INTRODUCTION
Intraoperative aneurysm rupture leading to subarachnoid hemorrhage (SAH) is one of the most feared neurological complications. It leads to significant morbidity and unfavorable outcomes.[1,2,3]
While comparing the outcomes of open surgical repair and endovascular repair procedures, poorer outcomes have been reported in the surgical procedures. The higher morbidity in open surgical procedures is due to surgery rather than rebleeding. Despite the medical advances, aneurysm rupture has been reported to be the most commonly reported intraoperative complication.[4]
Upon epidemiological analysis done by various studies, it has been found that more than eighty percent of nontraumatic SAH are caused by intracranial aneurysmal rupture.[4] Other causes of spontaneous SAH include other vascular lesions, inflammation, tumors, and drug or substance use.[1,4]
According to the existing literature, estimated incidence of SAH is 9.1/100,000/year worldwide. However, in some countries, notably, Japan and Finland, the incidence of nontraumatic SAH is higher, which is around 15–17/100,000/year.[5,6]
Unruptured cerebral aneurysms have an incidence of around 3%–4% as per various angiographic and prospective autopsy studies. The mean age group affected in SAH is around 50–60 years with a female predominance of 1.6 times over males.[5]
The incidence of unruptured aneurysms has been increasing globally; Intra-Operative Rupture (IOR) of aneurysms still remains a dreaded and most commonly encountered complication.[7,8,9] Reported incidence from retrospective case series during microvascular surgeries is described to be between 7% and 40%,[10,11,12,13,14,15] while it has been reported to be between 2% and 4.5% with endovascular procedures.[16,17] The wide variation in the incidence of IOR with microsurgery could be due to wide variations in the definition of IOR. Some authors consider only major intraoperative ruptures (MIOR), while others include even the trivial or minor bleeding which have no effect on the patient outcome. A systematic review conducted by Muirhead et al., reported that different definitions account for the differences in rupture rates.[4] According to the study conducted by Hsuet al., MIOR is defined as aneurysmal rupture during brain retraction, aneurysm dissection, or clipping. These require further vigorous management to control the hemorrhage including hypotension, local packing, suctioning, and temporary clipping.[18] Minor or trivial intraoperative ruptures are those that occur during clip application and stop after approximation of the clip.[18] Chandleret al. have defined IOR as bleeding that changes the course of microsurgical procedure and it does not include minor bleeding that can be easily controlled surgically.[19] In spite of major advancements in microvascular surgeries and endovascular procedures, rupture of aneurysms is associated with high mortality rates of around one-third and severe disability in nearly one-sixth of the patients.[20]
A study conducted in the United States of America over 2 years (1996–1998) with a follow-up of 5 years included 1010 patients aimed at reporting the predictors of intraprocedural rupture (IPR) during coiling and clipping. According to this study, IPR occurred in 14.6% of the total cases, of which 19% were categorized under the clipped group and 5% in the coiled group. In the clipped group, 31% of patients with IPR had periprocedural death or disability as compared to 18% with no IPR. The coiled group in this study reported that 63% of patients had periprocedural death or disability. This study also called the Cerebral Aneurysm Rerupture After Treatment (CARAT) study is one of the largest cohort studies that studied the clinical implications of IPR.[10]
PERIOPERATIVE FACTORS ASSOCIATED WITH ANEURYSMAL RUPTURE
According to literature, the risk of rupture of previously unruptured aneurysms is low 0.5%/year.[21] However, the prevalence of unruptured aneurysms is estimated to be around 0.65%–3.2% worldwide.[4]
PREOPERATIVE FACTORS
Demographics such as age, sex, and family history as well as pathological causes like size of the aneurysm, shape, location, presence of co morbid conditions, and surgical or neuroradiological procedure are linked with perioperative cerebral aneurysm rupture.[7,22] Asian and African races have been found to be independent predictors of rupture while coiling the aneurysm.[10] Similarly, genetics and family history has been found to be a major factor in the formation and rupture of an aneurysm.[23,24] The prevalence of aneurysm is 9.5% in those with a positive family history as reported by the European Stroke Organisation.[25] The risk of SAH increases with a history of polycystic kidney disease.[7]
The incidence of SAH is 1.6 times higher in females as compared to males with occurrence in the fifth decade predominantly followed by regression in incidence in the later decades.[5,6] Age has been shown to be an important factor in determining IOR with higher preponderance in elderly patients.[26,27] However, in a retrospective study conducted by Lakicevicet al., male gender has been implicated to be having more chances of rupture as compared to females.[28]
Another important risk factor concerned with rupture of aneurysm is its location. As per existing literature, aneurysms are formed most commonly in the middle cerebral artery (MCA) followed by the internal carotid artery (ICA), whereas the risk of rupture is higher in anterior and posterior communicating arteries (AcoA and PCoA, respectively) and giant aneurysms of basilar artery.[12,14,29] The incidence of rupture is higher in posterior circulation, large and symptomatic aneurysms as quoted by a Japanese publication, whereas an American study concluded that most of the ruptured aneurysms are located in the anterior circulation.[30,31]
Size of the aneurysm has also been implicated as a major cause of its rupture. International Study of Unruptured Intracranial Aneurysms has shown that larger aneurysms, those located in posterior circulation, and previous history of rupture have more chances of IOR.[24] Another large study showed that in addition to age of the patient, location and size of aneurysm are the main factors influencing the outcome of surgical clipping or endovascular coiling.[32] Sluzewskiet al. have shown that aneurysm size is a major factor in IOR, smaller the size, lesser the chances of rupture.[33] Juvela et al. have also described the size of the aneurysm as an important predictor for rupture.[26] A study published in the New England Journal of Medicine quotes eleven times higher rates of rupture in aneurysms more than 10 mm in diameter (0.5%/year) in contrast to those with diameter <10 mm (0.05%/year). In giant aneurysms (>25 mm), rate was 6%/year.[34]
Complement activation and inflammatory tissue damage inside the aneurysmal vessel wall has been studied to be an important mechanism. Interplay of several biochemical mechanisms has been studied in the phenomenon of IOR. Variation in endothelial nitric oxide synthetase due to genetic modulations has also been implicated in the aneurysmal SAH.[35,36] High catecholamine levels in cerebrospinal fluid (CSF) and serum S100 levels are associated with poor outcomes.[37,38]
Predictors of aneurysmal growth may include diameter of 10 mm or more and location at basilar artery, ICA, or bifurcations.[39] Some aneurysms at rare locations which pose a great threat of rupture and are difficult to manage include intrasellar aneurysms, which mimic pituitary tumors, pericallosal aneurysms, and blood blister type of aneurysms.[40,41,42,43,44,45] SAH related to nocturnal ruptures of aneurysms has also been found to be an independent risk factor for cerebral ischemia.[46] Aneurysms located at arterial bifurcations have wall shear stress acting at point of stress. However, in contrast, some studies have also reported contrast that aneurysms at junctions of PCoA as well as ICA do not have higher risk of rupture.[47,48]
Patient related co morbidities like coronary artery disease (CAD) are an important risk factor for IOR. Smoking, hyperlipidemia, and hypertension also alter the vascular fragility which are known risk factors for CAD.[37] Therefore, CAD may lead to cardiac as well as cerebrovascular devastations during aneurysm surgery, thus making thorough cardiac evaluation important preoperatively.
Cigarette smoking has been found to be an important independent risk factor by various case–control and cohort studies worldwide. 40% of SAH cases have been attributed to smoking.[49,50,51,52] In a prospective study, smoking and female sex have been found to be most significant factors in aneurysm formation and growth. Chronic obstructive pulmonary disease (COPD) has been found to be associated to IOR and cigarette smoking is the major cause of COPD. COPD patients have smoking related inflammatory changes along with biochemical changes like alpha-1 antitrypsin deficiency and high levels of matrix metalloproteinases, thus leading to a fragile vessel wall. Furthermore, loss of vascular smooth muscle, lesser collagen synthesis, and breakdown of extracellular matrix are other contributory factors. COPD also increases the resistance of airways causing a high transmural pressure gradient (TMPG) across the closed cranium.[51] The CARAT study also shows COPD to be major risk factor.[10] Faster growth rate of the aneurysm also increases the chances of rupture.[53]
Alcohol abuse has been studied by various researchers as one of the contributing factors to rupture of cerebral aneurysms and has been shown to be an independent risk factor of SAH in both males and females.[49,50,51] Ruigroket al. have concluded that more than 300 g of alcohol consumption/week may lead to 20% more chances of SAH, while alcohol consumption between 100g and 299 g/week increases the chances of SAH by 11%.[52]
Rupture can be precipitated by sudden blood pressure or intracranial pressure (ICP) fluctuations.[4] Hypertension is, thus, one of the most important risk factors for formation and rupture of intracranial aneurysms.[53,54] Poorly controlled hypertensives are at a high risk of aneurysm rupture. An increase in blood pressure increases the TMPG in the aneurysmal wall and also alters the vessel wall thickness. According to two case–control studies, the prevalence of hypertension is more in SAH patients than general population (20%–45%), yet after taking into account risk factors like age, gender, history of smoking and alcohol consumption, hypertension has not been shown to be a single significant risk factor.[51] However, general consensus of authors after combining the results of all case–control and cohort studies is to consider hypertension as a risk factor.[49] Researchers are also of the view that even though hypertensives do not show aneurysm growth more than normotensives, still hypertensive patients who use antihypertensive medication have a lower risk of aneurysm formation.[25]
Hypertension has been found to be more prevalent in multiple aneurysms and also makes a significant risk factor for the formation of new aneurysms and enlargement of the existing ones.[55]
Thus strict control of hypertension may improve the prognosis in cerebral aneurysm patients.[56] At the same time, cerebral vasospasm following rupture and hypotension as a measure to control it intraoperatively may lead to delayed ischemic neurological deficits.[57] Whereas, studies show that intraoperative hypotension or hypertension during aneurysm occlusion does not have any significant effect on the neurological outcome.[58]
This topic, thus, remains controversial, although studies recommend a strict control of systemic, diastolic, and mean arterial blood pressure.
Sudden rupture of aneurysm can also occur during induction of anesthesia in about 1%–2% of cases with a mortality rate of around 75%.[59,60] Tsementziset al. have reported that 8 patients out of 404 had an acute aneurysmal rupture during induction of anesthesia or while coughing and bucking during intubation, indicating sympathetic stimulation while airway manipulation.[59] Perioperatively, hypertension can occur during induction, intubation, positioning of patient, application of Mayfield pins on skull, pain at any time during local anaesthetic infiltration along the line of incision, during skin incision, periosteal flap dissection, opening of dura, coughing, or bucking anytime perioperatively, and extubation due to sympathetic surge. This increase in aneurysmal transmural pressure may lead to sudden rupture.[9,61]
Preoperative neurological status of the patient is an essential determinant of IOR and patient outcome. A previously ruptured aneurysm has a higher risk of IOR as compared to a previously unruptured aneurysm.[12,15]Preoperative Glasgow coma score is also an independent statistically significant predictor of major intraoperative rupture.[18] Evaluation of preoperative Hunt and Hess Grades (HH Grades) have shown that patients with HH Grades I and II have favorable outcome in 72.2% cases without IOR and 71.1% cases that had IOR. However, patients with HH Grades III and IV showed favorable outcomes in only 34.6% of cases without IOR and 23.1% of cases with IOR. Poor Fischer Grades (III and IV) are also associated with poor neurological outcomes postoperatively.[13] Schramm and Cedzich have stated that IOR affects the final outcome only if it occurs prematurely, while anesthetic induction or opening of dura.[14]
ICP is usually raised in patients with poor HH Grades. Sudden lowering of ICP may raise TMPG suddenly, leading to IOR.[62] Rapid large bolus of mannitol, excessive hyperventilation, rapid drainage of CSF via lumbar drains, or ventriculostomy catheters may cause IOR.[61] However, no substantial data is available to support the relation between ICP and IOR.[62] According to studies, application of Valsalva maneuver and positive end expiratory pressure may also lead to changes in aneurysmal transmural pressure.[61]
Timing of surgery after SAH in cases of already ruptured aneurysms has been found to be another factor involved in IOR. As stated by a study, incidence of IOR was three times greater in patients operated within 1st 3 weeks after SAH than in patients operated later (P < 0.05). Another study echoes similar results, in which 77 patients out of 222 who underwent surgery within 72 h of SAH had IOR in 40.2% cases, while the rate of rupture was 20.7% in the 145 patients who underwent operation after 72 h. However, mortality and severe morbidity after surgery was 2.6% in early surgery group, while it was 7.6% in late surgery group.[14]
Many variables are related to aneurysmal rupture during microvascular clipping or endovascular coiling. According to a study by Batjer and Samson, IOR of aneurysm is expected at three points. First is during the initial phase of surgery during craniotomy, dural opening, hematoma removal, and brain retraction (incidence of 7% and mortality 75%). Second stage is during blunt or sharp dissection (48% incidence). Third phase is during clip placement (incidence of 45%).[60] Inagawa concluded in the study that 9% intraoperative rupture occurs due to procedure itself, which is usually during dissection of aneurysm or dissection of adherent artery or clip application.[63] Posterior inferior cerebellar artery, ACoA, and PCoA are more likely to rupture intraoperatively as stated by another study.[64]
Experience of surgeon also plays a vital role in the IOR of aneurysm. Hsuet al. have conducted a multivariate analysis of 538 microsurgical clipping cases. They quoted that surgical experience is an independent predictor of MIOR. Experienced neurosurgeons encountered lesser number of MIOR (8%) as compared to novice surgeons (16%). Also, in cases of MIOR, the outcome was poorer in the hands of novice neurosurgeons by 1.9 fold. MIOR cases managed by experienced neurosurgeons had better prognosis than those by inexperienced neurosurgeons (poor outcome 22% vs. 60%).[18] Various other studies also have concordant results.[11,15] In contrast some authors have reported that MIOR has no relation with surgical experience.[10,65]
Management of very small aneurysm is challenging both surgically and endovascularly especially during endovascular embolization.[66] Iatrogenic rupture with coiling have been reported by Rasulićet al. in <4 mm and by Lakićevićet al. in <2 mm aneurysms.[67] The advantage of surgical intervention being the immediate access to the proximal and distal vessels and removal of blood from operative site.[68] It has also been quoted that IOR during endovascular coiling has a poorer outcome due to lack of direct exposure.[59] Cloft and Kallmes. conducted a metaanalysis and found that IOR rate was 2.7%, with a rate of rupture of 4.1% in previously ruptured aneurysms.[69] Greater fragility and subsequent IOR of smaller aneurysms could be due to larger surface area of previous rupture, causing coils to damage the weakened site. Additionally, presence of daughter aneurysms may be an added risk factor.[17] Various mechanisms of rupture during coiling include guidewire or microcatheter perforation, high pressure contrast injection into the aneurysm leading to high transmural pressure.[70] Careless handling of guidewire or catheter such that catheter potential energy propels it forward leading to perforation of the aneurysm. Also wedging of catheter between deposited coils and aneurysm wall, overpacking and oversizing of coils could lead to rupture. In case of use of balloon assisted coiling, balloon inflation across the neck of aneurysm may lead to rupture.[71] CLARITY trial has studied endovascular management of aneurysms. According to this trial IOR is related more to patients of <65 years age, hypertensives and MCA aneurysms.[72] Another study revealed that there are five times more chances of rupture in already ruptured small aneurysms and balloon assisted hemostasis has better outcome.[73]
Usually surgery is warranted for younger age group and embolization for elderly patients. One study states that minimization of temporary occlusion and use of intraoperative angiography has improved the surgical outcome.[74] IOR and temporary occlusion for more than 20 min have been found to be independent predictors of perioperative stroke.[75]
The contributory factors may be excessive CSF drainage, hypertension causing hemodynamic stress and trauma during surgical manipulation.[76] Recurrence of aneurysm and subsequent SAH from residual necks after clipping[77] and incomplete occlusion after coiling may lead to chances of re rupture.[4]
POSTOPERATIVE FACTORS
Diagnosis of intraprocedure rupture
Clinically, unexplained sudden hypertension and bradycardia may indicate an IOR during coiling or clipping procedures.[59] Sudden high ICP and herniation could cause blown pupil, arrhythmias, and ischemia on neurophysiological monitoring (NPM)[58] Surgeon may notice increase in ooze from scalp incision or unexpected brain bulge.[59] According to authors, in case of an unexpected tense brain, IOR should be kept as a differential diagnosis[78] During coiling, dye extravasations or prolonged contrast dye transit time may be noticed. High ICP could lead to flow arrest or flow reversal of external carotid artery.[79] Postoperatively, delayed consciousness, sudden deterioration of neurological status, changes in hemodynamics, seizures, or focal neurological deficits are usual signs of IOR.[80]
NPM is helpful in identifying this crisis. Electroencephalography (EEG) may also show decrease in the power spectrum with weak alpha and beta frequencies and predominance or loss of low frequency components. EEG is a sensitive indicator of brain ischemia showing burst suppressions and finally complete electrical silence.[81]
Evoked potentials (EP) show decrease in amplitude and increased latency. Somatosensory EPs (SSEPs) are considered to be more significant than motor EP or brainstem EP. However, EEG and EP monitoring may be affected by anesthetics, temperature and hemodynamic status leading to erroneous interpretations.[82] During use of induced cerebral protection while temporary clipping, metabolic demand of neural tissue decreases and burst suppression is employed. This could lead to missing out of ischemic events on EEG. During this time of burst suppression, SSEP although not very sensitive to detect brain ischemia, may be helpful by the way of careful examination of the territory. It has been found to be helpful in 93% of the cases.[83] Intraoperative use of transcranial Doppler, cerebral oximetry, and intraoperative imaging like CT, MRI, and angiography has been found to be useful to diagnose IOR.[84,85]
Management of IOR during surgical clipping
Before dural opening, various goals of management include ICP reduction and neuroprotection. Rapid lowering of ICP is not advocated, since ICP may have a protective tamponade effect which is beneficial to stop the bleeding. Gradual ICP reduction may be done using intravenous (IV) anesthetics like IV propofol or thiopentone sodium, moderate hyperventilation, and hypothermia.[86] IV anesthetics reduce the cerebral metabolic rate as well as ICP. Hypothermia has been quoted to have neuroprotective effects by lowering cerebral metabolism. It has free radical scavenging and membrane stabilizing effects. Different studies have variable views regarding induced hypothermia. Recent studies suggest use of mild hypothermia (32–35°) in good grade patients, but no benefit has been shown in poor grade patients.[87,88] Its role during IOR is still controversial.
Hyperventilation may help lower the ICP but vasoconstriction induced by hyperventilation may worsen the brain ischemia. Short periods of moderate hyperventilation may be safe.[86]
Hemodynamic goals include lowering of blood pressure by 20% from baseline during IOR.[59,61,86] Aggressive treatment of blood pressure may lead to secondary ischemia. Prompt surgical clipping improves the outcome.[59] Various techniques may be implemented to blunt sympathetic stimulation to achieve hemodynamic stability to avoid rupture or re bleed. These include use of IV lignocaine, esmolol, or labetalol to reduce stimulation during airway manipulation. Local anesthetic infiltration at the site of incision and pin sites reduces stimulation while pinning and bone flap creation. Prophylactic propofol bolus or use of continuous infusion of short acting opioids like remifentanil or bolus of short acting opioid is also helpful to maintain cerebral perfusion pressure, ICP, and MAP.[86]
Other management goals include reducing the cerebral metabolism and lowering the abruptly increased ICP by ventricular drainage.[71] Use of iv anesthetics, controlling of blood pressure, and moderate hyperventilation can be started immediately.[61,86] Urgent ventriculostomy or craniotomy may be the last resorts.[79]
After dural opening, induced hypotension with lowering of mean arterial pressure to 50 mmHg has been advocated by various authors. This helps improve surgical exposure and easy clipping of soft aneurysm neck.[59,86] However, MAP of 50 mmHg may be difficult to achieve and could also lead to worsening of cerebral ischemia.[86] This is more so in situation of an IOR, where cerebral autoregulation is already impaired.[89] Thus, normotension, normovolemia, euglycemia, and proper electrolyte balance are advocated.[61,86] Blood may be needed to be transfused in this situation.[90] During this phase, when dura is open, awareness or sudden movement under anesthesia must be avoided.[86] Neuromuscular monitoring is helpful. Temporary occlusion by clip application in case of IOR is imperative but difficult. This may be facilitated by transient circulatory arrest using adenosine.[91,92] Adenosine induced flow arrest transiently may improve aneurysmal neck visualization. It is recommended to be started at a dose of 0.3–0.4 mg/kg to achieve profound hypotension for 45 s, along with remifentanil, low-dose volatile anesthetics, and propofol infusion.[91] Use of ventricular pacing for transient flow arrest has been found to be safe and effective during IOR.[93] The authors have recommended temporary interruption of arterial flow as a routine method for aneurysm clipping.[11]
During embolization, management includes reversal of heparin using protamine sulfate. Further continuing the packing with coils usually stops hemorrhage if bleeding is due to coil herniation.[11] Willinsky and terBrugge. have advocated leaving the microcatheter in situ, in case of perforation with it and introducing new catheter.[94]
Neuroprotection
Various neuroprotective mechanisms include hypothermia, hyperoxygenation, avoiding hyperthermia, maintaining euglycemia, hemodilution, hypervolemia, and hypertension. Other neuroprotective agents include calcium channel blockers, antifibrinolytic drugs, magnesium, anesthetic agents, and erythropoietin.[95,96] Intraoperative hypothermia for aneurysmal surgery trial has stated that these neuroprotective drugs and mechanisms have no protective effects in the outcome.[97] Nitrous oxide used during anesthesia may also affect short term outcomes negatively, while no effect has been seen on long term outcomes.[97] However, during an episode of IOR, cerebral metabolic rate as well as blood pressure may be reduced using Propofol or thiopentone. Barbiturates have been found to have protective effects other than above.[98] Use of volatile anesthetics is recommended during IOR by authors, while their use during embolization should be avoided due to their effect in increasing cerebral blood volume and hence ICP.
Surgical management includes temporary occlusion of aneurysm in order to assist proper clipping and also decreases the chances of IOR. It has been seen that extra axial SAH or intraventricular hemorrhage have better outcomes then intraparenchymal hemorrhage[99] IOR is best prevented than treated. Various techniques include adequate exposure, proximal control, sharp dissection, and temporary clipping. Ruptures could also be prevented if small aneurysms <3 mm are not treated endovascularly.[67]
CONCLUSION
Our review concludes that thorough knowledge of the pathophysiology of intraoperative cerebral rupture and identifying the risk factors is the mainstay in better patient outcome. The management of this fearsome complication demands a synergistic approach from the surgeon, neuroradiologist, and the anesthesiologists.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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