- Email: [email protected]
Comparison of Acute Moyamoya Disease−Related and Idiopathic Primary Intraventricular Hemorrhage in Adult Patients
Original Article
Comparison of Acute Moyamoya DiseaseRelated and Idiopathic Primary Intraventricular Hemorrhage in Adult Patients Zhiyuan Yu1, Rui Guo1, Jun Zheng1, Mou Li2, Dingke Wen1, Hao Li1, Chao You1, Lu Ma1
OBJECTIVE: Primary intraventricular hemorrhage (PIVH) is a rare condition in adult patients. PIVH occurs frequently in adult hemorrhagic Moyamoya disease (MMD). Idiopathic PIVH is defined as PIVH without cerebrovascular abnormalities. This study is aimed to compare the baseline characteristics and outcomes of acute MMD-related and idiopathic PIVH.
-
METHODS: Adult patients with acute MMD-related or idiopathic PIVH were retrospectively included. Baseline characteristics and outcomes at discharge were obtained and compared. Chi-square test, Student’s t-test, or ranksum test were used in statistical analyses.
-
RESULTS: This study finally included 32 patients with acute MMD-related PIVH and 112 with acute idiopathic PIVH. Patients with acute MMD-related PIVH were significantly younger (53.3 15.8 vs. 42.8 12.2 years, P < 0.001). The admission systolic blood pressure in patients with acute idiopathic PIVH was significantly higher (161.7 30.9 vs. 134.6 24.6 mm Hg, P < 0.001). Patients with acute idiopathic PIVH had significantly higher admission serum urea (5.68 2.66 vs. 4.34 1.62 mmol/L, P [ 0.008), cystatin C (0.97 0.72 vs. 0.68 0.16 mg/L, P [ 0.023), and uric acid (309.01 105.97 vs. 242.24 77.65 mmol/L, P [ 0.001). In patients with acute MMD-related PIVH, only one (3.1%) patient was dead at discharge. In contrast, a total of 22 (19.6%) patients with acute idiopathic patients died at discharge (P [ 0.027).
-
function. Moreover, patients with acute MMD-related PIVH have lower short-term mortality.
INTRODUCTION
P
rimary intraventricular hemorrhage (PIVH), which refers to intraventricular hemorrhage without any intraparenchymal hemorrhage and subarachnoid hemorrhage, is a rare condition in adult patients.1 In some patients with PIVH, cerebrovascular abnormalities can be found, such as intracranial aneurysm, arteriovenous malformation, and moyamoya disease (MMD).2 MMD is a rare cerebrovascular disease with chronic occlusion of the terminal part of internal carotid arteries.3 Hemorrhage MMD is a subtype of this uncommon disease, and PIVH is relatively frequent in adult patients with hemorrhagic MMD.4,5 Nah et al6 reported that PIVH occurs in about 37.6% of patients with MMD-related intracerebral hemorrhage. In contrast, cerebrovascular abnormalities are not identified in some PIVH patients, which is defined as idiopathic PIVH.7 Although MMD-related PIVH shares similar imaging manifestations with idiopathic PIVH, its characteristics and outcomes can be different.8 However, the study comparing MMD-related and idiopathic PIVH is still lacking. Therefore this study is aimed to compare the baseline characteristics and outcomes of acute MMD-related and idiopathic PIVH. MATERIAL AND METHODS
-
CONCLUSIONS: Compared with patients with acute idiopathic PIVH, patients with acute MMD-related PIVH have younger age, lower blood pressure, and better renal
Study Design Patients admitted to West China Hospital, Sichuan University between January 2010 and September 2018 were retrospectively
Key words - Characteristics - Moyamoya disease - Outcome - Primary intraventricular hemorrhage
From the Departments of 1Neurosurgery and 2Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Abbreviations and Acronyms CT: Computed tomography GCS: Glasgow Coma Scale MMD: Moyamoya disease mGS: Modified Graeb score mRS: Modified Rankin Scale PIVH: Primary intraventricular hemorrhage
WORLD NEUROSURGERY -: e1-e6, - 2019
To whom correspondence should be addressed: Lu Ma, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.070 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
reviewed. The inclusion criteria were 1) adult patients admitted to our hospital in acute phase after PIVH (72 hours after onset of initial symptoms); 2) PIVH confirmed by admission computed tomography (CT) scan, without intraparenchymal hemorrhage or subarachnoid hemorrhage; 3) MMD-related PIVH defined as PIVH related to angiographically confirmed MMD (Figure 1); and 4) idiopathic PIVH defined as PIVH without any structural cerebrovascular abnormality, such as intracranial aneurysm, arteriovenous malformation, moyamoya disease, trauma, and brain tumor (Figure 2). Patients diagnosed with moyamoya-like disease or moyamoya syndrome were excluded.
02. In contrast, unfavorable functional outcome was defined as mRS score 36. Statistics Data were described as frequency, mean standard deviation, or median (interquartile range) if proper. Chi-square test, Student’s t-test, or rank-sum test were used in statistical analyses based on the various categories of data. All statistical analyses were performed using SPSS 24.0. If P < 0.05, it was considered as statistically significant. RESULTS
Baseline Characteristics Baseline characteristics of included patients were obtained via reviewing medical records including age, gender, admission Glasgow Coma Scale (GCS) score, blood pressure, main medical histories, and important laboratory data. Serum urea, creatinine, cystatin C, and uric acid were routinely examined at admission in our hospital and used to evaluate patients’ renal function. On the basis of admission CT scan, modified Graeb score (mGS) and hydrocephalus were assessed. Treatment In our hospital, treatment for patients with PIVH was decided by a team of experienced neurosurgeons and neurologists. Informed consent was obtained before any treatment. If necessary, surgical treatment including surgical hematoma evacuation, external ventricular drainage, or lumbar drainage could be performed. Information about treatment was collected using medical records. Outcomes at Discharge On the basis of medical records, mortality, modified Rankin Scale (mRS) score, pneumonia, and any infection at discharge were collected. Favorable functional outcome was defined as mRS score
Figure 1. Illustrative example for acute moyamoya disease-related primary intraventricular hemorrhage. (A) Primary intraventricular hemorrhage shown on
e2
www.SCIENCEDIRECT.com
Between January 2010 and September 2018, we finally found 32 patients with acute MMD-related PIVH in our hospital. In the same period, a total of 112 patients were found to have acute idiopathic PIVH. Thus we compared the baseline characteristics and outcomes in these 144 patients. Baseline Clinical Characteristics Comparing with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH were significantly younger (53.3 15.8 vs. 42.8 12.2 years, P < 0.001). In patients with acute MMDrelated PIVH, 62.5% of them were female. In contrast, only 43.8% of patients with acute idiopathic PIVH were female (P ¼ 0.061). The median admission GCS score was 12 (8.25, 15) in patients with acute MMD-related PIVH and 11.5 (9, 15) in patients with acute idiopathic PIVH (P ¼ 0.749). The admission systolic blood pressure in patients with acute idiopathic PIVH was significantly higher than in those with acute MMD-related PIVH (161.7 30.9 vs. 134.6 24.6 mm Hg, P < 0.001). Moreover, the admission diastolic blood pressure in patients with acute idiopathic PIVH was also significantly higher than in those with acute MMDrelated PIVH (93.8 19.6 vs. 79.2 19.1 mm Hg, P < 0.001). In patients with acute MMD-related PIVH, the history of
computed tomography scan. (B) Moyamoya disease confirmed by digital subtraction angiography.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Figure 2. Illustrative example for acute idiopathic primary intraventricular hemorrhage. (A) Primary intraventricular hemorrhage shown on computed
hypertension was significantly less frequent than in those with acute idiopathic PIVH (18.8% vs. 52.7%, P ¼ 0.001). (Table 1)
Baseline Imaging Characteristics In patients with acute MMD-related PIVH, the median mGS was 18.5 (15, 22.75). In contrast, the median mGS was 17 (11, 21) in patients with acute idiopathic PIVH (P ¼ 0.107). There were 9 (28.1%) cases of hydrocephalus in acute MMD-related PIVH and 23 (20.5%) in acute idiopathic PIVH (P ¼ 0.362) (Table 1).
tomography scan. (B) No structural cerebrovascular abnormality is shown on digital subtraction angiography.
Baseline Laboratory Data In patients with acute idiopathic PIVH, the baseline platelet count was lower than in those with acute MMD-related PIVH, but not significantly (158.86 66.87 vs. 181.53 54.94 109/l, P ¼ 0.082). In addition, patients with acute MMD-related PIVH had lower admission blood glucose than those with acute idiopathic PIVH, but not significantly (7.62 2.05 vs. 8.76 3.56 mmol/L, P ¼ 0.087). Patients with acute idiopathic PIVH had significantly higher admission serum urea than those with MMD-related PIVH (5.68 2.66 vs. 4.34 1.62 mmol/L, P ¼ 0.008). The level of
Table 1. Baseline Clinical and Imaging Characteristics MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
42.8 12.2
53.3 15.8
<0.001
20
49
0.061
GCS score
12 (8.25, 15)
11.5 (9, 15)
0.749
SBP, mm Hg
134.6 24.6
161.7 30.9
<0.001
DBP, mm Hg
79.2 19.1
93.8 19.6
<0.001
Age, year Female
Hypertension
6
59
0.001
Diabetes mellitus
1
12
0.298
Previous stroke
5
10
0.274
Smoking
6
32
0.266
Alcohol abuse
7
28
0.716
18.5 (15, 22.75)
17 (11, 21)
0.107
9
23
0.362
mGS Hydrocephalus
Data are mean standard deviation, median and interquartile range, or number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; GCS, Glasgow Coma Scale; SBP, systolic blood pressure; DBP, diastolic blood pressure; mGS, modified Graeb score.
WORLD NEUROSURGERY -: e1-e6, - 2019
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Table 2. Baseline Laboratory Data
RBC, 1012/L 9
WBC, 10 /L PLT, 109/L BG, mmol/L Urea, mmol/L Scr, mmol/L
MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
4.45 0.61
4.42 0.77
0.812
14.34 5.36
12.37 6.55
0.123
181.53 54.94
158.86 66.87
0.082
7.62 2.05
8.76 3.56
0.087
4.34 1.62
5.68 2.66
0.008
63.66 18.39
89.38 78.26
0.068
Cystatin C, mg/L
0.68 0.16
0.97 0.72
0.023
Uric acid, mmol/L
242.24 77.65
309.01 105.97
0.001
PT, s
11.83 1.05
12.29 4.14*
0.542
APTT, s
25.81 3.94
27.55 15.94*
0.542
INR
1.03 0.09
1.09 0.37*
0.439
MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; RBC, red blood cell; WBC, white blood cell; PLT, platelet count; BG, blood glucose; Scr, serum creatinine; PT, prothrombin time; APTT, activated partial thromboplastin time; INR, international normalized ratio; s, seconds. *Available in 110 patients. Data are mean standard deviation, median and interquartile range, or number of patients.
serum creatinine in patients with acute idiopathic PIVH was also higher than in those with MMD-related PIVH, but not significantly (89.38 78.26 vs. 63.66 18.39 mmol/L, P ¼ 0.068). Moreover, the levels admission serum cystatin C was also different in patients with acute MMD-related and idiopathic PIVH (0.68 0.16 vs. 0.97 0.72 mg/L, P ¼ 0.023). In addition, patients with acute MMDrelated PIVH had significantly lower admission serum uric acid than those with acute idiopathic PIVH (242.24 77.65 vs. 309.01 105.97 mmol/L, P ¼ 0.001) (Table 2).
Treatment In patients with acute MMD-related PIVH, 24 (75.0%) patients received conservative treatment, 1 (3.1%) received hematoma evacuation, 4 (12.5%) received external ventricular drainage, 1 (3.1%) received lumbar drainage, and 2 (6.3%) received both external ventricular drainage and lumbar drainage. In contrast, in patients with acute idiopathic PIVH, 78 (69.6%) patients received conservative treatment, 6 (5.4%) received hematoma evacuation, 17 (15.2%) received external ventricular drainage, 8 (7.1%) received lumbar drainage, and 3 (2.7%) received both external ventricular drainage and lumbar drainage (Table 3).
Outcomes at Discharge In patients with acute MMD-related PIVH, only one (3.1%) patient was dead at discharge. In contrast, a total of 22 (19.6%) patients with acute idiopathic PIVH died at discharge (P ¼ 0.027). There were 14 (43.8%) cases with unfavorable functional outcome at discharge in patients acute MMD-related PIVH. Among patients with acute idiopathic PIVH, 51 (45.5%) had unfavorable functional outcome at discharge (P ¼ 0.858). Patients with acute MMD-related and idiopathic PIVH had similar incidences of pneumonia or any infection at discharge (Table 4).
e4
www.SCIENCEDIRECT.com
DISCUSSION This study compared the characteristics and outcomes of MMDrelated and idiopathic PIVH in the acute phase. Comparing with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH were significantly younger (P < 0.001) and had significantly lower admission systolic blood pressure (P < 0.001) and diastolic blood pressure (P < 0.001). Moreover, patients with acute idiopathic PIVH had significantly higher levels of admission serum urea (P ¼ 0.008), cystatin C (P ¼ 0.023), and uric acid (P ¼ 0.001) than those with acute MMD-related PIVH. In addition, patients with acute MMD-related PIVH had significantly lower mortality at discharge than patients with acute idiopathic PIVH (P ¼ 0.027). PIVH is a rare cerebrovascular disorder adult patients.9 A study using diffusion tensor imaging showed the white matter injury in periventricular area after PIVH.10 Moreover, PIVH may be related to various etiologies.11A retrospective study by Passero et al12 showed
Table 3. Treatment MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
Conservative treatment
24
78
Hematoma evacuation
1
6
EVD
4
17
LD
1
8
EVD þ LD
2
3
Data are number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; EVD, external ventricular drainage; LD, lumbar drainage.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Table 4. Outcomes at Discharge MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
Death
1
22
0.027
Unfavorable functional outcome
14
51
0.858
Pneumonia
4
19
0.785
Any infection
5
21
0.685
Data are number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage.
that vascular malformation was found in 31% of PIVH patients. Flint et al13 reported that about 56% of PIVH patients had positive results in angiographic examinations, and the most common cause was arteriovenous malformation. In contrast, Zhang et al2 suggested that vascular malformation could be found in 53.3% of patients with PIVH and MMD was the most common vascular malformation in PIVH patients in a Chinese population. MMD is a unique cerebrovascular disease that is more common in Asian countries.14 MMD has different subtypes including ischemic MMD, hemorrhagic MMD, and asymptomatic MMD.15 Hemorrhagic MMD is more common in adult patients.16 In adult patients with hemorrhagic MMD, PIVH is relatively common.4,5,17 Therefore in order to have a better understanding of hemorrhagic MMD, it is important to explore the characteristics of MMD-related PIVH. In this study, we found 32 patients with acute MMD-related PIVH. Hypertension was not common in acute MMD-related PIVH. Moreover, short-term mortality in these patients was low (3.1%). In contrast, no cerebrovascular abnormality can be found in some PIVH patients, which is defined as idiopathic PIVH.7 Hypertension is the main cause for idiopathic PIVH.7 In Zhang et al’s2 study, patients with idiopathic PIVH had younger age and more frequent presence of hypertension than those with different cerebrovascular abnormalities. However, those studies did not focus on the acute phase after PIVH and the difference between MMD-related and idiopathic PIVH was not well described. This study included 32 patients with acute MMD-related PIVH and 112 patients with acute idiopathic PIVH. Patients with acute idiopathic PIVH had significantly older age and higher admission blood pressure than those with acute MMDrelated PIVH. Moreover, we found patients with acute idiopathic PIVH had significantly higher levels of biomarkers for renal function than patients with acute MMD-related PIVH. In addition, patients with acute idiopathic PIVH had significantly higher mortality at discharge than those with acute MMD-related PIVH. Thus although patients with acute MMD-related and idiopathic PIVH have similar features on admission CT scan, their clinical characteristics and outcomes are different. The optimal treatment for intraventricular hemorrhage is still controversial.18 In the study by Hanley et al19 comparing external ventricular drainage alone, external ventricular drainage plus intraventricular fibrinolysis could significantly reduce mortality, but not significantly improve functional outcome, in patients with severe intraventricular hemorrhage. A meta-analysis suggested that intraventricular fibrinolysis could decrease morality
WORLD NEUROSURGERY -: e1-e6, - 2019
and potentially improve functional outcome in patients with intraventricular hemorrhage.20 In Staykov et al’s21 study, intraventricular fibrinolysis plus lumbar drainage could be a better treatment than intraventricular fibrinolysis in patients with severe intraventricular hemorrhage. Song et al22 suggested that endoscopic surgery could have the better performance in hematoma removal and outcome improvement than external ventricular drainage in patients with severe intraventricular hemorrhage. However, the evidence for management of acute MMD-related and idiopathic PIVH is still lacking. This study showed that conservative treatment, hematoma evacuation, external ventricular drainage, lumbar drainage, or combination of external ventricular drainage and lumbar drainage could be adopted in patients with acute MMD-related or idiopathic PIVH on the basis of the individual condition of each patient. However, the optimal treatment for these patients in the acute phase should be explored in further studies. Although patients with acute MMD-related PIVH had lower mortality at discharge than those with acute idiopathic PIVH in this study, it does not mean patients with acute MMD-related PIVH have good long-term outcome. In Nah et al’s6 study, patients with hemorrhagic MMD had a higher rate of rebleeding than those with spontaneous intracerebral hemorrhage. To improve their long-term outcome, surgical revascularization after acute phase can be necessary.23 Jiang et al24 reported that bypass surgery can decrease rebleeding rate in patients with hemorrhagic MMD. The study by Jo et al25 showed that surgical revascularization may decrease the risk of recurrent stroke via correcting abnormal perfusion. Hence although patients with acute MMD-related PIVH may have relatively good short-term outcome, appropriate treatment after acute phase of PIVH is crucial for improving their long-term outcome. Comparing with patients who had acute MMD-related PIVH, patients with acute idiopathic PIVH had higher short-term mortality, which could be related to their different baseline characteristics. This study showed that patients with idiopathic PIVH had a higher burden of blood pressure. Higher blood pressure is correlated with poor outcome after hemorrhagic stroke.26 However, the role of intensive blood pressure reduction is still controversial in the management of intracerebral hemorrhage.27,28 For patients with acute idiopathic PIVH, early blood pressure control is reasonable but the optimal target should be explored further. This study also showed that patients with acute idiopathic patients had worse renal function. Previous studies have shown that biomarkers for renal function are related to outcome in intracerebral hemorrhage.29,30 Therefore renal function should be noticed in the management of patients with acute idiopathic PIVH. This study has some limitations. First, this retrospective study was conducted in a single center and the sample size was still small, which could affect its reliability. Second, the long-term outcome was insufficient for analysis. Therefore the results in this study should be confirmed by further studies. CONCLUSIONS Compared with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH have younger age, lower admission blood pressure, and better renal function. Moreover, patients with acute MMD-related PIVH have lower short-term mortality.
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
REFERENCES 1. Weinstein R, Ess K, Sirdar B, Song S, Cutting S. Primary intraventricular hemorrhage: clinical characteristics and outcomes. J Stroke Cerebrovasc Dis. 2017;26:995-999. 2. Zhang S, Jia B, Li H, You C, Hanley DF, Jiang Y. Primary intraventricular hemorrhage in adults: etiological causes and prognostic factors in Chinese population. J Neurol. 2017;264:382-390. 3. Fujimura M, Bang OY, Kim JS. Moyamoya disease. Front Neurol Neurosci. 2016;40:204-220. 4. Ge P, Zhang Q, Ye X, et al. Clinical features of hemorrhagic moyamoya disease in China. World Neurosurg. 2017;106:224-230. 5. Jang DK, Lee KS, Rha HK, et al. Clinical and angiographic features and stroke types in adult moyamoya disease. AJNR Am J Neuroradiol. 2014;35: 1124-1131. 6. Nah HW, Kwon SU, Kang DW, Ahn JS, Kwun BD, Kim JS. Moyamoya disease-related versus primary intracerebral hemorrhage: [corrected] location and outcomes are different. Stroke. 2012;43: 1947-1950. 7. Guo R, Ma L, Shrestha BK, Yu Z, Li H, You C. A retrospective clinical study of 98 adult idiopathic primary intraventricular hemorrhage cases. Medicine. 2016;95:e5089. 8. Lee SH, Park KJ, Park DH, Kang SH, Park JY, Chung YG. Factors associated with clinical outcomes in patients with primary intraventricular hemorrhage. Med Sci Monitor. 2017;23:1401-1412. 9. Giray S, Sen O, Sarica FB, et al. Spontaneous primary intraventricular hemorrhage in adults: clinical data, etiology and outcome. Turk Neurosurg. 2009;19:338-344. 10. Yeo SS, Choi BY, Chang CH, et al. Periventricular white matter injury by primary intraventricular hemorrhage: a diffusion tensor imaging study. Eur Neurol. 2011;66:235-241. 11. Angelopoulos M, Gupta SR, Azat Kia B. Primary intraventricular hemorrhage in adults: clinical features, risk factors, and outcome. Surg Neurol. 1995;44:433-436. 12. Passero S, Ulivelli M, Reale F. Primary intraventricular haemorrhage in adults. Acta Neurol Scand. 2002;105:115-119.
e6
www.SCIENCEDIRECT.com
13. Flint AC, Roebken A, Singh V. Primary intraventricular hemorrhage: yield of diagnostic angiography and clinical outcome. Neurocrit Care. 2008;8: 330-336.
24. Jiang H, Ni W, Xu B, et al. Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg. 2014;121:1048-1055.
14. Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7:1056-1066.
25. Jo KI, Kim MS, Yeon JY, Kim JS, Hong SC. Recurrent bleeding in hemorrhagic moyamoya disease: prognostic implications of the perfusion status. J Kor Neurosurg Soc. 2016;59:117-121.
15. Wan M, Duan L. Recent progress in hemorrhagic moyamoya disease. Br J Neurosurg. 2015;29:189-191. 16. Miyamoto S, Yoshimoto T, Hashimoto N, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45:1415-1421.
26. Butcher KS, Jeerakathil T, Hill M, et al. The Intracerebral Hemorrhage Acutely Decreasing Arterial Pressure Trial. Stroke. 2013;44:620-626. 27. Qureshi AI, Palesch YY, Barsan WG, et al. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med. 2016;375: 1033-1043.
17. Li Q, Qu L, Yuan Y, et al. Analysis of the clinical characteristics of hemorrhagic moyamoya disease in the Jilin province of northeastern China: a single-center study of 212 cases. Biomed Rep. 2018; 8:191-197.
28. Anderson CS, Heeley E, Huang Y, et al. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med. 2013;368: 2355-2365.
18. Garton T, Hua Y, Xiang J, Xi G, Keep RF. Challenges for intraventricular hemorrhage research and emerging therapeutic targets. Expert Opin Therapeut Targets. 2017;21:1111-1122.
29. You S, Shi L, Zhong C, et al. Prognostic significance of estimated glomerular filtration rate and cystatin c in patients with acute intracerebral hemorrhage. Cerebrovasc Dis (Basel, Switzerland). 2016;42:455-463.
19. Hanley DF, Lane K, McBee N, et al. Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial. Lancet (London, England). 2017; 389:603-611.
30. Kim JK, Shin JJ, Park SK, Hwang YS, Kim TH, Shin HS. Prognostic factors and clinical outcomes of acute intracerebral hemorrhage in patients with chronic kidney disease. J Kor Neurosurg Soc. 2013; 54:296-301.
20. Baker AD, Rivera Perla KM, Yu Z, et al. Fibrinolytic for treatment of intraventricular hemorrhage: a meta-analysis and systematic review. Int J Stroke. 2018;13:11-23. 21. Staykov D, Kuramatsu JB, Bardutzky J, et al. Efficacy and safety of combined intraventricular fibrinolysis with lumbar drainage for prevention of permanent shunt dependency after intracerebral hemorrhage with severe ventricular involvement: a randomized trial and individual patient data metaanalysis. Ann Neurol. 2017;81:93-103. 22. Song P, Duan FL, Cai Q, et al. Endoscopic surgery versus external ventricular drainage surgery for severe intraventricular hemorrhage. Curr Med Sci. 2018;38:880-887.
Conflict of interest statement: No funding was received, and the authors report no conflicts of interest. Received 4 December 2018; accepted 5 January 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.070 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
23. Jiang H, Yang H, Ni W, et al. Long-term outcomes after combined revascularization surgery in adult hemorrhagic moyamoya disease. World Neurosurg. 2018;116:e1032-e1041.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070
Comparison of Acute Moyamoya DiseaseRelated and Idiopathic Primary Intraventricular Hemorrhage in Adult Patients Zhiyuan Yu1, Rui Guo1, Jun Zheng1, Mou Li2, Dingke Wen1, Hao Li1, Chao You1, Lu Ma1
OBJECTIVE: Primary intraventricular hemorrhage (PIVH) is a rare condition in adult patients. PIVH occurs frequently in adult hemorrhagic Moyamoya disease (MMD). Idiopathic PIVH is defined as PIVH without cerebrovascular abnormalities. This study is aimed to compare the baseline characteristics and outcomes of acute MMD-related and idiopathic PIVH.
-
METHODS: Adult patients with acute MMD-related or idiopathic PIVH were retrospectively included. Baseline characteristics and outcomes at discharge were obtained and compared. Chi-square test, Student’s t-test, or ranksum test were used in statistical analyses.
-
RESULTS: This study finally included 32 patients with acute MMD-related PIVH and 112 with acute idiopathic PIVH. Patients with acute MMD-related PIVH were significantly younger (53.3 15.8 vs. 42.8 12.2 years, P < 0.001). The admission systolic blood pressure in patients with acute idiopathic PIVH was significantly higher (161.7 30.9 vs. 134.6 24.6 mm Hg, P < 0.001). Patients with acute idiopathic PIVH had significantly higher admission serum urea (5.68 2.66 vs. 4.34 1.62 mmol/L, P [ 0.008), cystatin C (0.97 0.72 vs. 0.68 0.16 mg/L, P [ 0.023), and uric acid (309.01 105.97 vs. 242.24 77.65 mmol/L, P [ 0.001). In patients with acute MMD-related PIVH, only one (3.1%) patient was dead at discharge. In contrast, a total of 22 (19.6%) patients with acute idiopathic patients died at discharge (P [ 0.027).
-
function. Moreover, patients with acute MMD-related PIVH have lower short-term mortality.
INTRODUCTION
P
rimary intraventricular hemorrhage (PIVH), which refers to intraventricular hemorrhage without any intraparenchymal hemorrhage and subarachnoid hemorrhage, is a rare condition in adult patients.1 In some patients with PIVH, cerebrovascular abnormalities can be found, such as intracranial aneurysm, arteriovenous malformation, and moyamoya disease (MMD).2 MMD is a rare cerebrovascular disease with chronic occlusion of the terminal part of internal carotid arteries.3 Hemorrhage MMD is a subtype of this uncommon disease, and PIVH is relatively frequent in adult patients with hemorrhagic MMD.4,5 Nah et al6 reported that PIVH occurs in about 37.6% of patients with MMD-related intracerebral hemorrhage. In contrast, cerebrovascular abnormalities are not identified in some PIVH patients, which is defined as idiopathic PIVH.7 Although MMD-related PIVH shares similar imaging manifestations with idiopathic PIVH, its characteristics and outcomes can be different.8 However, the study comparing MMD-related and idiopathic PIVH is still lacking. Therefore this study is aimed to compare the baseline characteristics and outcomes of acute MMD-related and idiopathic PIVH. MATERIAL AND METHODS
-
CONCLUSIONS: Compared with patients with acute idiopathic PIVH, patients with acute MMD-related PIVH have younger age, lower blood pressure, and better renal
Study Design Patients admitted to West China Hospital, Sichuan University between January 2010 and September 2018 were retrospectively
Key words - Characteristics - Moyamoya disease - Outcome - Primary intraventricular hemorrhage
From the Departments of 1Neurosurgery and 2Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Abbreviations and Acronyms CT: Computed tomography GCS: Glasgow Coma Scale MMD: Moyamoya disease mGS: Modified Graeb score mRS: Modified Rankin Scale PIVH: Primary intraventricular hemorrhage
WORLD NEUROSURGERY -: e1-e6, - 2019
To whom correspondence should be addressed: Lu Ma, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.070 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
reviewed. The inclusion criteria were 1) adult patients admitted to our hospital in acute phase after PIVH (72 hours after onset of initial symptoms); 2) PIVH confirmed by admission computed tomography (CT) scan, without intraparenchymal hemorrhage or subarachnoid hemorrhage; 3) MMD-related PIVH defined as PIVH related to angiographically confirmed MMD (Figure 1); and 4) idiopathic PIVH defined as PIVH without any structural cerebrovascular abnormality, such as intracranial aneurysm, arteriovenous malformation, moyamoya disease, trauma, and brain tumor (Figure 2). Patients diagnosed with moyamoya-like disease or moyamoya syndrome were excluded.
02. In contrast, unfavorable functional outcome was defined as mRS score 36. Statistics Data were described as frequency, mean standard deviation, or median (interquartile range) if proper. Chi-square test, Student’s t-test, or rank-sum test were used in statistical analyses based on the various categories of data. All statistical analyses were performed using SPSS 24.0. If P < 0.05, it was considered as statistically significant. RESULTS
Baseline Characteristics Baseline characteristics of included patients were obtained via reviewing medical records including age, gender, admission Glasgow Coma Scale (GCS) score, blood pressure, main medical histories, and important laboratory data. Serum urea, creatinine, cystatin C, and uric acid were routinely examined at admission in our hospital and used to evaluate patients’ renal function. On the basis of admission CT scan, modified Graeb score (mGS) and hydrocephalus were assessed. Treatment In our hospital, treatment for patients with PIVH was decided by a team of experienced neurosurgeons and neurologists. Informed consent was obtained before any treatment. If necessary, surgical treatment including surgical hematoma evacuation, external ventricular drainage, or lumbar drainage could be performed. Information about treatment was collected using medical records. Outcomes at Discharge On the basis of medical records, mortality, modified Rankin Scale (mRS) score, pneumonia, and any infection at discharge were collected. Favorable functional outcome was defined as mRS score
Figure 1. Illustrative example for acute moyamoya disease-related primary intraventricular hemorrhage. (A) Primary intraventricular hemorrhage shown on
e2
www.SCIENCEDIRECT.com
Between January 2010 and September 2018, we finally found 32 patients with acute MMD-related PIVH in our hospital. In the same period, a total of 112 patients were found to have acute idiopathic PIVH. Thus we compared the baseline characteristics and outcomes in these 144 patients. Baseline Clinical Characteristics Comparing with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH were significantly younger (53.3 15.8 vs. 42.8 12.2 years, P < 0.001). In patients with acute MMDrelated PIVH, 62.5% of them were female. In contrast, only 43.8% of patients with acute idiopathic PIVH were female (P ¼ 0.061). The median admission GCS score was 12 (8.25, 15) in patients with acute MMD-related PIVH and 11.5 (9, 15) in patients with acute idiopathic PIVH (P ¼ 0.749). The admission systolic blood pressure in patients with acute idiopathic PIVH was significantly higher than in those with acute MMD-related PIVH (161.7 30.9 vs. 134.6 24.6 mm Hg, P < 0.001). Moreover, the admission diastolic blood pressure in patients with acute idiopathic PIVH was also significantly higher than in those with acute MMDrelated PIVH (93.8 19.6 vs. 79.2 19.1 mm Hg, P < 0.001). In patients with acute MMD-related PIVH, the history of
computed tomography scan. (B) Moyamoya disease confirmed by digital subtraction angiography.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Figure 2. Illustrative example for acute idiopathic primary intraventricular hemorrhage. (A) Primary intraventricular hemorrhage shown on computed
hypertension was significantly less frequent than in those with acute idiopathic PIVH (18.8% vs. 52.7%, P ¼ 0.001). (Table 1)
Baseline Imaging Characteristics In patients with acute MMD-related PIVH, the median mGS was 18.5 (15, 22.75). In contrast, the median mGS was 17 (11, 21) in patients with acute idiopathic PIVH (P ¼ 0.107). There were 9 (28.1%) cases of hydrocephalus in acute MMD-related PIVH and 23 (20.5%) in acute idiopathic PIVH (P ¼ 0.362) (Table 1).
tomography scan. (B) No structural cerebrovascular abnormality is shown on digital subtraction angiography.
Baseline Laboratory Data In patients with acute idiopathic PIVH, the baseline platelet count was lower than in those with acute MMD-related PIVH, but not significantly (158.86 66.87 vs. 181.53 54.94 109/l, P ¼ 0.082). In addition, patients with acute MMD-related PIVH had lower admission blood glucose than those with acute idiopathic PIVH, but not significantly (7.62 2.05 vs. 8.76 3.56 mmol/L, P ¼ 0.087). Patients with acute idiopathic PIVH had significantly higher admission serum urea than those with MMD-related PIVH (5.68 2.66 vs. 4.34 1.62 mmol/L, P ¼ 0.008). The level of
Table 1. Baseline Clinical and Imaging Characteristics MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
42.8 12.2
53.3 15.8
<0.001
20
49
0.061
GCS score
12 (8.25, 15)
11.5 (9, 15)
0.749
SBP, mm Hg
134.6 24.6
161.7 30.9
<0.001
DBP, mm Hg
79.2 19.1
93.8 19.6
<0.001
Age, year Female
Hypertension
6
59
0.001
Diabetes mellitus
1
12
0.298
Previous stroke
5
10
0.274
Smoking
6
32
0.266
Alcohol abuse
7
28
0.716
18.5 (15, 22.75)
17 (11, 21)
0.107
9
23
0.362
mGS Hydrocephalus
Data are mean standard deviation, median and interquartile range, or number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; GCS, Glasgow Coma Scale; SBP, systolic blood pressure; DBP, diastolic blood pressure; mGS, modified Graeb score.
WORLD NEUROSURGERY -: e1-e6, - 2019
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Table 2. Baseline Laboratory Data
RBC, 1012/L 9
WBC, 10 /L PLT, 109/L BG, mmol/L Urea, mmol/L Scr, mmol/L
MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
4.45 0.61
4.42 0.77
0.812
14.34 5.36
12.37 6.55
0.123
181.53 54.94
158.86 66.87
0.082
7.62 2.05
8.76 3.56
0.087
4.34 1.62
5.68 2.66
0.008
63.66 18.39
89.38 78.26
0.068
Cystatin C, mg/L
0.68 0.16
0.97 0.72
0.023
Uric acid, mmol/L
242.24 77.65
309.01 105.97
0.001
PT, s
11.83 1.05
12.29 4.14*
0.542
APTT, s
25.81 3.94
27.55 15.94*
0.542
INR
1.03 0.09
1.09 0.37*
0.439
MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; RBC, red blood cell; WBC, white blood cell; PLT, platelet count; BG, blood glucose; Scr, serum creatinine; PT, prothrombin time; APTT, activated partial thromboplastin time; INR, international normalized ratio; s, seconds. *Available in 110 patients. Data are mean standard deviation, median and interquartile range, or number of patients.
serum creatinine in patients with acute idiopathic PIVH was also higher than in those with MMD-related PIVH, but not significantly (89.38 78.26 vs. 63.66 18.39 mmol/L, P ¼ 0.068). Moreover, the levels admission serum cystatin C was also different in patients with acute MMD-related and idiopathic PIVH (0.68 0.16 vs. 0.97 0.72 mg/L, P ¼ 0.023). In addition, patients with acute MMDrelated PIVH had significantly lower admission serum uric acid than those with acute idiopathic PIVH (242.24 77.65 vs. 309.01 105.97 mmol/L, P ¼ 0.001) (Table 2).
Treatment In patients with acute MMD-related PIVH, 24 (75.0%) patients received conservative treatment, 1 (3.1%) received hematoma evacuation, 4 (12.5%) received external ventricular drainage, 1 (3.1%) received lumbar drainage, and 2 (6.3%) received both external ventricular drainage and lumbar drainage. In contrast, in patients with acute idiopathic PIVH, 78 (69.6%) patients received conservative treatment, 6 (5.4%) received hematoma evacuation, 17 (15.2%) received external ventricular drainage, 8 (7.1%) received lumbar drainage, and 3 (2.7%) received both external ventricular drainage and lumbar drainage (Table 3).
Outcomes at Discharge In patients with acute MMD-related PIVH, only one (3.1%) patient was dead at discharge. In contrast, a total of 22 (19.6%) patients with acute idiopathic PIVH died at discharge (P ¼ 0.027). There were 14 (43.8%) cases with unfavorable functional outcome at discharge in patients acute MMD-related PIVH. Among patients with acute idiopathic PIVH, 51 (45.5%) had unfavorable functional outcome at discharge (P ¼ 0.858). Patients with acute MMD-related and idiopathic PIVH had similar incidences of pneumonia or any infection at discharge (Table 4).
e4
www.SCIENCEDIRECT.com
DISCUSSION This study compared the characteristics and outcomes of MMDrelated and idiopathic PIVH in the acute phase. Comparing with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH were significantly younger (P < 0.001) and had significantly lower admission systolic blood pressure (P < 0.001) and diastolic blood pressure (P < 0.001). Moreover, patients with acute idiopathic PIVH had significantly higher levels of admission serum urea (P ¼ 0.008), cystatin C (P ¼ 0.023), and uric acid (P ¼ 0.001) than those with acute MMD-related PIVH. In addition, patients with acute MMD-related PIVH had significantly lower mortality at discharge than patients with acute idiopathic PIVH (P ¼ 0.027). PIVH is a rare cerebrovascular disorder adult patients.9 A study using diffusion tensor imaging showed the white matter injury in periventricular area after PIVH.10 Moreover, PIVH may be related to various etiologies.11A retrospective study by Passero et al12 showed
Table 3. Treatment MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
Conservative treatment
24
78
Hematoma evacuation
1
6
EVD
4
17
LD
1
8
EVD þ LD
2
3
Data are number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage; EVD, external ventricular drainage; LD, lumbar drainage.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
Table 4. Outcomes at Discharge MMD-Related PIVH (n [ 32)
Idiopathic PIVH (n [ 112)
P
Death
1
22
0.027
Unfavorable functional outcome
14
51
0.858
Pneumonia
4
19
0.785
Any infection
5
21
0.685
Data are number of patients. MMD, moyamoya disease; PIVH, primary intraventricular hemorrhage.
that vascular malformation was found in 31% of PIVH patients. Flint et al13 reported that about 56% of PIVH patients had positive results in angiographic examinations, and the most common cause was arteriovenous malformation. In contrast, Zhang et al2 suggested that vascular malformation could be found in 53.3% of patients with PIVH and MMD was the most common vascular malformation in PIVH patients in a Chinese population. MMD is a unique cerebrovascular disease that is more common in Asian countries.14 MMD has different subtypes including ischemic MMD, hemorrhagic MMD, and asymptomatic MMD.15 Hemorrhagic MMD is more common in adult patients.16 In adult patients with hemorrhagic MMD, PIVH is relatively common.4,5,17 Therefore in order to have a better understanding of hemorrhagic MMD, it is important to explore the characteristics of MMD-related PIVH. In this study, we found 32 patients with acute MMD-related PIVH. Hypertension was not common in acute MMD-related PIVH. Moreover, short-term mortality in these patients was low (3.1%). In contrast, no cerebrovascular abnormality can be found in some PIVH patients, which is defined as idiopathic PIVH.7 Hypertension is the main cause for idiopathic PIVH.7 In Zhang et al’s2 study, patients with idiopathic PIVH had younger age and more frequent presence of hypertension than those with different cerebrovascular abnormalities. However, those studies did not focus on the acute phase after PIVH and the difference between MMD-related and idiopathic PIVH was not well described. This study included 32 patients with acute MMD-related PIVH and 112 patients with acute idiopathic PIVH. Patients with acute idiopathic PIVH had significantly older age and higher admission blood pressure than those with acute MMDrelated PIVH. Moreover, we found patients with acute idiopathic PIVH had significantly higher levels of biomarkers for renal function than patients with acute MMD-related PIVH. In addition, patients with acute idiopathic PIVH had significantly higher mortality at discharge than those with acute MMD-related PIVH. Thus although patients with acute MMD-related and idiopathic PIVH have similar features on admission CT scan, their clinical characteristics and outcomes are different. The optimal treatment for intraventricular hemorrhage is still controversial.18 In the study by Hanley et al19 comparing external ventricular drainage alone, external ventricular drainage plus intraventricular fibrinolysis could significantly reduce mortality, but not significantly improve functional outcome, in patients with severe intraventricular hemorrhage. A meta-analysis suggested that intraventricular fibrinolysis could decrease morality
WORLD NEUROSURGERY -: e1-e6, - 2019
and potentially improve functional outcome in patients with intraventricular hemorrhage.20 In Staykov et al’s21 study, intraventricular fibrinolysis plus lumbar drainage could be a better treatment than intraventricular fibrinolysis in patients with severe intraventricular hemorrhage. Song et al22 suggested that endoscopic surgery could have the better performance in hematoma removal and outcome improvement than external ventricular drainage in patients with severe intraventricular hemorrhage. However, the evidence for management of acute MMD-related and idiopathic PIVH is still lacking. This study showed that conservative treatment, hematoma evacuation, external ventricular drainage, lumbar drainage, or combination of external ventricular drainage and lumbar drainage could be adopted in patients with acute MMD-related or idiopathic PIVH on the basis of the individual condition of each patient. However, the optimal treatment for these patients in the acute phase should be explored in further studies. Although patients with acute MMD-related PIVH had lower mortality at discharge than those with acute idiopathic PIVH in this study, it does not mean patients with acute MMD-related PIVH have good long-term outcome. In Nah et al’s6 study, patients with hemorrhagic MMD had a higher rate of rebleeding than those with spontaneous intracerebral hemorrhage. To improve their long-term outcome, surgical revascularization after acute phase can be necessary.23 Jiang et al24 reported that bypass surgery can decrease rebleeding rate in patients with hemorrhagic MMD. The study by Jo et al25 showed that surgical revascularization may decrease the risk of recurrent stroke via correcting abnormal perfusion. Hence although patients with acute MMD-related PIVH may have relatively good short-term outcome, appropriate treatment after acute phase of PIVH is crucial for improving their long-term outcome. Comparing with patients who had acute MMD-related PIVH, patients with acute idiopathic PIVH had higher short-term mortality, which could be related to their different baseline characteristics. This study showed that patients with idiopathic PIVH had a higher burden of blood pressure. Higher blood pressure is correlated with poor outcome after hemorrhagic stroke.26 However, the role of intensive blood pressure reduction is still controversial in the management of intracerebral hemorrhage.27,28 For patients with acute idiopathic PIVH, early blood pressure control is reasonable but the optimal target should be explored further. This study also showed that patients with acute idiopathic patients had worse renal function. Previous studies have shown that biomarkers for renal function are related to outcome in intracerebral hemorrhage.29,30 Therefore renal function should be noticed in the management of patients with acute idiopathic PIVH. This study has some limitations. First, this retrospective study was conducted in a single center and the sample size was still small, which could affect its reliability. Second, the long-term outcome was insufficient for analysis. Therefore the results in this study should be confirmed by further studies. CONCLUSIONS Compared with patients who had acute idiopathic PIVH, patients with acute MMD-related PIVH have younger age, lower admission blood pressure, and better renal function. Moreover, patients with acute MMD-related PIVH have lower short-term mortality.
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE ZHIYUAN YU ET AL.
ACUTE MOYAMOYA DISEASERELATED VERSUS IDIOPATHIC PRIMARY INTRAVENTRICULAR HEMORRHAGE IN ADULTS
REFERENCES 1. Weinstein R, Ess K, Sirdar B, Song S, Cutting S. Primary intraventricular hemorrhage: clinical characteristics and outcomes. J Stroke Cerebrovasc Dis. 2017;26:995-999. 2. Zhang S, Jia B, Li H, You C, Hanley DF, Jiang Y. Primary intraventricular hemorrhage in adults: etiological causes and prognostic factors in Chinese population. J Neurol. 2017;264:382-390. 3. Fujimura M, Bang OY, Kim JS. Moyamoya disease. Front Neurol Neurosci. 2016;40:204-220. 4. Ge P, Zhang Q, Ye X, et al. Clinical features of hemorrhagic moyamoya disease in China. World Neurosurg. 2017;106:224-230. 5. Jang DK, Lee KS, Rha HK, et al. Clinical and angiographic features and stroke types in adult moyamoya disease. AJNR Am J Neuroradiol. 2014;35: 1124-1131. 6. Nah HW, Kwon SU, Kang DW, Ahn JS, Kwun BD, Kim JS. Moyamoya disease-related versus primary intracerebral hemorrhage: [corrected] location and outcomes are different. Stroke. 2012;43: 1947-1950. 7. Guo R, Ma L, Shrestha BK, Yu Z, Li H, You C. A retrospective clinical study of 98 adult idiopathic primary intraventricular hemorrhage cases. Medicine. 2016;95:e5089. 8. Lee SH, Park KJ, Park DH, Kang SH, Park JY, Chung YG. Factors associated with clinical outcomes in patients with primary intraventricular hemorrhage. Med Sci Monitor. 2017;23:1401-1412. 9. Giray S, Sen O, Sarica FB, et al. Spontaneous primary intraventricular hemorrhage in adults: clinical data, etiology and outcome. Turk Neurosurg. 2009;19:338-344. 10. Yeo SS, Choi BY, Chang CH, et al. Periventricular white matter injury by primary intraventricular hemorrhage: a diffusion tensor imaging study. Eur Neurol. 2011;66:235-241. 11. Angelopoulos M, Gupta SR, Azat Kia B. Primary intraventricular hemorrhage in adults: clinical features, risk factors, and outcome. Surg Neurol. 1995;44:433-436. 12. Passero S, Ulivelli M, Reale F. Primary intraventricular haemorrhage in adults. Acta Neurol Scand. 2002;105:115-119.
e6
www.SCIENCEDIRECT.com
13. Flint AC, Roebken A, Singh V. Primary intraventricular hemorrhage: yield of diagnostic angiography and clinical outcome. Neurocrit Care. 2008;8: 330-336.
24. Jiang H, Ni W, Xu B, et al. Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg. 2014;121:1048-1055.
14. Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7:1056-1066.
25. Jo KI, Kim MS, Yeon JY, Kim JS, Hong SC. Recurrent bleeding in hemorrhagic moyamoya disease: prognostic implications of the perfusion status. J Kor Neurosurg Soc. 2016;59:117-121.
15. Wan M, Duan L. Recent progress in hemorrhagic moyamoya disease. Br J Neurosurg. 2015;29:189-191. 16. Miyamoto S, Yoshimoto T, Hashimoto N, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45:1415-1421.
26. Butcher KS, Jeerakathil T, Hill M, et al. The Intracerebral Hemorrhage Acutely Decreasing Arterial Pressure Trial. Stroke. 2013;44:620-626. 27. Qureshi AI, Palesch YY, Barsan WG, et al. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med. 2016;375: 1033-1043.
17. Li Q, Qu L, Yuan Y, et al. Analysis of the clinical characteristics of hemorrhagic moyamoya disease in the Jilin province of northeastern China: a single-center study of 212 cases. Biomed Rep. 2018; 8:191-197.
28. Anderson CS, Heeley E, Huang Y, et al. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med. 2013;368: 2355-2365.
18. Garton T, Hua Y, Xiang J, Xi G, Keep RF. Challenges for intraventricular hemorrhage research and emerging therapeutic targets. Expert Opin Therapeut Targets. 2017;21:1111-1122.
29. You S, Shi L, Zhong C, et al. Prognostic significance of estimated glomerular filtration rate and cystatin c in patients with acute intracerebral hemorrhage. Cerebrovasc Dis (Basel, Switzerland). 2016;42:455-463.
19. Hanley DF, Lane K, McBee N, et al. Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial. Lancet (London, England). 2017; 389:603-611.
30. Kim JK, Shin JJ, Park SK, Hwang YS, Kim TH, Shin HS. Prognostic factors and clinical outcomes of acute intracerebral hemorrhage in patients with chronic kidney disease. J Kor Neurosurg Soc. 2013; 54:296-301.
20. Baker AD, Rivera Perla KM, Yu Z, et al. Fibrinolytic for treatment of intraventricular hemorrhage: a meta-analysis and systematic review. Int J Stroke. 2018;13:11-23. 21. Staykov D, Kuramatsu JB, Bardutzky J, et al. Efficacy and safety of combined intraventricular fibrinolysis with lumbar drainage for prevention of permanent shunt dependency after intracerebral hemorrhage with severe ventricular involvement: a randomized trial and individual patient data metaanalysis. Ann Neurol. 2017;81:93-103. 22. Song P, Duan FL, Cai Q, et al. Endoscopic surgery versus external ventricular drainage surgery for severe intraventricular hemorrhage. Curr Med Sci. 2018;38:880-887.
Conflict of interest statement: No funding was received, and the authors report no conflicts of interest. Received 4 December 2018; accepted 5 January 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.01.070 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
23. Jiang H, Yang H, Ni W, et al. Long-term outcomes after combined revascularization surgery in adult hemorrhagic moyamoya disease. World Neurosurg. 2018;116:e1032-e1041.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.01.070