Quantitative Evaluation of Local Control and Wound Healing Following Surgery and Stereotactic Spine Radiosurgery for Spine Tumors

doi:10.1016/j.wneu.2015.10.075

World Neurosurgery

Volume 87, March 2016, Pages 48-54

https://doi.org/10.1016/j.wneu.2015.10.075 Get rights and content

Objective

The present study evaluated the optimal measuring criteria to assess spinal tumor response to surgery followed by stereotactic spine radiosurgery (SRS) and reports the local control and wound complication rates following combined multimodality treatment.

Methods and Materials

Prospectively collected patient information was retrospectively reviewed to identify patients treated with spine surgery followed by SRS. Tumor sizes and volumetric assessment were formally measured. Local control status was defined according to World Health Organization (WHO, bidimensional), RECIST (unidimensional), or volumetric size change. Statistical comparative assessments of tumor measurements were performed.

Results

Twenty-two patients were eligible for evaluation after having undergone surgery followed by single-fraction SRS within a 2-month period. Seventeen had follow-up magnetic resonance imaging (MRI) with a mean patient follow-up of 12.59 months (range 3–36 months). None developed wound complication after radiation therapy (95% lower confidence bound 13%). Two patients had clinical recurrence while 15 of 17 achieved local control (88.3%). A test of marginal homogeneity for RECIST versus WHO was not statistically significant, P = 1.0 suggesting similar response classifications with both systems. Spearman correlations among 1) volumetric assessment, 2) bidimensional size, and 3) unidimensional size were significant for all groups (P < 0.05).

Conclusion

High local control rates can be achieved with surgery followed by SRS. Further, adjuvant SRS following spine tumor surgery delivers less radiation to the wound than conventional radiation and thus potentially reduces wound complications. Unidimensional, bidimensional, and volumetric tumor assessments demonstrate similar results. Hence the use of the simpler RECIST criteria is suitable and appropriate for evaluating the response to treatment after spine radiosurgery.

Introduction

The management of metastatic spine tumors has extensively changed in the recent decades. Previously, the lack of spinal instrumentation and inability to approach the spine by ventral or lateral approaches yielded poor surgical results and showed no benefit over conventional radiation.1, 2, 3, 4, 5, 6 However, advances in operative skill sets and instrumentation have allowed surgeons to directly decompress the spinal cord, swinging the pendulum back to operative management of spine tumors. This paradigm shift became widely recognized as an appropriate standard of care for patients with metastatic epidural spinal cord compression (MESCC) after the randomized study by Patchell et al.⁷ They demonstrated superior results in terms of ambulation and pain control with surgery followed by fractionated radiation when compared with radiation alone in patients with single-site MESCC with nonradiosensitive pathologies. However, in the postoperative setting, it is well known that radiation treatment can impede the wound healing process and may cause elevated rates of wound complications.8, 9, 10, 11

Similar to the changes seen in the surgical management of patients with spine tumors, there are novel radiation targeting and delivery methods that offer significant advantages.3, 12, 13, 14, 15 One such method is stereotactic spine radiosurgery (SRS) that delivers a highly conformal, high dose of ionizing radiation with a steep dose fall-off in 1–5 sessions for the treatment of spine tumors. This modality has been shown in several studies to be safe and effective, and many patients are now experiencing greater and more rapid relief of pain with SRS, as well as higher local control rates when compared with conventional radiation treatments.12, 13, 14, 16 Another advantage of SRS over conventional radiation in the postoperative setting is the potential sparing of regions at risk, such as the fusion or instrumentation site and the operative wound.¹⁷

In 2006, Rock et al.¹⁸ described their series of 18 patients with metastatic spine tumors treated with surgery followed by SRS. At 7 months' mean follow-up, 92% of these patients remained neurologically stable or improved. This series, however, did not formally evaluate the radiographic impact of treatment with SRS. Laufer et al.¹⁹ reported the results of 186 patients operated and treated with SRS. The local control rate reported was 83.6% at 1 year post SRS on the basis of a blinded neuroradiologist evaluation using computed tomography (CT) and magnetic resonance imaging (MRI) scans for tumor measurement and incorporating a 6-point epidural spinal cord compression (ESCC) scale²⁰ to determine the response to treatment or recurrence. The radiosurgery literature lacks reports of formal radiologic evaluation of tumor response and determining the most reliable response criteria for the evaluation of these lesions.

The World Health Organization (WHO) criteria to evaluate local control, recurrence, and progression in solid tumor, first published by Miller et al.,²¹ measures the largest tumor diameter multiplied by its largest perpendicular dimension. A 50% tumor size reduction was defined as partial response (PR), and a 25% increase was defined as progressive disease (PD). Otherwise, the disease is considered stable disease (SD). In 2000 the Response Evaluation Criteria In Solid Tumors (RECIST) criteria were introduced and tumor response was evaluated, using the largest tumor measurable in a unidimensional manner.22, 23 A 30% tumor diameter reduction was defined as partial response (PR), and a 20% increase was defined as PD. Otherwise, the disease is SD. In recent years, the improved imaging technology, combined with advanced computational abilities, allow for volumetric measurements of tumor load.23, 24 These measurement criteria, however, have never been applied or directly compared to evaluate and quantify the effect of treatment in spine metastases.

This paper addresses the benefits of SRS following spine surgery in terms of wound complications and radiographic local control and evaluates optimal local control assessment methods.

Section snippets

Methods and Materials

A retrospective review of patient records prospectively collected through the Cleveland Clinic Spine Tumor Board database was performed. After the study was approved by the Cleveland Clinic Institutional Review Board, the authors reviewed the records of 925 spine tumor patients added to the database from 2006–2009. These patients had undergone various treatment regimens including surgery, chemotherapy, radiotherapy, radiosurgery, or various combinations. Patients included in this series had

Results

Twenty-two patients with spine tumors were treated with open surgery followed by SRS within 2 months at our center during the study period. Five patients were operated by a combined ventral and dorsal approach, while the rest were operated either via a ventral (13 patients) or dorsal (4 patients) approach only according to the clinical indications and treating surgeon preference. Six patients had a decompression-only procedure, 1 had uninstrumented fusion, and 15 had undergone decompression

Wound Complication Results

In terms of perioperative infections, of the 22 patients, 1 patient had a postoperative urinary tract infection and 2 patients had postoperative superficial wound infections evident on postoperative days 4 and 7 (pre-SRS, no prior radiotherapy) that were treated with antibiotics only.

Overall, 57 imaging studies (range 2–9 for each treated) were directly measured by a single neuroradiologist (TE) who was blinded to the patient's clinical course or outcome. The preoperative median tumor's

Clinical Response to Treatment

Fifteen patients (88.3%) had a clinical response to treatment, and 2 patients (11.7%) had a clinical progression. The first was an 80-year-old gentleman diagnosed with metastatic lung cancer, 5 months following L1 vertebrectomy, fusion, and SRS (14 Gy). He complained of increasing pain, and the MRI demonstrated evidence of tumor growth. The second patient was a 62-year-old gentleman with a T12 renal cell carcinoma who underwent dorsal decompression and fusion, followed by SRS (14 Gy). Eighteen

Radiologic Response to Treatment

Radiographic evidence of recurrence was noted in 2 patients according to the RECIST criteria and in 4 patients according to the WHO criteria. Both clinical recurring patients were scored as PD according to the WHO criteria. One was scored as PD according to the RECIST, and the other was scored as SD as the unidimensional change was only 18.9% rather than 20%. The volumetric percent change in these patients was a 12% and 26% increase, respectively. One patient demonstrated a PR according to the

Discussion

Patchell et al.⁷ demonstrated that patients with spine metastases who were treated with surgery followed by conventional radiation had a higher probability of maintaining or regaining their ability to walk and required less corticosteroids and analgesics when compared with the radiation monotherapy group. This key paper changed the treatment paradigm for epidural metastases from conservative radiation to surgery and radiation. Unfortunately, radiation has also been shown to reduce the ability

Conclusion

Spine surgery with adjuvant SRS appears to be beneficial in reducing wound dose and potentially wound complications. Further, similar to other studies, we determined that SRS in the postoperative setting achieves high local control rates. However, until now no data existed regarding the best way to quantitatively evaluate response post stereotactic radiosurgery. This is the first study to evaluate this issue and recommends a standardized assessment strategy. We formally compared 3 approaches to

Acknowledgment

We gratefully acknowledge Ms. Christine Moore for editorial support.

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Cited by (21)

Oncologic and Functional Outcomes After Stereotactic Body Radiation Therapy for High-Grade Malignant Spinal Cord Compression
2024, Advances in Radiation Oncology
Although surgical decompression is the gold standard for metastatic epidural spinal cord compression (MESCC) from solid tumors, not all patients are candidates or undergo successful surgical Bilsky downgrading. We report oncologic and functional outcomes for patients treated with stereotactic body radiation therapy (SBRT) to high-grade MESCC.
Patients with Bilsky grade 2 to 3 MESCC from solid tumor metastases treated with SBRT at a single institution from 2009 to 2020 were retrospectively reviewed. Patients who received upfront surgery before SBRT were included only if postsurgical Bilsky grade remained ≥2. Neurologic examinations, magnetic resonance imaging, pain assessments, and analgesic usage were assessed every 3 to 4 months post-SBRT. Cumulative incidence of local recurrence was calculated with death as a competing risk, and overall survival was estimated by Kaplan-Meier.
One hundred forty-three patients were included. The cumulative incidence of local recurrence was 5.1%, 7.5%, and 14.1% at 6, 12, and 24 months, respectively. At first post-SBRT imaging, 16.2% of patients with initial Bilsky grade 2 improved to grade 1, and 53.8% of patients were stable. Five of 13 patients (38.4%) with initial Bilsky grade 3 improved to grade 1 to 2. Pain response at 3 and 6 months post-SBRT was complete in 45.4% and 55.7%, partial in 26.9% and 13.1%, stable in 24.1% and 27.9%, and worse in 3.7% and 3.3% of patients, respectively. At 3 and 6 months after SBRT, 17.8% and 25.0% of patients had improved ambulatory status and 79.7% and 72.4% had stable status.
We report the largest series to date of patients with high-grade MESCC treated with SBRT. The excellent local control and functional outcomes suggest SBRT is a reasonable approach in inoperable patients or cases unable to be successfully surgically downgraded.
Stereotactic Radiosurgery for Postoperative Spine Malignancy: A Systematic Review and International Stereotactic Radiosurgery Society Practice Guidelines
2022, Practical Radiation Oncology
Citation Excerpt :
A P value threshold of .05 was used for statistical significance. A total of 461 patients and 499 segments treated across 12 studies were included in this analysis.14-25 Surgical techniques were heterogenous, and a description of technique used per study is outlined in Table 2.
To determine safety and efficacy of postoperative spine stereotactic body radiation therapy (SBRT) in the published literature, and to present practice recommendations on behalf of the International Stereotactic Radiosurgery Society.
A systematic review of the literature was performed, specific to postoperative spine SBRT, using PubMed and Embase databases. A meta-analysis for 1-year local control (LC), overall survival (OS), and vertebral compression fracture probability was conducted.
The literature search revealed 251 potentially relevant articles after duplicates were removed. Of these 56 were reviewed in-depth for eligibility and 12 met all the inclusion criteria for analysis. 7 studies were retrospective, 2 prospective observational and 3 were prospective phase 1 and 2 clinical trials. Outcomes for a total of 461 patients and 499 spinal segments were reported. Ten studies used a magnetic resonance imaging (MRI) scan fused to computed tomography (CT) simulation for treatment planning, and 2 investigations reported on all patients receiving a CT-myelogram at the time of planning. Meta-analysis for 1 year LC and OS was 88.9% and 57%, respectively. The crude reported vertebral compression fracture rate was 5.6%. One case of myelopathy was described in a patient with a previously irradiated spinal segment. One patient developed an esophageal fistula requiring surgical repair.
Postoperative spine SBRT delivers a high 1-year LC with acceptably low toxicity. Patients who may benefit from this include those with oligometastatic disease, radioresistant histology, paraspinal masses, or those with a history of prior irradiation to the affected spinal segment. The International Stereotactic Radiosurgery Society recommends a minimum interval of 8 to 14 days after invasive surgery before simulation for SBRT, with initiation of radiation therapy within 4 weeks of surgery. An MRI fused to the planning CT, or the use of a CT-myelogram, are necessary for target and organ-at-risk delineation. A planning organ-at-risk volume (PRV) of 1.5 to 2 mm for the spinal cord is advised.
Drivers of Readmission and Reoperation After Surgery for Vertebral Column Metastases
2021, World Neurosurgery
To determine those clinical, demographic, and operative factors that predict 30-day unplanned reoperation and readmission within a population of adults who underwent spinal metastasis surgery at a comprehensive cancer center.
Adults who underwent spinal metastasis surgery at a comprehensive cancer center were analyzed. Data included baseline laboratory values, cancer history, demographics, operative characteristics and medical comorbidities. Medical comorbidities were quantified using the modified Charlson Comorbidity Index (CCI). Values associated with the outcomes of interest were then subjected to multivariable logistic regression to identify independent predictors of readmission and reoperation.
A total of 345 cases were identified. Mean age was 59.4 ± 11.7 years, 56% were male, and the racial makeup was 64% white, 29% black, and 7.3% other. Forty-two patients (12.2%) had unplanned readmissions, most commonly for wound infection with dehiscence (14.2%), venous thromboembolism (14.2%), and bowel obstruction/complication (11.9%). Thirteen patients required reoperation (4%), most commonly for wound infection with dehiscence (39%) or local recurrence (23%). Multivariable analysis showed that the modified CCI (odds ratio [OR], 1.25; 95% confidence interval [CI] 1.03–1.52; P = 0.03) was an independent predictor of 30-day readmission. Independent predictors of 30-day unplanned reoperation were: black (vs. white) race (OR, 0.08; 95% CI, 0.01–0.41; P < 0.01), length of stay (OR, 1.05 per day; 95% CI, 1.00–1.09; P = 0.04), and CCI (OR, 1.72 per point; 95% CI, 1.29–2.28; P < 0.01).
Increasing medical comorbidities is independently predictive of both 30-day unplanned readmission and reoperation after spinal metastasis surgery. Unplanned reoperation is also positively predicted by a longer index admission. Neither tumor pathology nor age predicted outcome, suggesting that poor wound-healing factors and increased surgical morbidity may best predict these adverse outcomes.
Local Tumor Control for Metastatic Epidural Spinal Cord Compression Following Separation Surgery with Adjuvant CyberKnife Stereotactic Radiotherapy or Image-Guided Intensity-Modulated Radiotherapy
2020, World Neurosurgery
We sought to compare local tumor control after conventionally fractionated image-guided intensity-modulated radiotherapy (IMRT) versus adjuvant CyberKnife stereotactic body radiotherapy (SBRT) in patients who underwent separation surgery for metastatic epidural spinal cord compression (MESCC).
We retrospectively reviewed patients with MESCC who were treated at our hospital. The Kaplan-Meier method was used to estimate local progression and overall survival.
Fifty-six patients with MESCC underwent separation surgery between 2013 and 2018, among whom 6 were lost to follow-up, 24 received conventionally fractionated image-guided IMRT, and 26 were treated with CyberKnife SBRT. The median follow-up was 16.5 months (range, 2.1–47.5 months). Eleven patients experienced local failure including 9 and 2 from the IMRT and SBRT groups, respectively. The local progression-free survival rates were significantly higher in the SBRT group than IMRT group at 6 months (95.5% vs. 82.0%), 1 year (90.9% vs. 71.8%), and 2 years (90.9% vs. 57.6%) (P = 0.035). Multivariate Cox proportional hazards regression analysis identified radiotherapy method (P = 0.034) and receipt of preoperative radiotherapy (P = 0.047) as significant predictors of local control, while visceral metastasis (P = 0.048) and high-malignancy primary tumor type (P = 0.002) were negative predictors of overall survival. Moreover, postoperative SBRT was noninferior to IMRT in terms of pain control, adverse effects, and performance in treating irradiated spinal metastases.
Hybrid surgery-radiosurgery therapy is a safe and effective treatment option for patients with MESCC. SBRT provided higher local control rates compared with IMRT. Thus postoperative SBRT should be considered for patients expected to have relatively long survival.
A Phase 2 Study of Post-Operative Stereotactic Body Radiation Therapy (SBRT) for Solid Tumor Spine Metastases
2020, International Journal of Radiation Oncology Biology Physics
Citation Excerpt :
Given the increasing long-term cancer survivorship and the resultant need for more durable local control, stereotactic body RT (SBRT) is being used as an alternative to low-dose conventionally fractionated RT, allowing the delivery of a higher biologically equivalent dose in fewer fractions. Numerous retrospective and single arm series suggest excellent outcomes after SBRT to both intact and postoperative lesions, with local control ranging from 70% to 100% across tumor histologies.3-21 In addition, a single prospective study comparing 24 Gy in a single fraction using SBRT to 3-dimensional conformal radiation to a total dose of 30 Gy in 10 fractions found significantly lower pain scores after SBRT at 6 months after completion of therapy. 22
In patients with spinal instability, cord compression, or neurologic deficits, the standard of care is surgery followed by radiation therapy (RT). Recurrence rates after conventional RT remain high. The purpose of this study is to prospectively examine the efficacy of postoperative stereotactic body RT (SBRT) in patients who have undergone surgical intervention for spine metastases. We hypothesize that postoperative SBRT to the spine would be associated with higher local control than historical rates after conventional RT.
Thirty-five adult patients with a Karnofsky Performance Status score ≥40 and spine metastases from solid tumors with no prior overlapping RT and target volumes ≤3 consecutive vertebral levels were enrolled. Thirty-three patients were treated. Two patients underwent treatment to 2 target volumes for a total of 35 target volumes. All patients received SBRT 30 Gy in 5 fractions. Patients were followed with neurological examinations and computed tomography and/or magnetic resonance imaging every 3 months. Neurologic function was assessed at the same time points using the American Spinal Injury Association (ASIA) impairment score. Pain was rated according to the 10-point visual analogue scale and MD Anderson Cancer Center brief pain index. Toxicity was recorded according to National Cancer Institute Common Toxicity Criteria for Adverse Events Version 4. The primary objective was the rate of radiographic local recurrence at 12 months after completion of SBRT.
Patient characteristics were as follows: 34.3% had radioresistant primaries; 71.4% were ASIA E and the remainder ASIA D; and the median baseline Karnofsky Performance Status score was 70 (range, 50-100). Radiographic and symptomatic local control at 1 year were 90% (95% confidence interval, 76%-98%). The median time to recurrence in these 3 patients was 3.5 months (range, 3.4-5.8 months), all had radiosensitive tumors, and all recurrences were epidural. No patients experienced wound dehiscence, hardware failure, or spinal cord myelopathy. The median time to return to systemic therapy was 0.5 months (range, 0-9.4 months).
This prospective study of postoperative spine SBRT demonstrates excellent local control with low toxicity. These data suggest superior rates of local control compared with conventional RT; however, a formal comparative study is warranted.
Consensus Contouring Guidelines for Postoperative Stereotactic Body Radiation Therapy for Metastatic Solid Tumor Malignancies to the Spine
2017, International Journal of Radiation Oncology Biology Physics
To develop consensus contouring guidelines for postoperative stereotactic body radiation therapy (SBRT) for spinal metastases.
Ten spine SBRT specialists representing 10 international centers independently contoured the clinical target volume (CTV), planning target volume (PTV), spinal cord, and spinal cord planning organ at risk volume (PRV) for 10 representative clinical scenarios in postoperative spine SBRT for metastatic solid tumor malignancies. Contours were imported into the Computational Environment for Radiotherapy Research. Agreement between physicians was calculated with an expectation minimization algorithm using simultaneous truth and performance level estimation with κ statistics. Target volume definition guidelines were established by finding optimized confidence level consensus contours using histogram agreement analyses.
Nine expert radiation oncologists and 1 neurosurgeon completed contours for all 10 cases. The mean sensitivity and specificity were 0.79 (range, 0.71-0.89) and 0.94 (range, 0.90-0.99) for the CTV and 0.79 (range, 0.70-0.95) and 0.92 (range, 0.87-0.99) for the PTV), respectively. Mean κ agreement, which demonstrates the probability that contours agree by chance alone, was 0.58 (range, 0.43-0.70) for CTV and 0.58 (range, 0.37-0.76) for PTV (P<.001 for all cases). Optimized consensus contours were established for all patients with 80% confidence interval. Recommendations for CTV include treatment of the entire preoperative extent of bony and epidural disease, plus immediately adjacent bony anatomic compartments at risk of microscopic disease extension. In particular, a “donut-shaped” CTV was consistently applied in cases of preoperative circumferential epidural extension, regardless of extent of residual epidural extension. Otherwise more conformal anatomic-based CTVs were determined and described. Spinal instrumentation was consistently excluded from the CTV.
We provide consensus contouring guidelines for common scenarios in postoperative SBRT for spinal metastases. These consensus guidelines are subject to clinical validation.

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: Conflict of interest statement: All co-authors report no conflicts of interest or disclosures, with the exception of Samuel Chao: honorarium from Varian. There were no sources of support for this paper.

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Original ArticleQuantitative Evaluation of Local Control and Wound Healing Following Surgery and Stereotactic Spine Radiosurgery for Spine Tumors

Objective

Methods and Materials

Results

Conclusion

Introduction

Section snippets

Methods and Materials

Results

Wound Complication Results

Clinical Response to Treatment

Radiologic Response to Treatment

Discussion

Conclusion

Acknowledgment

Lancet Neurol

Eur J Cancer

Lancet

Radiother Oncol

World Neurosurg

Eur J Cancer

Int J Radiat Oncol Biol Phys

J Surg Res

Clin Plast Surg

Clin Dermatol

J Clin Epidemiol

Interventions for the treatment of metastatic extradural spinal cord compression in adults

Cochrane Database Syst Rev

Clinical outcome and survival after palliative surgery for spinal metastases: palliative surgery in spinal metastases

Cancer

Laminectomy for metastatic epidural spinal cord tumors. Posterior stabilization, radiotherapy, and preoperative assessment

Clin Orthop Relat Res

Treatment of spinal epidural metastases. Randomized prospective comparison of laminectomy and radiotherapy

J Neurosurg

Surgical site infection in spinal metástasis: risk factors and countermeasures

Spine (Phila Pa 1976)

Timing of surgery and radiotherapy in the management of metastatic spine disease: a systematic review

Int J Oncol

Complications of postoperative and preoperative radiation therapy in head and neck cancers. A comparative study

Arch Otolaryngol

Stereotactic spine radiosurgery (SRS) for pain and tumor control in patients with spinal metastases from renal cell carcinoma: a prospective study

Int J Radiat Oncol Biol Phys

Intensity-modulated stereotactic radiotherapy of paraspinal tumors: a preliminary report

Neurosurgery

Original Article
Quantitative Evaluation of Local Control and Wound Healing Following Surgery and Stereotactic Spine Radiosurgery for Spine Tumors