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Original research
Predictors of parenchymal hemorrhage after endovascular treatment in acute ischemic stroke: data from ANGEL-ACT Registry
  1. Dapeng Sun1,
  2. Baixue Jia1,
  3. Xu Tong1,
  4. Peter Kan2,
  5. Xiaochuan Huo1,
  6. Anxin Wang3,
  7. Raynald1,
  8. Gaoting Ma1,
  9. Ning Ma1,
  10. Feng Gao1,
  11. Dapeng Mo1,
  12. Ligang Song1,
  13. Xuan Sun1,
  14. Lian Liu1,
  15. Yiming Deng1,
  16. Xiaoqing Li1,
  17. Bo Wang1,
  18. Gang Luo1,
  19. Yongjun Wang3,
  20. Zeguang Ren4,
  21. Zhongrong Miao1
  22. on behalf of ANGEL-ACT study group
    1. 1 Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
    2. 2 Department of Neurosurgery, University of Texas Medical Branch, Galveston, Texas, USA
    3. 3 China National Clinical Research Center for Neurological Diseases, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
    4. 4 Department of Neurosurgery, Cleveland Clinic Martin Health, Port St Lucie, Florida, USA
    1. Correspondence to Dr Zhongrong Miao, Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Beijing, China; zhongrongm{at}; Dr Zeguang Ren, Department of Neurosurgery, Cleveland Clinic Martin Health, Port St Lucie, Florida, USA; renzem{at}


    Background Parenchymal hemorrhage (PH) is a troublesome complication after endovascular treatment (EVT).

    Objective To investigate the incidence, independent predictors, and clinical impact of PH after EVT in patients with acute ischemic stroke (AIS) due to anterior circulation large vessel occlusion (LVO).

    Methods Subjects were selected from the ANGEL-ACT Registry. PH was diagnosed according to the European Collaborative Acute Stroke Study classification. Logistic regression analyses were performed to determine the independent predictors of PH, as well as the association between PH and 90-day functional outcome assessed by modified Rankin Scale (mRS) score.

    Results Of the 1227 enrolled patients, 147 (12.0%) were diagnosed with PH within 12–36 hours after EVT. On multivariable analysis, low admission Alberta Stroke Program Early CT score (ASPECTS)(adjusted OR (aOR)=1.13, 95% CI 1.02 to 1.26, p=0.020), serum glucose >7 mmol/L (aOR=1.82, 95% CI 1.16 to 2.84, p=0.009), and neutrophil-to-lymphocyte ratio (NLR; aOR=1.05, 95% CI 1.02 to 1.09, p=0.005) were associated with a high risk of PH, while underlying intracranial atherosclerotic stenosis (ICAS; aOR=0.42, 95% CI 0.22 to 0.81, p=0.009) and intracranial angioplasty/stenting (aOR=0.37, 95% CI 0.15 to 0.93, p=0.035) were associated with a low risk of PH. Furthermore, patients with PH were associated with a shift towards to worse functional outcome (mRS score 4 vs 3, adjusted common OR (acOR)=2.27, 95% CI 1.53 to 3.38, p<0.001).

    Conclusions In Chinese patients with AIS caused by anterior circulation LVO, the risk of PH was positively associated with low admission ASPECTS, serum glucose >7 mmol/L, and NLR, but negatively related to underlying ICAS and intracranial angioplasty/stenting.

    Trial registration number NCT03370939.

    • stroke
    • hemorrhage
    • thrombectomy

    Data availability statement

    Data are available upon reasonable request. Not applicable.

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    Data availability statement

    Data are available upon reasonable request. Not applicable.

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    • Collaborators List of ANGEL-ACT study group:Beijing Tiantan Hospital, Beijing, China: Zhongrong Miao, MD; Langfang Changzheng Hospital, Hebei, China: Liqiang Gui, MD; Liaocheng Third People’s Hospital, Shandong, China: Cunfeng Song, MD; The First People’s Hospital of Changzhou, Jiangsu, China: Ya Peng, MD; The Second Affiliated Hospital of Nanjing Medical University, Jiangsu, China: Jin Wu, MD; Fengrun District People’s Hospital of Tangshan City, Hebei, China: Shijun Zhao, MD; SiPing Central People’s Hospital, Jilin, China: Junfeng Zhao, MD; Yijishan Hospital of Wannan Medical College, Anhui, China: Zhiming Zhou, MD; The 2nd Affiliated Hospital of Harbin Medical University, Heilongjiang, China: Yongli Li, MD; The Central Hospital of Wuhan, Hubei, China: Ping Jing, MD; The First Hospital of Shijiazhuang, Hebei, China: Lei Yang, MD; Shenzhen Hospital of Southern Medical University, Guangdong, China: Yajie Liu, MD; The People’s Hospital of Longhua, Guangdong, China: Qingshi Zhao, MD; Jingjiang People’s Hospital, Jiangsu, China: Yan Liu, MD; The Third People’s Hospital of Hubei Province, Hubei, China: Xiaoxiang Peng, MD; The Second Affiliated Hospital of Guangzhou Medical University, Guangdong, China: Qingchun Gao, MD; Tianjin TEDA Hospital, Tianjin, China: Zaiyu Guo, MD; Zhangzhou Affiliated Hospital of Fujian Medical University, Fujian, China: Wenhuo Chen, MD; Taiyuan Central Hospital, Shanxi, China: Weirong Li, MD; The First Affiliated Hospital of Xinjiang Medical University, Xinjiang, China: Xiaojiang Cheng, MD; Affiliated Drum Tower Hospital of Nanjing University Medical School, Jiangsu, China: Yun Xu, MD; The First People’s Hospital of Wenling, Zhejiang, China: Yongqiang Zhang, MD; The Second Affiliated Hospital of Xi’an Jiaotong University, Shaanxi, China: Guilian Zhang, MD; The First People’s Hospital of Yulin, Guangxi, China: Yijiu Lu, MD; Zhenjiang First People’s Hospital, Jiangsu, China: Xinyu Lu, MD; Qitaihe Coal General Hospital Heilongjiang, China: Dengxiang Wang, MD; People’s Hospital of Tangshan City, Hebei, China: Yan Wang, MD; Affiliated Hospital of Guilin Medical University, Guangxi, China: Hao Li, MD; The Affiliated Hospital of Guizhou Medical University, Guizhou Province, China: Yang Hua, MD; The Affiliated Hospital of Xuzhou Medical University, Jiangsu, China: Deqin Geng, MD; Qingdao Central Hospital, ShanDong, China: Haicheng Yuan, MD; The Fourth People’s Hospital of Langfang City, Hebei, China: Hongwei Wang, MD; Beijing Daxing hospital, Beijing, China: Haihua Yang, MD; Weifang People’s Hospital,ShanDong, China: Zengwu Wang, MD; Luoyang General Hospital Affiliated to Zhengzhou University, Henan, China: Liping Wei, MD; Dongguan Kanghua Hospital, Guangdong, China: Xuancong Liufu, MD; Shunde Hospital of Southern Medical University, Guangdong, China: Xiangqun Shi, MD; Handan Central Hospital, Hebei, China: Juntao Li, MD; The 981 hospital of the Chinese People’s Liberation Army, Hebei, China: Wenwu Yang, MD; Linfen people’s Hospital, Shanxi, China: Wenji Jing, MD; Anshun people’s Hospital of Guizhou, China: Xiang Yong, MD; Changle People’s Hospital, Shandong, China: Leyuan Wang, MD; The Second People’s Hospital of Dongying, Shandong, China: Chunlei Li, MD; Tangshan Gongren hospital, HeBei, China: Yibin Cao, MD; PLA 985th Hospital of the Joint Logistics Support Force, Shanxi, China: Qingfeng Zhu, MD; Gaomi People’s Hospital, ShanDong, China: Peng Zhang, MD; Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Hubei, China: Xiang Luo, MD; Chongqing Sanxia Center Hospital, Chongqing, China: Shengli Chen, MD; Hospital of Traditional Chinese Medicine of Qiannan, Guizhou, China: WenWu Peng, MD; Guangdong Hospital of Chinese Medicine, Guangdong, China: Lixin Wang, MD; People’s hospital of Yangjiang,Guangdong, China: Xue Wen, MD; The Third Affiliated Hospital of CQMU, Chongqing, China: Shugui Shi, MD; General Hospital of The Yangtze River Shipping, Hubei, China: Wanming Wang, MD; First People’s Hospital of Bijie City,Guizhou, China: Wang Bo, MD; Suqian People’s Hospital of Nanjing Drum-Tower Hospital Group, Jiangsu, China: Pu Yuan, MD; Weifang TCM Hospital, Shandong, China: Dong Wang, MD; The Third Affiliated Hospital of Guangzhou Medical University, Guangdong, China: Haitao Guan, MD; Karamay Central hospital, Xinjiang, China: Wenbao Liang, MD; The third people’s Hospital of Xinjiang Uygur Autonomous Region, Xinjiang, China: Daliang Ma, MD; Wulanchabu City Central Hospital, Inner Mongolia, China: Long Chen, MD; Hospital of Xinjiang Production & Construction Corps, Xinjiang, China: Yan Xiao, MD; Jiaozuo Second people’s hospital, Henan, China: Xiangdong Xie, MD; 904th Hospital of Joint Logistic Support Force of PLA, Jiangsu, China: Zhonghua Shi, MD; Ganzhou People’s Hospital, Jiangxi, China: Xiangjun Zeng, MD; 967 Hospital of the Joint Logistics Support Force of PLA, Liaoning, China: Fanfan Su, MD; The Affiliated Hospital of Northwest University Xi’an No.3 Hospital, Shaanxi, China: MingZe Chang, MD; The Second Hospital of Liao Cheng, Shandong, China: Jijun Yin, MD; Jilin Province People’s Hospital, Jilin, China: Hongxia Sun, MD; People’s Hospital of Huanghua City, Hebei, China: Chong Li, MD; Shanghai Forth People’s Hospital, Shanghai, China: Yong Bi, MD; Wanbei Coal-electricity Group Gneral Hospital, Anhui, China: Gang Xie, MD; Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China: Yuwu Zhao, MD; Binzhou Medical University Hospital, Shandong, China: Chao Wang, MD; The 988 hospital of the people’s liberation army, Henan, China: Peng Zhang, MD; Linyi People’s Hospital, Shandong, China: Xianjun Wang, MD; Yingkou City Central Hospital, Liaoning, China: Dongqun Li, MD; Yantaishan Hospital, Shandong, China: Hui Liang, MD; Mianyang Central hospital, Sichuan, China: Zhonglun Chen, MD; Chengdu Fifth People’s Hospital, Sichuan, China: Yan Wang, MD; Hengshui Fifth Hospital of Heng shui City, HeBei, China: Yu Xin, Wang, MD; Second Hospital of Dalian Medical University, Liaoning, China: Lin Yin, MD; Boai Hospital of Zhongshan, Guangdong, China: HongKai Qiu, MD; The First People’s Hospital of Yibin, Sichuan, China: Jun Wei, MD; Shanxi provincial people’s hospital, Shanxi, China: Yaxuan Sun, MD; Shandong Provincial Third Hospital, Cheeloo College of Medicine, Shandong University, Shandong, China: Xiaoya Feng, MD; Chuxiong State People’s Hospital, Chuxiong, Yunnan, China: Weihua Wu, MD; The Fourth Affiliated Hospital of China Medical University, Liaoning, China: Lianbo Gao, MD; Taihe Hospital, Shiyan, Hubei, China: Zhibing Ai, MD; Qingdao Municipal Hospital,Shandong, China: Tan Lan, MD; The First People’s Hospital of Yunnan Province, Yunnan, China: Li Ding, MD; The NO.2 People’s Hospital of Lanzhou. Gansu, China: Qilong Liang, MD; Taizhou First People’s Hospital, Zhejiang, China: Zhimin Wang, MD; Hunan Provincial People’s Hospital, Hunan, China: Jianwen Yang, MD; First People’s Hospital of Changde City, Hunan, China: Ping Xu, MD; Zhejiang Yuyao People’s Hospital, Zhejiang, China: Wei Dong, MD; AideBao Hospital, HeBei, China: Quanle Zheng, MD; The First Hospital of Fangshan District, Beijing, China: Zhenyun Zhu, MD; Tianjin Xiqing Hospital, Tianjin, China: Liyue Zhao, MD; People’s Hospital of Zunhua, Hebei, China: Qingbo Meng, MD; Xingtai Third Hospital, Hebei, China: Yuqing Wei, MD; Qingyuan People’s Hospital, Guangdong, China: Xianglin Chen, MD; Fengcheng City Central Hospital,Liaoning, China: Wei Wang, MD; People’s Hospital of Hejian City, Hebei, China: Dong Sun, MD; Hangzhou Third People’s Hospital, Zhejiang, China: Yongxing Yan, MD; Xiangtan Central Hospital, Hunan, China: Guangxiong Yuan, MD; People’s Hospital of Nanpi Country, Hebei, China: Yadong Yang, MD; Liuzhou Railway Central Hospital, Guangxi, China: Jianfeng Zhou, MD; Maoming People’s Hospital, Guangdong, China: Zhi Yang, MD; Tongde Hospital of Zhejiang Province, Zhejiang, China: Zhenzhong Zhang, MD; The First Affiliated Hospital of Jinzhou Medical University, Liaoning, China: Ning Guan, MD; Xishan coal electricity group worker general hospital, Shaanxi, China: Huihong Wang, MD.

    • Contributors DS was involved in the conception and design, interpretation of data, literature search, drafting the manuscript, and critical revision for important intellectual content. BJ and XT were involved in the conception and design. AW was involved in data acquisition, data analysis. ZM and ZR were involved in study supervision, critical revision for important intellectual content, and guarantee for overall content. All other authors read and approved the final manuscript.

    • Funding This Study funded by the National Key Research and Development Program of China, grant number 2016YFC1301500.

    • Competing interests ZR: consultant to Penumbra Company, USA.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.