TECHNIQUE APPLICATIONS

IN SITU BYPASS IN THE MANAGEMENT OF COMPLEX INTRACRANIAL ANEURYSMS: TECHNIQUE APPLICATION IN 13 PATIENTS
Alfredo QuionesHinojosa, M.D.
Department of Neurological Surgery, Center for Stroke and Cerebrovascular Disease, University of California, San Francisco, San Francisco, California

Michael T. Lawton, M.D.

Department of Neurological Surgery, Center for Stroke and Cerebrovascular Disease, University of California, San Francisco, San Francisco, California Reprint requests: Michael T. Lawton, M.D., Department of Neurological Surgery, University of California, San Francisco, 505 Parnassus Avenue, Moffitt Hospital, Room M779, Box 0112, San Francisco, CA 94143-0112. Email: lawtonm@neurosurg.ucsf.edu Received, December 6, 2004. Accepted, February 7, 2005.

OBJECTIVE: Cerebral revascularization is an important part of the treatment of complex intracranial aneurysms that require deliberate occlusion of a parent artery. In situ bypass brings together intracranial donor and recipient arteries that lie parallel and in close proximity to one another rather than using an extracranial donor artery. An experience with in situ bypasses was retrospectively reviewed. METHODS: Thirteen aneurysms were treated with in situ bypasses between 1997 and 2004. During this time, 1071 aneurysms were treated microsurgically and 46 bypasses were performed as part of the aneurysm treatment. RESULTS: Treated aneurysms were located at the middle cerebral artery (MCA) in five patients, posteroinferior cerebellar artery (PICA) in three patients, vertebral artery in three patients, and anterior communicating artery in two patients. Seven aneurysms were fusiform or dolichoectatic, and six aneurysms were saccular. Microsurgical revascularization techniques included side-to-side anastomosis of intracranial arteries in eight patients and aneurysm excision with end-to-end reanastomosis of the parent artery in five patients. In situ bypasses included A3A3 anterior cerebral artery bypass in two patients, anterior temporal artery-MCA bypass in one patient, MCAMCA bypass in one patient, and PICAPICA bypass in four patients. Aneurysm excision with arterial reanastomosis included three MCA aneurysms and two PICA aneurysms. On angiography, all aneurysms were completely obliterated and 12 bypasses were patent. CONCLUSION: In situ bypass is a safe and effective alternative to extracranialintracranial bypasses and high-flow bypasses using saphenous vein or radial artery grafts. Although in situ bypasses are more demanding technically, they do not require harvesting a donor artery, can be accomplished with one anastomosis, and are less vulnerable to injury or occlusion.
KEY WORDS: Intracranial aneurysm, Microsurgery, Revascularization, Subarachnoid hemorrhage
Neurosurgery 57[ONS Suppl 1]:ONS-140ONS-145, 2005
DOI: 10.1227/01.NEU.0000163599.78896.F4

ost intracranial aneurysms can be managed with microsurgical clipping or endovascular coiling, but a subset of aneurysms with complex anatomy or fusiform/ dolichoectatic morphology may require an alternative approach using revascularization. Despite disappointing results from national trials examining the therapeutic efficacy of extracranial-tointracranial (ECIC) bypass surgery for ischemic stroke, this technique remains a critical part of the neurosurgeons armamentarium for treating complex and giant intracranial aneurysms, particularly when the treatment involves the deliberate sacrifice or occlusion of a parent artery that supplies the aneurysm (4, 8, 10). ECIC bypass surgery typically involves the anastomosis of the superficial temporal artery (STA) or occipital artery (OA) (9) to an intracranial recip-

ient artery but may also use saphenous vein or radial artery grafts connected to donor arteries more proximally (i.e., to the internal, external, or common carotid artery), which delivers increased blood flow. These two types of bypasses constitute the majority of procedures used in the management of complex intracranial aneurysms, but an important and elegant third type is the in situ or intracranialto-intracranial (ICIC) bypass. In situ bypass requires that donor and recipient arteries lie parallel and in close proximity to one another. Anatomically, there are at least four sites where this requirement is met: the anterior cerebral arteries (ACAs) as they course over the genu and rostrum of the corpus callosum (A2 and A3 segments); the middle cerebral artery (MCA) branches, including the anterior temporal artery, as they

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course through the sylvian fissure; the posterior cerebral artery (PCA) and superior cerebellar artery (SCA) as they course around the midbrain through the ambient cistern; and the posteroinferior cerebellar arteries (PICAs) as they course around the posterior medulla and tonsils in the cisterna magna. These in situ bypasses are appealing because they are entirely intracranial, are less vulnerable to injury or occlusion, do not require harvesting an extracranial artery or graft, use donor and recipient arteries with diameters that are well matched, and require just one anastomosis (1, 3, 5, 7). We reviewed our experience with in situ bypasses to evaluate their utility and to share our technical lessons learned.

PATIENTS AND METHODS

Patients with aneurysms treated at the University of California, San Francisco, by the senior author (MTL) were identified from the cerebrovascular diseases database. Between August 1997 and August 2004, 1071 aneurysms were treated microsurgically in 864 patients. Among the cohort, 46 patients underwent bypass surgery as part of the management of their aneurysm. High-flow bypasses with saphenous vein or radial artery grafts were performed in 21 patients, and low-flow ECIC bypasses with STA or OA grafts were performed in 12 patients. In situ bypasses were performed in the remaining 13 patients. Included in these in situ bypasses were aneurysms

that were excised with primary end-to-end reanastomosis of the parent artery. Medical records, neurological examinations, angiograms, operative reports, and postoperative courses for these patients were retrospectively reviewed. There were six women and seven men, with a mean age of 42.5 years (range, 1677 yr). Aneurysm rupture was the most common presentation (eight patients). The other five patients presented with headache or other neurological complaints, and unruptured aneurysms were detected during diagnostic evaluation (Table 1). During surgery, brain relaxation was achieved with mannitol and cerebrospinal fluid drainage through a ventriculostomy or through a window created in the lamina terminalis. Mild hypothermia and barbiturates titrated to achieve electroencephalographic burst suppression were used to increase tolerance to cerebral ischemia during the time when the anastomosis was performed and the parent arteries were temporarily occluded. Blood pressure was increased with pressor agents during this time if changes in somatosensory evoked potentials or the electroencephalogram were observed.

RESULTS
Aneurysms treated with in situ bypass were located at the MCA in five patients, PICA in three patients, vertebral artery

TABLE 1. Summary of in situ bypass casesa Patient no. 1 2 3 4 5 6 7 8 9 10 11 12 13 Sex/age (yr) F/78 F/48 F/16 M/19 F/40 F/23 M/36 M/44 M/52 F/51 M/77 F/47 M/30 SAH N Y N Y Y Y N N Y Y N Y Y Aneurysm location L ACA A ComA L MCA R MCA L MCA L MCA R MCA R PICA L PICA R VA R PICA L VA R VA Morphology Saccular Saccular Saccular F/D Saccularb Saccularb F/D F/D F/D F/D Saccular F/D F/D Bypass location A3A3 A3A3 ATAMCA MCA E/R MCA E/R MCAMCA MCASTAMCA PICA E/R PICA E/R PICAPICA PICAPICA PICAPICA PICAPICA Arterial occlusion Endovascular Endovascular Surgical Surgical Surgical Surgical Surgical Surgical Surgical Endovascular Endovascular None Endovascular Radiographic outcome Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Obstructed bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm Patent bypass, obliteration of aneurysm

a SAH, subarachnoid hemorrhage; N, no; L, left; ACA, anterior cerebral artery; Y, yes; A ComA, anterior communicating artery; MCA, middle cerebral artery; ATA, anterior temporal artery; F/D, fusiform/dolichoectatic; E/R, excision-reanastomosis; STA, superficial temporal artery; PICA, posteroinferior cerebellar artery; VA, vertebral artery. b Mycotic.

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in three patients, and anterior communicating artery in two patients (Table 1). Seven aneurysms were fusiform or dolichoectatic, and six aneurysms were saccular. Two aneurysms were mycotic or infectious. Microsurgical revascularization techniques included side-toside anastomosis of intracranial arteries in eight patients and aneurysm excision with end-to-end reanastomosis of the parent artery in five patients. ICIC bypasses included A3A3 ACA bypass in two patients (Fig. 1), anterior temporal artery-MCA bypass in one patient, MCAMCA bypass in one patient, and PICAPICA bypass in four patients (Fig. 2). Aneurysm excision with arterial reanastomosis included three MCA aneurysms and two PICA aneurysms (Fig. 3). Reanastomosis of one of the MCAs required an interposition graft from the STA. No additional or unexpected difficulties were encountered in the eight patients who presented with ruptured aneurysms compared with the five patients who presented with unruptured aneurysms. Seven aneurysms were surgically trapped after performing the bypass during a single surgical stage. Five aneurysms were occluded endovascularly in a second stage. By means of angiography, all aneurysms were completely obliterated and

12 bypasses were patent. The occluded bypass was the MCA STAMCA reconstruction performed after aneurysm excision because of inability to reapproximate the arterial ends without the interposition graft. No adverse ischemic complications were observed clinically or radiographically in this patient or in any of the other patients.

DISCUSSION
The requirement for in situ bypass that donor and recipient arteries lie parallel and in close proximity makes at least four bypasses possible to perform. On the basis of this clinical experience, only three were applicable to aneurysms located at the anterior communicating artery, MCA, and PICA. On the basis of the anatomy of these arteries, the PCASCA bypass is possible, but we did not need this bypass in this experience. The PCASCA bypass might have utility in the management of a basilar apex aneurysm when clipping cannot preserve flow in the ipsilateral P1 PCA, the posterior communicating artery is diminutive or occluded, and the STA is also diminutive or unavailable. In this case, a PCASCA bypass per-

FIGURE 1. Scans and intraoperative photographs showing an A3A3 bypass in Patient 1. This 78-year-old woman presented with aphasia and headaches. A, head computed tomographic scan demonstrating a giant and partially thrombosed anterior communicating artery aneurysm and obstructive hydrocephalus attributable to compression of the foramen of Monro by the aneurysm. B, left internal carotid artery angiogram (anteroposterior view) revealing a superiorly projecting aneurysm without a clippable neck. The left A1 and A2 ACA segments were separated by the base of the aneurysm, indicating fusiform/dolichoectatic morphology. A multimodality strategy was planned, with a bypass to the distal ACA as the first stage and endovascular coil occlusion of the aneurysm and left A1 ACA as the second stage. She underwent a bifrontal craniotomy via an

interhemispheric approach and A3A3 ACA side-to-side anastomosis to revascularize the ACA territory distal to the aneurysm. The back walls of the anastomosis were sutured from within the arterial lumen first (C); then, the front walls were sutured (D). E, depth of this surgical corridor is shown. F, postoperative left carotid artery angiography demonstrating a patent bypass with good distal flow in bilateral ACA territories. G and H, patient then underwent coil occlusion of the aneurysm and the proximal left A1 ACA, with right carotid artery angiography demonstrating obliteration of the aneurysm and blood flow in bilateral ACA territories originating from the right A2 ACA and crossing to the left hemisphere through the bypass. The anastomosis site is indicated by the large black arrow in H.

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FIGURE 2. Scans and intraoperative photographs showing a PICA PICA bypass in Patient 13. A 30-year-old man presented with subarachnoid hemorrhage (A) and a right vertebral artery dissecting aneurysm (B). The patient was taken to the operating room for a suboccipital craniotomy, where the PICAs were brought together between the tonsils (C) with a side-to-side anastomosis to allow the contralateral PICA to supply the ipsilateral PICA in a retrograde fashion (D). E, arteries maintained

good flow after the release of the temporary clips. F, aneurysm could be appreciated through the craniotomy. G, on postoperative Day 2, the patient underwent a postoperative angiogram revealing the bypass to be fully patent (site of the anastomosis illustrated by arrow). H, endovascular occlusion of the vertebral artery with coils was performed, and the final angiogram revealed a fully patent bypass and obliteration of the aneurysm.

formed before clipping the aneurysm might enable the patient to tolerate an occlusion of the P1 PCA after aneurysm clipping. In addition to these ICIC bypasses, aneurysm excision with arterial reanastomosis is another variant of in situ bypass that can be performed with aneurysms at any location, provided that there is enough redundancy in the arterial ends to reapproximate them without tension. Excision-reanastomosis is particularly applicable to infectious and fusiform aneurysms that are small in size and often distally located (2). In situ bypasses are appealing because they eliminate the need to harvest a donor artery extracranially, saving the neurosurgeon time and effort and also sparing the patient a second or third incision when saphenous vein or radial artery grafts are used. Bypasses that use the STA or OA as a donor artery do not spare the patient an additional incision, but these arteries can sometimes be so diminutive in caliber that the adequacy of the bypass can be uncertain. In other cases, particularly after prior surgery or trauma, these arteries may be occluded and unavailable. In situ bypass has conceptual advantages as well, with no length to the bypass and therefore a reduced risk of delayed occlusion. Its intracranial location protects it from exogenous occlusion or injury. With ACA bypass, the STA is not long enough to reach the A3 segment, necessitating more complex ECIC bypasses like the bonnet bypass, with a long saphenous vein graft from the

cervical carotid artery or STA (11). In these cases, the A3A3 ACA bypass is more elegant and less invasive. All in situ bypasses in this experience were part of a planned surgical strategy that reflected the availability and size of extracranial donor arteries, aneurysm location, and neurosurgeon preferences. A small or previously occluded STA necessitates an alternative approach for MCA aneurysms and increases the appeal of in situ bypasses. The deep midline location of ACA aneurysms renders the STA insufficient. The OA is more cumbersome to dissect and seems to be more prone to postoperative occlusion than the STA. Consequently, with PICA aneurysms, surgeon preference for using the adjacent PICA over the OA accounted for the PICAPICA bypass being the most common one in this patient series. In situ bypass requires temporary occlusion of two major intracranial arteries to perform the side-to-side anastomosis instead of just temporarily occluding one recipient artery with a traditional ECIC bypass. Furthermore, any complication with the anastomosis that compromises the flow or patency of the donor and recipient arteries is potentially more dangerous because of the extra artery involved. However, this concern did not materialize in this clinical experience. There were no occlusions in the side-to-side anastomoses. We attributed this to a long arteriotomy, with a length that is typically three times the diam-

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FIGURE 3. Scans and intraoperative photographs showing a PICA aneurysm excision and arterial reanastomosis in Patient 8, a 44-year-old man. A, patient presented with a giant thrombotic right PICA aneurysm (with symptoms related to mass effect on his medulla) and a left PICA aneurysm. The patient underwent a right far lateral craniotomy; for trapping/debulking of the giant thrombotic right PICA aneurysm, reanastomosis of the right PICA (B and C), and clip reconstruction of the left PICA aneurysm (D and E) (arrow in C illustrates the temporary clip application). F and G, postoperative angiogram demonstrating excellent obliteration of the aneurysm, and a patent bypass as shown by arrows.

eter of the arteries. The one occlusion that did occur (Patient 7) was attributed to an interposition graft in an end-to-end reanastomosis, emphasizing the diminished patency rate associated with two serial anastomoses and the need to mobilize the arterial ends aggressively to avoid the need for an interposition graft. If this one atypical case is excluded, the overall patency rate with in situ bypasses compares favorably with that of conventional ECIC bypasses using STA donor artery or saphenous vein grafts. In the senior authors revascularization experience with 101 bypass procedures for aneurysms, ischemic diseases, and cranial base tumors, the patency rate for STA bypasses was 98.4% (61 of 62 bypasses) and that for saphenous vein bypasses was 92.3% (24 of 26 bypasses). Mobilization of donor and recipient arteries is equally important with the side-to-side anastomosis. These arteries should be touching, or nearly touching, before sutures are placed. If sutures are required to pull the arteries together, there is a risk of the sutures breaking or tearing through the arterial wall as they are tightened and a risk of kinking the afferent and/or efferent arteries, which can compromise their blood flow. Arteries that approximate without tension on the sutures remain in a parallel course that optimizes the flow through the bypass. The side-to-side anastomosis is not as familiar to neurosurgeons as the end-to-end anastomosis. It requires suturing the back wall of the anastomosis from inside the lumen (Fig. 1). The first bite after approximating the two arteries passes the needle from outside the lumen to inside the lumen. The next sutures are then placed in a continuous fashion to the opposite end of the arteriotomies, where the needle is again passed from inside the lumen to outside the lumen. These two reversing passes must be

remembered. Once these sutures are loosely placed along the entire line, they are tightened and tied to a second suture at the other end of the arteriotomy. The front wall of the anastomosis is performed with a simple continuous suture from outside the lumen. This anastomosis is often performed in a deep surgical corridor, making it essential to position a continuous suction drain at the depths of the field to keep it clear of blood. Half of the patients in this series were managed with a multidisciplinary approach combining microsurgical and endovascular techniques. The advantages of this strategy include minimizing the invasiveness of surgery, sometimes eliminating a second craniotomy, and delaying the aneurysm occlusion until the patients hemodynamics and general medical condition have been optimized (6). In summary, the ability to revascularize an intracranial artery creates options in aneurysm management beyond direct clipping or coiling, allowing deliberate arterial occlusion without the risk of ischemic stroke and neurological morbidity that would have occurred without a bypass. These strategies should be considered in the management of complex aneurysms, and these techniques should be part of the armamentarium of vascular neurosurgeons.

REFERENCES
1. Bederson JB, Spetzler RF: Anastomosis of the anterior temporal artery to a secondary trunk of the middle cerebral artery for treatment of a giant M1 segment aneurysm: Case report. J Neurosurg 76:863866, 1992. 2. Chun JY, Smith W, Halbach VV, Higashida RT, Wilson CB, Lawton MT: Current multimodality management of infectious intracranial aneurysms. Neurosurgery 48:12031214, 2001.

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3. Evans JJ, Sekhar LN, Rak R, Stimac D: Bypass grafting and revascularization in the management of posterior circulation aneurysms. Neurosurgery 55:10361049, 2004. 4. Hopkins LN, Budny JL, Spetzler RF: Revascularization of the rostral brain stem. Neurosurgery 10:364369, 1982. 5. Lawton MT, Hamilton MG, Morcos JJ, Spetzler RF: Revascularization and aneurysm surgery: Current techniques, indications, and outcome. Neurosurgery 38:8394, 1996. 6. Lawton MT, Quiones-Hinojosa A, Sanai N, Malek JY, Dowd CF: Combined microsurgical and endovascular management of complex intracranial aneurysms. Neurosurgery 52:263275, 2003. 7. Lemole GM Jr, Henn J, Javedan S, Deshmukh V, Spetzler RF: Cerebral revascularization performed using posterior inferior cerebellar arteryposterior inferior cerebellar artery bypass: Report of four cases and literature review. J Neurosurg 97:219223, 2002. 8. Newell DW, Skirboll SL: Revascularization and bypass procedures for cerebral aneurysms. Neurosurg Clin N Am 9:697711, 1998. 9. Roski RA, Spetzler RF, Hopkins LN: Occipital artery to posterior inferior cerebellar artery bypass for vertebrobasilar ischemia. Neurosurgery 10:4449, 1982. 10. Spetzler RF, Carter LP: Revascularization and aneurysm surgery: Current status. Neurosurgery 16:111116, 1985. 11. Spetzler RF, Roski RA, Rhodes RS, Modic MT: The bonnet bypass: Case report. J Neurosurg 53:707709, 1980.

unavailable or when the need for bypass arises unexpectedly during surgery, this strategy for revascularization provides a useful and elegant option. Sepideh Amin-Hanjani Robert F. Spetzler Phoenix, Arizona

Acknowledgment
Neither of the authors of this study has any financial interest in any of the instruments or methodologies used in this study.

uiones-Hinojosa and Lawton describe their experience using in situ bypasses for the management of complex intracranial aneurysms in 13 patients. This technique is essential and needs to be mastered by any microvascular surgeon who is currently treating complex intracranial aneurysms. There is no question that deconstructive procedures associated with bypass procedures are becoming more essential in the treatment of giant and complex intracranial aneurysms. Endosaccular occlusion certainly has a role; however, many aneurysms that cannot be treated by using endosaccular techniques also are unable to be treated by using standard microsurgical techniques and, therefore, require much more refined and sophisticated procedures. As the authors have alluded, the in situ bypass is an extremely attractive option, particularly for middle cerebral artery, anterior cerebral artery and PICA-to-PICA bypasses. The authors are to be congratulated on an impressive series. There is no question that this particular information should be kept in the file of every active operating microvascular surgeon. Robert H. Rosenwasser Philadelphia, Pennsylvania

COMMENTS
n this article, Quiones-Hinojosa and Lawton present a series of patients to illustrate the value of local or in situ anastasmosis in the management of intracranial aneurysms that cannot be coiled or clipped without revascularization. Based on my experience with cerebral revascularization in 73 patients with aneurysms and 10 in situ bypasses, I concur with the authors recommendations. In some patients, the flow provided by this type of anastamosis may be inadequate for the need; for instance, in basilar artery occlusion. In some patients, an extracranial to intracranial bypass may allow the aneurysm treatment to be provided in the same stage as the bypass operation. For instance, in the authors case 11, a posteroinferior cerebellar artery (PICA) aneurysm, a PICA-PICA anastamosis was performed, followed by endovascular obliteration in a second stage. An occipital to PICA anastamosis, followed by aneurysm clipping, could have been performed in a single operation, avoiding the need for a second procedure. This series and others demonstrate the need for either close collaboration or a single surgeon when performing endovascular and microsurgical aneurysm bypass procedures. Laligam N. Sekhar Seattle, Washington n this article, the authors nicely illustrate the strategy of intracranialintracranial bypass for distal revascularization in the treatment of complex intracranial aneurysms. Based on cardiac bypass experience, the long-term patency rates of in situ vessels may well be higher. However, with both donor and recipient territories at risk in the event of even rare bypass occlusion or extended cross-clamping, we would not consider intracranial-intracranial bypass as the first line of treatment. When suitable extracranial vessels or interposition grafts are

he number of intracranial aneurysms treated by using endovascular coil embolization has been growing very quickly in the past few years. Nowadays, in some neurosurgical centers, most small and simple aneurysms are being treated by using the endovascular approach. The fast and great development of new technologies of endovascular materials will probably permit the use of the endovascular route to treat most intracranial aneurysms in the coming years. Thus, in the near future, it is likely that open surgery will deal only with giant and complex aneurysms that cannot be treated by using the endovascular route and with cases for which endovascular treatment results in complications. Young neurosurgeons who want to work with vascular neurosurgery must learn interventionist neuroradiology and the techniques of cerebral revascularization. The authors have done a very good job with the technique of in situ bypass for aneurysm surgery. I fully agree with them: the in situ bypass is an excellent alternative to revascularize the brain when dealing with complex aneurysms. Another important remark is the multidisciplinary management of half of the cases. As stressed by the authors, this strategy minimizes the invasiveness of the surgery and delays the aneurysm occlusion until the patients hemodynamics and general conditions have optimized. They present an important series of cases with very good results. The only postoperative thrombosis was in the end-to-end reanastomosis of the middle cerebral artery with interposition of a graft. In my personal experience of in situ bypass, I had a similar case in which I interposed a saphenous vein graft that occluded in the postoperative period. Atos Alves de Sousa Belo Horizonte, Brazil