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. 2019 Nov 19;9(12):e01471. doi: 10.1002/brb3.1471

Efficacy of neuroendoscopic surgery versus craniotomy for supratentorial hypertensive intracerebral hemorrhage: A meta‐analysis of randomized controlled trials

Xu‐Hui Zhao 1,✉, Su‐Zhen Zhang 2, Jin Feng 3, Zhen‐Zhong Li 1, Zeng‐Lu Ma 1
PMCID: PMC6908893  PMID: 31743631

Abstract

Background

Hypertensive cerebral hemorrhage (HCH) is a potentially life‐threatening neurological condition with an extremely high morbidity and mortality. In recent years, neuroendoscopy has been used to treat intracerebral hemorrhage (ICH). However, the choice of neuroendoscopic surgery versus craniotomy for patients with intracerebral hemorrhages is controversial.

Aim

We conducted this meta‐analysis to assess the efficacy of neuroendoscopic surgery compared with craniotomy in patients with supratentorial hypertensive ICH.

Methods

A systematic electronic search was conducted of online electronic databases: PubMed, Embase, and the Cochrane Library updated on December 2017. The meta‐analysis only included randomized controlled studies.

Results

Three randomized controlled trials met our inclusion criteria. The pooled analysis of death showed that neuroendoscopic surgery decreased the rate of death when compared with craniotomy (RR = 0.58, 95% CI 0.26–1.29; p = .18). The pooled result of complications indicated that neuroendoscopic surgery has a tendency toward lower complications (RR = 0.37, 95% CI 0.28–0.49; p < .001).

Conclusions

Our results suggested that neuroendoscopic surgery has lower complications, but no superior advantages in morbidity rates. Since the advantage of neuroendoscopic surgery has been performed in some area, the continuation of multi‐center comparative investigation with craniotomy may be necessary. Moreover, some efforts need to be taken in selecting appropriate patients with different treatments.

Keywords: craniotomy, hypertensive intracerebral hemorrhage, meta‐analysis, neuroendoscopic surgery

Neuroendoscopic surgery significantly reduces the rate of complications in patients with HICH, when compared with craniotomy, while without improving death outcomes.

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1. INTRODUCTION

Hypertensive intracerebral hemorrhage (HICH) is a condition that may threaten the life of patients with a high mortality rate (Hemphill et al., 2015) and severe disabilities (Asch et al., 2010; Mayer & Rincon, 2005) . The management of primary intracerebral hemorrhage (ICH) remains controversial. Previous studies have shown that surgical treatment rather than conservative treatment was associated with better outcomes (p < .001) (Mendelow et al., 2013) for HICH. For the treatment of ICH, surgical procedures have been employed. However, the effect was weak due to heterogeneity among the studies. The studies included different strategies of surgical interventions, such as craniotomy and neuroendoscopic surgery (Batjer, Reisch, Allen, Plaizier, & Su, 1990; Bhattathiri, Gregson, Prasad, Mendelow, & STICH Investigators, 2006; Teernstra et al., 2003; Xi et al., 1998).

In the past several decades, craniotomy has played critical roles for HICH. However, several prospective randomized controlled trials have failed to show benefit in outcome in craniotomy patients (Mendelow et al., 2005; Teernstra et al., 2003). Endoscopic surgery has been applied for the treatment of HICH in recent years. Many studies suggested that endoscopic evacuation showed efficacy and safety benefit for HICH patients (Cho, Chen, Chang, Lee, & Tso, 2006; Nagasaka et al., 2011), when compared with traditional craniotomy (Wang et al., 2015; Yamashiro, Hitoshi, Yoshida, & Kuratsu, 2015). The result is in accordance with the latest systemic review (Xia et al., 2018). However, due to retrospective research or limited sample size, no conclusion could be drawn about the effects of endoscopic surgery on outcomes in HICH patients (Auer et al., 1989; Xu et al., 2018). Therefore, due to these controversial results, we performed this meta‐analysis to identify which type of surgical procedure was safer and more effective in promoting outcomes and reducing complications in patients with HICH.

2. METHODS

2.1. Retrieval strategy

Published articles on the efficacy and safety of neuroendoscopic surgery compared with craniotomy in patients with supratentorial HICH up to December 2017 were retrieved. The searched databases included PubMed, Embase, and the Cochrane Library. The process was established to find all articles based on the MeSH terms and the keywords: “craniotomy”, “neuroendoscopic surgery” and “hypertensive intracerebral hemorrhage”, and no limitation was used during the literature search. We identified full‐text papers from reference materials for further evaluation.

2.2. Eligibility criteria

Articles that met the following inclusion criteria were included in this analysis: (a) studies were designed as randomized controlled trials; (b) studies enrolled HICH patients; (c) trials compared craniotomy versus neuroendoscopic surgery; and (d) studies provided data of perioperative morbidity or mortality. Studies that did not meet the above inclusion criteria were excluded from the meta‐analysis.

2.3. Quality assessment

Two investigators independently rated the quality of the retrieved studies. We chose the risk of bias items (ROBI) recommended by The Cochrane Handbook for Systematic Reviews of Interventions.

2.4. Data extraction

Data were extracted by two authors independently. Disagreement was resolved by consensus. From each of the eligible studies, the main categories were based on the following: first author's family name, publication year, total number of study subjects, mean age, hematoma volume (ml), and the number of mortalities.

2.5. Statistical analysis

Meta‐analysis was performed by pooling the results of the reported incidence of death and complications. Results were expressed as the appropriate ratio/difference for dichotomous outcomes as determined by available data. The I 2 statistic test was performed to further examine statistical heterogeneity between the trials (Higgins & Thompson, 2002). Studies with an I 2 ≥ 50% were considered to indicate moderate and high heterogeneity, and I 2 < 50% was considered to have low heterogeneity, respectively (Higgins, Thompson, Deeks, & Altman, 2003). The random‐effects model was adopted if I 2 > 50%; otherwise, the fixed‐effects model was chosen.

A p value < .05 was considered to be statistically significant. All the meta‐analyses were performed by Review Manager version 5.3 software (Revman; The Cochrane Collaboration, Oxford, United Kingdom). The findings of our meta‐analysis were shown in forest plots. The risk of bias was evaluated using Begg's test and Egger's test.

2.6. Ethical approval

Ethical approval was waived because this study did not involve any human participants or animals.

3. RESULTS

3.1. Overview of literature search and study characteristics

A total of 213 studies were initially identified after the primary selection. Based on the criteria described in the methods, 206 irrelevant citations were further excluded based on review of titles and abstracts. Finally, a total of 3 RCTs (Cho et al., 2006; Feng, He, Liu, Yang, & Wang, 2016; Zhang et al., 2014) were included in this meta‐analysis (Figure 1). The major characteristics of included studies are depicted in Table 1.

Figure 1.

Figure 1

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The PRISMA flowchart of the selection process to identify studies eligible for pooling

Table 1.

The primary characteristics of the eligible studies in more detail

Author Years Total M/F Mean age Hematoma volume (ml) Death
NE C NE C NE C NE C NE C
Feng Y 2016 93 91 56/37 58/33 66.35 69.1     8 8
Zhang HZ 2014 21 24 16/5 22/8 59.9 61.45 58.28 62.16 0 3
Cho DY 2006 30 30 19/11 21/9 56.67 54.22 55.48 42.11 0 4
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3.2. Clinical and methodological heterogeneity

3.2.1. Pooled analysis of death after neuroendoscopic surgery versus craniotomy

The pooled analysis (Cho et al., 2006; Feng et al., 2016; Zhang et al., 2014) revealed no statistically difference in death between neuroendoscopic surgery and craniotomy (RR = 0.58, 95% CI 0.26–1.29; p = .18) (Figure 2).

Figure 2.

Figure 2

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Pooled analysis of death after neuroendoscopic surgery versus craniotomy

3.2.2. Pooled analysis of complications after neuroendoscopic surgery versus craniotomy

The random‐effects model was used to pool data on complications (Cho et al., 2006; Feng et al., 2016; Zhang et al., 2014). The pooled data showed that neuroendoscopic surgery had a lower risk of complications (RR = 0.37, 95% CI 0.28–0.49; p < .001) (Figure 3).

Figure 3.

Figure 3

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Pooled analysis of complications after neuroendoscopic surgery versus craniotomy

4. DISCUSSION

Hypertensive intracerebral hemorrhage (HICH) inflicts a major health burden with an extremely high morbidity and mortality. In case of a massive hematoma, surgical drainage is a crucial therapeutic option. Endoscopic evacuation has been investigated by comparison with traditional craniotomy (Cho et al., 2006). However, many questions regarding the minimally invasive surgery remain unanswered. Historically, craniotomy has been used as an appropriate therapy for HICH evacuation (Bosel, Zweckberger, & Hacke, 2015). A recent RCT showed that early craniotomy could reduce the mortality of ICH patients (Mendelow et al., 2013). Craniotomy had also some other advantages such as good view and immediate removal of hematoma and improvement in local blood circulation (Ohwaki et al., 2006), which could also help in outcomes. However, the therapies appear to have reached a plateau. Because of lack of large multi‐centric RCTs (Hemphill et al., 2015), many surgical trials have shown that craniotomy is associated with substantial adverse effects (Lee et al., 2003; Li, Yang, Xu, Li, & You, 2013; Prasad, Browman, Srivastava, & Menon, 1997). Craniotomy increased the operative time and the risk of infection. Therefore, minimally invasive surgery that causes minimal trauma to normal brain region during removal of hematoma has been under intensive investigation for treating ICH over craniotomy (Li et al., 2017).

In neuroendoscopic surgery, a small burr hole is created, a minimally invasive procedure in which a 5‐ to 8‐mm‐diameter endoscope is inserted into the brain tissue (Xu et al., 2018). The minimal invasive surgery is performed under a surgical microscope, which has the advantage of adequate hemostasis and small bone window craniotomy. Neuroendoscopic surgery, as the minimal invasive surgery, was successfully applied for hematoma evacuation with many advantages (Zhou et al., 2011). Some scholars have emphasized that site of hemorrhage, hemorrhage volume, and patient condition should be considered in the selection of surgical method (Li & Chen, 2014; Luo et al., 2008). Appropriate operative route is the key for success to treat SICH. The endoscopic removal of intracranial hematoma is proceeded within the cavity, which has made it possible to carry out minimally invasive interventions in brain tissues whether it is in the normal area or the surrounding damaged region (Zhang et al., 2014).

With regard to the incidence of complications, we found that patients that underwent neuroendoscopic surgery had fewer complications than those that underwent craniotomy. The neuroendoscopic surgery group had a reduced infection rate; the reasons for this benefit are multiple and include the following: (a) neuroendoscopic surgery provides multi‐angle observation and “observe around the corner” capability to manage intraoperative bleeding, which make up for the insufficiency of direct vision (Feng et al., 2016). (b) In some studies, to avoid brain tissue damage, some authors selected short and precise routes to the hematoma under direct vision and deep lesions without manipulating or exposing the unaffected areas (Zhang et al., 2014).

In conclusion, our results suggest that neuroendoscopic surgery significantly reduces the rate of complications in patients with HICH compared with craniotomy, while without improving death outcomes. When all these data were analyzed, it became obvious that these two methods had their own advantages and shortcomings, and every approach had its indications, so it was difficult to decide which one was better for HICH patients. Thus, it is an essential issue to select individualized treatment that will benefit from different methods. We hope that eligible RCTs are warranted to verify the efficacy of the neuroendoscopic approach for HICH in the future.

CONFLICT OF INTEREST

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers' bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent‐licensing arrangements), or nonfinancial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.

INFORMED CONSENT

Informed consent was not required because no human participants involved in this study.

Zhao X‐H, Zhang S‐Z, Feng J, Li Z‐Z, Ma Z‐L. Efficacy of neuroendoscopic surgery versus craniotomy for supratentorial hypertensive intracerebral hemorrhage: A meta‐analysis of randomized controlled trials. Brain Behav. 2019;9:e01471 10.1002/brb3.1471

DATA AVAILABILITY STATEMENT

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

REFERENCES

  1. Auer, L. M. , Deinsberger, W. , Niederkorn, K. , Gell, G. , Kleinert, R. , Schneider, G. , … Hanusch, S. (1989). Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: A randomized study. Journal of Neurosurgery, 70(4), 530–535. 10.3171/jns.1989.70.4.0530 [DOI] [PubMed] [Google Scholar]
  2. Batjer, H. H. , Reisch, J. S. , Allen, B. C. , Plaizier, L. J. , & Su, C. J. (1990). Failure of surgery to improve outcome in hypertensive putaminal hemorrhage. A prospective randomized trial. Archives of Neurology, 47(10), 1103–1106. 10.1001/archneur.1990.00530100071015 [DOI] [PubMed] [Google Scholar]
  3. Bhattathiri, P. S. , Gregson, B. , Prasad, K. S. , Mendelow, A. D. , & STICH Investigators (2006). Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: Results from the STICH trial. Acta Neurochirurgica Supplement, 96, 65–68. [DOI] [PubMed] [Google Scholar]
  4. Bosel, J. , Zweckberger, K. , & Hacke, W. (2015). Haemorrhage and hemicraniectomy: Refining surgery for stroke. Current Opinion in Neurology, 28(1), 16–22. 10.1097/WCO.0000000000000167 [DOI] [PubMed] [Google Scholar]
  5. Cho, D. Y. , Chen, C. C. , Chang, C. S. , Lee, W. Y. , & Tso, M. (2006). Endoscopic surgery for spontaneous basal ganglia hemorrhage: Comparing endoscopic surgery, stereotactic aspiration, and craniotomy in noncomatose patients. Surgical Neurology, 65(6), 547–555. 10.1016/j.surneu.2005.09.032 [DOI] [PubMed] [Google Scholar]
  6. Feng, Y. , He, J. , Liu, B. , Yang, L. , & Wang, Y. (2016). Endoscope‐assisted keyhole technique for hypertensive cerebral hemorrhage in elderly patients: A randomized controlled study in 184 patients. Turkish Neurosurgery, 26(1), 84–89. [DOI] [PubMed] [Google Scholar]
  7. Hemphill, J. C. , Greenberg, S. M. , Anderson, C. S. , Becker, K. , Bendok, B. R. , Cushman, M. , … Woo, D. (2015). Guidelines for the management of spontaneous intracerebral hemorrhage: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 46(7), 2032–2060. 10.1161/STR.0000000000000069 [DOI] [PubMed] [Google Scholar]
  8. Higgins, J. P. , & Thompson, S. G. (2002). Quantifying heterogeneity in a meta‐analysis. Statistics in Medicine, 21(11), 1539–1558. 10.1002/sim.1186 [DOI] [PubMed] [Google Scholar]
  9. Higgins, J. P. , Thompson, S. G. , Deeks, J. J. , & Altman, D. G. (2003). Measuring inconsistency in meta‐analyses. BMJ, 327(7414), 557–560. 10.1136/bmj.327.7414.557 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lee, J.‐I. , Nam, D.‐H. , Kim, J.‐S. , Hong, S.‐C. , Shin, H.‐J. , Park, K. , … Kim, J. H. (2003). Stereotactic aspiration of intracerebral haematoma: Significance of surgical timing and haematoma volume reduction. Journal of Clinical Neuroscience: Official Journal of the Neurosurgical Society of Australasia, 10(4), 439–443. 10.1016/S0967-5868(03)00061-4 [DOI] [PubMed] [Google Scholar]
  11. Li, F. , & Chen, Q. X. (2014). Risk factors for mental disorders in patients with hypertensive intracerebral hemorrhage following neurosurgical treatment. Journal of the Neurological Sciences, 341(1–2), 128–132. 10.1016/j.jns.2014.04.021 [DOI] [PubMed] [Google Scholar]
  12. Li, Q. , Yang, C. H. , Xu, J. G. , Li, H. , & You, C. (2013). Surgical treatment for large spontaneous basal ganglia hemorrhage: Retrospective analysis of 253 cases. British Journal of Neurosurgery, 27(5), 617–621. 10.3109/02688697.2013.765938 [DOI] [PubMed] [Google Scholar]
  13. Li, Y. , Yang, R. , Li, Z. , Yang, Y. , Tian, B. O. , Zhang, X. , … Li, L. (2017). Surgical evacuation of spontaneous supratentorial lobar intracerebral hemorrhage: Comparison of safety and efficacy of stereotactic aspiration, endoscopic surgery, and craniotomy. World Neurosurgery, 105, 332–340. 10.1016/j.wneu.2017.05.134 [DOI] [PubMed] [Google Scholar]
  14. Luo, J. B. , Peng, B. , Quan, W. , Cao, Z. K. , Xiao, G. C. , Lu, J. P. , … He, Z. W. (2008). [Therapeutic effects of aspiration with a directional soft tube and conservative treatment on mild hemorrhage in the basal ganglion]. Nan Fang Yi Ke Da Xue Xue Bao = journal of Southern Medical University, 28(8), 1352–1353. [PubMed] [Google Scholar]
  15. Mayer, S. A. , & Rincon, F. (2005). Treatment of intracerebral haemorrhage. The Lancet Neurology, 4(10), 662–672. 10.1016/S1474-4422(05)70195-2 [DOI] [PubMed] [Google Scholar]
  16. Mendelow, A. , Gregson, B. , Fernandes, H. , Murray, G. , Teasdale, G. , Hope, D. , … Barer, D. (2005). Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): A randomised trial. Lancet, 365(9457), 387–397. 10.1016/S0140-6736(05)70233-6 [DOI] [PubMed] [Google Scholar]
  17. Mendelow, A. D. , Gregson, B. A. , Rowan, E. N. , Murray, G. D. , Gholkar, A. , & Mitchell, P. M. (2013). Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): A randomised trial. Lancet, 382(9890), 397–408. 10.1016/S0140-6736(13)60986-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nagasaka, T. , Tsugeno, M. , Ikeda, H. , Okamoto, T. , Inao, S. , & Wakabayashi, T. (2011). Early recovery and better evacuation rate in neuroendoscopic surgery for spontaneous intracerebral hemorrhage using a multifunctional cannula: Preliminary study in comparison with craniotomy. Journal of Stroke and Cerebrovascular Diseases: The Official Journal of National Stroke Association, 20(3), 208–213. 10.1016/j.jstrokecerebrovasdis.2009.11.021 [DOI] [PubMed] [Google Scholar]
  19. Ohwaki, K. , Yano, E. , Nagashima, H. , Hirata, M. , Nakagomi, T. , & Tamura, A. (2006). Surgery for patients with severe supratentorial intracerebral hemorrhage. Neurocritical Care, 5(1), 15–20. 10.1385/NCC:5:1:15 [DOI] [PubMed] [Google Scholar]
  20. Prasad, K. , Browman, G. , Srivastava, A. , & Menon, G. (1997). Surgery in primary supratentorial intracerebral hematoma: A meta‐analysis of randomized trials. Acta Neurologica Scandinavica, 95(2), 103–110. 10.1111/j.1600-0404.1997.tb00078.x [DOI] [PubMed] [Google Scholar]
  21. Teernstra, O. , Evers, S. , Lodder, J. , Leffers, P. , Franke, C. L. , & Blaauw, G. (2003). Stereotactic treatment of intracerebral hematoma by means of a plasminogen activator: A multicenter randomized controlled trial (SICHPA). Stroke, 34(4), 968–974. 10.1161/01.STR.0000063367.52044.40 [DOI] [PubMed] [Google Scholar]
  22. van Asch, C. J. , Luitse, M. J. , Rinkel, G. J. , van der Tweel, I. , Algra, A. , & Klijn, C. J. (2010). Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: A systematic review and meta‐analysis. The Lancet Neurology, 9(2), 167–176. 10.1016/S1474-4422(09)70340-0 [DOI] [PubMed] [Google Scholar]
  23. Wang, W.‐H. , Hung, Y.‐C. , Hsu, S. P. C. , Lin, C.‐F. , Chen, H.‐H. , Shih, Y.‐H. , & Lee, C.‐C. (2015). Endoscopic hematoma evacuation in patients with spontaneous supratentorial intracerebral hemorrhage. Journal of the Chinese Medical Association: JCMA, 78(2), 101–107. 10.1016/j.jcma.2014.08.013 [DOI] [PubMed] [Google Scholar]
  24. Xi, G. , Wagner, K. R. , Keep, R. F. , Hua, Y. A. , de Courten‐Myers, G. M. , Broderick, J. P. , … Hoff, J. T. (1998). Role of blood clot formation on early edema development after experimental intracerebral hemorrhage. Stroke, 29(12), 2580–2586. 10.1161/01.STR.29.12.2580 [DOI] [PubMed] [Google Scholar]
  25. Xia, Z. , Wu, X. , Li, J. , Liu, Z. , Chen, F. , Zhang, L. , … Cheng, Q. (2018). Minimally invasive surgery is superior to conventional craniotomy in patients with spontaneous supratentorial intracerebral hemorrhage: A systematic review and meta‐analysis. World Neurosurgery, 115, 266–273. 10.1016/j.wneu.2018.04.181 [DOI] [PubMed] [Google Scholar]
  26. Xu, X. , Chen, X. , Li, F. , Zheng, X. , Wang, Q. , Sun, G. , … Xu, B. (2018). Effectiveness of endoscopic surgery for supratentorial hypertensive intracerebral hemorrhage: A comparison with craniotomy. Journal of Neurosurgery, 128(2), 553–559. 10.3171/2016.10.JNS161589 [DOI] [PubMed] [Google Scholar]
  27. Yamashiro, S. , Hitoshi, Y. , Yoshida, A. , & Kuratsu, J. (2015). Effectiveness of endoscopic surgery for comatose patients with large supratentorial intracerebral hemorrhages. Neurologia Medico‐Chirurgica, 55(11), 819–823. 10.2176/nmc.oa.2014-0136 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zhang, H.‐Z. , Li, Y.‐P. , Yan, Z.‐C. , Wang, X.‐D. , She, L. , Wang, X.‐D. , & Dong, L. (2014). Endoscopic evacuation of basal ganglia hemorrhage via keyhole approach using an adjustable cannula in comparison with craniotomy. BioMed Research International, 2014, 898762 10.1155/2014/898762 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zhou, H. , Zhang, Y. U. , Liu, L. , Huang, Y. , Tang, Y. , Su, J. , … Dong, Q. (2011). Minimally invasive stereotactic puncture and thrombolysis therapy improves long‐term outcome after acute intracerebral hemorrhage. Journal of Neurology, 258(4), 661–669. 10.1007/s00415-011-5902-7 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

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