The role of intraoperative ultrasound in management of spinal intradural mass lesions and outcome

The spinal intradural mass lesions represent a challenge in microsurgical practices. The intraoperative precise localization and characterization of these lesions must be achieved to avoid excessive exposure and neural tissue damage. This study aims to evaluate the role of intraoperative ultrasound during surgical dealing with spinal intradural mass lesions starting before bony work exposure. This prospective study had been done during the period from January 2022 to January 2023 with follow-up at least 6 months on 36 patients, suffered intradural spinal mass lesions and underwent microsurgical interventions aided with intraoperative ultrasound. MRI spine and Klekamp score were used as preoperative and postoperative parameters for assessment of the patients. Intraoperative ultrasound features were analyzed to evaluate its values. All lesions were visualized and characterized by intraoperative ultrasound beside spinal anatomical identification. Laminoplasty, laminectomy, durotomy and myelotomy were determined by IOUS. Gross total eradication was achieved in 28/36 (78%). Intraoperative ultrasonography definition of cystic component, well-defined borders and smooth shape of the masses were associated with significant Klekamp outcome improvement. Intraoperative ultrasound can be used safely to detect the spinal intradural mass lesions even before bony work for exposure with anatomical and pathological definition and has the ability to predict the outcome.


Background
Spinal tumors constitute about 15% of the central nervous system tumors, which can be located extradural in 60%, intradural extramedullary in 30% and intramedullary in 10% [1].Diagnosis of intradural tumors may be delayed as nonspecific manifestations of these lesions.The level of spinal lesion determines the neurologic manifestations, which often start by pain [2].Spinal intradural mass lesions do not include only tumors but other lesions may be found as spinal subdural abscess, which is a rare disease with more occurrences in adults [3].Surgeries of spinal intradural lesions are the standard option of treatment, with such hazards of neurological affection especially with myelotomy.Intraoperative ultrasound provided real-time information aiding in avoiding probable complications [4].This study aims to evaluate the role of intraoperative ultrasound during surgical treatment of spinal intradural mass lesions and the outcome.

Methods
This prospective observational study had been conducted on patients diagnosed as spinal intradural mass lesions either extramedullary or intramedullary and indicated for microsurgical intervention.During the period from January 2022 to January 2023, 36 patients were subjected to surgeries for treatment of spinal intradural mass lesions at our institute after approval from the institutional review board (IRB#:9168) and according to the code of ethics of the world medical association (Declaration of Helsinki) for studies on humans.All patients or their guardians were informed about the procedures, and consents were obtained before surgeries.All patients were operated in prone position under general anesthesia by the team authors with at least 10 years' experience in neurosurgeries regarding the main surgeon.Follow-up duration was at least 6 months.

Inclusion criteria
Patients with intradural spinal mass lesions either extramedullary or intramedullary in location of any pathological type.

Procedures
Intraoperative ultrasound machines were used in all surgeries with different probes.Frequencies ranges 5-11MHZ were used in this study to adopt the best depth resolution.Figure 1.The probe was covered by a sterile sleeve with acoustic gel entrapped anterior to the probe head.Real-time B mode was adjusted for clear view by choosing the appropriate megahertz and suitable gain, contrast and depth.The surgical cavity was filled by saline during ultrasound imaging.The level of surgery was determined according to the preoperative investigations and intraoperative fluoroscopy.At the start, we did ultrasound look before laminectomy or laminoplasty through the interlaminar space of the determined level with or without small laminectomy window (after fluoroscopic localization, skin incision and muscle splitting expose a single lamina with upper and lower interlaminar spaces and then the Burr-Hole probe adjusted at the lower and may be also at the upper interlaminar space near to the interspinous area to gain look to the spinal canal and if the artifacts of the bony structures obstacles the view, we make a widening for few millimeters from the upper lamina and may be the lower lamina near the base of the spinous processes to provide access of the ultrasound waves.This step was done by limited skin incision and muscle splitting, and the direction of wound extension is determined accordingly and then the bony work) to assure the mass location to decrease the bony exposure as minimal.The spinal canal exposure was done either by laminectomy or laminoplasty.The laminoplasty was either open door (Fig. 2c) or en bloc (Fig. 3B e) types.Real-time B-mode ultrasound was used before dural incision for localization, characterization of the intradural mass beside evaluation of its anatomical relation to neural and bony elements of the spinal canal; this was achieved by coronal, sagittal and oblique imaging.Microsurgical dural incision was determined according to the ultrasound localization, myelotomy incision in cases of intramedullary masses was at the midline of the spinal cord and its extension was according to ultrasound localization.During surgical procedure, the ultrasound was reused to evaluate the extent of resection.

Hitachi
The following data were used for assessment: 1. Klekamp score [5], for clinical evaluation, was used in preoperative, postoperative and during follow-up assessments.2. Klekamp improvement rate = 100 × (postoperative Klekamp score-preoperative Klekamp score)/ (20-preoperative Klekamp score).This equation was used to calculate the extent of clinical improvements during follow up.3. MRI spine with and without contrast for mass lesion evaluation was used in preoperative, postoperative and during follow-up assessments.4. Intraoperative ultrasound data about the mass lesion.

Statistical analysis
All data were collected, tabulated and statistically analyzed using SPSS IBM Corp. Released 2015.IBM SPSS Statistics 23.0.Armonk, NY: IBM Corp. Quantitative data were expressed as the mean ± SD and (range), and qualitative data were expressed as number and percentages.

Results
A total of 36 patients were subjected to microsurgical treatment of intradural spinal mass lesions.There were 6 children (16.7%) and 30 adults (83.3%).The mean age was 36.2 ± 14.4 years and the range was (5-60 years).Femaleto-male ratio was 2:1.Sensory manifestations were the first symptom in 30 (83.3%) patients and the presenting symptom in all patients.Table 1 represented the outcome according to Klekamp scale: 1.There were significant improvements in clinical condition after 6 months from surgeries regarding sensory, motor and gait disturbances.2. Klekamp scores after 24 h from surgeries showed no significant improvement (p1) while after 6 months, there were significant improvements (p2, p3). 3. 28(77.8%)patients showed improvement after 6 months with statistical significance, of whom 9 patient showed more than 75% improvement rate.
Table 2 represented the relation between demographic data, illness duration, imaging data and pathology with Klekamp outcome after 6 months, which were found insignificant.Table 3 represented the relation between intraoperative data and outcome after 6 months: 1. Exposure by laminectomy or laminoplasty, mass diameters and ultrasound echogenicities showed no significant difference.2. Total resection was of high significant association with Klekamp improvement after 6 months.
3. Ultrasound characterization, presence of cystic component, well margin definition and smooth contours were associated with significant improvement.
Operative complications in this study were 4 cases suffered cerebrospinal fluid leakage, one patient suffered wound infection and one patient suffered transient motor weakness.
Ultrasound detected all studied lesions including tumors, abscess and syringomyelia.Anatomical landmarks of the spinal cord and spinal bone were determined by intraoperative ultrasound beside the ability to real-time visualization of the intradural mass before bony work, dural incision and myelotomy, which was of great help to precise bony work, dural incision and also myelotomy as these steps may be a great obstacles to surgeons especially with small lesions.Ultrasound can be done by

Discussion
The real-time intraoperative ultrasound was well documented in brain surgeries either during mass lesion resection or catheter placement [6,7].The well definition of anatomical landmarks of the spinal canal including bone and soft tissues Fig. 1 with the flexibility of ultrasound imaging in different orientation plans, made the intraoperative ultrasound a valuable surgical tool, which may be used during dealing with intradural mass lesions.
Exposures of intradural mass lesions during surgeries account an important issue for the neurosurgeon.CT, MRI and neuronavigators cannot be afforded in most neurosurgical operative theaters, instead intraoperative ultrasound may offer the benefits and avoid the hazards and fallacies of those tools [8,9].One of the well-known benefits of intraoperative ultrasonography use is limitation of dural incision and myelotomy incision, which of course decrease the hazards of such surgeries [10,11].The incidence of wrong localization during intradural spinal surgeries reported to be 0.032-15% and wrong myelotomy may lead to severe neurological affections [12].
We added a novel ultrasound look through interlaminar space or small laminectomy window to fashionate the laminoplasty or the laminectomy to the least extension, this technique was well achieved.Maiuri et al. [13] proposed 3 steps during intraoperative ultrasound use in spinal intradual surgeries; first step before dural incision, second step before myelotomy and the third step during and after resection.The pre laminectomy/ laminoplasty look may be added to these steps as we described in our study.
Intraoperative ultrasound delineated all intradural spinal lesions wherever intramedullary or extramedullary and of all sizes, and this was documented in many studies [14].All pathologies, tumors, abscesses and syringomyelia were detected by ultrasound.The general benefits of intraoperative ultrasound during intradural spinal surgeries were assurance of bony exposure and the extension of dural incision; during intramedullary surgeries, the ultrasound provides the data of myelotomy site and guide the surgical process, and during extramedullary surgeries, the role of intraoperative ultrasound may be ended after dural incision except in some cases with complex location of the lesion as shown in Fig. 5. Vasudeva et al. [15] concluded their literature review on intraoperative ultrasound during spinal surgeries, which IOUS remains the only real-time modality and must be used in all intradural lesion surgeries and also in anterior located extradural lesions when approached from posterior and advised to teach it in all spinal surgery programs.Klekamp score improvements after 6 months of surgeries were achieved in 28(78%) with statistic significant.The pathological type, location, extension, duration of illness, method of exposure and demographic data were without significant implication on the outcome.Total resection affected the outcome significantly, which was achieved in 28/36 (78%) patients in our study.Han et.al [10] reported (71.4%) improvement after intramedullary tumor resection under contrast enhanced ultrasonographic guide with total resection achieved in all of the 14 cases.Toktas et al. [16] achieved total tumor resection in 22 (84%) of 26 patients suffered intradural lesions (14 extramedullary and 12 intramedullary) under ultrasound guidance.
Ultrasonographic parameters, which were associated with significant better outcome, were the prescence of cystic component, well-defined border and smooth shapes.Well-defined border was detected in all extramedullary lesions and 18/24 (75%) of intramedullary lesions.These parameters may be considered the ultrasound predictors for the outcome.Platt et al. [17] reported 11/14 (78%) of their studied intramedullary tumors showed welldefined margins, which facilitated total resection, and they documented the accuracy of the IOUS in detected the cystic components even better than MRI and CT.The intraoperative ultrasound is just a tool, which can be used during brain and spinal surgeries but the microsurgical practices and the learning curve of how to use this machine is very important.Intraoperative ultrasound during brain surgery is much easier than during spine surgeries.Limited working area during spinal intradural surgeries mandates small probe size, image adjustment by suitable frequency, gain, depth and brightness and gentle manipulation.

Conclusion
Intraoperative ultrasonography can be used during spinal intradural mass lesion surgeries to minimize the exposure area, not only dural incision and myelotomy but also bony exposure.All types of the mass lesions can be evaluated by IOUS with the ability to predict the outcome.

Fig. 2 Fig. 3
Fig. 2 Lumber intradural mass lesions.A Intradural abscess (female patient 5 years old, laminoplasty); a preoperative T1MRI without and with contrast, b follow-up T1MRI with contrast 6 months after surgery, c intraoperative photo; arrow 1 points to the pus and d intraoperative photo shows the cavity of the abscess.e sagittal and axial intraoperative ultrasound images; arrow 2 the spinal cord and 3 the abscess cavity.B Intradural epidermoid cyst (male patient 16 years old, laminoplasty); a preoperative T2MRI, T1MRI with contrast, b early postoperative T1MRI, c intraoperative photo; arrows 1 points to open-door laminoplasty and e sagittal and axial ultrasound images; arrow 2; the spinal cord, arrows 3; epidermoid cyst and arrow 4 cerebrospinal fluid

Fig. 4 Fig. 5
Fig. 4 Intradural extramedullary mass lesions.A Upper cervical meningioma (female patient, 40 years old, laminectomy); a preoperative T1MRI with contrast, b early postoperative T1 MRI, c follow-up T1 MRIwith contrast after 6 months, d intraoperative photo and e ultrasound images; arrow 1; compressed spinal cord, 2; the tumor and 3; the spinal cord after tumor resection.B Dorsal meningioma (male patient, 35 years old, laminectomy); a preoperative MRI, b early postoperative MRI, c follow-up T1 MRIwith contrast after 6 months, d intraoperative photo and e ultrasound images; arrows 1; the tumor, 2; the spinal cord

Table 3
Association between intraoperative data and Klekamp outcome χ 2 :Chi-square test, f = Fisher exact test of significant, *P < 0.05 significant