- Email: [email protected]
Multimodal Intraoperative Neuromonitoring in Aneurysm Surgery
Accepted Manuscript Multimodal Intraoperative Neuromonitoring In Aneurysm Surgery Giovanni Grasso, MD, PhD, Alessandro Landi, MD, Concetta Alfaci, MD PII:
S1878-8750(17)30276-0
DOI:
10.1016/j.wneu.2017.02.103
Reference:
WNEU 5334
To appear in:
World Neurosurgery
Received Date: 12 February 2017 Accepted Date: 15 February 2017
Please cite this article as: Grasso G, Landi A, Alfaci C, Multimodal Intraoperative Neuromonitoring In Aneurysm Surgery, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.02.103. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Multimodal Intraoperative Neuromonitoring In Aneurysm Surgery Giovanni Grasso MD, PhD1*, Alessandro Landi, MD, and Concetta Alfaci MD.
Section of Neurosurgery, Department of Experimental Biomedicine and Clinical Neurosciences
(BIONEC), University of Palermo, Palermo, ITALY, 2
Department of Neurology and Psychiatry, Neurosurgery, "Sapienza" University of Rome, Rome,
Italy. Department of Neurosurgery, University of Messina, Italy
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Corresponding Author: Giovanni Grasso, M.D., Ph.D. Section of Neurosurgery, Department of Experimental Biomedicine and Clinical Neurosciences Policlinico Universitario di Palermo Via del Vespro 129 90100 Palermo, ITALY e-mail: [email protected] Tel: +39 091 6552399 Fax: +39 091 6552399
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1
1
ACCEPTED MANUSCRIPT
Following aneurysmal subarachnoid hemorrhage, the primary goal of the treatment is to exclude the vascular malformation from the intracranial circulation while preserving the parent artery. In unruptured aneurysms, the decision as to whether to treat or observe the malformation is
RI PT
made on a case-by-case basis. In this regard, the International Study of Unruptured Intracranial Aneurysm (ISUIA) have suggested that aneurysm size and location were independent predictors for aneurysm rupture (1). ISUIA examined 1692 patients with cerebral aneurysms with a mean follow-
SC
up of 4.1 years. Rupture rates differed depending on size and location, ranging from 0 % in
aneurysms less than 7 mm located in the internal carotid artery, anterior circulation, or middle
M AN U
cerebral artery to up to 50% in aneurysms greater than 25 mm in size located in the posterior circulation (1). Most recently, the Unruptured Cerebral Aneurysm Study (UCAS) yielded results similar to the ISUIA (2). However, other evidence has contradicted these studies, reporting a higher percentage of small aneurysms among their case series of ruptured intracranial aneurysms (3-5). This
TE D
indicates a discrepancy between the ISUIA and UCAS data and the size of ruptured aneurysms seen in routine clinical practice. The conclusions reported from ISUIA have stimulated many controversies because they were based on data-driven post-hoc reconstructions of artificial
EP
subgroups too small to be reliable. Although ISUIA is the largest prospective study on unruptured aneurysms it is actually quite small when one considers the ambitions of the study, the retention of
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patients and length of follow-ups, and the intention to analyze numerous subgroups. Accordingly, the conclusions made about aneurysm size concerning rupture rate are still open to question. For ruptured cerebral aneurysms, it is well known that the exclusion of the vascular malformation from the cerebral circulation should be performed as soon as possible (6). In this scenario, both surgical clipping and endovascular techniques are valid treatment modalities to achieve such a goal. Among the main randomized, prospective studies published, the International Subarachnoid Aneurysm Trial (ISAT) (7) have strongly modified the management of ruptured cerebral aneurysm since it reported an improved survival with coiling which was statistically significant when 2
ACCEPTED MANUSCRIPT compared with surgical treatment at 12 months follow-up. Although the rate of occlusion was higher in clipped aneurysms as compared to coiled aneurysms, coiling resulted in a significantly decreased rate of death or dependency as compared to clipping. Although the results of this study stimulated a number of criticisms, the treatment of ruptured cerebral aneurysms is dramatically
RI PT
changed over the years being, to date, the endovascular treatment the approach chosen for most ruptured intracranial aneurysms.
SC
While a number of technological innovations have taken place for the endovascular
procedures, little technological advancements have been entered in the microsurgery. Most of them
M AN U
have been shown to aid in preventing intra and post-operative complications. Pitfalls after microsurgical clipping include accidental vessel occlusion by the permanent clip, temporary occlusion for proximal control, iatrogenic vasospasm or thromboembolism by surgical manipulation, small vessel injury during dissection, and ischemia following brain retraction (8). As shown in various studies, ischemic complications account for 6.7% of all complications after
TE D
microsurgical clipping (8), and even for unruptured aneurysms located in the anterior circulation, the risk of a new postoperative motor deficit is approximately 5% (9). Several methods have been
EP
developed to prevent ischemic complications, such as intraoperative neuromonitoring (IONM) using somatosensory evoked potentials (SSEPs) and motor evoked potentials (MEPs),
AC C
microvascular Doppler sonography, and indocyanine green angiography (ICGA). In this regard, IONM using SSEPs and/or MEPs has been shown to successfully assess the cerebral blood flow supply based on neuronal function (10). It also has provided evidence in detecting inappropriate blood flow from small perforating arteries involved in surgical procedures (10). In this issue of WORLD NEUROSURGERY Staarmann and collaborators (11) retrospectively examined the sensitivity and specificity of intraoperative neuromonitoring (IONM) using MEPs and SSEPs, and quantified the safety of temporary clipping by duration and vascular territory. A total of 123 consecutive patients with 133 cerebral aneurysms were considered. Of 133 3
ACCEPTED MANUSCRIPT clipped aneurysms, 15 cases of IONM changes occurred, including 12 temporary without new postoperative deficit, and 3 permanent with new postoperative deficit. SSEP monitoring predicted 1 of the permanent deficits and transcranial MEP predicted the other 2 deficits. Overall, they found a
these two modalities were used in combination.
RI PT
sensitivity of 33% for SSEP and 66% for MEP alone. Accordingly, the percentage was 100% when
Though this study involves a potential selection bias owing to its retrospective nature, it brings new information on the topic worthy of consideration.
SC
Although SSEPs monitoring has high specificity, can be performed continuously during operative procedures and it is less affected by anesthetic agents (10), the sensitivity of SSEP monitoring may
M AN U
be not adequate to detect a lesion by operative procedures outside the lemniscal system. In this regard, a significant rate up to 10% of cases with new postoperative motor deficits has been observed after surgery for anterior circulation aneurysms, despite unaltered intraoperative SSEP recordings (12). This because the sensitivity of SSEP monitoring is not adequate to detect damage to
TE D
deep perforating arteries of the MCA such as lenticulostriate arteries and cortical MCA branches that supply the descending motor pathways (13, 14). Therefore, including MEP monitoring, which involves higher sensitivity for detection of motor deficits and allows for the detection of blood flow
EP
insufficiency earlier than SSEPs monitoring, offers the opportunity to overcome the limitations of SSEP monitoring (15). In aneurysm surgery, MEPs are superior to SSEPs in most situations since
AC C
they allow the surgeon to react promptly, just before SSEP changes occur. Accordingly, during aneurysm surgery both MEPs and SSEPs monitoring are desirable to reduce the risks of injury. The study by Staarmann and collaborators (11) provide evidence that IONM is a simple, safe, and reliable tool for the prediction of postoperative ischemic complications. The ischemic complications can be reduced via prompt corrective measures taken on the basis of IONM changes during aneurysm surgery.
4
ACCEPTED MANUSCRIPT A randomized controlled study would definitively confirm the ability of IONM in reducing morbidity in aneurysm surgery. However, considering that IONM is potentially beneficial makes it
AC C
EP
TE D
M AN U
SC
RI PT
challenging to conduct such a study without ethical concerns.
5
ACCEPTED MANUSCRIPT REFERENCES
6.
7.
8.
9.
10.
11.
12.
RI PT
SC
5.
M AN U
4.
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3.
EP
2.
Wiebers DO, Whisnant JP, Huston J, 3rd, Meissner I, Brown RD, Jr., Piepgras DG, Forbes GS, Thielen K, Nichols D, O'Fallon WM, Peacock J, Jaeger L, Kassell NF, KongableBeckman GL, Torner JC, International Study of Unruptured Intracranial Aneurysms I Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment Lancet 362: 103-110, 2003 Investigators UJ, Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T The natural course of unruptured cerebral aneurysms in a Japanese cohort The New England journal of medicine 366: 2474-2482, 2012 Juvela S, Poussa K, Lehto H, Porras M Natural history of unruptured intracranial aneurysms: a long-term follow-up study Stroke; a journal of cerebral circulation 44: 2414-2421, 2013 Wardlaw JM, White PM The detection and management of unruptured intracranial aneurysms Brain : a journal of neurology 123 ( Pt 2): 205-221, 2000 Winn HR, Jane JA, Sr., Taylor J, Kaiser D, Britz GW Prevalence of asymptomatic incidental aneurysms: review of 4568 arteriograms Journal of neurosurgery 96: 43-49, 2002 Bederson JB, Connolly ES, Jr., Batjer HH, Dacey RG, Dion JE, Diringer MN, Duldner JE, Jr., Harbaugh RE, Patel AB, Rosenwasser RH, American Heart A Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association Stroke; a journal of cerebral circulation 40: 994-1025, 2009 Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P, International Subarachnoid Aneurysm Trial Collaborative G International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion Lancet 366: 809-817, 2005 Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, Kale SP, Cruz-Flores S Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm Stroke 41: 1471-1476, 2010 Krayenbühl N, Erdem E, Oinas M, Krisht AF Symptomatic and silent ischemia associated with microsurgical clipping of intracranial aneurysms: Evaluation with diffusion-weighted MRI Stroke 40: 129-133, 2009 Penchet G, Arné P, Cuny E, Monteil P, Loiseau H, Castel JP Use of intraoperative monitoring of somatosensory evoked potentials to prevent ischaemic stroke after surgical exclusion of middle cerebral artery aneurysms Acta Neurochirurgica 149: 357-364, 2007 Staarmann B, O’Neal K, Magner M, Zuccarello M Sensitivity and Specificity of Intraoperative Neuromonitoring for Identifying Safety and Duration of Temporary Aneurysm Clipping Based on Vascular Territory, a Multimodal Strategy World Neurosurgery 2017 Wiedemayer H, Sandalcioglu IE, Armbruster W, Regel J, Schaefer H, Stolke D False negative findings in intraoperative SEP monitoring: Analysis of 658 consecutive neurosurgical cases and review of published reports Journal of Neurology, Neurosurgery and Psychiatry 75: 280-286, 2004
AC C
1.
6
ACCEPTED MANUSCRIPT
RI PT
SC M AN U TE D
15.
EP
14.
Friedman WA, Chadwick GM, Verhoeven FJS, Mahla M, Day AL Monitoring of somatosensory evoked potentials during surgery for middle cerebral artery aneurysms Neurosurgery 29: 83-88, 1991 Horiuchi K, Suzuki K, Sasaki T, Matsumoto M, Sakuma J, Konno Y, Oinuma M, Itakura T, Kodama N Intraoperative monitoring of blood flow insufficiency during surgery of middle cerebral artery aneurysms Journal of Neurosurgery 103: 275-283, 2005 Yeon JY, Seo DW, Hong SC, Kim JS Transcranial motor evoked potential monitoring during the surgical clipping of unruptured intracranial aneurysms Journal of the Neurological Sciences 293: 29-34, 2010
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13.
7
S1878-8750(17)30276-0
DOI:
10.1016/j.wneu.2017.02.103
Reference:
WNEU 5334
To appear in:
World Neurosurgery
Received Date: 12 February 2017 Accepted Date: 15 February 2017
Please cite this article as: Grasso G, Landi A, Alfaci C, Multimodal Intraoperative Neuromonitoring In Aneurysm Surgery, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.02.103. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Multimodal Intraoperative Neuromonitoring In Aneurysm Surgery Giovanni Grasso MD, PhD1*, Alessandro Landi, MD, and Concetta Alfaci MD.
Section of Neurosurgery, Department of Experimental Biomedicine and Clinical Neurosciences
(BIONEC), University of Palermo, Palermo, ITALY, 2
Department of Neurology and Psychiatry, Neurosurgery, "Sapienza" University of Rome, Rome,
Italy. Department of Neurosurgery, University of Messina, Italy
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Corresponding Author: Giovanni Grasso, M.D., Ph.D. Section of Neurosurgery, Department of Experimental Biomedicine and Clinical Neurosciences Policlinico Universitario di Palermo Via del Vespro 129 90100 Palermo, ITALY e-mail: [email protected] Tel: +39 091 6552399 Fax: +39 091 6552399
M AN U
SC
3
RI PT
1
1
ACCEPTED MANUSCRIPT
Following aneurysmal subarachnoid hemorrhage, the primary goal of the treatment is to exclude the vascular malformation from the intracranial circulation while preserving the parent artery. In unruptured aneurysms, the decision as to whether to treat or observe the malformation is
RI PT
made on a case-by-case basis. In this regard, the International Study of Unruptured Intracranial Aneurysm (ISUIA) have suggested that aneurysm size and location were independent predictors for aneurysm rupture (1). ISUIA examined 1692 patients with cerebral aneurysms with a mean follow-
SC
up of 4.1 years. Rupture rates differed depending on size and location, ranging from 0 % in
aneurysms less than 7 mm located in the internal carotid artery, anterior circulation, or middle
M AN U
cerebral artery to up to 50% in aneurysms greater than 25 mm in size located in the posterior circulation (1). Most recently, the Unruptured Cerebral Aneurysm Study (UCAS) yielded results similar to the ISUIA (2). However, other evidence has contradicted these studies, reporting a higher percentage of small aneurysms among their case series of ruptured intracranial aneurysms (3-5). This
TE D
indicates a discrepancy between the ISUIA and UCAS data and the size of ruptured aneurysms seen in routine clinical practice. The conclusions reported from ISUIA have stimulated many controversies because they were based on data-driven post-hoc reconstructions of artificial
EP
subgroups too small to be reliable. Although ISUIA is the largest prospective study on unruptured aneurysms it is actually quite small when one considers the ambitions of the study, the retention of
AC C
patients and length of follow-ups, and the intention to analyze numerous subgroups. Accordingly, the conclusions made about aneurysm size concerning rupture rate are still open to question. For ruptured cerebral aneurysms, it is well known that the exclusion of the vascular malformation from the cerebral circulation should be performed as soon as possible (6). In this scenario, both surgical clipping and endovascular techniques are valid treatment modalities to achieve such a goal. Among the main randomized, prospective studies published, the International Subarachnoid Aneurysm Trial (ISAT) (7) have strongly modified the management of ruptured cerebral aneurysm since it reported an improved survival with coiling which was statistically significant when 2
ACCEPTED MANUSCRIPT compared with surgical treatment at 12 months follow-up. Although the rate of occlusion was higher in clipped aneurysms as compared to coiled aneurysms, coiling resulted in a significantly decreased rate of death or dependency as compared to clipping. Although the results of this study stimulated a number of criticisms, the treatment of ruptured cerebral aneurysms is dramatically
RI PT
changed over the years being, to date, the endovascular treatment the approach chosen for most ruptured intracranial aneurysms.
SC
While a number of technological innovations have taken place for the endovascular
procedures, little technological advancements have been entered in the microsurgery. Most of them
M AN U
have been shown to aid in preventing intra and post-operative complications. Pitfalls after microsurgical clipping include accidental vessel occlusion by the permanent clip, temporary occlusion for proximal control, iatrogenic vasospasm or thromboembolism by surgical manipulation, small vessel injury during dissection, and ischemia following brain retraction (8). As shown in various studies, ischemic complications account for 6.7% of all complications after
TE D
microsurgical clipping (8), and even for unruptured aneurysms located in the anterior circulation, the risk of a new postoperative motor deficit is approximately 5% (9). Several methods have been
EP
developed to prevent ischemic complications, such as intraoperative neuromonitoring (IONM) using somatosensory evoked potentials (SSEPs) and motor evoked potentials (MEPs),
AC C
microvascular Doppler sonography, and indocyanine green angiography (ICGA). In this regard, IONM using SSEPs and/or MEPs has been shown to successfully assess the cerebral blood flow supply based on neuronal function (10). It also has provided evidence in detecting inappropriate blood flow from small perforating arteries involved in surgical procedures (10). In this issue of WORLD NEUROSURGERY Staarmann and collaborators (11) retrospectively examined the sensitivity and specificity of intraoperative neuromonitoring (IONM) using MEPs and SSEPs, and quantified the safety of temporary clipping by duration and vascular territory. A total of 123 consecutive patients with 133 cerebral aneurysms were considered. Of 133 3
ACCEPTED MANUSCRIPT clipped aneurysms, 15 cases of IONM changes occurred, including 12 temporary without new postoperative deficit, and 3 permanent with new postoperative deficit. SSEP monitoring predicted 1 of the permanent deficits and transcranial MEP predicted the other 2 deficits. Overall, they found a
these two modalities were used in combination.
RI PT
sensitivity of 33% for SSEP and 66% for MEP alone. Accordingly, the percentage was 100% when
Though this study involves a potential selection bias owing to its retrospective nature, it brings new information on the topic worthy of consideration.
SC
Although SSEPs monitoring has high specificity, can be performed continuously during operative procedures and it is less affected by anesthetic agents (10), the sensitivity of SSEP monitoring may
M AN U
be not adequate to detect a lesion by operative procedures outside the lemniscal system. In this regard, a significant rate up to 10% of cases with new postoperative motor deficits has been observed after surgery for anterior circulation aneurysms, despite unaltered intraoperative SSEP recordings (12). This because the sensitivity of SSEP monitoring is not adequate to detect damage to
TE D
deep perforating arteries of the MCA such as lenticulostriate arteries and cortical MCA branches that supply the descending motor pathways (13, 14). Therefore, including MEP monitoring, which involves higher sensitivity for detection of motor deficits and allows for the detection of blood flow
EP
insufficiency earlier than SSEPs monitoring, offers the opportunity to overcome the limitations of SSEP monitoring (15). In aneurysm surgery, MEPs are superior to SSEPs in most situations since
AC C
they allow the surgeon to react promptly, just before SSEP changes occur. Accordingly, during aneurysm surgery both MEPs and SSEPs monitoring are desirable to reduce the risks of injury. The study by Staarmann and collaborators (11) provide evidence that IONM is a simple, safe, and reliable tool for the prediction of postoperative ischemic complications. The ischemic complications can be reduced via prompt corrective measures taken on the basis of IONM changes during aneurysm surgery.
4
ACCEPTED MANUSCRIPT A randomized controlled study would definitively confirm the ability of IONM in reducing morbidity in aneurysm surgery. However, considering that IONM is potentially beneficial makes it
AC C
EP
TE D
M AN U
SC
RI PT
challenging to conduct such a study without ethical concerns.
5
ACCEPTED MANUSCRIPT REFERENCES
6.
7.
8.
9.
10.
11.
12.
RI PT
SC
5.
M AN U
4.
TE D
3.
EP
2.
Wiebers DO, Whisnant JP, Huston J, 3rd, Meissner I, Brown RD, Jr., Piepgras DG, Forbes GS, Thielen K, Nichols D, O'Fallon WM, Peacock J, Jaeger L, Kassell NF, KongableBeckman GL, Torner JC, International Study of Unruptured Intracranial Aneurysms I Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment Lancet 362: 103-110, 2003 Investigators UJ, Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T The natural course of unruptured cerebral aneurysms in a Japanese cohort The New England journal of medicine 366: 2474-2482, 2012 Juvela S, Poussa K, Lehto H, Porras M Natural history of unruptured intracranial aneurysms: a long-term follow-up study Stroke; a journal of cerebral circulation 44: 2414-2421, 2013 Wardlaw JM, White PM The detection and management of unruptured intracranial aneurysms Brain : a journal of neurology 123 ( Pt 2): 205-221, 2000 Winn HR, Jane JA, Sr., Taylor J, Kaiser D, Britz GW Prevalence of asymptomatic incidental aneurysms: review of 4568 arteriograms Journal of neurosurgery 96: 43-49, 2002 Bederson JB, Connolly ES, Jr., Batjer HH, Dacey RG, Dion JE, Diringer MN, Duldner JE, Jr., Harbaugh RE, Patel AB, Rosenwasser RH, American Heart A Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association Stroke; a journal of cerebral circulation 40: 994-1025, 2009 Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P, International Subarachnoid Aneurysm Trial Collaborative G International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion Lancet 366: 809-817, 2005 Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, Kale SP, Cruz-Flores S Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm Stroke 41: 1471-1476, 2010 Krayenbühl N, Erdem E, Oinas M, Krisht AF Symptomatic and silent ischemia associated with microsurgical clipping of intracranial aneurysms: Evaluation with diffusion-weighted MRI Stroke 40: 129-133, 2009 Penchet G, Arné P, Cuny E, Monteil P, Loiseau H, Castel JP Use of intraoperative monitoring of somatosensory evoked potentials to prevent ischaemic stroke after surgical exclusion of middle cerebral artery aneurysms Acta Neurochirurgica 149: 357-364, 2007 Staarmann B, O’Neal K, Magner M, Zuccarello M Sensitivity and Specificity of Intraoperative Neuromonitoring for Identifying Safety and Duration of Temporary Aneurysm Clipping Based on Vascular Territory, a Multimodal Strategy World Neurosurgery 2017 Wiedemayer H, Sandalcioglu IE, Armbruster W, Regel J, Schaefer H, Stolke D False negative findings in intraoperative SEP monitoring: Analysis of 658 consecutive neurosurgical cases and review of published reports Journal of Neurology, Neurosurgery and Psychiatry 75: 280-286, 2004
AC C
1.
6
ACCEPTED MANUSCRIPT
RI PT
SC M AN U TE D
15.
EP
14.
Friedman WA, Chadwick GM, Verhoeven FJS, Mahla M, Day AL Monitoring of somatosensory evoked potentials during surgery for middle cerebral artery aneurysms Neurosurgery 29: 83-88, 1991 Horiuchi K, Suzuki K, Sasaki T, Matsumoto M, Sakuma J, Konno Y, Oinuma M, Itakura T, Kodama N Intraoperative monitoring of blood flow insufficiency during surgery of middle cerebral artery aneurysms Journal of Neurosurgery 103: 275-283, 2005 Yeon JY, Seo DW, Hong SC, Kim JS Transcranial motor evoked potential monitoring during the surgical clipping of unruptured intracranial aneurysms Journal of the Neurological Sciences 293: 29-34, 2010
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7