Surgical approaches and long-term outcomes of intramedullary spinal cord cavernous malformations: a single-center consecutive series of 219 patients

Jian Ren Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Tao Hong Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Chuan He Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Xiaoyu Li Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Yongjie Ma Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Jiaxing Yu Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Feng Ling Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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Hongqi Zhang Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, China International Neuroscience Institute, Beijing, China

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OBJECTIVE

Optimal surgical strategies for intramedullary spinal cord cavernous malformations (ISCCMs) are not optimized and remain problematic. In this study the authors identify rational surgical strategies for ISCCMs and predictors of outcomes after resection.

METHODS

A single-center study was performed with 219 consecutive surgically treated patients who presented from 2002 to 2017 and were analyzed retrospectively. The American Spinal Injury Association (ASIA) Impairment Scale was used to evaluate neurological functions. Patient characteristics, surgical approaches, and immediate and long-term postoperative outcomes were identified.

RESULTS

The average ISCCM size was 10.5 mm. The spinal level affected was cervical in 24.8% of patients, thoracic in 73.4%, and lumbar in 1.8%. The locations of the lesions in the horizontal plane were 30.4% ventral, 41.6% dorsal, and 28.0% central. Of the 214 patients included in the cohort for operative evaluation, 62.6% had superficially located lesions, while 37.4% were embedded. Gross-total resection was achieved in 98.1% of patients. The immediate postoperative neurological condition worsened in 10.3% of the patients. Multivariate logistic regression identified mild preoperative function (p = 0.014, odds ratio [OR] 4.5, 95% confidence interval [CI] 1.4–14.8) and thoracolumbar-level lesions (p = 0.01, OR 15.7, 95% CI 1.9–130.2) as independent predictors of worsening. The mean follow-up duration in 187 patients was 45.9 months. Of these patients, 63.1% were stable, 33.2% improved, and 3.7% worsened. Favorable outcomes were observed in 86.1% of patients during long-term follow-up and were significantly associated with preoperative mild neurological and disability status (p = 0.000) and cervically located lesions (p = 0.009). The depths of the lesions were associated with worse long-term outcomes (p = 0.001), and performing myelotomy directly through a yellowish abnormal surface in moderate-depth lesions was an independent predictor of worsening (p = 0.023, OR 35.3, 95% CI 1.6–756.3).

CONCLUSIONS

Resection performed with an individualized surgical approach remains the primary therapeutic option in ISCCMs. Performing surgery in patients with mild symptoms at the thoracolumbar level and embedded located lesions requires more discretion.

ABBREVIATIONS

ADREZotomy = anterior to dorsal root entry zone myelotomy; ASIA = American Spinal Injury Association; CI = confidence interval; CM = cavernous malformation; DREZotomy = dorsal root entry zone myelotomy; ISCCM = intramedullary spinal cord CM; OR = odds ratio.

OBJECTIVE

Optimal surgical strategies for intramedullary spinal cord cavernous malformations (ISCCMs) are not optimized and remain problematic. In this study the authors identify rational surgical strategies for ISCCMs and predictors of outcomes after resection.

METHODS

A single-center study was performed with 219 consecutive surgically treated patients who presented from 2002 to 2017 and were analyzed retrospectively. The American Spinal Injury Association (ASIA) Impairment Scale was used to evaluate neurological functions. Patient characteristics, surgical approaches, and immediate and long-term postoperative outcomes were identified.

RESULTS

The average ISCCM size was 10.5 mm. The spinal level affected was cervical in 24.8% of patients, thoracic in 73.4%, and lumbar in 1.8%. The locations of the lesions in the horizontal plane were 30.4% ventral, 41.6% dorsal, and 28.0% central. Of the 214 patients included in the cohort for operative evaluation, 62.6% had superficially located lesions, while 37.4% were embedded. Gross-total resection was achieved in 98.1% of patients. The immediate postoperative neurological condition worsened in 10.3% of the patients. Multivariate logistic regression identified mild preoperative function (p = 0.014, odds ratio [OR] 4.5, 95% confidence interval [CI] 1.4–14.8) and thoracolumbar-level lesions (p = 0.01, OR 15.7, 95% CI 1.9–130.2) as independent predictors of worsening. The mean follow-up duration in 187 patients was 45.9 months. Of these patients, 63.1% were stable, 33.2% improved, and 3.7% worsened. Favorable outcomes were observed in 86.1% of patients during long-term follow-up and were significantly associated with preoperative mild neurological and disability status (p = 0.000) and cervically located lesions (p = 0.009). The depths of the lesions were associated with worse long-term outcomes (p = 0.001), and performing myelotomy directly through a yellowish abnormal surface in moderate-depth lesions was an independent predictor of worsening (p = 0.023, OR 35.3, 95% CI 1.6–756.3).

CONCLUSIONS

Resection performed with an individualized surgical approach remains the primary therapeutic option in ISCCMs. Performing surgery in patients with mild symptoms at the thoracolumbar level and embedded located lesions requires more discretion.

In Brief

The authors reviewed 219 consecutive surgically treated patients who presented with intramedullary spinal cord cavernous malformations (ISCCMs) at their institution to provide a more detailed analysis of the clinical and radiological characteristics, surgical indications, and optimal surgical approaches taken according to anatomical location and long-term outcomes observed in these patients. Resection performed with an individualized surgical approach remains the primary therapeutic option in ISCCMs. Performing surgery in patients with mild symptoms at the thoracolumbar level and embedded located lesions requires more discretion. This appears to be the largest single series of ISCCMs to be reported in the literature to date.

Cavernous malformations (CMs) constitute 5%–10% of the vascular malformations that occur in the CNS and mostly occupy the intracranial compartment.2,10 Intramedullary spinal cord CMs (ISCCMs) are very rare, constituting 5%–12% of all spinal vascular diseases.8 Compared with their intracranial counterparts, ISCCMs are more aggressive because the narrow spinal cavity contributes to a low tolerance for space-occupying lesions.3,4,10 Resection of the lesions remains the only treatment method for most symptomatic ISCCMs to eliminate the associated subsequent lifelong hemorrhagic risk.12,26 The clinical presentations, surgical management, and long-term outcomes of ISCCMs have been discussed in recent decades, especially in several large series.1–3,5–7,11,12,15,16,18,19,24,26 However, the indications for surgical management and the selection of surgical approaches available in ISCCMs remain unoptimized and problematic, especially in asymptomatic, transient, or minimally symptomatic patients with ventral or deeply located ISCCMs.12,13,15

We previously reported our initial experiences in 96 patients who harbored ISCCMs.12 In another article previously published by this institution, a new surgical approach, i.e., anterior to dorsal root entry zone myelotomy (ADREZotomy), was reported for use in ventrolateral deep ISCCMs.20 In this paper we review 219 consecutive surgically treated patients who presented with ISCCMs in our institution to provide a more detailed analysis of the clinical and radiological characteristics of, and surgical indications for, optimal surgical approaches taken according to anatomical location and long-term outcomes observed in these patients. This represents the largest series of ISCCMs reported in the literature to date.

Methods

Data pertaining to 219 patients with ISCCMs who were surgically treated between January 2002 and September 2017 were selected and retrospectively reviewed from combined prospectively maintained spinal vascular disease databases. Our institution is a referral medical center focused on the treatment of spinal vascular lesions. The patients’ clinical characteristics, MRI results, and follow-up outcomes were analyzed. The American Spinal Injury Association (ASIA) Impairment Scale was used to evaluate neurological and disability status, and scores were obtained pre- and postoperatively and during long-term follow-up. The local ethics board of our institution approved this study, which was performed in accordance with the ethical standards of the 1964 Declaration of Helsinki. Patient consent was obtained for all patients enrolled in this study.

Participants

A total of 219 patients harboring 222 ISCCMs who underwent surgical treatment by the senior authors between January 2002 and September 2017 were included. Patient ages ranged from 3 to 68 years old at the time of diagnosis (mean age 35.2 years old).

Definition of Variables

The clinical presentations were divided into five differing types observed in the 219 cases, based on the four types described in the Ogilvy classification:17 1) discretely occurring episodes exhibiting neurological decline with different degrees of recovery; 2) acute onset and rapidly declining symptoms and neurological status; 3) acute onset of mild symptoms with consequent progressive worsening lasting weeks to months; 4) acute onset of mild symptoms with subsequent stable asymptomatic, transient, or minimally symptomatic status lasting months; and 5) slowly progressive neurological decline. We defined the duration of symptoms as the time from the onset of symptoms until surgical treatment. Severe neurological and disability status was defined as a grade on the ASIA scale from A to C, and mild neurological and disability status was defined as a grade on the ASIA scale of D or E.

The sizes of the ISCCMs were calculated as the maximum transverse diameter measured on preoperative T1-weighted MR images. The spinal level of the ISCCMs was designated cervical, thoracic, or lumbar. The locations of the ISCCMs in the horizontal plane were defined as ventral, central, or dorsal with reference to the midline and dentate ligament planes. All images were reviewed by independent neuroradiologists. The ISCCMs were divided into 3 groups according to the depth of the lesions: superficial, moderate, and deep. Superficially located lesions reached the pial surface, apparently protruded, and were purple or stained dark red; lesions with moderate depth were mildly protruded and stained light yellow; and a smooth spinal cord surface and normal color indicated deep lesions. Lesions of moderate and deep depth were categorized as embedded lesions. The division between superficial and embedded was determined based on intraoperative findings because of the poor accuracy of MRI for predicting whether an ISCCM abuts the pial surface.3,22,23

Individualized Surgical Approach

Surgical approaches were planned and performed on a case-by-case basis after considering the proximity of the ISCCM to the pial surface, its location in the horizontal plane, and preoperative neurological symptoms.

For superficial lesions, myelotomy was performed through the abnormal surface. Approaches across the safe entry zone (i.e., trans safe entry zone) were used for embedded lesions. For dorsally or centrally located deep lesions, a traditional posterior midline myelotomy was performed through the dorsal median sulcus.15 For ventrolaterally located deep lesions, a new surgical approach called the ADREZotomy was performed at our institution.20 Lateral myelotomy between the ventral and dorsal nerve roots and dorsal root entry zone myelotomy (DREZotomy, equivalent to the posterolateral sulcus approach) were performed only in select patients due to the relatively high risk of worsened neurological conditions (Fig. 1).6,15

FIG. 1.
FIG. 1.

Surgical approaches used in ISCCMs through safe entry zones. A: Surgical approach for dorsally located ISCCMs. Preoperative MRI indicated dorsally located ISCCMs. Intraoperative photographs show the myelotomy performed through the posterior midline. Illustration showing posterior midline myelotomy for dorsal/central lesions, with an arrow indicating the approach to posterior lesions through the dorsal median sulcus. B: Surgical approach for posterolateral ISCCMs. Preoperative MRI indicated posterolateral ISCCMs. Intraoperative photographs show the DREZotomy. Illustration show the approach used in posterolateral lesions through the substantia gelatinosa and the posterolateral tract of Lissauer (arrow). C: Lateral approach for lateral ISCCMs. Preoperative MRI indicated lateral ISCCMs. Intraoperative photographs and illustration show the lateral myelotomy performed between the ventral and dorsal nerve roots on the ventral side of the dentate ligament (arrow). D: ADREZotomy for ventrolateral ISCCMs. Preoperative MRI indicated ventrolateral ISCCMs. The spinal cord was entered between the dorsolateral tract and the dorsal spinocerebellar tracts, anterior to the lateral fasciculus proprius of the spinal cord and posterior to the lateral corticospinal tract. Artwork is published with the permission of the artist, Jian Ren. Figure is available in color online only.

Postoperative Evaluation and Follow-Up Outcomes

Immediate postoperative outcomes were evaluated before patient discharge. Long-term follow-up was defined as a last follow-up duration at least 6 months after surgery.2 We defined a favorable outcome at follow-up as an ASIA grade of D or E and defined improvement or worsening as a change by at least one grade compared to the preoperative baseline score on the ASIA scale.19

Statistical Analysis

We used the Fisher’s exact test or Pearson’s chi-square test (with or without Yates continuity correction) for categorical variables and the Student t-test for continuous variables to evaluate differences in clinical variables and outcomes. Logistic regression analysis was used to assess the impact of multiple variables on binary ASIA scale outcomes (worsened vs improved or stable). Odds ratios (ORs) and 95% confidence intervals (CIs) are presented for findings in multivariate logistic regression analyses. All analyses were performed under the guidance of an epidemiologist using SPSS software (version 25, IBM Corp.). All p values were 2-sided, and we considered statistical significance as a value of p < 0.05.

Results

A total of 219 patients harboring 222 ISCCMs were enrolled in the review of clinical charts and neuroimaging (Supplemental Digital Content). Finally, 214 patients were included in the cohort of operative evaluations (5 patients were excluded due to incomplete data). Microsurgical resections were performed in 216 lesions in these 214 patients. Follow-up evaluations were performed in 187 patients (87.4%; 27 patients were excluded due to loss to follow-up).

Patient Characteristics

The study included 125 males and 94 females (ratio 1.33 to 1) with a mean age of 35.2 years. Twenty-three were pediatric patients (< 18 years of age). Of the 222 lesions, the spinal level was cervical in 55 patients (24.8%), thoracic in 163 (73.4%), and lumbar in 4 (1.8%). Eight patients (3.7%) harbored multiple CM lesions, including two with 2 or more ISCCMs. Associated cerebral CMs occurred in 6 patients. Two patients (0.9%) had associated cutaneous CMs.

We identified 242 symptomatic hemorrhage events in 8017 patient-years of life, and we retrospectively calculated the annual symptomatic hemorrhage rate as 3.0%/patient/year. The demographic and other characteristics of the 219 included patients are summarized in Table 1.

TABLE 1.

Demographic and clinical characteristics of 219 patients with ISCCMs

VariableValue
Age, yrs
 Range3–68
 Mean ± SD35.2 ± 1.0
Sex, n (%)
 Male125 (57.1)
 Female94 (42.9)
Duration of symptoms, mos
 Range0–312
 Mean ± SD20.1 ± 2.7
Symptoms, n (%)
 Pain124 (56.6)
 Weakness186 (84.9)
 Sensory deficits212 (96.8)
 Bowel/bladder dysfunction138 (63.0)
 Other symptoms9 (4.1)
Type of symptoms/modified Ogilvy grade, n (%)
 I (discrete, acute)55 (25.1)
 II (acute, rapid)50 (22.8)
 III (acute, gradual)39 (17.8)
 IV (stable)58 (26.5)
 V (slow, progressive)17 (7.8)
Preop neurological function/ASIA scale, n (%)
 A18 (8.2)
 B20 (9.1)
 C39 (17.8)
 D130 (59.3)
 E12 (5.5)

Surgical Approaches

Of the 214 patients who were included in the cohort for operative evaluation, 134 (62.6%) had superficially located lesions, and 80 (37.4%) had embedded lesions (27 were of moderate depth and 53 were deep; Table 2). The locations of the lesions in the horizontal plane were ventral in 65 patients (30.4%), dorsal in 89 patients (41.6%), and central in 60 patients (28.0%). The mean size of the lesions was 10.5 mm ± 6.7 mm (range 3.0–55.0 mm).

TABLE 2.

Comparison of baseline and immediate postoperative outcomes in 214 patients undergoing resection

Univariate ModelMultivariate Model
VariableNo. of PtsImproved or StableWorsenedχ2p ValueOR (95% Cl)p Value
Sex2.7540.097
 Male1231149Ref
 Female9178132.042 (0.766–5.448)0.154
Age, yrs0.5540.758
 <1823212Ref
 18–49151134170.809 (0.156–4.201)0.801
 ≥50403730.547 (0.076–3.932)0.549
Preop function2.7690.096
 Severe73694Ref
 Mild141123184.472 (1.355–14.761)0.014
Spinal level4.5790.032
 Cervical55541Ref
 Thoracolumbar1591382115.704 (1.894–130.207)0.011
Maximum lesion size, mm0.0200.886
 ≤10.014312815Ref
 >10.0716471.296 (0.447–3.757)0.633
Lesion depth2.6720.263
 Superficial13412311Ref
 Moderate272253.556 (0.926–13.654)0.065
 Deep534762.331 (0.724–7.503)0.156
Locations in the horizontal plane0.4560.796
 Ventral65587Ref
 Dorsal898180.454 (0.143–1.442)0.180
 Central605460.693 (0.200–2.405)0.563

Pts = patients; ref = reference.

Boldface type indicates statistical significance.

In the 134 superficial cases, a myelotomy was performed through the abnormal surface in 119 cases. The other 15 superficial cases were treated using a trans safe entry zone approach according to the location of the lesions. For ventral superficial lesions, a slight rotation of the spinal cord was needed to achieve better visualization of the myelotomy.

Of the 27 moderate-depth cases, 9 cases were treated via a trans safe entry zone approach. The other 18 cases were treated directly through the yellowish abnormal surface. In all 53 deep cases, surgery was performed via a trans safe entry zone approach according to the location of the lesions. The surgical approaches are summarized according to the location and depth of the lesions in the Supplemental Digital Content.

Postoperative Outcomes and Prognostic Factors

Immediate Postoperative Outcomes

Of the 214 patients, gross-total resection was achieved in 210 (98.1%). Subtotal resection was performed in 4 patients in whom there was a blurred demarcation between the diffused lesions and the surrounding tissues after total resection was deemed unsafe.

Immediately after surgery, the neurological condition was worse in 22 patients (10.3%). Preoperative parameters were analyzed separately using univariate and multivariate analyses to determine predictors of immediate worse outcomes after ISCCM surgery. Spinal level was associated with worse immediate postoperative outcomes, with thoracolumbar-level lesions associated with a statistically significant increase in the likelihood of worse immediate postoperative outcomes (p = 0.032). In the multivariate analysis, mild preoperative function was a significant predictor of worse immediate postoperative status (p = 0.014, OR = 4.472, 95% CI 1.355–14.761). Thoracolumbar-level lesion was also a significant predictor of worse immediate postoperative outcomes in the multivariate analysis (p = 0.011, OR = 15.704, 95% CI 1.894–130.207; Table 2). We found no evidence, even after multivariable adjustment for the other predictors, that sex, age, lesion size, lesion depth, or location of the lesion in the horizontal plane affected immediate postoperative status. Other complications were wound infection in 1 patient, breakage of a drainage tube in 1 patient, and CSF leak in 2 patients.

Long-Term Follow-Up Outcomes

One hundred eighty-seven patients were included in the evaluation of long-term follow-up data with follow-up times ranging from 6 to 164 months. The mean follow-up duration was 45.9 ± 34.9 months. Compared with preoperative neurological status, the postoperative outcomes demonstrated that 118 patients (63.1%) were stable, 62 (33.2%) improved, and 7 (3.7%) worsened (Fig. 2). Favorable outcomes were observed in 161 patients (86.1%) and were significantly associated with preoperative mild neurological and disability status (p = 0.000) and cervically located lesions (p = 0.009). Two patients (1.1%) experienced recurrence of the lesions during the follow-up and underwent reoperation.

FIG. 2.
FIG. 2.

ASIA scale grades (A–E) at admission, immediately postoperative, and at the final follow-up clinical evaluation in 187 patients. Figure is available in color online only.

In the univariate and multivariate analyses, lesion depth was significantly associated with worse long-term outcomes (p = 0.001), while moderate-depth lesions (embedded lesions) were associated with a significant increase in the likelihood of worse long-term follow-up outcomes (p = 0.002, OR 47.566, 95% CI 4.070–555.936; Table 3). We found no evidence, even after multivariable adjustment for the other predictors, that sex, preoperative function, spinal level, lesion size, or the location of the lesion in the horizontal plane affected worsening during long-term follow-up.

TABLE 3.

Comparison of baseline and follow-up outcomes in 187 patients undergoing resection

Univariate ModelMultivariate Model
VariableNo. of PtsImproved or StableWorsenedχ2p ValueOR (95% Cl)p Value
Sex0.1710.679
 Male1061024Ref
 Female817920.384 (0.058–2.541)0.321
Preop function0.428*
 Mild1251196Ref
 Severe626200.142 (0.014–1.428)0.098
Lesion location0.1050.746
 Cervical50491Ref
 Thoracolumbar13713253.618 (0.337–38.802)0.288
Maximum lesion size, mm0.0001.000
 ≤10.01211174Ref
 >10.0666421.449 (0.188–11.203)0.772
Lesion depth14.5860.001
 Superficial1161151Ref
 Moderate depth2319447.566 (4.070–555.936)0.002
 Deep484627.419 (0.608–90.540)0.116
Locations in the horizontal plane0.8450.656
 Ventral58562Ref
 Dorsal767330.579 (0.081–4.155)0.587
 Central535210.418 (0.034–5.091)0.494

Boldface type indicates statistical significance.

Fisher’s exact test.

A univariate analysis in which baseline and follow-up outcomes were compared between patients with superficial and embedded ISCCMs (Table 4) demonstrated that patients with embedded lesions had a significantly shorter duration of symptoms (p = 0.003), smaller-sized lesions (p = 0.007), and worse long-term outcomes (p = 0.024).

TABLE 4.

Baseline and follow-up outcome between patients with superficial and embedded ISCCMs

VariableOverallSuperficial GroupEmbedded Groupχ2/t Scorep Value
No. of pts18711671
Females, n (%)81 (43.3)47 (40.5)34 (47.9)0.9740.324
Mean age ± SD, yrs35.9 ± 14.436.3 ± 14.235.3 ± 14.70.4930.623
Mean duration of symptoms ± SD, mos20.0 ± 38.625.5 ± 45.811.1 ± 19.42.9830.003
Mean lesion size ± SD, cm1.1 ± 0.71.2 ± 0.80.9 ± 0.52.7080.007
No. of pts w/ preop serious deficit, n (%)62 (33.1)36 (31.0)26 (36.6)0.6200.431
Location, n2.9160.088
 Cervical502624
 Thoracolumbar1379047
Side, %0.8080.668
 Ventral583523
 Dorsal765026
 Central533122
Mean FU duration ± SD, mos45.9 ± 34.948.0 ± 33.742.5 ± 36.71.0410.299
No. of pts w/ worsened ASIA grade
 At discharge201190.4700.493
 At FU7165.0910.024
No. of pts w/ FU serious deficit, %2613 (11.2)13 (18.3)1.8560.173

FU = follow-up.

Boldface type indicates statistical significance.

Considering the worse outcomes observed in patients with embedded-depth lesions, especially those with moderate-depth lesions, in our cohort we used a multivariate binary logistic regression to determine predictors of worse long-term follow-up outcomes in the 71 patients with embedded deep lesions. We found that for embedded deep lesions, the surgical approach to the lesion was associated with worse long-term outcomes, with myelotomy performed directly through the yellowish abnormal surface of a moderate-depth lesion associated with a significant increase in the likelihood of worse long-term follow-up outcomes (p = 0.023, OR 35.311, 95% CI 1.649–756.321; Table 5).

TABLE 5.

Surgical approach and follow-up outcome between patients with embedded-depth (deep and moderate-depth) ISCCMs

Multivariate Model
VariableNo. of PtsImproved or StableWorsenedOR (95% Cl)p Value
Sex
 Male37325Ref
 Female343310.046 (0.002–1.298)0.071
Preop function
 Mild45405Ref
 Severe262510.064 (0.003–1.199)0.066
Location
 Cervical24231Ref
 Thoracolumbar4742523.789 (0.932–607.284)0.055
Approach to lesion
 Safe entry zone57543Ref
 Directly through abnormal surface1411335.311 (1.649–756.321)0.023

Boldface type indicates statistical significance.

Discussion

To the best of our knowledge, this is the largest single series of ISCCMs to be reported in the literature thus far. We found that the annual hemorrhage rate in symptomatic ISCCMs was 3.0%/patient/year. The worsening rate immediately after surgery was 10.3%. Mild preoperative function and thoracolumbar-level lesions were independently associated with a statistically significant increase in the likelihood of worse immediate postoperative outcomes. Favorable outcomes were observed in 86.1% of patients during long-term follow-up and were significantly associated with preoperative mild neurological and disability status (p = 0.000) and cervically located lesions (p = 0.009). The worsening rate decreased from 10.3% immediately postoperatively to 3.7% after long-term follow-up and was associated with the depth of the lesion; myelotomy performed directly through the yellowish abnormal surface of moderate-depth lesions (embedded lesions) was associated with a significant increase in the likelihood of worse long-term follow-up outcomes (Fig. 3). However, age, sex, lesion size, and the location of the lesion in the horizontal plane did not contribute any additional prognostic information.

FIG. 3.
FIG. 3.

Images obtained in a 38-year-old woman who presented with transient pain in the back. Preoperative MRI (A and B) indicated thoracic ISCCMs dorsally located at the T7 vertebral level. The ASIA scale grade was E (normal). Intraoperative photographs (C and D) show the surgical procedures. A slightly yellowish abnormal surface was noticed at the left dorsal column (arrow). A myelotomy was performed through the abnormal surface. Gross-total resection was achieved. Immediately after surgery, the patient complained of a new symptom of numbness of the left lower extremity. The ASIA scale grade was D. During the follow-up of 12 years, the patient’s neurological function remained unchanged with numbness of the left lower extremity. This case highlights that myelotomy directly through the yellowish abnormal surface of the moderate-depth lesions may cause irreversible worsening after surgery and a myelotomy trans safe entry zone is still the first choice. Figure is available in color online only.

Treatment Strategies

The natural history of ISCCMs remains uncertain and varying. Patients with ISCCMs are a heterogeneous group of patients.9 Considering its unpredictable natural history and the fact that more aggressive symptoms are observed in ISCCMs due to the narrow spinal cavity, which contributes to a low tolerance for space-occupying lesions and a lifelong hemorrhage risk, the treatment strategies for ISCCMs are more proactive. Resection is the mainstay and definitive treatment method and can provide good outcomes.2,3,5,6,12,14,16,19,24,26 In our institution, all patients with symptomatic ISCCM, even those with transient or minimally symptomatic status, undergo resection as the optimal treatment. Of the 219 surgically treated patients, 142 (64.8%) presented with mild symptoms before surgery.

In the literature, the rate of transient worsening of neurological functions after surgery has ranged from 11% to 50%.2,7,16,22 In our operative evaluation cohort of 214 patients, 22 patients (10.3%) worsened during the immediate postoperative period, indicating a rate slightly lower than that reported in the literature. We found that mild preoperative function and thoracolumbar-level lesions were independently associated with a statistically significant increase in the likelihood of worse immediate postoperative outcomes. These findings emphasize that discretion should be used in the surgical management of asymptomatic, transient, or minimally symptomatic status patients with thoracolumbar-level located lesions.

In a retrospective review of conservatively treated ISCCMs performed by Zhang et al., 14.8% (4/27) of the patients worsened during a mean follow-up duration of 33.9 months.26 In a systematic review and meta-analysis reported in the literature by Badhiwala et al., 64 patients with ISCCM were conservatively treated, and 11.3% of these patients exhibited worse functions after follow-up than at initial presentation.3 In our series of surgically treated ISCCMs, favorable outcomes were observed in 161 patients (86.1%), and only 7 patients (3.7%) worsened during long-term follow-up. A comparison of our results with other groups of conservatively managed patients indicates that it appears reasonable to conclude that surgery is a better treatment option. In our experience, only when the patients are asymptomatic and stable with no overt hemorrhage events should they be conservatively managed. However, in terms of baseline imbalances, future studies should investigate and compare the effects of surgical treatment to conservative management using a prospective design and randomization and take into account those factors known to influence outcomes.

Surgical Approaches

Differences in the locations of ISCCMs and their preoperative symptoms support the importance of taking an individualized surgical approach. Surgical approaches were planned and performed on a case-by-case basis after considering the proximity of the ISCCM to the pial surface, its location in the horizontal plane, and preoperative neurological symptoms. The locations of the lesions were identified by the preoperative MRI and intraoperative ultrasound imaging, which were very useful for the deep lesions.

Superficial Lesions

To traverse the least amount of spinal cord tissue, a myelotomy is usually incised directly over superficial lesions. For ISCCMs, the definitions of superficial lesions provided in previous studies have been inaccurate. It is commonly recognized that superficial lesions reach the pial surface and are apparently prominent, purple, or dark red, while lesions with moderate depth are mildly protruded and stained light yellow, which have also been regarded as superficial lesions previously. However, mildly protruded lesions that are stained light yellow should be treated as embedded lesions and treated via a trans safe entry zone approach because the yellowish surface most likely contains normal spinal cord tissue. In a long-term follow-up of 187 cases, we found that the depths of the lesions were associated with worse long-term outcomes and that performing myelotomy directly through the yellowish abnormal surface of a moderate-depth lesion (embedded lesions) resulted in a significant increase in the likelihood of worse long-term follow-up outcomes.

Dorsal or Central Deep Lesions

With regard to a trans safe entry zone approach for embedded lesions, in our experience, a traditional posterior midline myelotomy is appropriate for dorsal or central deep lesions, especially when the patient already exhibited dorsal column dysfunctions before surgery. The main drawback of posterior midline myelotomy is the risk of inadvertent dissection through the dorsal columns, which can worsen proprioception after surgery. This is usually caused by the distortion of the midline raphe, which is difficult to identify based on surface anatomy (Fig. 1A).25

Dorsolateral Deep Lesions

DREZotomy is best for dorsolateral deep lesions and is associated with moderate or severe local pain.21 While DREZotomy requires the dissection of the substantia gelatinosa and the posterolateral tract of Lissauer, it often causes postoperative worsening of superficial sensation in the distribution of the nerve that emerges from that entry zone (Fig. 1B).6

Ventrolateral Deep Lesions

For lateral or ventrolateral deep lesions, a lateral myelotomy can be performed between the ventral and dorsal nerve roots at a location ventral to the dentate ligament; this approach requires more liberal lateral bone removal while the spinal cord is rotated to optimize exposure and poses both technical challenges and surgical risks due to its close association with the lateral corticospinal and spinothalamic tracts (Fig. 1C).15,16,20 The traditional posterior midline myelotomy would require a deep myelotomy and involvement of the posterior column tracts, which may cause postoperative dorsal column dysfunction. DREZotomy requires dissection of the substantia gelatinosa and the posterolateral tract of Lissauer, often associated with postoperative paresthesias and dysesthesias in the distribution of the nerve emerging from that entry zone. ADREZotomy, which we previously described, is best for ventrolateral embedded lesions; this new surgical safe entry zone adds more options for surgeons who may be reluctant to decide on an approach for ventral deep ISCCMs.20 The spinal cord was entered between the dorsolateral tract and the dorsal spinocerebellar tracts, anterior to the lateral fasciculus proprius of the spinal cord and posterior to the lateral corticospinal tract. This surgical corridor can provide satisfactory exposure for ventrolateral and deeply located lesions without disrupting the important spinal cord tracts or the need to rotate the spinal cord or broadly expose bone (Fig. 1D).20

The main limitation of this study was its lack of a prospective design and randomization because of the rare occurrence of ISCCMs. However, the results of this large single-center consecutive series of rare but fairly aggressive lesions support the notion that complete resection of ISCCMs with an individualized surgical approach remains the primary therapeutic option to prevent further neurological decline.

Conclusions

Resection remains the primary therapeutic option in ISCCMs and can provide good outcomes. Surgical management of asymptomatic, transient, or minimally symptomatic status patients with thoracolumbar-level lesions requires more discretion. An individualized surgical approach is indispensable for every patient, and even a moderate-depth lesion with a yellowish protruding surface requires a myelotomy performed in a trans safe entry zone.

Acknowledgments

The authors would like to thank Qingling Gao and Xiaodong Zhai for their kind support with the data collection. This work was supported by the National Natural Science Foundation of China (grant nos. 81171165 and 81671202), the Beijing Municipal Administration of Hospital Clinical Medicine Development Project (grant no. ZY201309), the Beijing Municipal Administration of Hospitals’ Ascent Plan (grant no. DFL20180801), and the Beijing Municipal Science and Technology Commission (grant no. D161100003816001).

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Zhang. Acquisition of data: Ren, Ma, Yu. Analysis and interpretation of data: Ren, Hong, He, Li. Drafting the article: Ren, Hong. Critically revising the article: Zhang. Reviewed submitted version of manuscript: Zhang. Approved the final version of the manuscript on behalf of all authors: Zhang. Statistical analysis: Li, Yu. Administrative/technical/material support: He, Ma, Ling. Study supervision: Zhang.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article.

References

  • 1

    Anson JA, Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations. J Neurosurg 78:446451, 1993

  • 2

    Azad TD, Veeravagu A, Li A, Zhang M, Madhugiri V, Steinberg GK: Long-term effectiveness of gross-total resection for symptomatic spinal cord cavernous malformations. Neurosurgery 83:12011208, 2018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Badhiwala JH, Farrokhyar F, Alhazzani W, Yarascavitch B, Aref M, Algird A, et al.: Surgical outcomes and natural history of intramedullary spinal cord cavernous malformations: a single-center series and meta-analysis of individual patient data: clinic article. J Neurosurg Spine 21:662676, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Cantu C, Murillo-Bonilla L, Arauz A, Higuera J, Padilla J, Barinagarrementeria F: Predictive factors for intracerebral hemorrhage in patients with cavernous angiomas. Neurol Res 27:314318, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Choi GH, Kim KN, Lee S, Ji GY, Oh JK, Kim TY, et al.: The clinical features and surgical outcomes of patients with intramedullary spinal cord cavernous malformations. Acta Neurochir (Wien) 153:16771685, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Gross BA, Du R, Popp AJ, Day AL: Intramedullary spinal cord cavernous malformations. Neurosurg Focus 29(3):E14, 2010

  • 7

    Jallo GI, Freed D, Zareck M, Epstein F, Kothbauer KF: Clinical presentation and optimal management for intramedullary cavernous malformations. Neurosurg Focus 21(1):e10, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Jellinger K: Vascular malformations of the central nervous system: a morphological overview. Neurosurg Rev 9:177216, 1986

  • 9

    Kharkar S, Shuck J, Conway J, Rigamonti D: The natural history of conservatively managed symptomatic intramedullary spinal cord cavernomas. Neurosurgery 60:865872, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kivelev J, Laakso A, Niemelä M, Hernesniemi J: A proposed grading system of brain and spinal cavernomas. Neurosurgery 69:807814, 2011

  • 11

    Labauge P, Bouly S, Parker F, Gallas S, Emery E, Loiseau H, et al.: Outcome in 53 patients with spinal cord cavernomas. Surg Neurol 70:176181, 2008

  • 12

    Liang JT, Bao YH, Zhang HQ, Huo LR, Wang ZY, Ling F: Management and prognosis of symptomatic patients with intramedullary spinal cord cavernoma: clinical article. J Neurosurg Spine 15:447456, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Martin NA, Khanna RK, Batzdorf U: Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 83:254261, 1995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Maslehaty H, Barth H, Petridis AK, Doukas A, Mehdorn HM: Symptomatic spinal cavernous malformations: indication for microsurgical treatment and outcome. Eur Spine J 20:17651770, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Mitha AP, Turner JD, Abla AA, Vishteh AG, Spetzler RF: Outcomes following resection of intramedullary spinal cord cavernous malformations: a 25-year experience. J Neurosurg Spine 14:605611, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Mitha AP, Turner JD, Spetzler RF: Surgical approaches to intramedullary cavernous malformations of the spinal cord. Neurosurgery 68:317324, 2011

  • 17

    Ogilvy CS, Louis DN, Ojemann RG: Intramedullary cavernous angiomas of the spinal cord: clinical presentation, pathological features, and surgical management. Neurosurgery 31:219230, 1992

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Park SB, Jahng TA, Chung CK: The clinical outcomes after complete surgical resection of intramedullary cavernous angiomas: changes in motor and sensory symptoms. Spinal Cord 47:128133, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Reitz M, Burkhardt T, Vettorazzi E, Raimund F, Fritzsche E, Schmidt NO, et al.: Intramedullary spinal cavernoma: clinical presentation, microsurgical approach, and long-term outcome in a cohort of 48 patients. Neurosurg Focus 39(2):E19, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ren J, He C, Hong T, Li X, Ma Y, Yu J, et al.: Anterior to dorsal root entry zone myelotomy (ADREZotomy): a new surgical approach for the treatment of ventrolateral deep intramedullary spinal cord cavernous malformations. Spine (Phila Pa 1976) 43:E1024E1032, 2018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Takami T, Naito K, Yamagata T, Kawahara S, Ohata K: Surgical outcomes of posterolateral sulcus approach for spinal intramedullary tumors: tumor resection and functional preservation. World Neurosurg 108:1523, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Vishteh AG, Sankhla S, Anson JA, Zabramski JM, Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations: delayed complications, long-term outcomes, and association with cryptic venous malformations. Neurosurgery 41:10941101, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Weinzierl MR, Krings T, Korinth MC, Reinges MH, Gilsbach JM: MRI and intraoperative findings in cavernous haemangiomas of the spinal cord. Neuroradiology 46:6571, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Tong X, Deng X, Li H, Fu Z, Xu Y: Clinical presentation and surgical outcome of intramedullary spinal cord cavernous malformations. J Neurosurg Spine 16:308314, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Yanni DS, Ulkatan S, Deletis V, Barrenechea IJ, Sen C, Perin NI: Utility of neurophysiological monitoring using dorsal column mapping in intramedullary spinal cord surgery. J Neurosurg Spine 12:623628, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Zhang L, Yang W, Jia W, Kong D, Yang J, Wang G, et al.: Comparison of outcome between surgical and conservative management of symptomatic spinal cord cavernous malformations. Neurosurgery 78:552561, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • FIG. 1.

    Surgical approaches used in ISCCMs through safe entry zones. A: Surgical approach for dorsally located ISCCMs. Preoperative MRI indicated dorsally located ISCCMs. Intraoperative photographs show the myelotomy performed through the posterior midline. Illustration showing posterior midline myelotomy for dorsal/central lesions, with an arrow indicating the approach to posterior lesions through the dorsal median sulcus. B: Surgical approach for posterolateral ISCCMs. Preoperative MRI indicated posterolateral ISCCMs. Intraoperative photographs show the DREZotomy. Illustration show the approach used in posterolateral lesions through the substantia gelatinosa and the posterolateral tract of Lissauer (arrow). C: Lateral approach for lateral ISCCMs. Preoperative MRI indicated lateral ISCCMs. Intraoperative photographs and illustration show the lateral myelotomy performed between the ventral and dorsal nerve roots on the ventral side of the dentate ligament (arrow). D: ADREZotomy for ventrolateral ISCCMs. Preoperative MRI indicated ventrolateral ISCCMs. The spinal cord was entered between the dorsolateral tract and the dorsal spinocerebellar tracts, anterior to the lateral fasciculus proprius of the spinal cord and posterior to the lateral corticospinal tract. Artwork is published with the permission of the artist, Jian Ren. Figure is available in color online only.

  • FIG. 2.

    ASIA scale grades (A–E) at admission, immediately postoperative, and at the final follow-up clinical evaluation in 187 patients. Figure is available in color online only.

  • FIG. 3.

    Images obtained in a 38-year-old woman who presented with transient pain in the back. Preoperative MRI (A and B) indicated thoracic ISCCMs dorsally located at the T7 vertebral level. The ASIA scale grade was E (normal). Intraoperative photographs (C and D) show the surgical procedures. A slightly yellowish abnormal surface was noticed at the left dorsal column (arrow). A myelotomy was performed through the abnormal surface. Gross-total resection was achieved. Immediately after surgery, the patient complained of a new symptom of numbness of the left lower extremity. The ASIA scale grade was D. During the follow-up of 12 years, the patient’s neurological function remained unchanged with numbness of the left lower extremity. This case highlights that myelotomy directly through the yellowish abnormal surface of the moderate-depth lesions may cause irreversible worsening after surgery and a myelotomy trans safe entry zone is still the first choice. Figure is available in color online only.

  • 1

    Anson JA, Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations. J Neurosurg 78:446451, 1993

  • 2

    Azad TD, Veeravagu A, Li A, Zhang M, Madhugiri V, Steinberg GK: Long-term effectiveness of gross-total resection for symptomatic spinal cord cavernous malformations. Neurosurgery 83:12011208, 2018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Badhiwala JH, Farrokhyar F, Alhazzani W, Yarascavitch B, Aref M, Algird A, et al.: Surgical outcomes and natural history of intramedullary spinal cord cavernous malformations: a single-center series and meta-analysis of individual patient data: clinic article. J Neurosurg Spine 21:662676, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Cantu C, Murillo-Bonilla L, Arauz A, Higuera J, Padilla J, Barinagarrementeria F: Predictive factors for intracerebral hemorrhage in patients with cavernous angiomas. Neurol Res 27:314318, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Choi GH, Kim KN, Lee S, Ji GY, Oh JK, Kim TY, et al.: The clinical features and surgical outcomes of patients with intramedullary spinal cord cavernous malformations. Acta Neurochir (Wien) 153:16771685, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Gross BA, Du R, Popp AJ, Day AL: Intramedullary spinal cord cavernous malformations. Neurosurg Focus 29(3):E14, 2010

  • 7

    Jallo GI, Freed D, Zareck M, Epstein F, Kothbauer KF: Clinical presentation and optimal management for intramedullary cavernous malformations. Neurosurg Focus 21(1):e10, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Jellinger K: Vascular malformations of the central nervous system: a morphological overview. Neurosurg Rev 9:177216, 1986

  • 9

    Kharkar S, Shuck J, Conway J, Rigamonti D: The natural history of conservatively managed symptomatic intramedullary spinal cord cavernomas. Neurosurgery 60:865872, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kivelev J, Laakso A, Niemelä M, Hernesniemi J: A proposed grading system of brain and spinal cavernomas. Neurosurgery 69:807814, 2011

  • 11

    Labauge P, Bouly S, Parker F, Gallas S, Emery E, Loiseau H, et al.: Outcome in 53 patients with spinal cord cavernomas. Surg Neurol 70:176181, 2008

  • 12

    Liang JT, Bao YH, Zhang HQ, Huo LR, Wang ZY, Ling F: Management and prognosis of symptomatic patients with intramedullary spinal cord cavernoma: clinical article. J Neurosurg Spine 15:447456, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Martin NA, Khanna RK, Batzdorf U: Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 83:254261, 1995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Maslehaty H, Barth H, Petridis AK, Doukas A, Mehdorn HM: Symptomatic spinal cavernous malformations: indication for microsurgical treatment and outcome. Eur Spine J 20:17651770, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Mitha AP, Turner JD, Abla AA, Vishteh AG, Spetzler RF: Outcomes following resection of intramedullary spinal cord cavernous malformations: a 25-year experience. J Neurosurg Spine 14:605611, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Mitha AP, Turner JD, Spetzler RF: Surgical approaches to intramedullary cavernous malformations of the spinal cord. Neurosurgery 68:317324, 2011

  • 17

    Ogilvy CS, Louis DN, Ojemann RG: Intramedullary cavernous angiomas of the spinal cord: clinical presentation, pathological features, and surgical management. Neurosurgery 31:219230, 1992

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Park SB, Jahng TA, Chung CK: The clinical outcomes after complete surgical resection of intramedullary cavernous angiomas: changes in motor and sensory symptoms. Spinal Cord 47:128133, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Reitz M, Burkhardt T, Vettorazzi E, Raimund F, Fritzsche E, Schmidt NO, et al.: Intramedullary spinal cavernoma: clinical presentation, microsurgical approach, and long-term outcome in a cohort of 48 patients. Neurosurg Focus 39(2):E19, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ren J, He C, Hong T, Li X, Ma Y, Yu J, et al.: Anterior to dorsal root entry zone myelotomy (ADREZotomy): a new surgical approach for the treatment of ventrolateral deep intramedullary spinal cord cavernous malformations. Spine (Phila Pa 1976) 43:E1024E1032, 2018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Takami T, Naito K, Yamagata T, Kawahara S, Ohata K: Surgical outcomes of posterolateral sulcus approach for spinal intramedullary tumors: tumor resection and functional preservation. World Neurosurg 108:1523, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Vishteh AG, Sankhla S, Anson JA, Zabramski JM, Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations: delayed complications, long-term outcomes, and association with cryptic venous malformations. Neurosurgery 41:10941101, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Weinzierl MR, Krings T, Korinth MC, Reinges MH, Gilsbach JM: MRI and intraoperative findings in cavernous haemangiomas of the spinal cord. Neuroradiology 46:6571, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Tong X, Deng X, Li H, Fu Z, Xu Y: Clinical presentation and surgical outcome of intramedullary spinal cord cavernous malformations. J Neurosurg Spine 16:308314, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Yanni DS, Ulkatan S, Deletis V, Barrenechea IJ, Sen C, Perin NI: Utility of neurophysiological monitoring using dorsal column mapping in intramedullary spinal cord surgery. J Neurosurg Spine 12:623628, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Zhang L, Yang W, Jia W, Kong D, Yang J, Wang G, et al.: Comparison of outcome between surgical and conservative management of symptomatic spinal cord cavernous malformations. Neurosurgery 78:552561, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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