Multifidus Muscle Changes After Biportal Endoscopic Spinal Surgery: Magnetic Resonance Imaging Evaluation

Original Article

Multifidus Muscle Changes After Biportal Endoscopic Spinal Surgery: Magnetic Resonance Imaging Evaluation Jae-Sung Ahn1, Ho-Jin Lee1, Eugene J. Park1, Sang Bum Kim1, Dae-Jung Choi2, Youk-Sang Kwon3, Hyung-Jin Chung1

OBJECTIVE: We used magnetic resonance imaging (MRI) to assess the radiological status of the multifidus muscles (MFMs) after biportal endoscopic spinal surgery (BESS) and evaluated the extent of MFM injury and atrophy.

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METHODS: A total of 88 patients who had met the inclusion and exclusion criteria were enrolled in the present study. T2-weighted signal intensity MRI was performed 3 times: preoperatively, immediately postoperatively, and at the final follow-up examination. We measured the cross-sectional area of the MFM on both sides (ipsilaterally and contralaterally) and recorded the operative times. The association between the interval from surgery to the final follow-up MRI and changes in the MFMs and between the operative time and changes in the MFMs were analyzed. For the group comparisons, the patients were divided into 3 groups according to the follow-up interval. Group 1 was followed up within 2 weeks, group 2 within 2e4 weeks, and group 3 after 4 weeks. The MFM changes were recorded.

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RESULTS: The operative time correlated significantly with the percentage of change in the T2-weighted signal intensity ratio (SIR) for both sides (P < 0.01). At the final follow-up examination, the SIR of the ipsilateral side had decreased in group 3 (P [ 0.002). The percentage of change in the SIR was smallest in group 3 (P [ 0.004).

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CONCLUSIONS: The MFM change on MRI after BESS became significant on both sides as the operative time

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Key words Biportal endoscopic spinal surgery - Lumbar vertebrae - Magnetic resonance imaging - Minimally invasive spine surgery - Multifidus muscles -

Abbreviations and Acronyms BESS: Biportal endoscopic spinal surgery CSA: Cross-sectional area MFM: Multifidus muscle MILD: Muscle-preserving interlaminar decompression MRI: Magnetic resonance imaging ROI: Region of interest

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increased. However, the change showed a tendency to reverse within several months, and no substantial change in the MFM cross-sectional area was found. We have concluded that MFM changes after BESS might correlate with an increased operative time but will resolve over time.

INTRODUCTION

M

inimally invasive spinal surgery has many advantages compared with the traditional procedure, including reduced pain, shorter hospitalization, and rapid functional recovery1-4 owing to the preservation of the surrounding soft tissues.5-7 Such surgery has become popular worldwide, and many minimally invasive techniques that spare the dorsal rami and minimize approach-related morbidity have been developed. Minimally invasive surgery has achieved results comparable to those with traditional invasive approaches with less invasiveness.8 Minimally invasive spinal surgery using a microscope or endoscope has become very common.9-12 However, minimally invasive spinal surgery has several limitations, including the narrow view, steep learning curve, and specific technical issues.13-16 In particular, uniportal percutaneous endoscopic interlaminar decompression to treat degenerative lumbar stenosis has remained challenging, even for experienced surgeons.17,18 These have been major problems in traditional endoscopic surgery.13-16 Such surgery should be performed only by experienced

SIR: Signal intensity ratio VAS: Visual analog scale From the 1Department of Orthopaedic Surgery, Chungnam National University School of Medicine, Daejeon; 2Department of Orthopaedic Surgery, Himnaera Hospital, Busan; and 3 Department of Orthopedic Surgery, Daejeon Centum Hospital, Daejeon, South Korea To whom correspondence should be addressed: Ho-Jin Lee, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.148 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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endoscopic spine surgeons. The guidelines of the International Society for Minimal Intervention in Spinal Surgery have suggested that large central disc herniation should not be treated using traditional endoscopic surgery.19 Recently, many preliminary technical studies on biportal endoscopic spinal surgery (BESS) have been reported, using different names for the operation, and have shown that BESS can provide resolution to the reported issues.20-28 BESS can be used, not only for lumbar disc herniation, but also for degenerative lumbar stenosis, with many advantages. The technique is more accessible compared with the uniportal method because an independent working tube is used. Also, BESS does not require special endoscopic instruments and has excellent image quality.20-23,25 However, an issue exists related to the invasiveness of BESS,29 because the procedure uses 2 portals, and the soft tissues, including the muscles, ligaments, and fascia, between the 2 portals could be damaged during the creation of the operative field. Also, the saline irrigation applied throughout the entire procedure can damage the tissues around the paraspinal muscles to a greater extent than during conventional minimally invasive surgery. To access the invasiveness of BESS, we sought to determine the changes in the multifidus muscle (MFM) status after BESS. The MFMs are most vulnerable to injury during conventional open posterior spinal surgery because they are innervated only by the medial branch of the dorsal ramus, lacking an intersegmental nerve supply like the other paraspinal muscles. MFM injury and atrophy have been common after conventional open lumbar spine surgery and associated with low back pain, functional disability, and failed back surgery syndrome.1,30 Therefore, we used magnetic resonance imaging (MRI) to assess the radiological status of the MFMs and evaluated the extent of MFM injury and atrophy. MRI has been increasingly used for functional muscle imaging and provides high-quality information of soft tissue structures.31,32 A high T2-weighted signal intensity of the skeletal muscles can be observed in patients with a variety of conditions, including exertional muscle injury, necrosis, and inflammatory myopathies.33-35 A high T2-weighted signal intensity of the postoperative MFMs at the level of exposure has been correlated with the extent of MFM injury during surgery.36,37 The degree of MFM atrophy after surgery can be evaluated by measuring the MFM cross-sectional area (CSA) on axial MRI scans. We assessed 1) the association between the follow-up period after BESS and changes in MFM status on MRI; and 2) the correlation between the BESS operative time and the MFM status postoperatively. METHODS The present study featured retrospective case evaluation after institutional review board approval had been obtained. All the patients had provided written informed consent. Patient Selection From March 2015 to May 2017, we performed BESS for patients with a diagnosis of lumbar spinal stenosis or lumbar disc herniation combined with radicular leg pain or neurogenic claudication at our institution. A total of 88 patients who had met the inclusion and exclusion criteria (Table 1) were enrolled in the present study. The inclusion criteria were as follows: intolerable leg pain despite

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Table 1. Inclusion and Exclusion Criteria Criteria Inclusion Diagnosed with a central spinal canal lesion on MRI, correlating with neurogenic symptoms LDH LSS Underwent 1-level BESS using a unilateral interlaminar approach MRI performed 3 times using the same scanner Preoperatively Postoperatively (within 3 days after surgery) During follow-up Exclusion Segmental instability* Lytic spondylolisthesis BESS performed via an extraforaminal approach Coexisting pathological conditions Spinal infection Spinal tumor Performance of BESS at >2 levels Previous lumbar surgery LDH, lumbar disc herniation; LSS, lumbar spinal stenosis; BESS, biportal endoscopic spinal surgery; MRI, magnetic resonance imaging. *More than 4.5 mm of translation or 15
of angulation between adjacent segments 38 evident on flexioneextension radiographs.

>3 months of conservative treatment (including nonsteroidal antiinflammatory medications, physical therapy, and selective nerve root blocks) and single-level central spinal canal lesions confirmed by MRI with correlating neurogenic symptoms, including stenosis and disc herniation with or without degenerative spondylolisthesis. All the patients had undergone BESS using a unilateral interlaminar approach. MRI was performed 3 times: preoperatively, immediately postoperatively (within 3 days after surgery), and at the final follow-up examination. The patients who had not undergone all 3 MRI evaluations were excluded. The final followup MRI scan was performed for patients with unsatisfactory postoperative results determined by the leg visual analog scale (VAS) score and modified Macnab criteria. Poor outcomes were indicated by leg VAS score improvement of <50% or fair or poor outcomes using the modified Macnab criteria. Every patient underwent T2-weighted MRI to measure the MFM intensity and CSA on the ipsilateral and contralateral sides. The exclusion criteria were segmental instability,39 lytic spondylolisthesis, performance of BESS using an extraforaminal approach,28 or the presence of coexisting pathological conditions such as infection or tumor. Patients with >2 spinal levels requiring surgery and those who had undergone previous lumbar surgery were also excluded (Table 1).

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Surgical Procedures Patient Preparation. All procedures were performed by a single surgeon (H.J.L.). The diameter of the endoscopes was 4 mm, with a field view of 0
or 30
. The endoscopes had been officially certified for spinal surgery in South Korea (Endocare [BMK, Seoul, South Korea]). Both 0
and 30
endoscopes were used as needed, depending on the operative field. Ordinary spinal and arthroscopic instruments were used (Figure 1). After induction of general or epidural anesthesia, the patients were placed prone on a Jackson table in a kneeling position.

MRI EVALUATION OF MFM CHANGES AFTER BESS

to the endoscope, set to a pressure of 25e30 mm Hg, and controlled within this range throughout the operation, depending on the condition of the surgical view. The continuous flow of saline is essential to control minor bleeding and to keep the surgical field clear. During surgical field construction, a temporary guide pin was inserted at the junction of the proximal lamina and the spinous process to confirm that we were at the desired surgical level (Figure 2). After exposing the margin of the interlaminar space, the medial aspect of the facet joint, and the base of the transverse process, the soft tissue remnants and bleeding were effectively managed using a shaver, a pituitary rongeur, and radiofrequency probes.

Portal Placement. With anteroposterior C-arm fluoroscopic guidance parallel to the upper endplate of the proximal vertebral body at the operative level, 2 spinous processes and the bony margins of the left and right interlaminar spaces were marked on the skin. Two separate 1-cm vertical incisions were made 1-cm lateral to the interspinous line Video available at on the upper and lower margin of the interlaminar space www.sciencedirect.com (Figure 2). Surgical Field Construction. Usually, the endoscope was inserted through the left portal (viewing portal) and the surgical instruments through the right portal (working portal; Figure 3), although this could be reversed depending on the surgeon’s preference. Through the incisions, the soft tissues were gently detached from the lamina, interlaminar spaces, and bases of the spinous processes at the targeted level using a small periosteal or a narrow Cobb elevator. Initially, a 0
endoscope was inserted through the viewing portal after insertion of a cannula. A saline irrigation pump was connected

Figure 1. Standard instruments used. (A) Endoscopes with angles of 0
and 30
, diameter of 4 mm; and length of 175 mm. (B) From top to bottom: a 90
hook electrode extension for radiofrequency probes, a side-electrode extension for radiofrequency probes, a

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Discectomy. After exposing the upper and lower margins of the target interlaminar space, ipsilateral partial laminotomy was performed using a pneumatic burr and Kerrison punch (Supplementary Video 1). The ligamentum flavum was detached using a curette and removed with the Kerrison punch and pituitary rongeur. In addition, the medial facet was resected to afford full mobilization of the lateral border of the traversing nerve root, and discectomy was performed without nerve retraction (Figure 4). After annulotomy using a Penfield dissector or a microknife, discectomy was performed using a pituitary rongeur and curved curette. Decompression. Ipsilateral laminotomy and resection of the ligamentum flavum were performed in a manner similar to that use for discectomy (Supplementary Video 2). The bases of the upper and lower spinous processes were partially resected

blade extension for the arthroscopic shaver, and a burr extension for the arthroscopic shaver. (C) Angled curettes. (D) From top to bottom: a double-ended freer, a Penfield elevator, a blunt nerve hook probe, and a microknife.

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Closure. After adequate hemostasis using a radiofrequency probe, a suction drain was inserted through the instrument portal (working portal), and the endoscope and instruments were extracted. Any remaining saline within the body was removed by manual squeezing around the portals. The skin was repaired using a skin stapler after nonabsorbable suture (1ne subcutaneous stitch; Figure 3). Postoperative Care and Discharge The initial neurological assessment was performed in the recovery room after surgery. The patients were monitored every 8 hours for postoperative problems and were discharged when they could walk without any complications.

Figure 2. Portal placement. (A) Anteroposterior C-arm fluoroscopic image taken parallel to the upper endplate of the proximal vertebral body at the operating level. The black bar indicates the lateral margin of the interlaminar space. (B) Major anatomical structures (2 spinous processes and the margins of the left and right interlaminar spaces) were marked on the skin, and 1-cm vertical incisions (red lines) were created 1 cm lateral to the interspinous lines on the margins of the upper and lower interlaminar space. (C) Anteroposterior C-arm fluoroscopic image showing a guide pin inserted into the predicted junction of the proximal lamina and spinous process to confirm the location of the interlaminar space at the surgical level. (D) Lateral C-arm fluoroscopic image showing a guide pin was inserted into the predicted junction of the proximal lamina and spinous process to confirm the location of the interlaminar space at the surgical level.

using a burr and Kerrison punch to visualize the undersurface of the contralateral lamina. The contralateral side was decompressed using a pneumatic burr and Kerrison punch and bony decompression was performed, followed by flavectomy. The flavum was removed en bloc after bony decompression had been completed. The lateral recess of the contralateral side was also decompressed via partial removal of the superior articular processes of the lower vertebrae using a Kerrison punch. Decompression was continued until both the ipsilateral and contralateral traversing roots had been fully visualized and easily mobilized by the probe (Figure 5). Additional discectomy was performed in patients in whom incidental disc protrusion contributing to canal stenosis was found intraoperatively.

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Evaluation The interval to the final follow-up MRI study after BESS and the operative time for each patient were recorded. MRI (1.5-Tesla system [Siemens, Munich, Germany]) was performed 3 times, as described (Figure 6). The images were saved in DICOM (digital imaging and communications in medicine) format, and the axial images at each intervertebral disc level were evaluated using the PACS (picture archiving and communication system) imaging software (M-view [Maro Tech Inc., Seoul, Korea]). T2-weighted images were analyzed using 2 methods to assess the MFM status. We calculated the mean signal intensity and total MFM CSA. We calculated the signal intensity and MFM CSA according to previously reported studies.38,40,41 Measurements were performed on the ipsilateral side (where the incisions were made) and the contralateral side. MFM signal intensity was quantitatively assessed on the axial images using the grayscale histogram of the PACS software, with a higher score indicating greater signal intensity. A region of interest (ROI) was drawn bilaterally around the outer perimeter of the MFM, including any areas of intramuscular fat (Figure 7). The signal intensity of the psoas muscle on the same axial image was evaluated using a 0.773-cm2 circular ROI placed in the center of the left-sided psoas (Figure 7). The T2-weighted signal intensity ratios (SIRs) of the gross MFMs to the psoas of both sides were recorded 3 times, preoperatively, immediately postoperatively, and at the final follow-up examination, and the percentage of changes between the preoperative and final follow-up values were recorded. To determine the total MFM CSA, an ROI was drawn bilaterally around the MFM in the same manner, and the CSA of both sides was recorded (Figure 7). The percentage of changes between the preoperative and final follow-up values were recorded. All images were measured twice at 2-week intervals, by 1 of us and an independent, experienced musculoskeletal radiologist, to reduce the intra- and interobserver bias. Furthermore, the 2 assessors were kept unaware of the operative side and the postoperative evaluation point. We recorded the mean values of the 2 measurements. Data Analysis The data from 88 patients who had undergone all 3 MRI sessions (i.e., preoperatively, immediate postoperatively, and the final follow-up examination) were analyzed separately. Analysis of All Patients. The associations between the interval to the final follow-up evaluation and MFM changes (i.e., SIR,

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Figure 3. The 2 portals used in biportal endoscopic spinal surgery. (Left) The endoscope is inserted through the left portal and surgical instruments through the right portal, although this could be reversed

percentage of change in SIR, MFM CSA, and percentage of change in the MFM CSA on the ipsilateral and contralateral sides) were analyzed. We also investigated the associations between the operative time and the MFM changes. Analysis by Group. To explore the correlations between the interval to the final follow-up examation and specific MFM changes, all the patients were divided into 3 groups according to the interval to the final follow-up MRI. Group 1 was evaluated at <2 weeks postoperatively, group II at 2e4 weeks postoperatively, and group 3 at >4 weeks postoperatively. Changes in the MFM parameters (SIR, percentage of changes in SIR, MFM CSA, and percentage of changes in the MFM CSA for both ipsilateral and contralateral sides) were analyzed among these 3 groups. Statistical Analysis Statistical analysis was performed using SPSS software, version 24.0 (IBM Corp., Armonk, New York, USA). The normality of distribution was checked using the Kolmogorov-Smirnov test. For the analysis of the entire group, Pearson’s correlations were

Figure 4. Endoscopic image showing the herniated disc of axillary type. Triangle indicates the traversing nerve root; circle, the herniated disc; and square, the thecal sac.

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depending on surgeon preference. (Right) Repaired incisions after biportal endoscopic spinal surgery, with a suction drain inserted through 1 of the portals.

calculated to assess the associations between the final follow-up and operative times and the SIRs and percentage of changes in both SIR and MFM CSAs. The between-group differences were evaluated using one-way analysis of variance for continuous variables and the c2 or Fisher exact test for categorical variables. In all analyses, P < 0.01 was considered to reflect statistical significance. For the between-group comparisons, the data that were nonparametrically distributed were analyzed using the KruskalWallis test. Moreover, the Mann-Whitney U test was used for comparisons between pairs of groups (3 hypotheses; group 1 vs. 2, group 2 vs. 3, and group 1 vs. 3) as the post hoc test. P ¼ 0.003 was considered to indicate statistical significance (accounting for a Bonferroni correction; 0.01/3 ¼ 0.00333). RESULTS Demographic Data and Disease Characteristics A total of 88 patients were included in the present study. The Baseline patient demographics and disease characteristics are summarized in Table 2. The L4-L5 level was the most frequent

Figure 5. Endoscopic image showing the thecal sac after decompression via biportal endoscopic spinal surgery. Triangle indicates the ipsilateral traversing nerve root; circle, the thecal sac; and square, the contralateral traversing nerve root.

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Figure 6. Sequential changes of multifidus muscles on magnetic resonance image after discectomy, unilateral laminotomy, and bilateral decompression via biportal endoscopic spinal surgery. (Left) Preoperative, (Middle) postoperative, and (Right) final (3 months

level of surgery (70.6%), followed by L3-L4 (17.6%). The operative data and clinical outcomes are summarized in Table 3. The interval to the final follow-up evaluation was a mean duration of 42.9 days. The mean operative time was 104.1 minutes. The mean VAS score of radicular leg pain had decreased from 6.5  1.7 preoperatively to 4.4  1.4 at the final follow-up evaluation. The outcome using the modified Macnab criteria was fair in 81 patients and poor in 7 patients.

after biportal endoscopic spinal surgery) axial magnetic resonance images at L3-L4 intervertebral disc level. Adequate herniated disc removal and spinal canal expansion were identified, with preservation of multifidus muscles.

Correlations The operative time correlated significantly with the percentage of change in the SIRs for both the ipsilateral (r ¼ 0.47; P ¼ 0.002, Pearson correlation test) and the contralateral (r ¼ 0.43; P ¼ 0.004, Pearson correlation test). The final follow-up evaluation was associated with marginal significance with the SIR of both sides (P ¼ 0.016, ipsilateral; P ¼ 0.049, contralateral), the percentage of changes in SIR (P ¼ 0.029), and the CSA of the ipsilateral side (P ¼ 0.045). However, statistical significance was not attained (P > 0.01). Group Data Demographic Data and Disease Characteristics. The baseline patient demographics, disease characteristics, operative data, and clinical outcomes of the 3 groups are summarized in Tables 4 and 5. Of the 88 patients, 34 were in group 1, 24 in group 2, and 30 in group 3. The mean interval to the final follow-up examination (the last MRI session after BESS) was 5.9  2.8, 17.8  3.9, and 105.0  75.7 days in groups 1, 2, and 3, respectively. No significant between-group differences were found in the demographic data, disease characteristics, operative level, operative time, or mean VAS score (Tables 4 and 5).

Figure 7. Magnetic resonance image of multifidus muscles (MFMs) after biportal endoscopic spinal surgery. Both the mean signal intensity and the total cross-sectional area of the MFM T2-weighted image were analyzed to assess MFM status. The T2-weighted signal intensity ratios of the gross MFMs to that of the psoas muscle and the CSA of both sides were calculated and recorded.

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MFM SIR. The SIR and percentage of changes in SIR of the 3 groups are summarized in Table 6. The SIR of the ipsilateral side increased postoperatively in all groups, and no significant between-group difference was apparent. However, at the final follow-up evaluation, the SIR of the ipsilateral side had decreased in group 3. Significant differences were evident among the 3 groups (P ¼ 0.002). Moreover, in the post hoc test with Bonferroni’s correction, a significant difference was apparent between groups 1 and 3 (P ¼ 0.0005). The percentage of change in the SIR on the ipsilateral side was the smallest in group III. Significant differences were evident among the 3 groups (P ¼ 0.004). In the post hoc test with Bonferroni’s correction, a significant difference was apparent between groups 1 and 3 (P ¼ 0.0009). No significant differences in the SIRs of the contralateral side were evident among the 3 groups (P > 0.01; Table 4).

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Table 2. Patient Demographic Data and Disease Characteristics Characteristic Patients Age (years)

Table 4. Demographic Data and Disease Characteristics Stratified by Group Value

Characteristic

88 (100)

Patients (n)

56.4  14.9

Age (years)

Gender

Group 1

Group 2

Group 3

34

24

30

58.1  13.0 57.7  15.9 53.6  16.6

0.899

56 (64.0)

Male

22

14

20

Female

32 (36.0)

Female

12

10

10

Diagnosis

Diagnosis

0.832

Lumbar disc herniation

42 (47.7)

Lumbar disc herniation

18 (52.9)

10 (41.7)

14 (46.7)

Lumbar spinal stenosis

46 (52.3)

Lumbar spinal stenosis

16 (47.1)

14 (58.3)

16 (53.3)

Operative level

Operative level

0.441

L3-L4

10 (17.6)

L3-L4

6 (17.6)

2 (8.3)

2 (6.7)

L4-L5

56 (70.6)

L4-L5

24 (70.6)

12 (50.0)

20 (66.7)

L5-S1

22 (11.8)

L5-S1

4 (11.8)

10 (41.7)

8 (26.6)

Data presented as n (%) or mean  standard deviation.

Data presented as mean  standard deviation or n (%).

MFM CSA. The MFM CSAs and percentage of changes in the 3 groups are summarized in Table 6. The ipsilateral MFM CSA had increased postoperatively but had decreased at the final follow-up evaluation in all groups. However, no significant between-group differences were apparent. No significant differences in the percentage of CSA change on the ipsilateral side were evident among the groups. On the contralateral side, neither the CSA nor the percentage of change in the CSA differed among the groups.

DISCUSSION MFM injury and atrophy have been common after posterior lumbar spine surgery associated with low back pain and functional disability.1,30 Thus, significant efforts have been made to develop minimally invasive operative techniques to spare the dorsal rami and minimize approach-related morbidity and attain outcomes Table 3. Operative Data and Clinical Outcomes Value

similar to those of more traditional invasive approaches.8 BESS is an alternative minimally invasive technique affording many advantages and overcoming the limitations of conventional minimally invasive spine surgery. BESS is suitable because of the availability of an independent working tube, no requirement for special endoscopic instruments, and the excellent image quality.20-23,25 However, to the best of our knowledge, no previous study has used MRI to evaluate the extent of paraspinal muscle injury after BESS. Remarkable MFM changes were found on the immediate postoperative MRI scans after BESS on the ipsilateral and contralateral sides as the operative time had increased. However, the MFM changes tended to decrease within

Table 5. Operative Data and Clinical Outcomes Stratified by Group Characteristic

Group 1

Group 2

Group 3

Follow-up period (days)

5.9  2.8

17.8  3.9

105.0  75.7

Follow-up period (days)

42.9  62.7

Operative time (minutes)

Operative time (minutes)

104.1  39.5

VAS score

VAS score Preoperatively

6.5  1.7

At final follow-up examination

4.4  1.4

115.3  39.2 100.8  12.3 94.0  36.5

0.307

Preoperatively

6.5  1.8

6.6  1.8

6.3  1.5

0.799

At final follow-up evaluation

4.4  1.3

4.4  1.5

4.3  1.3

0.771

Fair

81

Fair

30

23

28

Poor

7

Poor

4

1

2

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P Value

Macnab criteria

Macnab criteria (n)

Data presented as mean  standard deviation or number of patients. VAS, visual analog scale.

0.671

Gender

Male

Characteristic

P Value

Data presented as mean  standard deviation or number of patients. VAS, visual analog scale.

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0.929 0.380 0.412 0.319 1.6  11.3 697.2  164.6 717.5  180.3 Pre, preoperative; Post, postoperative; SIR, T2-weighted signal intensity ratio of multifidus to psoas muscle; CSA, cross-sectional area. *Final follow-up evaluation. yPercentage of change between the preoperative and final follow-up value. zStatistically significant.

717.7  188.8 1.6  7.5 688.3  241.1 730.4  220.3 692.9  211.3 0.3  12.4 623.6  175.6 634.9  167.1 629.8  176.5

0.024 1.57  0.59 1.79  0.61 1.54  0.58 2.1  32.2 0.027 0.020 3.9  29.2 2.17  0.57 2.39  0.62 2.10  0.97 24.7  41.5 1.99  0.64 2.08  0.63 2.43  1.12 SIR

Contralateral

CSA (mm2)

0.090

0.094 0.657 0.236 0.575 4.2  10.5 701.9  194.1 772.5  191.6 727.3  171.5 2.5  12.7 708.4  252.3 751.1  263.7 733.7  279.9 5.7  15.5 660.4  163.9 689.8  169.4 631.2  174.0 CSA (mm2)

0.004z 0.554 0.263 1.6  41.3 1.80  0.66 2.26  1.0 1.72  0.87 31.8  47.7 2.08  0.81 2.57  0.69 2.58  0.92 52.0  51.2 1.98  0.63 2.45  0.83 2.91  1.13 Ipsilateral

SIR

FollowUp* Post Pre Side

MRI EVALUATION OF MFM CHANGES AFTER BESS

0.002z

FollowUp* FollowUp* Post Changey (%) FollowUp* Post Changey (%)

Pre

Group 2 (n [ 24) Group 1 (n [ 34)

Table 6. Magnetic Resonance Imaging Evaluation of Multifidus Muscles Stratified by Group

Pre

Group 3 (n [ 30)

Changey (%)

Pre Post

P Value

Changey (%)

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several months, and no significant change in the MFM CSA was noted. No evidence of postoperative MFM atrophy, as revealed by changes in the CSA, was found. Several factors were significantly associated with the MFM change after BESS. First, a strong positive correlation was evident between the operative time and the percentage of change in the T2-weighted SIR for both sides, showing that the operative time affected both MFM status and MFM recovery during the follow-up period. Previous studies had found that the extent of paraspinal muscle injury was directly associated with the muscle retraction time during surgery.37,42 Gejo et al.37 concluded that increased serial MRI T2-weighted signal intensity correlated with a longer muscle retraction time. BESS requires constant pump-controlled saline irrigation at 25e30 mm Hg of pressure. The constant saline flow is essential to control minor bleeding and keep the surgical field clear. Saline irrigation imparts hydrostatic pressure and can injure the MFMs by retraction. Hence, decreasing the operative time and saline-imparted hydrostatic pressure could minimize the MFM changes. The patients enrolled in the present study include the earliest cases and, thus, the learning curve period. Therefore, in the future, it will be necessary to compare these results of MFM changes found on MRI to the more recent MRI findings. Between-group comparisons revealed significant SIR differences at the final follow-up evaluation and significant percentage of changes (from preoperatively to the last follow-up evaluation) in the SIR of the ipsilateral side (Table 4). We divided the entire patient sample into 3 groups according to the final follow-up point and investigated the associations between the follow-up duration and MFM status changes. A positive correlation was evident between high-level, postoperative T2-weighted MFM signal intensity and the extent of MFM injury at the surgical level.36,37 The postoperative SIR was significantly greater than the preoperative SIR in all 2 groups (Table 4), which can be explained by MFM inflammation and edema during the acute postoperative phase. In group 3, both the T2-weighted signal intensity at the final follow-up evaluation and the percentage of change in the intensity were lower than those in group 1, with statistically significant differences. In addition, the SIR at the final follow-up evaluation was similar to the preoperative value. Although an irreversible change in paravertebral muscle signal intensity has often been noted after posterior lumbar surgery,36,37,43 our results indicate that the MFM high-signal intensity after BESS will gradually decreased during the follow-up period. Tonomura et al.38 used MRI to evaluate the extent of paravertebral muscle injury after muscle-preserving interlaminar decompression (MILD). MRI was performed preoperatively and at 3 and 12e18 months after surgery. The SIR of the MFM to the psoas muscle at 12e18 months after MILD was the same as the preoperative SIR; however, the SIR at 3 months after surgery was greater. In the present study, the SIR after BESS had returned to normal earlier than it had in the patients who had undergone MILD,38 because the mean follow-up period for group III was 105  75.7 days. No significant difference in the MFM CSA was apparent on either the ipsilateral or contralateral side. We found a weak negative correlation between the follow-up period and the percentage of change in the ipsilateral CSA, perhaps suggesting that the MFM volume after BESS decreased as the follow-up time

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MRI EVALUATION OF MFM CHANGES AFTER BESS

increased. However, statistical significance was not attained. The between-group comparisons revealed no significant differences in the CSA or the extent of MFM atrophy on either side (Table 4). The present study had certain limitations. The most important of which was that it lacked clinical correlation. Although we recorded the clinical outcomes using the VAS score of radicular pain and the modified Macnab criteria, we did not analyze the correlation between the radiological results and the clinical outcomes. In the future, it will be necessary to study the association of our radiographic results with the clinical symptoms, such as back pain, radicular pain, and quality of life index. Other limitations included the lack of a comparable control group and our small number of patients. However, to minimize the error from the small samples, we defined statistical significance as P < 0.01, instead of P < 0.05. The final follow-up MRI evaluation was performed only for patients with remnant symptoms or unsatisfactory results to determine the reason for the remnant pain under

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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 8 March 2019; accepted 19 June 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.148 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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