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ORIGINAL ARTICLE
Year : 2022  |  Volume : 18  |  Issue : 2  |  Page : 509-515

Percutaneous microwave ablation under ultrasound guidance for renal cell carcinomas at clinical staging T1 in patients aged 65 years and older: A comparative study


1 Department of Interventional Ultrasound, Chinese PLA General Hospital, Beijing, China
2 Beijing Engineering Research Center of Mixed Reality and Advanced Display, School of Optics and Photonics, Beijing Institute of Technology, Beijing, China

Date of Submission03-Mar-2022
Date of Decision04-Mar-2022
Date of Acceptance05-Mar-2022
Date of Web Publication20-May-2022

Correspondence Address:
Ping Liang
Department of Interventional Ultrasound, Chinese PLA General Hospital, No. 28, Fuxing Road, Beijing, 100853
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.jcrt_531_22

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 > Abstract 


Objectives: To ascertain the clinical outcomes of patients aged ≥65 years with clinical staging T1 (cT1) renal cell carcinoma (RCC) treated with percutaneous microwave ablation (MWA) under ultrasound control compared with those aged <65.
Materials and methods: From September 2009 to December 2016, clinical data of two groups, Group O (≥ 65 years) consisting of 75 patients (76 RCCs) and Group Y (< 65 years) consisting of 91 patients (99 RCCs), who underwent MWA treatment for RCC with comparable mean diameters at baseline, were retrospectively evaluated. The methodological effectiveness, cumulative overall survival (OS) and disease-free survival (DFS), local tumor progression (LTP), major and minor complications, and renal performance, including serum creatinine (Cr) and blood urea nitrogen (BUN) between the two categories, were statistically assessed by SPSS.
Results: After excision, there were no significant differences between the two groups concerning technical efficacy, LTP, and major and minor complications. The cumulative OS and DFS rates at 1, 3, and 5 years in Group O versus Group Y were 100%, 92.6%, and 92.6% versus 98.6%, 96.9%, and 90.9% (P = 0.701), and 100%, 92.5%, and 92.5% versus 98.6%, 96.9%, and 90.4% (P = 0.697), respectively. There was no significant variance between serum Cr and BUN between the two groups before MWA and at the last follow-up.
Conclusion: Due to the corresponding clinical outcomes for the treatment of cT1 RCCs in patients aged <65 years and ≥65 years, the US-guided MWA is a safe and effective method and may be suggested as one of the first-line nonsurgical options for identified older patients.

Keywords: Clinical results, microwave ablation, renal cell carcinoma, ultrasound guidance


How to cite this article:
Cheng Z, Yu X, Han Z, Liu F, Yu J, Yang J, Ai D, Liang P. Percutaneous microwave ablation under ultrasound guidance for renal cell carcinomas at clinical staging T1 in patients aged 65 years and older: A comparative study. J Can Res Ther 2022;18:509-15

How to cite this URL:
Cheng Z, Yu X, Han Z, Liu F, Yu J, Yang J, Ai D, Liang P. Percutaneous microwave ablation under ultrasound guidance for renal cell carcinomas at clinical staging T1 in patients aged 65 years and older: A comparative study. J Can Res Ther [serial online] 2022 [cited 2022 Jul 7];18:509-15. Available from: https://www.cancerjournal.net/text.asp?2022/18/2/509/345544




 > Introduction Top


Renal cell carcinoma (RCC) is the secondmost prevalent cancerous tumor of the urinary tract system in China.[1] With the extensive application of recent clinical imaging and the lengthening of the life expectancy of the populace, the likelihood of kidney cancers has demonstrated progressive trends. It has frequently been identified in patients aged ≥65 years.[2],[3] Additionally, the death rate has risen to 67.7%.[4] Therefore, there is an apparent difficulty in treating RCCs in most patients aged ≥65 due to inefficient renal function preservation or various comorbidities.[5] Therefore, partial nephrectomy (PN) has been suggested as the universal treatment[6],[7] for patients suffering from clinical T1 (cT1) RCCs[8] rather than radical nephrectomy.[9] Compared with PN, image-guided thermal ablations (TAs)[10] comprising of radiofrequency ablation (RFA), cryoablation, and microwave ablation (MWA), which demonstrates effective lasting local tumor regulation,[11] efficient preservation of renal functionality,[12],[13] and reduced significant difficulty rate,[7] has been regarded as one of the prominent suggestions[14] for designated cT1 RCC in older patients.[15] However, inferences from previous experiences suggest that there is no available literature to compare with the clinical outcomes following percutaneous MWA for treating cT1 RCCs in patients within the age range of <65 and ≥65 years. Therefore, this investigation assessed the clinical feedback comprising of oncological results, difficulties, serum creatinine (Cr), and blood urea nitrogen (BUN) between the patients with the aforementioned age distributions to determine the effectiveness and safety of percutaneous MWA under ultrasound (US) regulation in treating patients aged ≥ 65 years suffering from cT1 RCCs.


 > Materials and Methods Top


Patients and tumors

From September 2009 to December 2016, 170 patients suffering from cT1 RCC were treated via percutaneous MWA under US regulation; however, four patients were exempted because of no follow-up. Therefore, the clinical data derived from 166 patients (122 men and 44 women) with an average age of 62.6 ± 13.9 years (range: 21–85 years) were thoroughly examined and are presented in [Table 1]. The total amount of excised RCCs was 175 (98 on the right and 77 on the left) with an average maximum diameter of 2.87 ± 1.07 cm (range: 0.6–7.0 cm) because of the presence of 1, 2, and 3 tumors in 158, 7, and 1 patient, respectively.
Table 1: Clinical features of the patients and RCCs

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With regards to their age at excision, the registered patients were segmented into two categories, namely, 1) Group O: patients aged ≥65 years with an average age of 74.9 ± 6.4 years, and 2) Group Y: patients aged <65 years with an average age of 52.4 ± 9.5 years. All patients had submitted a written informed consent before this research. Due to follow-up, the patients accounted for 3.9% out of Group O (3/78) and 1.1% out of Group Y (1/92). This investigation was carried out according to the Declaration of Helsinki and was endorsed by the Research Ethics Committee of the Chinese PLA General Hospital. A written informed consent was derived from each patient.

Tumor classification and selection criteria

RCCs were histopathologically verified using the 18-guage core needle biopsy (CNB) under US regulation before excision. In addition, the clinical TNM classification was applied.[8] The selection requirement for the patients was as follows: 1) cT1 RCCs, comprising the highest diameter of the tumor of < 7.0 cm, RCCs restricted to the kidney, absence of cancer thrombi in the ipsilateral renal vein and inferior vena cava, absence of lymph node metastases at the renal hilum and retroperitoneum, and absence of distant metastases on imaging examinations prior to MWA; 2) American Society of Anesthesiologists (ASA) Physical Status (PS) Classification I to III in accordance with the ASA PS Classification System[16]; 3) the tumor could be identified using US or contrast-enhanced US (CEUS) imaging; 4) the prothrombin time, prothrombin functionality, and platelet counts were lower than 25 s, higher than 40%, and higher than 40 cells × 109, respectively; 5) surgical refusal or nonsurgical candidates due to the presence of an existing medical condition.

Therapeutic procedure of tumors

An MWA System (KY-2000; Kangyou Medical, Nanjing, China) was used to develop a 2,450-MHz microwave output. A cooled-shaft needle antenna (15-guage diameter and 18 cm in length) with a functioning tip of 0.5 cm or 1.1 cm was employed to convey microwave energy into the tissue.

Hydrodissection, CNB, and MWA protocols were carried out under a color Doppler US device regulation (Acuson Sequoia 512, Siemens Medical Solutions, Mountain View, California, USA) with a 3.0–4.5-MHz phased range multi-frequency transducer.

Hydrodissection[17],[18] using saline injection was applied to isolate the index RCC and the adjacent intestinal tract before excision when the gap between them was <0.5 cm on preoperative computed tomography (CT) or magnetic resonance imaging (MRI)[19] to reduce the thermal complications of intestinal tracts throughout MWA. After applying conventional anesthesia (i.e., 1% lidocaine) at the site to be excised, a 16-guage intravenous catheter (BD Angiocath; Sandy, UT, USA) with an estimated length of 15 cm was used to perform hydrodissection. When the tip of the catheter was inserted into the tissue underneath the abdominal peritoneum between the renal index tumor and the proximal intestinal tract under US regulation, numerous milliliters of saline solution were quickly introduced. Then, a small standard isolation of the liquid between the tumor and the bowel was demonstrated. The saline was constantly injected while the tip of the catheter was continuously advanced and inserted along with the standard liquid separation under US guidance until the disconnection between the tumor and the adjacent tract was effectively accomplished on the US image. After the inner stylet was separated, the exterior catheter was stored for additional saline instillation. For large tumors, another hydrodissection protocol could be carried out at a different location to differentiate the index tumor and the bowel. Saline was injected into the perirenal adipose capsule to achieve a successful separation. Due to previous abdominal surgery, it may have been tasking to separate the tumor from the intestinal tract.

The procedure was as follows. First, CNB was carried out using an 18-guage automatic cutting needle. After that, the antenna was introduced into the index tumor under US guidance. After all antenna insertions were thoroughly confirmed, the microwave output was executed at a power rating of 50 W or 60 W. The ablation was terminated when the hyperechoic zone enclosed the whole index tumor on US imaging. Then, a needle tract cauterization was customarily executed to reduce bleeding and tumor seeding during antenna extraction. Contrast-enhanced imaging, such as CEUS, contrast-enhanced CT, or MRI, was routinely utilized one to three days after the procedure to evaluate treatment response. An irregular peripheral enhancement of the ablated lesion typically demonstrated a plausible unoperated residual tumor; as a result, a subsequent MWA session was executed within one week.

A large proportion of the registered patients were treated under intravenous anesthesia after the pre-ablation examination of a proficient anesthetist, and the addition of Propofol (Diprivan; Zeneca Pharmaceuticals, Wilmington, Del, USA) and Ketamine (Shuanghe Pharmaceuticals, Beijing, China) was done. For patients who were not candidates of intravenous anesthesia due to bradycardia, severe emphysema, etc., the MWA procedure was carried out using standard anesthesia monitored by the anesthetist. A 21-guage diameter PTC (Percutaneous transhepatic cholangiography) needle 20 cm in length was inserted to alleviate the pain during excision. About 10–20 mL of 1% lidocaine solution was introduced along the puncture route of the microwave antenna.

Follow-up after MWA

The major and minor complications associated with the procedures were thoroughly recorded and managed after MWA, according to the definition of complications published for the standardization of the terminology and reporting requirement of image-guided tumor ablation.[20] Additionally, the precise moment and cause of death were documented. The contrast-enhanced imaging of CT or MRI and renal functional assays, including serum Cr and BUN was regularly performed at the 1st, 3rd, and 6th months after MWA and then at 6-month intervals. For patients having Cr exceeding the normal range, CEUS and plain CT or MRI were employed during follow-up.

The technical effectiveness was described as no enhancement of the entire tumor on contrast-enhanced imaging at one month follow-up post MWA. Local tumor progression (LTP) was defined as the uneven peripheral improvement in scattered, nodular, or eccentric pattern ensuing at the original sites formerly regarded as totally ablated during the follow-up period.

Statistical analysis

Data analysis was executed with the SPSS software, version 22.0 (SPSS Inc. Chicago, IL, USA) and GraphPad Prism software version 5.0 for Windows (GraphPad Software, San Diego, California, USA). These software programs were used to analyze the data and draw the graphs. Values for quantitative variables were presented as mean ± SD (range).

An independent-sample t test was performed between the two categories to compare the mean age, tumor diameters, excision energy, time and power, follow-up months, and disease-free survival (DFS) time. The Chi-squared test was employed for categorical variables, including gender distribution, the population of patients with multiple nodules, technical effectiveness, hydrodissection, intravenous anesthesia, major and minor complications, LTP, and death. The one-, three-, and five-year aggregate overall survival (OS) and DFS rates were evaluated using the Kaplan–Meier method.

All the tests were two-sided. P < 0.05 was considered to be significantly different.


 > Results Top


Comparisons of patients and tumors

A total number of 75 patients diagnosed with 76 RCCs with a mean diameter of 2.92 ± 0.93 cm and 91 patients diagnosed with 99 RCCs with a mean diameter of 2.83 ± 1.17 cm registered in Group O and Group Y, respectively, were subjected to percutaneous MWA under US guidance [Figure 1]. The relationships between the registered patients and the clinical features of RCCs between the two groups are presented in [Table 2]. The mean age between the two groups was significantly different (P < 0.001).
Figure 1: A 69-year-old man with a right renal tumor medically verified clear cell carcinoma. (a) Transverse contrast-improved CT shows a 3.3-cm hypo-enhancement tumor (arrow) situated at the lower pole of the right kidney adjacent to the colon (curve arrow) before MWA. (b) Coronal contrast-assisted CT shows the renal tumor (arrow) before MWA. (c) Transverse contrast-enhanced MRI one year after MWA indicates the tumor is utterly excised (arrow) adjacent to the colon (curve arrow). (d) Coronal contrast-enhanced MRI one year after MWA shows the excised tumor (arrow) adjacent to the colon (curve arrow)

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Table 2: Comparison of the enrolled patients and clinical characteristics of RCCs between the two groups

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Hydrodissection was used in 22 patients (13 in Group O and 9 in Group Y). Six patients, five in Group O and one in Group Y, were not included as candidates for intravenous anesthesia and, therefore, received MWA under local anesthesia. The procedure was effectively executed in all six patients.

Comparisons of oncological outcomes

The oncological results between the two categories are presented and compared in [Table 3]. Technical effectiveness rates for RCCs were 97.4% (74/76) and 100% (99/99) in Group O and Group Y, respectively, at one-month follow-up after MWA (P = 0.187). Active surveillance (AS) and oral sunitinib were applied to two patients without technical efficacy because of advanced age and site of the untreated tumor, who died 18 and 20 months after ablation, respectively, due to several metastases of RCC. The other two patients in Group O died due to cerebral hemorrhage and heart failure 20 and 34 months after MWA, respectively. Six patients in Group Y died, and the cause of death was a heart attack in one, pulmonary heart failure in another, several metastases of RCC in three, and multiple metastases of hepatocellular carcinoma in another. The death rates were 5.3% (4/75) and 6.6% (6/91) in Group O and Group Y (P = 1.000), respectively. The cumulative OS rate [Figure 2]a and DFS rate [Figure 2]b at 1, 3, and 5 years were 100%, 92.6%, 92.6% versus 98.6%, 96.9%, 90.9% (P = 0.701), and 100%, 92.5%, 92.5% versus 98.6%, 96.9%, 90.4% (P = 0.697) in Group O versus Group Y, respectively. The average DFS time was 38.2 ± 20.8 months (95% confidence interval, 33.6–42.9 months) and 36.9 ± 24.9 months (95% confidence interval, 31.3–42.1 months; P = 0.713) for Groups O and Y, respectively. With the exception of death cases, LTPs in Group O and Group Y were 1.4% (1/71) and 4.7% (4/85) (p = 0.377), respectively, and the average LTP time was 25.2 ± 12.6 months (range: 9–43 months).
Figure 2: Cumulative overall and infection-free survival rates between the two groups. Graph A shows the one-, three-, and five-year cumulative overall survival rates at 100%, 92.6%, and 92.6% vs 100%, 96.9%, and 90.9% in Group O vs Group Y, respectively. There were no significant differences between the two groups (P = 0.701). Graph B demonstrates the one-, three-, and five-year cumulative disease-free survival rates at 100%, 92.5%, and 92.5% vs 98.6%, 98.6%, and 90.4% in Group O vs Group Y, respectively. There were no significant differences between the two groups (P = 0.697). Cum: cumulative; Group O: patients aged ≥65 years; Group Y: patients aged <65 years

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Table 3: Comparison of the clinical results between the two groups

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Comparisons of complications

All major and minor complications encountered in this study are presented in [Table 3]. The major complication rates observed were 4.0% (3/75) and 2.2% (2/91) in Group O and Group Y (P = 0.659), respectively, comprising one intestinal puncture, one urinary leakage, two massive pleural effusion, and one hepatic encephalopathy. On the other hand, the minor complication rates were 10.7% (8/75) and 7.7% (7/91) in Group O and Group Y (P = 0.591), respectively (two hemoglobinuria, five gross hematuria, five perirenal hematomas, and three thermal injuries of psoas muscles).

Changes of renal function

The renal functional indexes comprising serum Cr and BUN differed significantly in patients on dialysis, so all death cases and four patients (one in Group O and three in Group Y) on dialysis prior to MWA in both groups were exempted to rationally compare the alteration of renal function between MWA and the last follow-up in the two categories. The modifications of Cr and BUN in the two categories are presented in [Figure 3]. There were no significant differences between the two groups in the average serum Cr and BUN before MWA (P = 0.645 and P = 0.423) and at the last follow-up (P = 0.954 and P = 0.915), respectively. Comparing the indexes at the final follow-up with those before MWA in each group, there were no significant differences in both Cr (P = 0.078) and BUN (P = 0.245) in Group O and both Cr (P = 0.183) and BUN (P = 0.564) in Group Y.
Figure 3: The serum creatinine (Cr) alterations and blood urea nitrogen (BUN) in the two groups. Graph A presents the alterations of Cr in the two groups. There were no significant differences in the average serum Cr level between the two groups before the MWA (P = 0.645) and at the last follow-up (P = 0.954). Also, there were no significant differences between the average serum Cr at the previous follow-up and before the MWA in Group O (P = 0.078) and Group Y (P = 0.183), respectively. Graph B represents BUN alterations in the two groups. There were no significant differences in the mean BUN level between the two groups before the MWA (P = 0.423) and at the last follow-up (P = 0.915). Additionally, there were no significant differences in the mean BUN at the previous follow-up compared with the MWA in Group O (P = 0.245) and Group Y (P = 0.564). MWA: microwave ablation; FU: follow-up; Group O: patients aged ≥65 years; Group Y: patients aged <65 years

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 > Discussion Top


Clinically oncological treatments for older patients[21] diagnosed with cancers required careful execution due to their inadequate preservation of organic function, several comorbidities, and evaluation of residual life expectancy. Therefore, to ascertain an alternate beneficial treatment for the older patients diagnosed with RCCs,[22] a thorough review to evaluate the balance of benefits and harm in the preservation of renal function, enhancement of quality of life, lengthening of survival, and plausibility of treatment risks and constraints would be applied before the oncological treatment selection.

Active surveillance (AS) is an entirely noninvasive protocol and has been used on older patients[23] coupled with several comorbidities or reduced life expectancy.[24] The tumor development required careful monitoring during the AS period because not all small kidney cancers were always indolent.[25] Therefore, for patients aged ≥65 years diagnosed with cT1 RCCs restricted to the kidney, it was essential to confirm a safe and efficient alternative therapy compared with the clinical results of patients who were aged <65 years. Percutaneous excision directed by imaging might be one of the therapeutic options because of comparable recurrence-free survival[26] to PN and efficient preservation of renal function[12],[13] for older patients. In the present study, the clinical data of cT1 RCCs after percutaneous MWA in the group of patients who were ≥ 65 years old were thoroughly evaluated and compared with those in the group of patients who were < 65 years old with the same tumor maximal diameters in the baseline. The outcome demonstrated matching technical efficacy, LTP, cumulative OS, and DFS rates, major and minor complications, and the renal function between the two groups; so, percutaneous MWA could be suggested as one of the optimally minimally invasive treatments for older patients diagnosed with clinical T1 RCCs. The 1, 3, and 5 years of cumulative OS and DFS rates were 100%, 92.6%, and 92.6% and 100%, 92.5%, and 92.5% in Group O, respectively, which were comparable with the results of other ablation techniques.[27] The likely reason was that all registered patients belonged to ASA PS Classification I to III, which had an independent association with existence rather than with age.[28] Additionally, the association of the mean serum Cr and BUN between the two groups exhibited no statistical significance after MWA, implying that percutaneous MWA could protect kidney functionality for older patients.

For safety, the entire prevalence of complications of all cases was 12.0% (20/166): almost the result of 11.0% stated in a published document of MWA therapy for RCCs.[29] Compared with PN, TA therapy exhibited a low occurrence of major complications in the management of RCCs.[7] Still, intestinal damage after TA as a major complication had to be given serious attention.[30] In this study, an 84-year-old lady diagnosed with left renal clear cell carcinoma, which was assessed clinically, encountered an intestinal opening caused by thermal lesions after MWA. The plausible reason was that the ileum adhered to the retroperitoneum adjacent to the index RCC because the patient had a surgical record of ovarian cancer resection. To reduce the significant difficulties of bowel injury after MWA, the US-guided hydrodissection demonstrates an efficient protocol to assist percutaneous MWA for patients having RCCs adjacent to intestinal tracts.[17] In this study, the entire amount of 22 cases (13 in Group O and 9 in Group Y) was ablated completely of their RCCs with the help of the US-guided hydrodissection, and no bowel injury ensued after MWA. Another 78-year-old lady underwent urinary leakage around the right kidney, and a 10-day catheter drainage was carried out. She had diabetes, and her ablated tumor was near the renal collection system. The plausible reason for the urinary leakage was due to the injured pelvis after TA. The patient diagnosed with hepatic encephalopathy, chronic hepatitis B, and liver cirrhosis recuperated after treatment of intravenous hepatoprotective medication for one week. The patients with massive pleural effusion were treated with catheter drainage for three days. However, the prevalence of major and minor complications was not statistically different between the two groups. Therefore, further investigation with large-scale registrations to compare would be necessary because both the major and minor complications likely occurred in Group O instead of in Group Y, according to the absolute occurrence of difficulties in the two groups.

Numerous restrictions, such as single participating centers, relative small-scale enrollment, small tumor diameters, and short-term follow-up period transpired in this retrospective investigation, and the outcome of an additional prospective study with large-scale and long-term examination would be more substantial. Additionally, because of small-scale registration, it was not adequate to execute stratification analyses regarding the tumor sizes between the cT1a and cT1b, and the tumor development configurations among exophytic, parenchymal, and endophytic ones, and other large-scale cases, which could be helpful to a stratified evaluation. Finally, comprehensive geriatric assessment information, such as comorbidity, functional status, and cognitive function, were not provided because of the limitation of this investigation.


 > Conclusion Top


In conclusion, the ultrasound-guided percutaneous microwave ablation is a safe and effective method and may be recommended as one of the first-line nonsurgical options for selected older patients because of the corresponding clinical results for treating clinical staging T1 renal cell carcinomas in patients aged less than 65 years and 65 years and older.

Financial support and sponsorship

This work was supported by the National Scientific Foundation Committee of China (Grants No. 82171941 & 81871374) and the National Clinical Research Center for Geriatric Diseases, Chinese PLA General Hospital (NCRCG-PLAGH-2019011).

Conflicts of interest

There are no conflicts of interest.



 
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[PUBMED]  [Full text]  
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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