Panduranga Seetahal-Maraj1,2, Sharies Arjoon1, Narindra Ramnarine1,
1Department of Neurosurgery, San Fernando General Hospital, Trinidad
2Department of Clinical Surgical Sciences, The University of the West Indies, St Augustine, Trinidad
DOAJ: 5c2cbf4ba7fb4a48b7a04b6a92c709ff
DOI: https://doi.org/10.48107/CMJ.2023.06.002
Copyright: This is an open-access article under the terms of the Creative Commons Attribution License which permits use, distribution, and reproduction in any medium, provided the original work is properly cited.
©2023 The Authors. Caribbean Medical Journal published by Trinidad & Tobago Medical Association
ABSTRACT
Objectives
Reports on the management and outcomes of intracranial aneurysms are sparse from the English-Speaking Caribbean. This study aimed to determine the characteristics and outcomes of surgically clipped ruptured intracranial aneurysms undertaken by a single neurosurgeon, under the unique challenges faced in a low-resources setting.
Methods
The neurosurgical operative logbook from the period July 1st 2018 – July 31st 2021 was examined to identify all patients who had surgically clipped cerebral aneurysms at a tertiary care teaching hospital in Trinidad and Tobago. Patients’ charts were reviewed to assess risk factors such as hypertension, smoking, positive family history, aneurysm grades and types, including presenting Hunt and Hess (HH) Grade, modified Fisher CT Grade, time to definitive surgery and Glasgow Outcome Scale – extended (GOSE).
Results
Twenty-six patients underwent open surgical aneurysmal clipping, between the ages of 20 – 73 years. Posterior communicating artery aneurysms (35%) and anterior communicating artery aneurysms (38%) were the most commonly encountered types of aneurysms. One half of patients were HH Grade 1, and 58% were Fisher Grade 4. Time to clipping ranged from 3 – 62 days, with a mean of 12 days. About 42% of aneurysms were clipped prior to the peak vasospasm period, while 61% were clipped within 14 days. Following the procedure, 62% of patients had GOSE score of 8 (maximum function).
Conclusion
Surgical clipping of ruptured intracranial aneurysms may yield good patient outcomes even in a low-resource setting, despite challenges faced due to limited resources and operating time. Clipping during peak vasospasm period did not result in worse outcomes. The establishment of a neurovascular service may be beneficial even in low-resource settings.
Keywords
Intracranial aneurysm; clipping; endovascular; Trinidad and Tobago; Caribbean
Introduction
Intracranial aneurysms are defined as abnormal, pathological dilatations of arteries, that usually occur at junctional points within the vessels.1 They are well-described in the neurosurgical literature and are associated with significant morbidity and mortality as sequelae of their rupture. The one-month mortality rate post-rupture ranges from 30-50%. 2,3 The prevalence of intracranial aneurysms is quoted to be 3.2% of the general population. Certain risk factors have been identified, and notably include hypertension, smoking, female gender, and a first-degree relative with intracranial aneurysms.1
The classical presentation of a ruptured aneurysm is that of a severe headache (‘thunderclap’), and can also include vomiting, meningism and seizures.1,3 Further to this, they can rebleed, which occurs in 20% of patients in the first two weeks post-ictus, and in 50% within the first six months.3 Patients can also develop hydrocephalus, cerebral vasospasm and delayed cerebral ischaemia.4 Cerebral vasospasm results from both impaired vasodilatory and overactive vasoconstrictive mechanisms, after subarachnoid blood bathes the vessels.3 This can result in the development of permanent ischaemic deficits/stroke.
Management strategies are broadly divided into surgical (clip) and endovascular (coil) therapies. In the past two decades, we have seen a proliferation of various techniques, particularly in the endovascular realm.1,2,4 As treatment modalities continue to evolve, it is incumbent upon us to ensure that the standard of care practiced in Trinidad and Tobago is congruent with current evidence-based guidelines.
Neurosurgery in Trinidad and Tobago began in 1956, and faced considerable resistance to be established as a dedicated service.5,6 However, the situation changed when a young relative of a government official suffered from cervical subluxation with quadriparesis. The services of a neurosurgical consultant were requested to manage this patient, who subsequently improved under such dedicated care. Since this era, there has been definite improvements in the attitude towards neurosurgery in Trinidad and Tobago. However, several challenges have prevented the growth and maintenance of a consistent neurosurgical service, particularly in tertiary institutes. These include lack of adequate staffing, equipment and support services to run a comprehensive neurosurgical service.
We report on the first documented series of aneurysm-clipping performed at a tertiary care teaching institution from South Trinidad, which serves a population of 600,000, and accepts neurovascular referrals from other hospitals in the country.7
Methods
The neurosurgical operative logbook at the surgical department in San Fernando General Hospital was reviewed, between the period July 1st, 2018 – July 31st, 2021. Approval was obtained from the Institutional Review Board (SWRHA Ref. 1/3/40-127). All patients with aneurysmal subarachnoid haemorrhage (SAH) that had been surgically clipped by a single surgeon were recorded, and data were retrieved from the individual patient files.
Demographics including age, gender, presence of hypertension, smoking history, first-degree relative with an aneurysm were obtained. The time from admission until surgery, aneurysm location, Hunt and Hess grade, Modified Fisher CT grade and Glasgow Outcome Scale-extended (GOSE) were all collated and analysed using Microsoft Excel™.
The Hunt and Hess (HH) grading distribution was utilised for classifying each admission, as this is correlated with patient survival.8 It ranges from one to five, and is as follows –
- Grade 1 – asymptomatic or minimal headache and slight neck stiffness (70% survival)
- Grade 2 – moderate to severe headache; neck stiffness; no neurologic deficit except cranial nerve palsy (60% survival)
- Grade 3 – drowsy; minimal neurologic deficit (50% survival)
- Grade 4 – stuporous; moderate to severe hemiparesis; possibly early decerebrate rigidity and vegetative disturbances (20% survival)
- Grade 5 – deep coma; decerebrate rigidity; moribund (10% survival)
The modified Fisher CT scale was utilised to characterise the SAH on presenting CT scan. 9 This scale has been used widely in neurosurgical centres to predict the risk of vasospasm:
- Grade 0 – no SAH, 0% symptomatic vasospasm
- Grade 1 – thin SAH without intraventricular haemorrhage (IVH), 24% symptomatic vasospasm
- Grade 2 – thin SAH with IVH, 33% symptomatic vasospasm
- Grade 3 – thick SAH without IVH, 33% symptomatic vasospasm
- Grade 4 – thick SAH with IVH, 40% symptomatic vasospasm
The outcome parameter utilised was the Glasgow Outcome Scale-Extended (GOSE). This has become one of the most popular tools to assess global disability and recovery after neurological injury.10 It ranges from 1 to 8, and gives an idea of the patient’s level of disability, with 1 being death, and 8 being maximum function. Scores were obtained at one month postoperatively, and a score over 4 is deemed to be a good outcome (independent). 10
Results
Twenty-six patients with ruptured intracranial aneurysms were identified, who all proceeded to have open surgical clipping There were 20 females, and patients ranged from 20 – 73 years of age. The mean age was 52 years.
Hypertension was identified as a risk factor in 22 patients; 15 patients were active cigarette smokers and a positive family history of aneurysms identified in three patients. (Table 1)
Table 1. Demographic and clinical variables
Age (y)/ Gender
Male/Female (M/F) |
HTN
(Yes/ No) (Y/N) |
Smoker
(Y/N) |
Family history
(Y/N) |
Location of aneurysm | Time to clip
(h) |
Hunt and Hess Grade
(1-5) |
Modified Fisher
CT Grade (1-4) |
Glasgow Outcome Scale – Extended (1-8) | |
56 F | Y | N | N | PCom | 10 | 2 | 4 | 4 | |
47 F | Y | Y | N | ACom | 3 | 1 | 4 | 2 | |
52 M | Y | Y | N | ACom | 23 | 2 | 3 | 5 | |
44 F | Y | Y | Y | ACom | 17 | 2 | 1 | 8 | |
64 F | Y | Y | N | Terminal ICA | 20 | 2 | 4 | 1 | |
45 F | Y | Y | Y | ACom | 3 | 3 | 4 | 8 | |
70 F | Y | N | Y | PCom | 2 | 1 | 4 | 8 | |
51 F | Y | N | N | PCom | 5 | 1 | 4 | 8 | |
72 F | Y | N | N | ACom | 7 | 2 | 4 | 4 | |
64 M | Y | Y | N | ACom | 3 | 1 | 4 | 8 | |
66 F | Y | Y | N | PCom | 3 | 4 | 4 | 2 | |
39 F | Y | Y | N | PCom | 3 | 4 | 4 | 5 | |
66 F | Y | Y | N | MCA | 6 | 4 | 4 | 2 | |
46 F | Y | N | N | MCA | 2 | 2 | 3 | 7 | |
45 F | Y | N | N | PCom | 15 | 1 | 2 | 8 | |
45 F | Y | N | N | AChA | 15 | 1 | 2 | 8 | |
69 F | Y | Y | N | ACom | 62 | 4 | 3 | 1 | |
58 F | Y | N | N | ACom | 5 | 2 | 2 | 8 | |
50 F | Y | Y | N | MCA | 24 | 1 | 1 | 8 | |
73 F | N | Y | N | PCom | 26 | 1 | 3 | 8 | |
42 F | Y | Y | N | ACom | 17 | 2 | 4 | 8 | |
38 F | Y | N | N | ACom | 3 | 1 | 4 | 8 | |
44 F | N | N | N | Terminal ICA | 7 | 1 | 4 | 8 | |
20 F | N | N | Y | PCom | 16 | 1 | 1 | 8 | |
36 F | N | Y | N | PCom | 11 | 1 | 2 | 8 | |
51 F | Y | Y | N | PICA | 7 | 1 | 4 | 8 |
PCom – posterior communicating artery, ACom – anterior communicating artery, AChA – anterior choroidal artery,
MCA – middle cerebral artery, PICA – posterior inferior cerebellar artery
The Hunt and Hess scale distribution was 50% HH1, 31% HH2, 4% HH3 and 15% HH4. Three patients presented with modified Fisher CT grade 1, four each with Grades 2 and 3, and 15 with Grade 4 (Table 2).
Table 2. Patient distribution in accordance with the Grading systems
Grade | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 |
GOSE (n) | 2 | 3 | 0 | 2 | 2 | 0 | 1 | 16 |
Modified Fisher (n) | 3 |
4 |
4 | 15 | ||||
Hunt and Hess(n) | 13 |
8 |
1 |
4 |
The most commonly encountered aneurysms were located at the anterior communicating artery (n=10) and posterior communicating artery (n=9) (Tables 1, 3).
Table 3. Location of ruptured aneurysms
Aneurysm Location | Number of patients |
Anterior communicating artery | 10 |
Posterior communicating artery | 9 |
Middle cerebral artery | 3 |
Anterior choroidal artery | 1 |
Posterior inferior cerebellar artery | 1 |
Terminal internal carotid artery | 2 |
The duration of time from patient admission until surgical clipping ranged from 3 – 62 days. The mean time from admission to surgical clipping was 12 days. 42% of aneurysms were clipped prior to the peak vasospasm period (6 days), while 61% were clipped within 14 days (Table 4). All patients went to the High Dependency Unit postoperatively.
Table 4. Time to clipping of aneurysms in relation to the peak vasospasm period
Time to clipping (days) | Number of patients |
£ 6 (prior to peak vasospasm) | 11 |
7-14 (vasospasm) | 5 |
³ 15 (after peak vasospasm) | 10 |
Regarding the GOSE, 16 patients had a score of 8 at one-month post-clipping (maximum function), and 21 overall had a good outcome (GOSE 5-8). Five patients had a score less than 4 (dependent/dead) (Table 2). Patients with posterior communicating artery aneurysms and anterior communicating artery aneurysms tended to have higher GOSE scores (Table 5). Two patients died (GOSE 1), one from a pulmonary embolus, despite standard deep venous thrombosis prophylaxis being implemented. The other patient had a rebleeding while awaiting surgery. Although the aneurysm clipping was successful, the patient remained in a persistent vegetative state due to the neurologic insult, and eventually demised. All patients were followed up postoperatively at one month.
Table 5. Distribution of Hunt and Hess, modified Fisher and GOSE scores with respect to aneurysm location
ACom | PCom | Terminal ICA | Middle cerebral artery | Anterior Choroidal artery | Posterior inferior cerebellar artery | |
HH 1 | 3 | 6 | 1 | 1 | 1 | 1 |
HH2 | 5 | 1 | 1 | 1 | 0 | 0 |
HH3 | 1 | 0 | 0 | 0 | 0 | 0 |
HH4 | 1 | 2 | 0 | 1 | 0 | 0 |
HH5 | 0 | 0 | 0 | 0 | 0 | 0 |
Fisher 1 | 1 | 1 | 0 | 1 | 0 | 0 |
Fisher 2 | 1 | 2 | 0 | 0 | 2 | 0 |
Fisher 3 | 2 | 1 | 0 | 1 | 0 | 0 |
Fisher 4 | 6 | 5 | 2 | 1 | 0 | 1 |
GOSE 1 | 1 | 0 | 1 | 0 | 0 | 0 |
GOSE 2 | 1 | 1 | 0 | 1 | 0 | 0 |
GOSE 3 | 0 | 0 | 0 | 0 | 0 | 0 |
GOSE 4 | 1 | 1 | 0 | 0 | 0 | 0 |
GOSE 5 | 1 | 1 | 0 | 0 | 0 | 0 |
GOSE 6 | 0 | 0 | 0 | 0 | 0 | 0 |
GOSE 7 | 0 | 0 | 0 | 1 | 0 | 0 |
GOSE 8 | 6 | 6 | 1 | 1 | 1 | 1 |
PCom – posterior communicating artery, ACom – anterior communicating artery
Discussion
The study hospital provides neurosurgical care for a population of 600,000 persons based on the last census.7 Given a reported prevalence of unruptured intracranial aneurysms of 2% – 3.2%, this implies potentially 12-18,000 patients in the catchment area who may require management at some point in time. 1,4
The management of ruptured intracranial aneurysms has evolved in the recent past to favour endovascular therapy (EVT). The International Subarachnoid Aneurysm Trial (ISAT) is one of the landmark trials in contemporary neurosurgery, on which much of current aneurysm management practice is based. It has changed the landscape of aneurysm treatment, with its conclusion that if there is equipoise in management, EVT is associated with superior patient outcomes (better independence and cognitive function) at one year (6.9% absolute risk reduction). This benefit continues for at least seven years.1,11 As a result of this more favourable risk/benefit profile, many centres worldwide now offer EVT for the management of ruptured intracranial aneurysms.
However, in Trinidad and Tobago, this modality for intracranial aneurysm treatment is not readily available at public hospitals, and only in a select few private institutions. Significant infrastructure (catheter lab/angiography suite) along with consumables (catheters, coils, stents, flow diverters) and properly trained staff are required to safely and efficiently perform EVT. Additionally, regular equipment maintenance is required. This creates an additional cost, which might have been another factor for its unavailability in the public sector.
Maud et al. looked at costs of EVT and neurosurgical clipping in management of aneurysms in the post-ISAT era. The median estimated costs of endovascular and neurosurgical treatments (in US dollars) per patient with aneurysmal SAH were USD 45,493 and USD 41,769 respectively.12 Further to this, a meta-analysis by Zhang et al. revealed that the one-year medical costs of EVT was significantly lower than that of clipping in ruptured aneurysms. In addition, the length of stay of coiled patients was significantly shorter than clipped patients. 13
Hoh et al. reported in 2010 that clipping was associated with an average of 1.2-times more days in hospitalization for ruptured patients, and 1.8-times more days in hospitalization for unruptured patients (after adjustment for all-related factors). On average, clipping resulted in $15,325 USD more for ruptured patients and $11,263 USD more for unruptured patients, after considering all relevant hospital and patient characteristics. 14
It is incumbent upon the neurosurgeons to provide all available evidence-based treatment options to patients who present with ruptured intracranial aneurysms, including those that are not available at the study hospital. However, given the cost of EVT (catheter cerebral angiography alone ranges from $1,500 to 2,000 USD), very few patients can afford this modality. While financial aid does exist from the Ministry of Health through the Medical Social Worker route, this may take days to weeks for approval. Since there is a significant risk of rebleed and associated mortality, up to 23% in the first 72 hours after rupture, 20% in the first two weeks and up to 50% in the first six months, delays in treatment can be catastrophic. 3,15
At the study hospital, surgical clipping is the only therapeutic option currently available. However, certain aneurysms are better suited to EVT (such as posterior circulation aneurysms) due to the potential morbidity from the surgical approach.1 With the advent of newer endovascular devices, previous contraindications to EVT (wide-necked aneurysms, fusiform aneurysms) are also being revised. Our hope is that eventually EVT will become available in the study hospital, to enable comprehensive care for patients with aneurysmal SAH.
While most neurosurgeons undergo some degree of training in aneurysm-clipping, patients operated on by experienced neurovascular surgeons are found to have better outcomes. Hsu et al. reported on 538 intracranial aneurysm-clipping at a single centre in China. They compared two experienced neurovascular surgeons (minimum of 20 clippings annually) with 16 inexperienced neurosurgeons (maximum of five clippings annually). This revealed that 8% (18/225) of cases done by the two neurovascular surgeons had major intraoperative rupture, compared to 16% (50/313) done by the 16 less experienced neurosurgeons. Of those cases with major rupture, 22% (4/18) had a poor outcome (GOSE <5) when managed by an experienced vascular neurosurgeon, compared to 60% (30/50) of those managed by less experienced neurosurgeons. 16Evidence also suggests that high-volume centres (more than 10-50 cases per year) have superior patient outcomes (reduced mortality and GOSE scores >4) when managing aneurysmal subarachnoid haemorrhage.17
One of the benefits of having a dedicated neurovascular surgeon in the study hospital is prioritising early definitive management, thereby reducing the risk of rebleed and its associated mortality. 42% of patients were clipped within 6 days, and 61% within 14 days. Good outcomes (GOSE > 4) were seen in 62% of patients. This is despite the fact that 58% of patients presented with modified Fisher Grade 4 SAH, and 50% having a Hunt and Hess Grade of 2 or higher. Early securing of the aneurysm also facilitates blood pressure augmentation in the vasospasm phase, allowing for prevention/reversal of possible ischaemic deficits. Prior to this, systolic blood pressures are maintained between 120-160 mmHg, as there is a delicate balance between prevention of ischaemia and aneurysm re-rupture.3
Various aspects of care that are particular to patients with ruptured intracranial aneurysms were aggressively managed. These included electrolyte imbalances (specifically sodium derangement due to Syndrome of Inappropriate Anti-Diuretic Hormone secretion and Cerebral Salt Wasting), seizures, vasospasm leading to delayed ischaemic neurologic deficits, strokes and hydrocephalus. Availability of a dedicated neurovascular surgeon might have assisted in detecting these specific clinical parameters on a daily basis, and facilitated education and guidance of the junior team members and nursing staff in patient management.
Clipping of aneurysms was previously considered dangerous if done in the initial two weeks post-rupture. It was believed that the swollen brain and hostile intracranial environment would increase both the difficulty of surgery and the postoperative complication rate. This was thought to be especially true during the period of maximum vasospasm (days 4-14), and a popular practice was to postpone surgery until after this phase. 18,19However, a systematic review of a randomised controlled trial, as well as ten observational studies, found that early (days 0-3) and intermediate (days 4-7) surgery resulted in superior outcomes compared to late surgery. Building on this finding, a review of the patients undergoing aneurysm surgery in the ISAT study did not recommend postponing treatment during the vasospasm phase. Current evidence supports securing of the aneurysm as soon as possible.18,19 Our results show that the majority of patients would have been clipped within the first 14 days, which includes the peak vasospasm period, and had good outcomes.
The availability of an excellent neurosurgical microscope (OPMI-Pentero-Zeiss™) did immensely facilitate the surgical clipping of intracranial aneurysms at the study hospital. However, some items commonly found in high-resource settings that can enhance this procedure and thus improve the efficiency and safety profile, were not available. These include a neurosurgical chair, to promote surgeon ergonomics, which is critical in the performance of delicate microsurgical brain operations, and prevents mistakes due to fatigue/pain.20 A micro-doppler probe and indocyanine green are commonly used in neurosurgical centres, to confirm appropriate flow through the normal vessels and exclusion of flow in the aneurysm respectively. Papaverine can be applied to the vessels to reduce the degree of vasospasm and potential for intra/post-operative vasospasm and stroke. Haemostatic agents such as Tisseal/Surgiflo™ can be invaluable in arresting bleeding from vessels that cannot be cauterised (due to potential for creating infarction).
Post-haemorrhagic vasospasm is known to create significant morbidity and mortality in the form of ischaemic deficits/stroke in patients with ruptured aneurysms, and can account for up to 50% of deaths. 21 Nimodipine is a dihydropyridine agent that blocks voltage gated calcium channels, resulting in smooth muscle relaxation and vascular dilatation. It has been proven to reduce the incidence of aneurysmal post-haemorrhagic vasospasm. 21 In the study setting, there was varied availability based on existing local pharmaceutical supplies, therefore not every patient could have completed the recommended regimen of 21 days.
Ideally all ruptured aneurysm patients would be admitted to a high-dependency unit (HDU) or intensive care unit for continuous monitoring both pre- and post-operatively. One of the major benefits of this is blood pressure augmentation (inotropic support) in the vasospasm phase, to reduce the risk of ischaemic neurologic deficits. Due to limited bed availability in the study hospital, not all patients could be admitted pre-operatively. Fortunately, all patients went to the HDU postoperatively.
Time to operation varied significantly, and this was due to limited operating theatre time available in the study setting. In larger centres, there is usually a dedicated 24-hour neurosurgical emergency operating theatre, with separate elective operating theatres that run concomitantly during standard working-hours. In these settings, if a ruptured aneurysm is deemed worthy of clipping, it proceeds immediately to operating theatre. However, in the study hospital there is a single emergency theatre, shared by all surgical departments. Therefore, at any given time there can be major non-neurosurgical emergencies awaiting surgery. The decision as to which patient goes next is not easy, when multiple equally critically ill patients require intervention. This means that patients could experience delays (of days in some instances) while waiting for clipping to be done, and potentially re-bleed. In one patient, this resulted in a mortality. If the neurosurgical elective operating list (which is usually once a week) is nearer, then these patients would be clipped on the elective list, which may cause a domino effect on the other elective neurosurgical cases. This further adds to challenges in the neurosurgical service, as there is no capacity for dealing with a larger number of patients.
Additionally, the COVID-19 pandemic contributed to temporary suspension of elective operating lists, which created delays in getting patients to the operating theatre. 22 Our hope is that with the continued development of the service, these challenges will be addressed.
Other limitations included the lack of an electronic medical record system, which hindered the ease of access of complete patient files. In some cases, multiple volumes of patient charts were not always available. This also prevents creation of easily accessible databases, facilitating further research and development of management strategies for the local population.
Additionally, the COVID-19 pandemic led to changes in outpatient follow-up and prevented the standard face-to-face visits in many instances. Not all patients would have had their 3-month postoperative review.
In conclusion, this descriptive study demonstrates the characteristics and outcomes of surgical clipping of intracranial aneurysms by a single neurovascular surgeon. The overall outcomes were good despite limited resources, emphasising the necessity and importance of establishing and maintaining a dedicated neurovascular service.
Acknowledgements – none
Competing interests – none
Ethical approval – granted by Institutional Review Board
Funding – nil received
References
- Belavadi R, Gudigopuram SVR, Raguthu CC, Gajjela H, Kela I, Kakarala CL, et al. Surgical Clipping Versus Endovascular Coiling in the Management of Intracranial Aneurysms. Cureus. 2021;13(12).
- Loewenstein JE, Gayle SC, Duffis EJ, Prestigiacomo CJ, Gandhi CD. The natural history and treatment options for unruptured intracranial aneurysms. Int J Vasc Med. 2012;2012.
- Greenberg, Mark S. MD. Chapter 75 – Critical Care of Aneurysm Patients. In: Handbook of Neurosurgery. 9th ed. THIEME; 2020. p. 1230–50.
- Zhao J, Lin H, Summers R, Yang M, Cousins BG, Tsui J. Current Treatment Strategies for Intracranial Aneurysms: An Overview. Angiology [Internet]. 2017 Mar 30;69(1):17–30. Available from: https://doi.org/10.1177/0003319717700503
- Feb SG. Samuel Ghouralal [Internet]. 2017. p. 6437. Available from: http://icons.niherst.gov.tt/icon/samuel-ghouralal-tt2/
- Ghouralal S. Perspectives in International Neurosurgery: Neurosurgery in Trinidad, West Indies. Neurosurgery [Internet]. 1980 Jul 1;7(1):97–8. Available from: https://doi.org/10.1227/00006123-198007000-00016
- SWRHA. ABOUT SWRHA [Internet]. 2021. p. 2021. Available from: http://www.swrha.co.tt/content/about-swrha
- Hunt WE, Hess RM. Surgical Risk as Related to Time of Intervention in the Repair of Intracranial Aneurysms. J Neurosurg [Internet]. 1968;28(1):14–20. Available from: https://thejns.org/view/journals/j-neurosurg/28/1/article-p14.xml
- Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ESJ, et al. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery. 2006 Jul;59(1):21–7.
- Wilson L, Boase K, Nelson LD, Temkin NR, Giacino JT, Markowitz AJ, et al. A Manual for the Glasgow Outcome Scale-Extended Interview. J Neurotrauma. 2021 Sep;38(17):2435–46.
- Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: A randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and . Lancet. 2005;366(9488):809–17.
- Maud A, Lakshminarayan K, Suri MFK, Vazquez G, Lanzino G, Qureshi AI. Cost-effectiveness analysis of endovascular versus neurosurgical treatment for ruptured intracranial aneurysms in the United States. J Neurosurg. 2009 May;110(5):880–6.
- Zhang X, Li L, Hong B, Xu Y, Liu Y, Huang Q, et al. A Systematic Review and Meta-Analysis on Economic Comparison Between Endovascular Coiling Versus Neurosurgical Clipping for Ruptured Intracranial Aneurysms. World Neurosurg. 2018 May;113:269–75.
- Hoh BL, Chi Y-Y, Lawson MF, Mocco J, Barker FG 2nd. Length of stay and total hospital charges of clipping versus coiling for ruptured and unruptured adult cerebral aneurysms in the Nationwide Inpatient Sample database 2002 to 2006. Stroke. 2010 Feb;41(2):337–42.
- Calviere L, Gathier CS, Rafiq M, Koopman I, Rousseau V, Raposo N, et al. Rebleeding After Aneurysmal Subarachnoid Hemorrhage in Two Centers Using Different Blood Pressure Management Strategies [Internet]. Vol. 13, Frontiers in Neurology . 2022. Available from: https://www.frontiersin.org/articles/10.3389/fneur.2022.836268
- Hsu C-E, Lin T-K, Lee M-H, Lee S-T, Chang C-N, Lin C-L, et al. The Impact of Surgical Experience on Major Intraoperative Aneurysm Rupture and Their Consequences on Outcome: A Multivariate Analysis of 538 Microsurgical Clipping Cases. PLoS One. 2016;11(3):e0151805.
- Boogaarts HD, van Amerongen MJ, de Vries J, Westert GP, Verbeek ALM, Grotenhuis JA, et al. Caseload as a factor for outcome in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Neurosurg. 2014 Mar;120(3):605–11.
- Taha MM, Alawamry A, Abdelbary TH. Outcome of microsurgical clipping of anterior circulation aneurysms during the period of vasospasm: single center experience in Egypt. Egypt J Neurosurg. 2019;34(1).
- Dorhout Mees SM, Molyneux AJ, Kerr RS, Algra A, Rinkel GJE. Timing of aneurysm treatment after subarachnoid hemorrhage: Relationship with delayed cerebral ischemia and poor outcome. Stroke. 2012;43(8):2126–9.
- Gadjradj PS, Ogenio K, Voigt I, Harhangi BS. Ergonomics and Related Physical Symptoms Among Neurosurgeons. World Neurosurg. 2020 Feb;134:e432–41.
- Liu YF, Qiu HC, Su J, Jiang WJ. Drug treatment of cerebral vasospasm after subarachnoid hemorrhage following aneurysms. Chinese Neurosurg J [Internet]. 2016;2(1):1–8. Available from: http://dx.doi.org/10.1186/s41016-016-0023-x
- Seetahal-Maraj P, Arjoon SR, Ramnarine N, Thomas D, St Louis P. The Impact of COVID-19 on the Functioning of a Neurosurgical Service at a Tertiary Institute in a Low-Resource Setting. Cureus. 2022;14(2):10–4.