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. Author manuscript; available in PMC: 2022 Aug 17.
Published in final edited form as: J Neurosurg. 2021 Sep 10;136(4):1045–1051. doi: 10.3171/2021.3.JNS204347

Risk of tract recurrence with stereotactic biopsy of brain metastases: an 18-year cancer center experience

Joseph A Carnevale 1,2, Brandon S Imber 3, Graham M Winston 1,2, Jacob L Goldberg 1,2, Ase Ballangrud 4, Cameron W Brennan 1, Kathryn Beal 3, Viviane Tabar 1, Nelson S Moss 1
PMCID: PMC9383706  NIHMSID: NIHMS1829100  PMID: 34507279

Abstract

OBJECTIVE

Stereotactic biopsy is increasingly performed on brain metastases (BrMs) as improving cancer outcomes drive aggressive multimodality treatment, including laser interstitial thermal therapy (LITT). However, the tract recurrence (TR) risk is poorly defined in an era defined by focused-irradiation paradigms. As such, the authors aimed to define indications and adjuvant therapies for this procedure and evaluate the BrM-biopsy TR rate.

METHODS

In a single-center retrospective review, the authors identified stereotactic BrM biopsies performed from 2002 to 2020. Surgical indications, radiographic characteristics, stereotactic planning, dosimetry, pre- and postoperative CNS-directed and systemic treatments, and clinical courses were collected. Recurrence was evaluated using RANO-BM (Response Assessment in Neuro-Oncology Brain Metastases) criteria.

RESULTS

In total, 499 patients underwent stereotactic intracranial biopsy for any diagnosis, of whom 25 patients (5.0%) underwent biopsy for pathologically confirmed viable BrM, a proportion that increased over the time period studied. Twelve of the 25 BrM patients had ≥ 3 months of radiographic follow-up, of whom 6 patients (50%) developed new metastatic growth along the tract at a median of 5.0 months post-biopsy (range 2.3–17.1 months). All of the TR cases had undergone pre- or early post-biopsy stereotactic radiosurgery (SRS), and 3 had also undergone LITT at the time of initial biopsy. TRs were treated with resection, reirradiation, or observation/systemic therapy.

CONCLUSIONS

In this study the authors identified a nontrivial, higher than previously described rate of BrM-biopsy tract recurrence, which often required additional surgery or radiation and justified close radiographic surveillance. As BrMs are commonly treated with SRS limited to enhancing tumor margins, consideration should be made, in cases lacking CNS-active systemic treatments, to include biopsy tracts in adjuvant radiation plans where feasible.

Keywords: brain metastases, stereotactic biopsy, laser interstitial thermal therapy, radiosurgery, oncology

Brain metastases (BrMs) affect at least 20% of all cancer patients, with the true incidence likely higher considering the lack of routine CNS surveillance for most cancer diagnoses.1–3 This population is increasing in light of improving survival in a variety of cancer types, a growing palette of anticancer agents effective in the CNS, and an increasing use of multimodal therapy in recognition of the palliative importance of controlling CNS progression.4,5 Focused radiation via stereotactic radiosurgery (SRS) has been a keystone of multimodality BrM therapy given its efficacy, which approaches 90% in the upfront setting, and an improved neurocognitive toxicity profile compared to whole-brain irradiation.1–3,6–8 When necessary, resection plus adjuvant irradiation provides local control to approximately 85% of such treated lesions.9–11,41 Given the efficacy of these modalities, biopsy has historically been rarely required in the absence of any need for histological confirmation.

However, as the prevalence and longevity of BrM and cancer patients generally increase, a growing population of patients require such histological confirmation. These indications include patients with long-latent, otherwise nonmetastatic systemic disease, as well as those with the potential for a novel tumor such as a glioma, brain metastases of unknown origin, multiple malignancies, and increasingly, patients with previous irradiation and equivocal radiographic findings concerning for CNS progression. Generally, BrMs are removed when tissue is required, except in cases of high potential for neurological morbidity or when the patient’s functional status or preferences point against this. The role of BrM biopsy is also growing among previously SRS-treated lesions to distinguish tumor recurrence from radiation necrosis, particularly as biopsy can be performed in conjunction with focal therapy via laser interstitial thermal therapy (LITT) geared toward either detected process.12,42 Additional indications include tumor cyst decompression in order to shrink unresectable metastases for palliation or into a more attractive radiation target, or to rule out infectious or other nonneoplastic etiologies, particularly in cases of immune compromise in patients undergoing systemic cancer treatment.13 Finally, a still-limited but growing role may be developing in the age of genetically targeted therapies in light of evidence of discordance of actionable genetic mutations in parenchymal BrM versus systemic tumors in some 50% of cases.8

While the risk of tract seeding following biopsy is reassuringly low in series evaluating brain tumor biopsies in general, which heavily include gliomas and CNS lymphoma (CNSL), this risk has not been described in the BrM population.14,15 We hypothesize that the low rates of tract seeding seen in the former groups are not generalizable to biopsied BrMs for several reasons, including that gliomas and CNSL are more commonly treated with partial-brain or whole-brain radiation therapy (WBRT), whereas the more sparing use of these wide-field paradigms for BrM leave untreated tracts vulnerable to seeding. In addition, infiltrative progression with high rates of distant/discontiguous recurrence exhibited in the former diseases make the attribution of tract disease to the act of biopsy less plausible, and poor survival potentially makes such recurrences less likely to be observed than in more survivable forms of brain metastatic cancer with longer follow-up. We thus describe our indications for this procedure to shed light on its role in a busy neurosurgical oncology practice and report the rates of tract recurrence (TR) in what is to our knowledge the largest described cohort to date of biopsied brain metastases.

Methods

A retrospective review of a single National Cancer Institute (NCI)–designated cancer center institutional database was performed under an IRB privacy waiver. Consecutive intracranial stereotactic biopsy cases from January 2002 through October 2020 were reviewed. BrM cases were selected for additional review and were excluded if pathology was not available, consistent only with treatment effect, or otherwise without evidence of viable metastatic disease. Patient demographics, tumor radiographic characteristics, surgical decision-making, stereotactic planning, tumor histology, pre- and postoperative radiotherapy, pre- and postoperative CNS-directed and systemic treatments, and post-biopsy courses were collected. Tumor margins were defined as the enhancing edge of the tumor on the immediate pre-biopsy imaging. Tumor volume was obtained using the paint tool in Brainlab iPlan software. Surgical indications were obtained from the neurosurgeon’s pre-operative notes. Stereotactic planning was derived from postoperative MR and/or CT imaging in all cases, with tract length defined as the distance from the inner calvarial table at the site of the burr hole to the most superficial enhancing component of the BrM. Where visible on 3D reconstructions, the length of the actual trajectory taken was measured, and where not visible the shortest distance from the burr hole to the tumor’s enhancing margin was reported. Recurrence was evaluated using RANO-BM (Response Assessment in Neuro-Oncology Brain Metastases) criteria.

Results

In total, 499 consecutive patients who underwent stereotactic intracranial biopsy for any brain tumor diagnosis were evaluated. The majority of cases yielded pathology consistent with glioma (61%) or CNSL (19%). Overall, biopsies in 25 patients (5.0%) yielded pathologically confirmed viable BrM, and this proportion increased from 2.6% in 2002–2007 to 7.9% in 2015–2020 (Fig. 1; Fisher’s exact test for earliest to latest time period, p = 0.05), and this population served as the study sample for the remainder of the analysis. For comparison, 2730 patients underwent craniotomy for metastasis resection during the study period.

FIG. 1.

FIG. 1.

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The growing role of BrM biopsy at an NCI-designated cancer center. A: Brain biopsy pathology from 2002 through 2020 (n = 499) with biopsy indication for histologically confirmed BrMs (n = 25). B: Stereotactic biopsies at Memorial Sloan Kettering Cancer Center separated by year, showing an increase in percentage of biopsy-proven BrMs over this 18-year period. Left: 2002–2007 with 2.6% BrMs. Center: 2008–2014 with 4.2% BrMs. Right: 2015–2020 with 7.9% BrMs.

BrM histologies included non–small cell lung cancer (n = 7); small cell lung and squamous cell carcinoma (n = 3 each); breast cancer and melanoma (n = 2 each); and neuroendocrine (n = 2) and endometrial, ovarian, renal cell, urothelial and unknown carcinomas, and sarcoma (n = 1 each). Detailed biopsy indications are described in Fig. 1, with quiescent systemic cancer and therapeutic aspiration/thermal ablation for large unresectable tumors the most common. Among tumors sampled because of diagnostic ambiguity following prior radiation therapy, all were imaged with perfusion MRI (with hyperperfusion suspicious for recurrence), and two-thirds were studied with brain FDG-PET workup (both with suspicious hyperavidity) within 3 months preoperatively. The average patient age was 63.3 years (range 35–83 years) with a female pre-dominance (64.0%), and the median radiographic follow-up duration was 5.7 months (range 0.6–30.6 months). Biopsied lesions had a median maximal diameter of 2.88 cm (range 1.2–4.3 cm) and a median volume of 7.45 cm3 (range 0.8–26.5 cm3). Median biopsy tract length was 3.5 cm from the inner calvarial table to the superficial enhancing margin of the tumor (range 0.6–7.3 cm). There were no intraoperative or postoperative complications. Following biopsy, 88% (22/25) of patients underwent postoperative irradiation with either hypofractionated SRS (16/22, 73%) with plans that did not specifically target the biopsy tract, or WBRT (6/22, 27%). Ten patients (40%) were also treated with systemic cancer-directed chemotherapy or immunotherapy. Overall, 40% (10/25) of patients remain alive at last follow-up. Of the 15 patients who died, 10 succumbed to progressive systemic disease, 4 to CNS progression, and 1 patient to an unknown cause.

Twelve (48%) patients had ≥ 3 months of radiographic follow-up (median 11.9 months; range 3.0–30.6 months). Nine patients had no radiographic follow-up, and 4 had imaging < 3 months (range 18–85 days) post-biopsy. Of these 13 patients with inadequate follow-up, 10 had died within 10 months of biopsy, 2 biopsies were recently performed within 3 months of this writing, and 1 patient was lost to follow-up.

Of patients with ≥ 3 months of radiographic follow-up, 6 (50%) developed recurrence along the biopsy tract at a median of 5.0 months (range 2.3–17.1 months) post-biopsy. Table 1 characterizes the 6 patients with TR. Tracts trended toward being longer in cases in which TR ultimately developed, with a median tract length of 4.8 cm (range 2.4–7.3 cm) versus 2.9 cm (range 0.6–6.4 cm) for those cases in which TR did not subsequently develop (p = 0.10). The median distance of the recurrence from the tumor surface was 3.6 cm (range 0.5–5.5 cm). Two patients (patients 2 and 4) had post-SRS recurrences and were sampled in the setting of diagnostic ambiguity (patient 3 additionally had undergone WBRT for small cell carcinoma); both of these lesions underwent intraoperative LITT immediately following biopsy. The remaining 4 patients had newly diagnosed BrM and were treated with SRS post-biopsy; 1 patient also underwent post-biopsy LITT. These patients received focal radiation based on planning CT obtained 6–27 days post-biopsy at a prescription dose of 25 Gy in 5 fractions (1 patient) or 27 Gy in 3 fractions (3 patients) on a linear accelerator with a multileaf collimator using multiple coplanar and noncoplanar fields. Of the 6 patients with TR, 2 (patients 4 and 5) had other BrMs at the time of biopsy, both of which were stable at the time of TR. The biopsy tract was not included in any postoperative radiation treatment plans (Fig. 2). The tract areas all received a minimal, nontumoricidal exposure to prior focal radiation (< 5 Gy in 3–5 fractions). TRs were treated with resection (n = 2, both with pathologic confirmation), reirradiation (n = 2), or observation/systemic therapy.

TABLE 1.

Clinical and radiographic characteristics in patients with stereotactic biopsy TR

Pt No. Histology Pre-Biopsy Irradiation (Gy × no. fractions) Post-Biopsy Irradiation (Gy × no. fractions) LITT Post-Biopsy Cancer-Directed Therapy Biopsy Tract Length (cm) Biopsy to TR Time (mos) TR Diameter (cm) TR to Tumor Surface Distance (cm) Radiation Dose to Subsequent TR Site Salvage Op/Systemic Treatment for Recurrence
1 Ovarian NA SBRT (5 Gy × 5) N Carboplatin, doxorubicin 7.3 8.7 1.0 5.5 NA Carboplatin/doxorubicin
2 SCC SRS (18 Gy) + WBRT (2.5 Gy × 10) NA Y Temozolomide, carboplatin, etoposide 2.4 7.8 1.3 0.5 Declined WBRT Carboplatin/etoposide
3 RCC NA SBRT (9 Gy × 3) Y Ipilimumab, nivolumab 4.8 5.0 1.0 3.1 NA Ipilimumab + nivolumab; open resection w/intraop brachytherapy placement*
4 SqCC SBRT (5 Gy × 5) NA Y Nivolumab 4.7 4.2 1.3 3.8 PBRT (2 Gy × 18) Nivolumab; open resection w/intraop brachytherapy placement*
5 Melanoma NA SBRT (9 Gy × 3) N Nivolumab, bevacizumab 6.0 2.3 1.3 5.4 Proton (6 Gy × 5) NA
6 Neuroendocrine NA SBRT (9 Gy × 3) N Bevacizumab 3.0 3.0 2.4 1.1 SBRT (9 Gy × 3) NA
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NA = not applicable; PBRT = partial-brain radiotherapy; pt = patient; RCC = renal cell carcinoma; SBRT = stereotactic body radiotherapy; SCC = small cell carcinoma; SqCC = squamous cell carcinoma; SRS = single-fraction stereotactic radiosurgery.

*

Both patients had pathologic confirmation of viable disease upon resection.

FIG. 2.

FIG. 2.

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Radiographic highlights of the six biopsy TRs. Each row reflects a different patient organized by whether tract failure was post-SRS (patients 1, 3, 5, and 6 [A]) or postsalvage LITT (patients 2 and 4 [B]). A: The first column reflects representative pre-biopsy contrast-enhanced T1 MRI. The second two columns show a color-wash legend of the relative radiation dose delivered to the metastases as a percentage of the prescribed dose (i.e., 90% is 90% of the prescribed radiotherapy dose) and the dosimetry distributions in the coronal plane. Of note, the tract failures all subsequently developed outside of the high-dose radiation volume. The third column shows the biopsy TRs on T1 postcontrast MRI with the yellow boxes focused on the area of recurrence. B: The columns show MRI of the pre-biopsy MRI and TR, respectively. Figure is available in color online only.

Discussion

BrMs are treated with multimodality therapy, including local external-beam irradiation or resection, cancer-directed systemic therapy, and often with combined strategies. The use of stereotactic biopsy has historically therefore been limited to sampling in cases of diagnostic uncertainty, e.g., in patients without known systemic malignancy, with latent or multiple potentially responsible cancers, with lesions not amenable to resection, or when alternative diagnoses such as infection or primary brain tumor are plausible.14–17

In this 18-year experience, more than half of stereotactic BrM biopsies were performed in the last 5 years, and the importance of this indication will likely increase. This is in part due to the growing BrM patient population for whom aggressive multimodality therapy is indicated, and also to the growing population requiring post-SRS sampling in the setting of radiographic ambiguity and treatment effect. Promising early data support the potential for a growing theranostic LITT indication for this population.18 Indeed, one of our reported cases was such a patient. Biopsy may become additionally popularized as the menu of molecular alterations with CNS-efficacious therapies (and concern for discordance with extracranially sampled disease sites) expands.

Our study highlights the risk of BrM tract seeding following stereotactic biopsy. In addition to the commonly described complications of hemorrhage, infection, and nondiagnostic biopsy, we identified an additional complication specific to BrM biopsy that should be taken into consideration, both in patient counseling and postoperative treatment planning.19,20 Table 2 summarizes previous reports of stereotactic biopsy TR in the literature. In one of the largest series of brain tumor biopsies, with 8 BrMs and 7 CNSLs among nearly 200 brain tumors, Grunert et al. identified no cases of TR, however this was not an a priori outcome, and radiographic follow-up was not specified, making its utility to answer this specific question limited.14 Various other case reports and series describe stereotactic biopsy TR in other pathologies, predominantly primary brain tumors. These include TR in pineoblastoma, germinoma, and craniopharyngioma.21–24 However, best-studied are gliomas, especially high-grade gliomas (HGGs), which have been shown to have tract dissemination rates ranging from 0.3% to 9%, and occurring some 3–6 months following biopsy.15,16,18,21,22,25–29

TABLE 2.

Literature review on stereotactic biopsy TR

Authors & Year No. of Stereotactically Biopsied Viable Tumors Pathology, No. (%) TR, No. (%)
Case series
 Karlsson et al., 199715 22* 22 BrM (100%) 2/22 (9%)
 Regis et al., 199621 370* (all pineal region) 101 (27%) germinoma, 98 (27%) glioma, 10 (3%) BrM, 2 (1%) lymphoma 1/370 (0.3%), not a priori outcome measure in series
 Current series 25, 12 w/ ≥3 mos of radiographic follow-up 25 BrM (100%) 6/12 (50%)
Case reports
 Rosenfeld et al., 199022 1 Pineoblastoma 1
 Perrin & Bernstein, 199826 1 Glioma: AA 1
 Pierallini et al., 199928 1 Glioma: GBM 1
 Aichholzer et al., 200127 1 Glioma: GBM 1
 Steinmetz et al., 200118 1 Glioma: GBM 1
 Kim et al., 200325 1 Glioma: AA 1
 Bianco et al., 200623 1 Craniopharyngioma 1
 Choi et al., 200724 1 Germinoma 1
 Pinggera et al., 201716 1 BrM: RCC 1
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AA = anaplastic astrocytoma; GBM = glioblastoma.

*

Duration of radiographic follow-up was not specified for either of these series.

Acknowledging small numbers, one hypothesis for the differences in the tract failure rates from our reported BrM experience compared to published HGG and CNSL series reflects typical adjuvant treatment paradigms. For example, nominally lower tract failures in CNSL cases are likely due to the fact that this is treated as a more disseminated disease: post-biopsy treatments include systemic, methotrexate-based chemotherapy regimens and/or WBRT, which address the biopsy tract in addition to the sampled gross disease. Adjuvant radiotherapy fields for HGG are also typically broad, extending several centimeters from visible postcontrast and/or FLAIR abnormalities on postoperative MR images.30,31 Therefore, it is plausible that the biopsy tracts are more often partially or completely contained within the irradiated area, reducing the risk of subsequent tract failure. In contrast, the standard of care for limited BrM remains stereotactic radiotherapy, which by design attempts to minimize the dose to the surrounding unaffected brain tissue. Importantly, in contrast to our legacy institutional practice of not treating tracts in metastasis biopsy cases, expert consensus contouring guidelines for adjuvant SRS in post–open metastasis resection cases call for tract coverage.32 This theoretical risk of local recurrence for open resection cases has even prompted the exploration of neoadjuvant SRS, which may reduce in-field/tract recurrence via cytoreduction prior to any seeding.33,34

We do not have the requisite numbers to test the hypothesis that BrM patients who receive post-biopsy WBRT have fewer tract failures versus those who received stereotactic treatments. This comparison may also be confounded by the fact that patients who undergo WBRT are likely to have greater intracranial disease burden or poorer performance status, both of which might influence the propensity to develop tract failures.

Given the historical rarity of BrM biopsy, no systematic evaluation of such patients has been performed in the MRI era. Case series have reported TR in renal cell carcinoma and non–small cell lung cancer.16,35 In a series of 22 patients who underwent stereotactic, frame-based tumor biopsy from 1984 to 1996, 2 (9%) developed biopsy tract seeding on follow-up imaging. The authors did not enumerate the proportion of patients who had radiographic follow-up, or the length of such follow-up. However, it is likely that patient survival was significantly shorter in the era > 20 years earlier than in the current series, prior to the advent of many efficacious cancer therapies and the widespread use of SRS. The increased rate of TR reported herein is also likely related to the improved sensitivity of MRI relative to CT-based surveillance available in the earlier series.

The current data serve to demonstrate a potential risk factor of biopsy in the era of focused local CNS therapy for brain metastases. While laboratory data have shown that some 103–104 cells are drawn into the biopsy tracts, and some 104–106 cells are needed to establish a successful metastatic implant, the most robust (and reassuring) brain tumor biopsy seeding data are from glioma brain malignancy populations in which patients are also treated with wide-field irradiation and/or brain-penetrant and active systemic therapy, including WBRT and temozolomide.16,36,37 Prospective validation of this finding is unfeasible given the still-relative rarity of this procedure and the limited life expectancy of these patients, and the morbidity of TR, are not always clinically significant (though notably all patients underwent additional treatment, and 2 required resection of recurrences). In many cases, these data justify close imaging surveillance and focused radiation of any recurrence. It may also make sense to consider upfront expanded-field irradiation to include biopsy tracts for lesions that are otherwise planned for SRS, in the absence of appropriate CNS-active systemic therapy, for example, anaplastic lymphoma kinase (ALK)–directed or epidermal growth factor receptor (EGFR)–third-generation EGFR-directed therapy.38–40,43,44

This decision will undoubtedly be case specific, as the addition of at-times long biopsy tracts could result in significantly larger or spatially irregular treated volumes. In general, increasing SRS treatment volumes increases the subsequent risk of radionecrosis, though this may not be the case for the addition of a narrow cylindrical field.10 Furthermore, for certain patients, safely treating expanded fields may necessitate SRS dose reduction, thus forcing a balance between local control and potential toxicity risks. Identification of robust predictors of tract failure (e.g., histology, tract length, lesion size, or intracranial disease trajectory) would help to better tailor SRS treatment fields.

Conclusions

Brain metastasis biopsy, a rare but increasingly indicated procedure, carries a nontrivial risk of tract recurrence requiring close imaging surveillance. While recurrence can be managed in many cases with focused radiation, in some cases this can impose morbidity or require additional procedures. In selected cases, upfront tract-directed irradiation can be considered in the absence of CNS-active cancer therapy options.

Acknowledgments

This research was funded in part through the National Institutes of Health/National Cancer Institute Cancer Center Support Grant P30 CA008748.

ABBREVIATIONS

BrM

brain metastasis

CNSL

CNS lymphoma

HGG

high-grade glioma

LITT

laser interstitial thermal therapy

NCI

National Cancer Institute

SRS

stereotactic radiosurgery

TR

tract recurrence

WBRT

whole-brain radiation therapy

Footnotes

Disclosures

Dr. Brennan: direct stock ownership, AVEO Pharma; patent holder, Elucida Oncology. Dr. Moss: received consulting fees in the last year from AstraZeneca.

Supplemental Information

Previous Presentations

Presented at the online Society for Neuro-Oncology Brain Metastasis Symposium in August 2020 and the online Society for Neuro-Oncology Meeting in November 2020.

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