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Annals of Surgical Oncology 10:291-296 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Chordoma: Natural History and Results in 28 Patients Treated at a Single Institution

D. Baratti, MD, A. Gronchi, MD, E. Pennacchioli, MD, L. Lozza, MD, M. Colecchia, MD, M. Fiore, MD and M. Santinami, MD

From the Departments of Surgery (DB, AG, EP, MF, MS), Radiation Oncology (LL), and Pathology (MC), National Cancer Institute of Milan, Italy.

Correspondence: Address correspondence and reprint requests to: Alessandro Gronchi, MD, Department of Surgery, National Cancer Institute of Milan, Via Venezian 1, 20133, Milano, Italy; Fax: 39-02-23902404; E-mail: alessandro.gronchi{at}istitutotumori.mi.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The natural history of chordoma is characterized by a high failure rate and a poor functional outcome. The purpose of this study was to review the long-term outcome of our institutional experience.

Methods: The clinical features, type of treatment, pathologic assessment, and follow-up of 56 consecutive patients with chordoma were reviewed.

Results: Fifty sacral and six mobile spine chordomas (median size, 13 cm; range, 2–30 cm) were treated at our center between January 1933 and December 2000. Twenty-eight patients affected by sacrococcygeal chordoma and operated on after 1977 form the basis of our study. Surgical margins were rated as wide in 11 cases, marginal in 13 cases, and intralesional in 4 cases. The median follow-up was 71 months (range, 15–200 months). Seventeen patients’ disease recurred. Ten patients died as a result of disease. Nine patients remained continuously free of disease. The estimated 5- and 10-year overall survival was, respectively, 87.8% and 48.9%; disease-free survival was 60.6% and 24.2%. Radiotherapy was considered for marginal and intralesional resections.

Conclusions: High sacral amputation can achieve a good rate of wide-margin resections for sacrococcygeal chordomas. Adjuvant radiotherapy may offset the negative effect in the prognosis of marginal resections.

Key Words: Chordoma • Sarcoma • Sacrococcygeal tumors • Prognosis • Surgery • Radiotherapy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Chordoma is a rare malignant neoplasm arising from remnants of the primitive notochord.1 The estimated yearly tumor incidence is .5 cases per million inhabitants, accounting for 1% to 4% of all skeletal tumors. It occurs exclusively in the axial skeleton; the most common site is the sacrococcygeal region (50%), followed by the skull base (35%) and the vertebral bodies (15%).2,3 Chordoma is considered a low-grade and slow-growing tumor, but a poor long-term prognosis is generally observed, despite its low tendency to metastasize.4–7 The delay in diagnosis because of unspecific clinical presentation and the proximity to neurological and other vital structures are the major challenges of therapeutic management. Because of poor responsiveness to chemotherapy and radiotherapy (RT), surgery is commonly considered the mainstay of treatment, and caudal localizations are reported as more favorable for surgical excision.8–10 However, safe margins and preservation of postoperative urinary and anorectal function are difficult to obtain.11–14

Because of the rarity of this disease, only a few cancer centers have developed extensive experience in its management, and the largest clinical reports have been based on series collected over a long period of time with highly variable treatment. The early results of our experience were previously published in 1965 and 1988.15,16 This study was mainly intended to evaluate the clinical long-term outcome of the entire series, with a special focus on sacrococcygeal chordomas operated on in recent years, according to current surgical techniques and oncological adequacy criteria.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A review was undertaken of all patients treated at the National Cancer Institute of Milan (Milan, Italy) from January 1933 to December 2000. Cases were identified through either the discharge diagnosis according to International Classification of Diseases revision 9 coding or the sarcoma prospective database set up in 1980.

Therapeutic indications, surgical techniques, and criteria of oncological adequacy have varied widely through the 67 years of the study. Since the beginning of the experience described herein, surgical resection was considered the treatment of choice for the eligible patients. However, a clear rationale in the management of sacral chordomas was not always evident, particularly when cases before 1970 were reviewed. During the 1970s, advances in preoperative staging, more reliable surgical techniques, and a stronger definition of oncological adequacy supported a more aggressive surgical approach and the development of a new rationale for treatment of sacral chordoma.17,18

Since 1977, 28 patients underwent radical surgery. Therefore, these patients form the basis of our study. As described in a previous article,19 the surgical technique adopted in our department for these more recent cases consisted of high amputation of the sacrum by a posterior approach. Two patients were operated on by a combined abdominal/posterior approach because of a massive involvement of S1. According to the current definition of oncological adequacy, the goal of the surgical procedure was to perform an uncontaminated removal of the tumor with a surrounding cuff of normal tissue. Care was taken to excise previous scars, as well as biopsy or drain tracts. Careful attention was paid to spare as many sacral nerve roots as possible. Wound closure was performed primarily; Prolene (Ethicon, Rome, Italy) mesh was used to close posterior defects and prevent visceral hernias.

Medical charts were used to obtain the age, sex, preadmission clinical history, type of operation performed at our center, type of RT or chemotherapy given, and functional outcome. The pathologic diagnoses of the patients operated on after 1977 were also reviewed, with particular emphasis on the quality of margins and size of the tumor.

We were therefore able to define size (largest diameter), site (most proximal vertebral level involvement), level of nerve resection, and quality of margins (intralesional, marginal, or wide), as well as neurological sequelae, local recurrence, metastasis, and survival. Surgery was considered adequate only if wide margins had been achieved.

Patients were regularly followed up after surgery with computed tomographic scan or magnetic resonance imaging of the pelvis and chest x-ray every 3 months for the first 2 years, then every 6 months for the following 3 years and every year for the remaining 5 years. Actuarial overall and disease-free survival rates were calculated by the Kaplan-Meier method.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The whole series included 56 patients treated between January 1933 and December 2000, 28 of whom were operated on after 1977 and form the basis of our study. The main clinical characteristics of the patients are listed in Table 1. The male:female ratio was almost 2:1, with a median age of 59 years. All patients treated after 1977 had disease at the sacral level, because of a selection of the referred patients to our institution.


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  		TABLE 1. Patient characteristics and treatment details for the entire series and for the recent series
 
All the patients presently alive belong to the group operated on after 1977, whereas all of the ones followed up before eventually died of their disease, with a median follow-up time of 39 months. The median follow-up of 28 patients with sacral chordoma who underwent surgery after 1977 was 71 months (range, 15–200 months). Five of these 28 patients were referred for recurrent chordoma after 1 (3 patients) or 2 (2 patients) local relapses. The remaining 23 patients were observed for primary disease; 3 underwent previous inadequate surgery, whereas 7 had an open biopsy and 13 a needle biopsy for pathologic diagnosis.

The highest level of tumor involvement was S1 in 2 patients, S2 in 13, S3 in 9, S4 in 3, and S5 in 1. The level of sacral resection was as follows: through the body of S1 in 2 patients, between S1 and S2 in 4, through S2 in 11, between S2 and S3 in 3, through S3 in 6, between S3 and S4 in 1, and through S4 in 1. All patients underwent sacral resection by posterior approach, except in two cases, in which sacral bone was resected through the body of S1 by means of a combined abdominal and posterior approach.

The median size of the tumors was 12 cm (range, 2.5–30 cm). Surgical margins were rated as wide in 11 cases, marginal in 13, and intralesional in 4. RT was postoperatively administered to 10 patients after marginal or intralesional operations; adjuvant RT was indicated but not performed in 6 patients for the following reasons: delayed wound healing (n = 2), previous pelvic irradiation (n = 3), and refusal (n = 1).

The RT was started 4 to 6 weeks after surgery. Fields were designed to encompass the area of the primary tumor with wide margins. The daily dose was 2 Gy for five fractions a week, for a total dose of 50 to 60 Gy delivered over 5 to 6 weeks. RT was generally well tolerated, and no major side effects were registered.

Postoperative functional outcome and its correlation with nerve root preservation are listed in Table 2. No patients with bilateral preservation of S3 experienced urinary or bowel symptoms. The bilateral preservation of S2, although followed in most cases by temporary urinary retention, fecal incontinence, or both, was then characterized by recovery of normal bowel and urinary function in most cases. The preservation of only one S2 root was followed in all cases by urinary and/or bowel symptoms, which were only occasionally recovered. All the patients with preservation of only S1 roots experienced definitive bowel and urinary dysfunction, and nobody recovered.


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  		TABLE 2. Neurological deficits and functional outcome after sacral amputation
 
The second most relevant surgical morbidities were wound-related complications, which affected 15 patients (53.5%). Additional surgical procedures were needed in seven cases, as were operative draining and debridement in three and skin grafting in three, and infected Prolene mesh had to be removed in one patient.

One patient died of cardiac arrest during surgery. One patient died of liver cirrhosis 98 months after the sacral resection but had experienced local recurrence. Ten patients died of disease. The remaining 16 patients are presently alive, 9 of whom are continuously free of disease (3 of them after >10 years of follow-up).

Overall survival at 5 and 10 years from operation was, respectively, 87.8% and 48.9%, with a median survival of 71 months; disease-free survival at the same intervals was 60.6% and 24.2% (Fig. 1). Seventeen patients’ disease recurred once or more; the first relapse was local recurrence in 15 cases, concurrent local and distant failure in 1, and distant metastases preceding local recurrence in 1. Local failure was generally quite delayed and occurred after a median interval of 35 months (range, 3–168 months) and after 5 years in six patients (35%). The median survival of this subset of patients with recurring disease was 27 months.



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  		FIG. 1. Overall survival (OS) and disease-free survival (DFS) for the 28 patients.

 
Surgical margins at the primary operation were rated as wide in six cases and marginal in eight; three of four patients who underwent intralesional sacral amputation experienced local recurrence, and the fourth patient was not assessable because he was the one who died during surgery. In detail, local failure developed once in 10 patients, twice in 5, three times in 1, and four times in 1; thus, the total number of local relapses was 27.

Recurrences frequently occurred in the soft tissue surrounding the sacrum, the rectum, and the perianal and gluteal areas (21 cases), whereas the sacral stump was less commonly involved (6 cases). We were able to treat local recurrence by complete surgery in 12 cases; postoperative RT was added in 4 of them. In the remaining 15 cases, the following palliative treatments were performed: inadequate surgery with or without RT (five cases), palliative RT (two cases), chemotherapy (two cases), and no therapy (six cases). First recurrences were treated by complete surgery in 9 of 17 cases, whereas second or further recurrences were so treated only in 3 of 10 cases; none of the 7 patients who developed >=2 consecutive local relapses could be rendered free of disease, and only 1 is presently alive.

As far as the primary treatment is concerned, all patients who underwent inadequate (marginal or intralesional) surgery without postoperative radiation inevitably had disease progression. However, the incidence of relapse among patients with inadequate margins at primary operation treated by postoperative RT (5 of 10) was similar to the incidence of relapse after wide excision with uncontaminated margins (6 of 11), as shown in Table 3. No statistical correlation could be attempted because of the small numbers of the groups.


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  		TABLE 3. Correlation of local relapse with several clinical variables
 
Distant failure involved the lung in three cases and the vertebral bodies in two; a recurrent subcutaneous dissemination at the entire trunk and girdles developed in one additional patient. Distant metastases preceded local failure in one patient, followed it in four patients, and were concurrent in one patient. The median metastasis-free interval was 92 months, and median survival after the development of metastasis was 11 months. All the patients with distant failure died.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Chordoma is the most common primary sacral neoplasm.12,20–24 Early diagnosis of sacral chordoma is virtually impossible, because its onset is usually asymptomatic. Radicular pain at the sacral level or irradiated to the lower limbs, with possible areas of sensitivity disorders in the perineum, is related to nerve root compression and generally occurs in case of extensive local tumor spread with involvement of sacral foramina.12,13 As reported in our previous survey, as well as in the major articles, milder symptoms could have been present for a median period of 12 to 24 months before the diagnosis was established. Tumors then are generally very large at the time of detection.6,9,16,23

The large size of chordoma at presentation and the complexity of sacral anatomy preclude the effectiveness of treatment and account for the high rate of local recurrence. Our results reflect the experience of the literature, both in terms of survival and disease-free survival.6–8,11,13,16,22,25–27

Surgery is the mainstay of treatment. The goal is to achieve wide margins both at the bone and the soft tissue levels. Because of the improved surgical procedures of the past years, an en-bloc resection of the sacrum has not generally presented any problem, and the marginality at that level has been occasional in our series.

More relevant, it has been the contiguity with the visceral organs of the lower pelvis, together with the absence of proper anatomical structures, that has been able to contain the local spread of the tumor in the soft tissue (perirectal fat, ischiorectal spaces, perianal areas, and gluteal muscles). Only the presacral lamina presents a natural barrier to that contamination, but it is a weak fascia and most of the time at diagnosis is already infiltrated. This is why most of our recurrences have been not at the sacral stump, but in the soft tissues. Most of these recurrences, although amenable to further complete surgery, have eventually led to death.

All the patients operated on with marginal or intralesional margins inevitably had disease progression. The risk of an inadequate procedure was mainly related to the extension of the disease in the soft tissue and was increased in previously treated patients, as reported by several authors.9,23,26,27 However, only half of the patients operated on with wide margins experienced a local recurrence. This result underlines once more the importance of adequate margin resections in the control of skeletal tumors.

Different surgical approaches have been described to achieve an adequate resection, and many authors recommended a combined abdominal and posterior approach.18,24 Most of them agree that the choice of surgical approach depends on which sacral segment is involved. Combined exposure is advocated for lesions at the level of the second or more proximal segments, whereas the posterior approach is advised for distal chordomas.6,9,19,21 Recently, Conlon and Boland27 described a combined procedure in which hypogastric artery ligation and rectal mobilization was performed laparoscopically, with encouraging results. In accordance with the experience of the Massachusetts General Hospital,6 we found that the posterior approach is feasible, satisfactory, and safe. However, we believe that sacral resections through the body of S1 need a combined approach to allow a complete tumor excision because of the proximity of vascular and other vital structures.

The value of RT as primary or adjuvant treatment has been debated.6,11,13,16,26–33 Whereas some investigators have reported little effect with RT, others have described improved local control and prolonged disease-free survival after RT as adjuvant treatment. Our study seems to suggest a role for RT in controlling local disease. Indeed, half of the patients operated on with inadequate margins and then treated with RT had no recurrence, whereas all the patients with inadequate margins and no RT did have recurrence. Furthermore, the median time to progression of these patients was much shorter in the group that did not receive RT, whether they were operated on with wide or marginal margins (15 months for inadequate resections and 22 months for adequate ones vs. 75 months for inadequate resection plus RT). Again, these data seem to suggest that RT may favorably affect prognosis, at least prolonging the time to progression, and might be also considered for wide resections.

Nevertheless, we can only suggest the possible benefit of adjuvant radiation because of the small number of patients treated, but at least we have recognize a trend, in accordance with several other authors.6,11,13,16,26,31–33 Only a randomized study could definitively answer this question, but it is very unlikely to be performed because of the rarity of this disease. Therefore, taking these suggestions into account, we consider RT for all patients in whom a wide margin could not be achieved.

Occurrence of distant metastases ranges in the literature from 5% to 40% and is generally more delayed and rare than occurrence of local relapse.6,7,9,25 Sundaresan et al.5 and Sundaresan21 reported detection of metastases from 1 to 10 years after surgery. In our experience, two patients developed distant failure 3 and 7 months after operation, whereas metastasis-free survival was longer than 55 months for the remaining five cases. All the patients who developed distant failure experienced local relapse. Therefore, our data seem to support the observations of Yonemoto et al.,7 who observed that distant metastases mostly occurred in patients with advanced stages, lacking local control of the disease.

Neurological deficit after partial sacrum amputation can be predicted. As reported by Stener and Gunterberg18 and Gunerberg et al.,34 impairment of ambulatory ability, sphincteral function, and sexual capacity is related to the number of preserved nerve roots. The loss of bilateral S1 markedly diminishes the ability to ambulate; urinary and fecal continence are impaired when at least one S2 root is transected, whereas most patients retain normal sphincter control if a monolateral S3 is spared. In this series, patients were forced to use diapers, to empty the bowel regularly, and to perform intermittent catheterization when at least one S2 was the most proximal nerve spared; urinary diversions were needed in two cases and permanent colostomy in one. Patients who had preservation of bilateral S2 retained almost normal sphincter control for 6 to 8 months, except one patient, for whom colostomy and permanent urinary diversion were necessary.

In conclusion, our experience suggests that wide excision in the form of high sacral amputation gives the best chance of cure for sacrococcygeal chordomas and that RT may play a relevant role as a part of a multidisciplinary treatment plan. Local failure is the major factor affecting postoperative outcome, but aggressive management of recurrence is mandatory to allow long-term survival even to patients with local relapse.


   Acknowledgments
 
The acknowledgments are available online at www.annalssurgicaloncology.org.


   Footnotes
 
The treatment and outcome of a consistent series of sacrococcygeal chordoma were reviewed. Wide-margin resection as the primary treatment has proven to achieve local control at least in half of the patients. The role of adjuvant radiotherapy should be investigated.

Received for publication June 4, 2002. Accepted for publication October 17, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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