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First published online October 1, 2007
British Journal of Radiology (2007) 80, 790-797
© 2007 British Institute of Radiology
doi: 10.1259/bjr/20938070
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Imaging findings of radiation-induced sarcoma of the head and neck

Y Makimoto, MD 1 S Yamamoto, MD 1 H Takano, MD 2 K Motoori, MD 1 T Ueda, MD 3 T Kazama, MD 1 K Kaneoya, MD 1 R Shimofusa, MD 1 T Uno, MD 1 H Ito, MD 1 T Hanazawa, MD 4 Y Okamoto, MD 4 and K Hayasaki, MD 5

1 Department of Radiology, Chiba University Hospital, 1-8-1 Inohana, Chuou-ku, Chiba City, Chiba, Japan 260-8670, 2 Department of Radiology, Chiba Cancer Center, 666-2 Nitona-chou, Chuou-ku, Chiba City, Chiba, Japan 260-8717, 3 Department of Radiology, Institute of Clinical Medicine, University of Tsukuba, 2-1-1 Amakubo, Tsukuba City, Ibaraki, Japan 305-8576, 4 Department of Otolaryngology, Chiba University Hospital, 1-8-1 Inohana, Chuou-Ku, Chiba, Japan, 5 Department of Head and Neck Surgery, Chiba Cancer Center, Chiba, Japan

Correspondence: Seiji Yamamoto, Department of Radiology, Chiba University Hospital, 1-8-1 Inohana, Chuou-ku, Chiba City, Chiba, Japan 260-8670. E-mail: seikichi{at}faculty.chiba-u.jp


   Abstract
Top
 Abstract
Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
 References
 
We set out to retrospectively review the clinical and imaging features of patients with post-radiation sarcoma, especially in the head and neck region. We reviewed the records of 4194 patients with carcinoma of the head and neck region who had a history of radiation. They had undergone CT and/or MRI. Medical records were reviewed for the primary diagnosis, radiation history and latency period to the development of sarcoma. The patients included four men and two women with a mean age of 64.5 years. The mean latency period for the development of sarcoma was 11.5 years. Primary diagnoses were maxillary carcinoma, nasopharyngeal carcinoma, adenoid cystic carcinoma of the oral floor, tonsilar carcinoma, soft palate carcinoma and tongue carcinoma. Histopathological examinations revealed osteosarcoma, spindle cell sarcoma, chondrosarcoma, malignant peripheral nerve sheath tumour, spindle cell carcinoma and malignant fibrous histiocytoma, respectively. Common findings were a heterogeneous and well-enhanced soft tissue mass and bone destruction. There is at present little or no prospect for the effective prevention of radiation-induced sarcoma of the head and neck. This emphasizes the importance of the earliest possible diagnosis for such patients. The imaging findings are not diagnosis specific, but strict follow-up within the radiation field by CT and MRI and an appreciation of the expected latency period may help to provide the diagnosis. When radiotherapy is performed for head and neck neoplasms, periodic follow-up observations may be necessary for many years.


   Introduction
Top
 Abstract
 Introduction
Methods and materials
 Results
 Discussion
 Conclusions
 References
 
The earliest description of post-radiation sarcoma of which we are aware was reported in 1922 by Beck [1] and, to the best of our knowledge, the earliest description of sarcoma developing after radiation therapy for cancer was reported in 1936 by Warren and Sommer [2]. Cahan et al [3] defined the criteria for post-radiation bone sarcoma: (a) histological or radiological proof that there was no previous tumour in the involved bone; (b) development of sarcoma in an irradiated area; (c) a sufficiently long interval between irradiation and the development of sarcoma; and (d) histological proof of sarcoma. These authors suggested a latent period of 5 years, although 3–4 years was thought to be sufficient by Arlen et al [4].

The utility of radiation therapy to the head and neck region has been established. The incidence of radiation-induced sarcoma of the head and neck (RISHN) is, however, likely to increase because of the progressive ageing of the population combined with the improved survival rates of head and neck cancer patients resulting from better treatment regimens. The purpose of our study was to review the imaging findings of RISHN and to determine if any of the findings were diagnosis specific.


   Methods and materials
Top
 Abstract
 Introduction
 Methods and materials
Results
 Discussion
 Conclusions
 References
 
Patients
A retrospective study of post-radiation sarcoma treated at Chiba University Hospital and Chiba Cancer Center was undertaken at the two institutions. The database contained 4194 patients who underwent radiotherapy treatment for head and neck tumours. These patients are followed up at 6 months and then yearly. Follow-up imaging is only performed if there is clinical suspicion of possible recurrence or RISHN. The purpose of this study was to document the incidence, natural history and prognosis of RISHN as well as the imaging features. Among all of the patients who were followed up we found six cases that met the RISHN criteria. CT and MRI images of their initial cancers were not available. Inclusion criteria were confirmed for the primary diagnosis and post-radiation diagnosis of sarcoma. Investigated parameters included age at diagnosis of primary tumour, dose of radiation delivered, age at diagnosis of sarcoma, histological type of sarcoma, anatomical location, interval between irradiation and development of sarcoma, treatment of sarcoma, survival after diagnosis of sarcoma and cause of death.

Procedures
The six cases of RISHN all underwent CT and MRI examinations. All CT scans were performed with a single helical 4 or a 16 multidetector-row CT scanner (Light-speed QXi or HiSpeed Advantage; GE Medical Systems, Milwaukee, WI, and ProSpeed Plus system; GE Medical Systems, Milwaukee, WI) after an intravenous bolus administration of 100 ml of non-ionic contrast material (iohexol, Omnipaque 300; Daiichi Pharmaceutical Corporation, Tokyo, Japan) at a rate of 2 ml s–1. Helical scanning of the head and neck was performed using 5 mm collimation and a pitch of 1.5 or a section thickness of 1.25 mm following a 50 s delay after injection.

All MRI examinations were performed using 1.5-T MR units (GE Medical Systems, Milwaukee, WI) with a neurovascular array coil. T1 weighted (T1W) images (300–500/9–20 (repetition time in ms/echo time in ms)) of the axial plane, short tau inversion recovery (STIR) images (4000/30, 12 (echo train length), 150 (inversion time in ms)) of the same axial plane as in T1W images and T2 weighted (T2W) spin-echo (SE) images (4000/104, 16 (echo train length)) of the same axial or coronal plane were obtained at a section thickness of 5–6 mm, an intersection gap of 1–1.5 mm, an acquisition matrix of 256 x 256 and a field of view of 22 x 22 cm. Contrast-enhanced MR images were obtained with fat suppression T1W images (300–500/9–20 (repetition time in ms/echo time in ms)) with gadodiamide hydrate (Omniscan; Daiichi Pharmaceutical Corporation, Tokyo, Japan) being administered (0.2 ml kg–1 body weight).


   Results
Top
 Abstract
 Introduction
 Methods and materials
 Results
Discussion
 Conclusions
 References
 
Among the 4194 patients, six (four men and two women; frequency 0.143%) were confirmed to have RISHN. The analytical findings are presented in Table 1Go. The mean age at the time of diagnosis of the primary tumour was 56.3 years (range 38–68). The primary tumours were maxillary carcinoma, tonsilar carcinoma, nasopharyngeal carcinoma, adenoid cystic carcinoma, soft palate carcinoma and tongue carcinoma. The patients underwent external-beam radiation therapy and one patient also underwent interstitial irradiation with Au grains. The beam type used was high energy X-rays in five patients and cobalt in one patient. The total mean dosage of external irradiation was 66 Gy (range 60–72 Gy) and interstitial irradiation was 62 Gy.


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  		Table 1.
 
At the time of diagnosis of RISHN the mean age of the patients was 64.5 years (range 51–80 years) and the mean interval between irradiation and diagnosis was 11.5 years (range 6–17 years). All tumours arose within the field of radiation.

The histological diagnosis of sarcoma types is shown in Table 1Go. Four of the six patients underwent complete tumour resection and three of them were still alive at the time of this investigation. The fourth treated patient had recurrent tumour regrowth and died 11 months post-surgery. The patients without treatment died 11 months and 13 months post-diagnosis, respectively.

Imaging findings
Case 1: 80-year-old woman
The primary tumour, left maxillary carcinoma, received radiation therapy of 60 Gy. The recurrent neoplasm was a chondrosarcoma, diagnosed 12 years post-radiation. Total maxillary sinus resection and reconstruction with a dermal flap were performed. The maxillary bone where radiation therapy had been performed did not reveal destruction, although bone thickening was observed, likely as a result of the radiation. Soft tissue growth with bone destruction was evident at the root of the nose (Figure 1aGo). On T1W images the tumour showed a low signal intensity area; there was marginal enhancement on post-contrast T1W images (Figure 1b,cGo). The patient refused treatment and died from the tumour. This tumour had recurred in the radiation field, where apparently characteristic evidence was osseous change.


Figure 1
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  		Figure 1. Case 1: 80-year-old woman. (a) Axial CT image showing bone thickening that resulted from radiation therapy (arrow). There was soft tissue growth around the root of the nose bilaterally, and bone destruction was observed (arrowhead). (b) Axial T1 weighted spin-echo MR image (400/9) showing a low signal intensity tumour. (c) Contrast-enhanced axial T1 weighted spin-echo MR image (400/20) showing marginal enhancement of the tumour. The tumour showed right orbital invasion.

 
Case 2: 66-year-old man
The primary tumour, tonsilar carcinoma, was exposed to radiation therapy of 70 Gy. The recurrent neoplasm was a malignant peripheral nerve sheath tumour. The interval between irradiation and diagnosis was 17 years. Left tonsil tumorectomy was performed. Thickening was seen in the maxillary bone where radiation therapy had been performed, in comparison with the contralateral side. The lateral maxillary wall was destructed and an expansive mass occupied the left maxillary sinus (Figure 2a,bGo). Differentiation from a post-operative maxillary cyst can sometimes be a problem but this tumour showed asymmetrical contrast enhancement at the border region occupying the maxillary sinus on post-contrast T1W images (Figure 2c,dGo). Total resection of the left maxillary sinus was performed. The tumour was milk-white with a smooth surface and lobulation, showing polypoid growth into the intranasal cavity. S100 protein was positive and manifestation of desmin was found in the tumour.


Figure 2
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  		Figure 2. Case 2: 66-year-old man. (a) Axial CT image showing the damaged lateral wall of the maxilla and an expansive mass occupying the left maxillary sinus. (b) Coronal CT image showing maxillary bone and temporal bone thickening where they had been exposed to radiation therapy (arrow). (c) Contrast-enhanced axial T1 weighted spin-echo MR image (300/20) showing heterogeneously enhanced tumour occupying the maxillary sinus. (d) Contrast-enhanced coronal T1 weighted spin-echo MR image (300/20) showing heterogeneously enhanced tumour with a damaged lateral wall of the maxilla and invasion of the right nasal cavity.

 
Case 3: 62-year-old man
The primary tumour, nasopharyngeal carcinoma, received radiation therapy of 64 Gy. The recurrent neoplasm, a spindle cell sarcoma, was found 12 years post-radiation, occupying the right mastoid air cell. All bones such as the clivus were thickened asymmetrically by radiation therapy but there was distinct bone destruction in the area of the recurrent tumour (Figure 3aGo). The tumour showed marked enhancement on post-contrast T1W images (Figure 3bGo). In this case, by using contrast media for MR imaging, the extent of the tumour was able to be confirmed more distinctly for the first time.


Figure 3
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  		Figure 3. Case 3: 62-year-old man. (a) Axial CT image showing the right mastoid air cell occupied by the recurrent tumour, which was difficult to detect on CT. Only the part of the tumour invading the posterior fossa can be seen (arrow). Bone destruction in the area of the recurrent tumour is shown in the bone window. (b) Contrast-enhanced axial T1 weighted spin-echo MR image showing significant enhancement of tumour. The tumour was widely attached to the dura, showing dural enhancement.

 
The patient was not treated and died of local disease 13 months later.

Case 4: 69-year-old woman
The primary tumour, adenoid cystic carcinoma of the oral floor, was treated with radiation therapy of 60 Gy. The second tumour, discovered 9 years later, was osteosarcoma of the jaw. The jaw showed bone sclerosis and the tumour could be detected with spicula and a round soft tissue mass of the left-side mandible (Figure 4a,bGo). Total resection of the mandibular bone was performed but the patient died of local disease 11 months later. There was mandibular bone destruction and the tumour had a substantially white portion and an expansive cystic component. This osteosarcoma had an osteoblastic-type appearance.


Figure 4
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  		Figure 4. Case 4: 69-year-old woman. (a,b) Axial CT images and contrast-enhanced axial T1 weighted spin-echo MR image (400/20) showing the sclerosed mandible, a result of radiation therapy. The tumour could be detected with spicula. It showed heterogeneous contrast uptake and formed a soft tissue mass around the mandible extending to the right side.

 
Case 5: 59-year-old man
The primary tumour, soft palate carcinoma, was treated with external irradiation therapy of 72 Gy and with interstitial irradiation with Au grains of 62 Gy. The recurrent neoplasm was a spindle cell carcinoma of the left mandible, diagnosed 6 years post-radiation. The lower left mandible branch was destroyed and the tumour was identified mainly in the masticator space (Figure 5a,bGo). The tumour showed heterogeneous contrast enhancement and the posterior wall of the left mandible was also destroyed. Partial maxillectomy, suprahyoidal neck dissection, total parotidectomy and dissection of the temporal and infratemporal fossa were performed. The patient is alive but has recurrence at 5 years post-surgery.


Figure 5
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  		Figure 5. Case 5: 59-year-old man. (a) Enhanced CT image showing a damaged left mandible branch and a soft tissue mass mainly in the masticator space. The tumour showed heterogeneous contrast uptake and the posterior wall of the left mandible was also destroyed. (b) Contrast-enhanced axial T1 weighted spin-echo MR image (500/11) showing heterogeneously enhanced tumour in the left masticator space.

 
Case 6: 51-year-old man
The primary tumour, tongue carcinoma, was treated with radiation therapy of 40 Gy with an additional local dose of 30 Gy. The recurrent neoplasm was a malignant fibrous histiocytoma of the mandible (Figure 6Go). The interval between irradiation and diagnosis was 13 years. Mandibulectomy combined with excision of facial skin and reconstruction using a scapular bone flap was performed. The patient is alive and free of disease at 7 years post-surgery.


Figure 6
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  		Figure 6. Case 6: 51-year-old man. Contrast-enhanced CT image showing the recurrent neoplasm destroying the anterior wall of the right mandible and forming a soft tissue mass (arrow).

 

   Discussion
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
Conclusions
 References
 
Several authors have attempted to determine the incidence of radiation-induced sarcoma. For example, Phillips and Sheline [5] estimated a 0.23% frequency of sarcoma after irradiation for breast cancer, and others reported similar results [6–9]. In the case of gynaecological tumours, Mark et al [10] estimated the absolute risk of post-radiation sarcoma to be 0.03–0.8%. The frequency of RISHN in our study was 0.143%, which was lower than the frequency of sarcoma after irradiation for breast carcinoma and gynaecological tumours.

Despite the considerable increases in the survival rate for head and neck cancers with the improvement in therapeutic methods, it is still inferior to that of breast cancer; the 5 year survival rate for head and neck cancers is around 60%, whereas those for breast cancer and gynaecological cancer are more than 80% [11–17]. In this regard, it was considered that part of the reason for the low incidence of RISHN in the head and neck is the higher mortality rate of head and neck cancers. As for osteosarcomas, Huvos et al [18, 19] and Souba et al [20] estimated that approximately 5% of sarcomas developed after therapeutic or accidental irradiation. Lagrange et al [21] reviewed 80 patients with a confirmed histological diagnosis of sarcoma occurring after radiation therapy. In this study, high-grade malignant fibrous histiocytoma was the most frequent type of secondary sarcoma, followed by high-grade osteosarcoma. In our cases, both types of secondary sarcoma were seen. In the head and neck region, Patel et al [22] also reported that malignant fibrous histiocytoma was the most common pathological diagnosis.

Prognosis in patients with post-radiation sarcoma is generally poor. Lagrange et al [21] reported an overall survival rate of 48% at 2 years and 29% at 5 years, with a median survival of 23 months [95% confidence interval (CI):16, 29 months]. In this series, 86% of the patients died of secondary tumour, whereas only 8% died of primary tumour. Robinson et al [23] reported a median survival of 12 months, with survival rates of 22% at 2 years and 11% at 5 years. This poor prognosis was confirmed by results from other series [24–27]. Most studies quote a poor outcome for RISHN [22], with Mark et al [28] reporting a 5 year disease-free survival of only 8%. Because RISHN are rare tumours, no series with significant patient numbers have been reported, and statistical comparisons with other patients with non-radiation-induced sarcomas of the head and neck have not been possible. Patel et al [22] reported that the 5 year survival rate in a RISHN group was considerably worse than the overall actuarial 5 year disease-free survival for sarcomas of the head and neck. They explained the poor prognosis of RISHN on the basis of a combination of factors: (a) a delay in diagnosis caused by the unreliability of clinical examinations because of local post-radiation changes; (b) the proximity of the tumour to major neurovascular structures, possibly placing constraints on the limits of surgical resection; (c) limited treatment options because of the dangers of irradiating a previously irradiated field as well as the relatively poor sensitivity of these tumours to chemotherapy; (d) host immunosuppression caused by the first tumour and/or its treatment.

The clinical diagnosis of RISHN can be difficult because of induration and fibrosis within the field of radiation. Prompt investigation based on the patient's symptoms, especially the appearance of, or a change in the character of, pain in the irradiated area, can lead to an early diagnosis and a correspondingly better chance of complete surgical excision. When the previous history of irradiation is taken into account, surgical excision of RISHN remains the only definitive treatment option. By the time that most RISHN are diagnosed they have extended beyond the local confines of their origin and are consequently often difficult to resect completely without causing unacceptable functional and cosmetic deformities. Surgical management of RISHN is also challenging because of the technical difficulties in determining adequate surgical margins and the poor healing and wound complications associated with radiation changes. Lagrange et al [21] reported that survival was better in patients treated with surgery or with surgery plus chemotherapy, but there was no difference in survival between complete and partial excision.

It is difficult to analyse the relationship between the total irradiation dose received and the incidence of RISHN. Kirova et al [9] showed that most reported cases of RIS after breast irradiation occurred after receiving doses of 60–80 Gy with a minimal dose of 10 Gy in standard fractions. Karlsson et al [29] found that the risk for sarcomas other than angiosarcomas increased linearly with an integral dose of 150–200 J, stabilizing at higher energies. However, there are no studies available that provide data on the relationship between prescribed radiation dose and radiation-induced sarcoma.

Early detection provides a chance for cure, provided that wide-margin resection is performed. To achieve this result, the suspicion of post-radiation sarcoma must be reached early, when alterations or symptoms occur in a previously irradiated region [30]. In our study, the tumour arose within the radiation field, and irradiated bone appeared thicker than normal bone. If the area that has received radiotherapy treatment is not clear, thickening of bone will serve as an indicator. In this study, the imaging findings were not diagnosis specific or characteristic. If RISHN could be judged boldly, all tumours were heterogeneous and well enhanced. To improve the chance for early detection, CT and MRI should certainly be carried out. This means that early diagnosis will depend on strict and long-term follow up, including CT and MRI when warranted, within the radiation field.


   Conclusions
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
References
 
There is at present little or no prospect for effective prevention of RISHN. This highlights the importance of an early diagnosis for these patients, for whom the best hope for a complete recovery is surgery. Follow-up imaging findings did not reveal distinctive or characteristic features that would directly result in a diagnosis, but all tumours were heterogeneous and well-enhanced. Because RISHN is rare and the latent period long, routine surveillance imaging is not appropriate. However, early cross-sectional imaging should be employed if any clinical features suggestive of RISHN develop.

Received for publication February 15, 2006. Revision received December 14, 2006. Accepted for publication January 7, 2007.


   References
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
 References
 

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