Effect of hemorrhagic cerebrospinal fluid drainage on cognitive function after intracranial aneurysm clipping

2.1 Patients

The patient selection criteria were as follows: (1) Intracranial aneurysm was diagnosed using whole cerebral angiography. (2) Computed tomography (CT) showed subarachnoid hemorrhage without extensive intracranial hematoma. (3) Preoperative Hunt–Hess grade was I–II. (4) The patients ranged in age from 20 to 70 years and had at least primary school education. (5) Craniotomy aneurysm clipping was successful. (6) Preoperative and postoperative cognitive function MoCA scores were available.

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

2.2 Data collection

In this study, 59 patients with aneurysmal subarachnoid hemorrhage from October 2017 to October 2018 were treated in our Neurosurgery Department and confirmed by digital subtraction angiography. Patients with surgical contraindications, severe hepatic and renal dysfunction, and estimated survival time of < 12 months were excluded. All patients underwent intracranial aneurysm clipping within 3 days of onset. Because the Hunt–Hess grades of the selected patients in this study were all Grades I and II, and preoperative CT showed subarachnoid hemorrhage, CSF drainage was required for all patients postoperatively.

The indications for continuous and intermittent CSF drainage in this study were the same as follows: (1) Preoperative Hunt–Hess grades of the selected patients were Grades I and II. (2) Preoperative CT scan showed subarachnoid hemorrhage. In this study, different CSF drainage methods were randomly adopted according to the operation date of the patient. The patients underwent repeated lumbar puncture treatment on even-numbered days and lumbar cistern drainage treatment on odd-numbered days. According to the drainage mode of hemorrhagic CSF, the patients were assigned to either the repeated lumbar puncture drainage group (Group A; n = 28, 16 males, 12 females; mean age, 41.89 ± 15.19 years; range, 20~69 years), or the continuous lumbar cistern drainage group (Group B; n = 31; 17 males, 14 females; mean age, 44.52 ± 15.47 years; range, 23~73 years) (Table 1). Patients in Group A included 12 patients with Hunt-Hess Grade I and 16 patients with grade II. In Group B, there were 13 patients with Hunt-Hess Grade I and 18 patients with Grade II (Table 2). No statistically significant differences were noted in sex, age, and Hunt–Hess grade between the two groups (P > 0.05).

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Table 1.

Comparison of basic data between the two groups

Group	n	Sex
		Male		Female	Age (years)
A	28	16		12	41.89 ± 15.19
B	31	17		14	44.52 ± 15.47
t or χ 2			0.032		0.656
P			0.859		0.515

Group A is the repeated lumbar puncture drainage group;

Group B is the continuous lumbar drainage group.

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Table 2.

Comparison of preoperative Hunt-Hess grades between the two groups

Group	n (Grade I)	n (Grade II)	χ 2	P
A	12	16
			0.005	0.943
B	13	18

Group A is the repeated lumbar puncture drainage group; Group B is the continuous lumbar drainage group. The preoperative Hunt–Hess grading composition of the two groups was determined by performing the chi-square test, χ² = 0.005, P = 0.943 (not significant).

The sex compositions of the patients in the two groups were tested by performing the chi-square test, χ² = 0.032, P = 0.859, and the difference in sex compositions was not statistically significant.

The age distribution of patients in the two groups was normal, represented by mean ± standard. t = 0.656, P = 0.515, the difference in age distributions was not statistically significant.

2.3 Treatment options

The patients’ symptoms were treated with nimodipine, blood dilution, and induced hypertension after surgery. The patients began to use different drainage methods on the first day after surgery: intermittent lumbar puncture was performed in Group A to release 25~35 mL of CSF once a day for 7 consecutive days, and continuous lumbar cistern drainage was performed in Group B with the CSF flow controlled at 150 to 200 mL/d for 7 days.

2.4 Cognitive function assessment test method

The Chinese version of the MoCA scale was used to evaluate the patients. The Chinese version of the MoCA scale was previously revised according to the Chinese cultural background: (1) In the visuospatial and executive tests, “A, B, C, D, E” of the connection test were revised to the Chinese pronunciation of “Jia, Yi, Bing, Ding, Wu” respectively. (2) In the naming test, “rhino” was revised to “cow”, an animal familiar to the Chinese. (3) In the memory test, “velvet” and “church” were revised to “silk” and “hotel”, respectively, which are familiar to the Chinese. (4) In the attention test, identifying the English letter A was revised to identifying the Arabic number 1, which is familiar to the Chinese. (5) In the language repeat test, “I only know that John is the one to help today” and “The cat always hid under the couch when dogs were in the room” were revised to “He has not returned since he went out” and “He returned home to find the room full of his friends”, respectively, for the Chinese aphasia examination. (6) In the fluency test, “Name the maximum number of words in 1 minute that begins with the letter F” was revised to “Say as many animal names as possible in 1 minute”. The Chinese version of MoCA was used to score the cognitive function of Groups A and B before and 30 days after surgery, respectively. The MoCA scale had a total score of 30 points, scores of 26~30 points were defined as normal, and scores < 26 points were defined as cognitive impairment.

2.5 Statistical analysis

SSPS version 23.0 statistical software was used to analyze the data. The t test and chi-square test were used. At the level of a = 0.05, P < 0.05 was considered to be indicative of statistical significance, and all chi-square tests and P values were bilateral.

3.1 Comparison of the incidences of cognitive impairment between the two groups before surgery (number of cases)

The incidence of cognitive impairment was 46% (13/28) in Group A, and 32% (10/31) in Group B before surgery (Table 3). No significant difference was noted in the incidences of cognitive impairment between the two groups (P > 0.05).

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Table 3.

Comparison of the incidences of preoperative cognitive function between the two groups (number of cases).

Group	n (normal)	n (impairment)	χ 2	P
A	15	13
			1.242	0.265
B	21	10

Group A is the repeated lumbar puncture drainage group; Group B is the continuous lumbar drainage group. The incidences of preoperative cognitive impairment in the two groups were determined by chi-square test, χ² = 1.242, P = 0.265 (not significant).

3.2 Comparison of the incidences of cognitive impairment between the two groups 1 month after surgery (number of cases)

The incidence of cognitive impairment was 35% (10/28) in Group A and 12% (4/31) in Group B at 1 month after surgery (Table 4). A significant difference was noted in the incidences of cognitive impairment at 1 month after surgery between the two groups (P < 0.05). Compared with repeated lumbar puncture after aneurysm surgery, continuous lumbar cistern drainage after aneurysm clipping significantly reduced the incidence of cognitive impairment in the patients.

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Table 4.

Comparison of the incidences of cognitive impairment 1 month after surgery between the two groups (number of cases)

Group	n (normal)	n (impairment)	χ 2	P
A	18	10
			4.230	0.040
B	27	4

Group A is the repeated lumbar puncture drainage group; Group B is the continuous lumbar drainage group. The chi-square test was used to determine the incidence of cognitive impairment in the two groups 1 month after surgery, χ² = 4.230, P = 0.040 (significant).

4.1 Intracranial aneurysm clipping and cognitive impairment

To fully expose the aneurysmal tumor body and neck during surgery, it is inevitable that the surrounding brain tissue be pulled, which affects the blood supply to some brain tissue by causing ischemic injury and eventually cognitive impairment [13, 14]. However, there is increasing evidence that the most important factor associated with cognitive impairment caused by aneurysmal subarachnoid hemorrhage is the hemorrhage itself and the secondary brain injury related to the hemorrhage rather than the location or surgical intervention of the aneurysm [15]. In patients with aneurysmal subarachnoid hemorrhage, no significant difference in long-term cognitive function after craniotomy with clamps or interventional therapy has been found. Subarachnoid hemorrhage is the primary cause of cognitive impairment; thus, surgery does not cause new cognitive impairment [15 –17].

4.2 Hemorrhagic CSF drainage and cognitive impairment after intracranial aneurysm occlusion

Cognitive impairment refers to the absence of attention, feeling, intelligence, thinking, memory, self-knowledge positioning, and other psychological activities, which results in abnormal thinking and judgment and impairment of the brain’s advanced intelligent processing associated with learning and memory, thus causing damage to the composite function. An important cause of cognitive impairment is aneurysmal subarachnoid hemorrhage [17], after which, most patients suffer from shortterm or long-term cognitive impairment to varying degrees, with an incidence rate ranging from 7% to 60%, and even severe cognitive impairment 4~7 years after onset [18]. Studies have found that aneurysmal subarachnoid hemorrhage causes brain injury and cognitive impairment due to multiple factors, which include delayed cerebral ischemia, direct injury to cerebral hematoma, increased intracranial pressure, and chronic hydrocephalus [19]. Although surgery can clip aneurysms and prevent blood from entering the subarachnoid space through ruptured aneurysms, surgery cannot remove all subarachnoid hematoceles, so residual hematoceles can still lead to vasospasm in patients, thus affecting cognitive function. Therefore, drainage of hemorrhagic CSF after aneurysmal clipping is very important to reduce the incidence of postoperative cognitive impairment in patients.

4.3 Advantages and disadvantages of lumbar cistern continuous drainage

Lumbar puncture is an important auxiliary examination commonly used for neurological diseases, which is of great value for the diagnosis and treatment of diseases. On the basis of conventional lumbar puncture, Vourc'h G [20] first reported in 1963 regarding lumbar drainage treatment of CSF in patients with a large pool and obtained good curative effect. After nearly 50 years of development, large waist pool catheter drainage of CSF has become a common indispensable procedure in neurosurgery for treatment of diseases of the nervous system, and the scope of applications is increasing.

The results of this study showed that the incidence of cognitive impairment was significantly lower in Group B (continuous drainage) than in Group A (repeated drainage) 1 month after surgery (P < 0.05). This finding indicates that continuous lumbar cistern drainage reduced the incidence of cognitive impairment in patients after aneurysmal clipping. Under normal circumstances, the rate of CSF generation in adults is 0.35 mL/min, and about 500 mL of CSF can be produced every day. The continuous lumbar cistern drainage adopted in this study mainly follows the law of human CSF circulation and regeneration. Under the premise of being close to human physiological pressure, the larger the drainage volume, the shorter the time to remove hematoceles, reduce the hematocele residue, and effectively relieve the cerebral vasospasm. However, in this study, some patients in the lumbar cistern continuous drainage group still had cognitive impairment after surgery, which was primarily due to diffuse brain injury and secondary complications caused by subarachnoid hemorrhage, such as cerebral vasospasm and intracranial pressure increase, resulting in cognitive impairment [14, 21]. Repeated lumbar puncture drainage with a large waist pool and larger flow can accelerate the rate of removal of subarachnoid hemorrhage, reduce the stimulation of hemorrhagic cerebrovascular CSF, reduce the degree of cerebral vasospasm, and reduce the incidence of postoperative cognitive impairment in patients with aneurysms, but the disadvantage is that large pool drainage is not absolutely safe, so the following factors must be considered: (1) The rate of drainage and total amount of drainage must be controlled every day. An excessively fast drainage speed can easily lead to low cranial pressure or even cerebral hernia. Dagnew et al. [22] comprehensively reviewed previous studies, it is thought that excessive drainage of symptomatic I cerebellar tonsillar hernia deformity will lead to an incidence < 10% and a degree of asymptomatic I degree cerebellar tonsillar hernia deformity rate > 70%. (2) The operation must be standardized, principles of sterility should be followed, iatrogenic infection should be avoided, and the fixed pipeline should be changed regularly. (3) The puncture needle in the lumbar epidural kit is extremely sharp. During the operation, appropriate force should be exerted to grasp the needle and move it forward slowly. It is important not to exert too much force that may cause lumbar spine and nerve root injury. (4) The pipe must be properly fixed and some space reserved for the patient to roll over and move on the bed. (5) The drainage time must be strictly controlled because an excessively long time will increase the risk of intracranial infection.

Our results suggest that continuous lumbar cistern drainage is a very effective method for the treatment of aneurysmal subarachnoid hemorrhage, and it can reduce the incidence of postoperative cognitive impairment. Therefore, the first choice for hemorrhagic CSF drainage after aneurysmal clipping should be continuous lumbar cistern drainage.