Long-term outcomes of stereotactic ablative brachytherapy for recurrent aggressive fibromatosis: an eight-year retrospective multicenter study

doi:10.21203/rs.3.rs-3562126/v1

Background

Aggressive fibromatosis (AF) was characterized by a high potential of recurrence even following initial definitive treatment. There were considerable controversies regarding the management of recurrent AF. This study aimed to explore the long-term outcomes of iodine-125 (I-125) seed stereotactic ablative brachytherapy (SABT) for recurrent AF.

Methods

A multicenter retrospective study reviewed 38 recurrent AF patients receiving I-125 seed SABT from July 2013 to July 2021.The clinical outcomes including overall response rate (ORR), disease control rate (DCR), local control time (LCT), overall survival (OS), adverse events (AEs), and symptom relief rate were statistically assessed.

Results

The ORR and DCR reached 76.3% and 100.0% respectively. The 3-, 5 and 9-year LCT rates were 81.0%, 68.6% and 62.3% respectively. The 3-, 5 and 9-year OS rates reached 94.5%, 84.8% and 60.4% respectively. Multivariate analyses showed that smaller tumor volume and higher dose were significantly positive prognostic factors of LCT (P = 0.034, P = 0.047). Prognostic factors of OS were not found. 20 (52.6%) patients presented with various symptoms at diagnosis, of which 90% (18 patients) achieved complete or partial relief after SABT. The AEs were generally graded ≤ 1 and well-tolerated.

Conclusions

SABT was an effective and safe alternative treatment for recurrent AF with high safety.

Aggressive fibromatosis

Iodine-125

Stereotactic ablative brachytherapy

Interstitial brachytherapy

Aggressive fibromatosis (AF), also called “desmoid tumor”, a rare fibrous tumor originating from deep mesenchymal tissues from head to foot, was characterized by lowgrade malignancy and high recurrent rate (1). Generally, AF locally invaded the surrounding tissues and didn’t metastasize to distant sites.

Although the optimal management of AF was still controversial, historically the main treatment for untreated AF was surgical resection. This tumor infiltrated along the fascial planes and lacked for tumor capsule (2). Therefore, it was quite difficult to distinguish the boundary of AF, and resection with a negative margin was almost impossible(2). Even though radical resection was achieved, it was reported that the recurrent rate reached approximately 30% and the local control rate was 47–86% (3, 4).

The patients with primary AF unfit for surgery usually received external beam radiotherapy (EBRT). However, the local recurrence rate reached approximately 25% and the local control rate varied from 65–83% (4, 5).

After the failure of initial treatments (eg. surgery or radiotherapy), there was no consensus on the management of the recurrent AF. Although the salvage surgical resection, generally, was considered as the preferred treatment in the past, no sufficient and powerful evidence confirmed the superiority of surgery over other therapies which have lower potential of complication(6). Moreover, recurrent AF following repeated resections would tend to invade surrounding tissues in a concentric way, which would gradually invade more tissues, important organs and major vessels. What’s harder, the boundaries of the tumors after prior resections were difficult to distinguish intraoperatively from scars and connective tissue, which made R0 resection difficult, especially in mesenteric desmoid disease as the mortality of surgery was 10–60% and the recurrence rate was 78%(7, 8). Furthermore, after surgery AF not only recurred in situ but also in adjacent areas, therefore it was unable to preserve normal tissues well and was likely to lead to function loss(9). Additionally, most of the patients have cosmetic concern on resection. Considering that surgery itself was one of the etiological factors of AF and the disadvantages mentioned above, surgery should be selected with caution.

In regards to the patients receiving EBRT as the initial treatment, re-EBRT was often difficult to deliver enough high lethal doses to the recurrent disease, especially in the previously irradiated area, due to the dose limitation of the organs at risks (OARs).

The difficulties mentioned above increased due to the fact that most patients have undergo complex multimodal treatment including multiple times of surgeries, radiotherapies, chemotherapies, and various combinations of these treatments. Most of these patients were reluctant to salvage surgery, EBRT and chemotherapy. Therefore, novel therapeutic strategies for the recurrent AF were urgently warranted.

Stereotactic ablative brachytherapy (SABT), characterized by delivering high radiation dose to the tumor and well sparing the adjacent normal tissues, may resolve this puzzle. The studies in increasing number demonstrated that SABT was an effective and safe alternative for most recurrent and oligometastatic cancers (10–21). Previous experiences in our center echoed these studies in recurrent head and neck soft tissue sarcoma (13), recurrent cervical cancer (17), recurrent head and neck cancer (12) and rectal cancer (18). SABT was recommended by Rectal Cancer NCCN Guidelines as a salvage treatment for locally recurrent rectal carcinoma (22) and recommended by ESMO clinical guidelines as an ablative treatment for hepatocellular carcinoma (23). This study aimed to explore the long-term outcomes of iodine-125 (I-125) seed SABT to provide more therapeutic options for recurrent AF.

Patients

The patients, diagnosed with recurrent AF, undergoing I-125 seed SABT in 3 different centers from July 2013 to July 2021 were reviewed consecutively.

Inclusion and exclusion criteria

The inclusion criteria were as follows: 1) recurrent AF confirmed by pathologic or imaging diagnosis; 2) disease size ≥ 1 cm and ≤ 10 cm; 3) medically inoperable or individual refusal to resection; 4) Karnofsky performance status (KPS) ≥ 60; 5) adequate hematological reserves, hepatic function, renal function and heart function; 7) expected survival > 3 months. The exclusion criteria mainly included: 1) unconfirmed mass; 2) tumor invading the skin or mucous membrane; 2) patients with severe bleeding tendency; 3) patients with active infectious disease, trauma and severe wounds; 4) patients with any mental disorder; 5) patients with other somatic comorbidities of clinical concern; 6) pregnancy and lactation.

Treatment

The personalized SABT procedure mainly consisted of individualized preoperative treatment planning, intraoperative radioactive seed implantation and postoperative dosimetric evaluation (Fig. 1). All procedures were performed as per relevant guidelines and regulations.

Preoperative treatment planning

Following setup and CT simulation, the delineation of gross tumor volume (GTV) and OARs was performed by radiation oncologists. Then the pretreatment plans were made by the medical physicists using the brachytherapy treatment planning system (B-TPS; Beijing Feitian Industries Inc. and Beijing University of Aeronautics and Astronautics, Beijing, China). The goal of the pretreatment plan was that 90% of the GTV (GTV D90) received the prescription dose as much as possible. The OARs received as lower dose as possible through optimization.

Intraoperative implantation

After a treatment plan was designed in the B-TPS, a coplanar 3D-printing template model including the information of needle distribution (Fig. 1d-f) was printed by the 3D printer. After re-setup, the 3D-printing template was aligned to the surface of the operative region according to the positioning line on the body, alignment line on the 3D printing template and positioning laser. Then the disposable needles (Mick Radio Nuclear Instruments, Mount Vernon, NY, USA) were inserted to the predetermined depth through the guide holes on the template. "Fine-tuning”, if necessary, was carried out. After insertion of the needles, the I-125 seeds (CIAE-6711; Chinese Atomic Energy Science Institution, Beijing, China) were implanted into the tumor through these needles.

Postoperative evaluation

The CT scan was immediately conducted to validate the postoperative distribution of seeds and calculate the actual dose distribution in the tumor volume. Usually, D90 was used to evaluate the dosimetry, where D90 indicated the dose delivered to 90% of GTV.

Follow-up

The follow-up of the patients was performed every 3 to 6 months for the first 2 years, then every 6 to 12 months from 3 to 5 years and then annually thereafter.

Clinical outcomes

The clinical outcomes included objective response rate (ORR), disease control rate (DCR), local control time (LCT), overall survival (OS), adverse events (AEs), and symptom relief rate. The clinical responses were assessed by Response Evaluation Criteria in Solid Tumors (RECIST) version 1.1 including complete response (CR), partial response (PR), stable disease (SD), and progressive disease (PD). ORR was calculated from patients achieving CR and PR and the DCR was likewise calculated from the patients of CR, PR and SD. LCT was defined as the time from SABT to local progression; OS was defined as the time from SABT to death from any cause. The AEs were evaluated as per Radiation Therapy Oncology Group (RTOG) guidelines. The numeric rating scale (NRS) was used to evaluate the pain levels before and after treatment and the pain relief rate was calculated from the patients achieving pain relief after SABT.

Statistical analysis

The parameters of the patients and SABT were expressed as categorical variables or continuous variables using descriptive statistics analysis. The LCT and OS were descripted by the Kaplan–Meier method and compared by the log-rank test. The Cox proportional hazard regression model was used to conduct univariate and multivariate analyses for LCT and OS. Symptom relief rate and pain relief rate were described statistically. The pain scores before and after SABT were compared by paired T test. P < 0.05 was considered as statistically significant. The statistical analyses were conducted by the SPSS software version 21.0.

Patient characteristics

A total of 38 consecutive patients intended to receive SABT over 8 years, while 5 patients were finally excluded: 2 patients with coagulopathy, 2 patients with low KPS, 1 patient with mental disease and 1 patient with refractory hypertension. Finally, the SABT was performed freehand with the guidance of CT for 29 patients and was performed with the assistance of 3D-printing template and the guidance of CT for other 9 patients. The characteristics of the 38 patients were shown in Table 1.

Table 1. The characteristics of the patients.

Parameter	Variable	Value
Patient variable
Age	Median (range)	37.5 (13-61)
Sex	Male	14 (36.8)
	Female	24 (63.2)
KPS	＜90	24 (63.2)
	≥90	14 (36.8)
Previous treatment
Surgery	Yes	33 (86.8)
	No	5 (13.2)
Radiotherapy	Yes	27 (71.1)
	No	11 (28.9)
Systemic treatment	Yes	1 (2.6)
	No	37 (97.4
Tumor variable
GTV (cc)	Median (range)	83.5 (7.0-670.0)
Tumor sites	Neck	4 (10.0)
	Trunk	32 (84.2)
	Extremity	2 (5.3)
SABT variable
No. of Seeds	Median (range)	55 (13-211)
Seed activity (mCi)	Median (range)	0.645 (0.50-0.8)
D90 (Gy)	Median (range)	124 (77.5-181.4)
SABT method	CT-guided	29 (76.3)
	CT-guided and template-assisted	9 (23.7)

Abbreviations: SABT, Stereotactic ablative brachytherapy; KPS, Karnofsky Performance Score; GTV, Gross tumor volume; D90, Dose received by 90% of the GTV；cc, cubic centimeter

Treatment response

According to the RECIST 1.1 criteria, PR and SD were observed in 29 patients, and 9 patients respectively after SABT (Figure 2a-c). CR and PD were not observed. The ORR and DCR reached 76.3% and 100.0% respectively.

LCT and OS

The median follow-up time was 55.0 months. During the follow-up, 10 patients developed progression. The median LCT was not achieved and the 3-, 5 and 9-year LCT rates were 81.0%, 68.6% and 62.3% respectively. Of the 38 patients, 7 passed away. There was no treatment-related death. The median OS was not achieved with the 3-, 5 and 9-year OS rates reached 94.5%, 84.8% and 60.4% respectively. (Figure 2d-e).

Univariate and multivariate analyses of the LCT

Univariate analyses showed that smaller GTV and higher D90 were significantly associated with better LCT. Further multivariate analyses showed that the GTV and D90 were both significantly independent prognostic factors of LCT (Figure 3, Figure 4).

Univariate analyses and multivariate analyses showed no independent prognostic factors of OS (Figure 5).

Symptom relief

20 (52.6%) patients presented with various symptoms at diagnosis, of which 90.0% (18 patients) achieved complete or partial relief after SABT. Of the patients with symptoms, 13 patients suffered from mild to moderate pain before SABT, which was one of the main reasons for medical treatment. After the SABT, 100% (13/13) of these patients feel complete or partial pain relief (Figure 6). The mean pain score was significantly lower after SABT than that before SABT (1.38 vs 3.15, p=0.011).

AEs

All the AEs were graded ≤ 1 and well-tolerated (Table 2). No patient developed postoperative infection and bleeding and treatment-related death.

Table 2. Adverse events.

Adverse events	Category	N(%)
Skin reaction	I	4 (10.5)
	II	0 (0.0)
	III	0 (0.0)
	IV	0 (0.0)
Mucositis	I	0 (0.0)
	II	0 (0.0)
	III	0 (0.0)
	IV	0 (0.0)
Induration/fibrosis	I	2 (5.3)
	II	0 (0.0)
	III	0 (0.0)
	IV	0 (0.0)

In this study, most of the patients underwent previous surgical resection (86.8%, 33/38) and/or EBRT (71.1%, 27/38). Even 10 patients received two times of resection. It was a real difficulty to treat these patients with local recurrence after the multiple failures of previous treatment. These patients in the present study were deemed as inoperable as per the surgeon's consultation or personal refusal. Additionally, re-EBRT, due to the dose limitation of the normal structures or individual choice, was not recommended.

In theory, enough high radiation dose can be delivered to the tumor and the adjacent normal tissues are well spared with SABT due to the more rapid dose fall-off and lower dose rate of SABT compared with EBRT (24). The theory was validated by the facts soon that SABT had been recommended as one of the standard cares for prostate carcinoma by NCCN guidelines and for hepatocellular carcinoma by ESMO guideline for years (23, 25). Additionally, it was also recommended by expert consensus to treat most kinds of cancers including head and neck cancer, thoracic cancer, abdominal cancer, pelvic cancer and limb cancer (10, 11, 26). The SABT technique continued to advance over time, especially the invention of 3D-printing template (Patent No. ZL 2016 2 0414011.9 from our center) that significantly improved the accuracy, efficacy, security and productivity of the SABT. Therefore, SABT may be an appropriate alternative for the inoperable recurrent AF. So far, data regarding SABT for AF was little. As far as we know, this was the first multicenter study with the largest sample size, reporting the long-term outcomes of the SABT for inoperable recurrent AF. Moreover, this work firstly described the application of the advanced SABT method (3D-printing template assisted and CT-guided SABT) in recurrent AF.

In this study, the short-term efficacy was favorable with the ORR and DCR of 76.3% and 100.0% respectively. As to the long-term survival of the patients, the present study showed that the 3-, 5 and 9-year LCT rates were 81.0%, 68.6% and 62.3% respectively and the 3-, 5 and 9-year OS rates reached 94.5%, 84.8% and 60.4% respectively which indicated a favorable local control and survival of SABT for these inoperable recurrent AF patients. These favorable results were consistent with previous studies. Huang et al.(27) reported the efficacy of CT-guided SABT for AF in a small sample size study (14 patients) that the local control rate was 100% and the median OS reached 52.3 months. Zheng et al.(28) reconfirmed a good efficacy of SABT for AF in a study that the local control rate of sole brachytherapy was 100% in 5 pediatric patients. In the present study, the AEs of SABT for AF patients was mild and well acceptable. Previous studies aforementioned similarly reported that the AEs were in low probability and slight(27, 28). Collectively, our study echoed previous studies in the largest sample size indicating that SABT was characterized not only by good efficacy but also by low and accepted toxicity in recurrent AF. Ergen et al. (29) reported the efficacy and toxicity of radiotherapy for primary or recurrent AF patients with prior irradiation. In the study, the 2- and 5-year LCT rate of radiotherapy (18 patients received solo EBRT, 1 received EBRT combined with brachytherapy and 1 received solo brachytherapy) for AF was 80% and 69% respectively with a median LCT of 33 months. As to toxicity, in Ergen’s study, the most common radiation-related acute side effects were skin effects that the rate of Grade 1 and Grade 2 acute dermatitis was 55% and 35% respectively and the late side effects of radiotherapy was observed in 55% of the patients. What’ worse, one patient developed radiation-induced sarcoma after 14 years. It was worth noting that the efficacy of SABT for recurrent AF in our study was comparable with EBRT, but the AEs of SABT were significantly lower than EBRT, which indicated that SABT may be a good alternative treatment for the recurrent AF patients.

Multivariate analyses for LCT showed that the patients with smaller tumor volume and higher dose were significantly associated with a lower probability of local failure and longer LCT. Ji et al. (12) also reported that smaller tumor volume and higher radiation dose were significantly related with better local control in recurrent head and neck cancer. Qu et al. (17) released similar results in recurrent cervical carcinoma. These results were also consistent with our routine clinical experience. Enhancing local control can be achieved through dose escalation and careful selection of patients with smaller tumors.

Different from the previous studies in which the SABT was performed with free hand guided by CT, in our study, 9 patients were treated with SABT assisted by the 3D-printing template and guided by the CT. Wang et al. reported that the template assistance significantly improved the accuracy and efficacy of SABT for the recurrent rectal cancer (30). In this study, the 3D-template-assisted and CT-guided SABT showed a trend of better local control compared with CT-guided SABT, but the differences were insignificant (HR, 0.42, P=0.410) possibly due to that the sample size of the patients receiving advanced SABT was small. Moreover, the template assistance indeed increased the efficiency, shorten operation time and improve puncture accuracy of SABT.

Most of the patients in this study obtained symptom relief after SABT, especially the symptom of pain. Similar results were observed in previous studies (31-34). These consistent results suggested that SABT was effective not only on the local control of the tumor but also on the symptom relief.

As to limitations, the retrospective nature of this study lowered the evidence level of this study. Even so, it provided a new piece of evidence for SABT to treat the locally recurrent AF. More studies were warranted to further confirm the role of SABT in AF.

For patients with locally recurrent AF, SABT showed a satisfactory symptom relief, high response rate, long-term local control and favorable survival in accompany with a good safety, which suggested that SABT was a prospective effective and safe alternative option.

AF, Aggressive fibromatosis

I-125, iodine-125

SABT, stereotactic ablative brachytherapy

ORR, overall response rate

DCR, disease control rate

LCT, local control time

OS, overall survival

AEs, adverse events

RTOG, Radiation Therapy Oncology Group

NRS, numeric rating scale

EBRT, external beam radiotherapy

OARs, organs at risks

KPS, Karnofsky performance status

GTV, gross tumor volume

B-TPS, brachytherapy treatment planning system

RECIST, Response Evaluation Criteria in Solid Tumors

CR, complete response

PR, partial response

SD, stable disease

PD, progressive disease

Ethics approval and consent to participate

For this retrospective study, a waiver of informed consent to participate was obtained through the Ethics Committee of Peking University Third Hospital. The study protocol was approved by the Ethics Committee of Peking University Third Hospital (No. S2023757).

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This work was supported by special fund of National Key Research and Development Program of China (2019YFB1311305) and National Clinical Key Specialty Construction Program, P. R. China (2021).

Authors' contributions

Conceptualization, JJW and XQH; methodology, YC, CH and ZJ; Statistical analysis, YC and CH; Validation, ZJ and XFY; Data collection, XFY, YL, CH, YLJ; data curation, JJW and YC; writing—original draft preparation, YC; writing—review and editing, CH, XFY, JZ, YLJ, HTS, YL, XQH and JJW; visualization, YC, ZJ and HTS; supervision, YLJ; project administration, JJW and XQH; funding acquisition, JJW. All authors have read and agreed to the published version of the manuscript.

Acknowledgements

We are grateful to Mr. Edwin Leong for his help with editing and improvements of this manuscript.

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No competing interests reported.

Long-term outcomes of stereotactic ablative brachytherapy for recurrent aggressive fibromatosis: an eight-year retrospective multicenter study

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Background

Methods

Patients

Inclusion and exclusion criteria

Treatment

Preoperative treatment planning

Intraoperative implantation

Postoperative evaluation

Follow-up

Clinical outcomes

Statistical analysis

Results

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1