The etiology of recurrent chordoma presenting as a neck mass: metastasis vs. surgical pathway seeding.

Abstract

Chordomas are rare tumors of notochordal origin that arise along the vertebral axis. These slowly growing yet highly destructive tumors are associated with an alarming rate of recurrence, although surgical resection followed by proton, proton/photon, or conventional radiotherapy has been somewhat successful in terms of recurrence-free survival. Still, recurrent disease as a result of metastasis or surgical pathway seeding does occur. We retrospectively reviewed the case of a 64-year-old woman who presented with a left neck mass at level II. She had a history of recurrent chordomas involving the occipital portion of the clivus that had been treated with multiple resections and proton-beam irradiations over a period of several years. The new mass was found to have infiltrated the superior end of the sternocleidomastoid muscle. Neck dissection was performed. Pathology revealed no lymphoid tissue in the main specimen and no evidence of chordoma in any of the lymph nodes. We believe that this latest clival chordoma might have occurred as a result of surgical pathway seeding during a previous operation anterior to the sternocleidomastoid muscle, although metastasis cannot be ruled out. We also review the literature on clival and skull base chordomas as it relates to recurrence, metastasis, and seeding.

Introduction

Chordomas are rare tumors of notochordal origin that arise along the vertebral axis. In terms of location, the most common types are spinal (32.8% of cases), cranial (32%), and sacral (29.2%). (1) Chordomas are typically slowly growing tumors, yet they can be extremely destructive because of their local invasiveness and a high rate of recurrence. These tumors have a predilection for males (2:1), their incidence peaks in the fourth decade of life, and they tend to affect a higher proportion of whites than blacks. (1,2)

Cranial chordomas usually occur in the area of the clivus. The most common presenting complaint is diplopia, which is caused by cranial nerve compression. Tumor recurrence is common; local recurrence rates as high as 95% have been reported. (3) Following resection, recurrence at a secondary site may occur as a result of metastasis or tumor seeding along the surgical pathway. The latter type of recurrence has been defined as a secondary tumor growth outside the primary site that arises along the surgical route or where other tissue was harvested intraoperatively. (4,5)

The reported incidence of distant metastasis for all types of chordoma ranges from 10 to 43%, but most of these occur in cases of sacrococcygeal or vertebral chordoma. (6-8) Clival chordomas rarely metastasize; local destruction is a hallmark feature. (6) On the other hand, the potential for cranial chordomas to metastasize is being increasingly recognized, with some authors reporting rates of 7 to 14%. (9,10) The most common sites of metastasis from skull base chordomas are the lungs, lymph nodes, and bone. (6,11,12) Likewise, surgical pathway seeding of skull base chordomas is being increasingly recognized as a mode of recurrence, with reported rates ranging from 5 to 7.3% of resections. (3-5,13-15)

We present the case of a patient with a neck mass that developed after treatment for recurrent clival chordomas. Since she had a surgical history of chordoma excision in that area, it is possible that her tumor was caused by surgical pathway seeding, although metastasis cannot be ruled out.

Case report

In December 2001, a 60-year-old white woman presented with a history of progressive headaches. Magnetic resonance imaging (MRI) revealed the presence of a 5 x 4-cm mass in the occipital portion of the clivus (figure 1). The tumor extended laterally to the left and involved the occipital condyle and the hypoglossal canal on that side. Further extension was noted on the left into the bone of the C1 vertebra, the prevertebral soft tissues of the nasopharynx and oropharynx, and the deep soft tissues of the neck. The left internal carotid artery was displaced but not encased.

In January 2002, the patient underwent resection via a transoral palate- splitting approach. Resection continued laterally to the left occipital condyle and posterior to C1. A microsurgical technique was used to completely excise the tumor. At the completion of the procedure, abdominal fat was harvested with a different set of instruments and inserted into the surgical bed along with fibrin glue. Pathology revealed that all surgical sections were positive for chordoma.

In April 2002, a follow-up MRI detected a 1-cm mass at the clivus and prevertebral space at the site of the previous resection. Again, the tumor had invaded the occipital condyle and the hypoglossal canal on the left. This recurrence resulted in instability of the cervical spine. The patient underwent an occipitocervical fusion in preparation for excision of the recurrent tumor via a left transcondylar approach. The tumor was accessed through a C-shaped incision in the left retroauricular area. The tumor was identified in the occipital condyle, and extension was noted to the clivus, retropharyngeal space, and up to the odontoid process of C1. All visible tumor was resected, including the intradural extension. Pathology of the mass revealed numerous atypical cells indicative of chordoma; the Ki-67 labeling index was 10 to 12%. Postoperative MRI showed that the lesion had been completely removed. Thereafter, the patient underwent several proton-beam radiation treatments at another institution.

In November 2002, MRI showed no evidence of tumor recurrence. However, metrizamide computed tomography detected a mild cerebrospinal fluid leak into the left nasal cavity. The leak was repaired in January 2003 via a left radical mastoidectomy and obliteration.

[FIGURE 1 OMITTED]

The patient remained recurrence-free until January 2005, when an MRI detected a ring-enhancing mass just anterior to the left occipital condyle between the left vertebral artery and the left internal carotid artery. In March 2005, she underwent surgery via a left postauricular transcondylar approach to the skull base along a plane anterior to the left sternocleidomastoid muscle. Prior to excision, Tisseel fibrin-glue-coated patties were placed along the surgical pathway to prevent tumor seeding. After intraoperative pathology indicated the presence of a malignant tumor at the operative margins, the area of the tumor was extensively curetted.

Follow-up MRI in June 2005 revealed postsurgical changes at the resection site, as well as a ring-enhancing area in the left retropharyngeal space. No change in this lesion was noted on repeat imaging in July, September, and December 2005.

In January 2006, the patient, who was now 64 years old, returned to our clinic with a complaint of swelling over her left parotid area. She said that she had first noticed the swelling more than 1 year earlier and that it had been slowly increasing in size. On examination, a fixed, nontender, 2 x 2-cm mass was noted at level II inferior to the parotid tail. Upon review of her most recent MRI, which had been obtained the previous month, a 2.3 x 2-cm necrotic area mass was noted inferior to the tail of the parotid; it appeared to be separate from the gland (figure 2). The results of fine-needle aspiration cytology were consistent with a chordoma; the histopathology was similar to that of her previous clival tumor.

[FIGURE 2 OMITTED]

The patient underwent selective left neck dissection later that month. An incision was made from the mastoid tip across the midline. The mass had entirely infiltrated the sternocleidomastoid muscle, and the muscle was excised along with the mass. No other masses were noted, and the tumor was sent for analysis. Histopathology identified a chordoma within the surrounding soft tissue (figure 3). Lymphoid tissue was noted near the tumor margin, but it appeared to be related to local inflammation and was not indicative of a nodallocation. Immunohistochemistry was positive for cytokeratin and S-100 protein. All 15 lymph nodes that were removed were negative for metastatic chordoma. However, the patient's clival tumor again recurred. She was not deemed operable, and she was given palliative chemotherapy until she died in the autumn of 2007.

[FIGURE 3 OMITTED]

Discussion

There are two possibilities that would explain our patient's most recent tumor--regional metastasis and surgical pathway seeding:

* Metastasis. Skull base chordomas are rarely known to metastasize; to the best of our knowledge, only 9 cases of soft-tissue metastasis from a skull base chordoma have been reported. (16-24) Since our patient's tumor was not located within a lymph node histologically, the possibility of a distant metastasis would not be absolute.

* Seeding. Since our patient had undergone previous chordoma excisions through the auricular region and around the superior sternocleidomastoid muscle, her tumor might have occurred as a result of surgical pathway seeding during one of her previous operations. However, during the resection of her neck mass in January 2006, our surgical approach was inferior to that of her previous incision, and we encountered no scar tissue in the plane of the approach or near the tumor.

Further review of the pathology did not enable us to determine whether the most recent chordoma was the result of a metastasis or seeding.

Recommendations for the aggressive management of skull base chordomas call for maximal surgical excision followed by proton and/or photon radiotherapy or, if they are not available, conventional radiotherapy. (9,25) Some authors have suspected that there is a correlation between pathway seeding and focal radiotherapy. In a study of 204 patients with skull base chordoma who were treated with proton/photon radiotherapy, Fagundes et al reported surgical pathway recurrences in 1.5% of all patients and in 5% of those with a detectable relapse. (3) Similarly, Arnautovic and Al-Mefty studied 6 cases of surgical seeding and found that 5 of these patients had undergone postoperative radiotherapy, including 1 who had undergone surgical implantation of the thigh in the area where fat grafts had been taken intraoperatively. (4)

Fischbein et al suggested that seeding becomes possible as an unintended consequence of the increased precision of more conformal proton-beam radiotherapy. (5) Because the delivery of radiation to the area of tumor is so localized, the surrounding areas, including the surgical pathway, are not likely to receive any radiation. Arnautovic and Al-Mefty have even suggested that surgical pathway tumors may be of positive prognostic value in that they may indicate tumor recurrence sooner and therefore allow for earlier, more aggressive management. (4) We do not believe that previous radiotherapy was a factor in our patient's case. Although she had undergone proton radiotherapy previously, this occurred prior to the resections through the left auricular/neck region.

In summary, we believe that the recurrence of the clival chordoma in our patient might have occurred as a result of seeding during a previous surgical approach anterior to the sternocleidomastoid muscle, although metastasis is still a possibility.

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Jennings R. Boyette, MD; John W. Seibert, MD; Chun-Yang Fan, MD, PhD; Brendan C. Stack Jr., MD, FACS, FACE

From the Department of Otolaryngology-Head and Neck Surgery (Dr. Boyette, Dr. Seibert, and Dr. Stack) and the Department of Pathology (Dr. Fan), University of Arkansas for Medical Sciences, Little Rock.

Corresponding author: Brendan C. Stack Jr., MD, Department of Otolaryngology-Head and Neck Surgery, University of Arkansas for Medical Sciences, 4301 W. Markham St., Slot 543, Little Rock, AR 72205-7199. Phone: [phone]; fax: [phone]; e-mail: [e-mail]