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Arquivos de Neuro-Psiquiatria

Print version ISSN 0004-282XOn-line version ISSN 1678-4227

Arq. Neuro-Psiquiatr. vol.74 no.6 São Paulo June 2016

http://dx.doi.org/10.1590/0004-282x20160064 

ARTICLES

Clinical outcomes of surgical clipping for intracranial aneurysms in patients with a Hunt and Hess grade 4 or 5

Desfechos clínicos da clipagem cirúrgica de aneurismas intracranianos de graus 4 e 5 segundo a escala de Hunt & Hess

Yang Zhang1 

Xiaobo Zhu1 

Kun Hou1 

Jinchuan Zhao1 

Xianfeng Gao1 

Yang Sun1 

Wei Wang1 

Xiaona Zhang2 

1The First Affiliated Hospital of Jilin University, Department of Neurosurgery, Changchun, Jilin, China

2The First Affiliated Hospital of Jilin University, Department of Anesthesiology, Changchun, Jilin, China.

ABSTRACT

We retrospectively evaluated the records of 49 grade 4 and 5 patients with 42 intracranial aneurysms treated within 72 h of subarachnoid hemorrhage (SAH). In total, 35 patients (71%) were grade 4, and 14 (29%) were grade 5. A total of 42 (85%) patients had one aneurysm, 6 (12%) had two aneurysms, and 1 (3%) had three aneurysms. Out of 49 patients, one technical (2%) and one clinical (2%) complication occurred at surgery. Twenty-one (43%) patients recovered well, including 7 with postoperative hematoma requiring an immediate evacuation of a clot. Fourteen (29%) patients had hydrocephalus and required a ventriculo-peritoneal shunt; 12 patients underwent tracheotomy postoperatively due to coma and pulmonary infection. We found that patients with Hunt and Hess grade 4 and 5 aneurysms can undergo successful neurosurgical clipping of the aneurysms after SAH. However, the morbidity and mortality rates remain high because of their poor clinical condition and a high incidence of vasospasm during treatment.

Key words: cerebral aneurysm; surgical instruments; subarachnoid hemorrhage

RESUMO

Avaliamos retrospectivamente os registros de 49 pacientes com 42 aneurismas intracranianos de graus 4 e 5, tratados nas primeiras 72 horas após uma hemorragia subaracnóidea (HSA). Trinta e cinco pacientes (71%) apresentavam grau 4 e catorze (29%) grau 5. Quarenta e dois pacientes (85%) tinham um único aneurisma, seis (12%) tinham dois aneurismas, e um paciente (3%) tinha três aneurismas. Dos 49 pacientes, uma complicação técnica (2%) e uma complicação clínica (2%) ocorreram durante a cirurgia. Vinte e um pacientes (43%) recuperaram-se bem, incluindo sete que tiveram hematomas pós-operatórios que requereram a imediata evacuação do coágulo. Catorze pacientes (29%) tiveram hidrocefalia e submeteram-se à derivação ventrículo-peritoneal; doze pacientes submeteram-se à traqueostomia no pós-operatório, devido a coma e infecção pulmonar. Pacientes com aneurismas de graus 4 e 5, segundo a escala de Hunt & Hess podem submeter-se com sucesso à clipagem dos aneurismas após HSA. Entretanto, as taxas de morbidade e mortalidade ainda são altas, devido à condição clínica precária e à alta incidência de vasoespasmo durante o tratamento.

Palavras-Chave: aneurisma cerebral; instrumentos cirúrgicos; hemorragia subaracnóidea

The management of subarachnoid hemorrhage (SAH), which becomes more likely with advancing age, is a clinical challenge. Despite modern microsurgical techniques and intensive care medicine, there remains high morbidity and mortality resulting from SAH, generally caused by a ruptured aneurysm of the intracranial arteries1. It is generally accepted that the patient’s outcome correlates with their preoperative clinical status. Therefore, it is very important to make early an diagnosis for the endangered patient and to perform the operation when the patient’s physical condition is good to improve the outcome. Most aneurysmal SAH patients frequently present with sudden severe headache accompanied by photophobiameningism, nausea, and loss of consciousness2.

Historically, patients with severe Hunt and Hess grades (4 and 5) have fared poorly and generally consist of approximately 20–30% of those admitted to the hospital with aneurysmal SAH. There is a controversy regarding the timing of surgery, which has a significant impact on the prognosis3,4.

In a previously published retrospective review, patients with Hunt and Hess grade 4 or 5 after SAH experienced successful coil embolization of the aneurysms5. Early case reports emphasized that the surgery for grade 4 and 5 patients should be delayed until their clinical condition improves from grades 1 to 3. This treatment mode produced a favorable result in 3.8–18% of cases, with a mortality rate of 68–87.4%. Later in early 1990s, several clinical reports indicated that early aggressive medical and surgical treatment could lead to better outcomes, with success rates that ranged from 7% to 42.6%3,4,6,7.

With hundreds of varieties of aneurysm clips in different shapes and sizes, surgical clipping has been the gold standard for the treatment of both ruptured and unruptured cerebral aneurysms since the 1960s due to the the mechanical complexity of existing clips as well as the emergence of the operating microscope. However, it remains an invasive and technically challenging procedure8,9. The aim of this study was to evaluate the clinical outcome of neurosurgical clipping (NSC) in patients with Hunt and Hess grade 4 or 5 after SAH.

METHOD

We performed a retrospective review of the records of 49 patients with a Hunt and Hess grade 4 or 5 between June 2005 and January 2011 and who were treated with neurosurgery clipping at our institution. The patients included 35 males and 14 females who were 31–82 [average (56.6±25.2)] years old. Eligible SAH patients had a ruptured aneurysm suitable for NSC. All patients were evaluated by a combined neurosurgery and interventional neuroradiology team and treated within 72h of the onset of SAH. For each patient, the following data were analyzed: age, sex, and clinical status according to the Hunt and Hess grading scale. A transfemoral selective four-vessel cerebral angiography was used to identify the localization of the ruptured aneurysm.

All procedures were performed with the patient under general anesthesia and with neurophysiologic monitoring using somatosensory evoked potentials and electroencephalographic monitoring. All patients were treated with surgical clipping within 24h after head computed tomography angiography (CTA) examination. For multiple aneurysms, the most likely aneurysm to have bled was identified on the basis of CT and angiographic images. If the most likely bleeding aneurysm could not be identified, we chose NSC as the treatment for more than one aneurysm.

During the procedure, the following complications were checked: preoperative hemorrhage, intra-operative rupture of the aneurysm, symptomatic vasospasm, hydrocephalus requiring the implantation of a shunt, ventriculitis, postoperative wound infection, and re-bleeding. The outcome was examined according to the Glasgow outcome scale at the time of discharge and during the follow-up period. After 30 days, surviving patients were followed for up to 23 months on an average (range: 6–44 months).

RESULTS

The patient and aneurysm characteristics are outlined in Table 1. From a total of 49 cases of 57 aneurysms, 55 aneurysms were treated. Seven cases had more than one aneurysm. The Hunt and Hess grade at admission was 1–3 in 33% of the cases and changed to grade 4 or 5 because the aneurysms ruptured during examination. There were 35 cases of grade 4 and 14 cases of grade 5. One SAH case was found without aneurysm after two head screw CTA examinations initially, but was confirmed with one aneurysm 1 month after the head CTA.

Table 1 Characteristics of surgical patients. 

Variable n
Total 49
Male 35
Female 14
Average Age 56.6±25.2
GOS Grade
IV 35
V 14
Aneurysm
1 42
>1 7
Aneurysm location
anterior communicating artery 21
middle cerebral artery 17
posterior communicating artery 17
anterior cerebral artery 2

Surgical clipping of the ruptured aneurysms was performed in 37 patients after external ventricular drainage. Four patients having two aneurysms each underwent clipping in one side initially, and then underwent a secondary clipping of the other aneurysm after a good recovery. One patient had three aneurysms and abandoned further treatment after the first clipping surgery failed on one side. Twenty-one patients recovered well, including 7 cases with postoperative hematoma requiring an immediate evacuation of the clot; 13 cases had acceptable recovery; 14 cases were complicated with hydrocephalus and underwent a ventriculo-peritoneal shunt procedure; and 15 cases had poor recovery. Postoperatively, 12 cases underwent tracheotomy due to coma and pulmonary infection.

For an aneurysm patient with SAH, the length of hospitalization and recovery are determined by the severity of the hemorrhage but not by the treatment modality. Most SAH patients will remain hospitalized for a minimum of 2 weeks to monitor the risk of cerebral vasospasm and other complications due to the hemorrhage, including hydrocephalus. Treatment on an inpatient or outpatient basis, with a varied rehabilitation period, may be necessary. Postoperative re-bleeding of a clipped aneurysm occurred once, leading to a poor outcome. Age, surgery, Hunt and Hess grade, re-bleeding, and other factors related to prognosis are analyzed in Table 2.

Table 2 The prognosis analysis. 

Variable Number of patients Prognosis

Good Bad
Age
< 60y 18 14 4
≥ 60y 10 4 6
Hunt-Hess grade
IV 16 10 6
V 12 8 4
Rebleeding (24h)
Yes 18 9 9
No 10 9 1
Complication
Hypertension 14 8 6
Hemorrhage 16 10 6

DISCUSSION

In this report, 49 patients in our hospital were analyzed to identify the clinical outcome and complications for neurosurgical clipping treatment. The findings of the present study can be generalized to elderly patients similar to those enrolled, i.e., patients with a good Hunt and Hess grade who have a ruptured anterior circulation aneurysm with a suitable anatomy for NSC10. Complications particularly related to NSC include stroke, vasospasm, seizure, and bleeding.

Previous studies have shown that early neurosurgical aneurysm treatment is inappropriate in elderly patients with a poor Hunt and Hess grade; moreover, in many centers, conservative treatment has been advocated for patients > 60 years. At present, the neurosurgical treatment of a ruptured aneurysm would be considered, even in elderly patients (> 80 years old), if their prior physical condition and life quality were good. Nevertheless, elderly SAH patients have a greater risk of poor outcomes than younger patients11,12,13. We confirmed that the reasons that the elderly patients have a poorer prognosis are that they have less active management, poorer clinical grades on admission, and a higher frequency of comorbidity. In addition, patients > 50 years tolerate craniotomy and clipping of intracranial aneurysms less well.

The clinical outlook also depends on whether any brain damage occurred from bleeding pre-, intra-, or postoperatively14,15,16. Brain aneurysm with no symptoms can usually be prevented from becoming larger and rupturing by treating with open surgery or endovascular repair. A highly feared intra-procedural complication during neurosurgical clipping of an intracranial aneurysm is aneurysm rupture and re-bleeding, which is associated with less favorable outcomes. Here, the aneurysmal re-bleeding rate during treatment was 64%, and there was a statistically significant relationship between re-bleeding and early surgery treatment17. The prognosis rate was 50% for the non-re-bleeding group and even better (90%) for the non-re-rupturing group. The patient’s clinical outcome is often related to the location of the ruptured aneurysm. When patients were broken down into groups in terms of right- or left-sided aneurysms, aneurysm neck size, lumen diameter, WFNS or Fisher grade, and patient age, previous studies have revealed that there is no difference in outcome between the treatment groups. However, because of the limited number of patients with ruptured aneurysms, these results must be interpreted with caution. Further studies and additional follow-up are warranted to document its efficacy and safety.

The patients who underwent NSC were more likely to suffer infections and pulmonary complications, particularly those patients who had prolonged bed rest, artificial ventilation, and an increased length of intensive care unit stay16,17,18,19. Furthermore, it was reported that out of 159 Hunt and Hess 4–5 grade patients (44%) that had intracranial hematoma, the prognosis for the majority of Hunt and Hess grade 4 patients improved (53.9%), in contrast to 24.1% of Hunt and Hess grade 5 patients. Early surgical intervention is highly recommended for patients with intracranial hematoma. In our study, 37 patients underwent intraventricular penetrating, ventricular drainage, and decompressive craniectomy to control intracranial pressure and cerebral perfusion before aneurysm surgery, which improved the overall prognosis rate (55%). Previous literature has also reported that high blood pressure can be an independent factor affecting the prognosis of high-grade aneurysms; however, our results were not statistically significant.

In summary, in our study, although the patients with Hunt and Hess grade 4 or 5 after SAH have a poor medical condition and a high risk of vasospasm during treatment, they can still undergo successful neurosurgical clipping. Microsurgical techniques and the prevention of cerebral vasospasm might be the key to success for early aneurysm surgery.

References

1. Sacco RL, Wolf PA, Bharucha NE, Meeks SL, Kannel WB, Charette LJ et al. Subarachnoid and intracerebral hemorrhage: natural history, prognosis, and precursive factors in the Framingham Study. Neurology. 1984;34(7):847-54. doi:10.1212/WNL.34.7.847 [ Links ]

2. Fortuny LA, Adams CB, Briggs M. Surgical mortality in an aneurysm population: effects of age, blood pressure and preoperative neurological state. J Neurol Neurosurg Psychiatry. 1980;43:879-82. doi:10.1136/jnnp.43.10.879 [ Links ]

3. Kassell NF, Torner JC, Haley E Jr, Jane JA, Adams HP, Kongable GL. The international cooperative study on the timing of aneurysm surgery: Part 1: overall management results. J Neurosurg. 1990;73(1):18-36. doi:10.3171/jns.1990.73.1.0018 [ Links ]

4. Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP. The International cooperative study on the timing of aneurysm surgery: Part 2: surgical results. J Neurosurg. 1990;73(1):37-47. doi:10.3171/jns.1990.73.1.0037 [ Links ]

5. Weir RU, Marcellus ML, Do HM, Steinberg GK, Marks MP. Aneurysmal subarachnoid hemorrhage in patients with Hunt and Hess grade 4 or 5: treatment using the Guglielmi detachable coil system. AJNR Am J Neuroradiol. 2003;24(4):585-90. [ Links ]

6. Sengupta RP, Lassman LP, Hankinson J. Scope of surgery for intracranial aneurysm in the elderly: a preliminary report. BMJ. 1978;2(6132): 246-7. doi:10.1136/bmj.2.6132.246 [ Links ]

7. Ross N, Hutchinson PJ, Seeley H, Kirkpatrick PJ. Timing of surgery for supratentorial aneurysmal subarachnoid haemorrhage: report of a prospective study. J Neurol Neurosurg Psychiatry. 2002;72:480-4. [ Links ]

8. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28(1):14-20. doi:10.3171/jns.1968.28.1.0014 [ Links ]

9. Gillingham FJ. The management of ruptured intracranial aneurysms. Scott Med J. 1967;12(10):377-83. [ Links ]

10. Alaraj A, Charbel FT, Amin-Hanjani S. Peri-operative measures for treatment and prevention of cerebral vasospasm following subarachnoid hemorrhage. Neurol Res. 2009;31(6):651-9. doi:10.1179/174313209X382395 [ Links ]

11. Ellenbogen BK. Subarachnoid haemorrhage in the elderly. Gerontol Clin (Basel). 1970;12:115-20. doi:10.1159/000245269 [ Links ]

12. Hugosson R. Intracranial arterial aneurysms. Considerations on the upper age limit for surgical treatment. Acta Neurochir (Wien). 1973;28(3):157-64. doi:10.1007/BF01432227 [ Links ]

13. Rosenørn J, Eskesen V, Schmidt K. Age as a prognostic factor after intracranial aneurysm rupture. Br J Neurosurg. 1987;1(3):335-41. doi:10.3109/02688698709023775 [ Links ]

14. Jennett B, Bond M. Assessment of outcome after severe brain damage: a practical scale. Lancet. 1975;1(7905): 480-4. doi:10.1016/S0140-6736(75)92830-5 [ Links ]

15. Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR. Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg. 1996;85(1):39-49. doi:10.3171/jns.1996.85.1.0039 [ Links ]

16. Duke BJ, Kindt GW, Breeze RE. Outcome after urgent surgery for grade IV subarachnoid hemorrhage. Surg Neurol. 1998;50(2):169-72. doi:10.1016/S0090-3019(97)00449-7 [ Links ]

17. Edner G, Ronne-Engström E. Can early admission reduce aneurysmal rebleeds? A prospective study on aneurysmal incidence, aneurysmal rebleeds, admission and treatment delays in a defined region. Br J Neurosurg. 1991;5(6):601-8. doi:10.3109/02688699109002883 [ Links ]

18. Hijdra A, Gijn J, Nagelkerke NJ, Vermeulen M, Crevel H. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke. 1988;19(10):1250-6. doi:10.1161/01.STR.19.10.1250 [ Links ]

19. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6(1):1-9. doi:10.1227/00006123-198001000-00001 [ Links ]

Received: January 03, 2016; Accepted: February 01, 2016

Correspondence: Xiaona Zhang; Department of Anesthesiology, The First Affiliated Hospital of Jilin University; 71 Xinmin Avenue, Changchun, Jilin, China; E-mail: zhang.xiaona@yahoo.com

Conflict of interest: There is no conflict of interest to declare.

Creative Commons License  This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.