Staged Open Cranial Surgery for Primary Intra-axial Neoplasms: A Systematic Review

doi:10.21203/rs.3.rs-2591960/v1

Background

Staged surgery for skull base lesions has been utilized to facilitate maximal safe resection and optimize outcomes while minimizing morbidity and complications. Conversely, staged surgery for primary intraparenchymal neoplasms is less commonly performed and has not been reported as extensively within the literature. As such, we performed a systematic review to examine the unique surgical indications for staging, timing between stages, specific surgical approaches employed, and postoperative complications of staged surgery for primary intra-axial neoplasms.

Methods

A literature search was conducted in August 2021 using PubMed, Web of Science, and Cochrane databases using the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) recommendations. Titles and abstracts were evaluated independently by two authors, after which articles were selected for final analysis based on application of strict inclusion criteria during full text screen. Each included article was then qualitatively assessed and relevant variables – including operative approaches, timing, and outcomes – were extracted for synthesis.

Results

Of 115 results, 7 articles were included for final analysis and consisted of 17 pediatric and 4 adult patients. Staged approaches were more commonly utilized in the pediatric patient population for resection of astrocytoma and glioma. Pediatric patients had a timing of surgeries ranging from 5–10 days between operations, compared to 18 days-4 months in adult patients. Complications in pediatric patients were most commonly hemiparesis, hydrocephalus, CN VI and VII palsies, truncal ataxia, and cerebellar mutism, while complications in adult patients included language and abstract thinking deficits, respiratory failure, and motor weakness.

Conclusion

This study reports the first comprehensive review of staged surgical procedures for primary, intra-axial cranial neoplasms. There exists a large degree of heterogeneity in complications resulting from staged surgeries for intra-axial neoplasms, which are similar to complications associated with single-stage surgery for intraparenchymal lesions as well as multi-stage surgeries for skull base lesions.

Neurosurgery

staged

multi-stage

indications

complications

astrocytoma

glioma

cranial nerve palsies

timing

Staged resection of intramedullary spinal cord tumors was first described in 1911, and then subsequently, open staged resection of large intracranial lesions was reported by Dandy in 1925.^{1, 2} Advancement of the staged surgical approach resulted in staged surgeries readily being employed in the resection of petroclival meningiomas³ vestibular schwannomas⁴, trigeminal schwannomas,⁵ and various other skull base lesions.⁶ These “staged” (or “multiple-stage”) surgeries have also been carried out for vascular tumors,^{1, 7} giant aneurysms,⁸ and arteriovenous malformations (AVMs).^{9, 10} Despite this, there is a paucity of data regarding open staged resection of intrinsic, intra-axial neoplasms. Considerations, including the timing between surgeries, indications for staged approaches, and clinical outcomes following staged resection of intra-axial neoplasms remain poorly understood.

By improving long-term outcomes, minimizing operative morbidity and complications, and facilitating a safe maximal extent of resection, staged surgeries often combine two or more different surgical approaches in the resection of intra-axial tumors.¹⁰ This is particularly relevant in the resection of large tumors that span intracranial compartments (e.g., posterior and middle cranial fossae, infra- and supra-tentorial compartments) to minimize the disruption of or damage to surrounding neurovascular structures.

To date, a systematic review on staged open cranial surgery for the resection of primary intra-axial neoplasms has not – to the authors’ knowledge – been conducted. As such, we queried the published literature on open staged surgical resection of intra-axial neoplasms. We focus our discussion on four aspects of staged cranial surgery, including the surgical indications for staging, the timing between stages, involved surgical approaches, and postoperative complications.

Search Strategy

On August 1st, 2021, a literature search was conducted using PubMed, Web of Science, and Cochrane databases using the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) recommendations.¹¹ To enable the inclusion of as many relevant articles as possible, there were no restrictions on the date of publication when searching databases. The following Boolean search term was used: ("staged approach" OR "staged surgery" OR "staged treatment" OR "staged procedure" OR "staged operation" OR "2-staged" OR "two-staged" OR "multi-staged" OR "3-staged" OR "three-staged") AND (resection OR removal) AND (intra-axial OR intracranial OR brain) AND (tumor OR neoplasm OR glioblastoma OR glioma).

Screening of Included Studies

Titles and abstracts of studies for this systematic review were evaluated independently by two authors (NJB, JG). The reviewers then compared these selections, and disagreements were resolved by further discussion with the senior author (FPKH). Final selections were chosen by both authors independently after examining full-text articles. The reference lists from articles identified during our search were analyzed individually for additional studies that met inclusion criteria.

Variables and Inclusion/Exclusion criteria

All articles reviewed were subject to the following inclusion criteria: (1) English only, (2) primary clinical studies investigating intrinsic (malignant or benign), intra-axial, intracranial tumors treated with open surgery (craniotomy or craniectomy) with staged procedures separated by 1 day or more. All articles reviewed were also subject to the following exclusion criteria: (1) endoscopic endonasal approaches (EEA) for skull base lesions, (2) articles that appeared to be from a non-peer-reviewed medium, (3) articles with no clear description of patient data, and (4) articles of patients with extra-axial tumors (for which staged surgery has already been extensively described) such as meningiomas, vestibular schwannomas, trigeminal schwannomas, glomus jugulare tumors, hemangioblastomas, and craniopharyngiomas.

Qualitative Analysis

After the final articles were selected the Methodological Index for Nonrandomized Studies (MINORS) criteria was used to objectively evaluate the quality of the studies and assess the risk of bias for selected studies.¹² Each item on the MINORS checklist was independently scored by two authors (NJB, JG) as 0 (not reported), 1 (reported but inadequate), and 2 (reported and adequate). Since all selected articles were noncomparative studies, the maximum score was 16. As previously described,¹³ the authors considered a score of below 5 as poor, between 6 and 10 as moderate, and between 11 and 16 as good. Because scores were averaged, non-integer values were rounded down to reduce the risk of overestimating study quality.

Data Extraction

Following qualitative assessment, data was extracted for the following variables: sample size, year of publication, institution, nationality, patient demographics (i.e. gender and age), whether tumors were benign or malignant, location of tumors, tumor type, the timing between staged surgeries, indications for a staged approach, and complications.

Database Search

Our search yielded 58 results from PubMed, 50 results from Web of Science, and 1 result from Cochrane, with a total of 60 unique articles after the removal of duplicates (Fig. 1). Of the 60 unique papers from the database search and review of reference lists, 13 papers were examined in full-text review. An additional six papers were selected for full-text review after scrutinizing the references of included articles. Finally, 7 papers were selected (Table 1) and included for further analysis.^14–23 Types of papers included 3 case series, 3 case reports, and 1 technical note (Table 1). The study publication dates ranged from 1998–2019. The sample size across all the studies was 52 patients, and after filtering out inclusion and exclusion criteria per individual patient, the final cohort was 21 patients. The cohort consisted of 9 (43%) malignant, 5 (24%) benign, 5 (24%) unspecified, 2 (10%) WHO grade II. Although not mutually exclusive, a total of 5 studies covered the pediatric patient population, while 4 studies covered the adult patient population.

The pediatric patient population consisted of 17 patients with 6 (35%) males, 5 (29%) females, and 6 (35%) of unspecified sex treated between 2009–2019 (Table 2). The ages ranged from 18 months-17 years (mean 9 years). Tumor pathologies consisted of 5 (29%) astrocytomas, 2 (12%) ependymomas, 2 (12%) teratoid rhabdoid tumors, 2 (12%) oligodendromas, 1 (6%) glioma, 1 (6%) dysembryoplastic neuroepithelial tumor, 1 (6%) meningioangiomatosis, 1 (6%) pleomorphic xanthoastrocytoma, 1 (6%) ganglioglioma, and 1 (6%) germ cell tumor. The tumor primary sites consisted of 4 (24%) temporal lobe, 3 (18%) thalamic, 3 (18%) thalamopeduncular, 3 (18%) frontal lobe, 2 (12%) posterior fossa, 1 (6%) cerebral hemisphere, and 1 (6%) fronto-parietal lobe. The timing between surgeries was specified for 2 reports with times varying between 5–10 days. Three of the studies reported complication profiles; specified complications included subtle hemiparesis, hydrocephalus, CN VI and VII palsies, truncal ataxia, and cerebellar mutism.

Our adult patient population consisted of 4 patients with 1 male, 2 females, and 1 patient of unspecified sex treated between 1998–2019 and is summarized in Table 3. The ages ranged from 18–32 years (mean 25.5 years). Tumor pathologies consisted of 2 (50%) astrocytomas, 1 (25%) ependymoma, and 1 (25%) neuroectodermal tumor. The tumor primary sites consisted of 1 (25%) frontal lobe, 1 (25%) temporal lobe, 1 (25%) cerebellopontine angle tumor, and 1 (25%) mid- and parasagittal convexity tumor. The timing between surgeries was specified for 2 reports, with 1 report specifying 18 days and the other specifying 4 months. Three of the studies reported complication profiles including language and abstract thinking deficits, respiratory failure, and motor weakness.

The mean MINORS criteria score was 8.0 (range: 5.5–11) for the seven studies selected for this systematic review, corresponding to “moderate” overall quality. The study by Nkusi et al. received the highest score with 11 and only 1 study was considered “poor” quality; all 8 remaining studies were considered “moderate” quality.

The present study is – to the authors’ knowledge – the first systematic review on the utilization of staged surgical approaches for the resection of intra-axial (as opposed to extra-axial skull-base) neoplasms. There are a limited number of reported cases in the literature regarding surgical staging for intracranial neoplasms, with case reports or single-institutional retrospective case series comprising the majority. We observed that, in recent years, most staged intracranial surgeries for intra-axial neoplasms were performed within the pediatric patient population. Additionally, we found that neither the timing between staged procedures nor the associated cost of surgery were consistently reported in the included studies. The complications described for multi-staged approaches included neurological deficits that have previously been described for these same approaches when employed as a single stage.²⁴ Furthermore, no obvious complications occurred as a result of prolonged anesthesia, multiple inductions of anesthesia, peri-operative infections, or other complications associated with multiple procedures and/or hospitalizations. This systematic review highlights the paucity of data available on staged intra-axial tumor surgery and provides some evidence that performing a staged approach does not yield a significant increase in complications.

Although surgeries for large skull-base tumors are often staged successfully, staged surgeries for intra-axial tumors are rarely done intentionally, rather these tumors undergo second operations because residual tumor is found and associated with worse survival outcomes. ^1–6 Dandy first described the utilization of staged surgical resection for large tumors in 1925, there has been a relative scarcity of large case series presenting clinical outcomes for patients undergoing multiple-stage operations for the resection of intra-axial neoplasms. The majority of the published data on staged cranial surgeries has focused on benign extra-axial lesions such as petroclival meningiomas,³ vestibular schwannomas,²⁵ trigeminal schwannomas,²⁶ and pituitary adenomas.²⁷

Intracranial tumors that may require staging are those that are slow-growing and reach a large tumor volume at time of symptom onset. Tumors like glioblastomas are typically not resected through staged approaches due to rapid growth, and symptom onset with tumor volumes of 35 cm³ on average.^3–6 For example, in 1995 Comey et al. reported on 83 vestibular schwannoma patients who underwent staged resection, noting that residual tumor in the second stage was less tightly adherent to the brain stem.²⁸ Furthermore, in 2012 Raslan et al. reported that staged resection of large vestibular schwannomas improved facial nerve outcomes without added morbidity.⁴

In 1998, Nakase et al. reported on staged surgical resection of skull base tumors extending into the sub- and epidural spaces, and demonstrated that the blood supply to the tumors decreased following resection of the epidural tumor following the first operation.²⁷ Furthermore, the residual subdural tumors were soft and less vascular in the second stage which facilitated tumor resection. In 1990, Sekhar et al. reported on 41 patients with clival meningiomas and noted that staged operations, in conjunction with specific approaches and surgeon experience, correlated with fewer postoperative complications.²⁹

At present, reported outcomes on staged intracranial surgeries are mostly limited to small single-institutional case series and case reports. Many of these cases are benign intracranial neoplasms, with a small subset of malignant neoplasms reported in the pediatric population. Although multiple-staged surgeries may carry an increased risk of infection and venous thromboembolism, the argument in support of their utilization centers around planning multiple operations for maximum safe resection. While doing so theoretically poses an additional operative risk, it can be argued that potential benefits may outweigh long-term consequences of subtotal resection and subsequent recurrence.³⁶

Furthermore, increased risk of surgical infection in staged surgeries is theoretical and has never been established. In our review, we found no case of reported peri-operative infection in any staged surgery patient. Additionally, the benefits of a single, long-duration surgery, as opposed to numerous shorter surgeries, remain unclear. It can be argued that a single surgery may be more cost-effective and pose less risk with respect to intra- and post-operative complications, however, the risk of intraoperative complications correlates with surgical length, and the patient may actually benefit from two shorter procedures as opposed to one longer procedure.³⁰ Additionally, studies comparing costs between single and multi-staged surgeries are required before definitive conclusions regarding cost-effectiveness can be made.

Interestingly, the cost is not the only gray area in need of further evaluation as the optimal timing between individual components of a multiple-stage surgery remains poorly understood. The second operation would ideally be performed prior to the development of scar tissue or revascularization of the tumor. From the limited data currently available, Comey et al. reported an inter-stage interval ranging from 0.5 to 32 weeks (mean: 4.5 weeks), dependent upon computed tomography (CT) imaging demonstrating less brain stem compression from the tumor.²⁸ By contrast, Nakase et al. reported an inter-stage interval ranging from 4 to 12 weeks (mean: 5.9 weeks).²⁷ As more robust evidence is required before consensus statement can be offered, further investigation into the optimal inter-stage timing between procedures is warranted. In our study, timing between surgeries varied from 5 days to a few weeks in pediatric patients and 18 days to four months in adult patients with no clear benefit for any timeframe reported.

With respect to the clinical reasoning behind staging cranial surgery, there are several indications for staged approaches to the resection of primary CNS neoplasms. First, staged surgery may be indicated for large volume tumors in which initial tumor debulking allows for removal of a large percentage of the tumor, after which tumor tissue and cleavage plan are easier to recognize due to time elapsed prior to the subsequent surgery (and the resulting cessation of irritation of the surgical space).³¹ Furthermore, in a study on the extent of resection of diffuse intra-axial tumors, Kavouridis et al. reported that higher preoperative tumor volume and higher postoperative tumor residuals were associated with worse overall survival, progression-free survival, and malignant progression-free survival³². This trend was evident across all intra-axial neoplasms but was distinctly pronounced in more aggressive astrocytoma subtypes. These results indicate that staged resection may be favored when attempting maximum safe resection for astrocytomas and other high-grade lesions. In their report on an atypical choroid plexus papilloma, Takahashi and colleagues suggested that the exceptionally vascular nature of the tumor described ultimately led to their decision to stage surgery.¹⁴ Similar reports in the literature describe instances in which significant vascularity of intra-axial tumors has led to the decision to pursue a staged surgery intraoperatively. Kumabe et al. reported a case in which multi-stage surgery separating debulking and subcortical mapping was used in a case of anaplastic astrocytoma, and gross total resection without neurological deficit was achieved.¹⁷ In the studies analyzed in our review, we discovered pediatric intra-axial tumors were staged for two reasons. First, is the intraoperative concern of hemorrhage during the surgery, leading to profound hypotension and inability to continue the resection safely. This led neurosurgeons to prematurely stop resection and continue total removal through a second staged procedure. The second reason reported is planned staging due to large tumors requiring resection around eloquent areas of speech and motor cortices that allowed for awake functional mapping after a primary resection around less eloquent structures.²⁰

Potential indications for staged surgery for lower-grade gliomas have been previously discussed in the literature, including size > 100 cm³, multi-lobar (e.g. fronto-temporo-insular, temporo-parietal-occipital) extension, and intervening eloquent fasciculi and/or critical neurovascular structures that create an anatomic partition.⁸ Further indications may be ascertained from reports regarding the staging of complex skull base procedures, which are far more commonly described than staged surgery for intraparenchymal lesions. For example, it is notable that Nakamura utilized a staged retrosigmoid lateral suboccipital and frontolateral approach to remove a retrosellar upper clival meningioma extending to the suprasellar region in order to minimize the disruption of venous drainage and damage to surrounding neurovascular structures.¹⁵ Additionally, Xu and colleagues reported that resection of petroclival meningiomas using staged orbitozygomatic and retrosigmoid approaches require separate procedures, incisions, and general anesthetic inductions that may not be beneficial unless an experienced neurootologist is available for temporal bone exposure.³³ Ogiwara et al. reported a single case in which a staged surgery was employed in order to mitigate blood loss that occurred intraoperatively during the first surgery in a pediatric patient with a choroid plexus papilloma.²¹ Futhermore, Nkusi et al. reported on 12 patients with staged meningioma resection, with a subset of patients in which the decision to stage surgery was made intraoperatively.¹⁹ This decision was based on the presence of cerebral edema, profuse bleeding with hemodynamic instability, and tumor abutment into cranial nerves (e.g., in the case of CPA tumors). Nakamura et al. report that an intraoperative decision to stage a surgery for supratentorial anaplastic ependymoma was made based on tumor hypervascularity, size, and location.¹⁵ Todeschini et al. reported that the second stage of a giant olfactory groove meningioma resulted in relaxation of brain tissue, less edema, reduced need for retraction, and facilitation of gross total resection.³⁴ Finally, staged surgery may be all but required for particularly expansive or complex lesions occupying more than one compartment. For example, Foreman describes utilization of a two-stage approach in for resection of an atypical teratoid rhabdoid tumor occupying the supra- and infratentorial compartments in a pediatric patient.¹⁸

In their study on staged surgery for patients with glomus jugulare tumors with significant intracranial extension, Jayashankar and colleagues provide their reasons for staging surgery as a summary rationale that draws upon the main takeaway indications for staging surgery. These include 1) removal of extensive intracranial lesions in close proximity to the lower cranial nerves; 2) devascularization of the tumor during the first stage to decrease intraoperative hemorrhage during the second stage (also causes the tumor to shrink and facilitates excision); and 3) to facilitate the sealing of dural defects in the second stage due to a smaller area of exposure.³⁵ Complete resection by staged surgeries has been associated with minimized operative morbidity and improved long-term clinical outcomes, therefore staging may be an important tool to fully resect intra-axial tumors.^1,2,7

Limitations

This systematic review presents a few limitations worth discussing. First, due to the paucity of literature available on the topic, making definite conclusions is quite arduous. Future prospective evaluations comparing complication profiles of patients undergoing staged versus non-staged resections for large intracranial tumors are warranted. As has been previously noted, the available literature describing the exact parameters in which staged surgery for primary intra-axial brain lesions is indicated is a shortcoming.³⁶ Furthermore, another data limitation is that many studies omitted specific characteristics of their patient cohorts or related outcomes making comparisons between single and multi-staged surgery difficult. Additionally, due to reporting within the studies, we did not find any papers that included both staged and non-staged procedures to accurately compare via meta-analysis the complication profiles between these approaches. As such, this topic warrants future investigation via retrospective cohort studies and prospective randomized clinical trials comparing single versus staged surgical resections.^37–41 Unfortunately, we were not able to compare complication profiles between pediatric and adult cases as our cohort size for adults was limited to 4 patients. Finally, none of the papers in our review discussed differences in cost between single versus staged procedures. Future studies should elucidate this difference and assess for cost-effectiveness of staged cranial surgery for primary brain lesions. Nonetheless, despite these limitations, our study provides the first systematic review on staged intracranial tumor resection reporting on the surgical indications, timing between surgeries, surgical approaches, complication profiles, and clinical outcomes staged approaches to resection of intra-axial lesions.

This study comprises what is – to the author’s knowledge – the first systematic review on staged surgical procedures for primary intra-axial neoplasms. We found that within the literature, staged approaches were most commonly reported for the pediatric patient population as compared to adult patients and were most associated with diagnoses of astrocytoma and glioma. Overall, there exists a large heterogeneity of staged intracranial surgeries in terms of surgical approach and timing between surgeries. Finally, the staged approach does not appear to increase complication rates, which makes intuitive sense because it should offer theoretical advantages that outweigh risks when properly indicated. Future studies are warranted to investigate the long-term clinical outcomes of patients undergoing staged resection of primary intra-axial lesions compared to single stage surgeries.

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Table 1

Study Authors

Year

Title

Journal

Study Design

Institution

Sample Size

Number of Patients

Malignant/Benign

Pediatrics/Adult

MINORS Score

Indication for Staging (planned/intraoperative/unclear)

Nakamura T, Fukuoka K, Ikeda J, Yoshitomi M, Udaka N, Tanoshima R, Tateishi K, Yamanaka S, Ichimura K, Yamamoto T.¹⁵

2017

Encouraging option of multi-staged gross total resection for a C11orf-RelA fusion-positive supratentorial anaplastic ependymoma.

Brain Tumor Pathology

Case report

Yokohama City University, Department of Neurosurgery

1

Malignant

Pediatric

7

Planned

Cinalli G, Aguirre DT, Mirone G, Ruggiero C, Cascone D, Quaglietta L, Aliberti F, Santi SD, Buonocore MC, Nastro A, Spennato P.¹⁶

2018

Surgical treatment of thalamic tumors in children.

Journal of Neurosurgery: Pediatrics

Case series

Santobono-Pausilipon Children's Hospital, Department of Pediatric Neurosurgery

28

6

4/6 benign; 2/6 malignant

Pediatric

9.5

Unclear

Kumabe T, Nakasato N, Suzuki K, Sato K, Sonoda Y, Kawagishi J, Yoshimoto T.¹⁷

1998

Two-staged resection of a left frontal astrocytoma involving the operculum and insula using intraoperative neurophysiological monitoring--case report.

Neurol Med Chir (Tokyo)

Case report

Tohoku University School of Medicine, Department of Neurosurgery

1

Malignant

Adult

7.5

Planned

Foreman PM, Madura CJ, Johnston JM, Rocque BG¹⁸

2016

Two-stage surgical resection of an atypical teratoid rhabdoid tumor occupying the infratentorial and supratentorial compartment in children under two years: Report of two cases

International Journal of Surgery Case Reports

Case series

University of Alabama, Department of Neurosurgery

2

Malignant

Pediatric

7.5

Case 1: Intraoperative hemmorhage Case 2: Planned Resection

Nkusi AE, Muneza S, Hakizimana D, Nshuti S, Munyemana P, Shingiro E¹⁹

2019

Staged brain tumour resection for better outcomes: Management challenges and lessons learned from a series of 12 patients at a tertiary referral hospital in Kigali, Rwanda

East and Central African Journal of Surgery

Case series

King Faisal Hospital

12

2

WHO Grade II

Pediatric and Adult

11

Case 1: Intraoperative hemmorhage Case 2: Planned Resection

Bollo RJ, Carlson C, Schevon C, Wisoff JH, Devinsky O, Weiner HL.²⁰

2009

Extraoperative Functional Mapping and Staged Resection of Supratentorial Tumors near Eloquent Cortex in Children

Pediatric Neurosurgery

Technical note

NYU Langone Medical Center and New York University School of Medicine, Department of Neurosurgery

8

2/8 malignant, 1/8 benign, 5/8 not specified

Pediatric and Adult

8

Planned

Kouyialis AT, Boviatsis EI, Karampelas IK, Korfias S, Korkolopoulou P, Sakas DE²².

2005

Primitive supratentorial neuroectodermal tumor in an adult

Journal of Clinical Neuroscience

Case report

University of Athens Medical School, Department of Neurosurgery

1

Malignant

Adult

5.5

Planned

Table 2

Table 3 is not available with this version

The authors declare no competing interests.

Staged Open Cranial Surgery for Primary Intra-axial Neoplasms: A Systematic Review

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

Introduction

Methods

Search Strategy

Screening of Included Studies

Variables and Inclusion/Exclusion criteria

Qualitative Analysis

Data Extraction

Results

Database Search

Discussion

Limitations

Conclusion

References

Tables

Additional Declarations

Status:

Version 1