentorial
Anterior midbrain/upper pons
Pterional/orbitozygomatic transsylvian Subtemporal
Anterior pons
Retrosigmoid Anterior transpetrosal (Kawase) Presigmoid/retrolabyrinthine
Anterior medulla
Far lateral Transoral
Floor of fourth ventricle
Telovelar Transvermian
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approach in the literature (40). Overall, patients with CM of the ventral pons have generally fared better than their counterparts with dorsal lesions requiring approaches via the floor of the fourth ventricle (16, 18, 40). This may be in part attributable to “safer” entry zones in the ventrolateral pons (16, 18, 43) as well as the generally low morbidity of the oft-used retrosigmoid approach. Nevertheless, this approach is limited in true ventral exposure because it requires ample retraction of the cerebellum. To overcome this, a recent report by Ohue et al. (37) presented the retrosigmoid suprafloccular transhorizontal fissure approach. The horizontal fissure of the cerebellum is dissected between the superior semilunar lobule and flocculus, affording far easier access to the root entry zone of the fifth nerve and limiting requisite cerebellar retraction. The authors used this approach for 10 pontine CM, with complete resection in nine cases and only one patient experiencing long-term worsening of condition (37). At times, a more direct ventral approach is still required, necessitating either an anterior transpetrosal (Kawase) (24, 48) or presigmoid (retrolabyrinthine) approach (21, 46). Hauck et al. (21) recently demonstrated the added ventral exposure afforded by the latter in nine patients. All CM were completely resected, and only one patient experienced long-term morbidity (hearing loss). Regardless of the selected approach, care must be taken to identify and preserve associated developmental venous anomalies (2, 16, 18). After drainage of the hematoma and definition of a peripheral cleavage plane, the lesion is often removed piecemeal to avoid undue traction on the brainstem, with subsequent meticulous hemostasis and inspection for residual lesion. As we demonstrate, 62% of residual lesions will bleed postoperatively (often early), emphasizing the importance of complete resection. Radiosurgery As acknowledged by Lunsford et al. (31), stereotactic radiosurgery (SRS) is a potential alternative to observation of aggressive CM, not to microsurgery. Two of the largest series of CM SRS have recently been reported (31, 34). Both were primarily comprised of brainstem CM, and rates of post-SRS hemorrhage ranged from 11% to 15% per year
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in the first 2 years after SRS, decreasing to 1% to 2.4% thereafter. Adverse radiation events occurred in approximately 15% of patients in each series. The pre-SRS hemorrhage rates are inflated by selection bias implicit in these studies. In addition, several patients, intuitively with high-risk CM, are selected to undergo surgery after SRS, deflating postSRS hemorrhage rates with time. One must also question whether post-SRS hemorrhage rates in these studies differ from the natural history of these lesions. One natural history study has already demonstrated inherent clustering of CM hemorrhages (4). The lack of impact of CM size on postSRS bleed rate is also notable. Given the fact that CM size has been repeatedly shown not to impact natural hemorrhage rate (19, 26, 33), by extrapolation from the literature on arteriovenous malformation SRS (38, 41), one would expect small CM to have significantly lower post-SRS hemorrhage rates than larger ones. This has not yet been reported (34), reinforcing uncertainty about the actual effects of SRS on CM. Indeed, as is well known, SRS can in fact induce de novo CM development (35), ironically even after SRS for other CM (54). CONCLUSION Brainstem CMs continue to present a considerable microsurgical challenge, with high early postoperative morbidity rates (45%) and long-term worsening in approximately 15% of patients after surgery. Complete excision, achieved in 91% of cases overall, should be the goal, as 62% of partially resected CMs rebled postoperatively. Even as an alternative only to observation, CM SRS is still reviewed with skepticism.
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 13 January 2012; accepted 3 April 2012; published online 5 April 2012 Citation: World Neurosurg. (2013) 80, 1/2:89-93. http://dx.doi.org/10.1016/j.wneu.2012.04.002 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
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