Evaluation of radioactive 125I seed implantation for the treatment of refractory malignant tumors based on CT-guided 3D template assisted technique: efficacy and safety

doi:10.21203/rs.2.17493/v2

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Evaluation of radioactive 125I seed implantation for the treatment of refractory malignant tumors based on CT-guided 3D template assisted technique: efficacy and safety

https://doi.org/10.21203/rs.2.17493/v2

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Background: To observe the medium-and long-term clinical efficacy and safety of radioactive 125I seed implantation for refractory malignant tumors based on a CT-guided 3D template-assisted technique. Methods: Twenty-five patients with refractory malignant tumors who received radioactive 125I seed implantation based on a CT-guided 3D template-assisted technique were selected. The post-operative adverse reactions were recorded; the number of puncture needles and particles used in the operation, dosimetric parameters, post-operative physical strength scores, and tumor response were statistically analyzed. The overall survival time and survival rate were counted, and the effect and prognosis were assessed. Results: 125I seed implantation was successful in all patients and no serious complications occurred. The average number of implanted puncture needles was 17 (19.12±13.00) and the median number of particles was 52 (55.12±32.97). The D90 in the post-operative clinical target volume (CTV) (93.24±15.70 Gy) was slightly lower than pre-operative CTV (93.92±17.60 Gy; P>0.05). The D90 in the postoperative planning target volume (PTV) (142.16±22.25 Gy) was lower than the pre-operative PTV (145.32±23.48 Gy; P>0.05). The tumor responses at 6 months post-operatively: complete remission (CR), 20%(5/25); partial remission (PR), 48%(12/25); stable disease (SD), 24%(6/25); progressive disease (PD), 8%(2/25); CR+PR, 68%(17/25); and local control rate, 92%(23/25). The 6-, 12-, and 24-month survival rates were 100%, 88%, and 52%, respectively. The post-operative physical strength score (Karnofsky performance score, KPS) exhibited a gradual trend towards recovery, which rose to the highest value 12 months after seed implantation, then decreased slightly, but the average score was still > 90 points. There was one intra-operative pneumothorax and two patients with superficial malignant tumors developed skin ulcerations. Multivariate analysis of prognosis showed that tumor sites and types were independent risk factors affecting survival. The number of needles and particles, and template type were not factors that affected prognosis. Conclusions: 3D template combined with CT-guided radioactive 125I seed implantation was shown to improve the rational distribution of radiation dose in the tumor target area because accurate radioactive 125I particle implantation was achieved. It has fewer complications and can further extend the overall survival and quality of life in patients with refractory malignant tumors.

Oncology

125I seed

refractory malignant tumors

3D template

efficacy

safety

With the advent and clinical application of 3D printing technology, radioactive ¹²⁵I seeds have facilitated improved treatment of malignant tumors. ¹²⁵I seed implantation assisted by a 3D template has made the treatment of malignant tumors more precise and has significantly reduced the complication rate. ¹²⁵I seed implantation assisted by a 3D template has become an effective means for the treatment of advanced malignant tumors, especially in the treatment of refractory malignant tumors, including brain metastases, pancreatic cancer, soft tissue tumors, and advanced tumors with post-operative recurrences and metastases [1-4]. With technologic advances, the type and volume of malignant tumors treated by radioactive ¹²⁵I seed implantation has gradually increased. It has not been reported, however, if seed implantation for the treatment of malignant tumors increases the incidence of severe complications, such as implant and distant metastases, due to the increased use of transplant needles during surgery.

1 General clinical data

From August 2016 to March 2017, a total of 25 patients received seed implantation in our hospital, including 17 male and 8 female patients. The average age was 65 years (64.64±14.12 years) and the age range was 44-87 years. Eight patients had lung tumors, 6 had bone metastases, 2 had pancreatic cancer, 1 had cervical and inguinal lymph node metastases, 1 had a bladder cancer recurrence, 1 had pelvic metastases, 1 had lung cancer with adrenal gland metastases, 1 had a maxillary sarcoma, 1 had lung cancer with liver metastases, 1 had a vulvar cancer recurrence, and 1 had liver cancer with brain metastases. The pre-operative physical strength score (Karnofsky performance score, KPS) was > 60, the WBC count was ≥4.0×10⁹/L, the expected survival time was > 3 months. Inclusion criteria: the patients with tumor progression after radiotherapy and chemotherapy or patients who cannot receive chemoradiotherapy were included. All patients were aware of their disease status and understood the treatment effect and adverse reactions. All patients voluntarily accepted the treatment method and signed a consent form for seed implantation surgery. The study was approved by the Ethics Committee of our hospital.

2 Materials and devices

Domestic radioactive ¹²⁵I seeds have a half-life of 60.2 d, an activity of 0.6-0.8 mCi (1 Ci= 3.7×l0¹⁰ Bq), and γ-ray energy of 27-35 keV. A brachytherapy treatment planning system [BTPS] (Beijing Astro Technology Ltd., Co., Beijing, China), domestic particle puncture needles (Japan Baguang Company, Japan) a TRH-BXQ implant gun (China), a TRH-J implant positioning navigation device, and a GE 64-row spiral CT.

3 Planning before BTPS surgery

Parameters (planned target dose, PTD), particle activity, and CT data) were inputted into the BTPS to simulate needle insertion and develop a pre-operative plan, from which additional parameters were derived. The pre-operative plan was completed jointly by the operator and the physicist after a thorough discussion, and the patient imaging position was adjusted to the actual operating position to ensure that the intra-operative needle insertion was consistent with the pre-operative plan. The PTD was controlled to be 110-180 Gy, and the clinical target dose (CTD) was controlled at 80-100 Gy.

4 ¹²⁵I seed implantation technology method

The position of the patients was determined according to the position of the tumor. A CT scan was used for localization. Local and intravenous anesthesia was administered. The positioning navigation device was installed according to the surface marking laser positioning line, the template was installed and adjusted, the position and angle of the needle insertion was controlled, and the needle channel was established according to pre-operative pre-plan. Beginning in the center plane of the tumor, the needles were arranged in layers with a lateral margin of 1 cm and a depth of 0.5 cm from the distal edge. A CT scan was performed to determine the exact position and the implantation was completed layer-by-layer with the implant gun. The particles were > 1 cm away from the skin to avoid damage to the skin. If necessary, an intra-operative planning correction and target dose optimization were performed.

5 Post-operative dose verification

Additional parameters were inputted to the BTPS for particle reconstruction and post-operative dose verification. The relevant dosimetric parameters of the clinical target volume (CTV) and the planned target volume (PTV) 1 cm outside the CTV before and after surgery were calculated, including the dose of 90% of the target volume (D₉₀), 90% of the prescribed dose (CTD and PTD) covered target volume (V₉₀), 100% (CTD and PTD) of the covered target volume (V₁₀₀), 150% (CTD and PTD) of the covered target volume (V₁₅₀), the conformal index (CI), and the external index of the target index (EI). Based on the American Association of Brachytherapy Association standards, the D₉₀ should reach or exceed the PTD (V₁₀₀ ≥ 90%), otherwise the D₉₀ was not satisfied. The dose parameters before and after particle implantation surgery are shown in Tables 1 and 2.

6 Post-operative treatment and observation

The post-operative physical score (KPS) and adverse reactions were recorded. The tumor response was followed for 6 months according to the solid tumor efficacy evaluation standard (version 1.1), including complete remission (CR), partial remission (PR), progressive disease (PD), stable disease (SD), effective rate (CR+PR), and local control rate (CR+PR+PD). The survival time and the survival rate at 6, 12, and 24 months were noted and summarized, and the follow-up evaluations concluded in March 2019 or at the time of patient death.

Statistical analysis

Statistical analysis was performed using SPSS 20.0 software. Measurement data are expressed as the mean ± standard deviation ( ). A t-test was used for comparison of normal distribution data between groups. The rank-sum test was used for comparison of non-normal distribution data between groups. A r test was used for comparison of count data between groups. A P<0.05 was considered significant. A t-test was used for comparison between groups, the Kaplan-Meier method was applied to determine the survival rate, the log-rank test was used for single factor analysis, and the Cox model was used for multivariate analysis of the survival rate.

1 Comparison of pre- and post-operative dosimetric parameters

Under the guidance of a 3D template-assisted CT, seed implantation was successfully completed in all patients and the implantation process was uncomplicated. The average number of puncture needles implanted was 17 (19.12±13.00) and the median number of particles implanted was 52 (55.12±32.97). The D₉₀ of the post-operative CTV was 93.24±15.70 Gy, which was slightly lower than the D₉₀(93.92±17.60 Gy) of the pre-operative CTV, but there was no statistical difference between the two groups (P>0.05). The D₉₀ of the post-operative PTV was 142.16±22.25 Gy, which was lower than the D₉₀ (145.32±23.48 Gy) of the pre-operative PTV, and there was no significant difference between the two groups (P>0.05). The pre- and post-operative CTV dose parameter, EI, was close to zero. There were no significant differences in other related dosimetric parameters (P>0.05, Tables 1 and 2), and the post-operative verification results were considered satisfactory. Figure 1 shows the surgical procedure for ¹²⁵I seed implantation in patients with lung cancer and the follow-up imaging.

2 Tumor responses after seed implantation

A CT or MRI was conducted 1, 2, 4, and 6 months after surgery for dynamic imaging observations. Tumor response was evaluated 6 months after surgery in combination with radioactive ¹²⁵I seed attenuation characteristics. The tumor responses 6 months post-operatively were as follows, as shown in Table 3: CR, 20% (5/25); PR, 48% (12/25); SD, 24% (6/25); PD, 8% (2/25); effective rate (CR+PR), 68% (17/25); and local control rate, 92% (23/25) .

3 Statistics on survival time of patients

No patients in either group were lost to follow-up. All patients were followed according to the plan and the follow-up evaluation data concluded in March 2019. The 6-, 12-, and 24-month survival rates were 100% (25/25), 88% (22/25), and 52% (13/25), respectively (Table 4). The median survival time for the entire group of patients was 24 months (Figure 2).

4 Physical strength score (KPS) and adverse reactions

The physical strength score (KPS) of the entire group gradually recovered and increased, and reached the highest value 12 months after seed implantation, then decreased slightly; however, the mean KPS score was still > 90 points (Figure 3). There was a statistical difference between the two groups (F=6.428, P=0.003 <0.05). One patient with CR had an intra-operative pneumothorax that was treated with closed pleural drainage. Two patients with superficial malignant tumors patients and skin ulcerations were treated symptomatically; the scars were healed by 6 months post-operatively. There were no uncontrollable major hemorrhages in the entire group and no serious complications, such as puncture and implant metastases post-operatively.

5 Prognostic multivariate analysis

The log-rank test was used for univariate analysis and the Cox model was used for multivariate analysis. Univariate and multivariate analyses included age, gender, template type, number of puncture needles, number of particles, and tumor location and type for the 25 patients. The location and type of tumor were independent risk factors for median overall survival (mOS); however, the number of puncture needles and particles were not factors that affected the prognosis of patients (Table 5).

The incidence of malignant tumors has increased year-after-year worldwide [5, 6]. In 2008, US President Barack Obama introduced the concept of precision medicine. In the following 10 years, the concept of precision medicine has been shown to have enormous value and given oncologists more hope and choices. Nevertheless, there are a large number of immunosuppressive substances or factors in the tumor microenvironment that impair the immune system from functioning normally. At present, the precise radical treatment of malignant tumors at the genetic level cannot be achieved. As the product of a number of minimally invasive disciplines, radioactive ¹²⁵I particle implantation technology is a relatively accurate treatment in clinical practice. Radioactive ¹²⁵I particle implantation technology has developed rapidly in recent years, the application range of which covers nearly all types of malignant solid tumors, including common brain metastases, lung cancer, pancreatic cancer, liver cancer, bone metastases, and various metastatic lymph node and soft tissue tumors [1-4, 7-12]. Due to the need to adjust the needle during surgery, the larger the tumor, the greater the number of implants needed. Indeed, there are no domestic reports which have determined if puncture needles promote the release and escape of tumor cells, thus leading to complications, such as puncture tract transfer and distant organ metastases.

In the current study 25 patients with advanced refractory malignant tumors underwent continuous seed implantation and no serious complications occurred in the entire group, such as implant and distant organ metastases. Thus, although the number of implanted needles was increased, the application of 3D printing technology rendered template-assisted seed implantation accurate, shortened the operative time, and decreased the number of intra-operative needle adjustments; as a result, the complications caused by repeated punctures were decreased. The study further illustrated the feasibility and safety of radioactive ¹²⁵I seed implantation with a 3D template guidance for the treatment of malignant tumors.

Because the pre-operative use of the BTPS to develop a rational treatment plan and implementation of the treatment plan intra-operatively, CT-guided 3D template-assisted ¹²⁵I seed implantation for the treatment of malignant tumors is more accurate [4, 13-15] and extends the survival time and quality of life in patients with advanced malignancies. Mo et al. [11] applied CT-guided seed implantation combined with chemotherapy to treat metastatic soft tissue tumors after 4-6 cycles of first-line chemotherapy. The results showed that the 1- and 2-year survival rates were 46.7% and 28.9%, respectively, while the 1- and 2-year survival rates of the control group with second-line chemotherapy were 6.3% and 0%, respectively [11]. Although the overall survival time was 16.9±5.01 and 12.1±4.8 months, respectively, and there was no statistical difference between the groups, the experimental group had a significantly improved symptom remission rate and quality of life [11].

Wang et al. [12] utilized ¹²⁵I seed implantation in the treatment of pelvic metastases and showed that the 1- and 2-year survival rates were 81.8% and 45.5%, respectively. The Wang et al. [12] results were consistent with the results reported herein. All 25 patients in this study had refractory advanced malignant tumors that progressed after radiotherapy or chemotherapy or were unable to undergo radiotherapy and chemotherapy. The 1- and 2-year survival rates were 88% and 52%, respectively, and the median survival time was 24 months, which were higher than the results reported by other similar studies. The local control rate of the tumor was 92% 6 months after surgery. This result is difficult to achieve in patients with advanced refractory malignant tumors; the result was demonstrated vis-à-vis a gradual increase in the physical strength score (KPS). No patients were administered systemic chemotherapy or other treatments from seed implantation to the completion of follow-up. The analysis of prognostic factors in this study also suggested that the tumor site and type are influential factors for CT-guided 3D template-assisted ¹²⁵I particle implantation technology, and other factors, such as template type, are not factors that affect prognosis [13].

With the development and clinical application of gene sequencing technology, the treatment of malignant tumors is more comprehensive and precise, which further improves the clinical benefit for malignant tumors [16, 17]; however, the multidisciplinary treatment model is still preferred for the treatment of malignant tumors. A single method often has less of an effect in the treatment of tumors. Patients with refractory advanced malignancies, including patients with progression after chemoradiotherapy and patients who are not suitable for chemoradiotherapy and end-stage chemotherapy patients, have a very poor prognosis. The expected survival time of such patients is approximately 3 months [18, 19]. Radioactive ¹²⁵I seed implantation is a more accurate radiotherapy technique for the treatment of malignant tumors. Radioactive ¹²⁵I seed implantation is guided by imaging to implant radioactive ¹²⁵I seed into the tumor through a puncture needle, so that the particles disseminate radioactivity inside the tumor. This method has a long-lasting effect and the side effects of this method are significantly lower than other radiotherapy methods. With the clinical development and application of 3D printing technology, CT-guided 3D template-assisted ¹²⁵I seed implantation technology further improves the efficacy of radiation in tumor target areas, while sparing surrounding vulnerable tissues and organs. Needle puncture and arrangement rely entirely on surgeon experience. Due to an inability to effectively control quality, it is relatively easy to have a localized cold dose of the tumor, which inevitably leads to tumor progression.

The results of this study showed that the D₉₀ of the PTV and CTV target areas were not statistically different from the corresponding values pre-operatively, which further indicated that the method can improve the actual dose distribution. At the same time, the V₁₀₀ and V₁₅₀ parameters were not statistically different from the pre-operative plan. Considering that seed implantation is under template control, bleeding and motion artifact are decreased, thus the target dose is precisely controlled on the basis of better control of the tumor target volume, which is consistent with recent reports in the literature [13, 14].

The data also suggest that 3D printed coplanar and non-coplanar templates, and the number of needles and particles do not influence prognosis, further suggesting the safety of this treatment for advanced malignant tumors. Therefore, as a precise comprehensive treatment, a 3D template combined with CT-guided radioactive ¹²⁵I seed implantation can be repeated for the treatment of recurrent tumors [20]. Moreover, we also observed that the EI value of the CTV target correlation index was close to 0, suggesting that optimizing the clinical target area may be more valuable in reducing peripheral tissue damage and increasing the actual intratumor particle dose distribution. This finding may also be the main reason for the good efficacy demonstrated in the current study. The importance of this observation and dose study of the CTV target area has not been previously reported.

CT-guided ¹²⁵I seed implantation in the treatment of malignant tumors is included in the treatment protocols in China, which makes this treatment more standardized [21]. In the current study, the long-term efficacy and safety of a CT-guided 3D template-assisted ¹²⁵I seed implantation in the treatment of malignant tumors for refractory malignancies was confirmed, and a 2-year clinical follow-up observation, combined with post-operative verification of relevant dosimetric parameters, further confirmed the clinical efficacy and safety of the technique as a rational form of treatment. Changes in the number of circulating tumor cells in peripheral blood tumors post-operatively was not determined in the current study [22]. Whether this method can promote tumor micrometastasis is still uncertain, and the number of samples in this study was small, which was also a shortcoming of this study.

In conclusion, this preliminary study showed the safety and efficacy of CT-guided 3D template-assisted ¹²⁵I seed implantation in the treatment of malignant tumors, the rationality of radiologic dose division, and the delivery of a safe and effective treatment to patients with refractory advanced malignant tumors, which is worthy of further clinical application

CTV: clinical target volume; PTV: planning target volume; CR: complete remission; PR: partial remission; SD: stable disease; PD: progressive disease; KPS: Karnofsky performance score; PTD: planned target dose; CTD: clinical target dose; CI: conformal index; EI: target index; mOS: median overall survival.

Ethics approval and consent to participate

The study was approved by the Ethics Committee of Affiliated Zhongshan Hospital of Dalian University.

Consent for publication

All the patients participate in the study have signed the informed consent.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Competing interests

The authors declare that they have no competing interests.

Funding

None.

Authors' contributions

GSZ: responsible for clinical trial research and paper writing; SL and LY: responsible for patient follow-up and data statistics; CL and YWW: responsible for experiment management; YWZ and JZ: responsible for project design and experimental implementation. All authors read and approved the final manuscript.

Acknowledgements

Not Applicable.

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Table 1 Comparison of dosimetric parameters of clinical target volume (CTV) before and after seed implantation of 25 patients with refractory malignant tumor

Parameters	Before surgery			After surgery			P
Parameters	Interval	Median	Mean value	Interval	Median	Mean value	P
D90	50-112	93	93.92±17.60	54-116	106	93.24±15.70	0.28
V100	42-90.8	74.3	71.68±13.34	43.7-91	70.1	72.05±11.70	0.26
V150	21.7-61.2	44.8	42.88±11.40	23.9-62	43.1	43.09±11.05	0.44
CI	0.4-0.82	0.63	0.63±0.10	0.43-0.79	0.63	0.62±0.08	0.14
EI	0.01-0.25	0.05	0.08±0.07	0.01-0.31	0.07	0.08±0.07	0.46
HI	0.3-0.64	0.4	0.42±0.09	0.26-0.61	0.4	0.39±0.08	0.41

Table 2 Comparison of dosimetric parameters of panned target volume (CTV) before and after seed implantation of 25 patients with refractory malignant tumor

Parameters	Before surgery			After surgery			P
Parameters	Interval	Median	Interval	Median	Interval	Median	P
D90	114-181	148	145.32±23.48	105-180	128	142.16±22.25	0.39
V100	76.6-100	96.3	94.63±5.76	73.7-100	95	93.47±6.29	0.33
V150	46.2-90.4	64.5	67.35±14.07	46.7-89.6	66.1	66.72±12.11	0.23
CI	0.4-0.8	0.66	0.63±0.11	0.42-0.82	0.61	0.63±0.11	0.42
EI	0.18-1.1	0.42	0.46±0.27	0.21-1.3	0.46	0.50±0.29	0.38
HI	0.09-0.61	0.31	0.31±0.13	0.1-0.59	0.34	0.31-0.12	0.40

Table 3 Evaluation of tumor response in patients at 6 months after seed implantation

CR		PR		SD		PD		Objective remission		Disease control
n	%	n	%	n	%	n	%	n	%	n	%
5	20	12	48	6	24	2	8	17	68	23	92

CR: Complete remission; PR: partial remission; SD: stable disease; PD: progressive disease.

Table 4 The survival time and survival rate of patients after seed implantation

6-month survival rate		12-month survival rate		24-month survival rate		Median survival time
n	%	n	%	n	%	24.00
25	100	22	88	13	52	24.00

Table 5 Multivariate analysis on the factors that affect the treatment prognosis

Factors	n	Univariate			Multivariate
Factors	n	HR	95%CL	P	HR	95%CL	P
Age
<60 years old	9	1			1
≥60 years old	16	0.985	0.546-1.809	0.961	0.853	0.460-1.581	0.621
Gender
Male	17	1			1
Female	8	0.746	0.390-1.425	0.375	0.934	0.457-1.740	0.813
Template type
Coplanar	22
Non-coplanar	3	0.823	0.460-1.581	0.623	0.924	0.461-1.811	0.816
Number of puncture needle
<10	6	1			1
≥10<20	9	1.614	0.849-3.068	0.144	1.784	0.673-4.729	0.244
≥20	10	1.001	0.484-2.070	0.998	0.669	0.256-1.746	0.411
Number of seed implantation
<30	7	1			1
≥30<60	9	1.241	0.765-2.012	0.381	1.024	0.719-1.459	0.896
≥60	9	1.567	1.095-2.240	0.067	0.633	0.357-0.892	0.402
Tumor location
Thoracic tumor	7	1			1
Bone and soft tissue tumor	7	0.423	0.219-0.816	0.012	0.147	0.042-0.527	0.003
Abdominal tumor	4	0.167	0.051-0.634	0.008	4.995	2.557-9.582	0.003
Genitourinary tumor	4	0.342	0.192-1.357	0.019	0.297	0.119-0.731	0.007
Lymph node metastasis tumor	2	0.641	0.049-0.829	0.012	0.627	0.047-0.359	0.009
Head and neck cancer	1	0.378	0.161-0.653	0.026	0.254	0.103-0.545	0.001

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Evaluation of radioactive 125I seed implantation for the treatment of refractory malignant tumors based on CT-guided 3D template assisted technique: efficacy and safety

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