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Japanese Journal of Clinical Oncology Pages 164-170

Radiation-Induced Esophageal Carcinoma 30 Years after Mediastinal Irradiation: Case Report and Review of the Literature
Introduction
Case Report
   Clinical History
   Retrospective Dose Analysis
   Retrospective Case Analysis
Discussion
   Clinical History
   Retrospective Dose Analysis
   Retrospective Case Analysis
Conclusions
References
Radiation-Induced Esophageal Carcinoma 30 Years after Mediastinal Irradiation: Case Report and Review of the Literature

Radiation-Induced Esophageal Carcinoma 30 Years after Mediastinal Irradiation: Case Report and Review of the Literature

Oliver Micke, Ulrich Schäfer, Marco Glashörster, Franz-Josef Prott and Normann Willich

Department of Radiotherapy and Radiation Oncology, University of Münster, Münster, Germany

A 54-year-old man who had been irradiated in 1964 for cervical involvement by Hodgkin's disease was admitted in December 1994 to our clinic with strong complaints of dysphagia. The reason was a moderately differentiated squamous cell carcinoma of the proximal esophagus in the previously irradiated region. The patient had no risk factors (abuse of nicotine or alcohol) for the developement of esophageal carcinoma. A reirradiation was performed, but the disease progressed locally and two weeks after the beginning of the therapy the patient developed two tracheoesophagocutaneous fistulae. The radiation therapy was discontinued and the tumor stenosis was bridged by a tube closing the fistulae. A retrospective dose analysis to evaluate the applied doses will be performed. Furthermore, an overview of 66 cases of the literature with radiation-induced esophageal carcinoma analysed concerning applied dose and latent interval will be given. In conclusion the reported case fits the criteria for radiation-induced malignancies (Chudecki Br J Radiol 1972;45:303-4) known from literature: (1) a history of previous irradiation, (2) a cancer occurring within the irradiated area, (3) gross tissue damage due to an excessive dose of radiation, and (4) a long latent interval between irradiation and development of cancer. Esophageal carcinomas belong to the rare secondary malignancies after the therapeutic use of ionizing radiation. Nevertheless in patients with dysphagia they should be suspected as a differential diagnosis even many years after mediastinal irradiation. The treatment of these tumors is very difficult and is associated with a poor prognosis.

Key words: radiation-induced esophageal carcinoma - secondary malignancies - late effects of radiation therapy - Hodgkin's disease

INTRODUCTION

The carcinogenic effect of ionizing radiation is well-documented (1-4). As early as six years after the discovery of X-rays the first malignancy induced by ionizing radiation was described. It was a spinocellular carcinoma of the skin of the hand of a 33-year-old technician who regularly worked with X-rays (3,4).

A characteristic of radiation-induced secondary malignancies is the long latency (mostly 10 to 20 years) between radiation exposure and the development of cancer in the irradiated area (3, 5, 6).

With the recent advances in surgery, radiotherapy and chemotherapy significantly more long-term remissions can be achieved. Therefore the rate of secondary malignancies has also increased (7-9).

The exact incidence of radiation-induced malignancies is not well-defined because of their rarity and their long latency before appearance (10). There are some studies about secondary malignancies after the radiation treatment of Hodgkin's disease. Soft tissue sarcomas and osteosarcomas are the most frequently described solid radiation-induced tumors after radiotherapy of Hodgkin's lymphoma (7-9). On the other hand hematological malignancies, especially acute leukemias, have been observed after radiation exposure. These disorders were particularly found in the atomic bomb survivors of Hiroshima and Nagasaki (1).

The esophagus belongs to the organs of risk of an irradiation of the mediastinal or the sternal region (1,5,6,11). In most patients different degrees of esophagitis occur (11-13) immediately after mediastinal irradiation. In contrast esophageal carcinomas have been rarely reported in the literature as secondary solid tumors long periods of time after ionizing therapeutic irradiation (10). The majority of cases were diagnosed quite late and are difficult to treat for the radiooncologist (14).

A case of a radiation-induced esophageal carcinoma is now described and discussed in the context of the available literature.

CASE REPORT

Clinical History

A 54-year-old man was referred to our radiooncological clinic with hoarseness and progredient complaints of dysphagia in December 1994.

In March 1964 the patient was diagnosed to have a Hodgkin's disease stage I with left cervical involvement. He was treated with definitive radiotherapy using a single-field technique at a Cobalt-60 machine with a focus-skin distance of 50 cm. Doses of 50 Gy were applied over a left neck field (specified to 4 cm tissue depth), 35 Gy over a mediastinal field (specified to 6 cm) and 25 Gy over a left axillary field (specified to 4 cm). A single dose of 3.0 Gy surface dose was delivered five times a week.


Figure 1. Esophagoendoscopy showing an irregular wall shapening of esophagus between 21 and 25 cm.

The irradiation set-up was done clinically. Simulation and verifications were not performed. The patient tolerated the radiation therapy without significant early side effects.

Nine years later subcutaneous indurations developed in the previously irradiated left supraclavicular region. The patient complained of severe pain extending from the left shoulder to the left arm. In 1976 for the first time he showed impairments of arm movements and increasing parasthesia as a sign of radiation-induced plexus injury. Further the left cervical fibrosis got more pronounced. In 1983 a microsurgical neurolysis of the left plexus brachialis was performed. But no clear success in pain reduction could be achieved.

Because of dysphagic complaints esophagoscopy with biopsy was carried out in January 1995 (Fig. 1). A poorly differentiated squamous cell carcinoma (G3) of the upper thoracic esophagus (21 to 25 cm) could be proven (Fig. 2). An infiltration of the trachea was suspected by CT-scan. Additionally paraesophageal lymph nodes have been detected. There were no distant metastasis. According to the TNM-classification of the UICC (1992) a clinical stage T4 N1 M0 resulted.


Figure 2. Histology of the biopsy (HE-staining): poorly differentiated squamous cell carcinoma.

The patient had no evidence for typical risk factors (abuse of nicotine or alcohol) for developing esophageal carcinoma. Surgical resection was not possible, because of the tumor localization. An MRI of the chest was carried out for determination of tumor extent and radiation therapy treatment planning (Fig. 3).


Figure 3. T1-weighted sagittal MRI-sequence with gadolinium-DTPA showing an irregular shaped tumorous thickening of the wall of the proximal esophagus corresponding to the endoscopic proven esophageal carcinoma.

There was no further option for percutaneous irradiation due to the preirradiation and the marked subcutaneous fibrosis. For palliation of the pronounced dysphagia endoesophageal High-Dose-Rate-brachytherapy with Iridium-192-afterloading was performed using an bougie-applicator with a diameter of 1 cm. During radiation therapy the tumor locally progressed two weeks after the beginning of therapy and two applications of 5 Gy two tumorous tracheoesophagocutaneous fistulas arose (Fig. 4). The radiation treatment was then discontinued. The tumor stenosis of the esophagus was endoscopically bridged by a tube which closed the fistulas. One month later the patient died from aspiration pneumonia.


Figure 4. Computed tomography of the upper mediastinum showing one of the two tracheoesophagocutaneous fistulas.

Retrospective Dose Analysis

Having no sufficient documentation of the former irradiation, we tried to reconstruct the set-up using an actual CT-scan of the neck and mediastinum aided by a modern computer assisted treatment planning system (Cadplan®, Varian).

We assumed that the diameter and the contours of the patients body have not significantly changed.

Doses of 35 Gy specified to 6 cm tissue depth were applied over an anterior mediastinal field in which the radiation-induced esophageal carcinoma developed. The retrospective dose analysis resulted in a cumulative dose of 34 to 35 Gy at the upper thoracic esophagus (Fig. 5). Possible field overlaps resulting from the historically used single field irradiation technique could retrospectively not be evaluated. Of course it could not be excluded that areas of inadequate field matches could have caused considerable overdosage zones. One can speculate that from overlapping portals cumulative doses from over 65 Gy could result.


Figure 5. 3D-dose distribution of the reconstructed field arrangement showing the 36 Gy-isodose (white lines).

Retrospective Case Analysis

A review of the literature of the cases describing radiation-induced esophageal cancer will be presented (Table 1). They will be analysed concerning the relationship between applied dose and latent interval. So far 66 patients including the patient in this study have been reported. Most patients were female. The reported patients received doses between 18.6 and 68 Gy (median dose: 40 Gy) as primary treatment. The interval between radiation exposure and occurrence of the secondary esophageal carcinoma had a median of 15 years (ranging from 2 to 63 years). Most cases were moderately or poorly differentiated squamous cell carcinomas.

We statistically analysed the data of applied doses and latent interval from the literature overview including our own results using a linear regression model. The result of the analysis was statistically tendentially significant with P = 0.0738 (Fig. 6).


Figure 6. Linear regression of latency in correlation to the applied radiation doses (significance level = 0.0738).

In 43 of the 66 retrospectively analysed patients details about treatment of the radiation-induced esophageal carcinoma and the final outcome were available. Most patients (n = 26) received a surgical resection, 14 patients were treated with radiotherapy, two with chemotherapy and one patient received hyperthermic chemotherapy. Eleven of the 26 surgically treated patients (42.3%) achieved a long-term curation from surgical intervention. None of the patients treated with radiotherapy or chemotherapy could be cured. Only the patient who received hyperthermic chemotherapy had a long-term remission.

Table 1. Overview of the literature reporting radiation-induced esophageal carcinomas after mediastinal irradiation (SCC = Squamous cell carcinoma)
Author Primary diseases Dose Latency Histology
Slaughter et al. 1957 (17) Swollen glands ? 27 years Adenocarcinoma
Goolden 1957 (29) Thyreotoxicosis ? 37 years SCC
Garret 1959 (30) Thyreotoxicosis ? 25 years SCC
Thyreotoxicosis ? ? SCC
Fabrikant et al. 1964 (6) Laryngeal carcinoma 49 Gy 8 years SCC
McGraw et al. 1965 (31) Tuberculous adenitis ? 31 years SCC
Goolden et al. 1965 (32) Thyreotoxicosis ? 45 years SCC
Kobayashi et al. 1969 (33) Tuberculous adenitis 23.4 Gy 43 years SCC
Chudecki 1972 (5) Lymphosarcoma 26 Gy 10 years SCC
Rigaud et al. 1975 (34) Esophageal carcinoma 60 Gy 10 years Small cell cancer
Ito et al. 1978 (35) Breast cancer 41,8 Gy 12 years SCC
Breast cancer 18,6 Gy 16 years SCC
Charles et al. 1979 (36) Goiter ? 52 years ?
Goiter 40 Gy 50 years ?
Mullen et al. 1979 (37) Hodgkin's disease 40 Gy 10 years SCC
Yoshida 1979 (38) Laryngeal carcinoma ? 17 years ?
Laryngeal carcinoma 45 Gy 10 years SCC
Goffman et al. 1983 (39) Breast cancer 50 Gy 9 years SCC
Sherrill et al. 1984 (40) Embryonal testicular carcinoma 60 Gy 12 years SCC
Malignant teratoma 40 Gy 28 years SCC
OConnel et al. 1984 (25) Bronchial carcinoma 50 Gy 11 years SCC
Thyreotoxicosis 32 Gy 30 years SCC
Jones et al. 1985 (41) Hodgkin's disease 38 Gy 11 years SCC
Kai et al. 1985 (14) Mediastinal neoplasm 60 Gy 31 years SCC
Grosser et al. 1986 (10) Malignant thymoma 60 Gy 14 years SCC
Hodgkin's disease 36 Gy 21 years SCC
Marchese et al. 1986 (18) Thyreotoxicosis 32 Gy 40 years SCC
Renard et al. 1989 (42) Hodgkin's disease 32 Gy 19 years SCC
Davidson et al. 1990 (43) Breast cancer 29 Gy 12 years SCC
Breast cancer 30 Gy 7 years Small cell cancer
Breast cancer 24 Gy 17 years SCC
Breast cancer 30 Gy 14 years SCC
Breast cancer 24 Gy 34 years SCC
Breast cancer 31 Gy 8 years SCC
Shimizu et al. 1990 (28) Thyroid carcinoma 48 Gy 27 years SCC
Vanagunas et al. 1990 (13) Hodgkin's disease 39 Gy 21 years SCC
Thymus hyperplasia ? 24 years SCC
Ogino et al. 1992 (27) Goiter ? 44 years SCC
Thyroid carcinoma 40 Gy 30 years SCC
Breast cancer 53 Gy 20 years SCC
Breast cancer 36 Gy 23 years SCC
Taal et al. 1993 (22) Hodgkin's disease 40 Gy 11 years SCC
Breast cancer 35 Gy 2 years SCC
Breast cancer ? 5 years SCC
Laryngeal carcinoma 47 Gy 17 years SCC
Goiter ? 40 years SCC
Thyreotoxicosis ? 36 years SCC
Tuberculosis ? 63 years SCC
Breast cancer 50 Gy 6 years SCC
Hodgkin's disease ? 44 years SCC
Laryngeal carcinoma 40 Gy 9 years SCC
NHL 40 Gy 4 years SCC
Laryngeal carcinoma ? 36 years SCC
Bronchial carcinoma 53 Gy 8 years SCC
Bronchial carcinoma ? 9 years SCC
Hodgkin's disease 42 Gy 15 years SCC
NHL 40 Gy 6 years SCC
Fékété et al. 1993 (16) Hodgkin's disease 40 Gy 9 years SCC
Breast cancer 55 Gy 8 years SCC
Breast cancer 45 Gy 8 years SCC
Breast cancer ? 11 years SCC
Brink et al. 1994 (21) Bronchial carcinoma 68 Gy 9 years SCC
Bronchial carcinoma 40 Gy 9 years SCC
Hodgkin's disease 20 Gy 11 years SCC
Glanzmann et al. 1994 (7) Hodgkin's disease 40 Gy 15 years SCC
Own case Hodgkin's disease 35 Gy 30 years SCC
Total 66 patients 18.6 to 68 Gy
(Median: 40 Gy)		 2 to 63 years
(Median: 15 years)		 Mostly SCC

DISCUSSION

Clinical History

The reported case fits the criteria for radiation-induced malignancies of the esophagus known from literature reported by Chudecki in 1972 (5):

  1. A history of previous irradiation.
  2. A cancer occurring within the irradiated area.
  3. Gross tissue damage due to an excessive dose of radiation.
  4. A long latent interval between irradiation and development of cancer.

There is a close correlation between the spontaneous development of esophageal carcinoma and special nutritional factors as well as the abuse of nicotine and alcohol. Therefore the absence of these risk factors connected with a marked radiation exposure of the esophagus is a clear indication for a radiation-induced esophageal carcinoma (15).

Of course one is not able to confirm the diagnosis of a radiation-induced esophageal carcinoma unequivocally, because radiation-induced carcinomas do not differ histologically from spontaneously developed carcinomas (5,10,16).

The esophagus belongs to the less radiation-sensitive organs (2,11,13). The most important acute side effect is esophagitis of different degrees (13). Fibroses and scarred esophageal strictures are found as chronic radiation reactions (2,11,13). Radiation-induced esophageal carcinomas have been seldom described in the literature. The first scientific report is from the late 1950s (17). Radiation-induced tumors account for less than 1% of all carcinomas of the esophagus (18).

The development of radiation-induced esophageal carcinomas after the therapeutic application of ionizing radiation could be proven by experimental data in animal models (19). In a population-based retrospective cohort study Ahsan et al. (20) described a 5.42-fold increased risk for esophageal squamous cell carcinoma in women who had received radiation therapy for breast cancer compared to unirradiated breast cancer patients.

According to the literature, the therapy of choice in radiation-induced esophageal carcinomas is complete surgical resection (16,21,22). Frequently, a radical surgical approach is not possible because of tumor extension, the radiation damage or a reduced performance status of the patient. In these cases reirradiation alone or palliative chemotherapy can be carried out (21), because radiation-induced malignancies are not less sensitive to radio- and chemotherapy than their spontaneously developed counterparts (14). External beam reirradiation is seldom possible because of overlapping with the former portals. Endoluminal brachytherapy can provide an alternative (21).

The treatment with the highest curative potential according to literature is radical surgical intervention (16,22). Patients without radical resection died within a few months (22).

Retrospective Dose Analysis

The retrospective dose analysis resulted in a cumulative dose of 34 to 35 Gy at the upper thoracic esophagus. This is a dose which is in the range of doses reported in the literature.

Using a single field irradiation technique it could not be concluded that areas of inadequate field matches could have resulted in marked overdosage zones with doses of above 65 Gy.

Whether this phenomenon supported the induction of a secondary malignancy must remain unclear. The marked plexus injury the patient consecutively developed could have resulted from those incalculable overdosage zones. Emami et al. (2) reported a TD5/5 of 60 Gy and a TD50/5 of 75 Gy for developing brachial plexopathy. The speculated overdosage zones may be in this range, that the plexus injury can be assumed to be radiation-induced.

Further it should be taken into account that an increased daily dose had been applied with a surface dose of 3 Gy corresponding to a treatment target volume dose of about 2.5 Gy. It is well known from the literature that the incidence of radiation-induced plexus injuries is higher after increased single doses (23,24).

Retrospective Case Analysis

The relationship between applied dose and time interval between treatment and the occurrence of the secondary malignancy has been controversially discussed in literature. Some authors stated that higher doses shortened the latent interval (3,4,25,26). Experimental data from animal models could prove a time-dose relationship (26). Other authors could not find this correlation (10,27). Therefore we statistically analysed the data from the overview of literature including our own results using a linear regression model. The result of the analysis was statistically tendentially significant with P = 0.0738 (Fig. 6) supporting a time-dose relationship.

As shown above the treatment with the highest curative potential is radical surgical resection (16,22). None of the patients treated with radiotherapy could be cured.

Taal et al. (22) reported the largest series of eight patients with radiation-induced esophageal carcinomas treated with reirradiation. As in our case report not all patients were eligible for full dose radiotherapy. The reported survival in this series ranged between 2 and 13 months. Our reported patient survived only one month after the end of radiation treatment. The use of endoesophageal HDR-brachytherapy as a palliative treatment of radiation-induced esophageal carcinoma has not been described in the literature so far.

CONCLUSIONS

Esophageal carcinomas belong to the rare secondary malignancies after the therapeutic use of ionizing radiation. Nevertheless, they should be suspected in patients with dysphagia as a differential diagnosis even many years after mediastinal irradiation (28). The treatment of these tumors seems to be difficult and their overall prognosis is poor.

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Received August 17, 1998; accepted November 19, 1998
For reprints and all correspondence: Oliver Micke, Department of Radiotherapy and Radiation Oncology, University of Münster, Albert-Schweitzer-Str. 33, D-48129 Münster, Germany. E-mail: OMicke{at}aol.com
This work is dedicated to Tsugio Mimuro, who worked hard in strengthening the Japanese-German scientific relationship.

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