Abstract
Objectives
Drug-eluting beads transarterial chemoembolization (DEB-TACE) has shown promise as a treatment modality for primary liver cancer and colorectal cancer liver metastasis. However, its role in pancreatic cancer liver metastasis (PCLM) remains uncertain. This study aimed to investigate the efficacy and safety of DEB-TACE in PCLM patients.
Methods
A retrospective study included 10 PCLM patients who underwent DEB-TACE using CalliSpheres® microspheres as the chemoembolization material. Treatment response, survival outcomes, adverse events, and liver function indexes were comprehensively assessed.
Results
Among the patients, complete response, partial response, stable disease, and progressive disease rates were 0.0%, 40.0%, 30.0%, and 30.0%, respectively. The objective response rate was 40.0%, and the disease-control rate was 70.0%. The median progression-free survival (PFS) was 12.0 months (95% CI: 0.0-26.7), with a 1-year PFS rate of 48.0%. The median overall survival (OS) was 18.0 months (95% CI: 6.0-30.0), with a 1-year OS rate of 80.0%. Additionally, no significant differences were observed in any of the liver function indexes, including alanine aminotransferase, aspartate aminotransferase, gamma-glutamyl transpeptidase, etc., between pre- and posttreatment evaluations. Adverse events included pain, grade 1-2 vomiting, fever, and transient liver dysfunction.
Conclusions
DEB-TACE demonstrates a promising treatment response, favorable survival profile, and satisfactory safety in PCLM patients.
Advances in knowledge
This study adds to the current research by providing novel evidence on the efficacy, safety, and favorable survival outcomes of DEB-TACE in treating PCLM, highlighting its potential as an effective therapeutic option in this specific population.
Keywords: pancreatic cancer liver metastasis, drug-eluting beads, transarterial chemoembolization, survival outcomes, efficacy, safety
Introduction
Pancreatic cancer is an aggressive malignancy and a leading cause of cancer-related mortality on a global scale.1,2 Most pancreatic cancer cases are diagnosed at advanced stages, often accompanied by metastasis, with the liver being a commonly affected site.3,4 Despite numerous clinical trials investigating potential treatment modalities for pancreatic cancer liver metastasis (PCLM), no specific recommended treatment has emerged from current guidelines.5–7 Systematic chemotherapy, radiofrequency ablation, and conventional transarterial chemoembolization (cTACE) have shown promise but failed to significantly improve clinical outcomes, resulting in a median overall survival (OS) ranging from 5.77 to 19.00 months.8 Therefore, there is an urgent need to identify effective and safe treatment approaches to improve the prognosis of PCLM. The urgent need to discover effective and safe treatment options for PCLM patients is evident to improve prognosis.
One potential treatment modality that has shown promise in primary liver cancer and liver metastasis is drug-eluting beads transarterial chemoembolization (DEB-TACE). DEB-TACE involves embolizing tumour-feeding arteries in the liver and sustained release of chemotherapeutic drugs, exerting an anti-tumour effect.9–11 By embolizing tumour-feeding arteries in the liver and releasing chemotherapeutic drugs sustainably, DEB-TACE has shown promise in achieving high objective response rates (ORR) and disease control rates (DCR) in other types of metastatic liver cancers.12,13 For instance, the breast cancer patients with liver metastasis treated with DEB-TACE achieved an ORR of 71.4% and a DCR of 92.8% in the third month.12 Similarly, colorectal cancer patients with liver metastasis achieved a median OS of 25.0 months and a 1-year OS rate of 81.0% with DEB-TACE treatment.11 Notably, DEB-TACE has demonstrated an ORR of 82.9% and a DCR of 94.3% without severe complications in gastric cancer liver metastasis cases.13 Although these results are encouraging, limited information exists regarding the effectiveness and safety of DEB-TACE in PCLM patients.
Therefore, the present study aimed to investigate the treatment response, survival outcomes, and safety profile of DEB-TACE in patients with PCLM. By addressing this research gap, we seek to provide valuable insights into the potential of DEB-TACE as an effective and safe treatment option for PCLM patients, ultimately improving their overall prognosis.
Methods
Patients
This retrospective study included 10 PCLM patients who underwent treatment with DEB-TACE between November 2018 and July 2021. The study was conducted at the Department of Integrative Oncology, Fudan University Shanghai Cancer Center, and the Department of Oncology, Shanghai Medical College, Fudan University.
Inclusion criteria
Inclusion criteria included: (1) patients with a confirmed pathological diagnosis of primary pancreatic cancer; (2) patients presenting with liver metastasis as evidenced by clinical evaluation; (3) patients aged 18 years or older; (4) patients who received DEB-TACE as the primary treatment modality; and (5) patients with well-controlled primary lesions but progressive intrahepatic lesions.
Exclusion criteria
Exclusion criteria included: (1) patients for whom clinical data necessary for the study analysis were unavailable and (2) patients with concomitant primary cancers or other malignancies.
Ethics approval
This study obtained approval from the Ethics Committee by institutional guidelines and principles governing research involving human subjects.
Data collection
Data on clinical characteristics were collected for comprehensive analysis in this study. The collected variables included age, gender, pathological type of pancreatic cancer, Eastern Cooperative Oncology Group (ECOG) score, Child-Pugh score (for PCLM patients with coexisting liver cirrhosis), number of liver metastases (with multiple liver metastases defined as the presence of 6 or more liver metastases), size of liver metastases, presence of satellite lesions in liver metastases, blood routine examination results, tumour markers, liver function indexes, and information regarding previous treatments received.
Additionally, follow-up information was diligently recorded, with the final date of follow-up set as August 25, 2021. This meticulous data collection process ensured a thorough evaluation of the patient cohort. It facilitated a comprehensive analysis of treatment response, survival outcomes and safety profiles associated with DEB-TACE in PCLM patients.
Treatment procedure
The DEB-TACE procedures targeted partial intrahepatic lesions in the patients within the digital subtraction angiography room. Following meticulous disinfection, the Seldinger technique punctured the femoral artery. Subsequently, angiography was conducted to identify the tumour-feeding vessel. A 5F RH catheter was then introduced into the street by a super-selective catheterization. Sequentially, the chemoembolization materials consisting of a mixture of 1.0 g of CalliSpheres® microspheres (100-300 μm in diameter, Jiangsu Hengrui Medicine Co., Ltd, China) and 100 mg of irinotecan were slowly injected into the tumour-feeding vessel. The embolization process continued until either the blood flow within the tumour-feeding vessel stagnated or the tumour staining disappeared.
Outcome assessment
At approximately 3 weeks posttreatment, the treatment efficacy of liver metastasis was evaluated by assessing patient response and the response of embolized lesions, employing enhanced computerized tomography by the modified Response Evaluation Criteria in Solid Tumors (mRECIST).14 In addition, liver function indexes were prospectively collected 1 month after DEB-TACE to evaluate the safety of liver metastasis treatment meticulously. Detailed documentation of adverse events post-DEB-TACE treatment was meticulously obtained and graded by the standardized Common Terminology Criteria for Adverse Events (version 5.0). Furthermore, precise calculations for progression-free survival (PFS) and OS were conducted based on the comprehensive follow-up data. PFS was meticulously defined as the accurate duration from the initiation of DEB-TACE to either disease progression or the occurrence of mortality, whichever event transpired first. Conversely, OS was meticulously defined as the duration from DEB-TACE to the unfortunate demise of the patient. Notably, patients who did not experience any events related to PFS or OS during the rigorous analysis were appropriately censored at the date of their final disease assessment.
Statistical analysis
Statistical analysis was performed using SPSS software (v. 22.0, IBM Corp., USA), and GraphPad Prism software (v. 7.01, GraphPad Software Inc., USA) was utilized for constructing graphs. The comparison of liver function indexes before and after treatment was analyzed using the Wilcoxon signed-rank test. Survival analysis was conducted using the Kaplan-Meier curve. A P-value of less than .05 was considered statistically significant.
Results
Clinical characteristics
Among the cohort of 10 patients with PCLM, the mean age was 58.1 ± 9.2 years, with a distribution of 4 (40.0%) females and 6 (60.0%) males. Importantly, all patients exhibited an ECOG score of 0 and a Child-Pugh score of A, indicating favorable overall health status and liver function. Furthermore, the sole metastatic manifestation observed in all patients was liver metastasis, without the presence of other distant metastases. Notably, 7 (70.0%) patients displayed multiple liver metastases, while 3 (30.0%) presented with the satellite lesions associated with liver metastasis. Moreover, regarding the previous treatment history for liver metastasis, 6 (60.0%) patients had received 1 course, 3 (30.0%) patients had undergone 2 courses, and 1 (10.0%) patient had received 3 courses of treatment. Specifically, among the cohort, 7 (70.0%) patients received chemotherapy, 3 (30.0%) patients underwent transarterial chemoembolization), 3 (30.0%) patients underwent surgical resection, 1 (10.0%) patient received arterial infusion chemotherapy, and 1 (10.0%) patient underwent ablation as their respective treatment regimens for liver metastasis (Table 1).
Table 1.
Clinical characteristics.
| Items | PCLM patients (N = 10) |
|---|---|
| Age (years), mean ± SD | 58.1±9.2 |
| Gender, No. (%) | |
| Female | 4 (40.0) |
| Male | 6 (60.0) |
| Pathological type of pancreatic cancer, No. (%) | |
| PDAC | 10 (100.0) |
| ECOG score, No. (%) | |
| 0 | 10 (100.0) |
| Child-Pugh score, No. (%) | |
| A | 10 (100.0) |
| Metastasis, No. (%) | |
| Liver | 10 (100.0) |
| Others | 0 (0.0) |
| Tumour number of liver metastasis, No. (%) | |
| Single | 3 (30.0) |
| Multiple | 7 (70.0) |
| Tumour size of liver metastasis (cm), median (IQR) | 6.0 (5.4-7.8) |
| Satellite lesions of liver metastasis, No. (%) | |
| No | 5 (50.0) |
| Yes | 5 (50.0) |
| Blood routine examination, median (IQR) | |
| WBC (×109/L) | 8.0 (7.0-8.8) |
| GRAN (%) | 64.8 (50.7-73.6) |
| RBC (×1012/L) | 3.8 (3.7-4.3) |
| HGB (g/L) | 118.5 (110.5-139.3) |
| PLT (×1012/L) | 216.0 (173.0-409.3) |
| CRP (mg/L) | 14.2 (4.6-62.6) |
| Tumour markers, median (IQR) | |
| CA19-9 (U/mL) | 1000.0 (537.6-1000.0) |
| CA125 (U/mL) | 130.0 (37.8-702.5) |
| CA15-3 (U/mL) | 41.7 (16.8-103.2) |
| CA72-4 (U/mL) | 20.4 (8.2-53.0) |
| CA50 (U/mL) | 500.0 (276.4-500.0) |
| CA242 (U/mL) | 200.0 (29.2-200.0) |
| AFP (ng/mL) | 3.5 (3.0-4.8) |
| CEA (ng/mL) | 58.9 (29.9-76.1) |
| C-pep (ng/mL) | 1.6 (1.2-2.4) |
| Insulin (μU/mL) | 263.0 (143.8-631.1) |
| NSE (U/mL) | 18.6 (16.1-25.9) |
| Times of previous treatment for liver metastasis, No. (%) | |
| 1 | 6 (60.0) |
| 2 | 3 (30.0) |
| 3 | 1 (10.0) |
| Regimens of previous treatment for liver metastasis, No. (%) | |
| Chemotherapy | 7 (70.0) |
| TACE | 3 (30.0) |
| Surgical resection | 3 (30.0) |
| Arterial infusion chemotherapy | 1 (10.0) |
| Ablation | 1 (10.0) |
Abbreviations: AFP = alpha fetoprotein; CA = cancer antigen; CEA = carcinoma embryonic antigen; C-pep = C-peptide; CRP = C-reactive protein; ECOG = Eastern Cooperative Oncology Group; GRAN = granulocytes; HGB = hemoglobin; IQR = interquartile range; NSE = neuron-specific enolase; PCLM = pancreatic cancer liver metastasis; PDAC = pancreatic ductal adenocarcinoma; PLT = platelets; RBC = red blood cells; SD = standard deviation; TACE = transcatheter arterial chemoembolization; WBC = white blood cells.
Treatment response assessment and efficacy evaluation
To comprehensively evaluate the treatment efficacy, both the response of embolized lesions and patients were meticulously assessed by mRECIST criteria,15 as delineated in Table 2. The observed rates of complete response (CR), partial response (PR), stable disease (SD), and progressive disease (PD) for embolized lesions were determined to be 20.0%, 40.0%, 40.0%, and 0.0%, respectively. This lesion-specific assessment allows for a nuanced understanding of the treatment's impact on individual tumour sites. Consequently, an ORR of 60.0% and a DCR of 100.0% were obtained.
Table 2.
Treatment efficacy by mRECIST criteria.
| Items, No. (%) | Patients | Embolized lesions |
|---|---|---|
| Overall response | ||
| CR | 0 (0.0) | 2 (20.0) |
| PR | 4 (40.0) | 4 (40.0) |
| SD | 3 (30.0) | 4 (40.0) |
| PD | 3 (30.0) | 0 (0.0) |
| ORR (CR + PR) | 4 (40.0) | 6 (60.0) |
| DCR (CR + PR + SD) | 7 (70.0) | 10 (100.0) |
Abbreviations: CR = complete response; DCR = disease-control rate; mRECIST = modified Response Evaluation Criteria in Solid Tumors; ORR = objective response rate; PD = progressive disease; PR = partial response; SD = stable disease.
This lesion-specific assessment allows for a nuanced understanding of the treatment's impact on individual tumour sites. A detailed analysis revealed that out of the total cohort, none (0.0%), 4 (40.0%), 3 (30.0%), and 3 (30.0%) patients achieved CR, PR, SD, and PD, respectively. The ORR was calculated as 40.0%. Furthermore, the DCR was determined to be 70.0%. This difference in patient-level response versus embolized lesion-level response may occur because patients often have multiple lesions with varying responses to treatment. Notably, within the subset of patients exhibiting a response of SD in their embolized lesions, their overall treatment response was classified as PD.
Survival analysis and clinical outcomes
The survival profile of patients was meticulously examined, and pertinent data were derived from comprehensive follow-up assessments. The resultant analysis yielded crucial information regarding both PFS and OS, providing valuable insights into the long-term prognosis of the patient cohort.
Regarding PFS, the median PFS, accompanied by its corresponding 95% CI, was determined to be 12.0 (0.0-26.7) months, reflecting the average disease control duration in the patient population. Furthermore, the 1-year PFS rate was 48.0%, underscoring a significant proportion of patients experiencing sustained disease stability for at least 1 year (Figure 1A).
Figure 1.
The survival profile of patients. (A) The progression-free survival (PFS) of patients. (B) The overall survival rate (OS) of patients.
The median OS, along with its corresponding 95% CI, was calculated to be 18.0 (6.0-30.0) months, signifying the average survival duration from the initiation of treatment. Additionally, the 1-year OS rate was determined to be 80.0%, illustrating a notable proportion of patients achieving 1-year survival milestones (Figure 1B).
Safety profile and treatment outcomes
To comprehensively evaluate the safety profile of DEB-TACE, a meticulous assessment of liver function indexes was performed both before and 1 month after the DEB-TACE procedure. Notably, no statistically significant differences were observed in any of the measured liver function indexes before the patients accepted DEB-TACE therapy, including alanine aminotransferase (ALT), aspartate aminotransferase (AST), gamma-glutamyl transpeptidase, total protein, albumin, total bilirubin, direct bilirubin, and indirect bilirubin, between the pretreatment and posttreatment measurements (all P > .05) (Table 3). This finding underscores the absence of discernible detrimental effects on liver function resulting from DEB-TACE intervention. Regarding adverse events, pain was the most reported event experienced by all patients (10, 100.0%). Notably, 9 (90.0%) of these patients reported pain of grade 3-4 intensity, indicating moderate-to-severe discomfort. Additionally, after DEB-TACE treatment, vomiting, fever, and liver dysfunction were observed in 3 (30.0%), 1 (10.0%), and 1 (10.0%) patients, respectively; however, these events were all categorized as grade 1-2, indicative of mild to moderate severity (Table 4 and Table S1). These findings collectively suggest that adverse events associated with DEB-TACE were generally manageable and did not pose significant clinical concerns.
Table 3.
Liver function indexes.
| Items | Before treatment | After treatment | P value |
|---|---|---|---|
| ALT (U/L) | 39.1 (22.7-55.8) | 31.2 (15.6-44.0) | .097 |
| AST (U/L) | 26.5 (20.2-49.1) | 27.2 (20.6-35.6) | .515 |
| GGT (U/L) | 97.5 (61.3-251.8) | 307.5 (197.3-446.8) | .374 |
| TP (g/L) | 71.6 (67.7-74.2) | 72.2 (66.0-81.9) | .515 |
| ALB (g/L) | 43.6 (37.7-44.7) | 37.8 (35.7-39.7) | .066 |
| TBIL (μmol/L) | 10.1 (8.2-17.5) | 8.9 (5.0-12.3) | .093 |
| DBIL (μmol/L) | 4.2 (3.3-7.7) | 5.1 (2.3-8.5) | .575 |
| IBIL (μmol/L) | 5.0 (4.5-8.5) | 3.3 (2.8-4.7) | .069 |
Abbreviations: ALB = albumin; ALT = alanine aminotransferase; AST = aspartate aminotransferase; DBIL = direct bilirubin; GGT = gamma-glutamyl transpeptidase; IBIL = indirect bilirubin; TBIL = total bilirubin; TP = total protein.
Table 4.
Key characteristics and treatment outcomes of each patient.
| No. | Age (years) | Gender | Primary cancer | Liver metastasis | ECOG score | Child-Pugh score | Liver metastasis number | Liver metastasis size (cm) | Satellite lesions | Treatment response |
Patients’ progression | PFS (months) | Patients’ death | OS (months) | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| (3 weeks after treatment) | |||||||||||||||
| Patients | Embolized lesion | ||||||||||||||
| 1 | 56 | Male | PDAC | Yes | 0 | A | Single | 5.3 | No | PR | CR | No | 13 | Yes | 19 |
| 2 | 54 | Female | PDAC | Yes | 0 | A | Multiple | 5.4 | No | PR | CR | No | 17 | No | 17 |
| 3 | 38 | Female | PDAC | Yes | 0 | A | Multiple | 6.4 | Yes | SD | PR | Yes | 2 | Yes | 5 |
| 4 | 53 | Male | PDAC | Yes | 0 | A | Multiple | 8.5 | No | SD | PR | No | 11 | No | 11 |
| 5 | 57 | Female | PDAC | Yes | 0 | A | Multiple | 4 | No | SD | SD | Yes | 13 | Yes | 13 |
| 6 | 73 | Male | PDAC | Yes | 0 | A | Multiple | 6 | Yes | PR | PR | Yes | 12 | Yes | 18 |
| 7 | 63 | Male | PDAC | Yes | 0 | A | Multiple | 6 | Yes | PD | SD | Yes | 1 | Yes | 6 |
| 8 | 64 | Male | PDAC | Yes | 0 | A | Multiple | 6 | No | PR | PR | No | 23 | No | 23 |
| 9 | 64 | Female | PDAC | Yes | 0 | A | Single | 9.5 | Yes | PD | SD | Yes | 1 | Yes | 32 |
| 10 | 59 | Male | PDAC | Yes | 0 | A | Single | 7.6 | Yes | PD | SD | Yes | 1 | Yes | 3 |
Abbreviations: CR = complete response; ECOG = Eastern Cooperative Oncology Group; OS = overall survival; PDAC = pancreatic ductal adenocarcinoma; PFS = progression-free survival; PR = partial response; PD = progressive disease; SD = stable disease.
Discussion
The treatment response and survival outcomes in patients with pancreatic cancer liver metastases (PCLM) are critical considerations in clinical practice. Previous studies have reported varying treatment response rates for different therapeutic approaches. For instance, the ORR was reported to be 11.6% in patients undergoing cTACE,16 while a separate study demonstrated an ORR of 25.8% for intrahepatic lesions in PCLM patients receiving chemotherapy.6 However, the available data on the treatment response specifically for PCLM patients undergoing DEB-TACE remain limited.
Our current study observed an ORR and DCR of 40.0% and 70.0%, respectively, in PCLM patients treated with DEB-TACE. Notably, the ORR and DCR for embolized lesions were 60.0% and 100.0%, respectively. This enhanced response to DEB-TACE may be attributed to its ability to selectively embolize tumour-feeding arteries and sustain the release of chemotherapeutic drugs at a stable dose. Consequently, this sustained drug release leads to an elevated local concentration of chemotherapy agents, resulting in a promising treatment response among PCLM patients.17
Survival outcomes remain a critical endpoint in the management of PCLM patients. Previous studies have reported varying median OS rates for different treatment modalities. For example, thermal ablation therapy combined with chemotherapy achieved a median OS of 8.17 months, while chemotherapy alone resulted in a median OS of 5.77 months in PCLM patients.5 Additionally, hepatic artery infusion combined with chemotherapy demonstrated a median OS of 14.0 months in this patient population.6 Furthermore, cTACE achieved a 1-year OS rate of 60.0% among PCLM patients.16 In our study, we observed a median PFS of 12.0 months with a 1-year PFS rate of 48.0%, as well as a median OS of 18.0 months with a 1-year OS rate of 80.0% in PCLM patients treated with DEB-TACE. These results demonstrate higher survival rates than previous studies.5,6,16 The favorable survival profile associated with DEB-TACE may be attributed to several potential factors. First, DEB-TACE exhibited a favorable treatment response, as previously discussed, which likely contributed to prolonged survival among PCLM patients. Second, DEB-TACE may possess inherent anti-tumour properties by inhibiting tumour growth, angiogenesis, and metastasis, leading to a more favorable survival profile.18
Assessing the safety profile of DEB-TACE is crucial for effectively managing primary liver cancer and metastasis patients. Previous studies have reported manageable adverse events associated with DEB-TACE, such as mild pain and fever among patients with massive liver cancer.19 Liver function indexes, including ALT and AST, were found to be temporarily elevated at 4 days posttreatment but returned to normal levels by day 7. Moreover, no significant changes were observed in albumin and total bilirubin levels among patients with colorectal cancer liver metastases treated with DEB-TACE.11 In patients with gastric cancer liver metastases, DEB-TACE was associated with only tolerable nausea, vomiting, and no severe complications.13 Consistent with previous studies,11,13,19 our study found no significant differences in liver function indexes between PCLM patients before and after DEB-TACE. Mild adverse events, including vomiting, fever, and manageable liver dysfunction, as well as controllable pain, were reported among patients. These findings may be attributed to the localized delivery of loaded chemotherapeutic drugs directly into the target tumour, minimizing systemic toxicity.19–21 Therefore, DEB-TACE demonstrated a satisfactory safety profile among PCLM patients. Additionally, previous studies have reported similar adverse events, such as controllable fever, pain, and nausea, associated with cTACE, further supporting the safety profile of DEB-TACE observed in our study.22,23
Despite the promising results obtained, it is crucial to acknowledge the limitations of our study. First, our study employed a single-arm design, and therefore, future randomized controlled trials are necessary to comprehensively explore the efficacy and safety of DEB-TACE in PCLM patients. Additionally, it is important to note that all the PCLM patients included in our study had undergone prior treatments, which might have impacted the observed outcomes. Furthermore, the retrospective nature of our study and its relatively small sample size should be carefully considered when interpreting the findings.
In conclusion, our study underscores the potential of DEB-TACE as a viable local treatment modality, evident by its favorable treatment response, extended survival outcomes, and manageable adverse events among PCLM patients. These findings hold significant implications for optimizing the management and prognostication of PCLM patients. Nevertheless, further investigations encompassing larger-scale randomized controlled trials are imperative to corroborate the effectiveness and safety of DEB-TACE in this specific patient cohort. Such studies would furnish more comprehensive and robust evidence, ultimately facilitating the seamless integration of DEB-TACE into routine clinical practice for managing PCLM patients.
Supplementary Material
Contributor Information
Zhouyu Ning, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Ying Zhu, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Lin Xie, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Xia Yan, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Yongqiang Hua, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Zhiqiang Meng, Department of Integrative Oncology, Fudan University Shanghai Cancer Center, Shanghai 200032, China; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China.
Author contributions
Z. Ning and Y. Zhu should be considered the joint first authors.
Supplementary material
Supplementary material is available at BJR online.
Funding
Funding for this work was provided by the National Natural Science Foundation of China (award number 81820108032).
Conflicts of interest
No competing financial interests are declared by the authors.
Ethics approval statement
The present study was approved by the Fudan University Shanghai Cancer Center Institutional Review Board. Informed patient consent was obtained at hospital admission.
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