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Distal Posterior Inferior Cerebellar Artery Aneurysm: A Mysterious Course, Historical Controversies!
Accepted Manuscript Distal PICA aneurysm: A mysterious course, historical controversies! Parviz Dolati, M.D Christopher S. Ogilvy, M.D PII:
S1878-8750(14)01002-X
DOI:
10.1016/j.wneu.2014.10.008
Reference:
WNEU 2582
To appear in:
World Neurosurgery
Received Date: 20 September 2014 Accepted Date: 14 October 2014
Please cite this article as: Dolati P, Ogilvy CS, Distal PICA aneurysm: A mysterious course, historical controversies!, World Neurosurgery (2014), doi: 10.1016/j.wneu.2014.10.008. 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
Distal PICA aneurysm: A mysterious course, historical controversies!
Christopher S. Ogilvy, M.D
RI PT
Parviz Dolati, M.D and Christopher S. Ogilvy, M.D
M AN U
SC
Professor of Neurosurgery Director, Division of Cerebrovascular/Endovascular Operative Neurosurgery Harvard Medical School Beth Israel Deaconess Medical Center Director, Beth Israel Deaconess Medical Center Brain Aneurysm institute [email protected]
TE D
Aneurysms arising from the Posterior inferior cerebellar artery (PICA) are fortunately infrequent. Its incidence varies from 0.49% to 3% of all intracranial aneurysms in various published studies (1-8). Typically, most of PICA aneurysms originate from the PICA-VA junction. Only a small proportion of these aneurysms (<1%), which are called “Distal PICA Aneurysms”, arise from more peripheral segments of this tortuous artery (1, 8). Understanding the complex anatomy of this artery is absolutely critical to choosing the best surgical approach.
AC C
EP
PICA has a very complex and variable course. In 80–95% of cases, it arises from the intracranial portion of the VA (V4), about 8.6 mm above the foramen magnum and approximately 1 cm proximal to the vertebrobasilar junction (5). Based on its anatomical relationship to the medulla oblongata and the cerebellum, PICA can be divided into five anatomical segments and two loops. Thus, the aneurysms of PICA are defined based on their origin from each of these segments: 1) Anterior medullary, from the origin of the PICA to the inferior olivary prominence; 2) Lateral medullary, starting from lateral medulla, extending to the origins of the lower cranial nerves (XI-XII); 3) Tonsillomedullary, extending to the level of the tonsillar midportion (includes the caudal loop); 4) Telovelo-tonsillar, further extension of the PICA to the cortical surface of the cerebellum (includes the cranial loop); and finally 5) cortical, extending to the cerebellar vermis and hemisphere (5). Moreover, all surgeons treating aneurysms arising from PICA should always be cognizant of the critical perforators that branch off from the first three proximal medullary segments, and supply the lower brainstem. Lister et al reported that no brain stem perforator originated from distal to the medullary segments of the PICA in a microanatomical study of 50 hemispheres (5). PICA occlusion may cause infarction of the posterior inferior cerebellum, inferior cerebellar vermis and lateral medulla. However, PICA may have many collateral connections with other cerebellar arteries or even posterior meningeal artery and the extension of this infarction or ischemia is therefore
ACCEPTED MANUSCRIPT
highly dependent on the extent of these pre-existing collaterals.
M AN U
SC
RI PT
In the peripheral segments of PICA, hemodynamic and flow-related saccular aneurysms are again the most common type of aneurysms; however, dissecting or fusiform aneurysms of PICA are also relatively more common than other cerebellar arteries. Lewis et al. reported 22 distal PICA aneurysms, of which 13 were saccular and 9 were fusiform (4). In the current study, the authors report 91 distal PICA aneurysms 57% of them were saccular and 43% were fusiform. Interestingly, the typical bifurcation aneurysms like those in the anterior circulation are rare in distal PICA and it is apparent that these saccular aneurysms are morphologically different. Most of these aneurysms are located in the second and third segments of PICA. Distal PICA aneurysms usually have a very fragile wall and have a tendency to rupture in smaller sizes compared to the anterior circulation aneurysms. Over 80% of these aneurysms present with bleeding (1-8). In most case series, including the current study, the most common size of rupture was <7 mm (1-8). The small size and location in a tortious anatomy make diagnosis of these aneurysms very difficult and they may easily be misdiagnosed in the first CTA or conventional angiography. Therefore, considering their higher risk of rebleeding, these images, especially in patients presenting with SAH in posterior fossa associated with 4th ventricular hemorrhage must be ultra-visualized. If these images are regardless still negative, a repeat angiography is highly recommended in 7-10 days.
EP
TE D
The mysterious course and variable anatomy of the PICA, raises a historical controversy in the best surgical approach to these lesions. Obviously, no standard treatment strategy has yet been agreed upon and the general belief is that treatment option should be individualized. There are many microvascular and endovascular options. If a patient has presented with a ruptured distal PICA aneurysm associated with a large posterior fossa hematoma, the decision is straightforward. However, controversy remains in cases without significant hematoma. Although sacrifying the parent artery (PICA) is unavoidable in some cases, the best treatment option would be a technique that is able to obliterate the aneurysm safely while preserving PICA, particularly its proximal brain stem perforators.
AC C
The available microvascular techniques are direct clipping, wrapping, resection, proximal occlusion or trapping with revascularization, and finally, distal occlusion. In the current study, 93% of saccular and 68% of fusiform aneurysms have been clipped. Presence of SAH around the brain stem, relationship between the PICA aneurysms, lower cranial nerves, and medulla oblongata make microsurgical dissection of these aneurysms very difficult. In selected cases, occluding the PICA distal to its medullary segments could be safely performed without any brainstem injury. For more proximal occlusion, revascularization or possible endovascular techniques are recommended.
Current endovascular techniques include: selective coiling of the aneurysm, or occlusion of the parent artery with coil, Onyx, or n-butyl cyanoacrylate (n-BCA). Endovascular treatment, although successful in most cases, may be complicated by the
ACCEPTED MANUSCRIPT
aneurysm shape, broadness of the neck, angulation of the aneurysm and PICA in respect to the vertebral artery, tortuosity of PICA to be navigated with microcatheters, vasospasm and intra-procedural rupture of aneurysm.
M AN U
SC
RI PT
After reading the article by Lehto et al. in this issue of WORLD NEUROSURGERY, it is interesting to note how the authors have successfully characterized the features of distal PICA aneurysms and described their invaluable experience in microsurgical management of 91 distal PICA aneurysms in 80 patients. Surgical clipping of these fragile aneurysms around brainstem and cranial nerves, as we described earlier, is a risky maneuver and much of the risk occurs in an attempt to preserve patency of PICA and its perforators to the brain stem. However, The authors are to be commended for achieving such a good clinical outcome. Several aspects of their outcomes deserve special mention. Total occlusion was achieved in 94% of the saccular and in 88% of the fusiform aneurysms. Even more notable in their series is their clinical outcome that 91% of patients that were operated on for a distal PICA aneurysm, and survived beyond 1 year, recovered to the former or an independent state of life. This is a commendable achievement despite malignant presentation and poor initial Hunt&Hess grades in some of these cases.
AC C
EP
TE D
Finally, regardless of successful characterization of a large number of distal PICA aneurysms, the current series is highly biased towards microsurgical treatment of PICA aneurysms. The authors primarily embolized only one aneurysm and another was embolized after failed clipping. Other aneurysms were treated by microsurgical techniques or conservatively. For those surgeons treating these aneurysms, this study does not clearly answer the question of which technique (microsurgery vs endovascular) should be used to obtain the best outcomes, especially in this era with huge advancements of endovascular techniques. The authors state that endovascular treatment is associated with rather high rates of procedural rupture as well as morbidity and mortality. This statement does not perfectly match with the reported endovascular outcome for treatment of these aneurysms especially in recently published literatures. With the current advancements in endovascular techniques, coiling or embolization of a distal PICA aneurysms using Onyx or n-BCA, especially those distal to the medullary segments, dissecting aneurysms, or aneurysms associated with AVMs can be performed safely. Treating physicians should therefore have several treatment strategies available and use these options selectively based on the angiographic and morphological characteristics of a given distal PICA aneurysm. This flexible and adaptive approach will secure the least morbidity and the best outcome for patients with these high-risk lesions. Key Words: Posterior inferior cerebellar artery, distal, subarachnoid hemorrhage, aneurysm
ACCEPTED MANUSCRIPT
References: 1- Gács G, Viñuela F, Fox AJ, Drake CG: Peripheral aneurysms of the cerebellar arteries. Review of 16 cases. J Neurosurg 58:63–68, 1983
RI PT
2- Horiuchi T, Tanaka Y, Hongo K, Nitta J, Kusano Y, Kobayashi S: Characteristics of distal posterior inferior cerebellar artery aneurysms. Neurosurgery 53:589–95, 2003. 3-Isokangas JM, Siniluoto T, Tikkakoski T, Kumpulainen T: Endovascular treatment of peripheral aneurysms of posterior inferior cerebellar artery. AJNR Am J Neuroradiol 29:1783-1788, 2008 4- Lewis S. B., Change D. J, Peace D. A., Lafrentz P. J., Day A. L.: Distal posterior inferior cerebellar artery aneurysms: clinical features and management. J Neurosurg 97:756–766, 2002
SC
5- Lister JR, Rhoton AL Jr, Matsushima T, Peace DA: Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery 10: 170–199, 1982
M AN U
6-Locksley HB: Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage: Section V, Part 1—Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the Cooperative Study. J Neurosurg 25:219–239, 1966 7-Tokimura H, Yamahata H, Kamezawa T, Tajitsu K, Nagayama T, Sugata S, Takiguchi K, Taniguchi A, Niiro M, Hirahara K, Takasaki K, Oyoshi T, Arita K: Clinical presentation and treatment of distal posterior inferior cerebellar artery aneurysms. Neurosurg Rev 34:57–67, 2011.
AC C
EP
TE D
8-Wiebers DO, Whisnant JP, Huston J, Meissner I, Brown RD, Piepgras DG, Forbes GS, Thielen K, Nichols D, O'Fallon WM, Peacock J, Jaeger L, Kassell NF, Kongable-Beckman GL, Torner JC; International Study of Unruptured Intracranial Aneurysms Investigators. International Study of Unruptured intracranial Aneurysms (ISUIA): natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103–110, 2003.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
S1878-8750(14)01002-X
DOI:
10.1016/j.wneu.2014.10.008
Reference:
WNEU 2582
To appear in:
World Neurosurgery
Received Date: 20 September 2014 Accepted Date: 14 October 2014
Please cite this article as: Dolati P, Ogilvy CS, Distal PICA aneurysm: A mysterious course, historical controversies!, World Neurosurgery (2014), doi: 10.1016/j.wneu.2014.10.008. 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
Distal PICA aneurysm: A mysterious course, historical controversies!
Christopher S. Ogilvy, M.D
RI PT
Parviz Dolati, M.D and Christopher S. Ogilvy, M.D
M AN U
SC
Professor of Neurosurgery Director, Division of Cerebrovascular/Endovascular Operative Neurosurgery Harvard Medical School Beth Israel Deaconess Medical Center Director, Beth Israel Deaconess Medical Center Brain Aneurysm institute [email protected]
TE D
Aneurysms arising from the Posterior inferior cerebellar artery (PICA) are fortunately infrequent. Its incidence varies from 0.49% to 3% of all intracranial aneurysms in various published studies (1-8). Typically, most of PICA aneurysms originate from the PICA-VA junction. Only a small proportion of these aneurysms (<1%), which are called “Distal PICA Aneurysms”, arise from more peripheral segments of this tortuous artery (1, 8). Understanding the complex anatomy of this artery is absolutely critical to choosing the best surgical approach.
AC C
EP
PICA has a very complex and variable course. In 80–95% of cases, it arises from the intracranial portion of the VA (V4), about 8.6 mm above the foramen magnum and approximately 1 cm proximal to the vertebrobasilar junction (5). Based on its anatomical relationship to the medulla oblongata and the cerebellum, PICA can be divided into five anatomical segments and two loops. Thus, the aneurysms of PICA are defined based on their origin from each of these segments: 1) Anterior medullary, from the origin of the PICA to the inferior olivary prominence; 2) Lateral medullary, starting from lateral medulla, extending to the origins of the lower cranial nerves (XI-XII); 3) Tonsillomedullary, extending to the level of the tonsillar midportion (includes the caudal loop); 4) Telovelo-tonsillar, further extension of the PICA to the cortical surface of the cerebellum (includes the cranial loop); and finally 5) cortical, extending to the cerebellar vermis and hemisphere (5). Moreover, all surgeons treating aneurysms arising from PICA should always be cognizant of the critical perforators that branch off from the first three proximal medullary segments, and supply the lower brainstem. Lister et al reported that no brain stem perforator originated from distal to the medullary segments of the PICA in a microanatomical study of 50 hemispheres (5). PICA occlusion may cause infarction of the posterior inferior cerebellum, inferior cerebellar vermis and lateral medulla. However, PICA may have many collateral connections with other cerebellar arteries or even posterior meningeal artery and the extension of this infarction or ischemia is therefore
ACCEPTED MANUSCRIPT
highly dependent on the extent of these pre-existing collaterals.
M AN U
SC
RI PT
In the peripheral segments of PICA, hemodynamic and flow-related saccular aneurysms are again the most common type of aneurysms; however, dissecting or fusiform aneurysms of PICA are also relatively more common than other cerebellar arteries. Lewis et al. reported 22 distal PICA aneurysms, of which 13 were saccular and 9 were fusiform (4). In the current study, the authors report 91 distal PICA aneurysms 57% of them were saccular and 43% were fusiform. Interestingly, the typical bifurcation aneurysms like those in the anterior circulation are rare in distal PICA and it is apparent that these saccular aneurysms are morphologically different. Most of these aneurysms are located in the second and third segments of PICA. Distal PICA aneurysms usually have a very fragile wall and have a tendency to rupture in smaller sizes compared to the anterior circulation aneurysms. Over 80% of these aneurysms present with bleeding (1-8). In most case series, including the current study, the most common size of rupture was <7 mm (1-8). The small size and location in a tortious anatomy make diagnosis of these aneurysms very difficult and they may easily be misdiagnosed in the first CTA or conventional angiography. Therefore, considering their higher risk of rebleeding, these images, especially in patients presenting with SAH in posterior fossa associated with 4th ventricular hemorrhage must be ultra-visualized. If these images are regardless still negative, a repeat angiography is highly recommended in 7-10 days.
EP
TE D
The mysterious course and variable anatomy of the PICA, raises a historical controversy in the best surgical approach to these lesions. Obviously, no standard treatment strategy has yet been agreed upon and the general belief is that treatment option should be individualized. There are many microvascular and endovascular options. If a patient has presented with a ruptured distal PICA aneurysm associated with a large posterior fossa hematoma, the decision is straightforward. However, controversy remains in cases without significant hematoma. Although sacrifying the parent artery (PICA) is unavoidable in some cases, the best treatment option would be a technique that is able to obliterate the aneurysm safely while preserving PICA, particularly its proximal brain stem perforators.
AC C
The available microvascular techniques are direct clipping, wrapping, resection, proximal occlusion or trapping with revascularization, and finally, distal occlusion. In the current study, 93% of saccular and 68% of fusiform aneurysms have been clipped. Presence of SAH around the brain stem, relationship between the PICA aneurysms, lower cranial nerves, and medulla oblongata make microsurgical dissection of these aneurysms very difficult. In selected cases, occluding the PICA distal to its medullary segments could be safely performed without any brainstem injury. For more proximal occlusion, revascularization or possible endovascular techniques are recommended.
Current endovascular techniques include: selective coiling of the aneurysm, or occlusion of the parent artery with coil, Onyx, or n-butyl cyanoacrylate (n-BCA). Endovascular treatment, although successful in most cases, may be complicated by the
ACCEPTED MANUSCRIPT
aneurysm shape, broadness of the neck, angulation of the aneurysm and PICA in respect to the vertebral artery, tortuosity of PICA to be navigated with microcatheters, vasospasm and intra-procedural rupture of aneurysm.
M AN U
SC
RI PT
After reading the article by Lehto et al. in this issue of WORLD NEUROSURGERY, it is interesting to note how the authors have successfully characterized the features of distal PICA aneurysms and described their invaluable experience in microsurgical management of 91 distal PICA aneurysms in 80 patients. Surgical clipping of these fragile aneurysms around brainstem and cranial nerves, as we described earlier, is a risky maneuver and much of the risk occurs in an attempt to preserve patency of PICA and its perforators to the brain stem. However, The authors are to be commended for achieving such a good clinical outcome. Several aspects of their outcomes deserve special mention. Total occlusion was achieved in 94% of the saccular and in 88% of the fusiform aneurysms. Even more notable in their series is their clinical outcome that 91% of patients that were operated on for a distal PICA aneurysm, and survived beyond 1 year, recovered to the former or an independent state of life. This is a commendable achievement despite malignant presentation and poor initial Hunt&Hess grades in some of these cases.
AC C
EP
TE D
Finally, regardless of successful characterization of a large number of distal PICA aneurysms, the current series is highly biased towards microsurgical treatment of PICA aneurysms. The authors primarily embolized only one aneurysm and another was embolized after failed clipping. Other aneurysms were treated by microsurgical techniques or conservatively. For those surgeons treating these aneurysms, this study does not clearly answer the question of which technique (microsurgery vs endovascular) should be used to obtain the best outcomes, especially in this era with huge advancements of endovascular techniques. The authors state that endovascular treatment is associated with rather high rates of procedural rupture as well as morbidity and mortality. This statement does not perfectly match with the reported endovascular outcome for treatment of these aneurysms especially in recently published literatures. With the current advancements in endovascular techniques, coiling or embolization of a distal PICA aneurysms using Onyx or n-BCA, especially those distal to the medullary segments, dissecting aneurysms, or aneurysms associated with AVMs can be performed safely. Treating physicians should therefore have several treatment strategies available and use these options selectively based on the angiographic and morphological characteristics of a given distal PICA aneurysm. This flexible and adaptive approach will secure the least morbidity and the best outcome for patients with these high-risk lesions. Key Words: Posterior inferior cerebellar artery, distal, subarachnoid hemorrhage, aneurysm
ACCEPTED MANUSCRIPT
References: 1- Gács G, Viñuela F, Fox AJ, Drake CG: Peripheral aneurysms of the cerebellar arteries. Review of 16 cases. J Neurosurg 58:63–68, 1983
RI PT
2- Horiuchi T, Tanaka Y, Hongo K, Nitta J, Kusano Y, Kobayashi S: Characteristics of distal posterior inferior cerebellar artery aneurysms. Neurosurgery 53:589–95, 2003. 3-Isokangas JM, Siniluoto T, Tikkakoski T, Kumpulainen T: Endovascular treatment of peripheral aneurysms of posterior inferior cerebellar artery. AJNR Am J Neuroradiol 29:1783-1788, 2008 4- Lewis S. B., Change D. J, Peace D. A., Lafrentz P. J., Day A. L.: Distal posterior inferior cerebellar artery aneurysms: clinical features and management. J Neurosurg 97:756–766, 2002
SC
5- Lister JR, Rhoton AL Jr, Matsushima T, Peace DA: Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery 10: 170–199, 1982
M AN U
6-Locksley HB: Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage: Section V, Part 1—Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the Cooperative Study. J Neurosurg 25:219–239, 1966 7-Tokimura H, Yamahata H, Kamezawa T, Tajitsu K, Nagayama T, Sugata S, Takiguchi K, Taniguchi A, Niiro M, Hirahara K, Takasaki K, Oyoshi T, Arita K: Clinical presentation and treatment of distal posterior inferior cerebellar artery aneurysms. Neurosurg Rev 34:57–67, 2011.
AC C
EP
TE D
8-Wiebers DO, Whisnant JP, Huston J, Meissner I, Brown RD, Piepgras DG, Forbes GS, Thielen K, Nichols D, O'Fallon WM, Peacock J, Jaeger L, Kassell NF, Kongable-Beckman GL, Torner JC; International Study of Unruptured Intracranial Aneurysms Investigators. International Study of Unruptured intracranial Aneurysms (ISUIA): natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103–110, 2003.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT