The bony spine is overall the third most common site for distant cancer metastasis, with the cervical spine involved in approximately 8 to 20% of metastatic spine disease cases. Diagnosis and management of metastatic spine disease requires disease categorization into the compartment involved, pathology of the lesion, and anatomic region involved. The diagnostic approach should commence with careful physical examination, and the workup should include plain radiographs, magnetic resonance imaging, computed tomography, and bone scintigraphy. Management ranges from palliative nonoperative to aggressive surgical treatment. Optimal management requires proper patient selection to individualize the most appropriate treatment modality.
The skeletal system is the third most common site after the lungs and liver for distant cancer metastasis regardless of primary tumor pathology. Within the skeletal system, the bony spine is the most commonly affected site, with approximately 33% of cancer patients developing metastatic spine lesions. However, despite the bony spine being the most common site of osseous involvement for patients with metastatic cancer, the cervical spine is only involved in 8% to 20% of metastatic spine disease cases. Nonetheless, given the 1.5 million newly diagnosed cases of cancer annually, encountering metastatic lesions within the cervical spine is not of rare occurrence.
The initial approach to diagnosis and management of cervical spine tumors requires an organizational framework that categorizes a presentation according to the compartment involved, the pathology of the lesion, and the anatomic region involved. The compartment involved refers to whether the lesion is located in the epidural, intradural-extramedullary, or intramedullary compartment, and is essential in not only formulating an initial differential diagnosis but also in understanding the pathophysiology of the lesion as it pertains to patient presenting signs and symptoms. The pathology of the lesion is of utmost importance, as it has the largest role in dictating management. For example, if a lesion is of primary rather than metastatic origin, then a curative surgical intervention (ie, en bloc resection) is a possibility, whereas surgical intervention in the setting of a metastatic lesion may only serve a palliative role given that the patient is most likely also concomitantly afflicted with numerous systemic lesions. The anatomic region involved is divided into 3 component regions: the craniovertebral junction (CVJ; C0–C1), subaxial spine (C3–C7), and the cervicothoracic junction (C7–T1). Each of these component regions has unique biomechanical properties, thereby influencing management decisions. For example, the surgical approach to achieving en bloc resection of a tumor affecting the CVJ is very different from the approach if the same lesion is located within the subaxial spine. This article describes the diagnosis and management of metastatic epidural cervical spine tumors based on the latter considerations.
Epidemiology
Although the thoracic spine is most commonly occupied by metastatic lesions, the cervical spine harbors metastatic lesions in 8% to 20% of cases. It is thought that the wide range in the reported incidence of cervical spine affliction is attributable to whether asymptomatic or symptomatic involvement is reported. The most common primary tumor pathologies are breast, prostate, and non–small cell lung carcinoma. The highest incidence of spinal metastases occurs among individuals in the fourth and sixth decade, and men are more likely to be afflicted than women. There are several mechanisms by which a primary neoplasm can metastasize to the spine, with the mechanism depending on primary tumor pathology. Tumor pathology dictates primary tumor location and biological behavior, both of which are factors that influence spread mechanisms. Specifically, the 3 main mechanisms by which a lesion can metastasize to the spine are direct extension or invasion, hematogenous metastasis, and cerebrospinal fluid (CSF) seeding. Direct invasion or extension occurs through primary lesions becoming locally aggressive and extending to involve the bony spine. Hematogenous seeding is facilitated by the vast arterial supply of the vertebrae and via the valveless venous drainage plexi such as Batson’s plexus. Seeding of a primary lesion through the CSF occurs much less frequently and is most often caused by surgical manipulation of primary or metastatic cerebral lesions. A retrospective study by Chaichana and colleagues found that among lesions originating from breast, kidney, lung, gastrointestinal, and prostate cancers; breast metastatic lesions were the only ones found to have a statistically significant predisposition to metastasize to the cervical spine.
Presentation
Metastatic disease to the cervical spine can present with a variety of clinical signs and symptoms ; however, it is also not uncommon to detect asymptomatic cervical metastasis when working up an unrelated problem. Presenting symptoms include mechanical, nonmechanical, and referred pain due to pathologic fracture; as well as neurologic dysfunction due to spinal cord or nerve root compression. The most common presenting symptom with metastatic cervical lesions is localized nonmechanical pain, present in approximately 89% to 93% of patients. This pain is often described as not being related to any activities, progressively worsening, and exacerbated in the evening. Furthermore, the pain can be either unilateral or bilateral as well as either focal or referred. When referred, the pain often radiates to the shoulder and trapezial area. It is important to suspect and rule out the presence of metastatic disease in the setting of a patient with a previous history of carcinoma and a new onset of nonmechanical pain.
The next most common presenting symptom is mechanical pain. This type of pain is relieved by rest and/or stabilization and is exacerbated by motion. As in the thoracic and lumbar segments, the vertebral body of a cervical vertebra is the primary site of seeding of metastatic deposits. Lytic or erosive lesions of local cancellous bone thereby increase the risk of pathologic collapse. Due to the greater proportion of cancellous bone in the subaxial spine, the presentation of mechanical pain varies according to whether the lesion involves the atlantoaxial or subaxial spine. Collapse within the subaxial spine may lead to an angular kyphotic deformity resulting in mechanical pain and/or neurologic dysfunction. Unlike the subaxial spine, metastatic spread to the CVJ is rare, only accounting for 0.5% of all metastatic spine lesions. Given the anatomic uniqueness of the CVJ, cancellous bone destruction in the CVJ does not result in as much angular kyphosis and flexion/extension instability as in the subaxial spine. Instead, the biomechanical instability of the upper cervical spine is dependent on an intact transverse ligament and lateral articular masses. More commonly, destruction of the lateral masses results in painful rotational instability, and destruction of the C2 spinous processes accompanied by detachment of the paraspinal musculature often manifests as patients complaining of an inability to hold the head upright unassisted.
Neurologic dysfunction is the next most common presenting complaint, occurring in approximately 5% to 10% of patients. Cervical radiculopathy most commonly occurs as a result of foraminal invasion by the tumor and presents as a burning, dyesthetic type of pain. Long tract signs are the next most common and include atrophy of intrinsic hand muscles, ambulation difficulty, myelopathic hand syndrome, and extremity spasticity. Autonomic dysfunction such as sphincter disturbance is the least common, often being a late finding that indicates advanced disease and thus a poor prognosis for neurologic function recovery. In general, spinal cord compression occurs more commonly in the subaxial area for several reasons. First, tumor or retropulsed bone invading the anterior epidural space is more common with tumor in the subaxial spine vertebral bodies. Second, there is a relatively larger spinal canal in the atlantoaxial region compared with the subaxial spine, so lesions can grow larger at the craniocervical junction prior to spinal cord compression. Finally, the complex of craniocervical ligaments often serves as a barrier to invasion of the canal by ventrally situated tumors. In the subaxial spine, the only barrier is the diminutive posterior longitudinal ligament.
Presentation
Metastatic disease to the cervical spine can present with a variety of clinical signs and symptoms ; however, it is also not uncommon to detect asymptomatic cervical metastasis when working up an unrelated problem. Presenting symptoms include mechanical, nonmechanical, and referred pain due to pathologic fracture; as well as neurologic dysfunction due to spinal cord or nerve root compression. The most common presenting symptom with metastatic cervical lesions is localized nonmechanical pain, present in approximately 89% to 93% of patients. This pain is often described as not being related to any activities, progressively worsening, and exacerbated in the evening. Furthermore, the pain can be either unilateral or bilateral as well as either focal or referred. When referred, the pain often radiates to the shoulder and trapezial area. It is important to suspect and rule out the presence of metastatic disease in the setting of a patient with a previous history of carcinoma and a new onset of nonmechanical pain.
The next most common presenting symptom is mechanical pain. This type of pain is relieved by rest and/or stabilization and is exacerbated by motion. As in the thoracic and lumbar segments, the vertebral body of a cervical vertebra is the primary site of seeding of metastatic deposits. Lytic or erosive lesions of local cancellous bone thereby increase the risk of pathologic collapse. Due to the greater proportion of cancellous bone in the subaxial spine, the presentation of mechanical pain varies according to whether the lesion involves the atlantoaxial or subaxial spine. Collapse within the subaxial spine may lead to an angular kyphotic deformity resulting in mechanical pain and/or neurologic dysfunction. Unlike the subaxial spine, metastatic spread to the CVJ is rare, only accounting for 0.5% of all metastatic spine lesions. Given the anatomic uniqueness of the CVJ, cancellous bone destruction in the CVJ does not result in as much angular kyphosis and flexion/extension instability as in the subaxial spine. Instead, the biomechanical instability of the upper cervical spine is dependent on an intact transverse ligament and lateral articular masses. More commonly, destruction of the lateral masses results in painful rotational instability, and destruction of the C2 spinous processes accompanied by detachment of the paraspinal musculature often manifests as patients complaining of an inability to hold the head upright unassisted.
Neurologic dysfunction is the next most common presenting complaint, occurring in approximately 5% to 10% of patients. Cervical radiculopathy most commonly occurs as a result of foraminal invasion by the tumor and presents as a burning, dyesthetic type of pain. Long tract signs are the next most common and include atrophy of intrinsic hand muscles, ambulation difficulty, myelopathic hand syndrome, and extremity spasticity. Autonomic dysfunction such as sphincter disturbance is the least common, often being a late finding that indicates advanced disease and thus a poor prognosis for neurologic function recovery. In general, spinal cord compression occurs more commonly in the subaxial area for several reasons. First, tumor or retropulsed bone invading the anterior epidural space is more common with tumor in the subaxial spine vertebral bodies. Second, there is a relatively larger spinal canal in the atlantoaxial region compared with the subaxial spine, so lesions can grow larger at the craniocervical junction prior to spinal cord compression. Finally, the complex of craniocervical ligaments often serves as a barrier to invasion of the canal by ventrally situated tumors. In the subaxial spine, the only barrier is the diminutive posterior longitudinal ligament.
Diagnosis
Any patient with a known history of cancer presenting with persistent neck pain (including mechanical and nonmechanical) should be evaluated for a metastatic pathologic process. In addition, any patient with persistent nonmechanical pain should also receive evaluation for a neoplastic process involving the cervical spine. Physical examination is an essential part of the primary workup and should be performed meticulously to elicit important findings such as palpable masses, pain, and neurologic dysfunction—including both motor and sensory loss. The type of pain elicited can help localize the location of the lesion. Pain elicited on flexion/extension more commonly corresponds to lesions localized to the subaxial spine, whereas pain elicited on rotational motion more commonly corresponds to lesions involving the CVJ. In addition, a history of nocturnal pain and an ability to elicit local pain on applied pressure further increases the suspicion of a neoplastic process.
Early recognition of neurologic dysfunction is important, as pre-operative neurologic function is the most positive prognostic factor for postintervention neurologic status. Common signs of neurologic deficit include spasticity, hyperreflexia, paraparesis, Hoffman sign, abnormal plantar responses, and occasionally Brown-Sequard syndrome. Because tumors localized to the CVJ have a decreased incidence of neurologic manifestations due to the wider canal space of the CVJ, neurologic deficits are more often caused by antlantoaxial subluxation rather than direct cord compression. Lastly, cerebellar ataxia may occur if the neoplasm extends across the foramen magnum.
Following physical examination, imaging is the next most important step in the diagnostic workup and should include plain radiographs, magnetic resonance imaging (MRI), computed tomography (CT), and bone scintigraphy. Plain radiographs permit assessment of spinal stability, the location and extent of metastatic lesions, and evaluation of the disk space. Signs of spinal instability include progressive deformity, significant translation or angulation, and/or greater than 50% involvement of the vertebral body. Lesions are evidenced by a variety of destructive changes such as spinous process erosion, vertebral body osteolysis, and an inability to visualize the pedicle. In addition, elevation of soft-tissue shadows may also be observed. Cervical disk spaces in the setting of metastatic spine disease are well maintained unless the neoplastic process has resulted in pathologic collapse, in which case the space will be narrowed. Unfortunately, plain radiographs lack sensitivity in detecting lesions, as plain radiographs typically cannot detect lesions until 30% to 50% of the bone is demineralized.
The gold-standard imaging modality is MRI given its exceptional ability to visualize the bone-soft tissue interface, resulting in a highly detailed rendition of compression and/or invasion of osseous, neural, and paraspinal structures. For example, T2-weighted MRI can provide direct evidence of cord compression and the degree of spinal stenosis ( Fig. 1 ). Osseous invasion can be visualized as the replacement of normal marrow fat signal with neoplastic tissue. Specifically, bone marrow signal in tumor and infection shows increased and decreased intensity on T2-weighted and T1-weighted imaging, respectively. Furthermore, the use of gadolinium on T1-weighted imaging may further enhance visualization of marrow invasion by tumor tissue.
CT imaging is complementary to MRI in detecting and evaluating lesions, as it provides exceptional rendition detail of the bony spine, spinal canal, and any osseous compressive structures such as retropulsed bony fragments following pathologic collapse. Furthermore, CT with myelography is the gold-standard imaging modality for patients who have contraindications to MRI.
Of note, only 11% of metastatic cervical neoplasms are isolated lesions, with lesions also commonly occurring in both the axial and appendicular skeleton. Bone scintigraphy therefore may be used as a method for conducting a screen in search of additional metastatic lesions localizing to the skeletal system. Furthermore, bone scintigraphy is also an excellent modality to screen for possible bony metastatic lesions in high-risk patients (ie, patients with a history of prostate cancer). However, it must be remembered that bone scintigraphy is a measure of bone turnover, and findings are not specific to a neoplastic process and may be due to healing fractures, spondylosis, or infection—therefore, findings should always be confirmed by MRI or CT. Furthermore, bone scintigraphy cannot provide a detailed rendition of bony anatomy nor provide any information on the extent of cord compression.
Biopsy sampling establishes a histopathologic diagnosis and is essential in determining the surgical strategy and tumor stage. At the cervical level, an anterolateral approach with fine-needle aspiration under CT guidance can be performed to obtain a sample of the tissue in question.
Management
Optimal management of metastatic cervical spine disease requires a multidisciplinary approach including, but not limited to, medical, surgical, and radiation oncology cooperation. Treatment options range from palliative nonoperative treatment to aggressive surgical intervention; therefore, appropriate patient selection for a particular treatment modality is a crucial component of management.
Patient Selection
Patients’ characteristics such as age, medical history, current medical condition, and overall life expectancy must be considered when constructing a management plan. Although age is not an absolute contraindication to surgical management, a patient’s age must be considered in the context of systemic cancer disease and comorbid medical conditions to estimate an individual patient’s life expectancy and to assess whether that expectancy is sufficiently long enough to benefit from surgical intervention. Specifically, patients with a life expectancy of less than 8 to 12 weeks are generally more apt to undergo nonoperative management. Accurate determination of tumor pathology is also essential in patient selection, as it is the most significant prognostic factor for survival. For example, median survival of a metastatic bony lung tumor is 7 to 9 months whereas median survival for metastatic bony breast neoplasms is 30 months. A study conducted by Rao and colleagues found that the mean survival for all metastatic tumors to the bony cervical spine was 14.7 months.
Various classification systems have been published to objectively assess which patients are adequate candidates for surgical intervention in the setting of metastatic spine disease. Harrington classifies patients according to the degree of bony and neurologic compromise. Kostuik and colleagues assessed the necessity of surgical intervention based on the lesions’ likelihood of resulting in mechanical instability. DeWald and colleagues developed a system similar to that of both Harrington and colleagues and Kostuik and colleagues, with the additional component of scoring the immunocompetence of each patient. Tokuhashi and colleagues devised a system that not only assesses the pathology of the lesion in question but also considers additional spinal and extraspinal metastasis, as well as overall patient condition, neurologic status, and primary tumor pathology. Ultimately, regardless of which system is used, the practitioner must carefully weigh the risks and benefits for each individual patient when considering whether to offer surgical intervention.
Staging
Once a patient has been selected to undergo surgical management, determining the extent of surgical management (ie, palliative vs curative) requires staging of the lesion on the vertebral arch and the extent of paraspinal structure involvement. Various staging systems have been devised to determine the best form of therapeutic option ( Table 1 ). The main purpose of each system is to recommend whether a particular lesion is amenable to curative (ie, total vertebrectomy) versus palliative (ie, decompressive or debulking) surgical intervention. Of note, the scoring system proposed by Tokuhashi and colleagues allows for not only patient selection but also for planning the extent of surgical management.
| Rationale | Method | Recommendation | |
|---|---|---|---|
| Tomita Scoring System | Provides anatomic description of tumor extension within vertebrae and paravertebral tissues |
| Total en bloc spondylectomy recommended for type 2, 3, 4, and 5 lesions Relatively indicated for type 1 and 6 lesions Contraindicated for type 7 lesions |
| Weinstein-Boriani-Biagini Staging System | Precise data-gathering tool to describe tumor involvement of vertebral body and adjacent tissues |
| Tumor description using this system allows surgeon to plan surgery and gather data uniformly. Particularly useful in describing tumor involvement to other practitioners |
| Tokuhashi Scoring System | Considers extraspinal tumor involvement and overall condition to estimate patient prognosis and guide treatment |
| All categories range from 0 to 2 points with exception of primary tumor pathology (5 points maximum), placing highest prognostic weight on primary tumor site Score recommendation: <8 (<6 mo survival): nonoperative or palliative treatment 9–11 (>6 mo survival): palliative surgery or excisional surgery if single lesion and no extraspinal metastases 12–15 (≥1 year survival): excisional surgery |
Nonoperative Management
In general, nonsurgical management of metastatic spine disease is recommended when tumor involvement has not resulted in any of the following: (1) spinal instability, (2) neurologic deficit, and (3) pain nonresponsive to medical management.
Nonsurgical management includes radiotherapy, chemotherapy, hormonal therapy, and high-dose steroid therapy. Radiation therapy is most appropriate in the setting of the aforementioned indications. Additional indications for radiation therapy include the presence of multiple noncontiguous lesions affecting the bony spine and the caveat that the patient must not have been treated by this method before. The response to radiation therapy varies by tumor type, with prostate and breast tumor generally being more radiosensitive than renal and lung tumors. Positive response to tumor therapy can be measured by decreased tumor size and local pain.
Various optimal radiation-dose protocols have been proposed, but to date randomized control trials have not elucidated an optimal dosing regimen. Kaasa and colleagues, Nielsen and colleagues, and Maranzano and colleagues performed randomized controlled trials to evaluate comparative efficacies of single-dose versus fractionated-dose radiation therapy, and failed to find statistically significant differences in pain, functional, and complication outcomes.
Although radiation therapy as a primary management modality may be adequate in the absence of spinal instability and neurologic deficit, the efficacy of radiation therapy as a primary management modality in the setting of neurologic deficit without spinal instability versus that of surgical intervention has been a point of controversy. In 2005, Patchell and colleagues conducted a randomized controlled trial comparing the relative efficacy of surgery alone, radiotherapy alone, and radiotherapy and surgery combined. The group determined that both survival and functional outcomes were superior in the group undergoing both surgical and radiation therapy.
Novel stereotactic radiosurgery techniques have the advantage of delivery of high-intensity radiation with consistent precision and increased accuracy, permitting the delivery of higher doses while minimizing damage of adjacent radiosensitive structures. However, there are currently no randomized controlled studies that demonstrate a superior efficacy of this method to that of conventional radiation therapy. Nonetheless, current evidence indicates that radiosurgery is an efficacious management option. Wowra and colleagues conducted a prospective case series study (Class II evidence) with the objective of assessing the clinical results of 102 patients undergoing cyberknife fiducial free spinal radiosurgery. Outcomes measured included pain relief and complication rates. Treatment reduced median visual analog scale scores from 7 to 1 ( P <.001). An overall complication incidence of 2% was reported, which mainly included incidences of segmental neuropathy due to tumor hemorrhage, and vertebral instability. Gerszten and colleagues published a prospective case series (Class II evidence) of 500 patients who underwent radiosurgery for the treatment of spinal neoplasms. Parameters measured were functional outcome, pain relief, and tumor control. Eighty-five percent of patients with neurologic deficits before treatment exhibited improvement after treatment. An overall 86% of patients (which included both radiosensitive and radioresistant neoplasms) reported pain relief. Tumor control (measured both clinically and on imaging) was achieved on 86% of patients overall. Gibbs and colleagues prospectively analyzed outcomes (Class II evidence) in 74 patients with 102 spinal metastases treated with radiosurgery. The main parameters reported were functional improvement and complication rates. The study reported that an overall 84% of patients experienced a functional improvement, with only 2% of patients demonstrating deteriorating function. Complications occurred in only 3 patients (4%), all of which were myelopathies.
Acutely presenting symptoms of cervical epidural spinal cord compression by a neoplasm can be temporized by treatment with corticosteroids. The goal of corticosteroid administration is to decrease localized intramedullary edema. Optimal dosing is controversial, and there are few high-quality evidence-based studies comparing dosing regimens in the setting of metastatic spine disease. A Class I evidence study by Vecht and colleagues and a Class II evidence study by Heimdal and colleagues compared the relative efficacy of high-dose (96 mg intravenously) with low-dose (10 mg intravenously) dexamethasone in improving neurologic outcomes. The Class I study by Vecht and colleagues found increased efficacy, in terms of neurologic outcomes, for the low-dose dexamethasone (25% vs 8% rate of neurologic improvement). The Class II Study by Heimdal and colleagues found equal efficacy of neurologic outcome for both low-dose and high-dose cohorts, but found significantly higher rates of complications and side effects for the high-dose dexamethasone group. Hence, although there may not be a neurologic improvement benefit to giving low-dose versus high-dose steroids, evidence shows that low-dose steroids may have better outcomes based on their decreased incidence of complications.
Chemohormonal therapy may be used in the setting of sensitive tumors and is most often used as adjuvant therapy given that it cannot itself treat spinal instability. Breast, thyroid, and small cell lung carcinomas are generally sensitive to chemotherapy whereas gastrointestinal tract, squamous cell carcinoma of the lung, and renal cell carcinoma neoplasms are generally not. Tumor pathology obtained from biopsy can predict the susceptibility of a neoplasm to hormonal modulation. For example, determination of breast adenocarcinoma estrogen receptor status determines whether estrogen receptor modulation can be used as an adjuvant therapy. Furthermore, it is not uncommon for metastatic prostate lesions to present with hormone-insensitive tumors despite the original pathology demonstrating a hormone sensitive neoplasm. This event most often represents a phenomenon known as “hormonal escape” in which the primary hormone sensitive tumor was unsuccessfully managed via hormonal modulation, resulting in the selection of hormone-resistant clones.
Although not a primary method of treatment, bisphosphonate use in the setting of metastatic cervical spine disease is advocated, due to the ability of bisphosphonates to reduce the incidence of skeletal-related events (SREs). Specifically, Class I evidence exists demonstrating the efficacy of clonodrate, pamidronate, and zoledronate in decreasing the incidence of total SREs. However, evidence suggest that not all bisphosphonates have a similar efficacy n reducing the incidence of SREs specific to the spine, such as spinal cord compression. Rosen and colleagues conducted a randomized controlled trial (Class I evidence) directly comparing the efficacy of zoledronate to pamidronate. The study found that zoledronate was more efficacious in reducing the incidence of both pathologic vertebral fractures and cord compression.
Indications for Surgery in Metastatic Cervical Tumors
The general indications for surgical intervention are (1) neurologic dysfunction, (2) spinal instability, and (3) intractable pain. Indication for surgical intervention in the upper cervical spine is most often attributable to spinal instability. As discussed previously, neurologic dysfunction in the setting of an upper cervical tumor is more indicative of cord compression from spinal instability rather than direct tumor cord compression. An occipitocervical fixation alone is most often sufficient, given that the compression is not due to direct tumor impingement, thereby not requiring a decompressive laminectomy. Surgery is indicated more often in the lower cervical spine than in the upper cervical spine, due to metastatic lesions localizing more often to the subaxial spine, the relatively narrower subaxial canal resulting in an earlier onset of neurologic deficit versus the upper cervical spine, and a greater subaxial segmental mobility resulting in increased risk of spinal instability.
Although the staging scoring systems already discussed assist in indicating whether a palliative or curative surgery is most appropriate, palliative surgery is generally indicated in the setting of metastatic tumors. Curative surgery is mostly limited to primary spine tumors, but is possible in the rare cases of exceptionally isolated metastatic tumors. For example, the main indication for a curative wide surgical resection in the upper cervical spine is for treating predominantly isolated tumor to the posterior arch of C1 or C2. Nonetheless, even in such cases root and vertebral artery involvement must be considered, as it limits the aggressiveness of the surgical approach. In the case of root involvement, patients must be extensively informed about possible postoperative neurologic deficits in the upper limb if the root cannot be spared. The obstacle posed by the vertebral arteries can be managed by performing a unilateral or bilateral vascular bypass. Taking this approach underscores the necessity of obtaining a vertebral artery arteriography during the preoperative planning period.
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