Indian Spine Journal

ORIGINAL ARTICLES
Year
: 2021  |  Volume : 4  |  Issue : 2  |  Page : 155--162

Clinical and surgical outcomes of enneking stage III aneurysmal bone cysts of the spine


Sanjeev Kumar Pandey1, Edmond Jonathan Gandham2, Krishna Prabhu2,  
1 Department of Neurosurgery, Himalayan Institute of Medical Sciences, Dehradun, India
2 Department of Neurological Sciences, Christian Medical College, Vellore, India

Correspondence Address:
Krishna Prabhu
Department of Neurological Sciences, Christian Medical College and Hospital, Vellore 632004, Tamil Nadu.
India

Abstract

Objective: To study the clinicoradiological characteristics and surgical outcomes in patients with aggressive aneurysmal bone cyst (ABC) of spine. Materials and Methods: In this retrospective study, data was collected from patients with aggressive ABC of spine managed between January 2007 and December 2016. Clinical findings, radiological, and histological characteristics were studied. Follow-up was done either in the outpatient clinic or through a telephonic interview. Results: Seven patients (mean age, 15.6 years, range, 6–23 years) diagnosed with Enneking stage III aneurysmal bone cyst of the spine were included in the study. Local pain with restriction of movement was the most common presenting complaint (100%). Four patients presented with myelopathy. Thoracic spine was the most common site of involvement (43%). Of the patients, 71% had involvement of all three columns. All patients underwent surgical management; gross total resection in four patients (57%) and subtotal in three patients (43%). Of the seven patients, six required instrumented fusion. None of the patients developed any perioperative complication except for one patient who developed transient hip flexion worsening. Two patients received conformal radiation therapy (RT) postoperatively. The follow-up ranged from 40 months to 108 months (mean follow-up was 4.5 years). There were no recurrences. At last follow-up, all patients were alive and had significant improvement. Conclusions: ABC of the spine is found predominantly in the pediatric population. Intralesional en bloc resection with instrumented stabilization provides effective and fast relief from pain, early mobility, good surgical, and long-term outcomes. Conformal RT following a planned subtotal excision prevents the progression of the disease.



How to cite this article:
Pandey SK, Gandham EJ, Prabhu K. Clinical and surgical outcomes of enneking stage III aneurysmal bone cysts of the spine.Indian Spine J 2021;4:155-162


How to cite this URL:
Pandey SK, Gandham EJ, Prabhu K. Clinical and surgical outcomes of enneking stage III aneurysmal bone cysts of the spine. Indian Spine J [serial online] 2021 [cited 2022 Dec 4 ];4:155-162
Available from: https://www.isjonline.com/text.asp?2021/4/2/155/316662


Full Text



 Introduction



Aneurysmal bone cyst (ABC) was described as a distinct entity by Jaffe and Lichtenstein in 1942 as “large-sized peculiar blood containing cyst.”[1] It is an expanding osteolytic lesion consisting of blood-filled spaces of variable size, separated by connective tissue septa containing trabeculae or osteoid tissue and osteoclast giant cells as defined by WHO.[2] Several authors have defined it as a pseudotumoural hyperemic–hemorrhagic lesion of unknown etiology.[3],[4],[5],[6]

ABC forms 1% of primary bone tumors and 15% of primary tumors of the spine.[7],[8],[9]

ABC is seen in children and young adults. About 70% of ABCs are primary and 30% are secondary to some other pathology.[10] ABC has the predilection to involve the posterior spinal elements, but it may progress to involve the vertebral body in about 40% of cases.[11],[12] ABCs have the predilection for the lumbar and cervical spine and is observed mostly in patients with less than 20 years of age.[13] Although ABCs are benign lesions, it may behave aggressively. Recurrences after the primary treatment are difficult to manage and result in significant neurological impairment and structural damage.

Treatment for spinal ABCs include selective arterial embolisation (SAE), curettage, en bloc resection surgery with or without spine stabilization, radiation therapy (RT), intralesional injection of bone cement, intralesional injection of mesenchymal stem cells, bisphosphonates, and Denosumab.[14],[15] SAE has been used in limited number of patients, mainly vertebral, pelvic, and/or extensive ABCs.[16]

Enneking et al.[17],[18] classified ABCs into three types: Stage 1 (latent), which remains static, or heals spontaneously; Stage 2 (active), progressive growth without cortical destruction; and Stage 3 (locally aggressive), progressive growth with significant cortical destruction. Majority of the patients in Stage 2 can be managed with curettage with or without grafting but locally aggressive ABCs are better dealt with by wide excision. In past, majority of the patients were managed with curettage, without instrumented stabilization.[19],[20],[21] Recurrence following intralesional curettage is close to 25%.[19],[20],[21] In last two decades, authors have attempted wide excision with instrumented fusion specially for the aggressive disease with variable success.[22] En bloc resection with wide margins is ideal treatment of choice; however, in spine, this is not feasible because en bloc resection is associated with significant morbidity. A systematic review of the studies done for the management of cervical spine ABCs showed that 56% of the patients underwent spinal stabilization following surgery.[23] The treatment of ABC depends on patient characteristics, size of the lesion, location of the lesion, and surgeon’s familiarity with different procedures.

The literature on the outcome following an instrumented fusion of an aggressive ABC of spine was scarce; hence, we decided to study the clinicoradiological characteristics and surgical outcomes in these aggressive tumors.

 Materials and Methods



Patients

In this retrospective study, patients diagnosed with aggressive ABC of the spine (Enneking grade III) on the basis of computed tomography (CT), magnetic resonance imaging (MRI), and surgical findings, which were managed in our unit from January 2007 to December 2016, were included. There were seven patients (four males; three females; mean age, 15.6 years, range, 6–23 years). All the patients with ABCs involving vertebral elements were included, with or without the presence of the coexisting pathologies. Patients having ABC with Enneking grade I and II were excluded. Patients having ABCs, other than the vertebra, were excluded.

Clinical features

All the patients had pain with restriction of movement as the presenting complaint. Swelling was the second most common complaint in five patients (71.4%). Four patients (57%) had presented with motor weakness and two patients (28.6%) had bladder and bowel symptoms. Duration of presenting symptoms ranged from 1 month to 12 months; mean duration was 3.6 months.

Imaging

All the patients had preoperative X-ray, CT spine with reconstruction, and MRI spine with contrast of the relevant level. Postoperatively, patients were followed up with MRI spine at the region of interest and non-contrast CT scan of the region of interest. All patients had postoperative MRI spine. All the images were accessed through the institutional picture archival and communication system.

Surgery

The primary treatment of all the seven patients was surgical with attempted total excision. Six patients underwent instrumented fusion while in one it was not deemed necessary. We were able to achieve gross total excision in four patients whereas in three patients only subtotal excision was achieved. One patient with extensive lumbosacral disease underwent SAE preoperatively followed by surgery. Two patients with significant postoperative residue received radiotherapy. Average duration of the surgery and the blood loss were assessed.

Follow-up

Patients were followed up periodically in the outpatient clinic or through a telephonic interview to assess their functional status, ability to perform the activities of daily life independently, and survival. Patients underwent MRI, CT, and X-rays of the relevant region to ascertain the residual disease.

Surgical outcome

Surgical outcomes were assessed in terms of surgical morbidity, mobility, residual lesion, need for adjuvant therapy, change in the Frankel grade, and functional outcome.

Statistical methods

Data was entered in Excel software (Microsoft, Seattle, WA) and was analyzed using SPSS software, version 11.5 (SPSS, Inc., Chicago, IL).

 Results



Clinical features

Three patients (42.9%) had preoperative Frankel grade C, three (42.9%) had Frankel grade D, and one patient (14.3%) had Frankel grade E. All the Frankel grade D patients improved to grade E postoperatively. One Frankel E patient remained the same. Two of the Frankel grade C patients improved to grade E, but one patient was grade D after the surgery till the last follow-up. Four patients (57.1%) had evidence of neurological involvement, either in form of myelopathy or in the form of radiculopathy.

Radiological features

The radiological features of the tumors are summarized in [Table 1]. The patients were evaluated by an X-ray, a CT scan, and an MRI of the spine. The CT scan showed an expansile osteolytic lesion involving the vertebral elements. The tumors were common in the thoracic region (three cases, 42.9%), followed by cervical and lumbosacral (two cases each, 28.6%). Five cases (71.4%) had an involvement of all the three elements. One patient (14.3%) had an involvement of the anterior and middle elements and another patient (14.3%) had involvement of the middle and posterior elements.{Table 1}

Surgical aspects

Laminectomy + posterior instrumented fusion

Laminectomy comprises removing the entire disease part of the lamina, facets, and pedicles and the soft tissue till normal bone was seen all around [Table 2] and [Table 3]. Pedicle screws were placed two levels above and below the level of diseased lamina, and posterior fusion was done using the rods and caps.{Table 2} {Table 3}

360° fusion (anterior and posterior approach)

One patient with extensive lumbopelvic ABC underwent this procedure that began with an anterior approach in supine position with removal of the diseased portion in the pelvis. Through a posterior approach, the disease in the posterior compartment was cleared till normal bone was seen all around. This was followed by lumbopelvic fixation. One patient with extensive ABC in the cervical region involving the C5 body and posterior elements was successfully managed through a 360° fusion with Harm’s cage and plating anteriorly supported by cervical lateral mass fixation from behind with a very good disease control [Figure 1].{Figure 1}

360° fusion through a single-stage posterior approach alone

We had three patients who underwent this procedure. In two patients, the disease was confined to the thoracic region and one in the lumbar region. After positioning the patient prone for surgery, a midline skin incision exposed the laminae two levels above and below the region of interest. Pedicle screws were placed two levels above and below the diseased segment. A costotransversectomy at the level of the lesion on the more symptomatic side was done followed by a laminectomy to decompress the cord in the thoracic region tumors. Through the posterolateral corridor provided by the costotransversectomy, the diseased vertebra was removed using a high-speed diamond burr. A layer of anterior cortex was preserved, and a titanium mesh cage filled with autologous bone graft was placed into the corpectomy defect. On completing the ventral bone work, the rods were placed onto the screw heads and tightened [Figure 2]. In the patient with a lumbar ABC, we were able to clear the diseased body through a corridor created after facetectomy and laminectomy. Corpectomy defect was filled with a Harm’s cage followed by posterior fusion with rods and caps with a cross connector.{Figure 2}

The average blood loss was 750 mL, and the average duration of surgery including instrumentation was 3 hours. All patients underwent intralesional en bloc resection and the tumors were classified using the Weinstein, Boriani, and Biagini (WBB) classification. These results are summarized in [Tables 2] and [3].

Surgical morbidity and mortality

Postoperatively, none of the patients developed any complication except for one patient who underwent a lumbopelvic fixation and developed transient weakness of the hip flexion which resolved completely at the time of discharge. There was no perioperative surgical mortality.

Pathology

The histopathology was consistent with ABC in all the cases. This is depicted in [Figure 3].{Figure 3}

Adjuvant therapy

One patient received preoperative SAE before undergoing the gross total excision of the lumbosacral ABC and lumbopelvic fixation as the disease was extensive [Table 2]. This patient had small residue in the pelvic cavity that responded well to bisphosphonates. At last follow-up (8 years after the surgery), she had stable residue. One patient with C2 body ABC was treated with intralesional bone cement injection after laminectomy and supported by occipitocervical fusion as the disease was involving two columns and the C2 body was brittle due to tumor destruction. Two patients received postoperative radiotherapy as they underwent partial excision and had residual disease. All patients received 3D conformal RT (25–30 Gy) over 10–15 fractions. Patients tolerated RT well. They had no side effects related to radiation till their last follow-up.

Outcomes

At a mean follow-up of 4.5 years, all patients were disease-free with significant improvement in their neurological status. Majority of patients 6/7 (85%) had good postoperative Frankel grade E at follow-up.

 Discussion



ABC is generally considered as a rare, reactive, non-neoplastic, and hyperemic lesion of the bone.[19] Papagelopoulos et al.[19] in 1998 studied 52 cases and found the predilection of the spinal ABC in thoracic and cervical spine with a slight male predominance in contrast to the previous studies.[21],[24] Our study results were consistent with Papagelopoulos et al.[19] Although trauma has been considered as one of the causative factors for the ABC, especially due to their hemorrhagic nature,[13],[25] none of our patients had any history of trauma before presenting to us. Although these lesions are considered benign, aggressive ABCs are characterized by rapid progression and destruction of the bone with or without spinal instability or cord compression with neurological deficits. Reversal of the symptoms and deficits were noted soon after the surgical management of the pathology in multiple previous series.[5],[26] This was observed in our series too, as all our patients had significant improvement in their symptoms after the surgery [Table 2]. Our patients could be ambulated on the first postoperative day following the instrumented stabilization and showed excellent response toward the same. Some authors[27],[28],[29] practiced spinal fusion in case of instability resulting after the wide excision or the corpectomy in past with mixed results. We think that most extensive and aggressive lesions, involving all the three elements of the vertebra, especially in thoracic region, should be fused, as there are high chances of kyphoscoliosis without instrumentation.[30],[31],[32],[33] As per the Enneking’s recommendation, both inactive and active tumors can be successfully treated with simple curettage, while locally aggressive tumors should be treated with en bloc resection.[17] En bloc resection effectively controls the local recurrence and progression, but is associated with significant morbidity and potential neurological complications in comparison to the intralesional curettage.[33] Hence, en bloc resection of the ABC in the spine is difficult and technically demanding. Some authors found selective arterial embolization (SAE) an effective way of managing ABC.[33],[34],[35],[36],[37] Few authors prefer SAE as the first line of treatment of ABC; however, its contraindicated in patients with pathological fracture or with neurological deficits.[13],[33],[34],[35],[36],[37],[38] Terzi et al.[38] have found SAE to be a safe procedure with a healing rate of 74% with very few recurrences in their series; however, the efficacy of SAE was less than expected as 26% of their patients had deterioration in the course of therapy and warranted crossing over to surgery or to another therapy. Furthermore, the study lacked the description on the subgroup of the patients (as per the Enneking’s classification) who underwent SAE. Boriani et al.[32] found no treatment failures in patients undergoing SAE, but they frequently had patients with incomplete treatment. Of the spinal ABC in their series, 88% required two embolization procedures and more than one-third of patients required more frequent embolization. To achieve the results, several patients required two or more sittings. Most of the patients affected by the spinal ABCs are children. Multiple angiograms increase the radiation exposure and increase the risk of carcinoma in future.[39] At our center, most of the Enneking grade I and II, patients receive either SAE or curettage with or without grafting or both. All seven patients in this study had Enneking grade III lesions, which pose a significant challenge if treated with nonsurgical methods, as they are prone to get pathological fractures and instability. En bloc excision with spinal stabilization may be considered as a better option in this subgroup of the patients as they have gratifying results.

The use of embolization in our study was limited to reducing the vascularity before the definitive management, for embolization as a primary modality of treatment carries the disadvantage of delayed relief from the symptoms. It also carries the risk of disease progression. Some previous studies agree with the fact that, with rapidly worsening symptoms, especially if the weakness is one of the presenting complaints due to cord compression, there is hardly any time to consider embolization.[19]

Traditionally treatment of Enneking grade III ABC has been surgical as it gives the best chance of immediate neurological improvement. Aggressive surgery decreases the chance of recurrence. As most of the recurrences are seen at the end of first year after surgery, a closer follow-up is warranted in all patients who underwent less than en bloc resection.[39] Intralesional en bloc resection of the lesion is most important to obviate the risk of recurrence. Hence, we adopted this strategy for all our patients aiming for an intralesional en bloc resection to the extent possible. This is supported by instrumentation as adolescents have high incidence of postlaminectomy kyphosis and scoliois. Recent metanalysis by Parker et al.[40] reports recurrence rates of 42.3% with decompression and laminectomy, 37.5% with partial excision, and 25% recurrence rates with curettage as compared to 8.2% with complete excision. The results of their study revealed good surgical results, almost 0% recurrence rates in patients who have undergone curettage along with an adjuvant therapy that includes radiotherapy, phenol, or cryotherapy.

ABCs are radiosensitive. RT should be reserved for the progressive residue, rather than a routine postoperative adjuvant therapy as there is risk of post radiation sarcoma to the site[39] and risk of myelopathy.[40] In our study, two patients received postoperative radiation due to a significant surgical residue. RT following the SAE can be considered as a method for the inoperable cases.[33],[34] With advancement, novel approaches have been tried for treatment of ABC with varied results. Basu et al.[41] have described the usage of bone cement augumentation in two cases treated with curettage. Setting of bone cement is an exothermic reaction that results in thermal coagulation of the surrounding tissue, thus decreasing the blood loss during curettage and it also exerts the antitumor effect.[42] We have successfully used this technique in one patient with C2 body ABC after intralesional curettage.

Recent studies have thrown light on specific genetic translocations that occur in ABCs that offer a potential target for gene therapy.[43] As ABCs share same pathophysiology as giant cell tumor, encouraging results have been published by few authors who report the usage of denosumab, a monoclonal antibody that blocks RANKL interaction with RANK.[44],[45] The usage of denosumab has been approved for treatment of osteoporosis, multiple myeloma, and giant cell tumors. Long-term studies are required to study the efficacy and side-effects of these novel drugs.

 Conclusion



ABCs are benign lesions with aggressive local behavior. Aggressive ABCs pose a significant challenge due to faster growth, risk of spine instability, and postoperative recurrence. There are various treatment options, including intralesional curettage, en bloc resection, and SAE. En bloc excision with negative margin with or without instrumented stabilization provides effective and fast pain relief, early mobility, and is associated with good surgical and long-term outcomes. Clinical profile of the patient, expertise of surgeon, or interventional radiologist, location, size, and aggressiveness of lesion should be taken into account to individualize the primary treatment modality in spinal ABC.

Financial support and sponsorship

Nil.

Conflicts of interest

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

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