Accuracy of Contrast-Enhanced Ultrasound for Hepatocellular Carcinoma post Transcatheter Arterial Chemoembolization

doi:10.21203/rs.3.rs-4681673/v1

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Accuracy of Contrast-Enhanced Ultrasound for Hepatocellular Carcinoma post Transcatheter Arterial Chemoembolization

https://doi.org/10.21203/rs.3.rs-4681673/v1

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Purpose

This prospective pilot study was performed to evaluate non-inferiority between CEUS and the clinical gold standard of CECT/MRI in patients with HCC following TACE in a United States population using Lumason® contrast agent and Liver Reporting and Data System (LIRADS).

Methods

Following institutional review board protocols, adult patients with a first-time diagnosis of HCC were identified and consented for inclusion. Follow-up CT/MRI was directed by referring clinicians and CEUS was performed on the same day. CEUS evaluated for treated lesion(s), any new lesion(s), and portal vein thrombus before and after Lumason®. Any subsequent follow-up imaging was reviewed.

Results

In the 26 enrolled patients, 33 target lesions were identified, size ranging between 0.9 and 16.8 cm (mean 3 cm); 26 were LIRADS-5 or -M. CEUS identified 19 cases of residual tumor, 12 with no viable disease; while CT/MRI identified 17 cases of residual tumor, 16 with no viable disease (p = 0.617). Both CEUS and CT/MRI identified 5 portal vein thrombi, 2 lesions were missed or miscategorized on CEUS, while 6 were missed or miscategorized on CT/MRI (p = 0.289). Six new lesions were identified on both CEUS and CT/MRI ranging between 0.7 and 3.3 cm (mean 1.6 cm) on CEUS, and 0.7 and 2.8 cm (mean 1.7 cm) on CT/MRI. Of these new lesions, 4 were identified only on CT/MRI and 3 only by CEUS. Post-TACE, there was no significant difference in detecting residual tumor and no viable tumor between CEUS and CT/MRI (p = 0.617).

Conclusion

CEUS is non-inferior to CT/MRI performed at identical follow-up interval, in evaluating for residual versus treated HCC following first-time TACE. CEUS may represent an option for patients with contrast allergies or contraindications to MRI. CEUS can be used to examine small or isoechoic tumors after treatment.

Contrast-enhanced ultrasound (CEUS) has been in use globally for decades, but it has only more recently been approved for clinical use in the United States. The accuracy of CEUS is similar to MRI and CT scans in establishing the diagnosis of hepatocellular carcinoma (HCC) in at risk-patients, with guidelines established for non-invasive diagnosis by the American College of Radiology [1–3].

A common treatment for HCC is transcatheter arterial chemoembolization (TACE), which results in focal tumoral necrosis through catheter delivery of embolic and/or chemotherapeutic agents through the tumor arterial supply. Generally, 4-phase CT or dynamic MRI are performed 4–6 weeks after treatment to determine if the tumor is completely or partially treated, based on the recommendations of the Society of Interventional Radiology [4]. This time was established to allow the differentiation of peripheral viable tumors from inflammatory peritumoral infiltration since the elimination of lipiodol by Kupffer cell-mediated phagocytosis requires 3 to 4 weeks [5].

CEUS has many benefits over CT and MRI, including a lack of radiation, they are not-nephrotoxic, decreased cost, and overall accessibility – both availability of appointments, and patient tolerance to the examination (i.e. breath-holds, claustrophobia) [3, 6]. Intrinsically, ultrasound has high spatial resolution and has a potential for identifying residual or recurrent tumor at the same rates and potentially even earlier than a CT scan, where ethiodol can obscure subtle signs of residual tumor [7]. CEUS may also be useful in the event of a contrast shortage, in patients with allergies, or contra-indications to sedation. This would provide an additional imaging option to ensure that HCC patients are triaged appropriately and potentially decrease morbidity with a safe, accurate, and less expensive bridge to liver transplantation.

Although there are multiple case reports demonstrating the diagnostic equivalence of CEUS with CT/MRI for detecting HCC recurrence post TACE, there are limited studies performed in the United States (U.S.) using the purely intravascular (blood pool) contrast agent Lumason® ([Bracco Diagnostics], known as SonoVue [Bracco] outside of the U.S.) [8–15]. Several of the studies are at least a decade old, and many of the studies included small sample sizes, non-standard imaging timeframe after TACE, or variable definitions of residual tumor [9, 12, 15–17]. These results may not be generalizable to the U.S. patient population, since many of the prospective studies examined patient populations outside of the U.S., where most common etiology of HCC may differ from the U.S. population [13, 14].

In the U.S. patient population, there have been more recent case reports and small prospective studies, whose goals were to evaluate diagnostic accuracy in 15 patients at different time intervals post TACE, and to evaluate quantitative response in 17 patients at different post treatment intervals [18–20]. Thus, there is a need for additional, prospective, blinded studies utilizing Lumason® in the U.S. population, where most cases of HCC and cirrhosis are from non-hepatitis B risk factors, including alcohol related liver disease and metabolic dysfunction associated steatotic liver disease.

This prospective pilot study was performed to evaluate non-inferiority between CEUS and the clinical gold standard of CECT/MRI in patients with HCC following TACE treatments in a U.S. population using Lumason® contrast agent and Liver Reporting and Data System (LIRADS).

This single-institution, prospective study was approved by the Institutional Review Board. Adult patients (> 18 years of age) who received a first-time diagnosis of HCC and ≤3 lesions to be treated from December 2020 to May 2022 were enrolled. Exclusion criteria included previously treated HCC, pregnant patients, pediatric patients, or patients who were unable to consent. At our institution, all TACE orders are reviewed by a single interventional radiologist and patients appropriate for inclusion were identified at that time. Patients consented for inclusion in the study at the time of their TACE. They were instructed that they could withdraw at any time from the study and their involvement would not affect their treatment otherwise.

The clinician referring the patient for TACE also directed their follow-up CT/MRI timing to evaluate for residual tumor. During CT/MRI scheduling, patients were also scheduled for CEUS at the same visit as CT/MRI. The CEUS consisted of grayscale and color Doppler imaging looking for treated lesion(s), for any new lesion(s), and for portal vein thrombus. Lumason® (sulfur hexafluoride lipid-type A microspheres) was then administered intravenously (1 mL dose) to evaluate for residual tumor, and to characterize any new focal findings. The results of the CEUS were part of the study and not available to clinicians, who acted only upon the results of their ordered CT/MRI.

Utilizing Research Electronic Data Capture (REDCap), a secure web application for building and managing databases, patient demographics and etiology of cirrhosis were recorded, as was the number and size of the initial tumor diagnosed on CT/MRI.

Two radiologists (an abdominal fellowship trained radiologist with 9 years of clinical experience and a radiology fellow) reviewed the CEUS images on a later date and were able to view the initial, presenting imaging. However, they were blinded to the same-day post-treatment CT/MRI images and reports.

Presence or absence of residual tumor (LIRADS – treated versus viable) was recorded for CEUS, as well as the echogenicity of the lesion, and presence of any limitations. If new lesions were present, LIRADS category was assigned [1]. Portal vein patency or thrombus was recorded and if present, characterized as bland or tumoral. Viability after TACE was defined as arterial phase mass-like or nodular enhancement within a treated lesion. In contrast, non-viability was defined as no enhancement within a treated lesion. Thin, regular peripheral enhancement was not counted as viable, but was labeled as “post-treatment inflammatory rim-enhancement.”

The official reports of the corresponding post treatment CT or MRI performed that same day were mined for presence of absence of residual tumor, new lesions, portal vein thrombus, and evaluation for extrahepatic findings such as metastatic disease.

If the patient returned for additional interval follow-up imaging or for treatment of residual disease, the imaging reports were mined for the above data to serve as a tiebreaker if the CEUS interpretation and same-day CT/MRI report were discordant.

Statistical methods

Patient demographics and main clinical characteristics were summarized using descriptive statistics. To compare the results by CEUS vs CT/MRI, we used McNemar’s test for binary outcomes (such as whether or not residual tumor was identified) and paired-sample t-test for quantitative outcomes (such as the size of tumor). All analyses were performed using statistical software R version 4.4.0 (R Foundation for Statistical Computing, Vienna, Austria). All tests were two-sided, and the statistical significance level used was 0.05. Due to the exploratory nature of this study the significance level was not adjusted for multiple testing.

Demographics

Twenty-six patients were enrolled (19 male and 7 female) with a mean age of 66.6 years and mean BMI of 30.5. Most patients identified as white (84.6%), with the remaining patients identified as black (7.7%) or other (7.7%). Primary etiologies of cirrhosis included viral hepatitis C infection (n = 14, 53.8%), metabolic dysfunction associated steatotic liver disease (n = 6, 23.1%), and alcohol associated cirrhosis (n = 5, 19.2%). A total of 33 target lesions were identified from the initial imaging, size ranging between 0.9 cm and 16.8 cm (mean of 3 cm +/- 2.8 cm); 26 of these were characterized as LIRADS 5 or M on pre-procedural imaging. Additional lesions were diagnosed as HCC by biopsy.

Post-TACE Lesion Characteristics

CEUS identified 19 cases of residual tumor (61.3%) and 12 cases with no viable disease. Two lesions were not visualized on follow up CEUS, CT, or MRI, when compared to the pre-TACE imaging, which were concordant. CT/MRI identified 17 cases of residual tumor (51.5%) and 16 with no viable disease (48.5%), p = 0.617. Both CEUS and CT/MRI identified the same number of portal vein thrombi (n = 5) with results summarized in Table 1.

Table 1 Summary of lesion observations post TACE for both modalities. Thirty-three pre-treatment lesions were present, 2 of which were not visible by CEUS or CT/MRI, though overall more lesions were identified on CT/MRI than on CEUS.

	LIRADS treated	LIRADS viable	Lesion not visible	New lesion	Portal vein thrombus
CEUS	12 (38.7%)	19 (61.3%)	4	6	5
CT/MRI	16 (48.5%)	17 (51.5%)	3	6	5

Nine discordant lesions were present (Table 2). Two lesions were not visible on CEUS (6.7%) that were seen on CT/MRI. Six lesions were missed or miscategorized on CT/MRI (20%), which was not significantly different (p = 0.289). A total of 6 new lesions were identified on both CEUS and CT/MRI, ranging between 0.7 cm and 3.3 cm (mean 1.6 cm +/- 1 cm) on CEUS and 0.7 cm and 2.8 cm (mean 1.7 cm +/- 0.8 cm) on CT/MRI. However, of these new lesions, 4 were identified only on CT/MRI and 3 only by CEUS. Two target lesions (both of whom had more than one target lesion) were not seen by CEUS or CT.

Table 2

Discordant lesion summary (n = 9). Correct modality was determined by follow-up imaging results. Two lesions noted as discordant, are compared to the initial pre-imaging (8 and 9), otherwise, discordancy was between follow-up imaging.
Subject #	Correct modality	Target lesion or new lesion	LI-RADS	Additional information
1	CT	New	LR-4	CEUS showed new lesion LR-3. Follow-up CT the lesion progressed to LR-5
2	CT	New	LR-5	US did not identify new lesion
3	CT	New	LR-3	US did not see new lesion, progressed to LR-4 on follow-up
4	CT	Target	LR-treated	CEUS called residual tumor (Fig. 1), follow-up CT confirmed treated tumor
5	CT	Target	LR-treated	US was unable to see the target tumor at all
6	CEUS	Target	LR-viable	CT missed subtle disease at the periphery of the treated HCC (Fig. 3)
7	CEUS	Target	LR-treated	CT called residual tumor, follow-up CT showed the area was perfusional, not disease (Fig. 2)
8	Other	Target	Not seen	One of 2 target lesions was not seen on CEUS, CT, or follow-up CT
9	Other	Target	Not seen	One of 2 target lesions was not seen on CEUS, CT, or follow-up CT

When able to be determined, grayscale echogenicity of the lesions after TACE, included 10 hyperechoic lesions (33.3%), while 8 were isoechoic (26.7%), 7 were heterogeneous (23.3%), and 5 were hypoechoic (16.7%) (Table 3). Echogenicities were similar between treated tumors and those with residual disease, apart from hyperechoic lesions. Of the incompletely treated lesions, 8 of these were hyperechoic, while only 2 completely treated tumors were hyperechoic. Despite the trend, there was no statistically significant association between pre-contrast echogenicity and residual disease (p = 0.2870).

Table 3

Echogenicity of target lesions after TACE treatment as observed on grayscale ultrasound, prior to contrast administration.
Grayscale echogenicity of tumor after TACE	LIRADS - viable (n = 19)	LIRADS – treated (n = 11)
Hypoechoic	4 (21%)	1 (9%)
Isoechoic	3 (16%)	5 (45%)
Hyperechoic	8 (42%)	2 (18%)
Heterogeneous (mixed)	4 (21%)	3 (27%)

In this prospective pilot study (NCT04569799), CEUS and the clinical gold standard of CECT/MRI were evaluated for non-inferiority in patients with HCC following TACE treatments in a U.S. population using Lumason® contrast agent. Results of this study indicate that overall accuracies are comparable between CEUS and CT/MRI, demonstrating CEUS non-inferiority in evaluating residual HCC after TACE. All modalities identified residual tumors and portal vein thrombus with comparable accuracy.

Recently, Savsani et. al. published a larger multi-institutional prospective trial evaluating CEUS accuracy after TACE using the contrast agent Definity® (perflutren lipid microsphere).[21] They found that CEUS performed 4 to 6 weeks after TACE had a sensitivity higher than CT or MRI for detection of residual tumor, though with lower specificity. Unlike much of the previously existing literature that used variable and earlier time frames, our trial evaluated treatment response in a standard post treatment time frame of around 4 weeks post TACE, though ours with a smaller number of patients than that in the study by Savsani et al [16, 17]. Approximately half of patients in Savsani et al.’s study (n = 89) were imaged at 4 weeks.

Our study also found that CEUS was non-inferior to CT/MRI and was useful in identifying subtle residual tumor. In our study however, all patients were included without preceding knowledge of whether the lesion was sonographically visible on CEUS. This may be more akin to real world practice and allows inclusion of isoechoic lesions, in which comprised 26.7% of our cohort. Additionally, our study evaluated for the presence of portal venous thrombosis in CEUS compared with CT/MRI, allowed for inclusion of more than one lesion, evaluated for new lesions and was performed the same day as the CT/MRI.

Additionally, our study included smaller lesions. While the study by Savsani et al. does not list the average size pre-treatment, their treated lesion size was 3.8 cm, presumed from the CT/MRI, whereas our post treatment average size was only 2.3 cm for target lesions. Our study adds to the study by Savsani et al. and suggests that CEUS need not be limited to patients with only one lesion or only with larger lesions.

Some new lesions were seen only on CT/MRI, and some only on CEUS. On follow-up only one new tumor was missed (LR-5 on CT), whereas in two cases CEUS had a lower LIRADS score than CT for new lesions. For target lesions, only in one patient could the lesion not be seen on CEUS but was present on CT. Limitations to CEUS are the same as those in grayscale ultrasound: lesions may be obscured if they are obscured by body habitus or steatosis. Finally, CEUS overcalled one case as residual disease due to vague internal enhancement (Fig. 1), which was not seen on initial or 3-month CT follow-up.

CEUS excelled in differentiating adjacent perfusional change from residual tumor (Fig. 2) and small residual tumoral enhancement from completely treated disease in cases where Ethiodol presence likely masked the subtle enhancement (Fig. 3). This is concordant with Savsani et al. findings of CEUS’ utility prior to the expected complete resorption of ethiodol before the established 4 to 6-week timeframe.

Extrahepatic disease is unlikely to be diagnosed by CEUS, unless it is locoregional and seen on grayscale evaluation. While our study did not find that CEUS missed any extrahepatic findings, the sample size was small and did not include any patient with metastatic disease at follow-up.

While not statistically significant, the pre-contrast echogenicity of treated lesions may represent an area for future investigation and provide useful information to target Doppler and microvascular imaging (when available). Treated lesion pre-contrast echogenicity may also assist in targeting for CEUS and add diagnostic certainty of CEUS. Since HCC is often hypoechoic on initial diagnosis, it was not surprising that most of our cases with hypoechoic residual lesions represented viable residual disease. While we anticipated that echogenic lesions may represent successfully treated lesions given the presumed presence of retained ethiodol, we instead found more cases of viable tumor were present than not in these lesions (Table 3) [22]. Perhaps not a surprising result in heterogeneous lesions (both hyper-and hypoechoic) where the viable/non-viable split was nearly equal, the hyperechoic results were less expected. Lastly, isoechoic residual disease is the most difficult to detect on follow up grayscale ultrasound, necessitating a firm understanding of where the initial disease presented on pretreatment images as 16% of cases were mostly isoechoic yet still viable tumor.

There were several limitations to this study including the limited statistical power associated with a small sample size. For clinical adoption, there is a learning curve associated with the interpretation of post-TACE CEUS images, to help radiologists recognize and differentiate residual tumor versus post-inflammatory, smooth peripheral enhancement.

In conclusion, overall accuracies are comparable between CEUS and the gold standard CT/MRI, demonstrating CEUS non-inferiority in evaluating residual HCC after TACE. All modalities are comparable in identifying residual tumors and portal vein thrombus. CEUS may represent an option for patient with contrast allergies or who have contraindications to MRI such as claustrophobia. CEUS also may be beneficial in patient with a prognostically shortened lifespan or awaiting transplant, who require limited imaging for tumor viability or recurrence. In addition to the population in the study by Savsani et al, CEUS can also be considered as an alternate modality in patients where the lesion is isoechoic, small, and in cases with more than one lesion and CEUS remains accurate in assessment for portal vein thrombus.

Author Contribution

K.M., P.W., N.Y., and K.K. originated the concept. K.M. and W.P. collected the data.N.Y. Wrote the abstract. K.M. and W.P. wrote the main manuscript text. K.M. prepared the tables. K.M. and W.P. prepared the figures. J.Z. performed the statistical analysis. All authors reviewed and modified the manuscript.

Acknowledgement

Rebecca Jordan, study coordinator

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No competing interests reported.

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Accuracy of Contrast-Enhanced Ultrasound for Hepatocellular Carcinoma post Transcatheter Arterial Chemoembolization

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Abstract

Purpose

Methods

Results

Conclusion

Figures

INTRODUCTION

METHODS

Statistical methods

RESULTS

Demographics

Post-TACE Lesion Characteristics

DISCUSSION

Declarations

Author Contribution

Acknowledgement

References

Additional Declarations

Status:

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