Comparison of single versus fractionated dose of stereotactic radiotherapy for salvaging local failures of nasopharyngeal carcinoma: a matched-cohort analysis
© Chua et al; licensee BioMed Central Ltd. 2009
Received: 15 May 2009
Accepted: 23 May 2009
Published: 23 May 2009
wLocal failure is an important cause of morbidity and mortality in nasopharyngeal carcinoma (NPC). Although surgery or brachytherapy may be feasible in selected cases, most patients with local failure require external beam re-irradiation. Stereotactic radiation using single or multiple fractions have been employed in re-irradiation of NPC, but the optimal fractionation scheme and dose are not clear.
Records of 125 NPC patients who received salvage stereotactic radiation were reviewed. A matched-pair design was used to select patients with similar prognostic factors who received stereotactic re-irradiation using single fraction (SRS) or multiple fractions (SRM). Eighty-six patients were selected with equal number in SRS and SRM groups. All patients were individually matched for failure type (persistent or recurrent), rT stage (rT1-2 or rT3-4), and tumor volume (≤ 5 cc, >5–10 cc, or >10 cc). Median dose was 12.5 Gy in single fraction by SRS, and 34 Gy in 2–6 fractions by SRM.
Local control rate was better in SRM group although overall survival rates were similar. One- and 3-year local failure-free rates were 70% and 51% in SRS group compared with 91% and 83% in SRM group (p = 0.003). One- and 3-year overall survival rates were 98% and 66% in SRS group compared with 78% and 61% in SRM group (p = 0.31). The differences in local control were mainly observed in recurrent or rT2-4 disease. Incidence of severe late complications was 33% in SRS group vs. 21% in SRM group, including brain necrosis (16% vs. 12%) and hemorrhage (5% vs. 2%).
Our study showed that SRM was superior to SRS in salvaging local failures of NPC, especially in the treatment of recurrent and rT2-4 disease. In patient with local failure of NPC suitable for stereotactic re-iradiation, use of fractionated treatment is preferred.
Local recurrence is an important cause of treatment failure in nasopharyngeal carcinoma (NPC). Recent advances in radiotherapy planning and delivery and the use of concurrent chemo-radiotherapy have significantly reduced the incidence of local failure in NPC, and most modern series reported an overall 5-year local control rate of 76–91% [1–5]. In patients with advanced T stage and/or bulky tumor, local failure however remains an important cause of morbidity and mortality. Although surgical resection or brachytherapy can be used as salvage treatment in selected cases of local failure, most patients require external re-irradiation for retreatment of NPC. Conventional two-dimensional radiotherapy planning and delivery was commonly used in the past for external reirradiation of NPC, but treatment outcome was generally poor with a high incidence of severe late complications [6–8]. Three-dimensional conformal radiotherapy can achieve better target coverage and sparing of critical structures, but the incidence of late complication still appears to be high after reirradiation of NPC even with the use of conformal radiotherapy . The technique of stereotactic localization of target and treatment delivery has also been employed in salvaging local failures of NPC, which includes the use of single fraction of stereotactic re-irradiation (SRS) or multiple fractions of stereotactic re-irradiation (SRM). These two techniques were employed at Queen Mary Hospital in Hong Kong and Sun Yat Sen University Cancer Center in Guangzhou for re-irradiation of NPC, with adoption of SRS in the former center and SRM in the latter one. Different techniques were adopted at the two centers due to institutional preference and logistic reasons such as available machine time. Since there were no prospective studies comparing stereotactic re-irradiation using SRS or SRM, we conducted a retrospective study to compare the outcome of patients treated by SRS and SRT using a matched-pair design.
Selection of matched pair
This was a retrospective study comparing the outcome of patients with locally recurrent NPC treated by SRS and SRM. Records of patients who received SRS or SRM as salvage treatment of NPC at Queen Mary Hospital in Hong Kong and Sun Yat-Sen University in Guangzhou were reviewed for inclusion into the study. A matched pair study was used to select and analyze patients with similar prognostic factors from the two treatment groups. Only those patients who satisfied the following criteria were included in the matching process: history of poorly differentiated or undifferentiated carcinoma of the nasopharynx, completed a course of radical radiotherapy with or without chemotherapy, and histological proven local failure or progression of local disease documented by serial imaging. Patients who received SRS or SRM as a planned boost after external radiotherapy and those with disease elsewhere were excluded.
Individual patients from the two treatment groups were matched for important prognostic factors identified from previous studies: type of local failure (persistent disease, defined as local failure that occurred within 6 months of completion of primary radiotherapy, vs. recurrent disease, defined as local failure that occurred beyond 6 months of completion of primary radiotherapy), retreatment T stage (rT1-2 vs. rT3-4), and tumor volume (≤ 5 cc vs. > 5 – 10 cc vs. > 10 cc). Each patient in the SRS group was matched with another patient in the SRM group with respect to these factors, and only patients that were matched for all 3 factors were included in the study.
Characteristics of patients treated by stereotactic reirradiation using single and multiple fractions and for local failures of nasopharyngeal carcinoma
Stereotactic radiotherapy with single fraction
(n = 43)
Stereotactic radiotherapy with multiple fractions
(n = 43)
(n = 86)
Type of failure
Retreatment T stage
Time from 1st course of radiotherapy to reirradiation
≤ 12 months
> 12 – 24 monhts
> 24 – 48 months
> 48 months
10 (3 – 197)
10 (3 – 107)
10 (3 – 197)
≤ 5 cc
> 5 – 10 cc
> 10 cc
5.1 (1.3 – 30.7)
5.6 (0.8 – 24.7)
5.2 (0.8 – 30.7)
SRS and SRM treatment
Response assessment and follow-up
Nasopharyngoscopy +/- biopsy and imaging were performed at 8–12 weeks after treatment to document local disease status. Patients with controlled local disease were regularly followed up every 2–3 months in the first year and every 3–4 months thereafter. Computed tomography and/or magnetic resonance imaging were performed at least annually for 3 years after treatment.
Categorical variables were compared using chi square test or Fisher's exact test as appropriate, and continuous variables were compared using Student's t test. Treatment outcome of SRS and SRM groups were compared using the following endpoints: local failure-free rate, nodal failure-free rate, distant failure-free rate, failure-free rate and overall survival rate. The endpoints were analyzed using the product-limit method of Kaplan and Meier, and time was measured from the date of SRS or SRM until time of event occurrence, or most recent follow-up for censored observations. In patients with complete regression of disease after SRS or SRT, local failure was defined based on positive biopsy and/or radiological evidence of relapse. In patients who failed to achieve complete regression of disease after salvage treatment, local failure-free interval was set to zero. Likewise, neck node recurrence was used to define nodal failure-free rate, distant metastases was used to define distant failure-free rate, and any failure (loco-regional or distant) was used to define failure-free rate. In determining overall survival rate, event was defined as deaths due to any cause. Actuarial curves were compared between SRS and SRM groups and the significance of differences was calculated using log rank test, a p value less than 0.05 was considered to be statistically significant.
Tumor control and survival
Both SRS and SRM were well tolerated with no severe acute complications. The incidence of severe late complications was higher in SRS group compared with SRM group (33% vs. 21%), although the difference was not statistical significant (p = 0.22). Brain necrosis occurred in 7 patients after SRS (16%) and 5 patients after SRT (12%), with 2 fatal outcome. Massive heamorrhage occurred in 2 patients after SRS (2%) and 1 patient after SRM (4%), with 1 fatal outcome. Altogether there were 3 treatment-related deaths, all occurred in the SRM group.
Subgroup analysis of treatment outcome after stereotactic radiosurgery or radiotherapy for local failures of nasopharyngeal carcinoma
3-year local failure-free rate
3-year overall survival rate
Type of failure
≤ 5 cc
> 5 – 10 cc
> 10 cc
Aggressive treatment of local failure of NPC is generally recommended since a significant proportion of patients can still be successfully salvaged and long-term survivors are not uncommon with reported 5-year survival rates ranging from 54% after surgery  to 60–77% after brachytherapy [11, 12]. Although surgery and brachytherapy can produce excellent results, only selected cases of local failure of NPC with disease confined to nasopharynx are amenable to these treatments. Most patients with local failure of NPC require external beam radiotherapy but treatment results after re-irradiation using conventional technique remained poor. The reported five-year survival rates after external reirradiation ranged from 7.6% to 36% with the use of conventional two-dimensional treatment planning and radiotherapy (6–8), and 12.4% in a mixed cohort of patients treated either with conventional two-dimensional or three-dimensional conformal radiotherapy . A high incidence of late complication was commonly observed after external beam reirradiation, majority being neurological damage and soft tissue fibrosis. In a cohort of patients with local failure of NPC and all received re-irradiation by three-dimensional conformal technique, the incidence of severe late complications was still high with 5-year actuarial incidence of 100% for ≥ grade 3 toxicity and 49% for ≥ grade 4 toxicity (9).
The concept of applying SRS in the retreatment of NPC is attractive due to the frequent involvement of intracranium and base of skull in NPC and the general radiosensitivity of the tumor. There were several published reports of retreatment of NPC by SRS and the reported tumor control rates ranged from 53 to 86% [14–20], but most of these were small series with a relatively short follow-up. In a previous report based on patients treated by SRS at Queen Mary Hospital, 5-year local failure-free and overall survival rates were 47.2% and 46.9%, respectively . Neuroendocrine complications occurred in 27% of patients but there were no treatment-related deaths. The results of that report compared favorably with that of gold grain implantation based on outcome of patients treated at the same institution .
Based on radiobiology principle, fractionation will provide better therapeutic ratio and improve treatment outcome in retreatment of NPC, and SRM has subsequently been explored as a salvage treatment for NPC. Mitsuhashi et al treated 3 patients with rT1 NPC using SRM at a dose of 50–64 Gy, and all 3 patients achieved complete response and remained free of local disease at 4–61 months . The report by Mitsuhashi et al also included another patient with mucoepidermoid carcinoma of the nasopharynx treated by SRM after previous two courses of external radiotherapy, but the treatment was complicated by rupture of the internal carotid artery resulting in patient death. Using SRM at a dose of 24 Gy in 2 to 4 fractions, Orecchia et al reported a less satisfactory outcome in 13 patients with locally recurrent NPC, with a 3-year survival rate of 31% . Ahn et al treated 12 patients with recurrent NPC by SRM using a median dose of 54 Gy, and reported a 2-year local control rate of 92% . Yau et al compared the outcome of 52 patients with NPC treated by either brachytherapy or SRT for persistent disease, and observed a better tumor control after SRM . Xiao et al reported the outcome of 50 patients with persistent or recurrent nasopharyngeal carcinoma treated by SRM with a dose ranged from 14 to 35 Gy using a fraction dose of 5 to 15 Gy . Of the 31 evaluable patients with persistent disease, 94% had complete response with a one-year disease-free survival rate of 47%. Eighteen patients, most of them had rT3-4 tumor, were treated for recurrent disease. The complete response rate was 56% and 1-year disease-free survival rate was 47%. In Xiao's series, however, 16% of patients treated by SRM developed fatal haemorrhage, probably due to the relatively high cumulative dose delivered. The largest published series was from the primary data set of 90 SRT patients used for the current study . The reported 3-year local control rate was 89% for persistent disease and 19% for recurrent disease. Three-year disease-specific survival rate was 58%. The incidence of severe late complications was 19% and there were 3 treatment-related deaths.
Based on matched-pair data from the two largest reported SRS and SRM series for NPC, we demonstrated superior tumor control with SRM, but survival rates were similar. Possible explanations include different follow-up duration in the two groups, the higher incidence of treatment-related deaths in SRM group, the use of additional salvage treatments, and different failure patterns. In SRM groups, no additional radiotherapy was given after local failure due to the high cumulative dose, whereas in SRS group, additional radiotherapy was given whenever possible after documented treatment failure. Thus the use of second salvage treatment may partly account for comparable survival rates in the two groups. In addition, patients in SRM group had a higher incidence of distant metastases than SRS group probably related to the percentage of higher N stage in the former group, and the survival benefits obtained with improved local tumor control were likely to be offset by the occurrence of distant metastases.
Late complications are common in patients receiving re-irradiation for NPC. In view of the high radiation dose already received by patients during prior radiotherapy and the presence of numerous nearby critical structures, it is unrealistic to expect any new form of re-irradiation to be totally risk-free. Late complications, however, differ significantly in terms of incidence and severity among different techniques of re-irradiation. In general, patients with bulky disease and tumor extended beyond nasopharynx usually have a higher incidence of late complications. When patients with similar tumor extent and size are being considered, SRS or SRM usually leads to lower incidence of late complications compared with other techniques because of high dose conformity to the target. One severe and highly fatal complication that can occur after re-irradiation is massive hemorrhage in the nasopharynx, sometimes leading to fatal outcome. The reported incidence of severe hemorrhage after SRS or SRM was relatively high compared to other re-irradiation techniques. Possible causes of severe hemorrhage after re-irradiation include mucosal necrosis, tumor progression, and carotid aneurysm. The latter one is an important cause of uncontrolled bleeding which should not be overlooked. In order to reduce the risk of hemorrhage as a result of carotid aneurysm/rupture following re-irradiation, careful selection of patients and treatment planning are important. Patients with direct tumor encasement of cavernous sinus and internal carotid artery should not be treated by SRS, and the dose to carotid artery should be minimized in all cases. Dose per fraction is also important and most hemorrhage occurred after SRS or SRM using large fractional dose. In patients with tumor encasement of carotid artery, SRM instead of SRS should be used for reirradiation, and a small fractional dose not exceeding 6 Gy is recommended.
The superior tumor control rate achieved by SRM is likely due to the higher dose that can be delivered using this technique compared with SRS. Several reirradiation series have also recognized the important relationship between reirradiation dose and treatment outcome, although the optimal dose is not yet defined. Wang observed reirradiation dose ≥ 60 Gy was associated with improved survival, although most patients received high dose radiotherapy in his series had rT1-2 stage . Similarly, Öksüz et al also reported improved local control and survival after reirradiation with a dose of 60 Gy than < 60 Gy . Lee et al also reported improved survival when a reirradiation dose > 60 Gy was used . Teo et al however reported poor survival and high incidence of complications after high dose (≥ 60 Gy) reirradiation of NPC with radical intent, although the survival was still better than those treated with palliative intent using a lower dose of 40–50 Gy . In all these series, retreatment was primarily carried out using conventional two-dimensional radiotherapy. In a cohort of 186 NPC patients reirradiated with either conventional or conformal radiotherapy, Chang et al observed that reirradiation dose ≥ 50 Gy yielded better survival . Using intensity-modulated radiotherapy, Lu et al  reported excellent local control rate after high dose (68–70 Gy) retreatment of NPC, although the follow-up time in that study was still short for evaluation of late complications. In another series of reirradiation of NPC also using intensity-modulated radiotherapy, a dose range between 50–60 Gy yielded good tumor control for rT1-3 NPC but not for rT4 disease . Based on these reports, a dose of at least 50 Gy should be delivered using SRM for local failure of NPC, although the optimal fractionation schedule is still not clear. In patients with persistent disease, especially those with small volume disease confined to nasopharynx, a lower dose may be used judging from the results of SRS.
In conclusion, our study showed that SRM was superior to SRS in salvaging local failures of NPC, especially in patients with recurrent disease and tumor extended beyond nasopharynx. In patients with local failure of NPC, stereotactic re-irradiation using multiple fractions rather than single fraction to deliver a higher total is preferred.
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