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Year : 2018  |  Volume : 13  |  Issue : 3  |  Page : 539-545

Adenosine-induced flow arrest to facilitate intracranial complex aneurysm clip ligation: Review of the literature

1 Department of Neurosurgery, Banbuntane Hotokukai Hospital, Fujita Health University, Nagoya, Japan; Department of Neurosurgery, Heji Hospital, Changzhi Medical College, ChangZhi City, Shan Xi Province, China
2 Department of Neurosurgery, Banbuntane Hotokukai Hospital, Fujita Health University, Nagoya, Japan

Date of Web Publication31-Jul-2018

Correspondence Address:
Yoko Kato
3-6-10 Otobashi Nakagawa-ku, Nagoya, Aichi 454-8509
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ajns.AJNS_207_16

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Complex intracranial aneurysms (CIAs) rank high among the most technically demanding neurosurgical pathologies. Microsurgery and clip ligation can be challenging in CIAs as circumferential visualization of the aneurysm, parent vessels, branches, perforators, and other neurovascular structures is important to prevent residual aneurysms or strokes from vessel or perforator occlusion. Decompression of the aneurysm sac is often required for CIAs. We reviewed the literature and PubMed advanced search showed 13 results of adenosine-induced flow arrest to facilitate intracranial complex aneurysm clip ligation which included three independent case reports and ten cases in a case series from 1999 to May 2016. Few case series have described the use of adenosine in intracranial aneurysm surgery. Satisfactory aneurysm decompression was achieved in all cases, and all aneurysms were clipped successfully. We recommend that adenosine cardiac arrest is a relatively novel method for decompression of intracranial aneurysms to facilitate clip application. With appropriate safety precautions, it is a reasonable alternative method when temporary clipping of proximal vessels is not desirable or not possible.

Keywords: Adenosine-induced flow arrest, clip ligation, complex intracranial aneurysms

How to cite this article:
Wang X, Feletti A, Tanaka R, Yamada Y, Suyama D, Kawase T, Kato Y. Adenosine-induced flow arrest to facilitate intracranial complex aneurysm clip ligation: Review of the literature. Asian J Neurosurg 2018;13:539-45

How to cite this URL:
Wang X, Feletti A, Tanaka R, Yamada Y, Suyama D, Kawase T, Kato Y. Adenosine-induced flow arrest to facilitate intracranial complex aneurysm clip ligation: Review of the literature. Asian J Neurosurg [serial online] 2018 [cited 2020 Aug 6];13:539-45. Available from:

  Introduction Top

Complex intracranial aneurysms (CIAs) include not only giant aneurysms (classically larger than 25 mm in diameter) but also smaller aneurysms in difficult locations of the human brain and cranial base.[1] Such lesions are associated with a high risk of subarachnoid hemorrhage and progressive neurological deterioration or death caused by mass effect or stroke. Despite the fact that intracranial aneurysm treatment has evolved over the last 10 years and despite advances in endovascular techniques, microsurgical clipping remains an important treatment option for those patients who are not ideal candidates for endovascular therapy. This is particularly true for wide-necked, blister-like, large and giant, and complex cerebral aneurysms. Microsurgery and clip ligation can be challenging in CIAs as circumferential visualization of the aneurysm, parent vessels, branches, perforators, and other neurovascular structures is important to prevent residual aneurysms or strokes from vessel or perforator occlusion. Adenosine-induced flow arrest briefly reduces cerebral perfusion pressure and reduces the turgor of the aneurysm, thereby facilitating the clip ligation. Periods of flow arrest have to be carefully coordinated with the surgeon such that necessary working time is available for aneurysm dissection and clip placement. Adenosine-induced transient asystole is an alternative method of flow arrest.

We reviewed the literature and Pubmed advanced search showed 231 cases of intracranial aneurysms which used adenosine-induced flow arrest during microsurgery and clip ligation from 1999 to May of 2016 (Bebawy et al. have 3 published papers, there are some repeated cases in these 3 papers).

  Adenosine-Induced Transient Asystole Top

Adenosine is a nucleoside analog that decreases heart rate and prolongs conductance through the atrioventricular (AV) node. Adenosine binds to cardiac A1 receptors, decreasing adenylate cyclase activity and intracellular cyclic adenosine monophosphate. This results in decreased inward calcium conductance and diminishes the pacemaker current. Adenosine, which has a half-life between 0.6 and 10 s, is rapidly cleared from the circulation by uptake into erythrocytes and vascular endothelial cells. After a bolus injection of adenosine, the heart rate is reduced in a dose-dependent manner until complete AV node blockade occurs. The clinical effect of adenosine is seen 10–20 s after delivery of the bolus. The adenosine dose has a linear relationship with the duration of asystole that reaches a plateau between 40 and 60 s at 1 mg/kg.[2] After the period of asystole, there is a variable duration of relative hypotension that lasts up to 1 min. Clinically, adenosine is most commonly used for the treatment of supraventricular tachycardia.[3] Surgical uses for transient adenosine-induced asystole include endovascularaortic aneurysm repair [4],[5] and endovascular arteriovenous malformation treatment.[6],[7]

  Which are Indications of Adenosine-Induced Flow Arrest Using for Complex Aneurysm? Top

There are 3 earlier single patient case reports during 1999–2007. In the first reported case by Groff et al.,[8] adenosine was safely administered to facilitate clipping of a basilar apex aneurysm. The patient received 3 doses of adenosine, and no complications were encountered. The second case was reported by Nussbaum et al.[9] In this case, the authors used adenosine to control intraoperative rupture of an anterior communicating artery aneurysm after traditional methods of tamponade and temporary arterial occlusion failed to achieve adequate hemostasis. Adenosine allowed successful clipping in this case. The patient recovered without deficits, and no complications related to adenosine were reported. The third case reported by Heppner et al.[10] involved a giant basilar apex aneurysm. Temporary occlusion of the basilar artery above the superior cerebellar arteries failed to provide sufficient softening of the aneurysm to allow perforator visualization and clip placement. The authors then resorted to 3 sessions of adenosine-induced flow arrest. The first episode allowed perforator dissection; the second allowed permanent clip placement; and the third allowed readjustment. Unfortunately, this patient had a poor outcome, but it was judged to be unrelated to adenosine administration.

Recently, there are 10 case series describing the use of adenosine to facilitate intracranial aneurysm repair during 2010–May 2016.

For CIAs clip ligation, it is often difficult to find an anatomically suitable place for temporary arterial occlusion, such as aneurysms of the intracranial carotid artery proximal to its bifurcation into the middle and anterior cerebral arteries.[11],[12]

These aneurysms have required temporary extracranial cross-clamp of the carotid artery in the neck to facilitate intracranial clip ligation. There are alternative techniques, such as endovascular balloon occlusion with suction decompression or deep hypothermic circulatory arrest, but they require significant logistical support.[13],[14] In addition, these procedures may be associated with significant patient morbidity; endovascular procedures may result in dissection of friable arteries or distal arterial embolic occlusion, whereas cardiopulmonary bypass may result in arterial injury at the site of cannulation or arterial embolic phenomena related to aortic plaque. Furthermore, coagulopathies induced by cardiopulmonary bypass, independent of the required anticoagulation, result in a high incidence of postoperative intracranial hematomas.[15] When temporary arterial occlusion is impractical or difficult for anatomical reasons, adenosine administration can produce brief, profound systemic hypotension, and flow arrest as an alternative to logistically complex methods of decreasing parent artery blood flow.[8],[10],[16],[17],[18],[19]

At the same time, 57 (24.7%) of 231 patients who were given adenosine underwent surgery of posterior circulation aneurysm, which include 25 (10.8%) basilar artery aneurysm and 29 (12.55%) unsorted posterior circulation aneurysm. This probably refers to the fact that these operations are technically the most challenging ones [Table 1].[8],[10],[20],[21],[22],[23],[24],[25],[26]
Table 1: Location of the aneurysms (231 patients)

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Bendok et al.[23] reported a series of 40 patients using adenosine to facilitate surgery for intracranial aneurysms, they pointed out that use of temporary clips remains the gold standard. Adenosine should be regarded as an additional and potentially synergistic tool with temporary clips, not a replacement for them.

In conclusion, for intracranial aneurysms in which temporary occlusion is impractical or technically difficult, adenosine is a viable option to provide brief periods of flow arrest for facilitating aneurysm clip ligation with apparently low neurologic and cardiopulmonary morbidity in the perioperative period.

  About the Use of Adenosine-Induced Flow Arrest for Unruptured Aneurysms and Ruptured Aneurysms Top

As we all know, the first reported case by Groff et al.,[8] adenosine was safely administered to facilitate clipping of an unruptured basilar apex aneurysm. One hundred and sixty-one (69.7%) of 231 patients who were given adenosine underwent surgery of unruptured aneurysm, 70 (30.3%) of 231 patients who were given adenosine underwent surgery of unruptured aneurysm [Table 2].
Table 2: Review of adenosine for temporary flow arrest during intracranial aneurysm surgery cases

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Early rupture of an aneurysm may make temporary clip application unfeasible and potentially dangerous owing to poor exposure and visualization of the relevant proximal and distal vasculature. Hence, intraoperative rupture is the clearest indication for adenosine, particularly when rupture occurs early in the dissection before proximal and distal control have been achieved.

In the series of Bendok et al.,[23] adenosine was used for the purpose of controlling intraoperative rupture in 6 cases. In all 6 cases, the aneurysm was successfully clipped during adenosine-induced flow arrest.

Adenosine-induced flow arrest can clear the field for a long enough period to allow either definitive clipping or a corrective maneuver such as placing a pilot clip on the rupture site or trapping the aneurysm with temporary clips.

  Careful Patient Selection Top

Do not administer adenosine to patients with evidence of severe (>80%) left main coronary artery stenosis, severe multivessel coronary artery disease (3 vessels or grafts with >80% stenosis),[21],[22],[25] AV conduction defects (second degree AV block), or pacemakers.[21]

In addition, patients with severe reactive airway disease (i.e., requiring hospitalization in the previous 6 months and active perioperative wheezing) do not receive adenosine.[21],[22]

Patients are excluded from undergoing this procedure if they have a history of severe asthma, symptomatic asthma, or sick sinus syndrome/heart block.[27]

Careful patient selection in regard to cardiac history includes coronary artery disease, valvular disease, dysrhythmias, or conduction abnormalities. Patients with reactive airway disease have a relative contraindication to adenosine therapy owing to risk of bronchoconstriction.[22]

  About the Selection of an Appropriate Initial Dose: Single Dose or Multiple Boluses of Adenosine? Top

The optimal dose and administration manner of adenosine have not yet been established. Luostarinen et al. reported the first series of 16 patients demonstrating its safety and efficacy during surgery for ruptured intracranial aneurysm.[20] Of these 16 patients, 12 received a single adenosine bolus and 4 received repeated boluses. The median dose for a single bolus was 12 (6–18) mg, whereas the median total dose for multiple boluses was 27 (18–89) mg. Ten minutes after adenosine administration, all patients were hemodynamically stable and 13 patients required vasoactive drugs during the procedure. Bebawy et al. reported the second series of 24 patients using adenosine to facilitate surgery for intracranial aneurysms, a large number of which were internal carotid artery aneurysms with difficult anatomy for temporary clip.[21] They recommended an initial dose between 0.3 and 0.4 mg/kg ideal body weight as the starting dose to achieve approximately 45 s of profound systemic hypotension. The third case series reported by Powers et al. Case series included 6 patients, including 3 unruptured, 2 ruptured, and 1 intraoperative aneurysm ruptured. An adenosine dose-response curve is approximated for each patient. To do this, escalating doses of adenosine are given (6, 12, 18, 24, and 36 mg) and titrated to determine the dose that would result in approximately 30 s of asystole. Typically, the dose of adenosine is about 1 mg/s asystole. Moreover, they reported that they had not observed any complication from repeated adenosine dosing in patients with normal preoperative cardiac function who are allowed to fully recover between doses. Furthermore, although doses of adenosine as high as 90 mg have been reported for endovascular aortic aneurysm repair,[4] they have not had to give >60 mg as a single bolus during cerebral aneurysm clipping. Lee et al. reported their study, and they found that there was a linear relationship between the dose and the duration of asystole.[26]

About the dose of adenosine, because individual responses to adenosine vary, so, different patients may need different doses of adenosine.[20],[21],[22],[23],[24],[25],[26],[27],[28],[29] We recommend we should establish an individual dose–response relationship for each patient by injecting escalating doses of adenosine [Table 3].
Table 3: Preexisting medical conditions at admission and intraoperatively, postoperative complications

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  Advantages of Adenosine-Induced Transient Asystole Top

  1. Temporary flow arrest into the parent vessel, facilitating the circumferential exposure of the aneurysm and decreasing the risk of premature rupture during the dissection, and finally safe clip placement
  2. Short half-life and recovery of the normal circulation with almost no need for additional medications
  3. Adenosine may be administered repeatedly after recovery from the initial dose.

  Potential Risks, Complications of Adenosine-Induced Transient Asystole Top

Transient atrial fibrillation during cardiac rhythm recovery was reported with an incidence of 2.6%.[21],[23],[26] One of these patients required intraoperative treatment with amiodarone for conversion to sinus rhythm.[21] Troponin 1 elevation has been reported with an incidence of 1.73%,[21],[23] neither of these patients demonstrated any clinical (e.g., chest pain) or transthoracic echocardiographic evidence of cardiac dysfunction (e.g., decreased contractility and regional wall motion abnormality) in the postanesthesia care unit.

Khan et al. reported that adenosine-assisted intracranial aneurysm surgery is not associated with an increase in perioperative cardiac complications or mortality in patients with low risk of coronary artery disease.[25] However, in a large series of patients with abdominal aortic aneurysms who underwent adenosine-induced transient asystole, there was self-limited depression of the ST segment.[4] In another report on adenosine-induced cardiac arrest, ventricular tachycardia and atrial flutter were reported in patients who had a history of myocardial infarction.[17] Although most reported cardiac problems were safely controlled with medication, a medical history of coronary artery disease is a relative contraindication to this procedure.[22] Adenosine can also induce pulmonary problems such as bronchospasm.[30] In addition, caution is needed in patients with renal problems or purine metabolism abnormalities (in particular, gout) because adenosine is eliminated not only by cellular uptake but also through the kidney.[17] Close examination is crucial for the prevention of medical complications. If there is no choice but to use adenosine intraoperatively without a preoperative cardiopulmonary evaluation, particular attention is required.

Repeat administration of adenosine has another potential risk. Adenosine is rapidly metabolized and eliminated from the body; however, there was a report of prolonged hypotension (11 epochs or >5.5 min), following repeat doses of adenosine before hemodynamic recovery in a case of uncontrolled, intraoperative aneurysm rupture.[22] Because the situation was accompanied by massive blood loss and the cardiac rhythm was maintained, adenosine may not have been the only reason for the prolonged hypotension. However, it is generally understood that complete hemodynamic recovery is recommended before a repeat dose of adenosine is given.[22] If possible, sufficient arachnoid dissection, aneurysm exposure, and selection of the appropriate aneurysm clip should be achieved before the first administration to minimize the number of administrations needed.

Prolonged bradycardia or asystole is one of the potential risks; so several authors recommend the addition of the placement of transcutaneous pacemakers as a precaution for prolonged bradycardia or asystole.[27] We think it necessary to do so, because we think we should maximize the safety of patients and reduce potential risk during surgery.

  Conclusion Top

Given the limited number of studies that have reported on this topic, there is no consensus regarding the dose, regimen, efficacy, and potential risks of adenosine. We recommend that adenosine be available during intracranial aneurysm surgery and be used judiciously for scenarios in which temporary occlusion with clips is impractical, unsafe, or difficult. Further studies are warranted to further refine our understanding of the utility of adenosine during intracranial aneurysm surgery.

At the same time, in some countries, authorization from the Institutional Review Board (IRB) may be necessary in using adenosine at least in elective aneurysm surgery, so it needs to obtain the IRB's permission and it should be according to the IRB regulations.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Hanel RA, Spetzler RF. Surgical treatment of complex intracranial aneurysms. Neurosurgery 2008;62 6 Suppl 3:1289-97.  Back to cited text no. 1
Kahn RA, Marin ML, Hollier L, Parsons R, Griepp R. Induction of ventricular fibrillation to facilitate endovascular stent graft repair of thoracic aortic aneurysms. Anesthesiology 1998;88:534-6.  Back to cited text no. 2
Parker RB, McCollam PL. Adenosine in the episodic treatment of paroxysmal supraventricular tachycardia. Clin Pharm 1990;9:261-71.  Back to cited text no. 3
Kahn RA, Moskowitz DM, Marin ML, Hollier LH, Parsons R, Teodorescu V, et al. Safety and efficacy of high-dose adenosine-induced asystole during endovascular AAA repair. J Endovasc Ther 2000;7:292-6.  Back to cited text no. 4
Plaschke K, Böckler D, Schumacher H, Martin E, Bardenheuer HJ. Adenosine-induced cardiac arrest and EEG changes in patients with thoracic aorta endovascular repair. Br J Anaesth 2006;96:310-6.  Back to cited text no. 5
Hashimoto T, Young WL, Aagaard BD, Joshi S, Ostapkovich ND, Pile-Spellman J. Adenosine-induced ventricular asystole to induce transient profound systemic hypotension in patients undergoing endovascular therapy. Dose-response characteristics. Anesthesiology 2000;93:998-1001.  Back to cited text no. 6
Pile-Spellman J, Young WL, Joshi S, Duong H, Vang MC, Hartmann A, et al. Adenosine-induced cardiac pause for endovascular embolization of cerebral arteriovenous malformations: Technical case report. Neurosurgery 1999;44:881-6.  Back to cited text no. 7
Groff MW, Adams DC, Kahn RA, Kumbar UM, Yang BY, Bederson JB. Adenosine-induced transient asystole for management of a basilar artery aneurysm. Case report. J Neurosurg 1999;91:687-90.  Back to cited text no. 8
Nussbaum ES, Sebring LA, Ostanny I, Nelson WB. Transient cardiac standstill induced by adenosine in the management of intraoperative aneurysmal rupture: Technical case report. Neurosurgery 2000;47:240-3.  Back to cited text no. 9
Heppner PA, Ellegala DB, Robertson N, Nemergut E, Jaganathan J, Mee E. Basilar tip aneurysm-Adenosine induced asystole for the treatment of a basilar tip aneurysm following failure of temporary clipping. Acta Neurochir (Wien) 2007;149:517-20.  Back to cited text no. 10
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Fulkerson DH, Horner TG, Payner TD, Leipzig TJ, Scott JA, Denardo AJ, et al. Endovascular retrograde suction decompression as an adjunct to surgical treatment of ophthalmic aneurysms: Analysis of risks and clinical outcomes. Neurosurgery 2009;64 3 Suppl:ons107-11.  Back to cited text no. 13
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Young WL, Lawton MT, Gupta DK, Hashimoto T. Anesthetic management of deep hypothermic circulatory arrest for cerebral aneurysm clipping. Anesthesiology 2002;96:497-503.  Back to cited text no. 15
Lagerkranser M, Bergstrand G, Gordon E, Irestedt L, Lindquist C, Stånge K, et al. Cerebral blood flow and metabolism during adenosine-induced hypotension in patients undergoing cerebral aneurysm surgery. Acta Anaesthesiol Scand 1989;33:15-20.  Back to cited text no. 16
Owall A, Gordon E, Lagerkranser M, Lindquist C, Rudehill A, Sollevi A. Clinical experience with adenosine for controlled hypotension during cerebral aneurysm surgery. Anesth Analg 1987;66:229-34.  Back to cited text no. 17
Owall A, Lagerkranser M, Sollevi A. Effects of adenosine-induced hypotension on myocardial hemodynamics and metabolism during cerebral aneurysm surgery. Anesth Analg 1988;67:228-32.  Back to cited text no. 18
Sollevi A, Lagerkranser M, Irestedt L, Gordon E, Lindquist C. Controlled hypotension with adenosine in cerebral aneurysm surgery. Anesthesiology 1984;61:400-5.  Back to cited text no. 19
Luostarinen T, Takala RS, Niemi TT, Katila AJ, Niemelä M, Hernesniemi J, et al. Adenosine-induced cardiac arrest during intraoperative cerebral aneurysm rupture. World Neurosurg 2010;73:79-83.  Back to cited text no. 20
Bebawy JF, Gupta DK, Bendok BR, Hemmer LB, Zeeni C, Avram MJ, et al. Adenosine-induced flow arrest to facilitate intracranial aneurysm clip ligation: Dose-response data and safety profile. Anesth Analg 2010;110:1406-11.  Back to cited text no. 21
Guinn NR, McDonagh DL, Borel CO, Wright DR, Zomorodi AR, Powers CJ, et al. Adenosine-induced transient asystole for intracranial aneurysm surgery: A retrospective review. J Neurosurg Anesthesiol 2011;23:35-40.  Back to cited text no. 22
Bendok BR, Gupta DK, Rahme RJ, Eddleman CS, Adel JG, Sherma AK, et al. Adenosine for temporary flow arrest during intracranial aneurysm surgery: A single-center retrospective review. Neurosurgery 2011;69:815-20.  Back to cited text no. 23
Bebawy JF, Zeeni C, Sharma S, Kim ES, DeWood MS, Hemmer LB, et al. Adenosine-induced flow arrest to facilitate intracranial aneurysm clip ligation does not worsen neurologic outcome. Anesth Analg 2013;117:1205-10.  Back to cited text no. 24
Khan SA, McDonagh DL, Adogwa O, Gokhale S, Toche UN, Verla T, et al. Perioperative cardiac complications and 30-day mortality in patients undergoing intracranial aneurysmal surgery with adenosine-induced flow arrest: A retrospective comparative study. Neurosurgery 2014;74:267-71.  Back to cited text no. 25
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Powers CJ, Wright DR, McDonagh DL, Borel CO, Zomorodi AR, Britz GW. Transient adenosine-induced asystole during the surgical treatment of anterior circulation cerebral aneurysms: Technical note. Neurosurgery 2010;67(2 Suppl Operative):461-70.  Back to cited text no. 27
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Andrade-Barazarte H, Luostarinen T, Goehre F, Kivelev J, Jahromi BR, Ludtka C, et al. Transient cardiac arrest induced by adenosine: A tool for contralateral clipping of internal carotid artery-ophthalmic segment aneurysms. World Neurosurg 2015;84:1933-40.  Back to cited text no. 29
Malcolm AD, Garratt CJ, Camm AJ. The therapeutic and diagnostic cardiac electrophysiological uses of adenosine. Cardiovasc Drugs Ther 1993;7:139-47.  Back to cited text no. 30


  [Table 1], [Table 2], [Table 3]


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