Orthopedics

Feature Article 

Relationship Between Paralysis and the Epidural Spinal Cord Compression Scale in Spinal Metastasis

Hiroshi Uei, MD; Yasuaki Tokuhashi, MD; Masafumi Maseda, MD

Abstract

Patients with metastatic spinal tumors often experience paralysis caused by spinal cord compression. Several studies have investigated metastatic lesion–related spinal cord compression. This study is the first to examine the relationship between the epidural spinal cord compression (ESCC) scale, which measures circumferential compression, and the functional outcomes of treatment, which were assessed at regular intervals after treatment until death. A total of 191 patients who had grade D or worse paralysis on the American Spinal Injury Association (ASIA) classification scale and a grade 1b or more severe cord compression on the ESCC scale were included in the study. Patients had been treated with surgery combined with radiotherapy (n=146) or radiotherapy alone (n=45). Three spinal surgeons assessed the ESCC grade of for patient, and the grade agreed to by at least 2 surgeons was adopted. After 4 weeks, re-evaluations were conducted by the same examiners. The authors also calculated the mean kappa coefficients for inter- and intra-examiner variability (0.88 and 0.93, respectively). The distribution of the ASIA grade differed significantly among the ESCC scale grades (P=.0102). However, the degree of improvement in paralysis in terms of the ASIA grade (≥1 grade of improvement, no change, or ≥1 grade of aggravation) was not significantly associated with the ESCC grade (P=.2334). The ESCC scale was found to be a useful indicator of circumferential spinal cord compression but was not identified as a significant functional prognostic factor for paralysis. [Orthopedics. 2020;43(6):e567–e573.]

Abstract

Patients with metastatic spinal tumors often experience paralysis caused by spinal cord compression. Several studies have investigated metastatic lesion–related spinal cord compression. This study is the first to examine the relationship between the epidural spinal cord compression (ESCC) scale, which measures circumferential compression, and the functional outcomes of treatment, which were assessed at regular intervals after treatment until death. A total of 191 patients who had grade D or worse paralysis on the American Spinal Injury Association (ASIA) classification scale and a grade 1b or more severe cord compression on the ESCC scale were included in the study. Patients had been treated with surgery combined with radiotherapy (n=146) or radiotherapy alone (n=45). Three spinal surgeons assessed the ESCC grade of for patient, and the grade agreed to by at least 2 surgeons was adopted. After 4 weeks, re-evaluations were conducted by the same examiners. The authors also calculated the mean kappa coefficients for inter- and intra-examiner variability (0.88 and 0.93, respectively). The distribution of the ASIA grade differed significantly among the ESCC scale grades (P=.0102). However, the degree of improvement in paralysis in terms of the ASIA grade (≥1 grade of improvement, no change, or ≥1 grade of aggravation) was not significantly associated with the ESCC grade (P=.2334). The ESCC scale was found to be a useful indicator of circumferential spinal cord compression but was not identified as a significant functional prognostic factor for paralysis. [Orthopedics. 2020;43(6):e567–e573.]

Patients with metastatic spinal tumors often experience paralysis caused by spinal cord compression. Meta-static tumor–induced spinal cord compression occurs in 5% to 14% of all patients with cancer.1,2 It has been reported that recovery from complete spinal cord paralysis is difficult to achieve, so metastatic tumor–induced spinal cord paralysis should be surgically treated via direct decompression.2–5 The progression speed and severity of paralysis6,7 and the grade of spinal cord compression8,9 have been proposed as functional prognostic factors for metastatic tumor–induced spinal cord paralysis. However, until recently few studies had evaluated the grade of spinal cord compression in patients with metastatic tumor–induced spinal cord paralysis.3,8–12 Furthermore, such evaluations were limited to the early period after treatment (ie, paralysis was not evaluated at regular intervals until death).8

Bilsky et al10 proposed the epidural spinal cord compression (ESCC) scale as a tool for evaluating spinal cord compression, which is based on the findings of spinal cord compression on axial-view T2-weighted magnetic resonance imaging (MRI). This scale has been examined in validation and replication studies.8 Magnetic resonance imaging is the current standard diagnostic method for spinal metastasis,13 and its sensitivity and specificity are high.14 However, in patients with tumor-induced spinal cord compression, the MRI findings of spinal cord compression and the severity of paralysis are not necessarily correlated, and the current authors have also reported that the severity of paralysis in such cases depends on the level of the spine at which the greatest spinal cord compression is seen.15

The current study aimed to examine whether the grade of metastatic spinal tumor–induced spinal cord compression reflects the final functional outcome. Thus, the authors investigated the functional outcomes of locally treated paralysis in patients with metastatic tumor–induced spinal cord compression using the American Spinal Injury Association (ASIA) classification. In addition, they evaluated the relationship between paralysis, which was assessed at regular intervals until death, and the severity of circumferential spinal cord compression.

Materials and Methods

A total of 191 patients with a metastatic spinal tumor with grade D or worse paralysis on the ASIA scale who exhibited grade 1b or more severe spinal cord compression on the ESCC scale on a cross-sectional T2-weighted MRI were included. All patients died after receiving treatment at a single institution between January 1, 2001, and December 31, 2016. Of patients, 128 were men and 63 were women. Patients' ages ranged from 15 to 92 years (mean, 62.5 years). Most tumor-related spinal cord compressions occurred at the C1-T2, T3-L1, and L2-S1 levels (49, 89, and 53 patients, respectively). Mean±SD survival time was 13.0±21.2 months, and median survival time was 7.0 months.

Patient inclusion criteria were as follows: (1) developed ASIA grade D or worse paralysis; (2) exhibited an ESCC scale grade 1b or more severe metastatic tumor–induced spinal cord compression on cross-sectional T2-weighted MRI combined with osseous involvement; (3) received initial treatment, including local radiotherapy for the metastatic spinal tumor, at the authors' institution; (4) died during the follow-up period at greater than 2 months after the initial treatment; and (5) had their paralysis evaluated at regular intervals until death. Exclusion criteria were as follows: (1) metastatic tumor–induced spinal cord compression without osseous involvement; (2) spinal cord compression at greater than 2 distant locations; or (3) dropping out of the follow-up during the study period.

Surgery plus postoperative radiotherapy was performed in 146 patients (posterior decompression plus stabilization for 118 patients, and palliative posterior stabilization alone for 28 patients). Posterior decompression was performed via laminectomy combined with tumor curettage where possible. Stabilization was performed at 2 or 3 levels above and 2 or 3 levels below the pedicle screw fixation site.

Conventional postoperative radiotherapy was administered and consisted of a total dose of 40 Gy delivered in 2-Gy fractions. The 45 patients who did not undergo surgery received local conventional radiotherapy, involving a total dose of 40 Gy delivered in 2-Gy fractions (n=27) or a palliative dose of 24 Gy delivered in 8-Gy fractions (n=18). Across the surgery with radiotherapy group and the radiotherapy alone group, chemotherapy was administered to 83 patients (43.5%). A bisphosphonate (zoledronic acid) and anti-receptor activator of nuclear factor kappa-beta ligand antibodies (denosumab) were concomitantly administered to 118 (61.7%) and 39 (20.4%) patients, respectively.

The treatment strategy was as follows: (1) surgery plus radiotherapy was a priority for patients who were symptomatic; (2) radiotherapy without surgery was administered according to the patient's condition and wishes; and (3) adjuvant therapy was used whenever the patient's condition allowed it.

ESCC Scale

The ESCC scale is composed of 6 grades: grade 0 represents invasion localized in the bones (bone involvement alone); grade 1 represents epidural compression (epidural impingement); grade 2 represents spinal cord compression with visible cerebrospinal fluid (CSF) retention around the spinal cord (spinal cord compression with CSF visible); and grade 3 represents severe spinal cord compression without visible CSF around the spinal cord (spinal cord compression without CSF visible). Grade 1 is further divided into 3 subgroups: grade 1a represents epidural advancement without deformation of the dural canal (epidural impingement without deformation of the thecal sac); grade 1b represents dural canal compression without contact with the spinal cord (deformation of the thecal sac without spinal cord abutment); and grade 1c represents dural canal deformities involving contact with the spinal cord but without spinal cord compression (deformation of the thecal sac with spinal cord abutment but without compression; Figure 1). Because it is difficult to distinguish between ESCC grades 1c and 2 at the L2 or lower cauda equina level, cases corresponding to either grade were classified as ESCC grade 1c.

Schematic representation of the 6-point epidural spinal cord compression grading scale. Grade 0: bone involvement alone; grade 1: epidural impingement; 1a: epidural impingement without deformation of the thecal sac; 1b: deformation of the thecal sac without spinal cord abutment but without spinal cord abutment; 1c: deformation of the thecal sac with spinal cord abutment but without spinal cord compression; grade 2: spinal cord compression with cerebrospinal fluid visible around the spinal cord; and grade 3: spinal cord compression without cerebrospinal fluid visible around the spinal cord.

Figure 1:

Schematic representation of the 6-point epidural spinal cord compression grading scale. Grade 0: bone involvement alone; grade 1: epidural impingement; 1a: epidural impingement without deformation of the thecal sac; 1b: deformation of the thecal sac without spinal cord abutment but without spinal cord abutment; 1c: deformation of the thecal sac with spinal cord abutment but without spinal cord compression; grade 2: spinal cord compression with cerebrospinal fluid visible around the spinal cord; and grade 3: spinal cord compression without cerebrospinal fluid visible around the spinal cord.

Three spinal surgeons (H.U., Y.T., M.M.) judged the ESCC grade of each patient, and the grade agreed on by at least 2 of them was adopted. After 4 weeks, reevaluations were conducted by the same examiners. The authors also calculated the kappa coefficients for inter- and intra-examiner variability.

Transverse Localization of Tumors

The grade of metastatic tumor–induced spinal cord compression can be determined using the ESCC scale, but the ESCC scale does not take the axial localization of the tumor into account. Thus, the following 4 categories were newly added: (1) anterior compression alone (anterior), (2) anterior plus posterior compression (anterior+posterior), (3) anterior plus foraminal compression (anterior+foraminal), and (4) circumferential compression (anterior+posterior+ foraminal; Figure 2).

Transverse tumor localization. A, anterior compression alone; AP, anterior+posterior compression; AF, anterior+foraminal compression; APF, circumferential compression (anterior+posterior+foraminal compression).

Figure 2:

Transverse tumor localization. A, anterior compression alone; AP, anterior+posterior compression; AF, anterior+foraminal compression; APF, circumferential compression (anterior+posterior+foraminal compression).

Analyses

The patients' paralysis statuses were assessed at regular intervals until death, and the ASIA classification16 was used to evaluate the severity of spinal cord paralysis. Posttreatment improvements in paralysis of 1 ASIA grade were seen in 3 (50.0%), 7 (16.7%), 18 (22.2%), and 17 (27.4%) patients with an ESCC scale grade 1b, 1c, 2, and 3 spinal cord compression, respectively. Conversely, the posttreatment worsening of paralysis by 1 ASIA grade was seen in 1 (16.7%), 13 (31.0%), 25 (30.9%), and 14 (22.6%) patients with ESCC scale grade 1b, 1c, 2, and 3 spinal cord compression, respectively.

Factors influencing neurologic outcomes (age, the level of the spine that exhibited the greatest tumor-related spinal cord compression, the primary cancer site, the survival period, the pretreatment ASIA classification, the transverse location of the tumor, the ESCC scale grade, and the type of treatment) were analyzed.

Statistical Analyses

Univariate analyses of continuous variables were performed using the t test, Welch's method, the paired t test, analysis of variance, or Tukey's test. The significance of differences in noncontinuous variables was analyzed using the Mann–Whitney U test, chi-square test, or Kruskal–Wallis test. All statistical analyses were performed using the StatMate V, version 5, software (Atoms Co, Tokyo, Japan). P<.05 was considered statistically significant.

Results

Patients' Baseline Characteristics

Patients' baseline characteristics are shown according to the local treatments used in Table 1. The following parameters differed significantly between the patients treated with a combination of surgery and radiotherapy and the patients treated with radiotherapy alone: the primary cancer site (P=.0029), the transverse location of the tumor (Figure 2; P<.001), and the survival period (P<.001; Table 1).

Demographic and Pretreatment Data According to the Treatments Used

Table 1:

Demographic and Pretreatment Data According to the Treatments Used

Posttreatment Paralysis Status

The following neurologic outcomes were obtained for the 191 patients: ASIA grade A: 17 patients; ASIA grade B: 49 patients; ASIA grade C: 50 patients; ASIA grade D: 43 patients; and ASIA grade E: 32 patients. Regarding the degree of improvement in the patients' paralysis, 1 grade or greater improvement was observed in the ASIA grade in 45 patients (improvement group), no change was observed in 90 patients (maintenance group), and 1 grade or greater aggravation was observed in 56 patients (deterioration group). A breakdown of the data for the 45 patients in the improvement group is shown in Table 2.

Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

Table 2:

Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

Relationship Between the ESCC Grade and Paralysis Grade

Mean inter-examiner consistency rate of the ESCC scale evaluations among the 3 examiners was 95.8% (range, 95.0%–96.6%), and mean kappa coefficient was 0.88 (range, 0.86–0.90). Mean intra-examiner consistency rate was 97.0% (range, 96.6%–97.6%), and mean kappa coefficient was 0.93 (range, 0.90–0.97).

The distribution of ASIA grades, which was assessed at regular intervals after treatment until death, differed significantly among the ESCC scale grades (P=.0102; Figure 3; Table 3). In addition to the ESCC grade, the distribution of the ASIA grades differed significantly according to age (<70 vs ≥70 years), the spinal level that exhibited the greatest tumor-induced spinal cord compression, the primary cancer site (lung cancer, breast/prostatic/thyroid cancer, or others), the survival period (<6 vs ≥6 months), and the pretreatment ASIA grade (Table 3).

Posttreatment American Spinal Injury Association (ASIA) grades observed during assessments performed at regular intervals until death according to the epidural spinal cord compression (ESCC) grade.

Figure 3:

Posttreatment American Spinal Injury Association (ASIA) grades observed during assessments performed at regular intervals until death according to the epidural spinal cord compression (ESCC) grade.

Factors Associated With the Posttreatment ASIA Classification

Table 3:

Factors Associated With the Posttreatment ASIA Classification

However, the degree of improvement in paralysis in terms of the ASIA grade (≥1 grade of improvement, no change, or ≥1 grade of aggravation) was not significantly associated with the ESCC grade (P=.2334; Table 4). The primary cancer site and type of treatment were found to significantly affect the post-treatment improvement in the ASIA grade (P=.0152 and P<.001, respectively; Table 4). Concerning the effects of the type of treatment, the ASIA grade significantly improved by greater than 1 grade in the surgery plus radiotherapy group (P=.039). However, the ASIA grade significantly worsened by greater than 1 grade in the radiotherapy alone group (P<.001; Figure 4).

Factors Associated With a Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

Table 4:

Factors Associated With a Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

Bar graphs showing pre- and posttreatment American Spinal Injury Association (ASIA) grades observed during assessments performed at regular intervals from the start of treatment until death for the surgery plus radiotherapy group (left) vs the radiotherapy alone group (right). The ASIA grade improved significantly in the surgery plus radiotherapy group (P=.039). The ASIA grade worsened significantly in the radiotherapy alone group (P<.001).

Figure 4:

Bar graphs showing pre- and posttreatment American Spinal Injury Association (ASIA) grades observed during assessments performed at regular intervals from the start of treatment until death for the surgery plus radiotherapy group (left) vs the radiotherapy alone group (right). The ASIA grade improved significantly in the surgery plus radiotherapy group (P=.039). The ASIA grade worsened significantly in the radiotherapy alone group (P<.001).

Discussion

In a retrospective study of T2-weighted axial MRI images, Oshima et al9 reported that postoperative walking function can be predicted from the circumferential ratio of cord compression. They also stated that the compressed region (which is closely related to the direction of compression) is not associated with pretreatment paralysis or posttreatment walking function, and that nerve function depends on the grade of circumferential spinal cord compression rather than on the simple mechanical compressive force involved.9

In addition, they reported that a circumferential ratio of cord compression of greater than 50% is associated with poor ambulatory function, which indicates that the circumferential ratio of cord compression is a new MRI parameter that is useful for assessing the risk of metastatic tumor–induced spinal cord compression.9 Thus, the current authors investigated whether the posttreatment functional paralysis outcomes of patients with metastatic tumor–induced spinal cord compression can be predicted using the ESCC scale. As a result, it was demonstrated that the distribution of the ASIA grade, which was assessed at regular intervals after treatment until death, differed significantly among the various ESCC grades (P=.0102; Figure 3; Table 3). However, the degree of improvement in paralysis in terms of the ASIA grade (≥1 grade of improvement, no change, or ≥1 grade of aggravation) was not found to be significantly associated with the ESCC grade (P=.2334). Thus, different results were obtained depending on the method used to evaluate paralysis.

Quraishi et al8 also surveyed functional paralysis outcomes according to the ESCC scale and found that nerve recovery was achieved even when the grade of spinal cord compression was high. Similarly, the current authors did not detect any significant difference in the improvement in paralysis among the grades of the ESCC scale, and it was difficult to predict post-treatment recovery from paralysis based on the ESCC scale.

The transverse location of a spinal tumor on cross-sectional MRI does not indicate the severity of the associated spinal cord compression. Similarly, the ESCC scale only indicates the direction of spinal cord compression, not its severity. Furthermore, patients who are asymptomatic with ESCC grade 2 or 3 spinal cord compression are frequently encountered. Therefore, morphologic evaluations alone cannot be used to predict the ASIA paralysis grade or functional prognosis of patients with metastatic spinal tumors. Other factors that can be used to predict paralysis in such cases (eg, the time from the onset of paralysis to the start of treatment, the time until irreversible paralysis occurs) are required.

Among the other factors examined in the current study, only the primary cancer site (lung cancer, breast/prostatic/thyroid cancer, or others) and the type of treatment were shown to be significantly associated with the ASIA paralysis grade or a 1 grade or greater improvement in the ASIA grade after treatment. Conventional radiotherapy was administered to all patients in the surgery plus radiotherapy group. The combination of surgery and conventional radiotherapy was found to be superior to conventional radiotherapy alone in terms of its ability to improve paralysis. This was consistent with the results reported by Patchell et al2 and Cole et al.17 However, in the current series, significant differences were found in the primary cancer site, transverse location of the lesion, Tokuhashi score, and the survival period between the surgery plus radiotherapy group and the radiotherapy alone group (Table 1). In addition, the current study was not a randomized controlled trial.

As described above, the limitations of this study include the fact that it was not a randomized controlled study and did not involve multivariate analysis; therefore, it was not possible to completely rule out the effects of confounding factors. Furthermore, because different types of variables were examined, and each variable was subjected to various statistical procedures, the statistical power of the study might have been insufficient.

Other limitations of this study include the small number of patients and the fact that the effects of spinal cord compression in the craniocaudal direction, the duration of tumor-induced compression, the time from the onset of paralysis to the start of treatment, the time it took for irreversible paralysis to develop, the hardness of the primary tumor, and the circulation in the compressed spinal cord were not investigated. Therefore, further factors that might be associated with the posttreatment improvement in ASIA grade should be investigated in future studies. A prospective study including these elements should be performed.

Conclusion

The ESCC scale and neurologic outcomes were investigated in 191 patients with metastatic spinal tumors and paralysis. The ESCC scale according to axial-view MRI was found to be a useful indicator of circumferential spinal cord compression but was not identified as a significant functional prognostic factor for paralysis. The primary cancer site and the type of treatment were the only factors found to be significantly associated with the posttreatment ASIA paralysis grade or a 1 grade or greater improvement in the ASIA paralysis grade.

References

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Demographic and Pretreatment Data According to the Treatments Used

CharacteristicSurgery+Radiotherapy (n=146)Radiotherapy Without Surgery (n=45)P
Male:female, No.96:5032:13.5865
Age, mean±SD (range), y60.8±13.8 (15–92)61.1±12.9 (20–79).8260
Spinal level that exhibited the greatest tumor-related spinal cord compression, No.
  C1-T23514.1661
  T3-L16722
  L2-S1449
Primary site, No.
  Lungs3514.0029a
  Kidneys183
  Prostate153
  Liver1112
  Breast125
  Other558
VAS, score, mean±SD (range)77.8±8.9 (27–100)79.4±6.9 (41–100).5236
ASIA classification, No.
  A31.2735
  B215
  C6818
  D5421
  E00
Transverse location, No.
  A95<.001a
  AP44
  AF6719
  APF6617
ESCC scale, No.
  1b42.0677
  1c2913
  26120
  35210
Survival period, mean±SD (range), mo13.5±23.5 (0.25–68)6.1±5.4 (0.2–19)<.001a
Posttreatment VAS score, mean±SD (range)23.8±9.6 (0–48)25.4±10.2 (0–67).5982

Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

ParameterNo. (%)1-Grade Improvement
Age
  <70 y (n=141)31 (22.0)
  ≥70 y (n=50)14 (28.0)
Spinal level that exhibited the greatest tumor-related spinal cord compression
  C2-T2 (n=48)10 (20.8)
  T3-L1 (n=105)23 (21.9)
  L2-S1 (n=38)12 (31.6)
Primary site of the cancer
  Lungs (n=49)5 (10.2)
  Other (n=99)22 (22.2)
  Breast, prostate, thyroid (n=43)18 (41.9)
Survival period
  <6 mo (n=101)13 (12.9)
  ≥6 mo (n=90)32 (35.6)
Pre-ASIA classification
  A (n=4)1 (25.0)
  B (n=26)5 (19.2)
  C (n=86)20 (23.3)
  D (n=75)19 (25.3)
Transverse location
  A (n=14)2 (14.3)
  AP (n=8)1 (12.5)
  AF (n=86)19 (22.1)
  AFP (n=83)23 (27.7)
ESCC scale
  1b (n=6)3 (50.0)
  1c (n=42)7 (16.7)
  2 (n=82)18 (22.2)
  3 (n=61)17 (27.9)
Type of treatment
  Surgery plus radiotherapy (n=146)44 (30.1)
  Radiotherapy without surgery (n=45)1 (2.2)

Factors Associated With the Posttreatment ASIA Classification

ParameterP
Age <70 y (n=141) vs ≥70 y (n=50).0366a
The level of the spine that exhibited the greatest tumor-related spinal cord compression C2-T2 (n=48) vs T3-L1 (n=105) vs L2-S1 (n=38)<.001a
Primary cancer site
  Lungs (n=49)
  Other (n=99)
  Breast, prostate, thyroid (n=43)<.001a
Survival period <6 mo (n=101) vs ≥6 mo (n=90).0372a
Pre-ASIA classification A (n=4) vs B (n=26) vs C (n=86) vs D (n=75)<.001a
Transverse location A (n=14) vs AP (n=8) vs AF (n=86) vs AFP (n=83).3166
ESCC scale 1b (n=6) vs 1c (n=42) vs 2 (n=82) vs 3 (n=61).0102a

Factors Associated With a Posttreatment Improvement in Paralysis of 1 or More ASIA Grades

ParameterP
Age <70 y (n=141) vs ≥70 y (n=50).0605
Spinal level that exhibited the greatest tumor-related spinal cord compression C2-T2 (n=48) vs T3-L1 (n=105) vs L2-S1 (n=38).0915
Primary cancer site
  Lungs (n=49)
  Other (n=99).0152a
  Breast/prostate/thyroid (n=43)
Survival period <6 mo (n=101) vs ≥6 mo (n=90).1523
Pre-ASIA classification A (n=4) vs B (n=26) vs C (n=86) vs D (n=75).6010
Transverse location A (n=14) vs AP (n=8) vs AF (n=86) vs AFP (n=83).5603
ESCC scale 1b (n=6) vs 1c (n=42) vs 2 (n=82) vs 3 (n=61).2334
Type of treatment surgery plus radiotherapy (n=146) vs radiotherapy without surgery (n=45)<.001a
Authors

The authors are from the Department of Orthopaedic Surgery, Nihon University School of Medicine, Tokyo, Japan.

The authors have no relevant financial relationships to disclose.

Correspondence should be addressed to: Yasuaki Tokuhashi, MD, Department of Orthopaedic Surgery, Nihon University School of Medicine, 30-1 Oyaguchi-kamicho, Itabashi-ku, Tokyo, 173-8610 Japan ( tokuhashi.yasuaki@nihon-u.ac.jp).

Received: August 10, 2019
Accepted: September 30, 2019
Posted Online: August 20, 2020

10.3928/01477447-20200812-09

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