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Impact of Surgeon Experience on Postoperative Rehemorrhage in Spontaneous Basal Ganglia Intracerebral Hemorrhage
Original Article
Impact of Surgeon Experience on Postoperative Rehemorrhage in Spontaneous Basal Ganglia Intracerebral Hemorrhage Wen-Jian Zheng, Liang-Ming Li, Yong-Hua Zhu, Zi-Hui Hu, Wei Liao, Qi-Chang Lin, Wei-Biao Lin, Zheng-Kai Zhu, Jia-Hao Su, Shao-Hua Lin
BACKGROUND: Spontaneous intracerebral hemorrhage (SICH) is of high mortality and morbidity. SICH in the basal ganglia is usually attributed to chronic hypertension. Postoperative rehemorrhage is a severe complication, and it is relative to surgical techniques.
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METHODS: A retrospective survey was conducted on 123 patients with basal ganglia SICH who received surgery from January 2015 to January 2019. Postoperative rehemorrhage within 24 hours was recorded. Preoperative clinical parameters, surgeon experience (<10 and >20 years), operation time, surgical approach, and hemostasis technique were recorded and analyzed.
achieve definitive hemostasis in operation. The use of a transsylvian approach can significantly reduce the rehemorrhage rate. Packing hemostasis with gelatin sponge may increase complications.
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RESULTS: The total postoperative rehemorrhage rate was 12.2% (15/123). The univariable analysis showed general surgeons had a higher postoperative rehemorrhage rate than experienced surgeons (30.4% vs. 8.6%, respectively; P [ 0.068). The operation time (minutes) in experienced surgeons was significantly longer (164.9 53.5 vs. 137.7 30.8, P [ 0.016), but they had a higher chance to locate the responsible vessel (74.2% vs. 40.0%, P [ 0.001), respectively. Logistic analysis indicated that experienced surgeons significantly reduced the risk of rehemorrhage (odds ratio [OR], 0.242; P [ 0.021). Transsylvian approach was a protective factor for postoperative rehemorrhage (OR, 0.291; P [ 0.045).
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CONCLUSIONS: Surgeons’ experience plays the most important role in postoperative rehemorrhage. Surgeons with rich experience were willing to spend more time to
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INTRODUCTION
S
pontaneous intracerebral hemorrhage (SICH) is a devastating disease with high mortality and morbidity. The 1-month mortality rate is nearly 40%.1 Primary SICH refers to hemorrhages without an identifiable vascular malformation or coagulopathy, which is mostly attributed to chronic hypertension.2 One of the most commonly affected sites is the basal ganglia. Surgery is indicated for patients who have large blood volume and intractable intracranial pressure. However, postoperative rehemorrhage is a major complication which can dramatically worsen the outcome. Here, we present a retrospective study focusing on postoperative rehemorrhage in patients with primary SICH in the basal ganglia. MATERIALS AND METHODS A retrospective survey was conducted on 236 patients with basal ganglia SICH in our hospital from January 2015 to January 2019. Inclusion Criteria The inclusion criteria included the following: >18 years of age, indication for surgery was hematoma >30 mL or midline shift >10 mm, surgery was performed within 24 hours after symptom onset, surgery was performed in a pterional approach, and patients
Key words Basal ganglia - Postoperative rehemorrhage - Spontaneous intracerebral hemorrhage - Surgical technique
Department of Neurosurgery, Zhongshan City People’s Hospital, Zhongshan, China
Abbreviations and Acronyms CT: Computed tomography DC: Decompressive craniotomy ICH: Intracerebral hemorrhage ICU: Intensive care unit SICH: Spontaneous intracerebral hemorrhage
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To whom correspondence should be addressed: Wen-Jian Zheng, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.182
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE WEN-JIAN ZHENG ET AL.
REHEMORRHAGE FOR BASAL GANGLIA SICH
stayed in the intensive care unit (ICU) >24 hours after surgery. The family may decide to self-discharge within 24 hours when patients develop massive postoperative rehemorrhage; these patients were also included.
Exclusion Criteria The exclusion criteria included the following: history of cranial surgery, cranial radiotherapy, or cerebrovascular disease; received antiplatelet or anticoagulation treatment in the past 7 days; coagulopathy (international normalized ratio >1.5); thrombocytopenia (platelets <90,000/mm3); anemia (hemoglobin <100 g/L); renal or liver function impairment; head computed tomography (CT) scan showed lobar encephalomalacia probably because of prior injury or stroke (not including lacunar infarction); diagnosis of cerebral aneurysm, arteriovenous malformation, or Moyamoya disease; and incomplete clinical information.
Diagnosis of Postoperative Rehemorrhage Postoperative head CT scan was performed for all patients within 24 hours after surgery. Rehemorrhage was defined as a new hematoma >20 mL in the surgical area within 24 hours. We distinguished residual hematoma between rehemorrhage based on the surgeon’s surgical record (whether total evacuation of hematoma was performed) and the pre- and postoperative morphology of the hematoma. Of note, remote hemorrhage beside the surgical area or subcutaneous hemorrhage were not regarded as rehemorrhage. Patients who required reoperation in these situations were excluded.
Figure 1. (A) Packing hemostasis on postoperative head computed tomography scan. (B) Postoperative
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Data Collection Age, sex, history of hypertension, Glasgow Coma Scale score, and pupil size; blood pressure during hospitalization, hematoma diameter, volume, and modified Graeb score3; intracerebral hemorrhage (ICH) score,4 presence of black hole sign,5 or presence of blend sign6; symptom-surgery duration, surgical approach (transsylvian or transcortical), surgeon experience (3e10 or >20 years), use of packing hemostasis, and identified responsible vessel; and performance of decompressive craniotomy (DC), operation time, and postoperative blood pressure within 2 hours (whether systolic blood pressure was <140 mm Hg) were recorded. Head CT scan was evaluated by the first author (W.-J. Z.) for all cases. Hematoma volume was calculated using the ABC/2 formula. Packing hemostasis referred to evident sign (>1-cm diameter) of hemostatic material packing in the surgical area in the first postoperative head CT scan (Figure 1). Surgeons with 3e 10 years’ experience in neurosurgery were regarded as having general experience, whereas those with experience >20 years were regarded as experienced. There were 6 experienced surgeons (21e30 years’ experience) and 3 general surgeons (3, 5, and 10 years’ experience, respectively) involved in our study.
Surgical Technique The skin incision was designed depending on whether the surgeon planned to perform a DC. Usually, we tend to decompress for patients who are in a coma or with preoperative pupil dilation. In this case, an extended pterional craniotomy would be performed, and a bone flap 10- to 12-cm diameter was drilled. Otherwise, a 5- to 6-cm hook-mark skin incision was made around the pterion area, and a bone flap 3- to 5-cm diameter was drilled. All manipulation was performed under
rehemorrhage in a patient who received packing hemostasis.
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ORIGINAL ARTICLE WEN-JIAN ZHENG ET AL.
the microscope after opening the dura. A transsylvian or transcortical approach was chosen at the surgeons’ discretion. In a transcortical approach, the middle frontal gyrus or the superior temporal gyrus was the most common entry site. After dissecting the arachnoid with microscissors or a sharp scalpel, a small cortical corridor was made with a bipolar coagulator. In a transsylvian approach, the frontal side of the Sylvian vein was chosen as the entry site. The hematoma was exposed by a small incision in the insular cortex. Maximal hematoma evacuation was pursued in all cases. Squashed gelatin sponges were paved on the wound surface to achieve packing hemostasis in some cases. A drain was used in most patients, but an intracranial pressure monitor was only administrated in a few affordable patients. All patients were treated in ICU for at least 24 hours. Patients were sedated for 4e6 hours with propofol or midazolam to prevent postoperative irritability. Arterial blood pressure was monitored, and intravenous nicardipine or urapidil were used to control blood pressure at the aim of systolic blood pressure <140 mm Hg. Data Analysis Data were analyzed with SPSS 23.0 (SPSS Inc., Chicago, Illinois, USA). Statistical analyses of categorical variables were carried out using c2 tests or Fisher exact tests as appropriate. Statistics of means were carried out with independent Student t tests or nonparametric tests. Correlations of risk factors and postoperative rehemorrhage were evaluated by binary logistic regression. The odds ratio and 95% confidence interval were displayed. All statistical tests were 2-sided. P < 0.05 was considered statistically significant. RESULTS A series of 123 consecutive patients were eligible for the study. There were 90 men and 33 women, with an age range from 27 to 87 years (mean, 50.2 9.5 years). Patient information and clinical characteristics appear in Table 1. For continuous variables, values are expressed as mean SD. For dichotomous variables, values are percentage (number of patients). The total postoperative rehemorrhage rate was 12.2% (15/123). Among the 15 rehemorrhage patients, 8 patients underwent reoperation, 6 patients received conservative management, and 1 patient’s family withdrew further medical care. Univariate and Multivariate Analysis Univariate analysis showed surgeries performed by experienced surgeons had a relatively lower rehemorrhage rate (8.6% vs. 23.3%, P ¼ 0.068). Also, patients who received packing hemostasis technique were more likely to rehemorrhage (16.5% vs. 4.5%, P ¼ 0.053). For the 15 patients who developed rehemorrhage, 9 of them underwent primary DC. DC significantly reduced the reoperation rate (33.3% vs. 100.0%, P ¼ 0.028). Binary logistic analysis further confirmed that surgeon experience >20 years significantly reduced the risk of rehemorrhage. A transsylvian approach was also a protective factor for rehemorrhage (Table 2, model 1). Removal of the variable surgeon experience resulted in a decreased odds ratio of transsylvian approach (Table 2, model 2).
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Table 1. Patient Demographics and Clinical Characteristics Characteristic M/F Age (years)
None Rehemorrhage P (n [ 108) (n [ 15) Value 78/30
12/3
0.744
50.1 9.6
51.1 8.7
0.718
History of hypertension
60.2 (65)
60.0 (9)
0.989
Symptom-surgery duration (hours)
7.4 3.8
5.7 2.2
0.188*
SBP baseline (mm Hg)
196.2 33.0
Preoperative pupil dilation
24.1 (26)
46.7 (7)
0.224y
0
19.4 (21)
20.0 (3)
0.736y
1
33.3 (36)
20.0 (3)
2
37.0 (40)
46.7 (7)
3
10.2 (11)
13.3 (2)
54/54
7/8
0.809
Hematoma volume (mL)
44.6 24.3
55.0 41.4
0.557*
Maximal diameter (mm)
193.2 40.1 0.751
ICH score
Preoperative CT scan presentation Laterality (left/right)
57.3 11.7
61.8 19.0
0.260*
Midline shift (mm)
6.9 3.7
7.0 4.7
0.889
Black hole sign
27.8 (30)
33.3 (5)
0.887
Blend sign
36.1 (39)
46.7 (7)
0.429
Intraventricular hemorrhage
52.8 (57)
66.7 (10)
0.311
12.8 8.4
11.3 6.9
0.606
78.7 (85)
53.3 (8)
0.068
mGS score Surgery Experienced surgeons Transsylvian/transcortical
79/29
8/7
0.201
65.7 (71)
66.7 (10)
0.944
Packing hemostasis
61.1 (66)
86.7 (13)
0.053
Decompressive craniotomy
42.6 (46)
60.0 (9)
0.204
Operation time (minutes)
158.4 51.0
Identified responsible vessel
SBP <140 mm Hg in postoperative 2 hours
30.6 (33)
157.3 45.5 0.940 40.0 (6)
0.660
Values are number of patients, mean SD, % (number of patients), or as otherwise indicated. M, male; F, female; SBP, systolic blood pressure; CT, computed tomography; mGS, modified Graeb score; ICH, intracerebral hemorrhage. *Mann-Whitney U test. yFisher exact test.
There was no significant biological interaction between surgeon experience and surgical approach for postoperative rehemorrhage (relative excess risk because of interaction ¼ 1.990, ranged from 2.236 to 6.217; attributable proportion because of interaction ¼ 1.341, ranged from 0.9061.776).
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Table 2. Logistic Regression Analysis of Risk Factors in Postoperative Rehemorrhage Model 1
2
Variable
Table 3. Different Surgical Techniques in Experienced and General Surgeons
OR (95% CI)
P Value
Experience surgeon
0.242 (0.073e0.809)
0.021*
Transsylvian approach
0.291 (0.017e0.703)
0.045*
Symptom-surgery duration (hours)
0.809 (0.640e1.023)
0.077
Transsylvian approach
0.384 (0.124e1.187)
0.096
Packing hemostasis
4.443 (0.939e21.014)
0.060
Model 1 included age (years), sex (male/female), symptom-surgery duration (hours), ICH score, preoperative pupil dilation, presence of black hole sign or blend sign, surgical approach (transsylvian/transcortical), packing hemostasis, and surgeon experience (>15 years). The method was backward. Hosmer and Lemeshow test P value ¼ 0.947. Model 2 removed the variable surgeon experience in model 1. The method was backward. Hosmer and Lemeshow test P value ¼ 0.993. OR, odds ratio; CI, confidence interval; ICH, intracerebral hemorrhage. *Significant difference (P < 0.05).
Although the predictive factors of rebleeding or secondary hematoma expansion in conservatively treated patients have been widely studied, the studies focused on postoperative rehemorrhage SICH are still limited. It has been shown that the postoperative rehemorrhage rate in SICH is 4%e8%.7 The reported risk factors of postoperative rehemorrhage include history of diabetes mellitus,8 aspirin administration,9 early craniotomy,10 high blood pressure at admission,9 and midline shift8 and black hole sign11 in head CT scan. In this study, we focus on the immediate postoperative hemorrhage within 24 hours, which is highly associated with proper hemostasis and brain protection during the operation. These techniques are various and are relative to surgeon habit to a large extent.
Surgeon Experience Microsurgical technique is the footstone for neurosurgery. Generally, young surgeons start with traditional macrosurgery such as DC and epidural and subdural hematoma evacuation. In China, for neurosurgeons with a M.D. degree (7 or 8 years’ education), it is required that they have at least 2 years of surgical experience before they are qualified for microsurgery. Neurosurgeons have a long learning curve because microsurgery requires a high level of dexterity to handle delicate tissues. Logistic analysis has revealed that the general surgeons quadrupled the risk for postoperative hemorrhage (odds ratio, 4.132; P ¼ 0.021). The patient groups (ICH score and hematoma volume) were not a significant difference between the 2 groups of surgeons (Table 3). We found that although experienced surgeons had a longer operation time (P ¼ 0.016), they had a higher chance to locate the responsible vessel (P ¼ 0.001). In contrast, younger surgeons were more willing to stop microbleeding by packing hemostatic material in the surgical area (P ¼ 0.102), which can shorten the operation time.
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General Surgeon (n [ 30)
P Value
1.4 0.9
1.5 1.0
0.489
Volume (mL)
46.3 26.7
44.5 28.2
0.750
Postoperative rehemorrhage
8.6 (8)
30.4 (7)
0.068
164.9 53.5
137.7 30.8
0.016*
Identified responsible vessel
74.2 (69)
40.0 (12)
0.001*
Packing hemostasis
60.2 (56)
76.7 (23)
0.102
ICH score
Operation time (minutes)
Transsylvian approach
68.8 (64)
76.7 (23)
0.411
Decompressive craniotomy
43.0 (40)
50.0 (15)
0.503
Values are mean SD, % (number of patients), or as otherwise indicated ICH, intracerebral hemorrhage. *Significant difference (P < 0.05).
DISCUSSION
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Parameter
Experienced Surgeon (n [ 93)
Surgical Approach The transsylvian and transcortical approaches are 2 major techniques for accessing ICH in the basal ganglia. Complications and patient outcomes have been compared in many studies.12-14 The 2 approaches required a similar operation time in our study (158.2 minutes in the transcortical approach vs. 158.3 minutes in the transsylvian approach, P ¼ 0.996). In the transsylvian approach, the dissection of the Sylvian fissure forms a natural corridor, and the release of cerebrospinal fluid creates additional anatomic space. It is thought that this approach can lessen the use of brain retractor, decrease the risk of cerebral edema and injuries, and reduce subsequent postoperative hemorrhage.12,15 However, in our opinion, the benefit was built on a good Sylvian dissection. An inexperienced surgeon may damage the branches of the Sylvian vein. Furthermore, some may use electrocoagulation rather than compression to stop the bleeding. This may endanger the trunk and lead to catastrophic venous edema and hemorrhage. Although no significant biological interaction was indicated, logistic analysis in model 2 showed that surgeon experience acted as a suppressor variable for surgical approach. Therefore, without a sophisticated surgical technique, the advantage of the approach may turn into an obstacle instead. Responsible Vessel Intriguingly, logistic analysis has shown that identification of the responsible vessel did not reduce the occurrence for postoperative hemorrhage. First of all, the definition of responsible vessel is tricky. It was reassuring if an ejecting arteriole was discovered and coagulated definitively. However, some late hematomas may already be stable as the bleeding spot is halted.16 In this case, a suspicious clot may also be regarded to be responsible, whereas there is no other evident bleeding spot. This is indeed very subjective and may explain why this variable was not statically significant.
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ORIGINAL ARTICLE WEN-JIAN ZHENG ET AL.
REHEMORRHAGE FOR BASAL GANGLIA SICH
Rather than exactly identifying the responsible vessel, we thought that the process of seeking was more important. More experienced surgeons tended to spend additional time in reinspecting the surgical area, which increased the chance of discovering the suspicious spots. Contrarily, surgeons with less experience may easily give up searching as long as there is no visible bleeding spot, especially in the face of stress and anxiety during a long operation. Packing Hemostasis Packing hemostasis is a term we use when a surgeon fills the residual cavity with various hemostatic material. In our department, we use gelatin sponge because it has good expansibility and is low cost. The initial attempt is to create a high local pressure to prevent small, not arterial bleeding in the wound. Postoperative CT scan usually shows an obvious mass effect (Figure 1). Although it is a very common manipulation, it has not been discussed in the literature yet. Our results have indicated that this technique had run counter to surgeon expectation and increased postoperative hemorrhage (Table 2, model 2). First, packing hemostasis brought a semblance of normality, whereas the actual bleeding spot was stilled below. Before the closure, we regularly raised the systolic blood pressure to 140 mm Hg for 15 minutes to reinspect. However, some patients may have a much higher postoperative systolic blood pressure because of poor control. Hence, the arterioles without adequate hemostasis may be broken through. Second, the gelatin sponge will greatly expand after the absorption of cerebrospinal fluid and constantly rub the wound surface during each cerebral pulsation. It may cause mechanical disruption of the neighboring unstable clots, leading to rebleeding. Studies have elucidated that minimally invasive surgery does not increase rehemorrhage,17,18 suggesting compression of the gelatin sponge may not mimic the effect of the original hematoma. Therefore, when the surgeon was unconfident in hemostasis, partial removal of the hematoma may be superior to packing hemostasis after total removal.
REFERENCES 1. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9:167-176. 2. Guan J, Hawryluk GW. Targeting secondary hematoma expansion in spontaneous intracerebral hemorrhage - state of the art. Front Neurol. 2016;7: 187. 3. Morgan TC, Dawson J, Spengler D, et al. The Modified Graeb Score: an enhanced tool for intraventricular hemorrhage measurement and prediction of functional outcome. Stroke. 2013;44: 635-641. 4. McCracken DJ, Lovasik BP, McCracken CE, et al. The intracerebral hemorrhage score: a selffulfilling prophecy? Neurosurgery. 2019;84:741-748.
Perioperative Factors Studies have revealed that early surgery increases the risk of rehemorrhage.9,10 We also found a shorter symptom-surgery duration in rehemorrhage patients (P ¼ 0.188). The maximal diameter of the hematoma (P ¼ 0.260) was more relevant to postoperative rehemorrhage than its volume (P ¼ 0.557), suggesting that hematoma with a larger surface area has a higher rehemorrhage rate. Blend sign6 and black hole5 sign indicated active bleeding spots and predicted hematoma growth in medically treated patients. However, they did not predict rehemorrhage for surgically treated patients because most bleeding spots were accessed during the operation. The benefit of antihypertensive treatment in patients with SICH is still under debate.19,20 Our results show that strict control in blood pressure within 2 hours after the operation did not reduce the rehemorrhage rate. However, blood pressure control in our ICU was relatively poor, with only 31.7% of patients able to maintain their systolic blood pressure <140 mm Hg in 2 hours. This could have contributed to a higher rehemorrhage rate compared with other studies. CONCLUSIONS Surgeon experience plays the most important role in postoperative rehemorrhage. Surgeons with rich experience were willing to spend more time to achieve definitive hemostasis during operation. The use of the transsylvian approach can significantly reduce the rehemorrhage rate. Packing hemostasis with a gelatin sponge can provide a mass effect compressing the wound surface, but it did not reduce the rehemorrhage rate. Limitations The study is limited by its retrospective design and small sample size. The postoperative blood pressure control was poor, which increased bias in the comparison of other variables. Because our follow-up period was restricted in the postoperative 24 hours, patient long-term clinical outcome is unclear.
5. Li Q, Zhang G, Xiong X, et al. Black hole sign: novel imaging marker that predicts hematoma growth in patients with intracerebral hemorrhage. Stroke. 2016;47:1777-1781.
the rehaemorrhagia after surgery of hypertensive cerebral hemorrhage. Eur Rev Med Pharmacol Sci. 2015;19:795-799.
6. Li Q, Zhang G, Huang YJ, et al. Blend sign on computed tomography: novel and reliable predictor for early hematoma growth in patients with intracerebral hemorrhage. Stroke. 2015;46: 2119-2123.
10. Morgenstern LB, Demchuk AM, Kim DH, Frankowski RF, Grotta JC. Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage. Neurology. 2001;56: 1294-1299.
7. Ye Z, Ai X, Hu X, Fang F, You C. Comparison of neuroendoscopic surgery and craniotomy for supratentorial hypertensive intracerebral hemorrhage: a meta-analysis. Medicine (Baltimore). 2017; 96:e7876.
11. Shen Z, Wang L, Wu G, Li Q, Ren S, Mao Y. Computed tomographic black hole sign predicts postoperative rehemorrhage in patients with spontaneous intracranial hemorrhage following stereotactic minimally invasive surgery. World Neurosurg. 2018;120:e153-e160.
8. Ren Y, Zheng J, Liu X, Li H, You C. Risk factors of rehemorrhage in postoperative patients with spontaneous intracerebral hemorrhage: a casecontrol study. J Korean Neurosurg Soc. 2018;61:35-41. 9. Chen T, Xu G, Tan D, Wu C. Effects of platelet infusion, anticoagulant and other risk factors on
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12. Wang X, Liang H, Xu M, Shen G, Xu L. Comparison between transsylvian-transinsular and transcortical-transtemporal approach for evacuation of intracerebral hematoma. Acta Cir Bras. 2013; 28:112-118.
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13. Jianwei G, Weiqiao Z, Xiaohua Z, Qizhong L, Jiyao J, Yongming Q. Our experience of transsylvian-transinsular microsurgical approach to hypertensive putaminal hematomas. J Craniofac Surg. 2009;20:1097-1099.
17. Wang W, Zhou N, Wang C. Minimally invasive surgery for patients with hypertensive intracerebral hemorrhage with large hematoma volume: a retrospective study. World Neurosurg. 2017;105: 348-358.
14. Zhang Y, Ding W, Yang Y, Xu H, Xiong F, Liu C. Effects of transsylvian-transinsular approach to hypertensive putaminal hematoma operation and electroacupuncture on motor recovery. J Craniofac Surg. 2011;22:1626-1630.
18. Tang Y, Yin F, Fu D, Gao X, Lv Z, Li X. Efficacy and safety of minimal invasive surgery treatment in hypertensive intracerebral hemorrhage: a systematic review and meta-analysis. BMC Neurol. 2018;18:136.
15. Gao Z, Qian L, Niu C, et al. Evacuating hypertensive intracerebral hematoma with a cortical sulcus approach. World Neurosurg. 2016;95:341-347. 16. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. Stroke. 1996;27:1783-1787.
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19. Qureshi AI, Qureshi MH. Acute hypertensive response in patients with intracerebral hemorrhage pathophysiology and treatment. J Cereb Blood Flow Metab. 2018;38:1551-1563. 20. Zheng J, Li H, Lin S, et al. Perioperative antihypertensive treatment in patients with
spontaneous intracerebral hemorrhage. Stroke. 2017;48:216-218.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 11 June 2019; accepted 24 July 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.182 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.182
Impact of Surgeon Experience on Postoperative Rehemorrhage in Spontaneous Basal Ganglia Intracerebral Hemorrhage Wen-Jian Zheng, Liang-Ming Li, Yong-Hua Zhu, Zi-Hui Hu, Wei Liao, Qi-Chang Lin, Wei-Biao Lin, Zheng-Kai Zhu, Jia-Hao Su, Shao-Hua Lin
BACKGROUND: Spontaneous intracerebral hemorrhage (SICH) is of high mortality and morbidity. SICH in the basal ganglia is usually attributed to chronic hypertension. Postoperative rehemorrhage is a severe complication, and it is relative to surgical techniques.
-
METHODS: A retrospective survey was conducted on 123 patients with basal ganglia SICH who received surgery from January 2015 to January 2019. Postoperative rehemorrhage within 24 hours was recorded. Preoperative clinical parameters, surgeon experience (<10 and >20 years), operation time, surgical approach, and hemostasis technique were recorded and analyzed.
achieve definitive hemostasis in operation. The use of a transsylvian approach can significantly reduce the rehemorrhage rate. Packing hemostasis with gelatin sponge may increase complications.
-
RESULTS: The total postoperative rehemorrhage rate was 12.2% (15/123). The univariable analysis showed general surgeons had a higher postoperative rehemorrhage rate than experienced surgeons (30.4% vs. 8.6%, respectively; P [ 0.068). The operation time (minutes) in experienced surgeons was significantly longer (164.9 53.5 vs. 137.7 30.8, P [ 0.016), but they had a higher chance to locate the responsible vessel (74.2% vs. 40.0%, P [ 0.001), respectively. Logistic analysis indicated that experienced surgeons significantly reduced the risk of rehemorrhage (odds ratio [OR], 0.242; P [ 0.021). Transsylvian approach was a protective factor for postoperative rehemorrhage (OR, 0.291; P [ 0.045).
-
CONCLUSIONS: Surgeons’ experience plays the most important role in postoperative rehemorrhage. Surgeons with rich experience were willing to spend more time to
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INTRODUCTION
S
pontaneous intracerebral hemorrhage (SICH) is a devastating disease with high mortality and morbidity. The 1-month mortality rate is nearly 40%.1 Primary SICH refers to hemorrhages without an identifiable vascular malformation or coagulopathy, which is mostly attributed to chronic hypertension.2 One of the most commonly affected sites is the basal ganglia. Surgery is indicated for patients who have large blood volume and intractable intracranial pressure. However, postoperative rehemorrhage is a major complication which can dramatically worsen the outcome. Here, we present a retrospective study focusing on postoperative rehemorrhage in patients with primary SICH in the basal ganglia. MATERIALS AND METHODS A retrospective survey was conducted on 236 patients with basal ganglia SICH in our hospital from January 2015 to January 2019. Inclusion Criteria The inclusion criteria included the following: >18 years of age, indication for surgery was hematoma >30 mL or midline shift >10 mm, surgery was performed within 24 hours after symptom onset, surgery was performed in a pterional approach, and patients
Key words Basal ganglia - Postoperative rehemorrhage - Spontaneous intracerebral hemorrhage - Surgical technique
Department of Neurosurgery, Zhongshan City People’s Hospital, Zhongshan, China
Abbreviations and Acronyms CT: Computed tomography DC: Decompressive craniotomy ICH: Intracerebral hemorrhage ICU: Intensive care unit SICH: Spontaneous intracerebral hemorrhage
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WORLD NEUROSURGERY -: e1-e6, - 2019
To whom correspondence should be addressed: Wen-Jian Zheng, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.182
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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stayed in the intensive care unit (ICU) >24 hours after surgery. The family may decide to self-discharge within 24 hours when patients develop massive postoperative rehemorrhage; these patients were also included.
Exclusion Criteria The exclusion criteria included the following: history of cranial surgery, cranial radiotherapy, or cerebrovascular disease; received antiplatelet or anticoagulation treatment in the past 7 days; coagulopathy (international normalized ratio >1.5); thrombocytopenia (platelets <90,000/mm3); anemia (hemoglobin <100 g/L); renal or liver function impairment; head computed tomography (CT) scan showed lobar encephalomalacia probably because of prior injury or stroke (not including lacunar infarction); diagnosis of cerebral aneurysm, arteriovenous malformation, or Moyamoya disease; and incomplete clinical information.
Diagnosis of Postoperative Rehemorrhage Postoperative head CT scan was performed for all patients within 24 hours after surgery. Rehemorrhage was defined as a new hematoma >20 mL in the surgical area within 24 hours. We distinguished residual hematoma between rehemorrhage based on the surgeon’s surgical record (whether total evacuation of hematoma was performed) and the pre- and postoperative morphology of the hematoma. Of note, remote hemorrhage beside the surgical area or subcutaneous hemorrhage were not regarded as rehemorrhage. Patients who required reoperation in these situations were excluded.
Figure 1. (A) Packing hemostasis on postoperative head computed tomography scan. (B) Postoperative
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Data Collection Age, sex, history of hypertension, Glasgow Coma Scale score, and pupil size; blood pressure during hospitalization, hematoma diameter, volume, and modified Graeb score3; intracerebral hemorrhage (ICH) score,4 presence of black hole sign,5 or presence of blend sign6; symptom-surgery duration, surgical approach (transsylvian or transcortical), surgeon experience (3e10 or >20 years), use of packing hemostasis, and identified responsible vessel; and performance of decompressive craniotomy (DC), operation time, and postoperative blood pressure within 2 hours (whether systolic blood pressure was <140 mm Hg) were recorded. Head CT scan was evaluated by the first author (W.-J. Z.) for all cases. Hematoma volume was calculated using the ABC/2 formula. Packing hemostasis referred to evident sign (>1-cm diameter) of hemostatic material packing in the surgical area in the first postoperative head CT scan (Figure 1). Surgeons with 3e 10 years’ experience in neurosurgery were regarded as having general experience, whereas those with experience >20 years were regarded as experienced. There were 6 experienced surgeons (21e30 years’ experience) and 3 general surgeons (3, 5, and 10 years’ experience, respectively) involved in our study.
Surgical Technique The skin incision was designed depending on whether the surgeon planned to perform a DC. Usually, we tend to decompress for patients who are in a coma or with preoperative pupil dilation. In this case, an extended pterional craniotomy would be performed, and a bone flap 10- to 12-cm diameter was drilled. Otherwise, a 5- to 6-cm hook-mark skin incision was made around the pterion area, and a bone flap 3- to 5-cm diameter was drilled. All manipulation was performed under
rehemorrhage in a patient who received packing hemostasis.
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the microscope after opening the dura. A transsylvian or transcortical approach was chosen at the surgeons’ discretion. In a transcortical approach, the middle frontal gyrus or the superior temporal gyrus was the most common entry site. After dissecting the arachnoid with microscissors or a sharp scalpel, a small cortical corridor was made with a bipolar coagulator. In a transsylvian approach, the frontal side of the Sylvian vein was chosen as the entry site. The hematoma was exposed by a small incision in the insular cortex. Maximal hematoma evacuation was pursued in all cases. Squashed gelatin sponges were paved on the wound surface to achieve packing hemostasis in some cases. A drain was used in most patients, but an intracranial pressure monitor was only administrated in a few affordable patients. All patients were treated in ICU for at least 24 hours. Patients were sedated for 4e6 hours with propofol or midazolam to prevent postoperative irritability. Arterial blood pressure was monitored, and intravenous nicardipine or urapidil were used to control blood pressure at the aim of systolic blood pressure <140 mm Hg. Data Analysis Data were analyzed with SPSS 23.0 (SPSS Inc., Chicago, Illinois, USA). Statistical analyses of categorical variables were carried out using c2 tests or Fisher exact tests as appropriate. Statistics of means were carried out with independent Student t tests or nonparametric tests. Correlations of risk factors and postoperative rehemorrhage were evaluated by binary logistic regression. The odds ratio and 95% confidence interval were displayed. All statistical tests were 2-sided. P < 0.05 was considered statistically significant. RESULTS A series of 123 consecutive patients were eligible for the study. There were 90 men and 33 women, with an age range from 27 to 87 years (mean, 50.2 9.5 years). Patient information and clinical characteristics appear in Table 1. For continuous variables, values are expressed as mean SD. For dichotomous variables, values are percentage (number of patients). The total postoperative rehemorrhage rate was 12.2% (15/123). Among the 15 rehemorrhage patients, 8 patients underwent reoperation, 6 patients received conservative management, and 1 patient’s family withdrew further medical care. Univariate and Multivariate Analysis Univariate analysis showed surgeries performed by experienced surgeons had a relatively lower rehemorrhage rate (8.6% vs. 23.3%, P ¼ 0.068). Also, patients who received packing hemostasis technique were more likely to rehemorrhage (16.5% vs. 4.5%, P ¼ 0.053). For the 15 patients who developed rehemorrhage, 9 of them underwent primary DC. DC significantly reduced the reoperation rate (33.3% vs. 100.0%, P ¼ 0.028). Binary logistic analysis further confirmed that surgeon experience >20 years significantly reduced the risk of rehemorrhage. A transsylvian approach was also a protective factor for rehemorrhage (Table 2, model 1). Removal of the variable surgeon experience resulted in a decreased odds ratio of transsylvian approach (Table 2, model 2).
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Table 1. Patient Demographics and Clinical Characteristics Characteristic M/F Age (years)
None Rehemorrhage P (n [ 108) (n [ 15) Value 78/30
12/3
0.744
50.1 9.6
51.1 8.7
0.718
History of hypertension
60.2 (65)
60.0 (9)
0.989
Symptom-surgery duration (hours)
7.4 3.8
5.7 2.2
0.188*
SBP baseline (mm Hg)
196.2 33.0
Preoperative pupil dilation
24.1 (26)
46.7 (7)
0.224y
0
19.4 (21)
20.0 (3)
0.736y
1
33.3 (36)
20.0 (3)
2
37.0 (40)
46.7 (7)
3
10.2 (11)
13.3 (2)
54/54
7/8
0.809
Hematoma volume (mL)
44.6 24.3
55.0 41.4
0.557*
Maximal diameter (mm)
193.2 40.1 0.751
ICH score
Preoperative CT scan presentation Laterality (left/right)
57.3 11.7
61.8 19.0
0.260*
Midline shift (mm)
6.9 3.7
7.0 4.7
0.889
Black hole sign
27.8 (30)
33.3 (5)
0.887
Blend sign
36.1 (39)
46.7 (7)
0.429
Intraventricular hemorrhage
52.8 (57)
66.7 (10)
0.311
12.8 8.4
11.3 6.9
0.606
78.7 (85)
53.3 (8)
0.068
mGS score Surgery Experienced surgeons Transsylvian/transcortical
79/29
8/7
0.201
65.7 (71)
66.7 (10)
0.944
Packing hemostasis
61.1 (66)
86.7 (13)
0.053
Decompressive craniotomy
42.6 (46)
60.0 (9)
0.204
Operation time (minutes)
158.4 51.0
Identified responsible vessel
SBP <140 mm Hg in postoperative 2 hours
30.6 (33)
157.3 45.5 0.940 40.0 (6)
0.660
Values are number of patients, mean SD, % (number of patients), or as otherwise indicated. M, male; F, female; SBP, systolic blood pressure; CT, computed tomography; mGS, modified Graeb score; ICH, intracerebral hemorrhage. *Mann-Whitney U test. yFisher exact test.
There was no significant biological interaction between surgeon experience and surgical approach for postoperative rehemorrhage (relative excess risk because of interaction ¼ 1.990, ranged from 2.236 to 6.217; attributable proportion because of interaction ¼ 1.341, ranged from 0.9061.776).
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Table 2. Logistic Regression Analysis of Risk Factors in Postoperative Rehemorrhage Model 1
2
Variable
Table 3. Different Surgical Techniques in Experienced and General Surgeons
OR (95% CI)
P Value
Experience surgeon
0.242 (0.073e0.809)
0.021*
Transsylvian approach
0.291 (0.017e0.703)
0.045*
Symptom-surgery duration (hours)
0.809 (0.640e1.023)
0.077
Transsylvian approach
0.384 (0.124e1.187)
0.096
Packing hemostasis
4.443 (0.939e21.014)
0.060
Model 1 included age (years), sex (male/female), symptom-surgery duration (hours), ICH score, preoperative pupil dilation, presence of black hole sign or blend sign, surgical approach (transsylvian/transcortical), packing hemostasis, and surgeon experience (>15 years). The method was backward. Hosmer and Lemeshow test P value ¼ 0.947. Model 2 removed the variable surgeon experience in model 1. The method was backward. Hosmer and Lemeshow test P value ¼ 0.993. OR, odds ratio; CI, confidence interval; ICH, intracerebral hemorrhage. *Significant difference (P < 0.05).
Although the predictive factors of rebleeding or secondary hematoma expansion in conservatively treated patients have been widely studied, the studies focused on postoperative rehemorrhage SICH are still limited. It has been shown that the postoperative rehemorrhage rate in SICH is 4%e8%.7 The reported risk factors of postoperative rehemorrhage include history of diabetes mellitus,8 aspirin administration,9 early craniotomy,10 high blood pressure at admission,9 and midline shift8 and black hole sign11 in head CT scan. In this study, we focus on the immediate postoperative hemorrhage within 24 hours, which is highly associated with proper hemostasis and brain protection during the operation. These techniques are various and are relative to surgeon habit to a large extent.
Surgeon Experience Microsurgical technique is the footstone for neurosurgery. Generally, young surgeons start with traditional macrosurgery such as DC and epidural and subdural hematoma evacuation. In China, for neurosurgeons with a M.D. degree (7 or 8 years’ education), it is required that they have at least 2 years of surgical experience before they are qualified for microsurgery. Neurosurgeons have a long learning curve because microsurgery requires a high level of dexterity to handle delicate tissues. Logistic analysis has revealed that the general surgeons quadrupled the risk for postoperative hemorrhage (odds ratio, 4.132; P ¼ 0.021). The patient groups (ICH score and hematoma volume) were not a significant difference between the 2 groups of surgeons (Table 3). We found that although experienced surgeons had a longer operation time (P ¼ 0.016), they had a higher chance to locate the responsible vessel (P ¼ 0.001). In contrast, younger surgeons were more willing to stop microbleeding by packing hemostatic material in the surgical area (P ¼ 0.102), which can shorten the operation time.
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General Surgeon (n [ 30)
P Value
1.4 0.9
1.5 1.0
0.489
Volume (mL)
46.3 26.7
44.5 28.2
0.750
Postoperative rehemorrhage
8.6 (8)
30.4 (7)
0.068
164.9 53.5
137.7 30.8
0.016*
Identified responsible vessel
74.2 (69)
40.0 (12)
0.001*
Packing hemostasis
60.2 (56)
76.7 (23)
0.102
ICH score
Operation time (minutes)
Transsylvian approach
68.8 (64)
76.7 (23)
0.411
Decompressive craniotomy
43.0 (40)
50.0 (15)
0.503
Values are mean SD, % (number of patients), or as otherwise indicated ICH, intracerebral hemorrhage. *Significant difference (P < 0.05).
DISCUSSION
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Parameter
Experienced Surgeon (n [ 93)
Surgical Approach The transsylvian and transcortical approaches are 2 major techniques for accessing ICH in the basal ganglia. Complications and patient outcomes have been compared in many studies.12-14 The 2 approaches required a similar operation time in our study (158.2 minutes in the transcortical approach vs. 158.3 minutes in the transsylvian approach, P ¼ 0.996). In the transsylvian approach, the dissection of the Sylvian fissure forms a natural corridor, and the release of cerebrospinal fluid creates additional anatomic space. It is thought that this approach can lessen the use of brain retractor, decrease the risk of cerebral edema and injuries, and reduce subsequent postoperative hemorrhage.12,15 However, in our opinion, the benefit was built on a good Sylvian dissection. An inexperienced surgeon may damage the branches of the Sylvian vein. Furthermore, some may use electrocoagulation rather than compression to stop the bleeding. This may endanger the trunk and lead to catastrophic venous edema and hemorrhage. Although no significant biological interaction was indicated, logistic analysis in model 2 showed that surgeon experience acted as a suppressor variable for surgical approach. Therefore, without a sophisticated surgical technique, the advantage of the approach may turn into an obstacle instead. Responsible Vessel Intriguingly, logistic analysis has shown that identification of the responsible vessel did not reduce the occurrence for postoperative hemorrhage. First of all, the definition of responsible vessel is tricky. It was reassuring if an ejecting arteriole was discovered and coagulated definitively. However, some late hematomas may already be stable as the bleeding spot is halted.16 In this case, a suspicious clot may also be regarded to be responsible, whereas there is no other evident bleeding spot. This is indeed very subjective and may explain why this variable was not statically significant.
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ORIGINAL ARTICLE WEN-JIAN ZHENG ET AL.
REHEMORRHAGE FOR BASAL GANGLIA SICH
Rather than exactly identifying the responsible vessel, we thought that the process of seeking was more important. More experienced surgeons tended to spend additional time in reinspecting the surgical area, which increased the chance of discovering the suspicious spots. Contrarily, surgeons with less experience may easily give up searching as long as there is no visible bleeding spot, especially in the face of stress and anxiety during a long operation. Packing Hemostasis Packing hemostasis is a term we use when a surgeon fills the residual cavity with various hemostatic material. In our department, we use gelatin sponge because it has good expansibility and is low cost. The initial attempt is to create a high local pressure to prevent small, not arterial bleeding in the wound. Postoperative CT scan usually shows an obvious mass effect (Figure 1). Although it is a very common manipulation, it has not been discussed in the literature yet. Our results have indicated that this technique had run counter to surgeon expectation and increased postoperative hemorrhage (Table 2, model 2). First, packing hemostasis brought a semblance of normality, whereas the actual bleeding spot was stilled below. Before the closure, we regularly raised the systolic blood pressure to 140 mm Hg for 15 minutes to reinspect. However, some patients may have a much higher postoperative systolic blood pressure because of poor control. Hence, the arterioles without adequate hemostasis may be broken through. Second, the gelatin sponge will greatly expand after the absorption of cerebrospinal fluid and constantly rub the wound surface during each cerebral pulsation. It may cause mechanical disruption of the neighboring unstable clots, leading to rebleeding. Studies have elucidated that minimally invasive surgery does not increase rehemorrhage,17,18 suggesting compression of the gelatin sponge may not mimic the effect of the original hematoma. Therefore, when the surgeon was unconfident in hemostasis, partial removal of the hematoma may be superior to packing hemostasis after total removal.
REFERENCES 1. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9:167-176. 2. Guan J, Hawryluk GW. Targeting secondary hematoma expansion in spontaneous intracerebral hemorrhage - state of the art. Front Neurol. 2016;7: 187. 3. Morgan TC, Dawson J, Spengler D, et al. The Modified Graeb Score: an enhanced tool for intraventricular hemorrhage measurement and prediction of functional outcome. Stroke. 2013;44: 635-641. 4. McCracken DJ, Lovasik BP, McCracken CE, et al. The intracerebral hemorrhage score: a selffulfilling prophecy? Neurosurgery. 2019;84:741-748.
Perioperative Factors Studies have revealed that early surgery increases the risk of rehemorrhage.9,10 We also found a shorter symptom-surgery duration in rehemorrhage patients (P ¼ 0.188). The maximal diameter of the hematoma (P ¼ 0.260) was more relevant to postoperative rehemorrhage than its volume (P ¼ 0.557), suggesting that hematoma with a larger surface area has a higher rehemorrhage rate. Blend sign6 and black hole5 sign indicated active bleeding spots and predicted hematoma growth in medically treated patients. However, they did not predict rehemorrhage for surgically treated patients because most bleeding spots were accessed during the operation. The benefit of antihypertensive treatment in patients with SICH is still under debate.19,20 Our results show that strict control in blood pressure within 2 hours after the operation did not reduce the rehemorrhage rate. However, blood pressure control in our ICU was relatively poor, with only 31.7% of patients able to maintain their systolic blood pressure <140 mm Hg in 2 hours. This could have contributed to a higher rehemorrhage rate compared with other studies. CONCLUSIONS Surgeon experience plays the most important role in postoperative rehemorrhage. Surgeons with rich experience were willing to spend more time to achieve definitive hemostasis during operation. The use of the transsylvian approach can significantly reduce the rehemorrhage rate. Packing hemostasis with a gelatin sponge can provide a mass effect compressing the wound surface, but it did not reduce the rehemorrhage rate. Limitations The study is limited by its retrospective design and small sample size. The postoperative blood pressure control was poor, which increased bias in the comparison of other variables. Because our follow-up period was restricted in the postoperative 24 hours, patient long-term clinical outcome is unclear.
5. Li Q, Zhang G, Xiong X, et al. Black hole sign: novel imaging marker that predicts hematoma growth in patients with intracerebral hemorrhage. Stroke. 2016;47:1777-1781.
the rehaemorrhagia after surgery of hypertensive cerebral hemorrhage. Eur Rev Med Pharmacol Sci. 2015;19:795-799.
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10. Morgenstern LB, Demchuk AM, Kim DH, Frankowski RF, Grotta JC. Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage. Neurology. 2001;56: 1294-1299.
7. Ye Z, Ai X, Hu X, Fang F, You C. Comparison of neuroendoscopic surgery and craniotomy for supratentorial hypertensive intracerebral hemorrhage: a meta-analysis. Medicine (Baltimore). 2017; 96:e7876.
11. Shen Z, Wang L, Wu G, Li Q, Ren S, Mao Y. Computed tomographic black hole sign predicts postoperative rehemorrhage in patients with spontaneous intracranial hemorrhage following stereotactic minimally invasive surgery. World Neurosurg. 2018;120:e153-e160.
8. Ren Y, Zheng J, Liu X, Li H, You C. Risk factors of rehemorrhage in postoperative patients with spontaneous intracerebral hemorrhage: a casecontrol study. J Korean Neurosurg Soc. 2018;61:35-41. 9. Chen T, Xu G, Tan D, Wu C. Effects of platelet infusion, anticoagulant and other risk factors on
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12. Wang X, Liang H, Xu M, Shen G, Xu L. Comparison between transsylvian-transinsular and transcortical-transtemporal approach for evacuation of intracerebral hematoma. Acta Cir Bras. 2013; 28:112-118.
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13. Jianwei G, Weiqiao Z, Xiaohua Z, Qizhong L, Jiyao J, Yongming Q. Our experience of transsylvian-transinsular microsurgical approach to hypertensive putaminal hematomas. J Craniofac Surg. 2009;20:1097-1099.
17. Wang W, Zhou N, Wang C. Minimally invasive surgery for patients with hypertensive intracerebral hemorrhage with large hematoma volume: a retrospective study. World Neurosurg. 2017;105: 348-358.
14. Zhang Y, Ding W, Yang Y, Xu H, Xiong F, Liu C. Effects of transsylvian-transinsular approach to hypertensive putaminal hematoma operation and electroacupuncture on motor recovery. J Craniofac Surg. 2011;22:1626-1630.
18. Tang Y, Yin F, Fu D, Gao X, Lv Z, Li X. Efficacy and safety of minimal invasive surgery treatment in hypertensive intracerebral hemorrhage: a systematic review and meta-analysis. BMC Neurol. 2018;18:136.
15. Gao Z, Qian L, Niu C, et al. Evacuating hypertensive intracerebral hematoma with a cortical sulcus approach. World Neurosurg. 2016;95:341-347. 16. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. Stroke. 1996;27:1783-1787.
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19. Qureshi AI, Qureshi MH. Acute hypertensive response in patients with intracerebral hemorrhage pathophysiology and treatment. J Cereb Blood Flow Metab. 2018;38:1551-1563. 20. Zheng J, Li H, Lin S, et al. Perioperative antihypertensive treatment in patients with
spontaneous intracerebral hemorrhage. Stroke. 2017;48:216-218.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 11 June 2019; accepted 24 July 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.182 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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