Research ArticleClinical Studies
Open Access

Interstitial Brachytherapy of the Liver for Renal Cell Carcinoma: ADC Measurements Do Not Predict Overall Survival

MAXIMILIAN THORMANN, FRANZISKA HEITMANN, VANESSA WROBEL, CHRISTINE MARCH, MACIEJ PECH, ALEXEY SUROV, ROBERT DAMM and JAZAN OMARI
In Vivo November 2022, 36 (6) 2945-2951; DOI: https://doi.org/10.21873/invivo.13037

Abstract

Background/Aim: To assess the influence of pre-treatment apparent diffusion coefficient (ADC) measurements on outcomes in patients undergoing interstitial brachytherapy (iBT) for liver metastases from renal cell carcinoma. Patients and Methods: Patients undergoing iBT for renal cell carcinoma (RCC) liver metastases were retrospectively identified. Patients were eligible for inclusion if they had a pre-treatment magnetic resonance imaging (MRI) with diffusion weighted imaging (DWI) sequences. For each lesion, a region of interest (ROI) was placed along the contours of the entire lesion across all slices. For each ROI, ADC minimum, mean and maximum as well as the lesion area were noted, and the average was calculated for each lesion. ADC measurements were correlated with overall survival. Results: The analysis included 17 patients. Median overall survival was 36 months. Neither ADC measurement was significantly associated with overall survival. ADC min (HR=1.00, 95%CI=1.00-1.00, p=0.600), ADC max (HR=1.001, 95%CI=0.998-1.003, p=0.490), ADC mean (HR=0.999, 95%CI=0.996-1.003, p=0.638). Conclusion: ADC is not able to differentiate between groups with good and bad overall survival in patients undergoing iBT for RCC liver metastases.

Key Words:

Renal cell carcinoma (RCC) is the most common type of kidney cancer (1). There are distinct histological subtypes of RCC that vary in their biological and clinical characteristics (2). The most common subtypes are clear cell renal cell carcinomas, papillary carcinomas, and chromophobe carcinomas (3). At presentation, 15% of patients have metastatic disease and almost a third of patients will develop metastases after surgery (4, 5). The most common metastatic sites include the lymph nodes, lung, bone, and liver (6). Tumor stage and histologic subtypes are important predictors of patient outcome and tumor spread to the liver, brain, or pleura is associated with the shortest median overall survival (OS) (2, 7). Despite recent progress in therapy regimens, treatment for metastatic disease remains challenging.

For advanced disease stages, surgical resection, or local treatment of a limited number of metastases may be a reasonable approach. A systematic meta-analysis showed that patients with complete local treatment of RCC metastases showed an OS benefit (8). For patients not eligible for surgical resection, e.g., due to poor performance status, local therapy of liver metastases is a viable option. Treatment methods include radiofrequency ablation, cryotherapy, or interstitial brachytherapy (iBT) (9). Contrary to thermal ablation techniques, computed tomography (CT)- or magnetic resonance (MR)-guided iBT has no technical restrictions regarding lesion size or proximity to critical anatomical structures. IBT is still not widely used but has shown good treatment results in different settings (10, 11).

Patient selection is pivotal in interventional oncology. The Memorial Sloan Kettering risk criteria (MSKRC) provide a prognostic algorithm based on clinical and laboratory parameters. However, reliable imaging biomarkers that have prognostic value in metastatic disease are still warranted. Diffusion weighted imaging (DWI) has been studied as a predictive marker for therapy response in cancer patients (12-17). The literature shows that DWI derived apparent diffusion coefficient (ADC) can reflect cellularity in malignant tumors and therefore, provide important information about tissue composition (18-20). Studies have looked into the role of pretreatment baseline ADC to predict OS, with promising results (15, 21, 22). ADC could thus serve as a non-invasive tool for tumor characterization and treatment response prediction (23, 24).

To the best of our knowledge, the value of DWI has not yet been evaluated in iBT for renal masses. The purpose of this study was to assess the potential prognostic value of baseline ADC measurements in RCC liver metastases treated with iBT regarding OS.

Patients and Methods

Study design. We retrospectively identified 25 patients from our database who received iBT for histologically proven RCC liver metastases between 2008 and 2021 at our institution. Patients were eligible for our analysis if: 1) they had a pretreatment MRI with DWI sequences within 30 days of the procedure, 2) regular follow up data were available. A total of 17 patients were included. Twelve patients were male, 5 were female. A total of 46 metastases were treated. Every case was discussed in a multidisciplinary tumor conference prior to treatment. The decision to perform iBT was taken according to the following criteria: 1. No surgical resection possible or not favored by the attending surgeon; 2. Patient refused surgery; 3. Oligometastatic disease (<5 liver lesions); 4. East Coast Oncology Group (ECOG) performance status 0-1; 5. Adequate laboratory parameters [ALT/AST <2× upper limit of normal (ULN), platelet count >50,000/nl, international normalized ratio (INR) <1.5, partial thromboplastin time <50 s]. There was no upper limit to the maximum lesion diameter.

All patients were seen at our department for follow-up visits every three to six months following therapy. For the purpose of our study, we selected patients with available information on OS and who had received a pre-treatment baseline MRI with DWI and ADC sequences. The study was approved by the local ethics committee. Patient consent was waived due to the retrospective study design.

Prior to iBT, all patients had received surgical resection of the primary tumor, all of which were complete nephrectomies. Eight patients had the primary lesion on the left, and 9 on the right side. Three patients had received prior local therapy [2 selective internal radioembolization (SIRT), 1 RFA]. Median lesion size was 2.9 cm (range=1.3-15 cm). Median radiation dose was 15.9 cm. Patient and treatment characteristics are summarized in Table I.

View this table:
Table I.

Patient characteristics.

Interventional technique. IBT was performed as previously reported (9, 10). All procedures were performed under analgosedation. An Iridium 192 source was inserted percutaneously in the target lesions using CT-fluoroscopy or MR guidance using Seldinger’s technique. The number of catheters used was determined by the size and anatomy of the target lesion. The target reference dose for the clinical target volume (CTV) was 15 Gy. To preserve liver function, no more than 33% of liver parenchyma was exposed to more than 5 Gy (25). After treatment, the puncture tracks were closed with gel foam.

Imaging technique and image analysis. Imaging analysis was performed on DWI and ADC maps acquired from a 1.5 T clinical scanner (Achieva, Philips Healthcare, Best, the Netherlands). Imaging protocol included T2 weighted single-shot and turbo-spin echo sequences with and without fat suppression [repetition time/echo time (TR/TE): 1,600:100]. Contrast-enhanced scans were obtained after administration of Gd-EOB-DTPA (0.1 mmol/kg body weight, Primovist®, Bayer HealthCare, Leverkusen, Germany): dynamic T1 weighted gradient echo sequences in the arterial, portal-venous, and late venous phases as well as hepatobiliary imaging about 20 minutes after contrast application (TR/TE: 4:2) and a axial diffusion-weighted echo-planar imaging sequence [TR/TE: 1,959/59, field of view (FoV): 360×360, matrix 144×142, b factors 0 and 500 s/mm2, flip angle 90]. ADC maps were automatically created. ADC measurements were carried out on Infinitt PACS, Version 3.0 (Infinitt Healthcare, Seoul, Republic of Korea).

MRI analysis was conducted by two experienced radiologists (MT and AS with 3 and 16 years of experience in hepatobiliary MRI, respectively). Both were blinded to the clinical course of the patient. For each patient, a region of interest (ROI) was manually placed on the axial plane along the contours of the entire lesion, avoiding image artefacts (whole lesion method) (Figure 1). A ROI was drawn on each slice containing the tumor lesion, so that multiple axial measurements were done for larger lesions (whole volume method) (Figure 2) (26). For each ROI, ADC minimum, mean, and maximum as well as the lesion area were noted, and the average calculated for each lesion. In addition, the following ratios were calculated: mean measured lesion area per patient divided by the lesion’s ADC min and mean (ADCmean area, ADCmin and ADCmean area, ADCmean).

Figure 1.
Figure 1.

Exemplary depiction of apparent diffusion coefficient (ADC) measurements in a patient with renal cell carcinoma (RCC) liver metastases. A line was drawn manually along the contours of the tumor lesion on each slice. Necrotic areas and T2 shine through artifacts were left out. Minimum, maximum, and mean ADC values were noted for each slice and the average calculated for each lesion.

Figure 2.
Figure 2.

Sketch of apparent diffusion coefficient (ADC) measurement technique. ADC measurements were performed along the contours of the entire tumor lesion (whole lesion method) on each slice (whole volume method). The average ADC value was calculated for each lesion.

Statistical analysis. SPSS Version 26 was used for statistical analysis. For continuous variables, mean and standard deviation were calculated. For ordinal variables, median with range was given. A univariate cox regression analysis was used to assess the impact of baseline variables on patient survival. Tests were two-sided and statistical significance was defined at a p<0.05. All ADC values are given in 10−3 mm2/s. Ratios are given in arbitrary units (AU).

Results

Median overall survival time was 36 months (Figure 3). Twelve patients died during the observation period. At the time of censoring, 5 patients were still alive.

Figure 3.
Figure 3.

Kaplan-Meier curve for overall survival after interstitial brachytherapy for renal cell carcinoma liver metastases. Median overall survival time was 36 months.

Mean measured lesion area was 796.5 cm2 [standard deviation (SD)=1,031.3 cm2]. Mean sum of measured lesion area per patient was 5,364.9 cm2 (SD=8,737.5 cm2). Pretreatment average ADC min was 763.8 cm2 (SD=177.5 cm2), average ADC max 1,663.7 cm2 (SD=346.9 cm2), and average ADC mean 1,086.4 cm2 (SD=270.90 cm2). All ADC measurements are shown in Table II.

View this table:
Table II.

Univariate cox regression analysis.

In univariate analysis, neither ADC measurement was significantly associated with OS: ADC min (HR=1.00, 95%CI=1.00-1.00, p=0.600), ADC max (HR=1.001, 95%CI=0.998-1.003, p=0.490), ADC mean (HR=0.999, 95%CI=0.996-1.003, p=0.638). Combined ADC measurements did not have a significant effect on OS either: ADCmean area, ADCmin (HR=1.401, 95%CI=0.847-2.316, p=0.189), ADCmean area, ADCmean (HR=2.160, 95%CI=0.748-6.240, p=0.155). There was no significant association between mean measured lesion area (HR=1.000, 95%CI=1.00-1.001, p=0.314) or the sum of measured lesion areas with OS (HR=1.00, 95%CI=1.000-1.000, p=0.273).

Discussion

Our study assessed the influence of pretreatment ADC values on OS in patients undergoing iBT for RCC liver metastases. No association between either analyzed ADC parameter and OS was found in our cohort.

It has been shown that ADC is able to display clinically relevant histopathological features of tumor tissue. Studies have found that ADC values are inversely correlated with cellularity of several tumor entities (27, 28). It has also been demonstrated that ADC may successfully differentiate between benign and malignant lesions (29, 30). Other studies have shown associations between ADC values and the marker of cell proliferation Ki-67, Hif-1a, and VEGF (31, 32). The ability of ADC to predict treatment response after chemotherapy has been published for several tumor entities, such as rectal, esophageal, and breast cancers, amongst others (33-35).

Clear cell RCC is the most common type of kidney cancer and responsible for most metastatic diseases from renal malignancies (36). RCC lesions can be characterized based on their DWI-derived ADC value. For example, it has been shown that ADC is able to differentiate between clear-cell and non-clear cell carcinoma (37). DWI can help in the differentiation between benign and malignant lesions and may be able to differentiate low-grade from high-grade RCC (38-40). Available studies have measured ADC in the primary tumor. The literature on the value of ADC measurements in RCC metastases is still scarce. There are yet no studies assessing the performance of ADC in RCC liver metastases before surgery or local ablation techniques.

RCC metastases to the liver generally carry a poor prognosis and most patients are unsuitable for surgical resection (41). While the role of metastasectomy in RCC is inconclusive, resection of liver metastases might lead to benefits in survival after careful patient selection (42). Some evidence suggests that patients with resection of RCC liver metastases show a significantly longer OS (4). However, liver surgery is still associated with a high morbidity and mortality.

Local ablation methods such as radiofrequency ablation, microwave ablation, and interstitial brachytherapy are an emerging treatment arm in liver malignancies. The literature on liver metastasectomy for RCC is still sparse, with the available studies showing comparable results to surgical resection (9, 43, 44). Local ablative therapies might be suitable for patients not amenable to surgical or medical treatments (43). Careful patient selection is mandatory. So far, no prognostic parameters have been established for OS after iBT and – given the sparsity of the literature – no markers have been identified in iBT for RCC liver metastases.

The data from our cohort suggests that ADC may not be used to select patients for iBT in RCC liver metastases. The reason for this remains unclear. Disease dynamics in advanced RCC may have a greater impact on survival than tumor cellularity. Also, as patients allocated to iBT were deemed unsuitable for resection, tumor location may play an important role in clinical course. Further studies will need to assess the impact of clinical and tumor characteristics on survival after iBT in larger cohorts.

We used what we call a whole lesion and whole volume method for ADC measurements in our cohort. While the methods for measuring ADC values are not standardized, we believe that encircling the entire tumor volume is less prone to rater bias than placing a circular ROI in a given target volume. The placement of the ROI and in- or exclusion of cystic or necrotic areas significantly affects ADC values and their performance in predicting patient outcomes (1, 16, 45). It has been shown that whole lesion assessment provides better inter-reader agreement (46). We also believe that our method of whole volume measurements across image slices is able to better capture heterogeneous cellular characteristics of the lesions. The weight of each single slice measurement is lowered by determining the mean value of each of the two ADC parameters (ADC min and mean), potentially lowering rater bias. In order for ADC to become a valuable diagnostic parameter in clinical routine, a consensus on a uniform measurement technique will be needed. We believed that the ratio of mean measured lesion area and average ADC values per lesion might better account for the distinct influences of lesion size and cellularity than either parameter alone. However, we did not find a significant influence of calculated ratios.

Different MR systems and b-values across centers are an additional factor that may influence reproducibility of ADC measurements (47). While there does not seem to be a significant difference for ADC values in commonly used b-values (maximum values of 600 vs. 800 vs. 1,000), ADC values tend to decrease with increasing b-values (1). The b-values used on our scanners are relative low, which increases the weight of tissue perfusion over tissue diffusion (48). Some authors have suggested normalization of ADC measurements, e.g., by using the spleen as a reference organ (49). This might be an interesting approach and warrants further study for RCCs.

There are several limitations to our study. It was a retrospective analysis with data from a single interventional center. Patients were excluded if no baseline MRI with DWI and ADC maps were available, potentially leading to bias. Our sample size was small, limiting the expressive power of our study. However, given the rarity of local ablative treatments in metastatic RCC, especially of iBT, our cohort is one of the largest published so far. While the method of measurement of ADC values is still inconsistent, we applied a whole lesion measurement technique. The effect of the measurement technique on clinical outcome will need to be evaluated.

In conclusion, ADC is not able to differentiate between groups with good and bad OS in patients undergoing iBT for RCC liver metastases. Further studies will need to identify prognostic markers for outcome in this particular patient group.

Footnotes

  • Authors’ Contributions

    FH, VW, MP, CM: acquisition, analysis and interpretation of the data, statistical analysis, drafting and revision of manuscript. AS, RD, JO, MT: development of study concept and design, study supervision, acquisition, analysis and interpretation of the data, statistical analysis, drafting and revision of manuscript. All Authors approved the final version of the manuscript, including the authorship.

  • Conflicts of Interest

    The Authors declare no conflict of interest in relation to this study.

  • Received September 13, 2022.
  • Revision received September 26, 2022.
  • Accepted September 28, 2022.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Interstitial Brachytherapy of the Liver for Renal Cell Carcinoma: ADC Measurements Do Not Predict Overall Survival
MAXIMILIAN THORMANN, FRANZISKA HEITMANN, VANESSA WROBEL, CHRISTINE MARCH, MACIEJ PECH, ALEXEY SUROV, ROBERT DAMM, JAZAN OMARI
In Vivo Nov 2022, 36 (6) 2945-2951; DOI: 10.21873/invivo.13037
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