Sage Journals: Discover world-class research

Abstract

Purpose

This study aimed to evaluate the efficacy of computed tomography (CT) guided percutaneous cryoablation (CA) for the management of lung metastases in patients with metastatic colorectal cancer (mCRC).

Methods

Retrospective analysis was performed on 38 mCRC patients with lung metastases, who underwent CT-guided percutaneous CA at our center from May 1, 2020 to November 1, 2021. The technical success rate, 1-year local control (LC) rate, recurrence-free survival (RFS) and treatment-related complications were analyzed.

Results

The CA procedure was successfully performed in all patients, with a technical success rate of 100%. The 1-year LC rate was 94.7% (36/38), while 16 patients experienced new distant lung metastases during the follow-up period. The median RFS was 20 months (95% CI: 13.0-27.0). The median RFS of patients with and without extrapulmonary metastasis was 15 and 23 months, respectively. Complications were reported in 18 (47.4%) patients following the CA procedure. Pneumothorax was discovered in 15 (39.5%) patients, and five of these patients (13.2%) required chest tube intubation. Two patients (5.3%) presented with hemoptysis during the CA procedure. One patient developed subcutaneous emphysema as detected in the post-procedure follow-up imaging. All patients tolerated the peri-procedural pain well under local anesthesia, and the mean visual analog scale (VAS) score was 2.8.

Conclusion

Lung CA is a safe and well-tolerated treatment with a satisfactory local control rate for patients with lung metastases derived from mCRC.

Keywords

cryoablation lung cancer colorectal cancer outcomes safety

Introduction

Colorectal cancer (CRC) is one of the most frequently occurring malignant tumors, and is responsible for a growing number of cancer-associated deaths in China and worldwide.^1,2 Over 50% of CRC patients eventually develop metastases, and the recurrence rate of radically resected CRC is reported to be 30%.³ The lung is the second most frequent site of CRC metastasis, after the liver, and the site of metastasis directly affects the prognosis and overall survival (OS) of patients.^4–6 Currently, surgical resection remains the standard treatment for lung metastases. However, many patients are not suitable for surgery because of their advanced disease or refusal of treatment.⁷ Recent studies have shown that local therapies can effectively treat lung metastases with minimal invasiveness and high repeatability, especially for lung oligometastases.^8–11 Local ablation treatments such as radiofrequency ablation (RFA), microwave ablation (WMA), and cryoablation (CA) can be used for the treatment of primary and secondary lung tumors.^12,13 CA involves low temperature, which allows for the preservation of collagenous architectures, has a higher safety profile adjacent to critical structures, involves less intraprocedural pain, and elicits a systemic immune response.¹⁴ Previous high-quality studies have demonstrated encouraging results regarding the use of CA for lung tumors.^15,16

Compared to RFA and MWA, data concerning the efficacy of CA for the treatment of lung metastases are limited.^17,18 Therefore, this retrospective case series aimed to assess the safety and efficacy of CA for the treatment of lung metastases derived from metastatic CRC (mCRC), and evaluate the value of CA for the longitudinal management of mCRC patients.

Methods

Study Design

This retrospective study was approved by the institutional review board of Changhai Hospital (approval number: CHE02022-043), and the requirement for written informed consent was waived. The detailed patient data and personally identifiable information were de-identified. From May 1, 2020 to November 1, 2021, 63 patients with lung tumors were selected for percutaneous CA at the Department of Interventional Radiology of our hospital. The observational period was defined as the interval from initial treatment to death, or to the date of the last follow-up prior to the end of the study (November 1, 2022).

Patient Selection

The patient inclusion criteria consisted of: age ≥18 years; primary tumor was CRC, which was radically resected; pulmonary metastasis confirmed by imaging as new or growing nodules with histologically proven primary tumor; at most three unilateral metastases or ﬁve bilateral lesions, with the largest tumor < 35 mm in diameter; no local therapy received prior to the currently targeted pulmonary metastases; Eastern Cooperative Oncology Group (ECOG) performance score of 0–2; and a life expectancy > 3 months. Patients with extrapulmonary metastasis were included based on the inclusion criteria. Stable extrapulmonary metastasis was defined as the absence of recurrence after previous therapies at the time of lung CA. Based on previous relevant high-quality studies, the maximum lesion diameter of 35 mm was selected.^15,16 When a patient had metastases in both lungs, the treatment was conducted sequentially on different days. The patient exclusion criteria were: platelet count < 50,000/mm3; international normalized ratio (INR) > 1.5; uncontrolled systemic infection; uncontrollable primary or metastatic disease outside the lung; pulmonary ventilation disorder; and patients not suitable for CA, including refusal of the procedure.

Finally, data from a total of 38 patients with 50 lesions were used in the present study. The features of patients undergoing computed tomography (CT) percutaneous CA for lung metastases of CRC are summarized in Table 1. The characteristics of all lesions included in the study are shown in Table 2.

Table 1

Demographic and Clinical Characteristics of Included Patients.

Age (year), mean (range)	61.4, (47–77)
Gender, n
Male	22
Female	16
ECOG, n
Grade 1	11
Grade 2	27
Region of CCR, n
Ascending	5
Sigmoid	11
Recto sigmoid	3
Rectum	19
KRAS (mutation/wild), n	30/8
BRAF (mutation/wild), n	2/36
Extrapulmonary metastasis, n
None	13
Liver	24
Others	1
Other treatment for pulmonary metastasis before CA, n
None	15
Surgery	3
Chemotherapy	10
Chemotherapy + targeted therapy	7
Other local ablation	3

Abbreviations: ECOG, Eastern Cooperative Oncology Group; CCR, colorectal cancer; CA, cryoablation.

Table 2

Characteristics of Included Lesions.

Tumor Diameter, mean ± SD mm	12.7 ± 5.5
<10 mm, n	14
10mm-20 mm, n	31
>20 mm, n	5
Tumor Location, n
Adjacent to pleural	28
Adjacent to interlobar fissure	13
Normal intraparenchymal	9
Number of treated lesions, n
1	28
2	8
3	2

CA Procedure

All CA procedures were performed by an experienced interventional radiologist with approximately 20 years of experience in oncologic interventional radiology. The cryoablation system (AT-2008-II, AccuTarget MediPharma, China) was in a dedicated CT room equipped with a CT scanner (Philips Brillance iCT 256 slice CT). Fifteen minutes prior to the CA procedure, each patient was given an intravenous injection of Haemocoagulase Agkistrodon (2 units). Next, a suitable position for the operation was determined based on the location, size, and shape of the tumor. The prone position was preferred over the supine position since it limited movement and allowed for easier recovery. Local anesthesia (lidocaine) was administered to the skin and along the needle track and parietal pleura. Then, under CT guidance, a 1.5 mm-diameter cryoprobe was inserted into the target lesions. Since lesion firmness could prevent direct penetration, small lesions were bracketed rather than penetrated with several cryoprobes. For tumors < 20 mm in diameter, usually only one cryoprobe was inserted, while for those > 20 mm in diameter, two or more cryoprobes were needed to create an ice-ball large enough to cover the entire tumor with a safety ablation boundary > 5 mm. The CA protocol was initiated when the cryoprobe was satisfactorily placed. The probe temperature rapidly dropped to −165 °C within 1 min, and the freezing period lasted for 5–10 min. Next, the target area was warmed by increasing the temperature to > 50 °C, which was maintained for 5 min. Each CA procedure included three freeze-thaw cycles. Once the CA procedure was completed, another chest CT scan was conducted to confirm the presence of severe complication. All patients were observed in the interventional radiology ward for at least one day following the procedure.

Outcome and Safety Measure

Within 24 h after treatment, a chest x-ray was performed to identify the presence of delayed complications. Complications were graded based on the National Cancer Institute Common Terminology Criteria for Adverse Events (version 4.03). All patients were followed up at 1 month and every 3 months thereafter by chest CT. Technical success was defined as a completely successful CA procedure, with intraoperative CT images showing complete tumor coverage by the ablation range with a margin > 5 mm. The local control (LC) was defined as no recurrence in-field or marginal at the site following CA. Recurrence included in situ at the CA site or new distant metastases in the lung. Recurrence-free survival (RFS) was defined as the time between the CA procedure and recurrence in the lung during the follow-up period. Extrapulmonary recurrence without evidence of recurrence in the lung was subjected to treatment with other therapies and continually monitored until documented local progression or death. The visual analog scale (VAS) score was used to measure the degree of intraoperative pain.

Statistical Analysis

SPSS software (version 23.0; Chicago, IL, USA) was used for all statistical analyses. The technical success rate was expressed as a percentage. LC and RFS were calculated from the date of CA and were estimated using the Kaplan-Meier method.

Results

The CA procedure was successful in all patients, with a technical success rate of 100%. The median follow-up period was 18 months (range, 13-31 months). During the follow-up period, a total of 4 patients developed local progression, and the 1-year LC rate was 94.7% (36/38). Sixteen patients experienced new distant lung metastases. The median RFS was 20 months (95% CI 13.0-27.0) (Figure 1). Additionally, 25 patients (65.8%) had extrapulmonary metastases at the time of CA treatment. The median RFS of patients with and without extrapulmonary metastases was 15 and 23 months, respectively (Figure 2). Due to disease progression, four patients died after CA treatment during the follow-up period.

Figure 1.

Recurrence-free survival of total patients in study.

Figure 2.

Recurrence-free survival of patients with and without extrapulmonary metastasis in study.

Complications were reported in 18 (47.4%) patients after the CA procedure, as summarized in Table 3. Pneumothorax was the most common complication, which occurred in 15 (39.5%) patients, mostly immediately after the CA procedure. Five of these patients required chest tube intubation. During the CA procedure, two patients presented with a paroxysmal cough and minor hemoptysis (approximately 50 ml). One other had subcutaneous emphysema during the post-procedure follow-up imaging. No other serious procedure-related complications were observed. All patients tolerated the peri-procedural pain well under local anesthesia, and the mean VAS score was 2.8.

Table 3

Complications Related to CA Procedure.

Complication	Number of patients (occurrence rate)
None	20 (52.6%)
Pneumothorax	15 (39.4%)
Requiring chest tube	5 (13.2%)
Not-required chest tube	10 (26.3%)
Pleural effusion	0
Hemoptysis	2 (5.3%)
Subcutaneous emphysema	1 (2.6%)
VAS scores, mean ± SD	2.8 ± 1.3
<3	16 (42.1%)
3–6	20 (52.6%)
>6	2 (5.3%)

VAS, visual analog scale.

Discussion

Ablative therapies are used to treat lung metastases from various types of primary tumors.¹⁹ The consideration of local therapy without continued systemic therapy becomes relevant to achieve long-term disease control and contribute to overall survival (OS) at well-controlled sites of metastases. Due to the relatively short follow-up period, the 1-year LC rate and RFS were the focus of the current study, and recurrence included local progression at the site of CA as well as new distant lung metastases. In the present study, a total of four patients experienced local progression, the 1-year LC rate was 94.7% (36/38), and a total of 20 (52.6%) patients in this group developed recurrence in the lung during the follow-up period. The median RFS was 20 months (95% CI 13.0-27.0). It is important to note that the median RFS in the current study was worse than similar studies of pulmonary metastasectomy in mCRC patients.^20,21 In this study, 65.8% of patients had extrapulmonary metastases, primarily in the liver, which could have contributed to the less favorable outcome. RFA and MWA are the most common and well-studied local ablation treatments for primary and metastatic lung tumors, and the local control rates have been reported to be approximately 80–90% for the treatment of lung metastases from CRC.^22–25 A prospective, multicenter study of image-guided percutaneous CA for the treatment of lung metastases (ECLIPSE) reported a 94.6% LC rate at 1 year, 87.9% at 3 years and 79.2% at 5 years.^15,26 Another multicenter study of metastatic lung tumors targeted by interventional CA evaluation (SOLSTICE) demonstrated that the treatment efficacy was 85.1% at 12 months and 77.2% at 24 months after the initial treatment.¹⁶ In these two high-quality CA studies of lung metastases from primary tumors, CRC was the main primary tumor that developed metastatic lesions. In this present study, a total of 20 (52.6%) patients developed recurrence of lung cancer during the follow-up period. Four patients (10.5%) had local progression at the CA site, and the 1-year LC rate was 94.7%. Stereotactic body radiation therapy (SBRT) is another common effective local therapy for lung metastases. In comparison, when SBRT was used for the treatment of 50 patients with 125 metastatic pulmonary tumors, the local efficacy was 83% at 18.7 months.²⁷ Sharma et al reported that with SBRT treatment of 327 metastases in 206 patients, the local efficacy was 85% at 2 years.²⁸ The results presented here are encouraging in terms of short-term LC rates. In the absence of recurrence, most patients do not require systemic therapy, which contributes to an improved quality of life. The presence of extrapulmonary metastases was also a significant prognostic factor in several studies and was related to poor OS.^29–32 Importantly, pre-ablation tumor size and location are the most important factors to predict therapeutic efficacy. Yukiharu et al suggested that a tumor > 15 mm was an independent prognostic factor, which might become a comparatively strict criterion to select candidate patients for lung RFA.²⁹ Although CA is more suitable for larger lesions, tumor size is still related to an increased risk of local progression. However, there remains controversy regarding the cut-off (> 20 mm or > 30 mm) that should be used as a predictor of poor prognosis for lung CA.^33,34 In addition, the Kirsten rat sarcoma virus (KRAS) mutation is associated with a shorter time-to-lung metastasis, which also increases the risk of lung metastases by two fold during the disease course in patients with liver-restricted mCRC at diagnosis.³⁵ As such, this will impact decisions regarding treatment strategies. Unfortunately, it was impossible to analyze the influence of KRAS mutations on prognosis in the current study due to limitations of the data.

All patients well tolerated and successfully completed the CA procedure. There were no procedure-related deaths or severe complications in the current study. The most common complication of lung CA was pneumothorax. A total of 15 (39.4%) patients developed pneumothorax following the procedure, and five of these patients required chest tube intubation. The incidence of pneumothorax in this study was within previously reported ranges and equivalent to that reported in RFA studies.^36–38 Hemoptysis occurred in two patients (5.3%) during the CA procedure, which was a lower incidence compared to other similar studies. Notably, careful selection of the puncture path and use of a coagulation agent pre-procedure may be responsible for the low incidence of hemoptysis. Subcutaneous emphysema is a rare complication, but it was observed in one patient at the 1-month follow-up CT. However, it had resolved at the next follow-up CT without any medical care. Compared to other thermal ablation treatments, a distinct advantage of CA is the reduced intraprocedural pain. All patients in the current study could tolerate the peri-procedural pain under local anesthesia with lidocaine, and the mean VAS score was 2.8. CA could be accurately implemented, even when the tumors targeted for ablation are within the chest wall, located in the subpleural and juxta-pleural lung. Other thermal ablation methods including RFA and MWA are regarded as high-risk and prone to recurrence when used to treat lung tumors adjacent to high-risk sites, such as the subpleural lung, pericardium, or interlobar fissure due to an insufficiently safe ablation range. This can result in recurrence and severe pleural injury that may lead to the formation of bronchopleural fistulas.^39–41 In the current study, 82% (41/50) of lesions were at high-risk sites (Table 3), but all CA procedures were successfully completed without severe post-procedure complications.

The aim and treatment strategies for mCRC depend on numerous factors, including tumor- and disease-related characteristics, patient condition, and treatment-related side effects. Therefore, a multi-model treatment approach and multidisciplinary team care are particularly essential to improve patient prognosis. A growing number of studies have supported the use of local therapy for patients with oligometastatic disease in the lung. Percutaneous ablation can preserve the lung parenchyma for patients who have compromised respiratory function or may need repeat treatment over the course of disease management. There is a general suggestion that four or fewer lesions per lung can be managed safely and effectively with percutaneous ablation.⁴² Due to many advantages, CA is regarded as safer than RFA or MWA for both central and subpleural lesions of primary and metastatic lung tumors.^43,44 In the case of oligorecurrent disease, good tolerance of CA may provide the possibility of multiple sessions of treatment and delay resumption of systemic treatment.

However, certain limitations should be noted in the present study. Firstly, this was a retrospective case series without a control group. Although the short-term LC rate was satisfactory, additional large-scale and high-level clinical trials are required to confirm the long-term effect and OS of patients. Secondly, a portion of patients with extrapulmonary metastasis received other treatments after the CA procedure, which might have complicated the evaluation. In addition, since this was a retrospective study, the choice of CA was mainly related to the preference and experience of the doctor, or patients’ choice, which might have introduced bias that could not be accounted for.

Conclusion

These results suggest that lung CA is a safe and effective treatment for patients with mCRC. The procedure is simple and well-tolerated, and is a viable alternative for the management of mCRC patients.

Footnotes

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical Statement

This retrospective study was approved by Shanghai Changhai Hospital Ethics Committee, and the number of approval letter is CHEC2022-043.

ORCID iD

Fu-ming Wang

References

Islami

Ward

Sung

, et al. Annual report to the nation on the status of cancer, part 1: National cancer statistics. J Natl Cancer Inst. 2021;113(12):1648‐1669.

Xia

Dong

, et al. Cancer statistics in China and United States, 2022: Profiles, trends, and determinants. Chin Med J (Engl). 2022;135(5):584‐590.

Osterman

Glimelius

. Recurrence risk after up-to-date colon cancer staging, surgery, and pathology: Analysis of the entire Swedish population. Dis Colon Rectum. 2018;61(9):1016‐1025.

Watanabe

Saito

Sugito

, et al. Incidence and predictive factors for pulmonary metastases after curative resection of colon cancer. Ann Surg Oncol. 2013;20(4):1374‐1380.

Kim

Cho

Lee

, et al.

Pulmonary metastasectomy for colorectal cancer: How many nodules, how many times?

World J Gastroenterol. 2014;20(20):6133‐6145.

Desch

Benson

Somerfield

, et al. Colorectal cancer surveillance: 2005 update of an American Society of Clinical Oncology practice guideline. J Clin Oncol. 2005;23(33):8512‐8519.

Pastorino

Buyse

Friedel

, et al. Long-term results of lung metastasectomy: Prognostic analyses based on 5206 cases. J Thorac Cardiovasc Surg. 1997;113(1):37‐49.

Nguyenhuy

Maingard

, et al. A systematic review and meta-analysis of patient survival and disease recurrence following percutaneous ablation of pulmonary metastasis. Cardiovasc Intervent Radiol. 2022;45(8):1102‐1113.

Tselikas

Garzelli

Mercier

, et al. Radiofrequency ablation versus surgical resection for the treatment of oligometastatic lung disease. Diagn Interv Imaging. 2021;102(1):19‐26.

10.

Omae

Hiraki

Gobara

, et al. Long-term survival after radiofrequency ablation of lung oligometastases from five types of primary lesions: A retrospective evaluation. J Vasc Interv Radiol. 2016;27(9):1362‐1370.

11.

Venturini

Cariati

Marra

, et al. CIRSE standards of practice on thermal ablation of primary and secondary lung tumours. Cardiovasc Intervent Radiol. 2020;43(5):667‐683.

12.

Vogl

Eckert

Naguib

Beeres

Gruber-Rouh

Nour-Eldin

. Thermal ablation of colorectal lung metastases: Retrospective comparison among laser-induced thermotherapy, radiofrequency ablation, and microwave ablation. AJR Am J Roentgenol. 2016;207(6):1340‐1349.

13.

Nezami

Khorshidi

Mansur

Habibollahi

Camacho

. Primary and metastatic lung cancer: Rationale, indications, and outcomes of thermal ablation. Clin Lung Cancer. 2023;24(5):389-400.

14.

Palussière

Catena

Buy

. Percutaneous thermal ablation of lung tumors - radiofrequency, microwave and cryotherapy: Where are we going? Diagn Interv Imaging. 2017;98(9):619‐625.

15.

de Baère

Woodrum

Tselikas

, et al. The ECLIPSE study: Efficacy of cryoablation on metastatic lung tumors with a 5-year follow-up. J Thorac Oncol. 2021;16(11):1840‐1849.

16.

Callstrom

Woodrum

Nichols

, et al. Multicenter study of metastatic lung tumors targeted by interventional cryoablation evaluation (SOLSTICE). J Thorac Oncol. 2020;15(7):1200‐1209.

17.

Delpla

de Baere

Varin

Deschamps

Roux

Tselikas

. Role of thermal ablation in colorectal cancer lung metastases. Cancers (Basel). 2021;13(4):908.

18.

Ridge

Solomon

. Percutaneous ablation of colorectal lung metastases. J Gastrointest Oncol. 2015;6(6):685‐692.

19.

Matsui

Tomita

Uka

, et al. Up-to-date evidence on image-guided thermal ablation for metastatic lung tumors: A review. Jpn J Radiol. 2022;40(10):1024‐1034.

20.

Okumura

Boku

Hishida

, et al. Surgical outcome and prognostic stratification for pulmonary metastasis from colorectal cancer. Ann Thorac Surg. 2017;104(3):979‐987.

21.

Yıldız

Dae

Fındıkcıoglu

, et al. Survival outcome of pulmonary metastasectomy among the patients with colorectal cancers. Rev Assoc Med Bras (1992). 2021;67(7):1015‐1020.

22.

Fonck

Perez

Catena

, et al. Pulmonary thermal ablation enables long chemotherapy-free survival in metastatic colorectal cancer patients. Cardiovasc Intervent Radiol. 2018;41(11):1727‐1734.

23.

Kurilova

Gonzalez-Aguirre

Beets-Tan

, et al. Microwave ablation in the management of colorectal cancer pulmonary metastases. Cardiovasc Intervent Radiol. 2018;41(10):1530‐1544.

24.

Zhong

Palkhi

, et al. Long-term outcomes in percutaneous radiofrequency ablation for histologically proven colorectal lung metastasis. Cardiovasc Intervent Radiol. 2020;43(12):1900‐1907.

25.

Hasegawa

Takaki

Kodama

, et al. Three-year survival rate after radiofrequency ablation for surgically resectable colorectal lung metastases: A prospective multicenter study. Radiology. 2020;294(3):686‐695.

26.

de Baere

Tselikas

Woodrum

, et al. Evaluating cryoablation of metastatic lung tumors in patients–safety and efficacy: The ECLIPSE trial–interim analysis at 1 year. J Thorac Oncol. 2015;10(10):1468‐1474.

27.

Okunieff

Petersen

Philip

, et al. Stereotactic Body Radiation Therapy (SBRT) for lung metastases. Acta Oncol. 2006;45(7):808‐817.

28.

Sharma

Duijm

Oomen-de Hoop

, et al. Survival and prognostic factors of pulmonary oligometastases treated with stereotactic body radiotherapy. Acta Oncol. 2019;58(1):74‐80.

29.

Hiyoshi

Miyamoto

Kiyozumi

, et al. CT-guided percutaneous radiofrequency ablation for lung metastases from colorectal cancer. Int J Clin Oncol. 2019;24(3):288‐295.

30.

Matsui

Hiraki

Gobara

, et al. Long-term survival following percutaneous radiofrequency ablation of colorectal lung metastases. J Vasc Interv Radiol. 2015;26(3):303–310;quiz 311.

31.

Chua

Thornbury

Saxena

, et al. Radiofrequency ablation as an adjunct to systemic chemotherapy for colorectal pulmonary metastases. Cancer. 2010;116(9):2106‐2114.

32.

Baba

Watanabe

Yoshida

Kawanaka

Yamashita

Baba

. Radiofrequency ablation for pulmonary metastases from gastrointestinal cancers. Ann Thorac Cardiovasc Surg. 2014;20(2):99‐105.

33.

Yashiro

Nakatsuka

Inoue

, et al. Factors affecting local progression after percutaneous cryoablation of lung tumors. J Vasc Interv Radiol. 2013;24(6):813‐821.

34.

McDevitt

Mouli

Nemcek

, et al. Percutaneous cryoablation for the treatment of primary and metastatic lung tumors: Identification of risk factors for recurrence and major complications. J Vasc Interv Radiol. 2016;27(9):1371‐1379.

35.

Pereira

Rego

Morris

, et al. Association between KRAS mutation and lung metastasis in advanced colorectal cancer. Br J Cancer. 2015;112(3):424‐428.

36.

Zhang

Tian

Zhao

, et al. CT-guided conformal cryoablation for peripheral NSCLC: Initial experience. Eur J Radiol. 2012;81(11):3354‐3362.

37.

Pusceddu

Sotgia

Fele

, et al. CT-guided thin needles percutaneous cryoablation (PCA) in patients with primary and secondary lung tumors: A preliminary experience. Eur J Radiol. 2013;82(5):e246‐e253.

38.

Kennedy

Milovanovic

Dao

, et al. Risk factors for pneumothorax complicating radiofrequency ablation for lung malignancy: A systematic review and meta-analysis. J Vasc Interv Radiol. 2014;25(11):1671‐1681.e1.

39.

Kim

Hong

Ham

, et al. Complications after 100 sessions of cone-beam computed tomography-guided lung radiofrequency ablation: A single-center, retrospective experience. Int J Hyperthermia. 2020;37(1):763‐771.

40.

Tongdee

Tantigate

Tongdee

. Radiofrequency ablation of lung metastasis not suitable for surgery: Experience in Siriraj Hospital. J Med Assoc Thai. 2015;98(10):1019‐1027.

41.

Cao

Meng

Xue

, et al. Safety and efficacy of microwave ablation to treat pulmonary nodules under conscious analgosedation with sufentanil: A single-center clinical experience. J Cancer Res Ther. 2022;18(2):405‐410.

42.

Mouli

Kurilova

Sofocleous

, et al. The role of percutaneous image-guided thermal ablation for the treatment of pulmonary malignancies. AJR Am J Roentgenol. 2017;209(4):740‐751.

43.

Niu

Chen

Yao

, et al. Percutaneous cryoablation for stage IV lung cancer: A retrospective analysis. Cryobiology. 2013;67(2):151‐155.

44.

Hinshaw

Littrup

Durick

, et al. Optimizing the protocol for pulmonary cryoablation: A comparison of a dual- and triple-freeze protocol. Cardiovasc Intervent Radiol. 2010;33(6):1180‐1185.

CT-Guided Percutaneous Cryoablation for Lung Metastasis of Colorectal Cancer: A Case Series

Abstract

Purpose

Methods

Results

Conclusion

Keywords

Introduction

Methods

Study Design

Patient Selection

CA Procedure

Outcome and Safety Measure

Statistical Analysis

Results

Discussion

Conclusion

Footnotes

Declaration of Conflicting Interests

Funding

Ethical Statement

ORCID iD

References