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Ann Thorac Surg 2001;71:1900-1904
© 2001 The Society of Thoracic Surgeons


Original article: cardiovascular

Closed chest hypothermic circulatory arrest for complex intracranial aneurysms

Malek G. Massad, MDa, Fady T. Charbel, MDb, Rabih Chaer, MDa, Alexander S. Geha, MDa, James I. Ausman, MD, PhDb

a Division of Cardiothoracic Surgery, Department of Surgery, The University of Illinois at Chicago, Chicago, Illinois, USA
b Department of Neurosurgery, The University of Illinois at Chicago, Chicago, Illinois, USA

Accepted for publication March 2, 2001.

Address reprint requests to Dr Massad, Division of Cardiothoracic Surgery (MC 958), University of Illinois at Chicago, 840 S Wood St, Suite 417, Chicago, IL 60612
e-mail: mmassad{at}uic.edu


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Recent advances in techniques of cardiopulmonary bypass permitted hypothermic circulatory arrest (HCA) using groin cannulation with the chest closed (CC-HCA) and without direct access to the heart. Herein we describe our experience with this technique for complex intracranial aneurysms.

Methods. Between 1992 and 1999, 16 patients (4 men and 12 women) with a mean age of 52 years (range 32 to 61 years) with complex intracranial aneurysms underwent resection or clipping of their aneurysms at our institution using the technique of CC-HCA and groin cannulation. Groin access was obtained with 16F to 19F arterial and 18F to 20F venous cannulas placing the tips at the aortoiliac and atriocaval junctions, respectively. Patients were cooled to a nasopharyngeal temperature of 16°C.

Results. Mean circulatory arrest time was 32 minutes. No patient required conversion to standard sternotomy and central cannulation. There were no intraoperative deaths. The 30-day hospital mortality was 2 of 16 patients (12%). Of the 14 surviving patients (88%), 1 developed bilateral third nerve palsy and another left hemiparesis that improved on follow-up. Both were discharged to an extended care facility and continued to do well at home after discharge. Two patients developed deep venous thrombosis postoperatively and required anticoagulation. All patients continued to do well at a mean follow-up of 42 months.

Conclusions. The less invasive technique of CC-HCA through groin cannulation avoids complications associated with a sternotomy, is safe and is associated with little morbidity, reduced operative time, and early hospital discharge and rehabilitation.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The technique of hypothermic circulatory arrest (HCA) has been described and successfully used for approach of congenital heart abnormalities and for aortic arch operation. In 1960, Woodhall and colleagues [1] described its use to approach giant and complex cerebral aneurysms that would otherwise be considered inoperable by the standard methods. Recent advances in techniques of cardiopulmonary bypass have allowed HCA to be performed using groin cannulation with the chest closed (CC-HCA) and without direct access to the heart. Herein we describe our institutional experience with the technique of CC-HCA to approach complex intracranial aneurysms.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Between 1992 and 1999, 16 patients with complex intracranial aneurysms that would otherwise be considered inoperable by standard methods underwent resection or clipping of their aneurysms at our institution using the techniques of CC-HCA and groin cannulation. After reviewing the preoperative radiographic studies with 2 experienced neurosurgeons (J.I.A., F.T.C.), it was determined that these aneurysms were complex and that extracorporeal circulation, profound hypothermia, and circulatory arrest were appropriate. The term complex intracranial aneurysm referred to aneurysms in the anterior or posterior circulation that because of their size, location, and distinctive anatomic characteristics were deemed difficult to manage with the standard surgical methods available. These included situations in which exposure of the neck of the aneurysm or the inflow and outflow channels using the standard methods was deemed not possible. They also included patients who presented after rupture of their aneurysms and also patients who failed one or more attempts at endovascular coiling or direct clipping of their aneurysms without the need for HCA.

Preoperative workup for this group of patients, beside their neuroimaging, included complete blood count, coagulation profile (prothrombin and partial thromboplastin times), blood chemistry including liver enzymes and renal indices (blood urea nitrogen and creatinine), an electrocardiogram, a plain chest radiogram, and a resting surface echocardiogram to evaluate for aortic insufficiency. In patients older than 40 years with a strong family history of coronary artery disease, a stress (dobutamine) echocardiogram was performed to evaluate for left ventricular regional wall motion abnormalities; if these abnormalities were present, coronary angiography was performed. In older patients or in those with known peripheral vascular disease, a spiral computed tomography (CT) scan could often be helpful to assess iliac and femoral arterial disease. Patients were excluded from having this technique in the presence of significant aortic insufficiency on routine preoperative surface echocardiography. They were also excluded if they had coronary artery disease by angiography, pulmonary disease, hepatic or renal insufficiency, or coagulation disorders.

The technique of HCA has been described previously [24]. Anesthesia was induced with thiopental, fentanyl, and vecuronium; isoflurane was added. After induction of anesthesia, thiopental sodium (250 mg intravenously [IV]) was given as bolus and an IV infusion of 0.2 mg · kg-1 · min-1 was maintained for cerebral protection until the end of the procedure. The head, chest, and groin were scrubbed and draped. The intracranial aneurysm was initially exposed and dissected to the point at which clipping or decompression was required. Groin access was obtained through a groin incision. The patient was then heparinized (300 to 400 units/kg IV) to maintain an activated clotting time above 400 seconds. After obtaining proximal and distal control of the common femoral artery and vein, transverse incisions were made in the two vessels through which 16F to 18F arterial and 18F to 20F venous cannulas (Baxter Research Medical Inc, Midvale, UT) were introduced over guidewires. The tips of the arterial and venous cannulas were placed at the aortoiliac and atriocaval junctions, respectively. Temperatures were monitored by placing temperature probes in two or more of the following sites: brain, nasopharynx, tympanum, urinary bladder, and rectum, in addition to measurement of the blood temperature in all patients through the Swan-Ganz catheter. Patients were placed on a thermal mattress to facilitate cooling. The following variables were also measured on-line throughout the procedure: systemic and pulmonary arterial pressures, central venous pressure, cardiac output, and mixed venous oxygen saturation. In all patients, a transesophageal echocardiogram (TEE) probe was placed after induction of anesthesia to monitor ventricular filling and distension during cardiopulmonary bypass.

After the neurosurgical team exposed and dissected the intracranial aneurysm to the point at which clipping or decompression is required, the patients were placed on a cardiopulmonary bypass circuit with a membrane oxygenator and with a heat exchanger in the venous line. The patients were cooled with flow rates initiated at 50 to 60 mL · kg-1 · min-1 (2.2 to 2.5 L · m-2 · min-1) until the nasopharyngeal temperature approached 20°C, after which the rates were dropped to 40 mL · kg-1 · min-1 (1.8 L · m-2 · min-1). Cardiac fibrillation was achieved spontaneously as the body temperature neared 28° to 24°C. As the body temperature approached 22° to 18°C, the heart became asystolic. Cooling was then continued until a nasopharyngeal temperature of 16°C was reached. In 9 patients, the cardiopulmonary bypass circuit was stopped completely and in the remaining 7 patients it was allowed to trickle flow at a rate of 400 to 500 mL/min to maintain positive pressure in the circulatory system and to minimize the chance of air embolization. The mean arterial pressure during bypass was maintained between 40 to 80 mm Hg with the use of vasopressors.

After attaining a nasopharyngeal temperature of 16°C, the patients were exsanguinated by draining 30% of the blood volume into the venous reservoir to facilitate exposure. That allowed the aneurysm to collapse and enabled the neurosurgical team to dissect it out and clip its neck without fear of rupture and, when necessary, open the aneurysm to remove clot and debris. The dissection and clipping were done as quickly and expeditiously as possible, as a safe limit of 45 minutes for circulatory arrest should be respected. After completion of the neurosurgical procedure, the patient was placed back on cardiopulmonary bypass and the exanguinated blood volume was gradually returned into the body. The patient was then rewarmed gradually on cardiopulmonary bypass starting with flow rates of 40 mL · kg-1 · min-1 (1.8 L · m-2 · min-1) at temperatures between 16° and 20°C and then increasing the flow to 50 to 60 mL · kg-1 · min-1 (2.2 to 2.5 L · m-2 · min-1) until reaching a temperature of 37°C. The heart defibrillated spontaneously in 7 patients and was defibrillated transcutaneously in 9. The cardiac chambers were monitored by TEE for any evidence of distention during this period. Protamine sulfate was given before femoral decannulation to reverse the heparin dose administered before bypass. The transverse femoral arterial and venous incisions were repaired with interrupted 6-0 Prolene (Ethicon, Somerville, NJ) after decannulation.

The clinical variables analyzed included patient demographics and presenting symptoms, size, and location of the aneurysm. Intraoperative factors that were analyzed included duration of cardiopulmonary bypass and circulatory arrest, blood and body temperatures, and need for blood and blood product transfusions. Postoperative factors analyzed included surgical morbidity, postoperative bleeding, deep venous thrombosis, and neurologic outcome. Neurologic outcome scores were evaluated using Glasgow outcome scale (GOS) scores that were assigned to the patient on postoperative follow-up. Patients who died during or after the procedure were assigned a score of 5 if their death was related to the lesion. Outcomes were condensed to excellent/good (GOS scores of 1 and 2) and fair/poor (GOS scores of 3 and 4).


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The age, sex, location of the aneurysm, and clinical presentation of the patients are listed in Table 1. The patient population consisted of 4 men and 12 women with a mean age of 52 years (range 33 to 61 years). The intracranial aneurysms were equally distributed in number between the anterior and the posterior circulation (8 patients each). Their size ranged from 1 to 3.5 cm. All eight anterior circulation aneurysms were deemed nonamenable to management with standard techniques because of their size and complex nature (as defined earlier). Six of these aneurysms were large (larger than 1 cm) and two were giant (larger than 2.5 cm). Five arose from the middle cerebral artery, one from the internal carotid artery, one at the junction of the right ophthalmic and internal carotid arteries, and one from the posterior communicating artery. All eight posterior circulation aneurysms were deemed complex and nonamenable to management with the standard methods because of their location, size (five were large), or their distinctive anatomic properties. Six arose from the basilar artery, one from the vertebral artery, and one from the right superior cerebellar artery. Two patients with anterior and posterior circulation aneurysms (one each) presented after their aneurysms had ruptured. In the other 14 (88%), the aneurysm was intact on presentation. In 3 patients, all with aneurysms arising from the posterior circulation, a previous attempt was made at surgical clipping of their aneurysms without HCA. Accompanied illnesses were present in 4 patients, all women over the age of 50 years, of whom 3 patients (19%) had uncontrolled or partially controlled systemic hypertension (Table 1).


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Table 1. Clinical Characteristics of Patients With Complex Cerebral Aneurysms Who Underwent CC-HCA Between 1992 and 1999

 
Table 2 shows the mean duration of cardiopulmonary bypass, the cooling time required to reach the desired nasopharyngeal temperature (16°C), and circulatory arrest. The mean cerebral cooling and rewarming rates were 0.60°C/min and 0.46°C/min, respectively. There was no significant difference in the rate of warming between the 9 patients who had full circulatory arrest compared with the remaining 7 patients who had trickle flow (400 to 500 mL/min) at 16°C. Variations up to 10°C were noted between the nasopharyngeal and the urinary bladder temperature readings during the early period of rewarming. No patient had evidence of cerebral air embolization on postoperative CT scan. The multiorgan response to the hypothermic low flow state and to reperfusion was favorable as no significant changes were noted postoperatively in renal and hepatic functions, the coagulation system, or in serum amylase and lipase levels.


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Table 2. Mean Cardiopulmonary Bypass, Cooling, Circulatory Arrest, and Rewarming Time in the 16 Patients Who Underwent CC-HCA Between 1992 and 1999

 
No cardiac complications were observed during the procedure. Ventricular distension, reflected by TEE monitoring and pulmonary arterial pressures, was not seen in any of the patients during bypass. No patient required conversion to standard sternotomy and central cannulation. The need for blood and blood products were limited to 2 patients who received two units of packed red blood cell transfusions each at the conclusion of cardiopulmonary bypass and to 1 patient who received 10 U of platelets after bypass for bleeding encountered during manipulation of a complex posterior communicating artery aneurysm. One patient underwent reexploration of the aneurysm site because of bleeding and had an uneventful neurologic recovery. There were no intraoperative deaths and no postoperative deaths related to the technique of HCA. No groin wound infections occurred. The 30-day hospital mortality was 2 of 16 patients (12%) and was influenced by the patient’s primary neurologic condition rather than the technique of HCA. One patient developed intracerebral bleeding and edema in the immediate postoperative period and later died. The second patient developed middle cerebral artery thrombosis postoperatively that was treated with urokinase infusion to dissolve the clot. That treatment was complicated by intracerebral hemorrhage and resulted in death. Of the 14 surviving patients (88%), 1 developed bilateral third nerve palsy and another developed left hemiparesis that improved on follow-up. Both were discharged to an extended care facility for rehabilitation and physical therapy and continued to do well at home after their discharge. Two other patients developed deep venous thrombosis postoperatively and required anticoagulation. The mean postoperative hospital stay was 18 days (median 14 days). All discharged patients continued to do well as of a mean follow-up of 42 months (range 10 months to 7.5 years). Table 3 shows the GOS of the 16 operated patients. Twelve of the 14 surviving patients had excellent/good outcome with GOS of 1 to 2. The remaining 2 had a fair outcome (GOS of 3).


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Table 3. Glasgow Outcome Score (GOS) by Location and Nature of Aneurysm Among 16 Patients With Complex and Giant Intracranial Aneurysms Who Underwent CC-HCA Between 1992 and 1999

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Untreated giant and complex cerebral aneurysms are associated with a high mortality, particularly those involving posterior circulation. Peerless and colleagues [5] reported 2- and 5-year mortality rates of 68% and 85%, respectively, with severe neurologic deficits occurring among the survivors. Tsutumi and colleagues [6] followed-up 62 patients with untreated saccular aneurysms over a 12-year period. In those with large aneurysms (more than 1 cm), the 5- and 10-year cumulative risks of subarachnoid hemorrhage calculated by the Kaplan–Meier method were 33.5% and 55.9%, respectively [6]. Standard techniques that have been used for management of these aneurysms include percutaneous endovascular deployment of detachable coils to obliterate the lumen of the aneurysm, surgical bypass or trapping, and direct surgical clipping of the neck of the aneurysm with or without suction decompression of the aneurysm proper. In patients who are deemed unsuitable for management by the standard methods or who fail management by these techniques, it is intuitive to conceive that aggressive surgical intervention using the technique of CC-HCA may provide improved survival and less neurologic dysfunction compared with those seen with the natural history of the disease.

The few patients in this early experience with the closed-chest technique limits us from making any valid statistical analysis. However, it is clear from this experience and that of others with the open and closed chest techniques for HCA [710] that the patient’s primary neurologic condition did influence the overall outcome. From this early experience, we have observed that extensive intraoperative monitoring during CC-HCA adds to the safety of the operative technique and leads to improved outcome. The depth of hypothermia, the duration of circulatory arrest, barbiturate (thiopental) use for cerebral protection, and hemostasis are key elements in achieving a good outcome. Although extensive intraoperative monitoring was properly achieved, most of the data collected from this initial clinical experience were obtained retrospectively from reviewing the patient’s medical records and the perfusionist’s and anesthesia records. Hence, charting of body temperatures obtained from all the different sites (blood, brain, tympanic, nasopharynx, and urinary bladder) was incomplete and did not permit us to perform any valid analysis when comparing the temperature recordings among all the different sites. However, it was our observation, as well as the observation of others [11], that when profound hypothermia is induced rapidly and reversed as with the technique of HCA, the temperature measurements made at standard monitoring sites (urinary bladder, rectum) may not reflect the actual body and brain temperatures. Differences as high as 10°C were noticed between the nasopharyngeal and the urinary bladder temperatures, particularly during the period of early rewarming, probably due to uneven distribution of blood flow and also to uneven cooling [11, 12]. It was also our observation that the tympanic and nasopharyngeal temperatures correlated closely with the brain temperature during the periods of cooling and rewarming.

Retrograde dissection of the aorta because of femoral cannulation has been previously described [13]. Rajasinghe and coworkers [13] reported this complication in 2 of 55 patients (3.6%) who underwent groin cannulation for deep HCA. In our experience, we have not encountered this complication since we adopted the technique of arterial and venous cannulation over a guidewire introduced through a transverse incision made in the common femoral artery and vein. That technique ensures the location of the cannulas within the lumen and minimizes the chance of retrograde dissection or perforation of the vessel wall.

Deep venous thrombosis or pulmonary emboli were encountered in as many as 29% of the patients reported by Baumgartner and coworkers [8]. Although no patient in our series had pulmonary embolization, 2 developed deep venous thrombosis postoperatively. Several factors may have contributed to the occurrence of deep venous thrombosis in the 2 patients. These patients had a short interval of venous stasis in the lower extremities during the period of trickle flow or circulatory arrest, despite being given anticoagulant agents during that interval. Besides, cannulation of the common femoral and iliac veins for venous drainage may have predisposed them to thrombosis. Furthermore, the patients were confined to bed postoperatively because of their neurologic condition. To minimize these risks, we have adopted the technique of open groin exposure for cannulation of the femoral vessels. Cannulation is usually performed high through the common femoral vessels. Meticulous care is also taken at the end of the procedure to repair the femoral vessels after decannulation. Pneumatic compression stockings are used routinely during the procedure and the early postoperative period. Additionally, our neurosurgical team has adopted the policy of performing routine weekly screening of the lower extremities by venous duplex sonography in all patients who would require prolonged confinement. The team has also adopted the routine administration of subcutaneous heparin prophylaxis during the perioperative period. These measures may lessen the incidence of postoperative deep venous thrombosis.

Selected patients with complex or giant intracranial aneurysms that are deemed unapproachable by conventional surgical techniques can be treated successfully using HCA. The less invasive technique of CC-HCA through groin cannulation avoids the complications associated with a sternotomy, is safe, and is associated with little morbidity, reduced operative time, and early hospital discharge and rehabilitation. The depth of hypothermia, duration of circulatory arrest, barbiturate use, and hemostasis are key elements to achieving a good outcome.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Woodhall B., Sealy W.C., Hall K.D., Floyd W.L. Craniotomy under conditions of quinidine-protected cardioplegia and profound hypothermia. Ann Surg 1960;152:37-44.
  2. Ausman J.I., Malik G.M., Tomecek F.J., et al. Hypothermic circulatory arrest and the management of giant and large cerebral aneurysms. Surg Neurol 1993;40:289-298.[Medline]
  3. Spetzler R.F., Hadley M.N., Rigamonti D., et al. Aneurysms of the basilar artery treated with circulatory arrest, hypothermia, and barbiturate cerebral protection. J Neurosurg 1988;68:868-879.[Medline]
  4. Aerbert H., Brawanski A., Philipp A., et al. Deep hypothermia and circulatory arrest for surgery of complex intracranial aneurysms. Eur J Cardiothorac Surg 1998;13:223-229.[Abstract/Free Full Text]
  5. Peerless S.J., Wallace M.C., Drake C.G. Giant intracranial aneurysms. In: Youmans J.R., ed. Neurological surgery: a comprehensive guide to the diagnosis and management of neurological problems. Philadelphia: WB Saunders, 1990:1742-1763.
  6. Tsutsumi K., Ueki K., Morita A., Kirino T. Risk of rupture from incidental cerebral aneurysms. J Neurosurg 2000;93:550-553.[Medline]
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  8. Baumgartner W.A., Silverberg G.D., Ream A.K., et al. Reappraisal of cardiopulmonary bypass with deep hypothermia and circulatory arrest for complex neurosurgical operations. Surgery 1983;94:242-249.[Medline]
  9. Guegan Y., Scarabin J.M., Le Guilcher C., Guillou L., Logeais Y., Pecker J. Extracorporeal circulation with deep hypothermia and circulatory arrest in the treatment of intracranial arterial aneurysms. Surg Neurol 1985;24:441-449.[Medline]
  10. Silverberg G.D., Reitz B.A., Ream A.K. Hypothermia and cardiac arrest in the treatment of giant aneurysms of the cerebral circulation and hemangioblastoma of the medulla. J Neurosurg 1981;55:337-346.[Medline]
  11. Williams M.D., Rainer W.G., Fieger H.G., Murray I.P., Sanchez M.L. Cardiopulmonary bypass, profound hypothermia, and circulatory arrest for neurosurgery. Ann Thorac Surg 1991;52:1069-1075.[Abstract]
  12. Stone J.G., Young W.I., Smith C.R., et al. Do standard monitoring sites reflect true brain temperature when profound hypothermia is rapidly induced and reversed?. Anesthesiology 1995;82:344-351.[Medline]
  13. Rajasinghe HA, Edwards NM, Slater J, Sinha P, Solomon RA, Smith CR. Use of minimally invasive deep hypothermic circulatory arrest in repair of complex intracranial aneurysms [Abstract]. The 11th Annual Update in Cardiac and General Thoracic Surgery, American College of Chest Physicians, St. Thomas, US Virgin Islands, December 1999:1–3.



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