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ORIGINAL ARTICLE
Year : 2020  |  Volume : 16  |  Issue : 2  |  Page : 292-300

US-guided percutanous microwave ablation for early-stage hepatocellular carcinoma in elderly patients is as effective as in younger patients: A 10-year experience


1 Department of Interventional Ultrasound, Chinese PLA General Hospital, Beijing; Department of Ultrasound, The Affiliated Hospital of Inner Mongolia Medical University, Inner Mongolia, China
2 Department of Interventional Ultrasound, Chinese PLA General Hospital, Beijing, China

Date of Submission24-Nov-2019
Date of Decision06-Mar-2020
Date of Acceptance26-Mar-2020
Date of Web Publication28-May-2020

Correspondence Address:
Ping Liang
Department of Interventional Ultrasound, Chinese PLA General Hospital, 28 Fuxing Road, Beijing 100853
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_1021_19

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 > Abstract 

Objective: To compare the overall survival (OS), disease-free survival (DFS) and liver-cancer-specific survival (LCSS) of elderly (≥65 years) and younger patients (< 65 years) with early-stage hepatocellular carcinoma (HCC) using ultrasound-guided percutaneous microwave ablation (US-PMMA). Materials and Methods: From January 2002 to December 2017, 510 elderly and 1053 younger patients were diagnosed with early-stage HCC according to the Milan criteria. All of these patients were treatment-naïve to US-PMMA. Baseline characteristics were collected to identify any risk factors to determine the survival outcomes. OS, DFS, and LCSS probabilities were calculated with the Kaplan-Meier method and compared using the Log-rank test. Results: Complete ablation was achieved in all patients. Elderly patients were more likely to be, hepatitis C virus infection, comorbidities, cirrhosis, larger tumors, poor liver functional reservation, more ablation points, longer ablation time, longer hospital stays, and higher hospitalization costs (P < 0.05). Over the follow-up period (12–156 months), no significant differences were detected in OS, DFS, and LCSS between the two groups ( P = 0.092, 0.318, and 0.183). r-GT, ALB and ablation session were significant factors for OS, r-GT and ALB for LCSS, and cirrhosis, tumor number, AFP and ablation points for RFS in the multivariate analysis, respectively. No treatment-related deaths occurred in the two groups. Any complications were treated as appropriate. Conclusions: Although advanced age and comorbidities are intrinsic factors in elderly HCC patients, similar survival outcomes were obtained in elderly and younger HCC patients treated by US-PMWA, despite elderly patients having more comorbidities.

Keywords: Disease-free survival, elderly, hepatocellular carcinoma, liver cancer-specific survival, microwave ablation, overall survival


How to cite this article:
Wang Y, Cheng Z, Yu J, Li X, Hao G, Liu F, Han Z, Yu X, Liang P. US-guided percutanous microwave ablation for early-stage hepatocellular carcinoma in elderly patients is as effective as in younger patients: A 10-year experience. J Can Res Ther 2020;16:292-300

How to cite this URL:
Wang Y, Cheng Z, Yu J, Li X, Hao G, Liu F, Han Z, Yu X, Liang P. US-guided percutanous microwave ablation for early-stage hepatocellular carcinoma in elderly patients is as effective as in younger patients: A 10-year experience. J Can Res Ther [serial online] 2020 [cited 2020 Jul 16];16:292-300. Available from: http://www.cancerjournal.net/text.asp?2020/16/2/292/285178




 > Introduction Top


Globally, people are living longer, which has resulted in increased cancer-related morbidity and mortality.[1] Hepatocellular carcinoma (HCC) is the fifth most common cancer and the second most common cause of cancer mortality worldwide.[2],[3] The incidence of HCC has gradually declined for those under 50 years old and is expected to reach its highest prevalence among those aged ≥65 years old by 2030.[4],[5],[6] Improving the management of elderly patients with early-stage HCC is increasingly important. Categorizing patients with HCC has been challenging as the definition of 'elderly' has changed over time.[7] The United Nations agree that the term 'elderly' refers to people over 65 years old. Previous studies have used this as the cut-off for “elderly,”[8],[9],[10] and it may, therefore, be an appropriate threshold.[11] Elderly patients are considered “fragile” due to their comorbidities and altered drug metabolism and more vulnerable to treatment complications.[12] Therefore, treatment modalities should be chosen carefully.

Currently, liver transplantation (LT), surgical resection (SR), and thermal ablation (TA) are the primary treatment modalities used for early-stage HCC according to the Barcelona Clinic Liver Cancer guidelines. LT is not a viable option for most patients due to organ shortages, high cost, and strict patient selection criteria. SR and TA are often the initial treatment options recommended for early-stage HCC.[11],[13] However, elderly patients with HCC can have age-related deterioration of their liver function and higher incidences of comorbidities, such as hypertension, heart disease, diabetes, renal insufficiency, chronic lung disease, cerebral vascular disease, and esophageal or gastric varices.[14] However, many elderly patients cannot tolerate SR. Many studies have reported that a similar long-time prognosis could be achieved by SR and TA in early-stage HCC.[15] Therefore, TA has been established as the most common alternative treatment for elderly patients with small HCC. It has excellent antitumor effects, is less invasive, and has lower perioperative risks, with fewer deteriorative effects on liver function than SR.[16],[17] Among the TA techniques, microwave ablation (MWA) has higher thermal efficiency, which results in a larger ablation zone and decreased ablation and anesthesia time. These features may help to reduce complications.[18],[19] Few studies have compared the effect of MWA in elderly and younger patients with early-stage HCC. We compare the survival benefits of MWA in elderly and younger patients based on a large population database and influencing factors.


 > Materials and Methods Top


Patient selection

This is a single-center, retrospective study. The Ethics Committee of the Chinese PLA General Hospital (Beijing, China) approved the protocol. The study was conducted as per the Declaration of Helsinki. Two thousand and twenty-two treatment-naïve patients with early-stage HCC treated with ultrasound-guided percutanous microwave ablation (US-PMWA) were enrolled between January 2002 and December 2017. Written informed consent was obtained from each patient. Treating elderly patients with early-stage HCC is controversial, with no universally accepted protocol. After a pretreatment evaluation, a multidisciplinary team of radiologists, surgeons, hepatologists, and oncologists met and selected patients who were suitable to receive PMWA. The treatment option was then discussed with the patient and their family. Of these, 1563 patients were enrolled.

The inclusion criteria were: (1) Eastern Cooperative Oncology Group performance scores ≤2; (2) Child-Pugh A or B; (3) 5 cm < tumor maximum diameter and tumor number <3; (4) absence of vascular invasion or extrahepatic metastases; (5) a normal serum total bilirubin level or <50 μmol/L; (6) a normal albumin level or >25 g/L; (7) platelet count >50 × 109/L and prothrombin activity >50%; (8) final diagnosis was based on the pathologic findings from a biopsy immediately before ablation; (9) no history of other malignancies; (10) refuse to undergo hepatectomy or LT. The exclusion criteria were: (1) incomplete clinical data; (2) lost to follow-up within 3 months after ablation; (3) serious heart, lung, and renal function dysfunction, and severe active infection. As displayed in the flowchart [Figure 1], 1563 treatment-naïve patients with HCC were screened and classified into either the elderly (n = 510) or younger groups (n = 1053).
Figure 1: Patient enrollment flowchart. HCC = Hepatocellular carcinoma, ICC = Intrahepatic cholangiocarcinoma

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Data collection

The clinical data collected were: (1) Patient features (sex, age, comorbidities [hypertension, heart disease, diabetes, renal insufficiency, chronic lung disease, cerebral vascular disease, and esophageal or gastric varices], pathological differentiation degree, etiology, cirrhosis, Child-Pugh grade, and ascites); (2) tumor features (size, number, and location); (3) preoperative data (a-fetoprotein [AFP], alanine transaminase, glutamic-oxaloacetic transaminase, total Bilirubin [TBI], direct Bilirubin [DBI], albumin, cholinesterase [CHE], r-glutamyltranspeptidase [r-GT], creatinine [Cre], hemoglobin [Hb], platelet [PLA], prothrombin time [PT], international normalized ratio and); (4) ablation parameters (antenna number, ablation point, time and session); (5) clinical outcomes (hospital stays, cost, complications, recurrence, metastases, and survival).

Ultrasound-PMTA procedure

Two cooled-shaft microwave systems (KY-2000, Kangyou Medical, Nanjing, China) with frequencies of 2450 MHz were used. The needle antenna had a diameter of 1.9 mm and one 18 cm shaft that could be easily visualized. A narrow radiating segment of 3 mm was embedded on the shaft, 11 or 22 mm away from the tip. The microwave machine was equipped with a thermal monitoring system that continuously measured temperature during ablation. The thermal monitoring needle had a diameter of 0.8 mm.

An automatic biopsy gun with an 18G cutting needle was used to carry out a US-guided biopsy immediately before ablation. Consequently, the antennas were percutaneously inserted into the tumor and placed at a designated location under US guidance. For tumors ≤2.0 cm, one antenna was inserted. For tumors between 2.0–3.0 cm, and 3.0–5.0 cm, two antennae were used simultaneously with two insertions, and four insertions, respectively. A power output of 50–60W was routinely used during ablation. A thermal monitoring needle was inserted into the tumor margin for real-time temperature monitoring. After all insertions, intravenous anesthesia was administered during standard hemodynamic monitoring. When the heat-generated hyperechoic water vapor completely encompassed the entire tumor in the US image ablation was considered complete. As many of the tumors were located in at-risk locations and were larger than 3 cm, a three-dimensional visualization operative planning system, artificial pleural effusion, and ascites were also applied.[20],[21]

Follow-up

Contrast-enhanced images were performed to evaluate the treatment efficacy 3 days after ablation. If irregular peripheral enhancement occurred in a scattered, nodular, or eccentric pattern, another ablation was performed. Otherwise, routine contrast-enhanced images and serum tumor markers were repeated after 1 and 3 months, and every 6 months. Chest radiography was performed every 6 months. Bone scintigraphy was performed yearly to check for extrahepatic metastasis. The endpoints of this study were death or termination. Recurrence-free survival (RFS) was considered from the date of ablation to recurrence. Liver-cancer-specific survival (LCSS) was defined as a liver cancer-related cause of death. overall survival (OS) was calculated from the date of ablation to the date of death or last follow-up. Complications were classified according to the Society of Interventional Radiology Classification system for Complications by Outcome.[22],[23] If recurrence and metastasis were detected, proper treatments were administered.

Statistical analysis

Continuous data were expressed as a median with an interquartile range. The Kolmogorov–Smirnov test was used on continuous variables to check for normal distribution. Normally distributed data were compared using an unpaired t-test. Otherwise, the Mann-Whitney test was used. Chi-square or Fisher's exact tests were used to compare categorical variables. RFS, OS, and LCSS were graphically depicted by the Kaplan-Meier curve and compared using the Log-rank test. Univariate and multivariate Cox regression models were used to analyze the hazard ratios (HRs) of the baseline characteristics of RFS, OS, and LCSS. The variable selection method used in the multivariate analysis was “enter”. SPSS version 25.0 (SPSS, Chicago, IL, USA) was used for the data analysis. A P < 0.05 was considered statistically significant.


 > Results Top


Baseline characteristics and long-term survival

All patients' demographic and clinical characteristics are summarized in [Table 1]. Elderly patients were more likely to be hepatitis C virus infection (P < 0.001). Additionally, they also had a greater prevalence of comorbidities, cirrhosis, larger tumors, poor liver functional reservation, more ablation points, longer ablation time, longer hospital stays, and increased hospitalization cost (P < 0.05). Over the follow-up period, which ranged from 12 to 156 months, 667 (42.7%) patients died, of whom 211 (31.6%) were elderly, and 456 (68.4%) were younger. The median overall survival was comparable between the groups (elderly 47.1 months (95% confidence interval [CI], 43.1 – 51.2), younger 55.7 months (95% CI, 50.5 – 60.8). The OS rates at 1, 3, 5 and 10 years ere 95.0%, 64.0%, 34.1% and 5.8% in elderly group versus 95.5%, 65.3%, 45.8% and 10.6% in younger one, respectively [P = 0.077, [Figure 2]a. Among those patients that died, 175 (31.1%) and 387 (68.9%) were related to HCC in the elderly and younger groups, respectively. So, the 1, 3, 5 and 10-year LCSS were 96.2%, 69%, 43.1% and 7.9% in elderly group versus 96.7%, 70.3% 50.2% and 14% in younger one, respectively [P = 0.158, [Figure 2]b. Regarding recurrence and metastasis, there were 343 (32.3%) patients in the elderly group and 720 (67.7%) in the younger group. The disease-free survival (DFS) rates at 1, 3, 5 and 10 years were 67.0%, 33.7%, 17.5% and 0% in elderly group versus 66.8%, 37.2%, 24.4% and 0% in younger one, respectively [P = 0.310, [Figure 2]c.
Table 1: Demographic and clinical characteristics of all patients

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Figure 2: Kaplan-Meier curves of overall survival, liver-cancer-specific survival and disease-free survival of elderly and younger patients treated with ultrasound-PMWA. (a) Overall survival comparison, (b) Liver-cancer-specific survival comparison, (c) disease-free survival comparison

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Univariable and multivariate analysis of the factors associated with overall survival

A univariate and multivariate logistic regression analysis were performed to identify factors that could influence the long-term outcomes of elderly patients with early-stage HCC who underwent US-PMWA. The univariate analysis showed statistically significant differences in terms of OS, depending on the etiology of hepatitis C (HR: 0.75, 95% CI: 0.60–0. 94, P = 0.013), larger tumor size (HR: 1.224, 95% CI: 1.130–1.325, P < 0.001), child-P grade B (HR: 1.61,95% CI: 1.15–2.24, P = 0.005), higher AFP level (HR: 1.177, 95% CI: 1.010–1.372, P = 0.036), higher r-GT level (HR: 1.001, 95% CI: 1.000–1.001, P = 0.004), lower ALB level (HR: 0.953, 95% CI: 0.938-0.968; P < 0.001), higher TBI level (HR: 1.010, 95% CI: 1.003–1.018, P = 0.009), higher DBI level (HR: 1.024, 95% CI: 1.010–1.038, P = 0.001), lower CHE level (HR: 1.000, 95%: 1.000–1.000, P = 0.001), lower Hb level (HR: 0.996, 95%: 0.991–1.000, P = 0.033), more antenna number (HR: 1.143, 95% CI: 1.057–1.235, P = 0.001), more ablation points (HR: 1.059, 95% CI: 1.001–1.121, P = 0.045) and more ablation sessions (HR: 1.301, 95% CI: 1.100–1.538, P = 0.002). The multivariate analysis showed that the factors that significantly affected OS were higher r-GT level (HR: 1.001, 95% CI: 1.000–1.001, P = 0.010), lower Hb level (HR: 0.961, 95% CI: 0.946–0.976, P < 0.001) and more ablation sessions (HR: 1.371, 95% CI: 1.123–1.674, P = 0.002) [Table 2].
Table 2: Univariable and multivariate analysis of the factors associated with overall survival in elderly patients with early-stage hepatocellular carcinoma who underwent ultrasound-guided percutaneous microwave ablation

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Univariable and multivariate analysis of factors associated with liver-cancer-specific survival

A univariate and multivariate logistic regression analysis were performed to identify factors that could influence the long-term outcomes of elderly patients with early-stage HCC who underwent US-PMWA. The univariate analysis showed statistically significant differences in terms of LCSS, depending on larger tumor size (HR: 1.184, 95% CI: 1.084–1.292, P < 0.001), child-P grade B (HR: 1.655, 95% CI: 1.158–2.365, P = 0.006), higher AFP level (HR: 1.189, 95% CI: 1.006–1.404, P = 0.042), higher r-GT level (HR: 1.001, 95% CI: 1.000–1.001, P = 0.003), lower ALB level (HR: 0.955, 95% CI: 0.939–0.972, P < 0.001), higher TBI level (HR: 1.010, 95% CI: 1.001–1.019, P = 0.023), higher DBI level (HR: 1.024, 95% CI: 1.008–1.040, P = 0.003), higher CHE level (HR: 1.000, 95% CI: 1.000–1.000, P = 0.015), more antenna number (HR: 1.124, 95% CI: 1.032–1.224, P = 0.007), and more ablation sessions (HR: 1.277, 95% CI: 1.063–1.534, P = 0.009). The multivariate analysis showed that the factors that significantly affected the OS were higher r-GT level (HR: 1.001, 95% CI: 1.000–1.001, P = 0.008) and lower ALB level (HR: 0.965, 95% CI: 0.949–0.982, P < 0.001) [Table 3].
Table 3: Univariable and multivariate analysis of the factors associated with liver-cancer-specific survival in elderly patients with early-stage hepatocellular carcinoma who underwent ultrasound-guided percutaneous microwave ablation

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Univariable and multivariate analysis of factors associated with disease-free survival

A univariate and multivariate logistic regression analysis was performed to identify factors influencing the long-term outcomes of elderly patients with early-stage HCC who underwent US-PMWA. The univariate analysis showed statistically significant differences in terms of DFS, depending on cirrhosis (HR: 1.397, 95% CI: 1.073–1.819, P = 0.013), more tumor number (HR: 1.543, 95% CI: 1.319–1.803, P < 0.001), higher AFP level (HR: 1.195, 95% CI: 1.051–1.359, P = 0.007), higher r-GT level (HR: 1.001, 95% CI: 1.000–1.001, P = 0.021), higher DBI level (HR: 1.013, 95% CI: 1.001–1.026, P = 0.040), and more ablation points (HR: 0.951, 95% CI: 0.906–0.999, P = 0.046). The multivariate analysis showed that the factors that significantly affected the OS rate were cirrhosis (HR: 1.341, 95% CI: 1.029–1.746, P = 0.030), more tumor number (HR: 1.452, 95% CI: 1.238–1.703, P < 0.001), higher AFP level (HR: 1.169, 95% CI: 1.026–1.332, P = 0.019), and more ablation points (HR: 0.869, 95% CI: 0.813–0.928, P < 0.001) [Table 4].
Table 4: Univariable and multivariate analysis of the factors associated with disease-free survival in elderly patients with early-stage hepatocellular carcinoma who underwent US-PMWA

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Complications

Fever and pain were the most common complications. Posttreatment fever with an axillary temperature >39.0°C was observed in 1 patient in the younger group, who then developed a liver abscess. The patient was treated with antibiotics, and the abscess was drained using a catheter. The patient recovered after 48 days in hospital. One patient had a chest wall implantation detected and underwent another ablation. Nineteen patients had a pleural effusion, and 2 had ascites in the elderly group and 22 and 6 in the younger group, respectively. No differences were detected between the groups regarding complications suffered [Table 5].
Table 5: Complications and prognosis between the elderly and younger early-stage hepatocellular carcinoma patients after ultrasound-guided percutaneous microwave

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 > Discussion Top


As life expectancy is increasing worldwide, it is expected that there will be a larger number of elderly patients with HCC requiring oncological treatment. The clinicopathological characteristics differ between elderly and younger patients. In this study, elderly patients were more likely to be higher female proportion, have hepatitis C, a greater prevalence of comorbidities, cirrhosis, larger tumors. The average lifespan of females is longer, and their peak age is delayed by 5 years compared to males.[24] Hepatitis C is generally acquired in adulthood, which explains its prevalence in the elderly group. Contrastingly, hepatitis C frequently occurs earlier.[25],[26] The results are similar to a study reported in 2015.[27] Additionally, elderly patients have more comorbidities, along with liver disease progression. Multidisciplinary consultation for individualized treatment is necessary to optimize treatment outcomes. In elderly HCC patients, larger tumors and poor liver functional reservation were more prevalent. This might be due to less supervision and detection in elderly patients. Therefore, the treatment selected should be carefully considered for elderly patients. Our study includes the largest number of patients and includes unselected cases followed-up for more than 10 years. Therefore, it is conceivable that the results reflect those in clinical practice.

Despite a higher prevalence of comorbidities and a mean age that was higher by 18 years, elderly patients had similar OS, LCSS, and DFS rates at 1, 3, 5, and 10 years to their younger counterparts. Regarding the 5 and 10 years OS, elderly patients were lower than the younger patients. Regarding the 5 and 10 years LCSS, younger patients were higher than the elderly group. These results could reflect the low survival rate in the two groups (<50% at 5 years and <15% at 10 years), indicating that the occurrence of HCC outweighs the impact of both comorbidities and age. This agrees with previous reports. MWA was a safe and effective method for elderly HCC patients and could achieve promising long term survival.[18],[19],[27] Therefore, age and comorbidities were not an influencing factor for MWA in elderly HCC patients and might help to expand the indications of MWA in clinical practice.[28]

Regarding elderly HCC patients, the factors potentially influencing OS, LCSS, and DFS after MWA treatment were also analyzed using a univariable and multivariate analysis. The results suggest that tumor differentiated degree was an important factor for OS and LCSS, regardless of age or sex. The liver function reservation indexes of the r-GT level, Hb, and albumin levels were also factors for elderly patients. Improving liver function during the follow-up period might benefit long-time survival. Recurrence and metastases were short-time outcome indexes. The multivariate analysis results indicate that liver cirrhosis, higher AFP levels, more tumors, and more ablation points were significant factors for DFS. Regular detection of the AFP levels could be used to predict recurrence and metastases of HCC. More tumors and ablation points were related to the tumor size. To protect the liver and renal function, lower power, and a longer ablation strategy could be applied to elderly patients. Such ablation strategies may increase the number of ablations and ablation points and promote ablation precision.[20],[21]

Treatment-related complications must be considered in elderly patients. Nevertheless, in this study, no significant difference was found between the groups. Contrastingly, more serious complications were detected in the younger group, such as a liver abscess and tumor implantation.[29] However, the period and hospitalization costs in the elderly group were higher due to more preoperative evaluation examinations and extended postoperative observations. Therefore, more personalized treatment options and strategies in elderly patients are required.[6],[18],[27] With the emergence of new therapeutic methods, such targeted and immunotherapy therapeutical strategies can be developed. These could help to improve the long-term prognosis of elderly HCC patients.[30],[31]

There are several limitations to this study. Firstly, this was a single-center study. A multi-center study should be conducted to confirm the results. Secondly, due to its retrospective study design, inherent selection bias could not be eliminated. Thirdly, this study only focused on early-stage HCC patients. Further analysis with intermediate-stage and advanced-stage HCC patients should also be explored.


 > Conclusion Top


Similar short-time and long-time outcomes were obtained in elderly and younger HCC patients treated by US-PMWA. Treatment options for elderly patients should be personalized, and all treatment options available to younger patients should be available to the elderly. Careful preoperative evaluation of clinical status, tumor stage, comorbidities, and postoperative treatment is needed to ensure better treatment outcomes.

Acknowledgments

This work was supported by the National Key R&D Program of China (No. 2017YFC0112000), three grants from the National Scientific Foundation Committee of China (No. 81430039, 81627803 and 81801723), the Clinical Research Support Foundation of the Chinese PLA General Hospital (No. 2017FC-CXYY-3005 and National Clinical Research Center for Geriatric Diseases, Chinese PLA General Hospital (NCRCG-PLAGH-2019011).

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

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