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THE SPINE SCHOLAR VOLUME 1, NUMBER 1, 2017 SEATTLE SCIENCE FOUNDATION

REVIEW

Cervical Spine Aneurysmal : A Meta-Analysis of 114 Cases and Comparison of Clinical Features between Pediatric and Adult Patients

Matthew Protas1, Henry Wingfield2, Basem Ishak3, Rong Li4, Rod J. Oskouian2, Marios Loukas1, R. Shane Tubbs2

1 Department of Anatomical Sciences, St. George’s University, Grenada 2 Seattle Science Foundation, Seattle, WA, USA 3 Department of Neurosurgery, University of Heidelberg, Heidelberg, Germany 4 Department of Pathology, Children’s of Alabama, Birmingham, AL, USA http://thespinescholar.com https://doi.org/10.26632/ss.4.2017.1.1

Key words: pathology, children, disease, vertebrae, neck

ABSTRACT

Aneurysmal bone cysts have an unclear etiology and are most common during childhood. To our knowledge, a comprehensive review comparing adult and childhood aneurysmal bone cysts has, to date, not been performed. Using standard search engines, a review of aneurysmal bone cysts was conducted. Many differences were found comparing adult and pediatric ABC patients. For example, females were much more commonly affected than males in children and tumors were commonly idiopathic however, they were found after cervical spine trauma in children. Pediatric patients are significantly more likely to be affected by ABC than adults. The incidence of primary tumors is much higher than that of secondary tumors in both adults and children but there is no significant difference between the two groups. Radicular pain is more significantly associated with children with cervical ABC. Pediatric patients are at a significantly higher risk for tumor reoccurrence and suffer from more postoperative symptoms. Spine Scholar 1:21-29, 2017.

INTRODUCTION

Aneurysmal bone cysts (ABC) are benign osteolytic lesions of unknown etiology and are non-neoplastic and often rapidly-expanding (Aho et al., 1982) (Figs. 1 and 2). They represent roughly 15% of all primary spine tumors (Ameili, 1985) with a reported incidence rate of 1.4/100.000 (Boriani et al., 2001), and represent the third most frequent benign after osteoid osteoma and (Hay et al., 1978). The incidence of ABC is greatest within the first two decades of life and female patients are slightly more susceptible (Cottalorda et al., 2007). Clinical symptoms are swelling and pain or pathological fractures that lead patients to present themselves clinically. Neurological symptoms, especially when they involve the spine, are rare (McDonald et al., 1992; Mohan et al., 1989). Although ABC can affect all bone types, approximately 10- 30% are located in the thoracic and lumbar spine (Boriani et al., 2001). Of these spinal ABC, 2% involve the cervical spine and typically affect the posterior elements (Boriani et al., 2001; Adkbarnia et al., 1988; Hay et al., 1978). According to Enneking (1983), ABC are subdivided into three stages (1 to 3). A precise staging is of the upmost importance for determining operative strategies. The surgical treatment of cervical ABC can be challenging owing to their close proximity to neural and vascular structures and to the stabilization that is often required after surgery, especially for children and adolescents in whom the skeleton is still growing. Current strategies for surgical treatment of the cervical spine include en bloc excision of the cystic wall thorough curettage followed by spinal stabilization, selective arterial embolization and radiation therapy (Wang et al., 2014; Szendroi et al., 1992). A malignant transformation of ABC is extremely rare, but has been described after irradiation (Aho et al., 1982; Capanna et al., 1985; Farsetti et al., 1990). Therefore, this treatment option should be considered as a last resort when the patient is young.

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Figure 1: Coronal CT image of 14-year-old female with ABC of C3 body.

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Figure 2

There have been few accounts of cervical spine ABC in the literature and most of the available articles are case reports. Therefore, the best treatment strategy is still unclear. Since most patients (80%) are affected during the first two decades of life (Hsu et al., 2009), there is a lack of literature reports on adult patients who suffer from cervical spine ABC. There are no publications analyzing adult patients with cervical spine ABC or comparing them to pediatric patients. To improve understanding of its clinical features, a meta-analysis was performed on all published cases of cervical spine ABC in adult patients, with comparisons to pediatric cases.

METHODS

Search strategy A meta-analysis was conducted using PubMed, Emase, Scopos, Cochrane Library and Google Scholar to retrieve studies reporting ABC in the cervical spine; it was last updated in August 2016. The medical terms and text words used were “aneurysmal bone cysts + spine” or “aneurysmal bone cysts + cervical spine” or “cystic lesion + spine” or “cystic lesion + cervical spine”. Appropriate publications in the reference lists of the most relevant articles were also manually searched. There were no restrictions on the dates of publications reviewed in the meta-analysis. The final searches retrieved 71 available case studies of pediatric patients and 43 of adult patients suffering from ABC of the cervical spine. The adults were compared to the pediatric patients. Our definition of a pediatric patient was age 15 years or younger. Publications were excluded if not in English. Inclusion criteria required a confirmed diagnosis of a primary or secondary ABC from the cervical spine. A secondary

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ABC was defined as one being caused by another pathology such as fibrous dysplasia. Solid body ABCs were also included in this analysis.

RESULTS

The average age of the adult population was 24.6 years and that of the pediatric population 10.3 years. There was also a significant difference between the percentages of pediatric (62.23%) and adult (37.7%) patients affected (P < 0.001). There was no significant group difference between male (33.8% pediatric vs. 46.5% adult, P > 0.05) or female (66.2% pediatric vs. 53.5% adult, P > 0.05) patients, and there was no sex difference in the incidence of cervical spine ABC in the adult population (46.5% males vs. 53.5% females, P > 0.05). However, there was a significant difference between males and females in the pediatric population (33.8% males vs. 66.2% females, P < 0.0001).

PEDIATRIC* ADULT SIGNIF. PEDIATRIC ADULT AGE SIGNIF. POPULATION POPULATION AGE (YEARS) (YEARS)

P = 0.0001* P = 0.0001F

MALE 24* (33.80%) 20F (46.51%) P = 0.177 9.71±2.95 24.85±9.88 P < 0.0001

FEMALE 47* (66.20%) 23F (53.49%) P = 0.177 10.57±3.31 24.48±12.11 P < 0.0001

TOTAL 71 (62.28%) 43 (37.72%) P = 0.0002 10.28±3.10 24.65±11.13 P < 0.0001

Table 1. Demographics of pediatric and adult patients with cervical spine ABC. There was a significant difference between the adult and pediatric patient populations (P < 0.001). There was no significant difference between males (P = 0.117) and females (P = 0.117), between the adult and pediatric populations (P > 0.05), or between the numbers of males and females in the adult population. There were significant differences between males and females in the pediatric population (P < 0.0001)* and adults (P < 0.001)F.

No significant differences could be found between the incidences of primary (97.18% pediatric vs. 90.70% adults) and secondary (2.82% pediatric vs. 9.30% adults) cervical spine ABC between the adult and pediatric populations (P > 0.05). Among pediatric patients, 86.9% had an ABC not resulting from trauma; the corresponding percentage among the adults was 97.44%; the difference was not significant (P > 0.05). However, more of the pediatric patients had trauma-induced ABC of the cervical spine than ABC with other etiologies. The adult and pediatric populations did not differ significantly in the types of secondary ABC or in the prevalence of solid body tumors (P > 0.05) (Table 2).

TYPE OF ABC PEDIATRIC ADULT SIGNIFICANCE PATIENTS PATIENTS PRIMARY P < 0.0001* P < 0.0001F Total 69 (97.18)* 39 (90.70%)F P = 0.845 No trauma 60 (86.95%) 38 (97.44%) P = 0.826 Trauma 9 (13.04%) 1 (2.56%) P = 0.07 Solid body 2 (2.90%) 1 (2.56%) P = 0.919 SECONDARY Total 2 (2.82%)* 4 (9.30%)F P = 0.133 Giant Cell Tumor 1 (50%) 0 P = 0.212 Osteochondroma 1 (50%) 0 P = 0.212 0 2 (50%) P = 0.221 Radiation Induced 0 1 (25%) P = 0.438 Chondromyxoid 0 1 (25%) P = 0.438 Fibroma

Table 2. Type of cervical spine ABC in adult and pediatric patients as reported in case studies. There were no significant differences between any of the categories. There was a significant difference between the numbers of primary and secondary tumors in both pediatric and adult patients (P < 0.0001).

Of the 71 pediatric and 43 adult cases analyzed, only 59 and 31 respectively reported symptoms. There was a significant difference between the percentages of adult (3.22%) and pediatric (20.33%) patients who suffered from

THE SPINE SCHOLAR 24 VOLUME 1, NUMBER 1, 2017 radiculopathy as a result of cervical spine ABC (P < 0.05). There was no significant difference between the two populations in respect of other symptoms. However, in both populations, the most common symptom reported as a result of a cervical spine ABC was nonspecific neck and shoulder pain (81.36% pediatric, 77.41% adults) (Table 3).

SYMPTOMS PEDIATRIC PATIENTS ADULT PATIENTS SIGNIFICANCE NONSPECIFIC NECK OR 48 (81.36%) 24 (77.41%) P = 0.657 SHOULDER PAIN HEADACHES 5 (8.47%) 3 (9.68%) P = 0.849 RADICULAR PAIN 12 (20.33%)* 1 (3.22%)* P = 0.028* SPASTIC QUADRIPLEGIA 1 (1.69%) 2 (6.45%) P = 0.978 PARAPLEGIA 1 (1.69%) 0 P = 0.466 LIMB WEAKNESS 7 (11.86%) 7 (22.58%) P = 0.183 URINARY INCONTINENCE 2 (1.69%) 0 P = 0.300 TORTICOLLIS 4 (6.78%) 0 P = 0.138 PARESTHESIA 5 (8.47%) 0 P = 0.0954 URINARY RETENTION 0 1 (3.22%) P = 0.165 DYSPHAGIA 0 1 (3.22%) P = 0.165 DYSARTHRIA 0 1 (3.22%) P = 0.165

Tables 3. Symptoms reported by pediatric (n=59) and adult (n=31) patients. There was a significant difference between adult and pediatric patients suffering from radicular pain (P < 0.05) but no significance in any of the other categories (P > 0.05).

Of the 71 pediatric and 43 adult cases analyzed, only 70 and 43 respectively reported the spinal level affected by the cervical spine ABC. There were no significant differences between the adult and pediatric populations in the prevalence of ABC at any spinal level. Patients in both populations most frequently presented with ABC at the C2 (34.28% pediatric vs. 34.88% adult) followed by C5 (24.28% pediatric vs. 20.93 adult) (Table 4).

SPINAL LEVEL PEDIATRIC PATIENTS ADULT PATIENTS SIGNIFICANCE C1 7 (10%) 5 (11.63%) P = 0.785 C2 24 (34.28%) 15 (34.88%) P = 0.948 C3 15 (21.43%) 5 (11.62%) P = 0.185 C4 14 (20%) 7 (16.28%) P = 0.622 C5 17 (24.28%) 9 (20.93%) P = 0.681 C6 13 (18.57%) 7 (16.28%) P = 0.756 C7 11 (15.71%) 6 (13.95%) P = 0.799 MULTI-LEVEL 26 (37.14%) 11 (25.58%) P = 0.204 THORACIC INVOLVEMENT 6 (8.57%) 1 (2.32%) P = 0.215

Table 4. Spinal level affected by cervical ABC reported in pediatric (n=70) and adult (n=43) patients. There were no significant differences between the adult and pediatric patients at any level of the spine.

Only 52 of the 71 pediatric cases and 21 of the 43 adult cases reported the specific location affected by a cervical spine ABC. There were no significant differences between the pediatric and adult populations in the area of the spine affected (P > 0.05). Posterior elements were the most affected areas of each spinal level in both the pediatric (86.54%) and adult (85.71%) populations. Among the posterior elements, the lamina was most affected in pediatric patients (36.54%) while the pedicles, spinous process, and lateral mass (28.57% for all) were most likely to be affected in adults with a cervical spine ABC (Table 5).

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LOCATION IN VERTEBRAE PEDIATRIC PATIENTS ADULT PATIENTS SIGN. VERTEBRAL BODY 26 (50%) 10 (47.62%) P = 0.115 LAMINA 19 (36.54%) 4 (19.05%) P = 0.097 PEDICLE 8 (15.38%) 6 (28.57%) P = 0.195 SPINOUS PROCESS 11 (21.15%) 6 (28.57%) P = 0.497 LATERAL MASS 11 (21.15%) 6 (28.57%) P = 0.497 FACETS 5 (9.62%) 1 (4.76%) P = 0.494 ODONTOID PROCESS 3 (5.77%) 1 (4.76%) P = 0.864 POSTERIOR ELEMENTS 45 (86.54%) 18 (85.71%) P = 0.926 TRANSVERSE PROCESS 5 (9.62%) 0 P = 0.141 UNREPORTED* 19 22

Table 5. Location of the vertebrae affected by cervical ABC in pediatric (n=52) and adult (n=21) patients. There were no significant differences between the adult and pediatric patients for the area of the spine (P > 0.05). *Literature that did not report the specific location of the ABC in the vertebrae.

The exact treatment of ABC was reported in 50 pediatric cases and 30 adults. There was no significant difference between the surgical approaches to the pediatric and adult patients. Adult patients most frequently underwent posterior approaches for tumor resection (50%) while pediatric patients most frequently underwent dual approaches (50%). Both population groups frequently received further stabilization. The other treatment methods are shown in Table 6.

THERAPY PEDIATRIC PATIENTS ADULT PATIENTS SIGN. ANTERIOR APPROACH ONLY 6 (12%) 6 (20%) P = 0.332 POSTERIOR APPROACH ONLY 19 (38%) 15 (50%) P = 0.293 DUAL APPROACH 25 (50%) 9 (30%) P = 0.08 EXCISION WITH RECORDED APPROACH 50 30 - CALCITONIN AND 3 0 - METHYLPREDNISOLONE RADIOTHERAPY 15 7 - INTRAOSSEOUS INJECTION OF 1 0 - DOXYCYCLINE SELECTIVE ARTERIAL EMBOLIZATION 16 11 - SPINAL STABILIZATION 40 27 - CRYOABLATION 1 0 -

Table 6. Treatment used in cervical spine ABC for both pediatric and adult patients. There were no significant differences between the approaches in either population (P > 0.05).

Significantly more tumors reoccurred in the pediatric (28.17%) than the adult (6.98%) patients (P < 0.05). The reasons for reoccurrences of ABC between the adult and pediatric populations were not significantly different (P > 0.05) (Table 7). Postoperative complications were more prevalent in the pediatric population than the adults (Table 8).

REASON FOR RECURRENCE PEDIATRIC PATIENTS ADULT PATIENTS SIGN. SUBTOTAL RESECTION 4 (25%) 1 (33.67%) P = 0.602 EMBOLIZATION TREATMENT 4 (25%) 1 (33.67%) P = 0.602 INTRAOSSEOUS INJECTION OF 1 (4%) 0 P = 0.692 DOXYCYCLINE CALCITONIN AND 3 (15%) 0 P = 0.472 METHYLPREDNISOLONE UNKNOWN WHETHER TOTAL OR 7 (35%) 1 (33.67%) P = 0.955 PARTIAL EXCISION TOTAL RECURRENCES 20 (28.17%) 3 (6.98%) P = 0.006*

Table 7. Reasons for reoccurrences of cervical spine ABC in both pediatric and adult patients. There was a significant difference between the recurrence rates in adults and children (P < 0.05) but no significance in any of the other reasons for reoccurrence (P > 0.05).

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SYMPTOMS PEDIATRIC PATIENTS ADULT PATIENTS GRAFT 1 (7.69%) 1 (50%) WEAKNESS 2 (15.38%) 0 DYSPHONIA 1 (7.69%) 1 (50%) HORNER’S SYNDROME 4 (30.76%) 0 NONSPECIFIC NEUROLOGICAL 2 (15.38%) 0 DEFICITS THYROID FAILURE 1 (7.69%) 0 VERTEBRAL ARTERY INJURY 1 (7.69%) 0 SEROMA 1 (7.69%) 0 DYSPHAGIA 2 (15.38%) 0 RADICULOPATHY 1 (7.69%) 0 BETWEEN C1-C2 1 (7.69%) 0

Table 8. Postoperative complications in both pediatric and adult patients

DISCUSSION

Although the exact cause of ABCs is currently being debated, it is believed caused by local circulatory disturbances resulting in vascular engorgement (Cottalorda et al., 2007). Other suggested reasons are vascular destruction in the bone, improper repair of a traumatic injury involving a subperiosteal hemorrhage, or a hemorrhage secondary to a preexisting pathology (Boriani et al., 2001). Reactive reparative processes are thought to be the cause of secondary ABCs, which are due to existing pathologies such as giant cell tumors, osteoblastomas, or fibrous dysplasias (Boriani et al., 2001). Among the cervical spine ABC cases we studied, 87.5% were reported in patients before the second decade of life, which is slightly higher than that of the rest of the body as reported in the previous literature. Seventy percent of ABC are reported as primary while the remaining 30% are secondary to other associated pathologies (Fletcher et al., 2006). In this analysis of the cervical spine, we found a significant difference in the prevalence of primary (97.18% pediatric vs. 90.70% adult) and secondary (2.82% pediatric vs. 9.30% adult) cervical spine ABC, primary being more prevalent in both the adult and pediatric populations (P < 0.0001). Both were also much higher than the overall ABC occurrence rate reported in the literature. Trauma has been reported as a primary cause of cervical ABC (Boriani et al., 2001). In our analysis, trauma was the reported cause in 13.04% and 2.56% of the pediatric and adult patients respectively. In our opinion, the role of trauma in the pathogenesis of cervical ABC should not be underestimated. The cervical spine, especially in children, is especially susceptible to trauma. Pediatric patients who suffered from serious injuries presented immediately with symptoms (Doyle et al., 2015; Sebaaly et al., 2015). However, minor cervical trauma can lead to slowly growing ABC for which symptoms present either years later or not at all, so they are only discovered incidentally during imaging. However, there was no significant difference in this study between adults and pediatric patients in the reported incidence of trauma leading to cervical spine ABC. The male to female ratio in the largest study to date of pediatric patients is 1.6 F/M (n=47) (Sebaaly et al., 2015). In the present analysis of 114 patients, there was a higher prevalence of females with cervical spine ABC than previously reported in both pediatric patients (F/M = 1.9, n=71) and adults (F/M = 1.15, n=43). C2 (26%), followed by C5 (17%), are the most common vertebrae affected by ABC (Novias et al., 2011). The present analysis revealed a higher frequency of both C2 (34.28 pediatric vs. 34.88% adult) and C5 (24.28% pediatric vs. 20.93 adult) vertebra ABC than the previous literature. Posterior elements are the most frequently affected areas by an ABC, with a reported incidence of 75% in the literature (Sebbaly et al., 2015; Boriani et al., 2001; Ameli et al., 1985). The present analysis revealed a higher incidence of posterior element involvement in both pediatric (86.54%) and adult (85.71%) patients. The parts of the vertebrae most affected by cervical spine ABC according to the literature are the lamina, pedicles and spinous processes of the cervical spine (Mankin et al., 2005). There are no clear reports of the incidence rates of effects in these areas of the spine. There were some minor differences (not significant) between the adult and pediatric populations: The lamina was most affected in pediatrics while the pedicle, spinous process, and lateral masses were most affected in adults. The reason for this difference is unknown and needs to be further investigated. The general nature of the symptoms associated with cervical spine ABC make diagnostics difficult without imaging. Most commonly, both pediatric and adult patients presented with neck and shoulder pain, which makes the correct diagnosis difficult. Radicular pain presented significantly more in pediatric patients than adults. CT imaging will typically show a lytic lesion with ballooning of the cortex, described as an eggshell or honeycomb, which is characteristic of ABC of the cervical spine (Boriani et al., 2001; Zenonos et al., 2012). T2-weighted MRI is used to rule out any differential diagnosis such as fibrous dysplasia, telangiectatic osteosarcoma, , osteoblastoma or giant cell tumors, and to facilitate a definitive diagnosis that can only be confirmed by histological analysis (Liu et al., 2003; Caro et al., 1991; Boriani et al., 2001). A characteristic fluid-fluid interface on T2-weighted imaging and a heterogeneous appearance on T1-weighted images can also help in diagnosing a cervical spine ABC (Caro et al., 1991). Therapy options for a cervical spine ABC differ among cases and depend on factors such as location, symptoms, age, and vertebral artery involvement (Griauzde et al., 2015). This could account for the differences in approach chosen for pediatric and adult patients in removing cervical spine ABC. Optimal treatment is complete surgical resection of the tumor with

THE SPINE SCHOLAR 27 VOLUME 1, NUMBER 1, 2017 subsequent spine stabilization, if spinal instability develops after surgery (Boriani et al., 2001; Ameli et al., 1985). Spontaneous resolution is a possible option for asymptomatic elderly patients (Griauzde et al., 2015). However, this is not recommended owing to the rapidly expanding nature of ABC (Griauzde et al., 2015). The number of ABC that goes unnoticed and spontaneously resolves themselves in elderly patients is also unknown. The surgical approach will vary depending on the location of the tumor especially if it extends from the posterior elements into the vertebral body (Novias et al., 2011). The success rate of embolization-only depends on the vascularization of the tumor. The cervical spine is highly vascularized and it is difficult to reach the target, so embolization as an exclusive treatment is not recommended (Griauzde et al., 2015). Calcitonin and methylprednisolone acetate injections are effective treatments for inaccessible ABC (Szendroi et al., 1992). Their proposed therapeutic action is to inhibit osteoclastic activity and promote bone regrowth (Szendroi et al., 1992). Only partial healing of the ABC is noted, but the symptoms are typically alleviated (Gladden, 1976). The recurrence rate given in the literature is around 20-30% in the cervical spine (Garg et al., 2005; Novais et al., 2008; De Kleuver et al., 1998). There was a significant difference between the percentages of pediatric patients (28.17%) and adults (6.98%) who suffered tumor recurrence. The recurrence rate among pediatric patients in the populations analyzed could have been higher because they received more embolization-only treatments, treatments with calcitonin and methylprednisolone, and experimental treatments. The rate of complications in postoperative cervical spine treatments is reported as between 15 and 30% (Boriani et al., 2001; Sebaaly et al., 2015). The postoperative complication rate in pediatric patients (18.31%) was consistent with the previous literature, but the complication rate in adults was much lower (4.65%). A possible reason for the difference could be the more frequent use of a dual approach to tumor resection.

CONCLUSION

Pediatric patients are significantly more likely to be affected by ABC than adults. The F/M ratio is lower in adults than children but the difference is not significant. The incidence of primary tumors is much higher than that of secondary tumors in both adults and children but there is no significant difference between the two groups. Radicular pain is more significantly associated with children with cervical ABC. A dual approach for tumor resection was required more frequently in pediatric patients (50%) than adults, who received mostly posterior approaches (50%). Cervical stabilization was needed in most cases. Pediatric patients are at a significantly higher risk for tumor reoccurrence and suffer from more postoperative symptoms.

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Corresponding author: Matthew Protas, [email protected]

THE SPINE SCHOLAR 29 VOLUME 1, NUMBER 1, 2017