Occult Liver Nodules: their Detection and Characterization with CEUS

doi:10.21203/rs.3.rs-5000257/v1

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Occult Liver Nodules: their Detection and Characterization with CEUS

https://doi.org/10.21203/rs.3.rs-5000257/v1

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Objectives

Contrast enhanced ultrasound (CEUS) now joins the ranks of CT and MRI for noninvasive diagnosis of hepatocellular carcinoma (HCC). CEUS LI-RADS provides greater than 95% specificity for diagnosis within LR-5. Unlike CT/MRI, CEUS is nodule based. Currently, LI-RADS does not recommend CEUS of nodules occult or invisible on pre-contrast ultrasound except by experts. This study addresses our ability to find occult nodules using CEUS and characterize them with CEUS LI-RADS.

Methods

100 patients at risk for HCC, 81 with cirrhosis, with occult lesions were retrospectively identified from our archived patient logs. All patients had CEUS examination. Three specialized CEUS techniques (blindshot injection, portal venous (PVP) sweep of the liver, and on-top injection) are used to evaluate nodules.

Results

There were 114 occult lesions in 100 patients. The origin of 78(68%) lesions was an MRI (n = 69) or CT scan (n = 9) with an observation of abnormal enhancement, generally arterial phase hyperenhancement (APHE). All these patients had blindshot CEUS injection looking for a correlate with APHE. The remainder of occult lesions (n = 36)(32%) were first detected during CEUS, generally as washout foci on PVP sweeps or incidental APHE or washout nearby other targets. All washout areas had subsequent on-top injection to assess for APHE. Application of CEUS LI-RADS algorithm categorized 26 LR-5, 34 LR-4, and 5 LR-M. CEUS upgraded LI-RADS category of 24/50(48%) occult lesions reported on CT/MRI. 29(25%) occult lesions were offered treatment and from categories LR-5 and LR-M, 5 had biopsy confirmation and 15 were treated. From both sources, MR/CT and CEUS, there were 12 occult lesions scanned for treatment response, categorized as 7 LR-TR viable, 1 LR-TR nonviable, and 4 LR-TR equivocal on CEUS.

Conclusion

Our study shows we can find and characterize occult nodules using CEUS techniques and CEUS LI-RADS algorithm, with positive impact on clinical management.

Liver cancer is the third leading cause of cancer death worldwide in 2020 [1]. Associated mortality is projected to grow globally to an estimated 1.3 million deaths annually by 2040 [2]. Hepatocellular carcinoma (HCC) accounts for the majority of liver cancer cases [3] and primarily occurs in the setting of chronic liver disease.

In our center, magnetic resonance (MR), computed tomography (CT), and contrast-enhanced ultrasound (CEUS) are routinely used for liver surveillance and HCC diagnosis. However, radiation exposure remains a concern with multiphase CT and accessibility and cost influence choice of MR. Contrast-enhanced US (CEUS) is a safe, noninvasive, and cost-effective method whereby real-time blood flow can be assessed with microbubble contrast agent with high spatial resolution [4].

American College of Radiology (ACR) has published Liver Imaging Reporting and Data System (LI-RADS) guidelines for the assessment of liver lesions evaluated through MR/CT scan and CEUS [5]. In patients with identified liver risk factors, LI-RADS provides a probability scale for malignancy with categorization of lesions based on their size, enhancement characteristic, and washout (WO) pattern. This provides a precise and standardized evaluation of liver lesions with recommended guidelines for management dependent on tumor category.

As part of LI-RADS, there is an algorithm specific to CEUS for the categorization of focal liver lesions visible on greyscale ultrasound (US): CEUS LI-RADS [6]. CEUS is a nodule focused exam based on contrast enhancement changes in the arterial phase (AP) and portal venous phase (PVP). Nodules meeting LR-5 criteria have greater than 95% specificity of being HCC [7, 8] and in our center, treatment is initiated based on this result without a need for biopsy. CEUS LI-RADS also addresses evaluation of treatment sites in CEUS LI-RADS TRA, metastases, and benign tumors [6, 9].

CEUS LI-RADS does not recommend CEUS of nodules occult or invisible on pre-contrast ultrasound [6]. However, the most recent publication does make an exception for expert practitioners and there is anticipated inclusion in future guidelines [6]. Currently, our efforts to categorize occult nodules according to LI-RADS following successful CEUS is performed outside of the LI-RADS criteria, and management remains uncertain.

Occult nodules are universally found on all imaging modalities and can present as consequential findings, especially in the at-risk liver [10, 11]. Detection of these occult nodules remains crucial in the diagnosis and management of HCC and metastatic cancer. Nonetheless, investigation into specifically detecting and characterizing occult nodules on CEUS has received little attention. McGillen et al. have shown some success at retrospectively finding occult nodules with sweeps of the liver after injection of Lumason/SonoVue contrast agent, however with low incidence of malignancy of occult lesions in their patient population [12].

In our center, CEUS is established as a vital component of the imaging team in management of the high-risk patient for HCC. This study represents a compilation of experience from our investigators to visualize occult nodules. Firstly, we assess if it is possible to identify occult lesions on CEUS. If we can visualize these lesions, we determine feasibility to characterize them by applying CEUS LI-RADS without a greyscale visible nodule. Finally, we analyze the appropriateness of LI-RADS categorization by examination of impact on management.

Study design

This retrospective single-center study is approved by the institutional review board (HREBA.CC-23-0397). Informed consent was waived for this retrospective study. To answer the question of finding occult nodules, we manually searched for the term occult in our archived patient logs in an attempt to identify 100 patients with reported occult lesions.

We then looked at results of all CEUS examinations found to have reported at least one occult lesion and any associated MR or CT imaging prior to their CEUS exam with a positive enhancement observation that motivated the search for the occult lesion. Once identified, we determine correlation. We additionally evaluate ultimate management and any confirmed diagnoses.

We identified 100 at-risk patients who had a CEUS study between July 2017 to July 2024 who have at least one documented occult lesion reported on a CEUS study. 68 were male, 32 were female, and the median age was 66 years (IQR: 59–72). Multiple patients have multiple risk factors with cirrhosis present in 81 (81%) patients. 22 (22%) patients have HCV, 18 (18%) have HBV, 21 (21%) with ALD, 14 (14%) with MASH, and 10 (10%) with MASLD. 44 (44%) patients have had a previous HCC and 5 (5%) patients have a past medical history of non-hepatocellular cancer.

We further looked at details of the contrast enhanced scan to determine which CEUS techniques were commonly utilized to confirm identification of occult nodules. Then, to explore our objective of the potential to categorize these occult nodules, we evaluated AP enhancement as hyperenhancement, isoenhancement, or hypoenhancement. PVP evaluation determined WO, with its intensity and timing, or sustained enhancement or no WO. These characteristics allow categorization according to CEUS LI-RADS algorithm [6]. LR-5 categorization required APHE of any kind, late weak WO, and size ≥ 1cm. LR-M required rapid WO by 1 min. Next, we assessed in detail which features were most important in leading to the categorization of consequential LI-RADS lesions: LR-4, LR-5, LR-M, and LR-TR viable. Lastly, we evaluate if existing LI-RADS algorithm was appropriately applied to these nodules with no greyscale correlate. Specifically, we examine for positive pathology confirmation and treatment.

CEUS

Conventional technique

all participants are imaged by sonographers and greyscale images are captured. Full CEUS examination is conducted in our department by injection of one 0.2mL dose of Perflutren microspheres (Lantheus Medical Imaging, Billerica, MA) followed by 10mL saline flush, delivered as a rapid bolus. Probe frequency, mechanical index, and patient position were optimized for image quality. Dual displays of greyscale and CEUS are recorded. Cine clips are recorded immediately following contrast injection and to prevent excessive microbubble destruction, still-images are captured periodically up to 5 minutes post injection. Three ultrasound techniques of blindshot injection, sweeping the liver during PVP and late phase (LP) were utilized in CEUS exams.

Blindshot injection – looking for correlation with focus of suspicious enhancement from MR/CT scan

Blindshot injections are utilized to confirm a suspect nodule. One dose of contrast agent is injected with the ultrasound probe positioned to triangulate lesions based on anatomical or pathologic landmarks from MR/CT. Following injection, visualization of any arterial phase enhancement or PVP changes, that is WO, are documented. A focus of APHE may occasionally be immediately evident, whereas in many other circumstances, slight movement through the region of interest may lead to its detection or visualization of an area of WO (supplementary video 1).

PVP liver sweep – looking for WO zones as evidence of occult nodules

At any time following 45 seconds from contrast injection, the liver parenchyma will be nicely enhanced, and liver sweeps are performed with a full suspended inspiration, with movement of the probe in a sweeping motion across the right lobe of the liver, followed by the left lobe, in both the long axis and axial view (supplementary video 2). In most cases, evaluation is for WO (supplementary video 3). Although we regard the identification of WO as the most valuable benefit of this technique as it suggests malignancy, in fact, showing no WO, equivalent to sustained enhancement is equally valuable, most often suggesting benign disease.

On-top injection – verify AP enhancement features associated with an identified WO zone

Following WO of a lesion, a subsequent, on-top injection of contrast agent can be performed with the ultrasound probe directly targeting the identified area of WO (supplementary video 4). Subsequent AP enhancement and timing of WO can be recorded to further characterize any lesions.

Finding occult lesions

In our 100 patients, 114 occult lesions were identified, with some patients having more than one occult lesion. 102 nodules were found, including 99 independent nodules and an additional 3 as part of diffuse micronodularities. 12 lesions were associated with a treatment site, including 10 intralesional or perilesional nodules and 2 an occult treatment site. The average size of all measured nodules was 1.56cm (SD = 0.80).

Of the 114 lesions, 78 (68%) originated from MR (n = 69), or CT (n = 9) scan showing an indeterminate observation, especially APHE. From the 65 patients with at least one occult lesion originating from MR, 10 patients had a CEUS exam within 2 weeks, 18 between 2 weeks and 2 months, 27 between 2–6 months, and the remainder beyond 6 months. Suspicion for the remainder of the occult lesions (n = 36) (32%) began during the CEUS exam with fortuitous observation of APHE or WO.

In cases motivated by a focus of abnormal enhancement on MR scan, once a greyscale ultrasound failed to show a nodular correlate, we utilized the technique of blindshot injection focusing on the area of suspicion from MR in all cases (n = 69/69, 100%). If a focus of APHE was found on CEUS, the lesion was followed over time to see if there was any WO (Fig. 1) to allow categorization of these lesions in the absence of a greyscale nodule. It was also beneficial to perform a repeat injection focused on that nodule as additional satellite nodules were often detected (Fig. 2).

A second cohort is comprised of nodules suspected during the performance of a CEUS examination without prompting from MR or CT. This usually occurs when APHE or WO is noticed nearby another target or during a liver sweep (Fig. 3). In characterizing these nodules, on-top injection can be subsequently performed targeting a region of WO, to identify any associated APHE (Fig. 3).

Although overwhelmingly suspicion of occult nodules occurs in the circumstances described, that is following detection of indeterminate APHE focus on MRI or identification of unexplained APHE or WO on CEUS, other isolated unusual cases include the following. In a single case, on sweeping the liver, in one patient with a virtually normal background liver on greyscale US, multiple foci of APHE were noticed persisting as hyperenhanced nodules beyond 5 minutes. This unusual case was indeterminate on MRI which additionally showed indeterminate enhancement in AP with nodular enhancement in the delayed phase. Subsequent biopsy showed angiosarcoma (Fig. 4). Further, when evaluating treatment response, an on-top injection was performed in all but one CEUS LR-TR viable site (Fig. 5).

Categorizing Lesions

Based on AP enhancement changes and timing of WO, we attempted to categorize the occult lesions (Table 1) according to CEUS LI-RADS. Of the 114 occult lesions, 63% (n = 72) can be categorized as consequential: LR-4 (n = 34), LR-5 (n = 26), LR-M (n = 5), or LR-TR viable (n = 7) on CEUS. Of the 5 without assignment of a LI-RADS category, presence of WO was not clarified for 2 subcentimetre nodules on the CEUS report, 2 cases were reported as “equivocal”, and 1 treatment site was favoured to have post-surgical change.

Table 1 LI-RADS CATEGORIZATION OF OCCULT LESIONS

LI-RADS category was reported in 50 MR/CT scans. Interestingly, if CEUS does change LI-RADS categorization of an occult lesion, it upgraded the LI-RADS category reported from CT/MR in 24 lesions (48%), maintained LI-RADS category in 22 lesions (44%), downgraded 2 lesions (4%), changed 1 MR LR-4 to CEUS LR-M, and changed 1 from MR LR-M to CEUS LR-5. Notably, 7 LR-4 nodules were upgraded to LR-5 with the identification of washout on CEUS not shown on CT/MR scan.

We then analyzed which CEUS techniques and lesion characteristics were most important in identifying clinically relevant occult lesions. 68% (49/72) of LR-4, LR-5, LR-M, and LR-TR viable lesions were found through blindshot injection with the majority of LR-4 nodules (26/36) and LR-TR viable treatment sites (6/7) initially identified through blindshot injection (Table 2). Furthermore, we commonly use an on-top injection to better characterize these clinically relevant occult lesions (37/72).

Table 2 CEUS TECHNIQUES, FINDINGS, and TREATMENT IMPACTS on CONSEQUENTIAL LESIONS

Of the 26 LR-5 tumors, 4 of them were found with WO on late sweeps and 10 were found on the basis of APHE following blindshot injection. The remainder were found adjacent to other targets or WO was the first feature noticed following blindshot injection. 17 occult LR-5 lesions had other lesions reported in the same CEUS exam. For the 5 LR-M lesions, 3 were found on the basis of WO on a liver sweep and 2 from APHE following a blindshot injection. All LR-Ms had an on-top injection which showed rapid WO.

APHE was the most important characteristic in finding LR-4 nodules with 31 of the 34 LR-4 nodules first displaying APHE. Of these nodules first found due to APHE, 25 were seen following a blindshot injection, 1 during a liver sweep, and the remainder nearby another target. 3 LR-4 lesions were identified on the basis of WO with 1 found on a liver sweep, 1 seen nearby another nodule, and 1 through a blindshot injection. 20 occult LR-4 lesions also had other lesions reported on the same CEUS exam. APHE following blindshot injection targeting the treatment site was the most salient feature in 4 of the 7 LR-TR viable lesions and 1 was found with APHE nearby another target. 2 LR-TR viable lesions were first identified from WO following a blindshot injection.

Assessing appropriateness of LI-RADS categorization

Finally, in assessing if LI-RADS algorithm was appropriate to be applied to these occult lesions, we saw that 29 occult lesions have been offered treatment with 21 treated. 18/26 LR-5 lesions having been offered treatment (Table 2). Furthermore, of the total 21 treated lesions, 12 were treated with ablative therapy and 9 lesions were treated as multi-focal sites. Biopsy results of the occult lesion itself were sparse although we did identify 5 nodules from 15 treated LR-5 and LR-M nodules with positive pathology. No lesion was biopsied to be intrahepatic cholangiocarcinoma (ICC).

Method used in finding and characterizing occult nodules

The results including the source of occult nodules, the CEUS techniques used for their identification and characterization, and their LI-RADS categorization are shown in Table 3.

This study supports the investigation of suspect occult nodules encountered during CEUS liver imaging examinations to confirm their presence and their LI-RADS category for the diagnosis of HCC. Full LI-RADS categorization can have consequential impacts on patient management. With CEUS techniques, we can characterize occult nodules, allowing for their treatment without biopsy and influence management if multiple nodules are present. Furthermore, these CEUS techniques are not exclusive only to patients with isolated occult nodules but can be applied to other CEUS examinations including tumor response assessment. As shown in Fig. 3, all 3 CEUS techniques can be utilized during one scan and these techniques are versatile and contribute useful information for clinical management.

Over the course of investigating occult nodules, our CEUS techniques have evolved and are now frequently used in tandem to show our results with greater confidence. For example, a blindshot injection to confirm APHE can be reinforced by performing an on-top injection of the subsequently identified washout, providing us with two complete injections confirming APHE and WO for a single lesion.

Occult nodules found in our study are favoured to be HCC and do not show a normal distribution of HCC and ICC that we find in our population. We conjecture that in HCC, the similarity of the hepatocyte between normal liver and tumor may facilitate these lesions being occult whereas cholangiocarcinoma originates from bile duct epithelium. As with imaging elsewhere, these adenocarcinomas are morphologically different from liver tissue, offering an explanation for their absence within occult lesions.

Failure to identify a nodule may occur on CT, MR, and US scan. Although theories as to their origin are suggested, in the final analysis, they are largely unexplained. Management of occult nodules have been addressed by others, including radiologists performing MR scan and ultrasonographers performing CEUS. Methods include Primovist MR scan and the use of Sonazoid [13], an US contrast agent with a vascular phase and Kupffer phase, where reinjection has been utilized to augment visualization of any lesions seen as a defect in the Kupffer phase [14]. These techniques are beyond the scope of this manuscript.

In this manuscript, we focus on the value of CEUS in the patient at risk for HCC whereby there is an assumption that nodules detected and characterized are most likely to be HCC. However, CEUS is shown to be sensitive to both the timing and intensity of WO for the differentiation of HCC from nonHCC malignancy including metastases (Fig. 3) [15, 16].

The classification of over half of all occult lesions in our study as consequential suggests that exclusion of these occult nodules during multidisplinary discussions would lead to fewer diagnoses and treatments, and result in return visits for repeat MRI. It is seen that 28 patients in our study benefitted with having a CEUS exam within 2 months rather than waiting for a second MR scan. Added costs of downstream testing of indeterminate results can be reduced with CEUS, as can the time to diagnosis, impacting treatment and quality adjusted life years. All of these are important reductions for healthcare systems and warrant subsequent investigation.

Furthermore, we have shown that CEUS does have a tendency to upgrade CT/MR LI-RADS categories which is in agreement with Hu et al. in two publications [17, 18]. Upgrading is crucial in being able to treat with high confidence of malignancy for LR-5 lesions whereas treatment is not routinely offered for LR-4 lesions. We postulate that improved visualization of WO on CEUS relative to MR is due to the pure blood-pool nature of microbubble contrast agent.

Pathology correlation in today’s environment when LR-5 nodules are routinely treated without biopsy makes it such that we have less pathology confirmation than ideal and constitutes the greatest weakness of our study. However, positive pathology has been identified in some of our patients and treatment was carried out for multiple occult nodules. Additionally, the true frequency of occult lesions offered treatment is likely underestimated due to insufficient follow-up time. Due to the retrospective nature of our study, recruitment of patients is undoubtedly incomplete as we relied on operator reporting. Although we looked at files dating back to 2017, we believe 114 occult lesions is a vast underestimate. We recognize now that occult nodules are seen more frequently than we had anticipated and today we include a protocol for suspected occult nodules so that sonographers and physicians can uniformly assess patients to avoid missing occult nodules of significance.

A positive result of our study that was unexpected includes the large number of occult nodules that occur. Additionally, in our high-risk population, a large percentage of these occult nodules once characterized are recognized to be of clinical consequence. Our interventional radiologists are receptive to our recommendation to treat these occult nodules with US guidance. Certainly, impaired visualization of lesions could impact ablation feasibility [19]. With the ability to visualize occult lesions, CEUS expands the ability to first locate, then biopsy [20] and perform ablative therapies for occult lesions [21, 22]. Therefore, we feel motivated to encourage adoption of our CEUS techniques by others and their incorporation into CEUS LI-RADS. Further validation for applying CEUS-LI RADS to occult lesions would assist in resolving current ambiguity with assessing occult liver lesions.

Our objectives were to determine if we can find occult lesions in at-risk livers, categorize them on CEUS LI-RADS, and assess if it was appropriate to do so. We feel our study allows us to provide good answers to these questions. We certainly can find occult nodules, our characterization was quite straightforward missing only greyscale correlation, and we could apply CEUS LI-RADS algorithm reasonably without concern and indeed these occult lesions were often treated. Additionally, CEUS was able to upgrade lesions seen on MR/CT, influencing management strategies.

CEUS can detect and characterize occult liver lesions through three key CEUS techniques: blindshot injection, sweeping the liver during PVP and LP, and on-top injection. For cases originating from MR/CT, blindshot injection can be performed whereas other cases are found fortuitously on CEUS through visualization of APHE or WO from a liver sweep or next to another target. Enhancement changes can be subsequently characterized with an on-top injection. Through utilizing these techniques, occult lesions can be categorized according to CEUS LI-RADS with positive impacts on patient management.

Author Contribution

AQ performed a literature search, acquired and analyzed data, and prepared all figures and tables. AQ and SRW wrote the manuscript text. SRW formulated the concept for this manuscript. ASS and CM assisted with data collection and were consulted regularly on presentation and interpretation of patient material. MB functioned as a clinical consultant related to our initial project, our patient presentation, and manuscript preparation and review. All authors edited and reviewed the manuscript.

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No competing interests reported.

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Occult Liver Nodules: their Detection and Characterization with CEUS

Status:

Version 1

Abstract

Figures

Introduction

Methods

Study design

CEUS

Blindshot injection – looking for correlation with focus of suspicious enhancement from MR/CT scan

PVP liver sweep – looking for WO zones as evidence of occult nodules

On-top injection – verify AP enhancement features associated with an identified WO zone

Results

Finding occult lesions

Categorizing Lesions

Assessing appropriateness of LI-RADS categorization

Method used in finding and characterizing occult nodules

Discussion

Conclusion

Declarations

Author Contribution

References

Additional Declarations

Supplementary Files

Status:

Version 1