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Journal of bone oncology · 2025

Surgical management of spinal metastases: A cross-continental study in the United States and the Netherlands.

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Amelink JJGJ, van Munster BT, Bindels BJJ, Pierik RJB, van Tiel J, Groot OQ, Kasperts N, Tobert DG, Verlaan JJ

Аннотация

BackgroundThere is currently no consensus on the optimal surgical treatment for patients with spinal metastases. Investigating regional variations in surgical management could provide valuable insights to optimize care and refine surgical practices globally.ObjectiveTo investigate differences in patient populations, surgical management, and perioperative outcomes among patients who underwent surgery for spinal metastases in either Boston (United States) or Utrecht (Netherlands).Methods727 patients surgically treated for spinal metastases in Boston (n=539) and Utrecht (n=188) between 2018-2022 were included. Data on patient characteristics, surgical management, perioperative outcomes, and survival were collected. The Mann-Whitney U test was used for continuous data, and Fisher's exact test for categorical data.ResultsIn Boston, a higher percentage of patients had three or more spinal metastases (68% vs 59%; p=0.006) and brain metastases (16% vs 4.3%; pvs 54%; pvs 29 days [IQR:23-39]; p0.05).ConclusionsDifferences in patient populations and surgical management exist between tertiary hospitals on separate continents. Further research is needed to determine the optimal extent and timing of surgery to improve quality of life for patients with spinal metastases.

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https://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Introduction

Due to the spine's highly vascular nature, it is the most common site for bone metastases, affecting approximately 20 % of patients diagnosed with cancer [1] , [2] . Timely diagnosis and treatment of symptomatic spinal metastases are of utmost importance because of their potential debilitating consequences, such as severe pain, neurological deficit, and autonomic dysfunction [3] . For some patients with symptomatic spinal metastases, surgical intervention may be warranted, aiming to restore spine stability, alleviate epidural compression, and/or perform cytoreduction for local tumor control, which can also be achieved with radiotherapy as in separation surgery [4] , [5] , [6] .

Due to a lack of consensus regarding the ideal surgical management and optimal indication, a wide variety of procedures may be performed for patients with spinal metastases, ranging from minimally invasive percutaneous stabilization to en bloc vertebrectomies/corpectomies [7] , [8] . Such variations in surgical management may be attributed to cultural differences, local policies, and diverging philosophies between countries’ healthcare systems regarding best practices, with some prioritizing quality-of-life over quantity-of-life, and vice versa. Additionally, differences in medical characteristics of patient populations (e.g. comorbidities, extent of metastatic disease, amount of prior treatment) may also offer an explanation. Gaining better insight into regional variations in surgical management is crucial. Such understanding allows for the improvement of care worldwide, as surgical research from institutions in the United States and other countries (e.g. the Netherlands, Germany, Switzerland, Japan etc.) is frequently used to inform patient care globally [9] , [10] , [11] , [12] , [13] .

Therefore, the purpose of the present study is to investigate whether differences exist in patient populations, surgical management, and perioperative outcomes among a large cohort of patients who underwent surgery for spinal metastases at major cancer centers in either Boston (United States) or Utrecht (Netherlands).

Materials and methods

Study design and setting

This retrospective cross-continental cohort study evaluated data from two affiliated academic hospitals in Boston, the United States and one academic hospital in Utrecht, the Netherlands. The institutional review board at Mass General Brigham in Boston (registration: 2017P00838) approved a waiver of informed consent for this cohort study. The institutional review board at University Medical Center Utrecht (UMCU), under registration VOBU 23U-0528, granted a waiver of additional informed consent to use data from three existing registries of patients who had previously provided informed consent for the prospective collection of baseline demographics, treatment characteristics, and clinical follow-up data [14] . The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist for cohort studies was used to warrant adequate reporting (Appendix A) [15] .

Patient inclusion

Potentially eligible patients for the Boston cohort were identified using the International Classification of Diseases, Tenth Revision (ICD-10) diagnosis of secondary malignant neoplasm of bone and bone marrow (C79.5), diagnosis of multiple myeloma (C90.0), along with all CPT codes related to surgical procedures on the spine and vertebral column. For the Utrecht cohort, potentially eligible patients were identified from three registries: the Global Spine Tumour Study Group (GSTSG), the Metastatic Tumor Research and Outcomes Network (MTRON), and the PRospective Evaluation of interventional StudiEs on BoNe meTastases (PRESENT) cohort, all of which include patients undergoing surgery and/or radiotherapy for metastatic bone disease at the UMCU [16] .

We included patients aged 18 years or older who underwent surgical treatment for spinal metastases (including the entire spinal column from the occipital bone to the sacrum) between January 1 st , 2018, and December 31 st , 2022, at two affiliated academic hospitals in Boston: Massachusetts General Hospital (MGH) and Brigham and Women’s Hospital (BWH); or in Utrecht at the University Medical Center Utrecht (UMCU). Patients with spinal localizations of hematological tumors, specifically spinal lymphoma, plasmacytoma and multiple myeloma, were also included due to similarities in surgical treatment [17] , [18] . We excluded patients who were treated solely by kyphoplasty or vertebroplasty, radiosurgery, or undergoing revision procedures. The inclusion and exclusion criteria were applied uniformly across both cohorts. Only the first surgical procedure was considered for patients who underwent multiple procedures to maintain statistical independence [19] . The choice of treatment was determined through mutual agreement between both the surgeon and the patient. Fig. 1 illustrates the patient selection process. Fig. 1 Flowchart of inclusion and exclusion of patients in the study. US = United States; RPDR = Research Patient Data Registry; GSTSG = Global Spine Tumour Study Group; MTRON = Metastatic Tumor Research and Outcomes Network; PRESENT = PRospective Evaluation of interventional StudiEs on BoNe meTastases; N = number; BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group; ASA = American Society of Anaesthesiologists; ASIA = American Spinal Injury Association; SINS = Spinal Instability Neoplastic Score; ESCC = Epidural Spinal Cord Compression.

Fig. 1 Flowchart of inclusion and exclusion of patients in the study. US = United States; RPDR = Research Patient Data Registry; GSTSG = Global Spine Tumour Study Group; MTRON = M…
Fig. 1 Flowchart of inclusion and exclusion of patients in the study. US = United States; RPDR = Research Patient Data Registry; GSTSG = Global Spine Tumour Study Group; MTRON = Metastatic Tumor Research and Outcomes Network; PRESENT = PRospective Evaluation of interventional StudiEs on BoNe meTastases; N = number; BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group; ASA = American Society of Anaesthesiologists; ASIA = American Spinal Injury Association; SINS = Spinal Instability Neoplastic Score; ESCC = Epidural Spinal Cord Compression.

Data collection

For the Boston cohort, electronic medical records were manually reviewed to retrospectively retrieve demographic, clinical, oncologic, and operative data. In the Utrecht cohort, data were partially obtained from the three prospective registries and further supplemented for various variables through manual retrospective review of electronic medical records. The same definitions for all variables were applied consistently across both independently collected cohorts.

Demographic, clinical, and oncologic variables

Demographic variables included age, sex, body mass index (BMI), the modified Charlson comorbidity index, and additional comorbidities. Body mass index (BMI) was categorized as underweight (BMI<18.5 kg/m 2 ), normal weight (BMI 18.5 to 30 kg/m 2 ), and obese (BMI>30 kg/m 2 ). The modified Charlson comorbidity index was used to determine comorbidity status [20] . We dichotomized the comorbidity status into any additional comorbidity (in addition to the metastases) or none [21] . Clinical variables included preoperative Eastern Cooperative Oncology Group (ECOG) performance status, the American Society of Anaesthesiologists (ASA) score, preoperative neurologic status using the American Spinal Injury Association (ASIA) impairment scale, Spinal Instability Neoplastic Score (SINS), and Epidural Spinal Cord Compression (ESCC) score. The ECOG performance status was dichotomized into a relatively functional score (0, 1, or 2) or a poor score (3 to 4) [22] . The ASIA impairment scale was used to determine whether a patient had any neurological deficits (score of A, B, C, or D) or none (score of E) [23] . Patients with prior but no current deficits before surgery were classified as ASIA E. The SINS was categorized into stable (0 to 6), potentially unstable (7 to 12), and unstable (13 to 18) [24] . The ESCC score was dichotomized into low-grade ESCC (0 and 1) and high-grade ESCC (2 and 3) [25] . Oncologic variables included primary tumor type, the number of spinal metastases at time of surgery (categorized as one, two, or three or more), region of spinal metastases, the presence of visceral metastases (liver and/or lung); brain metastases or additional bone metastases (outside of the spine), previous systemic therapy, and prior local radiotherapy. Previous systemic therapy was defined as any nonsurgical and non-radiotherapeutic adjuvant treatment (including chemotherapy, immunotherapy, hormone therapy, and metabolic therapy) administered before the index surgery, regardless of dose and response. Prior local radiotherapy was defined as any radiation therapy targeting the operated spinal lesion administered prior to the index surgery, regardless of dose and response.

Surgical management and outcomes

Surgical management aspects included type of surgical procedure, surgical approach, number of spine levels included in the surgery (categorized as one, two, or three or more levels), number of instrumented spine levels (categorized as no, one to three, four to six, or seven or more levels), administration of postoperative local radiotherapy (defined as any form of radiotherapy administered to the spine levels included in the surgery within 3 months after surgery), and the time interval between surgery and start of postoperative local radiotherapy (days). Outcomes included estimated blood loss (milliliters), operating time (minutes), intraoperative complications (including dural tear, nerve injury, and intraoperative death), duration of hospitalization (days), postoperative neurological outcome, systemic postoperative complications within 30 days after surgery, reoperation at surgical site, and 90-day and 1-year survival. Type of surgical procedure was categorized in the following four categories: (1) vertebrectomy/corpectomy with stabilization, (2) open stabilization with or without decompression, (3) percutaneous stabilization with or without minimally invasive decompression, and (4) decompression only. These categories are mutually exclusive to ensure that each patient belonged to no more than one category. Surgical approach was categorized as (1) anterior (ventral), (2) posterior (dorsal), or (3) combined (both anterior and posterior). Estimated blood loss was based on surgeon and anesthesia reports. The duration of hospitalization was defined as the overall number of days patients remained hospitalized during the period when surgery was performed. Postoperative neurological outcome was quantified using the American Spinal Injury Association (ASIA) impairment scale and categorized as either favorable (improved neurological deficit or fully intact neurological status) or unfavorable (unchanged neurological deficit or neurological decline) [26] . Systemic postoperative complications within 30 days included pneumonia, pulmonary embolism, sepsis, myocardial infarction, wound infection, and hardware failure [27] . Reoperation at surgical site was defined as any successive surgical procedure performed during follow-up, without a specific time constraint being recorded. Survival was defined as the time from the surgical procedure until death from any cause, with the last date of follow-up on December 31 st , 2023 to ensure at least 1-year follow-up. The percentage of patients lost to follow-up was 6% (33/539) in Boston and 5% (9/188) in Utrecht.

Statistical analysis

Categorical variables were described as frequencies with percentages (%), and continuous variables as medians with interquartile ranges (IQR) as histograms suggested non-normal distributions. The Fisher's exact test was used for categorical variables, and the Mann–Whitney U test was used for continuous variables, as all continuous variables followed a non-normal distribution. Kaplan-Meier plots illustrated survival curves of both groups. Missing data were handled by complete-case analysis. Two tailed p-values of < 0.05 were considered statistically significant. Statistical analyses were performed using RStudio version 4.3.1 (2023–06-16 UCRT) and Mendeley Reference Manager (2.105.0) was used as reference software.

Results

Patient populations

In total, 727 patients were included; 539 (74%) patients in Boston and 188 (26%) in Utrecht. In the Boston cohort, a higher percentage of patients had obesity (25% vs 16%; p=0.023) and an ASA score of 3 (83% vs 47%; p<0.001). In the Utrecht cohort, more patients had a preoperative neurological deficit according to the ASIA impairment scale (47% vs 35%; p=0.005). The presence of three or more spinal metastases at the time of surgery was higher in Boston (68% vs 59%; p=0.006), with the number of patients with brain metastases also being higher within the Boston cohort (16% vs 4.3%; p<0.001). Additionally, more patients received preoperative systemic therapy in Boston than in Utrecht (60% vs 44%; p<0.001; Table 1 ). In both cohorts, the most common primary tumor type was lung cancer, and the second most common primary tumor was breast cancer. Within the Boston cohort, there were more patients with a primary tumor type of sarcoma (4.6% vs 0.5%; p=0.061) and melanoma (3.5% vs 1.6%; p=0.999), and fewer patients with colorectal tumors (2.8% vs 6.4%; p=0.447); however, no differences were found in primary tumor types between both cohorts (all p>0.05; Fig. 2 ; Appendix B). Table 1 Comparison of demographic, clinical, and oncologic characteristics of patients who underwent surgery for spinal metastases in Boston (n=539) or Utrecht (n=188). Characteristics N Boston ( n =539) Utrecht ( n =188) P-value Demographic Age in years 727 65 (57, 71) 65 (57, 72) 0,509 Female sex 727 239 (44) 81 (43) 0.798 BMI (kg/m 2 ) 723 † 0.023 >30 134 (25) 30 (16) 18.5–30 384 (71) 150 (82) <18.5 21 (3.9) 4 (2.2) Modified Charlson comorbidity index 727 8 (7, 10) 9 (8, 9) 0.552 Additional comorbidities § 727 249 (46) 77 (41) 0.233 Clinical ECOG performance status 664 † >0.999 Score 0 to 2 (≤50% of waking hours bed or chair bound) 403 (84) 155 (84) Score 3 to 4 (>50% of waking hours bed or chair bound) 77 (16) 29 (16) ASA score 719 † <0.001 ASA-1 1 (0.2) 4 (2.2) ASA-2 43 (8.0) 77 (43) ASA-3 447 (83) 84 (47) ASA-4 48 (8.9) 15 (8.3) ASIA impairment scale (preoperative) 712 † 0.005 No neurological deficit (E) 343 (65) 100 (53) Neurological deficit (A, B, C, or D) 182 (35) 87 (47) SINS category 677 † 0.350 Stable 49 (9.9) 16 (8.8) Potentially unstable 349 (70) 120 (66) Unstable 98 (20) 45 (25) ESCC score 677 † 0.537 Low-grade ESCC (0 and 1) 97 (19) 35 (21) High-grade ESCC (2 and 3) 414 (81) 131 (79) Oncologic Number of spinal metastases at time of surgery 727 0.006 1 level 110 (20) 37 (20) 2 levels 63 (12) 40 (21) ≥3 levels 366 (68) 111 (59) Region of spinal metastases 727 0.077 Cervical 34 (6.3) 4 (2.1) Thoracic 168 (31) 55 (29) Lumbar 65 (12) 20 (11) Combined 272 (50) 109 (58) Visceral metastases at time of surgery Lung and/or liver 727 242 (45) 88 (47) 0.671 Brain 727 87 (16) 8 (4.3) <0.001 Additional bone metastases at time of surgery 727 354 (66) 113 (60) 0.185 Previous systemic therapy 727 326 (60) 83 (44) <0.001 Prior local radiotherapy to spine levels undergoing surgery 727 137 (25) 37 (20) 0.136 Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05. BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group performance status; ASA = American Society of Anesthesiologists physical status classification system; ASIA = American Spinal Injury Association impairment scale; SINS = Spinal Instability Neoplastic Score category; ESCC; Epidural Spinal Cord Compression scale; N = number. † Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: BMI, 539 (100%) and 184 (98%); ECOG performance status, 480 (89%) and 184 (98%); ASA score, 539 (100%) and 180 (96%); ASIA impairment scale (preoperative), 525 (97%) and 187 (99%); SINS category, 496 (92%) and 181 (96%); ESCC score, 511 (95%) and 166 (88%). § These values were based on any comorbidity (addition to the metastases) or none following the modified Charlson comorbidity index. Fig. 2 Distribution and comparison of primary tumor types in patients who underwent surgery for spinal metastases in Boston (n=539) and Utrecht (n=188). Fisher’s exact test for count data with Bonferroni correction for multiple testing. *The following cancer types were included in this category for respectively the Boston and Utrecht cohorts: urological cancer (n=15; 2.8%) and (n=5; 2.7%); hepatocellular carcinoma (n=14; 2.6%) and (n=0; 0%); head and neck cancer (n=12; 2.2%) and (n=1; 0.5%); pancreas cancer (n=10; 1.9%) and (n=1; 0.5%); gynaecological cancer (n=8; 1.5%) and (n=5; 2.7%); gallbladder cancer (n=8; 1.5%) and (n=1; 0.5%); malignant lymphoma (n=7; 1.3%) and (n=3; 1.6%); esophageal cancer (n=6; 1.1%) and (n=5; 2.7%); gastric cancer (n=3; 0.6%) and (n=1; 0.5%); squamous cell carcinoma (n=2; 0.4%) and (n=2; 1.1%); pheochromocytoma (n=1; 0.2%) and (n=1; 0.5%); oral cancer (n=1; 0.2%) and (n=0; 0%); pituitary tumor (n=1; 0.2%) and (n=0; 0%); paraganglioma (n=1; 0.2%) and (n=0; 0%); and malignant neoplasm of thymus (n=1; 0.2%) and (n=0; 0%).

Table 1
Comparison of demographic, clinical, and oncologic characteristics of patients who underwent surgery for spinal metastases in Boston (n=539) or Utrecht (n=188).
Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05. BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group performance status; ASA = American Society of Anesthesiologists physical status classification system; ASIA = American Spinal Injury Association impairment scale; SINS = Spinal Instability Neoplastic Score category; ESCC; Epidural Spinal Cord Compression scale; N = number.
† Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: BMI, 539 (100%) and 184 (98%); ECOG performance status, 480 (89%) and 184 (98%); ASA score, 539 (100%) and 180 (96%); ASIA impairment scale (preoperative), 525 (97%) and 187 (99%); SINS category, 496 (92%) and 181 (96%); ESCC score, 511 (95%) and 166 (88%).
§ These values were based on any comorbidity (addition to the metastases) or none following the modified Charlson comorbidity index.

CharacteristicsNBoston ( n =539)Utrecht ( n =188)P-value
Demographic
Age in years72765 (57, 71)65 (57, 72)0,509
Female sex727239 (44)81 (43)0.798
BMI (kg/m 2 )723 †0.023
>30134 (25)30 (16)
18.5–30384 (71)150 (82)
<18.521 (3.9)4 (2.2)
Modified Charlson comorbidity index7278 (7, 10)9 (8, 9)0.552
Additional comorbidities §727249 (46)77 (41)0.233
Clinical
ECOG performance status664 †>0.999
Score 0 to 2 (≤50% of waking hours bed or chair bound)403 (84)155 (84)
Score 3 to 4 (>50% of waking hours bed or chair bound)77 (16)29 (16)
ASA score719 †<0.001
ASA-11 (0.2)4 (2.2)
ASA-243 (8.0)77 (43)
ASA-3447 (83)84 (47)
ASA-448 (8.9)15 (8.3)
ASIA impairment scale (preoperative)712 †0.005
No neurological deficit (E)343 (65)100 (53)
Neurological deficit (A, B, C, or D)182 (35)87 (47)
SINS category677 †0.350
Stable49 (9.9)16 (8.8)
Potentially unstable349 (70)120 (66)
Unstable98 (20)45 (25)
ESCC score677 †0.537
Low-grade ESCC (0 and 1)97 (19)35 (21)
High-grade ESCC (2 and 3)414 (81)131 (79)
Oncologic
Number of spinal metastases at time of surgery7270.006
1 level110 (20)37 (20)
2 levels63 (12)40 (21)
≥3 levels366 (68)111 (59)
Region of spinal metastases7270.077
Cervical34 (6.3)4 (2.1)
Thoracic168 (31)55 (29)
Lumbar65 (12)20 (11)
Combined272 (50)109 (58)
Visceral metastases at time of surgery
Lung and/or liver727242 (45)88 (47)0.671
Brain72787 (16)8 (4.3)<0.001
Additional bone metastases at time of surgery727354 (66)113 (60)0.185
Previous systemic therapy727326 (60)83 (44)<0.001
Prior local radiotherapy to spine levels undergoing surgery727137 (25)37 (20)0.136
Fig. 2 Distribution and comparison of primary tumor types in patients who underwent surgery for spinal metastases in Boston (n=539) and Utrecht (n=188). Fisher’s exact test for co…
Fig. 2 Distribution and comparison of primary tumor types in patients who underwent surgery for spinal metastases in Boston (n=539) and Utrecht (n=188). Fisher’s exact test for count data with Bonferroni correction for multiple testing. *The following cancer types were included in this category for respectively the Boston and Utrecht cohorts: urological cancer (n=15; 2.8%) and (n=5; 2.7%); hepatocellular carcinoma (n=14; 2.6%) and (n=0; 0%); head and neck cancer (n=12; 2.2%) and (n=1; 0.5%); pancreas cancer (n=10; 1.9%) and (n=1; 0.5%); gynaecological cancer (n=8; 1.5%) and (n=5; 2.7%); gallbladder cancer (n=8; 1.5%) and (n=1; 0.5%); malignant lymphoma (n=7; 1.3%) and (n=3; 1.6%); esophageal cancer (n=6; 1.1%) and (n=5; 2.7%); gastric cancer (n=3; 0.6%) and (n=1; 0.5%); squamous cell carcinoma (n=2; 0.4%) and (n=2; 1.1%); pheochromocytoma (n=1; 0.2%) and (n=1; 0.5%); oral cancer (n=1; 0.2%) and (n=0; 0%); pituitary tumor (n=1; 0.2%) and (n=0; 0%); paraganglioma (n=1; 0.2%) and (n=0; 0%); and malignant neoplasm of thymus (n=1; 0.2%) and (n=0; 0%).

Surgical management

Vertebrectomy/corpectomy with stabilization was performed in 54% of patients in Boston, whereas none of the patients in Utrecht underwent this procedure (p<0.001). Open stabilization, with or without decompression, was performed in 41% of patients in Boston, compared with 54% of patients in Utrecht (p<0.001). Percutaneous stabilization, with or without minimally invasive decompression, was performed in 1.3% of patients in Boston, compared with 39% of patients in Utrecht (p<0.001). Decompression only was performed in 3.9% of patients in Boston, compared with 6.4% of patients in Utrecht (p<0.001). Additionally, surgeons in Boston used an anterior or combined anterior and posterior approach in 6.6% of cases, whereas surgeons in Utrecht used a posterior approach in all cases (p<0.001). Furthermore, surgeons in Boston operated on three or more spine levels more frequently than surgeons in Utrecht (97% vs 94%; p=0.004), and they also more frequently instrumented seven or more spine levels (27% vs 3.2%; p<0.001). Postoperative local radiotherapy was administered in 54% of patients in Boston and 70% of patients in Utrecht (p<0.001). Additionally, postoperative local radiotherapy was initiated a median of 12 days earlier in patients in Utrecht compared with patients in Boston (17 days [IQR 12–24] vs 29 days [IQR 23–39]; p<0.001; Table 2 ). Table 2 Comparison of surgical management between Boston (n=539) and Utrecht (n=188). Characteristics N Boston ( n =539) Utrecht ( n =188) P-value Type of surgical procedure 727 <0.001 Vertebrectomy/corpectomy with stabilization 289 (54) 0 (0) Open stabilization with or without decompression 222 (41) 102 (54) Percutaneous stabilization with or without minimally invasive decompression 7 (1.3) 74 (39) Decompression only 21 (3.9) 12 (6.4) Surgical approach 727 <0.001 Anterior (ventral) 25 (4.6) 0 (0) Posterior (dorsal) 503 (93) 188 (100) Combined (both posterior and anterior) 11 (2.0) 0 (0) Number of spine levels included in the surgery 727 0.004 1 level 0 (0) 4 (2.1) 2 levels 16 (3.0) 8 (4.3) ≥3 levels 523 (97) 176 (94) Number of instrumented spine levels 727 <0.001 No levels 21 (3.9) 12 (6.4) 1 to 3 levels 110 (20) 76 (40) 4 to 6 levels 262 (49) 94 (50) ≥7 levels 146 (27) 6 (3.2) Postoperative local radiotherapy 727 290 (54) 132 (70) <0.001 Interval from surgery to start postoperative local radiotherapy (days) 417 † 29 (23, 39) 17 (12, 24) <0.001 Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05. † Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: interval from surgery to start postoperative local radiotherapy (days), 287/290 (99%) and 130/132 (98%).

Table 2
Comparison of surgical management between Boston (n=539) and Utrecht (n=188).
Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05.
† Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: interval from surgery to start postoperative local radiotherapy (days), 287/290 (99%) and 130/132 (98%).

CharacteristicsNBoston ( n =539)Utrecht ( n =188)P-value
Type of surgical procedure727<0.001
Vertebrectomy/corpectomy with stabilization289 (54)0 (0)
Open stabilization with or without decompression222 (41)102 (54)
Percutaneous stabilization with or without minimally invasive decompression7 (1.3)74 (39)
Decompression only21 (3.9)12 (6.4)
Surgical approach727<0.001
Anterior (ventral)25 (4.6)0 (0)
Posterior (dorsal)503 (93)188 (100)
Combined (both posterior and anterior)11 (2.0)0 (0)
Number of spine levels included in the surgery7270.004
1 level0 (0)4 (2.1)
2 levels16 (3.0)8 (4.3)
≥3 levels523 (97)176 (94)
Number of instrumented spine levels727<0.001
No levels21 (3.9)12 (6.4)
1 to 3 levels110 (20)76 (40)
4 to 6 levels262 (49)94 (50)
≥7 levels146 (27)6 (3.2)
Postoperative local radiotherapy727290 (54)132 (70)<0.001
Interval from surgery to start postoperative local radiotherapy (days)417 †29 (23, 39)17 (12, 24)<0.001

Perioperative outcomes and survival

Patients in Boston compared with patients in Utrecht experienced approximately twice as much blood loss during surgery (500 ml [IQR 250–1000] vs 250 ml [IQR 150–500]; p<0.001) and had nearly twice the duration of surgery (240 min [IQR 178–305] vs 131 min [IQR 99–164]; p<0.001). The occurrence of intraoperative complications did not differ between both cohorts (5.8% vs 2.7%; p=0.117). The median total duration of hospitalization was two days longer for patients in Boston compared with those in Utrecht (8 days [IQR 5–12] vs 6 days [IQR 4–12]; p=0.017). Favorable postoperative neurological outcome (78% vs 76%; p=0.477), occurrence of 30-day systemic postoperative complications (15% vs 15%; p=0.906), and reoperations at surgical site (14% vs 14%; p>0.999) did not differ between both cohorts. The 90-day (79% vs 78%; p=0.792) and 1-year survival rates (49% vs 50%; p=0.882; Appendix C) also did not differ ( Table 3 ). Table 3 Comparison of perioperative outcomes and survival between Boston (n=539) and Utrecht (n=188). Outcomes N Boston ( n =539) Utrecht ( n =188) P-value Estimated blood loss (ml) 686 † 500 (250, 1,000) 250 (150, 500) <0.001 Operating time (min) 727 240 (178, 305) 131 (99, 164) <0.001 Intraoperative complications 727 31 (5.8) 5 (2.7) 0.117 Duration of hospitalization (days) 727 8 (5, 12) 6 (4, 12) 0.017 Postoperative neurological outcome 722 † 0.477 Favorable 418 (78) 142 (76) Unfavorable 116 (22) 46 (24) Systemic postoperative complications within 30 days after surgery 727 80 (15) 29 (15) 0.906 Reoperations 727 75 (14) 26 (14) >0.999 Survival 90-day 719 † 424 (79) 145 (78) 0.792 1-year 685 † 247 (49) 89 (50) 0.882 Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05. ml = milliliters; min = minutes. † Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: estimated blood loss (ml), 531 (99%) and 155 (82%); postoperative neurological outcome, 534 (99%) and 188 (100%); 90-day survival, 534 (99%) and 185 (98%); 1-year survival, 506 (94%) and 179 (95%).

Table 3
Comparison of perioperative outcomes and survival between Boston (n=539) and Utrecht (n=188).
Categorical values were provided as number of patients, with the percentage in parentheses (%) and continuous values as the median and the interquartile range (IQR). Fisher’s exact test and Wilcoxon rank sum test were used to compare both groups. Bold p-values indicate statistical significance of p<0.05. ml = milliliters; min = minutes.
† Patient data were respectively available for the Boston cohort and Utrecht cohort, as follows: estimated blood loss (ml), 531 (99%) and 155 (82%); postoperative neurological outcome, 534 (99%) and 188 (100%); 90-day survival, 534 (99%) and 185 (98%); 1-year survival, 506 (94%) and 179 (95%).

OutcomesNBoston ( n =539)Utrecht ( n =188)P-value
Estimated blood loss (ml)686 †500 (250, 1,000)250 (150, 500)<0.001
Operating time (min)727240 (178, 305)131 (99, 164)<0.001
Intraoperative complications72731 (5.8)5 (2.7)0.117
Duration of hospitalization (days)7278 (5, 12)6 (4, 12)0.017
Postoperative neurological outcome722 †0.477
Favorable418 (78)142 (76)
Unfavorable116 (22)46 (24)
Systemic postoperative complications within 30 days after surgery72780 (15)29 (15)0.906
Reoperations72775 (14)26 (14)>0.999
Survival
90-day719 †424 (79)145 (78)0.792
1-year685 †247 (49)89 (50)0.882

Discussion

Currently, there is no international consensus on the surgical management or standardized treatment planning for patients with symptomatic spinal metastases requiring surgical intervention. Knowledge of variations in surgical care may offer valuable insights to guide surgical decision-making and support research efforts toward improving patient care. In our cross-continental cohort study, we identified differences in patient populations and surgical management between major cancer centers in Boston and Utrecht. Patients in Boston generally presented with a more advanced stage of metastatic disease at the time of surgery compared with patients in Utrecht. Notably, surgeons in Utrecht favoured less invasive, posterior techniques, while surgeons in Boston performed more extensive surgeries, including procedures such as corpectomy/vertebrectomy. Additionally, patients in Utrecht experienced less intraoperative blood loss, shorter operating times, and shorter hospital stays compared with patients in Boston; however, no differences in postoperative neurological outcome, complications, reoperation rates or survival were observed.

Patient populations

Overall, the Boston and Utrecht cohorts were largely comparable in demographic characteristics, including age, sex, and the presence of comorbidities. Additionally, the distributions of ECOG performance status, SINS category, and ESCC score were similar between both cohorts. Patients in the Boston cohort generally had a more advanced stage of metastatic disease at the time of surgery, as evidenced by a higher number of spinal metastases and more instances of brain metastases. One potential explanation for this difference in the stage of metastatic disease could be attributed to Utrecht’s recent efforts, prior to the start of inclusion in 2018, to identify patients with symptomatic spinal metastases earlier to prevent delays in treatment [28] , [29] . Furthermore, the more advanced stage of metastatic disease in the Boston cohort may explain the higher rate of preoperative systemic therapy. Since a more advanced stage of disease is associated with a poorer prognosis, assessing the response to systemic therapy before considering surgery may have been preferred in certain cases in Boston [30] . However, differences in clinical protocols and treatment guidelines between the United States and the Netherlands, particularly regarding the timing of systemic therapy, may also have contributed to the observed variation. The difference in the stage of metastatic disease, along with the higher proportion of patients with obese (BMI>30 kg/m 2 ) in the Boston cohort, could serve as an explanation for the difference in ASA score between both cohorts. However, differences in ASA scoring are likely to be further influenced by local regulations on availability of surgery or “upcoding”, where clinicians may have had incentives to underestimate or overestimate the ASA class to support their service, resulting in variations between countries [31] . The observed differences in patient populations between Boston and Utrecht, specifically the higher number of spinal metastases, may partly explain the variations in surgical management, as a more advanced stage of metastatic spinal disease can drive the decision to pursue more aggressive surgical approaches. Conversely, earlier identification and management of patients at an earlier stage of metastatic disease may allow for less invasive surgical approaches.

Variation in surgical management

In general, more extensive surgical procedures were performed in Boston compared with Utrecht. Specifically, open vertebrectomies/corpectomies involving substantial tumor resection were commonly used in Boston, whereas percutaneous surgery was predominantly used in Utrecht. Additionally, a greater number of patients in Utrecht received postoperative radiotherapy, with radiation starting a median of 12 days earlier than in Boston. The observed differences in surgery and postoperative radiotherapy may be attributed to differing treatment philosophies across centers. In Utrecht, the extensive use of percutaneous surgery and the higher number of patients receiving postoperative radiotherapy result from an increased collaboration between radiation oncologists and spine surgeons, which started in 2015 and has facilitated a clear allocation of responsibilities and tasks. This intensified collaboration means that if local tumor control can effectively be achieved through radiotherapy, spine surgeons primarily focus on restoring or maintaining spinal stability, minimizing mechanical (activity-related) pain, and facilitating the safe delivery of radiotherapy. Consequently, over the past decade, Utrecht has shifted towards using postoperative radiotherapy rather than surgical resection as the primary strategy to achieve local tumor control [28] , [29] . Alternatively in Boston, contemporary surgical procedures involving substantial tumor resection for cytoreduction are still regularly performed, suggesting a different strategy in which surgical resection continues to play a central role to achieve local tumor control. Differences in surgical strategies between North American and European centers have been previously noted, with Wright et al. [31] reporting that procedures involving resection of over 50 % of the metastatic lesion were more common in North American centers, whereas European centers more frequently performed procedures involving resection of less than 50 % of the metastatic lesion. Such variations in surgical strategies and treatment philosophies are likely influenced by a combination of financial, institutional, and cultural factors. An example of this is the relatively lower reimbursement for percutaneous procedures in the United States compared to more extensive surgeries [32] . Furthermore, cultural differences between the United States and the Netherlands regarding end-of-life care may also influence the difference in surgical management [33] . In the United States, clinicians tend to pursue more aggressive and resource-intensive treatment in end-of-life care, as evidenced by the higher rates of chemotherapy utilization and ICU admission among patients dying with cancer [34] . In the Netherlands, by contrast, end-of-life care is largely focused on conforming to patient preferences and symptom management [35] , [36] . Finally, surgeons' preferences and training are also likely to have played a significant role in this observed variation in surgical management.

Perioperative outcomes and survival

Patients in Utrecht experienced lower rates of intraoperative blood loss, shorter operating times and shorter total hospital stays compared with patients in Boston, possibly due to the adoption of less invasive surgical techniques. Pennington et al. [37] reported similar results when comparing minimally invasive versus conventional spine surgery for spinal metastases. Notably, the higher number of instrumented spine levels in the Boston cohort may have contributed to the observed differences in intraoperative blood loss and operating times. Despite variations in surgical management strategies, no differences were found between Boston and Utrecht in terms of intraoperative complications, postoperative neurological outcome, 30-day systemic postoperative complications, reoperations, or 90-day and 1-year survival. These findings are partially in line with the literature, as Hansen-Algenstaedt et al. [38] and Miscusi et al. [39] both reported similar findings, stating no difference in intraoperative and systemic postoperative complications in patients with spinal metastases treated with less invasive surgeries. Furthermore, although patients in Utrecht presented with a higher prevalence of preoperative neurological deficit and underwent less extensive decompressive surgery, postoperative neurological outcome was similar between the two cohorts, suggesting that minimally invasive decompression may be as effective as more extensive decompressive procedures, such as vertebrectomy/corpectomy. The similarities in postoperative neurological outcome, complication rates, and survival suggest that more extensive surgical procedures, which seem to be associated with increased intraoperative blood loss, longer surgeries and longer hospital stays, did not necessarily result in better clinical outcomes. However, these findings may have been influenced by the worse prognosis of Boston patients, who presented with more advanced metastatic disease at the time of surgery.

Implications for clinical practice

This study demonstrates that while there were differences in patient populations and surgical management across major cancer centers in two distinct countries, the clinical outcomes remained largely comparable. These findings suggest that if patients with symptomatic spinal metastases undergo surgery at an earlier stage of metastatic disease, percutaneous stabilization procedures combined with radiotherapy for local tumor control and pain alleviation may achieve similar survival outcomes when compared to more contemporary extensive surgical approaches. However, given the limited survival of patients with spinal metastases, treatment is increasingly focused on improving or preserving quality of life. It is conceivable that surgical management strategies involving less invasive procedures may improve quality of life more effectively, given the higher morbidity associated with more aggressive surgical approaches. Therefore, clinicians should carefully consider the extent of surgery required for patients with symptomatic spinal metastases and make efforts to prevent treatment delays to allow for minimally invasive surgical strategies at an earlier stage of metastatic disease. Future research should focus on evaluating integrated strategies that combine less invasive surgery with radiotherapy, as well as the extent and timing of surgery needed to improve or preserve quality of life for patients with spinal metastases.

Limitations

This study had several limitations. First, we were unable to determine the number of patients treated non-surgically among all patients treated for spinal metastases across different institutions. Consequently, we could not examine potential differences in patient selection for surgery; instead, we could only address differences in patients selected fit for surgery. Second, we were unable to investigate a definitive cause for the variation in surgical management. This likely stems from multiple factors, including cultural differences regarding end-of-life care, surgeons' training, increased focus on multidisciplinary collaboration between radiation oncologists and spine surgeons, and possible financial incentives, such as reimbursements [32] . Ideally, we would have collected data related to surgical treatment decision-making, but were unable to due to the retrospective design. Third, we were unable to compare patient satisfaction and quality-of-life outcomes, as these were not documented during routine case visits in Boston. Including such information could have further enhanced the impact of this study. Additionally, given the rising incidence of spinal metastases, it would have been interesting to study the cost-effectiveness of the varying surgical management across institutions, as this could provide insights into the financial implications of different treatment strategies. Furthermore, it would have been valuable to categorize separation surgery as a distinct type of surgical procedure. However, due to its relatively recent development and ongoing evolution, the technique remains insufficiently defined, resulting in substantial variability in its application across institutions, which precluded a meaningful comparison [40] , [41] . Finally, SINS scores were not always reported and had to be manually extracted from patient records. In Boston, pain characteristics such as mechanical pain were rarely included in admission notes or radiology reviews. However, we believe we were able to extract pain reasonably accurately from the consultation reference notes in the medical records. Despite these limitations, our large cross-continental cohort study enabled us to provide valuable insights into the differences in patients selected for surgery, surgical management, and outcomes between cross-continental tertiary institutions. Future studies investigating different surgical management strategies should include prospectively collected quality-of-life outcomes, patient satisfaction, and factors influencing treatment decision-making.

Conclusion

This retrospective study of patients surgically treated for spinal metastases identified differences in patient populations and surgical management between major cancer centers on separate continents. Overall, patients undergoing surgery for spinal metastases in Boston generally presented with a more advanced stage of metastatic disease at the time of surgery compared with patients in Utrecht. Additionally, the use of more extensive surgical procedures, such as anterior column resection, was greater in Boston, whereas in Utrecht, patients received postoperative radiotherapy more frequently and earlier than in Boston. Further research is needed to evaluate surgical management strategies that integrate less invasive surgery with radiotherapy and determine the required extent and optimal timing of surgery to improve the quality of life for patients with spinal metastases.

Institutions

Investigation was performed at the Department of Orthopaedic Surgery, Massachusetts General Hospital - Harvard Medical School, Boston, United States and the Department of Orthopaedic Surgery, University Medical Center Utrecht, the Netherlands.

IRB approval

2017P00838 (MGH) and VOBU 23U-0528 (UMCU).

Data availability statement

The datasets generated during and/or analysed during the current study are not publicly available due to legal restrictions arising from data-sharing agreements but are available from the corresponding author on reasonable request.

CRediT authorship contribution statement

Jantijn J.G.J. Amelink: Writing – review & editing, Writing – original draft, Methodology, Formal analysis, Data curation, Conceptualization. Bram T. van Munster: Writing – review & editing, Writing – original draft, Data curation, Conceptualization. Bas J.J. Bindels: Writing – review & editing, Validation, Methodology, Data curation. Robertus J.B. Pierik: Writing – review & editing, Project administration, Data curation. Jasper van Tiel: Writing – review & editing, Validation. Olivier Q. Groot: Writing – review & editing, Validation, Supervision, Methodology, Conceptualization. Nicolien Kasperts: Writing – review & editing, Validation. Daniel G. Tobert: Writing – review & editing, Validation, Supervision, Conceptualization. Jorrit-Jan Verlaan: Writing – review & editing, Validation, Supervision, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

1 Ciftdemir M. Kaya M. Selcuk E. Yalniz E. Tumors of the spine World J. Orthop. 7 2016 109 116 10.5312/wjo.v7.i2.109 26925382 PMC4757655

2 Fornasier V.L. Horne J.G. Metastases to the vertebral column Cancer 36 1975 590 594 10.1002/1097-0142(197508)36:2<590::aid-cncr2820360240>3.0.co;2-f 1157021

3 Prasad D. Schiff D. Malignant spinal-cord compression Lancet Oncol. 6 2005 15 24 10.1016/S1470-2045(04)01709-7 15629272

4 Nater A. Sahgal A. Fehlings M. Management - spinal metastases Handb. Clin. Neurol. 149 2018 239 255 10.1016/B978-0-12-811161-1.00016-5 29307356

5 Quraishi N.A. Gokaslan Z.L. Boriani S. The surgical management of metastatic epidural compression of the spinal cord J. Bone Joint Surg. Br. 92 2010 1054 1060 10.1302/0301-620X.92B8.22296 20675746

6 Bilsky M.H. Laufer I. Burch S. Shifting paradigms in the treatment of metastatic spine disease Spine (phila Pa 1976) 34 2009 S101 S107 10.1097/BRS.0b013e3181bac4b2 19829269

7 Sciubba D.M. Pennington Z. Colman M.W. Goodwin C.R. Laufer I. Patt J.C. Redmond K.J. Saylor P. Shin J.H. Schwab J.H. Schoenfeld A.J. NASS Spine Oncology Committee, Spinal metastases 2021: a review of the current state of the art and future directions Spine J. 21 2021 1414 1429 10.1016/j.spinee.2021.04.012 33887454

8 Laufer I. Bilsky M.H. Advances in the treatment of metastatic spine tumors: the future is not what it used to be J. Neurosurg. Spine 30 2019 299 307 10.3171/2018.11.SPINE18709 30835704

9 North R.B. LaRocca V.R. Schwartz J. North C.A. Zahurak M. Davis R.F. McAfee P.C. Surgical management of spinal metastases: analysis of prognostic factors during a 10-year experience J. Neurosurg. Spine 2 2005 564 573 10.3171/spi.2005.2.5.0564 15945430

10 Tomita K. Kawahara N. Kobayashi T. Yoshida A. Murakami H. Akamaru T. Surgical strategy for spinal metastases Spine (phila Pa 26 2001 1976 298 306 10.1097/00007632-200102010-00016 11224867

11 Weigel B. Maghsudi M. Neumann C. Kretschmer R. Müller F.J. Nerlich M. Surgical management of symptomatic spinal metastases. Postoperative outcome and quality of life Spine (phila Pa 24 1999 1976 2240 2246 10.1097/00007632-199911010-00012 10562991

12 Hubertus V. Gempt J. Mariño M. Sommer B. Eicker S.O. Stangenberg M. Dreimann M. Janssen I. Wipplinger C. Wagner A. Lange N. Jörger A.-K. Czabanka M. Rohde V. Schaller K. Thomé C. Vajkoczy P. Onken J.S. Meyer B. Surgical management of spinal metastases involving the cervicothoracic junction: results of a multicenter European Observational Study, Neurosurg Focus 50 2021 E7 10.3171/2021.2.FOCUS201067 33932937

13 Bollen L. Dijkstra S.P.D. Bartels R.H.M.A. de Graeff A. Poelma D.L.H. Brouwer T. Algra P.R. Kuijlen J.M.A. Minnema M.C. Nijboer C. Rolf C. Sluis T. Terheggen M.A.M.B. van der Togt-van Leeuwen A.C.M. van der Linden Y.M. Taal W. Clinical management of spinal metastases-The Dutch national guideline Eur J Cancer 104 2018 81 90 10.1016/j.ejca.2018.08.028 30336360

14 Pielkenrood B.J. Visser T.F. van Tol F.R. Foppen W. Eppinga W.S.C. Verhoeff J.J.C. Bol G.H. Van der Velden J.M. Verlaan J.-J. Remineralization of lytic spinal metastases after radiotherapy Spine J. 23 2023 571 578 10.1016/j.spinee.2022.12.018 36623735

15 von Elm E. Altman D.G. Egger M. Pocock S.J. Gøtzsche P.C. Vandenbroucke J.P. STROBE Initiative, Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies BMJ 335 2007 806 808 10.1136/bmj.39335.541782.AD 17947786 PMC2034723

16 van Tol F.R. Massier J.R.A. Frederix G.W.J. Öner F.C. Verkooijen H.M. Verlaan J.-J. Costs Associated With Timely and Delayed Surgical Treatment of Spinal Metastases., Global Spine J. 12 2022 1661 1666 10.1177/2192568220984789 PMC9609516 33511876

17 Flouzat-Lachaniette C.-H. Allain J. Roudot-Thoraval F. Poignard A. Treatment of spinal epidural compression due to hematological malignancies: a single institution’s retrospective experience Eur. Spine J. 22 2013 548 555 10.1007/s00586-012-2562-y 23143094 PMC3585643

18 Zadnik P.L. Goodwin C.R. Karami K.J. Mehta A.I. Amin A.G. Groves M.L. Wolinsky J.-P. Witham T.F. Bydon A. Gokaslan Z.L. Sciubba D.M. Outcomes following surgical intervention for impending and gross instability caused by multiple myeloma in the spinal column J Neurosurg Spine 22 2015 301 309 10.3171/2014.9.SPINE14554 25575166

19 Bryant D. Havey T.C. Roberts R. Guyatt G. How many patients? How many limbs? Analysis of patients or limbs in the orthopaedic literature: a systematic review J. Bone Joint Surg. Am. 88 2006 41 45 10.2106/JBJS.E.00272 16391248

20 Charlson M.E. Carrozzino D. Guidi J. Patierno C. Charlson Comorbidity Index: A Critical Review of Clinimetric Properties Psychother. Psychosom. 91 2022 8 35 10.1159/000521288 34991091

21 Karhade A.V. Thio Q.C.B.S. Ogink P.T. Bono C.M. Ferrone M.L. Oh K.S. Saylor P.J. Schoenfeld A.J. Shin J.H. Harris M.B. Schwab J.H. Predicting 90-Day and 1-Year Mortality in Spinal Metastatic Disease: Development and Internal Validation Neurosurgery 85 2019 E671 E681 10.1093/neuros/nyz070 30869143

22 Oken M.M. Creech R.H. Tormey D.C. Horton J. Davis T.E. McFadden E.T. Carbone P.P. Toxicity and response criteria of the Eastern Cooperative Oncology Group Am. J. Clin. Oncol. 5 1982 649 655 7165009

23 Rupp R. Biering-Sørensen F. Burns S.P. Graves D.E. Guest J. Jones L. Read M.S. Rodriguez G.M. Schuld C. Tansey-Md K.E. Walden K. Kirshblum S. International Standards for Neurological Classification of Spinal Cord Injury: Revised 2019 Top Spinal Cord Inj Rehabil 27 2021 1 22 10.46292/sci2702-1 PMC8152171 34108832

24 Fisher C.G. DiPaola C.P. Ryken T.C. Bilsky M.H. Shaffrey C.I. Berven S.H. Harrop J.S. Fehlings M.G. Boriani S. Chou D. Schmidt M.H. Polly D.W. Biagini R. Burch S. Dekutoski M.B. Ganju A. Gerszten P.C. Gokaslan Z.L. Groff M.W. Liebsch N.J. Mendel E. Okuno S.H. Patel S. Rhines L.D. Rose P.S. Sciubba D.M. Sundaresan N. Tomita K. Varga P.P. Vialle L.R. Vrionis F.D. Yamada Y. Fourney D.R. A novel classification system for spinal instability in neoplastic disease: an evidence-based approach and expert consensus from the Spine Oncology Study Group Spine (phila Pa 35 2010 1976 E1221 E1229 10.1097/BRS.0b013e3181e16ae2 20562730

25 Laufer I. Rubin D.G. Lis E. Cox B.W. Stubblefield M.D. Yamada Y. Bilsky M.H. The NOMS Framework: Approach to the Treatment of Spinal Metastatic Tumors Oncologist 18 2013 744 751 10.1634/theoncologist.2012-0293 23709750 PMC4063402

26 Pierik R.J.B. Amelink J.J.G.J. Groot O.Q. Som A. Munster B.T. Reus D.C. Chua T.L. Zijlstra H. Verlaan J.-J. Shin J.H. Rabinov J.D. Tobert D.G. Surgical outcomes after preoperative embolization in hypervascular spinal metastases: a propensity scored study of 191 patients Spine (Phila Pa 1976) 50 7 2025 437 446 10.1097/BRS.0000000000005182 39451152

27 Paulino Pereira N.R. Ogink P.T. Groot O.Q. Ferrone M.L. Hornicek F.J. van Dijk C.N. Bramer J.A.M. Schwab J.H. Complications and reoperations after surgery for 647 patients with spine metastatic disease Spine J. 19 2019 144 156 10.1016/j.spinee.2018.05.037 29864546

28 van Tol F.R. Suijkerbuijk K.P.M. Choi D. Verkooijen H.M. Oner F.C. Verlaan J.-J. The importance of timely treatment for quality of life and survival in patients with symptomatic spinal metastases Eur. Spine J. 29 2020 3170 3178 10.1007/s00586-020-06599-x 32948899

29 van Tol F.R. Versteeg A.L. Verkooijen H.M. Öner F.C. Verlaan J.-J. Time to Surgical Treatment for Metastatic Spinal Disease: Identification of Delay Intervals., Global Spine J. 13 2023 316 323 10.1177/2192568221994787 PMC9972289 33596711

30 Katagiri H. Takahashi M. Wakai K. Sugiura H. Kataoka T. Nakanishi K. Prognostic factors and a scoring system for patients with skeletal metastasis J. Bone Joint Surg. Br. 87 2005 698 703 10.1302/0301-620X.87B5.15185 15855375

31 Silman A.J. Combescure C. Ferguson R.J. Graves S.E. Paxton E.W. Frampton C. Furnes O. Fenstad A.M. Hooper G. Garland A. Spekenbrink-Spooren A. Wilkinson J.M. Mäkelä K. Lübbeke A. Rolfson O. International variation in distribution of ASA class in patients undergoing total hip arthroplasty and its influence on mortality: data from an international consortium of arthroplasty registries Acta Orthop. 92 2021 304 310 10.1080/17453674.2021.1892267 33641588 PMC8231354

32 Chung A.S. Ballatori A. Ortega B. Min E. Formanek B. Liu J. Hsieh P. Hah R. Wang J.C. Buser Z. Is Less Really More? Economic Evaluation of Minimally Invasive Surgery., Global Spine J. 11 2021 30S S36 10.1177/2192568220958403 PMC8076812 32975446

33 Angus D.C. Barnato A.E. Linde-Zwirble W.T. Weissfeld L.A. Watson R.S. Rickert T. Rubenfeld G.D. Robert Wood Johnson Foundation ICU End-Of-Life Peer Group, Use of intensive care at the end of life in the United States: an epidemiologic study Crit. Care Med. 32 2004 638 643 10.1097/01.ccm.0000114816.62331.08 15090940

34 Bekelman J.E. Halpern S.D. Blankart C.R. Bynum J.P. Cohen J. Fowler R. Kaasa S. Kwietniewski L. Melberg H.O. Onwuteaka-Philipsen B. Oosterveld-Vlug M. Pring A. Schreyögg J. Ulrich C.M. Verne J. Wunsch H. Emanuel E.J. International Consortium for End-of-Life Research (ICELR), Comparison of Site of Death, Health Care Utilization, and Hospital Expenditures for Patients Dying With Cancer in 7 Developed Countries J. Am. Med. Assoc. 315 2016 272 283 10.1001/jama.2015.18603 26784775

35 De Roo M.L. Leemans K. Claessen S.J.J. Cohen J. Pasman H.R.W. Deliens L. Francke A.L. EURO IMPACT, Quality indicators for palliative care: update of a systematic review J. PainSymptom Manage 46 2013 556 572 10.1016/j.jpainsymman.2012.09.013 23809769

36 Gomes B. Higginson I.J. Calanzani N. Cohen J. Deliens L. Daveson B.A. Bechinger-English D. Bausewein C. Ferreira P.L. Toscani F. Meñaca A. Gysels M. Ceulemans L. Simon S.T. Pasman H.R.W. Albers G. Hall S. Murtagh F.E.M. Haugen D.F. Downing J. Koffman J. Pettenati F. Finetti S. Antunes B. Harding R. PRISMA, Preferences for place of death if faced with advanced cancer: a population survey in England, Flanders, Germany, Italy, the Netherlands, Portugal and Spain Ann. Oncol. 23 2012 2006 2015 10.1093/annonc/mdr602 22345118

37 Pennington Z. Ahmed A.K. Molina C.A. Ehresman J. Laufer I. Sciubba D.M. Minimally invasive versus conventional spine surgery for vertebral metastases: a systematic review of the evidence Ann Transl Med 6 2018 103 10.21037/atm.2018.01.28 PMC5900071 29707552

38 Hansen-Algenstaedt N. Kwan M.K. Algenstaedt P. Chiu C.K. Viezens L. Chan T.S. Lee C.K. Wellbrock J. Chan C.Y.W. Schaefer C. Comparison Between Minimally Invasive Surgery and Conventional Open Surgery for Patients With Spinal Metastasis: A Prospective Propensity Score-Matched Study Spine (phila Pa 42 2017 1976 789 797 10.1097/BRS.0000000000001893 27584676

39 Miscusi M. Polli F.M. Forcato S. Ricciardi L. Frati A. Cimatti M. De Martino L. Ramieri A. Raco A. Comparison of minimally invasive surgery with standard open surgery for vertebral thoracic metastases causing acute myelopathy in patients with short- or mid-term life expectancy: surgical technique and early clinical results J. Neurosurg. Spine 22 2015 518 525 10.3171/2014.10.SPINE131201 25723122

40 Amelink J.J.G.J. Bindels B.J.J. Kasperts N. MacDonald S.M. Tobert D.G. Verlaan J.-J. Radiotherapy and surgery: can this combination be further optimized for patients with metastatic spine disease? Oncologist 30 2025 10.1093/oncolo/oyae359 PMC11745020 39832131

41 Lin J. Zhu X. Tang Q. Lu J. Xu H. Song G. Deng C. Wu H. Huang Y. Huang A. Xu Y. Chen H. Wang J. Minimally invasive separation surgery for the treatment of spinal metastases with small incision and freehand pedicle screw fixation: the surgical learning curve BMC Musculoskelet. Disord. 23 2022 273 10.1186/s12891-022-05191-2 35317753 PMC8939122

Supplementary data

The following are the Supplementary data to this article: Supplementary Data 1

Supplementary Data 2

Supplementary Data 3

Acknowledgements

None.

Funding sources

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Supplementary data to this article can be found online at https://doi.org/10.1016/j.jbo.2025.100676 .

ИП Урсолов Владлен Сергеевич

ИНН 500118482352 · ОГРНИП 314500117700049

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