Abstract
Objective: This research was designed to investigate the effects of craniotomy clipping and interventional embolization (IE) on the treatment efficacy, cognitive function and recovery of patients with subarachnoid hemorrhage (SAH). Methods: A total of 148 patients with aneurysmal subarachnoid hemorrhage (ASAH) who underwent surgery in our hospital from December 2017 to August 2019 were included. They were divided into the clipping group (CG) (68 cases) and intervention group (IG) (80 cases) according to different surgical methods. The former received craniotomy clipping, and the latter underwent IE. The postoperative clinical indexes of patients were observed. The immune function (IgG, IgM, IgA) and inflammatory indexes (TNF-α, IL-8, HS-CRP) were detected before and after operation. The improvement of cognitive function, neurological function and sleep quality before and after operation was evaluated. Three months after operation, the treatment efficacy was evaluated and the postoperative complications were recorded. Results: The time of operation and hospitalization of patients in the IG were dramatically less than those in the CG (P < 0.05). The levels of IgG, IgM and IgA in the IG were higher than those in the CG after operation, while those of TNF-α, IL-8 and hs-CRP in the IG were lower than those in the CG. The MOCA scores of patients in the IG were obviously higher than those in the CG (P < 0.05), and the NIHSS and PSQI scores of patients in the IG were markedly lower than those in the CG. The total effective rate of patients in the IG was remarkably higher than that in the CG (P < 0.05), while the total incidence of postoperative complications in the IG was markedly lower than that in the CG. Conclusion: IE is effective in the treatment of SAH patients, reducing the damage of immune, cognitive and nerve functions, with a high efficacy.
Keywords: Craniotomy clipping, interventional embolization, subarachnoid hemorrhage, cognitive function
Introduction
Subarachnoid hemorrhage (SAH) is the rupture of blood vessels caused by various reasons, making blood flow directly into the subarachnoid space and causing acute cerebrovascular issues; while cerebral hemorrhage is caused by rupture of an intracranial aneurysm and is the most common type [1]. It often leads to neurological dysfunction after relapse. In severe cases, patients will also suffer from cerebral hemorrhage, with high disability and mortality rates [2]. Clinically, aneurysmal subarachnoid hemorrhage (ASAH) may also cause cognitive decline, delayed cerebral ischemia and cerebral vasospasm [3]. Therefore, it is particularly important to carry out active and effective treatment.
Surgical treatment of ASAH is widely used in clinical practice [4]. Craniotomy clipping can effectively reduce the intracranial pressure of patients, effectively clear hematomas under direct vision, open subarachnoid space, release cerebrospinal fluid, prevent cerebrospinal fluid retention, and promote circulation. However, it has been shown that this kind of operation has great impact on patients, and its surgical wounds easily cause various complications, which is not conducive to later recovery [5,6] Thus, in this research, ASAH was intervened with interventional embolization (IE). Vascular IE is a controlled injection of ‘plugs’ into the supply vessels of diseased organs through arterial or intravenous catheters, causing occlusion and interruption of blood supply, so as to control bleeding, treat tumors and vascular diseases and prohibit the function of diseased organs [7]. It has also been shown [8] in that IE, that by using a separable coil, is a very popular way to blocking aneurysms, which can reduce the re-bleeding rate. For example, Bae IS et al. [9] confirmed that for patients with un-ruptured intracranial aneurysms, endovascular coil embolization could effectively reduce postoperative complications, improve the success rate of clinical treatment and obtain higher patient satisfaction. Another study has shown that [10] it is safe to provide patients with intracranial aneurysms a catheter embolization device. No major deaths or stroke in the nervous system occurred one year after operation, and the incidence of complete occlusion was also low.
The ASAH patients were given craniotomy clipping and IE, and their effects on postoperative clinical symptoms, cognitive function and recovery were analyzed, aiming to provide a feasible treatment plan.
Materials and methods
General data
A total of 148 ASAH patients treated in our hospital from December, 2017 to August, 2019 were included. Based on different surgical methods, they were divided into a clipping group (CG) (68 cases) and an interventional group (IG) (80 cases). Inclusion criteria were as follows: intracranial SAH confirmed by head CT and intracranial aneurysm confirmed by cerebral angiography [11]; general clinical data were complete, all cases were first onset; those who saw a doctor within 3 hours after onset; circumstances where craniotomy was unnecessary. This research was approved by the Ethics Committee of our hospital. All patients and their families were informed in advance, and a complete informed consent form was signed. Exclusion criteria were as follows: unable to tolerate surgery; complicated with infectious diseases; accompanied by other malignant diseases; preoperative hydrocephalus; obvious increased intracranial pressure; pregnant women; those who quit the experiment halfway; past history of mental illness; there was serious coagulation dysfunction or liver and kidney function damage; those who were lost to follow up.
Surgical methods
CG: patients received craniotomy clipping, pterion was taken as the surgical approach, and the appropriate arterial clip was selected in the light of aneurysm size. Afterwards, the blood accumulated in the visual field was observed by microscope, and diluted papaverine solution was given afterwards to prevent cerebral vasospasm, and then the bone flap was removed to achieve decompression effect. Finally, the drainage tube was inserted, and the operation was finished. Routine treatment was given after operation, and the vital signs were closely monitored.
IE was performed in the IG: the location, neck width, size, and the relationship between the perforator vessel and tumor body were determined by cerebral angiography. After general anesthesia, patients were punctured in their femoral artery, and the catheter was placed into the tumor-bearing artery under the guidance of digital radiography, and then the microcatheter was sent into the aneurysm. It is necessary to ensure the position of the microcatheter tip, and then put the embolic material (spring coil matching the tumor size). After the spring coil was coiled properly, it was released, and repeated radiography made sure whether the spring coil was stable. The tumor capsule was no longer developed, and the coil was put in and stopped after receiving a certain resistance. The related catheter was withdrawn under fluoroscopy, and the operation ended. After embolization, it was decided whether to perform lumbar puncture or lumbar cistern drainage in the light of the condition of patients. Subsequently, the puncture site was compressed and held for 24 h. Routine treatment was given after operation, and the vital signs were closely monitored.
Outcome measures
1. The postoperative clinical indexes (time of operation and hospitalization) of patients were observed.
2. Detection of immune and inflammatory indicators: before and after operation, 5 mL venous blood was collected and stored in a freezer at -70°C. For detection it was thawed and centrifuged at 1500× Xg for 10 min to separate the serum. The expression of the indexes of immunoglobulin G (IgG), immunoglobulin M (IgM), immunoglobulin A (IgA), tumor necrosis factor-α (TNF-α), interleukin-8 (IL-8) and high-sensitivity C-reactive protein (hs-CRP) were detected by enzyme-linked immunosorbent assay (ELISA) [12] in view of the instructions (Shanghai Blue Gene Biotechnology Co., Ltd., China).
3. Cognitive function: the cognitive function before and after operation was evaluated by the Montreal Cognitive Assessment Scale (MoCA) [13]. The scale mainly included six dimensions: language, abstraction, attention, visual space and executive ability, naming and delayed recall. The total score of the scale was 30 points, and the higher the score, the higher the cognitive function of the patient was.
4. Neurological function: the neurological function before and after operation [14] was evaluated by the National Institutes of Health Stroke Scale (NIHSS). There were 15 items in the scale, 42 points in total. The final score of patients was counted. The lower the score, the better the neurological function after nursing intervention was.
5. Sleep quality: it was assessed by Pittsburgh Sleep Quality Index (PSQI) [15], which had 7 dimensions and scores ranging from 0 to 21. The higher the score after evaluation, the worse the sleep quality of patients was.
6. Clinical efficacy: Glasgow Outcome Scale (GOS) [16] was performed 3 months after operation. It was divided into 5 dimensions, with a 5-point system. One point was death; 2 points was a vegetative state that patients only blinked, sucked and breathed spontaneously after operation; 3 was severe disability: patients were conscious; they completely lost the ability to exercise and feel, could not take care of themselves in daily life, and needed care; 4 was mild disability: patients still had mild hemiplegia, ataxia or nerve paralysis, but they could live independently and work under protection; 5 means good recovery: patients had mild defects but did not affect normal life and social activities; the scoring criteria of 4-5 points denote good prognosis; 1-3 bad prognosis; the good prognosis rate = (GOS score 4-5 points)/total cases × 100%.
7. The occurrence of postoperative complications was observed and recorded.
Statistical methods
SPSS 22.0 (Beijing Baiao Yijie Technology Co., Ltd., China) was used for statistical analysis. The intra-group counting data were expressed as number/percentage [n (%)], and the inter-group comparison was analyzed by Chi-square test. When the theoretical frequency was less than 5, continuous correction Chi-square test was put into use. The measurement data were expressed by mean ± standard deviation (mean ± SD), and the intra-group comparison before and after treatment was compared by independent-samples t test. P < 0.05 was considered to be statistically remarkable.
Results
General data
There was no marked difference in the general clinical data such as gender, average age, body mass index (BMI), aneurysm size and location, Fisher grade of bleeding, place of residence, nationality, education background, and history of smoking and drinking between the two groups (P > 0.05) (Table 1).
Table 1.
Comparison of general data between both groups [n (%)]/(mean ± SD)
| Classification | Clipping group (n=68) | Intervention group (n=80) | t/χ2 value | P value |
|---|---|---|---|---|
| Gender | 0.184 | 0.668 | ||
| Male | 35 (51.47) | 44 (55.00) | ||
| Female | 33 (48.53) | 36 (45.00) | ||
| Average age (years) | 56.43±4.54 | 56.74±3.43 | 0.473 | 0.637 |
| BMI (kg/m2) | 22.79±1.23 | 23.08±1.26 | 1.411 | 0.161 |
| Aneurysm size (mm) | 15.43±1.37 | 15.84±1.39 | 1.800 | 0.739 |
| Aneurysm location | 0.383 | 0.943 | ||
| Anterior communicating and anterior cerebral artery | 19 (27.94) | 26 (32.50) | ||
| Posterior communicating artery | 17 (25.00) | 19 (23.75) | ||
| Middle cerebral artery | 15 (22.06) | 17 (21.25) | ||
| Posterior circulation | 17 (25.00) | 18 (22.50) | ||
| Fisher grading of bleeding | 1.929 | 0.381 | ||
| Grade I | 11 (16.18) | 20 (25.00) | ||
| Grade II | 28 (41.18) | 27 (33.75) | ||
| Grade III | 29 (42.65) | 33 (41.25) | ||
| Place of residence | 0.169 | 0.680 | ||
| Cities and towns | 38 (55.88) | 42 (52.50) | ||
| Countryside | 30 (44.12) | 38 (47.50) | ||
| Nationality | 0.090 | 0.763 | ||
| Han | 40 (58.82) | 49 (61.25) | ||
| Ethnic minorities | 28 (41.18) | 31 (38.75) | ||
| Education background | 0.310 | 0.577 | ||
| ≥ high school | 43 (63.24) | 47 (58.75) | ||
| < high school | 25 (36.76) | 33 (41.25) | ||
| History of smoking | 0.193 | 0.660 | ||
| Yes | 39 (57.35) | 43 (53.75) | ||
| No | 29 (42.65) | 37 (46.25) | ||
| History of drinking | 0.147 | 0.701 | ||
| Yes | 37 (54.41) | 41 (51.25) | ||
| No | 31 (45.59) | 39 (48.75) |
Comparison of postoperative clinical indexes between patients
After observing the clinical indexes of both groups, we found that the time of operation and hospitalization of the IG were obviously less than those of the CG, and the difference was statistically marked (P < 0.05) (Table 2).
Table 2.
Comparison of postoperative clinical indexes between both groups (mean ± SD)
| Group | n | Operation time (min) | Hospital stay (d) |
|---|---|---|---|
| Clipping group | 68 | 156.37±14.62 | 22.07±2.48 |
| Intervention group | 80 | 91.32±9.04 | 15.74±1.63 |
| t | - | 33.060 | 18.590 |
| P | - | < 0.001 | < 0.001 |
Comparison of immune function indexes between patients before and after surgery
The immune function indexes before and after surgery were observed. There was no obvious difference in the levels of IgG, IgM and IgA before operation (P > 0.05), but after operation, the three levels decreased, and the levels in the IG were all higher than those in the CG (P < 0.05), with statistically marked difference (Figure 1).
Figure 1.

Comparison of immune function indexes between both groups of patients before and after surgery. A. There is no difference in preoperative IgG level between the two groups, but the postoperative level in the intervention group is significantly higher than that in the clipping group. B. There is no difference in preoperative IgM level between the two groups, but the postoperative level in the intervention group is significantly higher than that in the clipping group. C. There is no difference in preoperative IgA level between the two groups, but the postoperative level in the intervention group is significantly higher than that in the clipping group. Note: * < 0.05 compared with before surgery and ** < 0.01 compared with both groups.
Comparison of inflammatory factor indexes between both groups before and after surgery
The inflammatory indexes before and after surgery were observed. The levels of TNF-α, IL-8 and hs-CRP before surgery were not obviously different (P > 0.05), but after surgery, the three levels decreased, and the levels in the IG were lower than those in the CG, with statistically marked difference (P < 0.05) (Figure 2).
Figure 2.

Comparison of inflammatory factor indexes between both groups of patients before and after surgery. A. There is no difference in the TNF-α level between the two groups before surgery, but the level in the intervention group is significantly lower than that in the clipping group after surgery. B. There is no difference in the IL-8 level between the two groups before surgery, but the level in the intervention group is significantly lower than that in the clipping group after surgery. C. There is no difference in the hs-CRP level between the two groups before surgery, but the level in the intervention group is significantly lower than that in the clipping group after surgery. Note: * < 0.05 compared with before surgery and ** < 0.01 compared with both groups.
Comparison of MOCA scores between both groups of patients before and after surgery
The MOCA scores before and after surgery were observed. There was no marked difference in the scores before surgery (P > 0.05), but after surgery, the MOCA scores increased, and the scores in the IG were dramatically higher than those in the CG, with statistically remarkable difference (P < 0.05) (Table 3).
Table 3.
Comparison of MOCA scores between both groups of patients before and after surgery (mean ± SD)
| Group | n | Language | Abstract | Attention | |||
|
|
|
|
|||||
| Before surgery | After surgery | Before surgery | After surgery | Before surgery | After surgery | ||
|
| |||||||
| Clipping group | 68 | 1.97±0.18 | 3.46±0.22 | 2.48±0.16 | 3.48±0.24 | 2.38±0.15 | 3.62±0.19 |
| Intervention group | 80 | 2.01±0.19 | 4.08±0.21 | 2.51±0.17 | 4.05±0.26 | 2.41±0.17 | 4.22±0.23 |
| t | - | 1.307 | 17.510 | 1.099 | 13.770 | 1.129 | 17.110 |
| P | - | 0.193 | < 0.001 | 0.273 | < 0.001 | 0.261 | < 0.001 |
|
| |||||||
| Visual space and executive ability | Name | Delayed recall | Total score of scale | ||||
|
|
|
|
|
||||
| Before surgery | After surgery | Before surgery | After surgery | Before surgery | After surgery | Before surgery | After surgery |
|
| |||||||
| 2.76±0.24 | 3.50±0.26 | 2.86±0.18 | 3.42±0.24 | 2.76±0.25 | 3.58±0.25 | 15.72±1.18 | 21.06±1.98 |
| 2.78±0.23 | 4.12±0.27 | 2.88±0.21 | 3.87±0.26 | 2.74±0.22 | 4.19±0.29 | 15.43±1.05 | 24.53±2.01 |
| 0.516 | 14.160 | 0.616 | 10.870 | 0.517 | 13.580 | 1.582 | 10.540 |
| 0.606 | < 0.001 | 0.538 | < 0.001 | 0.605 | < 0.001 | 0.115 | < 0.001 |
Comparison of NIHSS scores between both groups of patients before and after surgery
The NIHSS scores of the two groups were observed before and after surgery. There was no remarkable difference before surgery (P > 0.05), but after operation, the NIHSS scores decreased, and the scores of the IG were markedly lower than those of the CG (P < 0.05) (Table 4).
Table 4.
Comparison of NIHSS scores between both groups of patients before and after surgery (mean ± SD)
| Group | n | NIHSS score | |
|---|---|---|---|
|
| |||
| Before surgery | After surgery | ||
| Clipping group | 68 | 28.35±2.16 | 17.34±1.54 |
| Intervention group | 80 | 28.56±2.21 | 14.02±1.31 |
| t | - | 0.582 | 14.170 |
| P | - | 0.561 | < 0.001 |
Comparison of PSQI scores between both groups of patients before and after surgery
The PSQI scores before and after surgery were observed. There was no marked difference before surgery (P > 0.05), but after surgery, the PSQI scores decreased, and the scores of the IG were remarkably lower than those of the CG, with statistical significance (P < 0.05) (Table 5).
Table 5.
Comparison of PSQI scores between both groups of patients before and after surgery (mean ± SD)
| Group | n | PSQI score | |
|---|---|---|---|
|
| |||
| Before surgery | After surgery | ||
| Clipping group | 68 | 14.34±1.58 | 8.76±0.85 |
| Intervention group | 80 | 14.27±1.73 | 6.23±0.79 |
| t | - | 0.255 | 18.750 |
| P | - | 0.798 | < 0.001 |
Comparison of GOS scores of postoperative clinical efficacy between both groups of patients
The total effective rate was 95.00% in the IG and 85.29% in the CG. It showed that the total effective rate of patients in the IG was dramatically higher than that in the CG, and the difference was statistically marked (P < 0.05) (Table 6).
Table 6.
Comparison of GOS scores of postoperative clinical efficacy between both groups [n (%)]
| Group | n | Recover well | Mild disability | Severe disability | Vegetative state | Death | Total efficacy (%) |
|---|---|---|---|---|---|---|---|
| Clipping group | 68 | 21 (30.88) | 37 (54.41) | 4 (5.88) | 4 (5.88) | 3 (4.41) | 58 (85.29) |
| Intervention group | 80 | 47 (58.75) | 29 (36.25) | 2 (2.50) | 1 (1.25) | 1 (1.25) | 76 (95.00) |
| χ2 | - | 11.491 | 4.907 | 1.081 | 2.416 | 1.397 | 4.043 |
| P | - | 0.001 | 0.026 | 0.298 | 0.120 | 0.237 | 0.044 |
Comparison of postoperative complications between both groups of patients
The postoperative complications were observed. The total incidence of postoperative complications was 7.50% in the IG and 22.06% in the CG. It manifested that the total incidence of postoperative complications in the IG was markedly lower than that in the CG, and the difference was statistically remarkable (P < 0.05) (Table 7).
Table 7.
Comparison of postoperative complications between the two groups [n (%)]
| Group | n | Intracranial infection | Re-bleeding | Hydrocephalus | Cerebral vasospasm | Total incidence rate (%) |
|---|---|---|---|---|---|---|
| Clipping group | 68 | 3 (4.41) | 5 (7.35) | 4 (5.88) | 3 (4.41) | 15 (22.06) |
| Intervention group | 80 | 1 (1.25) | 1 (1.25) | 2 (2.50) | 2 (2.50) | 6 (7.50) |
| χ2 | - | 1.397 | 3.520 | 1.081 | 0.411 | 6.399 |
| P | - | 0.237 | 0.060 | 0.298 | 0.521 | 0.011 |
Discussion
ASAH is a life-threatening disease, which usually leads to severe disability in relatively young and healthy people [17]. It is a dangerous type of SAH, and most patients die before they reach the hospital. With high disability and mortality [18], it is difficult to cure. Because there is no obvious clinical symptom before the rupture of the cerebral aneurysm, patients may have sudden headache, neurological dysfunction and even consciousness disorders after rupture [19]. In recent years, with the development of microsurgery and interventional neurosurgery [20], the diagnosis and treatment of ASAH has made new progress.
In this research, we gave two different surgical interventions to ASAH patients, and found that their prognosis was improved differently after treatment. Okuma Y et al. [21] claimed that embolization treatment for some patients with chronic subdural hematoma could effectively reduce the discharge time and postoperative recurrence rate. Compared with the postoperative clinical symptoms of patients, the time of operation and hospitalization of the IG were markedly less than those of the CG, which indicated that IE had less trauma and a convenient operation, reducing the time of operation and hospitalization and improving the recovery of patients. This research also found that the levels of IgG, IgM and IgA in the IG were higher than those in the CG. Similarly, Jin GY et al. [22] proved that IG caused less damage to patients’ immune function than craniotomy; which might be due to the greater trauma of a craniotomy and the injury to local blood vessels during surgery; thus affecting the immune system and leading to the decline of immune function; which can be avoided by methods in the IG, thus causing less damage to their immune function. A recent study has shown that [23] neuroinflammation plays a key role in injury progression and brain injury, and genetic susceptibility and related complications indicate that it may play a role in ASAH. This research found that the levels of TNF-α, IL-8 and hs-CRP in the IG were lower than those in the CG after surgery. It revealed that compared with craniotomy, IE had some advantages, such as small trauma and wound, thus reducing the incidence of postoperative infection. Hence, the expression of inflammatory factors of patients in the IG was low.
Another study has shown that the rupture of a cerebral aneurysm is a unique occurance in each cerebrovascular accident caused by various reasons. Although the current clinical point of view is to perform surgery to prevent severe SAH, most patients have cognitive dysfunction after surgery [24]. In this study, the postoperative MOCA scores of patients in the IG were markedly higher than those in the CG. This might be related to factors such as brain tissue pulling during craniotomy clipping, partial perforator vessels and temporary occlusion of vessels during operation. A recent study has shown that [25] the loss of cognitive function of patients undergoing craniotomy clipping is mainly due to the injury of surgery, while IE could reduce the brain damage of patients, thus reducing the incidence of cognitive dysfunction. Clinically, [26] after SAH, the risk of spontaneous rupture in patients with large intracranial aneurysms increases, and the prognosis of the nervous system is poor. However, this research showed that the NIHSS scores of patients in the IG were dramatically lower than those in the CG, indicating that IE can reduce the neurological damage of patients. The PSQI scores of patients in the IG were obviously lower than those in the CG, which indicated that IE could not only reduce the neurological damage, but also improve the sleep quality of patients. For example, Ma J et al. [27] pointed out that patients with arteriovenous malformations in skull functional areas were given arterial embolization. Compared with craniotomy, the improvement of clinical related symptoms of patients after arterial embolization was remarkably higher, and the incidence of complications reduced. This showed that IE could effectively treat ASAH, because it could reduce the exposed area of tissue and shorten the incision, thus reducing the incidence of postoperative complications. Finally, we followed up the two groups of patients for 3 months, and observed their postoperative efficacy. The results signified that the total effective rate of the IG was dramatically higher than that of the CG, revealing that patients receiving IE were not affected by intracranial hypertension and cerebral edema; the operation was safer, with a smaller incision and trauma, which was beneficial to later recovery.
Although this study confirmed that IE is a feasible treatment for ASAH, there is still room for improvement. We can add observations and analysis of factors affecting the prognosis of patients, and increase the investigation of postoperative recurrence rate and factors leading to recurrence. In future studies, it is necessary to extend the research time and add postoperative follow-up.
To sum up, IE is effective in ASH patients; it can reduce the damage of immune, cognitive and nerve functions, with a high treatment efficacy.
Disclosure of conflict of interest
None.
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