Baseline characteristics
From January 20, 2020, to March 25, 2020, nine patients were diagnosed with COVID-19 with positive nucleic acid testing (NAT) in our hospital for all kinds of emergency patients. A total of 127 aSAH patients referred to our emergency department, and 42 (33.1%) of them underwent craniotomy clipping (Figure 2). The patients’ mean age was 54.9±8.6 years (range 35-74 years) (Table 1). Eight cases (19.0%) were initially screened as preliminary undetermined COVID-19 cases, and 2 of them underwent craniotomy clipping surgery in the negative pressure operating room (OR). Since February 28, 12 cases (28.6%) received COVID-19 NAT upon admission and showed negative results, and the false-negative rate was 0.0%. The location of responsible aneurysms was mostly in the anterior communicating artery (ACoA, 31.0%), posterior communicating artery (PCoA, 35.7%), middle cerebral artery (MCA, 26.2%). The modified Fisher grade and Hunt-Hess grade was 3.0±1.1 and 1.9±0.5, respectively. The duration between admission and craniotomy was 34.8±18.5 hours. Two patients (4.8%) occurred generalized epilepsy during hospitalization before craniotomy.
Table 1. Comparison of emergency aSAH patients between the current period and the respective time period last year.
Characteristics
|
Current
|
Last year
|
P valuea
|
No. of patients
|
42
|
18
|
|
No. of aneurysms
|
45
|
19
|
|
Sex (male)
|
24 (57.1)
|
8 (44.4)
|
0.366
|
Age, years
|
54.9±8.6
|
49.4±10.7
|
0.039*
|
Admission stratification
|
|
|
|
Normal patient
|
34 (81.0)
|
|
|
Mild suspected patient
|
8 (19.0)
|
|
|
Suspected patient
|
0 (0.0)
|
|
|
Confirmed patient
|
0 (0.0)
|
|
|
COVID-19 NAT (n=12) (negative)
|
12 (100.0)
|
|
|
False negative COVID-19 NAT
|
0 (0.0)
|
|
|
Location of responsible aneurysm
|
|
|
|
ACoA
|
13 (31.0)
|
7 (38.9)
|
0.585
|
PCoA
|
15 (35.7)
|
5 (27.8)
|
ACA
|
2 (4.8)
|
0 (0.0)
|
MCA
|
11 (26.2)
|
6 (33.3)
|
others
|
1 (2.4)
|
0 (0.0)
|
Fisher grade
|
3.1±1.1
|
2.9±1.0
|
0.555
|
Modified Fisher grade
|
3.0±1.1
|
3.1±1.1
|
0.835
|
Hunt-Hess grade
|
1.9±0.5
|
2.4±0.6
|
0.003*
|
WFNS grade
|
2.7±0.9
|
2.8±1.1
|
0.690
|
GCS
|
12.9±1.2
|
12.0±2.3
|
0.367
|
Duration between rupture and craniotomy, hours
|
71.1±55.2
|
40.7±45.6
|
0.044*
|
Duration between admission and craniotomy, hours
|
37.1±16.8
|
28.7±11.7
|
0.058
|
Preoperative adverse events during hospitalization
|
|
|
|
Rebleeding
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Infarction
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Epilepsy
|
2 (4.8)
|
1 (5.6)
|
>0.99
|
Duration of surgery, hours
|
3.5±1.0
|
4.1±2.3
|
0.277
|
Intraoperative blood loss, ml
|
260.7±238.0
|
258.3±152.7
|
0.969
|
Mean hospital LOS, days
|
14.9±8.8
|
17.4±6.9
|
0.298
|
Hospitalization cost, dollarsb
|
13385.6±6973.4
|
14006.1±5640.4
|
0.740
|
Postoperative complications
|
|
|
|
Postoperative hemorrhage
|
0 (0.0)
|
1 (5.6)
|
0.660
|
Postoperative DCI
|
13 (31.0)
|
8 (44.4)
|
0.315
|
Postoperative DVT
|
10 (23.8)
|
1 (5.6)
|
0.190
|
Postoperative intracranial infection
|
5 (11.9)
|
4 (22.2)
|
0.528
|
Discharge mRS score
|
|
|
|
Mean
|
1.9±1.6
|
2.1±1.6
|
0.779
|
0-2
|
29 (69.0)
|
12 (66.7)
|
0.856
|
3-6
|
13 (31.0)
|
6 (33.3)
|
ACA = anterior cerebral artery; ACoA = anterior communicating aneurysm; aSAH = aneurysmal subarachnoid hemorrhage; COVID-19 = coronavirus disease 2019; CT = computed tomography; DCI = delayed cerebral ischemia; DVT = deep vein thrombosis; GCS = Glasgow Coma Scale; LOS = length of stay; MCA = middle cerebral artery; mRS = modified Rankin Scale; NAT = nucleic acid testing; PCA = posterior cerebral artery; WFNS = World Federation of Neurological Surgeons;
a P values indicate differences between the current period and the respective time period, and P less than 0.05 was considered statistically significant.
b The exchange rate between RMB and USD is 1 USD = 7.0942 RMB.
Values are numbers of cases (%) unless otherwise indicated. Mean values are presented with SDs.
Comparison between current and retrospective period last year
Eighteen emergency aSAH patients underwent craniotomy clipping in our hospital during the retrospective period last year (Table 1). Compared with them, the patients who received BTP were older (5.5, 95% confidence intervals [CI] 0.3 to 10.7, P=0.039) and had lower Hunt-Hess grades (0.5, 95% CI 0.2 to 0.8, P=0.003). There are no statistical differences in the duration between admission and craniotomy between the two groups (37.1±16.8 vs. 28.7±11.7; 8.4, 95% CI -0.3 to 17.1, P=0.058). It indicates that BTP may not prolong the duration of preoperative hospitalization. Finally, the incidences of preoperative hospitalized adverse events and postoperative neurofunctional outcomes (-0.1, 95% CI -1.0 to 0.8, P=0.779) were similar between the two groups. 13 cases (31.0%) in the BTP group and 8 cases (44.4%) in the control group occurred postoperative delayed cerebral ischemia (DCI) (0.6, 95% CI 0.2 to 1.7, P=0.315). According to propensity scores, we matched 9 cases with BTP to 9 cases last year (Table 2). The two groups were compared to verify that no significant differences in baseline characteristics after the PSM. Finally, we found there were no significant differences in preoperative adverse events during hospitalization (p>0.99), postoperative complications (p>0.99), and discharge mRS score (0.8, 95% CI -1.9 to 1.5, p=0.788).
Table 2. Comparison of emergency aSAH patients between the current period and the respective time period last year after propensity score matching (PSM).
Characteristics
|
Current
|
Last year
|
P valuea
|
No. of patients
|
9
|
9
|
|
No. of aneurysms
|
10
|
10
|
|
Sex (male)
|
5 (55.6)
|
4 (44.4)
|
>0.99
|
Age, years
|
50.11±9.3
|
45.3±11.3
|
0.342
|
Admission stratification
|
|
|
|
Normal patient
|
6 (66.7)
|
|
|
Mild suspected patient
|
3 (33.3)
|
|
|
Suspected patient
|
0 (0.0)
|
|
|
Confirmed patient
|
0 (0.0)
|
|
|
COVID-19 NAT (n=2) (negative)
|
2 (100.0)
|
|
|
False negative COVID-19 NAT
|
0 (0.0)
|
|
|
Location of responsible aneurysm
|
|
|
|
ACoA
|
3 (33.3)
|
4 (44.4)
|
0.599
|
PCoA
|
3 (33.3)
|
2 (22.2)
|
ACA
|
1 (11.1)
|
0 (0.0)
|
MCA
|
3 (33.3)
|
4 (44.4)
|
others
|
0 (0.0)
|
0 (0.0)
|
Fisher grade
|
3.0±1.2
|
2.9±1.1
|
0.839
|
Modified Fisher grade
|
3.2±1.0
|
2.7±1.2
|
0.302
|
Hunt-Hess grade
|
2.2±0.4
|
2.2±0.7
|
>0.99
|
WFNS grade
|
2.4±0.9
|
2.6±1.2
|
0.819
|
GCS
|
12.6±1.8
|
12.3±2.3
|
0.825
|
Duration between rupture and craniotomy, hours
|
56.9±52.8
|
56.2±60.5
|
0.980
|
Duration between admission and craniotomy, hours
|
35.6±15.3
|
31.9±12.3
|
0.577
|
Preoperative adverse events during hospitalization
|
|
|
|
Rebleeding
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Infarction
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Epilepsy
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Duration of surgery, hours
|
3.7±1.1
|
4.9±2.9
|
0.264
|
Intraoperative blood loss, ml
|
188.9±126.9
|
266.7±188.7
|
0.320
|
Mean hospital LOS, days
|
17.4±13.9
|
17.9±9.0
|
0.937
|
Hospitalization cost, dollarsb
|
17354.9±12110.1
|
13147.1±4200.9
|
0.339
|
Postoperative complications
|
|
|
|
Postoperative hemorrhage
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Postoperative DCI
|
4 (44.4)
|
4 (44.4)
|
>0.99
|
Postoperative DVT
|
3 (33.3)
|
1 (11.1)
|
>0.99
|
Postoperative intracranial infection
|
2 (22.2)
|
2 (22.2)
|
>0.99
|
Discharge mRS score
|
|
|
|
Mean
|
1.8±1.7
|
2.0±1.7
|
0.788
|
0-2
|
7 (77.8)
|
6 (66.7)
|
>0.99
|
3-6
|
2 (22.2)
|
3 (33.3)
|
ACA = anterior cerebral artery; ACoA = anterior communicating aneurysm; aSAH = aneurysmal subarachnoid hemorrhage; COVID-19 = coronavirus disease 2019; CT = computed tomography; DCI = delayed cerebral ischemia; DVT = deep vein thrombosis; GCS = Glasgow Coma Scale; LOS = length of stay; MCA = middle cerebral artery; mRS = modified Rankin Scale; NAT = nucleic acid testing; PCA = posterior cerebral artery; WFNS = World Federation of Neurological Surgeons;
a P values indicate differences between the current period and the respective time period, and P less than 0.05 was considered statistically significant.
b The exchange rate between RMB and USD is 1 USD = 7.0942 RMB.
Values are numbers of cases (%) unless otherwise indicated. Mean values are presented with SDs.
Subgroup analysis
There were no statistical differences in prognosis between the negative cases and preliminary undetermined COVID-19 cases (1) / (2) (F(2, 39)=0.393, P=0.678) (Table 3). Although patients undergoing COVID-19 NAT took slightly longer time from admission to a craniotomy (35.9±15.3 vs. 40.2±20.4 hours; 4.4, 95% CI -7.3 to 16.0, P=0.453), there were no differences in preoperative hospitalized adverse events and postoperative prognosis of the patients with or without COVID-19 NAT (-0.3, 95% CI -1.4 to 0.9, P=0.653, Table 4).
Table 3. Subgroup comparison of different preliminary COVID-19 screening result.
Characteristics
|
Normal
(Conventional OR)
|
Mild Suspected
(Conventional OR)
|
Mild Suspected
(Negative Pressure OR)
|
P valuea
|
No. of patients
|
34
|
6
|
2
|
|
Duration between admission and craniotomy, hours
|
38.5±17.6
|
32.8±7.4
|
25.5±23.3
|
0.456
|
Preoperative adverse events during hospitalization
|
|
|
|
|
Rebleeding
|
0 (0.0)
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Infarction
|
0 (0.0)
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Epilepsy
|
1 (2.9)
|
1 (16.7)
|
0 (0.0)
|
0.438
|
Duration of surgery, hours
|
3.4±0.9
|
3.3±0.9
|
5.5±0.0
|
0.007*
|
Intraoperative blood loss, ml
|
233.8±136.9
|
200.0±154.9
|
900±848.5
|
<0.001*
|
Mean hospital LOS, days
|
13.8±7.3
|
19.3±15.6
|
20.5±0.7
|
0.250
|
Hospitalization cost, dollarsb
|
12695.9±5226.2
|
17568.7±10863.7
|
12560.6±397.0
|
0.290
|
Postoperative complications
|
|
|
|
|
Postoperative hemorrhage
|
0 (0.0)
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Postoperative DCI
|
9 (26.5)
|
3 (50.0)
|
1 (50.0)
|
0.453
|
Postoperative DVT
|
9 (26.5)
|
1 (16.7)
|
0 (0.0)
|
0.497
|
Postoperative intracranial infection
|
3 (8.8)
|
2 (33.3)
|
0 (0.0)
|
0.255
|
Discharge mRS score
|
|
|
|
|
Mean
|
1.9±1.6
|
2.2±1.7
|
1.0±1.4
|
0.678
|
0-2
|
23 (67.6)
|
4 (66.7)
|
2 (100.0)
|
0.466
|
3-6
|
11 (32.4)
|
2 (33.3)
|
0 (0.0)
|
aSAH = aneurysmal subarachnoid hemorrhage; COVID-19 = coronavirus disease 2019; DCI = delayed cerebral ischemia; DVT = deep vein thrombosis; LOS = length of stay; mRS = modified Rankin Scale; OR= operating room;
a P values indicate differences among different preliminary COVID-19 screening result, and P less than 0.05 was considered statistically significant.
b The exchange rate between RMB and USD is 1 USD = 7.0942 RMB.
Values are numbers of cases (%) unless otherwise indicated. Mean values are presented with SDs.
Table 4. Comparison of emergency aSAH patients with/without COVID-19 NAT.
Characteristics
|
Absent
|
Accept
|
P valuea
|
No. of patients
|
30
|
12
|
|
No. of aneurysms
|
32
|
13
|
|
Sex (male)
|
16 (53.3)
|
8 (66.7)
|
0.430
|
Age, years
|
55.1±8.3
|
54.5±9.5
|
0.840
|
Admission stratification
|
|
|
|
Normal patient
|
26 (86.7)
|
8 (66.7)
|
0.151
|
Mild suspected patient
|
4 (13.3)
|
4 (33.3)
|
Suspected patient
|
0 (0.0)
|
0 (0.0)
|
Confirmed patient
|
0 (0.0)
|
0 (0.0)
|
Location of responsible aneurysm
|
|
|
|
ACoA
|
8 (26.7)
|
5 (41.7)
|
0.740
|
PCoA
|
11 (36.7)
|
4 (33.3)
|
ACA
|
2 (6.7)
|
1 (8.3)
|
MCA
|
10 (33.3)
|
2 (16.7)
|
others
|
1 (3.3)
|
1 (8.3)
|
Fisher grade
|
3.2±1.0
|
2.9±1.2
|
0.442
|
Modified Fisher grade
|
3.2±1.1
|
2.8±1.1
|
0.264
|
Hunt-Hess grade
|
1.9±0.5
|
1.9±0.5
|
0.928
|
WFNS grade
|
2.7±0.9
|
2.8±1.0
|
0.601
|
GCS
|
12.8±1.3
|
13.1±1.0
|
0.550
|
Duration between rupture and craniotomy, hours
|
71.7±55.3
|
70.0±57.4
|
0.931
|
Duration between admission and craniotomy, hours
|
35.9±15.3
|
40.2±20.4
|
0.453
|
Preoperative hospitalized adverse events
|
|
|
|
Rebleeding
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Infarction
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Epilepsy
|
1 (3.3)
|
1 (8.3)
|
0.513
|
Duration of surgery, hours
|
3.5±0.9
|
3.5±1.2
|
0.913
|
Intraoperative blood loss, ml
|
236.7±130.6
|
320.8±400.8
|
0.490
|
Mean hospital LOS, days
|
14.4±9.7
|
16.3±6.4
|
0.547
|
Hospitalization cost, dollarsb
|
14268.4±7811.7
|
11178.5±3596.8
|
0.198
|
Postoperative complications
|
|
|
|
Postoperative hemorrhage
|
0 (0.0)
|
0 (0.0)
|
>0.99
|
Postoperative DCI
|
9 (30.0)
|
4 (33.3)
|
0.833
|
Postoperative DVT
|
8 (26.7)
|
2 (16.7)
|
0.481
|
Postoperative intracranial infection
|
3 (10.0)
|
2 (16.7)
|
0.558
|
Discharge mRS score
|
|
|
|
Mean
|
2.0±1.6
|
1.8±1.5
|
0.653
|
0-2
|
20 (66.7)
|
9 (75.0)
|
0.874
|
3-6
|
10 (33.3)
|
3 (25.0)
|
aSAH = aneurysmal subarachnoid hemorrhage; COVID-19 = coronavirus disease 2019; DCI = delayed cerebral ischemia; DVT = deep vein thrombosis; LOS = length of stay; mRS = modified Rankin Scale; NAT= nucleic acid test;
a P values indicate differences between patients with or without COVID-19 NAT, and P less than 0.05 was considered statistically significant.
b The exchange rate between RMB and USD is 1 USD = 7.0942 RMB.
Values are numbers of cases (%) unless otherwise indicated. Mean values are presented with SDs.
Illustration case
A 61-year-old male presented with sudden severe headache for 23 hours with nausea and vomiting. Preoperative computed tomography angiography (CTA) revealed a right MCA M1 bifurcation irregular aneurysm (Figure 3). The modified Fisher grade was four, and the Hunt-Hess grade was 2. The preliminary COVID-19 screening suggested positive axillary temperature (38.4°C), positive lung CT, and negative COVID-19 NAT (once), and was classified as a preliminary undetermined (2) patient. The consultation group of COVID-19 prevention and control experts judged that the operation should be carried out in the negative pressure OR. The surgical team protected themselves according to the third-levels of protection standards. The operation was performed by a senior neurosurgeon (XLC) with 15 years of experience in aneurysm clipping. During the operation, the view field in the microscope was limited due to the fogging goggles. The operation duration was 5.5 hours. Intraoperative blood loss was about 300ml. The patient was transferred to the isolation negative pressure intensive care unit (ICU) after the operation, and the reexamination of COVID-19 NAT was still negative 24 hours after the first NAT. He was then transferred to the ordinary neurosurgical ward (single bed) on the second postoperative day. No postoperative complications occurred, and the patient was discharged on the 7th postoperative day, with a modified Rankin Scale (mRS) score of 0.