European Society of Radiology (ESR) Insights into Imaging
[Link]
(2019) 10:6
Insights into Imaging
STATEMENT Open Access
Abdominal applications of ultrasound
fusion imaging technique: liver, kidney,
and pancreas
European Society of Radiology (ESR)
Abstract
Fusion imaging allows exploitation of the strengths of all imaging modalities simultaneously, eliminating or minimizing
the weaknesses of every single modality. Ultrasound (US) fusion imaging provides benefits in real time from both the
dynamic information and spatial resolution of the normal US and the high-contrast resolution and wider field of view
of the other imaging methods. US fusion imaging can also be associated with the use of different ultrasound
techniques such as color Doppler US, elastography, and contrast-enhanced US (CEUS), for better localization and
characterization of lesions. The present paper is focused on US fusion imaging technologies and clinical applications
describing the possible use of this promising imaging technique in the liver, kidney, and pancreatic pathologies.
Keywords: Ultrasound, Fusion imaging, Liver, Oncologic imaging, Tumor ablation
Key points magnetic resonance (MR), and positron emission tomog-
raphy (PET).
Fusion imaging helps in the detection and During interventional procedures, this process is re-
localization of lesions with low conspicuity on ferred to as “cognitive fusion” or “visual registration”
standard B-mode US. and consists of the careful studying of an examination
US fusion imaging can also be associated with the acquired before the procedure, usually CT or MR, and
use of different ultrasound techniques such as color the subsequent use of US as a guide for the performance
Doppler US, elastography, and contrast-enhanced of the procedure, after mental superimposition of the
US (CEUS). spatial information from the prior study [1]. However,
The current principal use of US fusion imaging is this process can be difficult if the ideal US scanning
during hepatic interventional procedures. However, plane is different to the classical orthogonal CT or MR
new applications in both intra- and extra-abdominal image. Moreover, breathing and displacement and de-
areas are emerging more and more. formation of the abdominal structures due to pressure
from the US probe can affect the process of mental
registration [2].
Introduction Thanks to the recent improvements of technology and
Taking advantage of various imaging techniques to im- computing power, a real-time computerized fusion of
prove both diagnosis and interventional procedures has radiological images has been developed and imple-
become a very common process and is an integral part of mented in modern high-end US machines, to allow syn-
the work of the modern radiologist. Normally, the associ- chronous association of US images with one or more
ation process is a mental act that involves the integration other cross-sectional studies such as CT, MR, or PET,
of information coming from multiple imaging methods which are instantly reconstructed in the corresponding
such as ultrasound (US), computed tomography (CT), plane.
US guidance is still the guidance method of choice for
percutaneous interventional procedures, as it provides
* Correspondence: communications@[Link] real-time imaging, does not use ionizing radiation, is
Vienna, Austria
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License ([Link] which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
European Society of Radiology (ESR) Insights into Imaging (2019) 10:6 Page 2 of 6
easily accessible, and is cheap [3]. However, compared to Using anatomical landmarks alone, synchronization of
CT and MR, it has lower contrast resolution and a nar- the US images with CT/MR must be manual and re-
rower field of view and is affected by the presence of gas quires the identification of motionless anatomical struc-
and fat. The use of real-time fusion imaging allows ex- tures on the US (e.g., vessels, cysts, calcifications) that
ploitation of the strengths of all imaging modalities sim- are then manually matched on the tomographic exam
ultaneously, eliminating or minimizing the weaknesses [5]. If external markers are used, placed on the patient’s
of every single modality. Therefore, US fusion imaging skin during the CT acquisition phase, the image coup-
provides benefits in real time from both the dynamic in- ling process will be automatic, faster, and more reliable.
formation and spatial resolution of the normal US and When image matching is complete, real-time US and
the high-contrast resolution and wide field of view of CT/MR/PET images are arranged side-by-side or overlaid
the other imaging methods. US fusion imaging can also on the US monitor, displaying the same plane and moving
be associated with advanced US imaging techniques synchronously together (Figs. 1, 2, 3 and 4). Thus, fusion
such as color Doppler US, elastography, and contrast- imaging helps in the detection and localization of lesions
enhanced US (CEUS), for better localization and with low conspicuity on standard B-mode US [4]. It is also
characterization of lesions to be treated [4]. possible to indicate the desired needle route, which can
then be followed easily during the procedure.
Fusion imaging technology There are many applications of fusion imaging, but
There are several available spatial tracking methods for given the relative novelty of the technology, most are
US probes, including optical, image-based, and electro- still under investigation and require additional clinical
magnetic tracking [1]. The electromagnetic tracking sys- trials. The current principal use of US fusion imaging is
tem is the one mostly used for percutaneous during hepatic interventional procedures. However, new
interventional procedures. It comprises a magnetic field applications in both intra- and extra-abdominal areas
generator, located 20–30 cm from the patient, and a pos- are emerging more and more.
ition sensor attached to the probe, or integrated into the
needle. When the position sensor is moved in the mag- Liver
netic field, an induced electric current is generated, US is the method of choice for the interventional percu-
allowing the system to recognize its 3D spatial position taneous approach to hepatic lesions. Its advantages in
and orientation. this area are manifold, both for diagnostic procedures
The image fusion procedure begins with the import- such as biopsies and therapeutic procedures such as ab-
ation of data from a previous CT/MR/PET exam. Next lations. Firstly, it is a real-time method, allowing the liver
is the planning phase, which consists of several steps to to be constantly followed during respiratory movements.
study the target lesions and the structures involved in It allows identification of the most appropriate plane for
the procedure and to establish the spatial orientation of needle insertion; this does not have to be an axial plane
the patient with respect to the probe. To do this, both but can be oriented at will according to the circum-
anatomical landmarks and external markers can be used. stances. Furthermore, the use of color Doppler US
Fig. 1 CT-US fusion imaging. Treatment of very small hypervascular nodular recurrence of HCC adjacent to a previously ablated area
European Society of Radiology (ESR) Insights into Imaging (2019) 10:6 Page 3 of 6
Fig. 2 MR-US fusion imaging. Biopsy of very small liver nodule, hypointense on the late hepatobiliary phase of MR, with a final diagnosis
of a metastatic lesion
allows us to identify major vascular structures (e.g., hep- with the US. Furthermore, lesions and their margins are
atic arteries, portal vein branches, hepatic veins) which not always clearly visible on the B-mode US, even after
should preferably be avoided during needle insertion. Fi- the administration of contrast medium, particularly in the
nally, fused CEUS can be useful to increase the conspi- inhomogeneous and cirrhotic livers. The most common
cuity of lesions to be treated and vascular structures to causes of mistargeting during US-guided radiofrequency
be avoided [3]. ablation (RFA) of hepatocellular carcinoma (HCC) are
However, US has some weaknesses which can affect the confusion with cirrhotic nodules, poor conspicuity of the
success of the procedure. Firstly, it is an operator- target lesion, and poor acoustic window [2]. Lesions lo-
dependent method and has a lower contrast resolution cated deep in the most distal sectors of the acoustic cone
than CT and MR. Air contained in the hollow organs or in can be blurred and difficult to identify. Using fusion im-
the biliary tract (in the case of pneumobilia) may limit the aging technologies, it is possible to place beside or overlay
available acoustic window. Even air in the lung paren- upon the US image images from modalities that do not
chyma, bones, and calcification (e.g., gallstones) interferes suffer from all these problems, such as CT and MR. In this
Fig. 3 CT-US fusion imaging. Biopsy of pancreatic neck carcinoma, hypodense on CT and hypoechoic on the US
European Society of Radiology (ESR) Insights into Imaging (2019) 10:6 Page 4 of 6
Fig. 4 CT-US fusion imaging. Radiofrequency ablation planning of pancreatic neck carcinoma, hypodense on CT and hypoechoic on Doppler US
(performed to highlight the peripancreatic vessels)
way, radiologists can exploit all the strengths of the differ- lesions. However, with only B-mode US, it can often be
ent methods in a single session, increasing the safety, difficult to distinguish between simple and complex or
speed, and results of the procedure and improving the neoplastic cysts. Even in the case of solid renal lesions,
confidence of the operator. there may be difficulties with the B-mode US in terms
Some hepatic tumors which can be visualized by of detection and characterization. For these reasons, it
CT or MR cannot be seen on the US due to their is often necessary to exploit second-level methods such
small size, their location, or their echogenicity. In as CT and MR for the study of renal lesions. CEUS is
these cases, fusion imaging has been proven to en- also emerging as a useful technique to study cystic le-
hance the conspicuity of HCC nodules and to in- sions and their related septal vascularization, as well as
crease the feasibility of percutaneous RFA of HCCs solid lesions, during ablative procedures [9, 10]. In
not visible on the conventional US [4–6]. If HCCs interventional procedures, fusion imaging can be
are still not visible after fusion imaging, anatomic extremely helpful in identifying the renal lesions to be
landmarks surrounding the lesions can be used for treated, especially those with poor conspicuity on
correct needle placement [5]. Thus, with the use of normal B-mode US. The combination of CEUS with fu-
fusion imaging, a larger population can benefit from sion imaging is effective in the classification of indeter-
US-guided ablation procedures instead of undergoing minate renal lesions and can also improve the
CT-guided ablation or major surgery, which are more characterization of cystic lesions [11]. Therefore, in the
harmful and expensive techniques. case of tumors, the use of CEUS with fusion imaging al-
Fusion imaging can also reduce false-positive lesion lows minimization of the risk of treating benign lesions
detection during US-guided RFA and consistently im- surgically or the risk of missing cancer [12].
prove the detection of HCCs, especially when these When targeting renal lesions during a percutaneous
are smaller than 2 cm [7]. The ability of fusion im- procedure, fusion imaging can help in recognizing the
aging to reduce false positives also applies to the most appropriate part of the lesion to biopsy (especially
evaluation of local tumor progression after RFA and for cystic lesions) or the best position to place the elec-
TACE [8]. trodes for ablation. In the case of multiple lesions, fusion
imaging allows us to distinguish the specific lesion to be
Kidney treated with greater confidence, allowing the margins of
US is the usual first-line imaging method for the assess- the lesion to be more precisely distinguished. Further-
ment of the kidneys. Thanks to their retroperitoneal lo- more, the use of fusion imaging is valuable in determin-
cation, in the lumbar region below the rib cage, an ing the correct path for the needle, avoiding harm to
excellent acoustic window is generally available, with- structures such as the renal vessels, renal pelvis, adrenal
out the interposition of air-containing structures or glands, spleen, and colon.
bones. Most renal lesions are incidental findings and However, the use of fusion imaging in renal disease is
are frequently asymptomatic. The main utility of US is still under investigation in the literature and requires
the precise discrimination of solid lesions from cystic further clinical studies.
European Society of Radiology (ESR) Insights into Imaging (2019) 10:6 Page 5 of 6
Pancreas central ones, which are more fixed in position by the
When used by experienced operators, US allows the presence of the hepatic pedicle. In the periphery of the
pancreas to be studied in excellent detail. As US is a liver, there are also fewer anatomical landmarks such as
real-time method, radiation-free, and can be performed the vessels. For this reason, registration error during fu-
at the bedside, it is an important aid for guiding pancre- sion imaging especially affects the peripheral portions of
atic percutaneous procedures such as ablation of lesions the liver and patients with large respiratory movements
or drain positioning [13]. However, since the pancreas is [11]. Although retroperitoneal, registration errors may
a retroperitoneal organ, it may be difficult to visualize it also affect the kidney, as it is a mobile organ subject to
entirely if there is an interposition of hollow organs; this movement with breathing. Registration errors occur
is particularly true with respect to the tail, sometimes when the respiratory phase of the reference examination
called the “blind area” of the pancreas. CT and MR, on is different from that during image synchronization.
the other hand, are superior to US in permitting full Therefore, MR, which is normally performed in expir-
visualization of the pancreas, providing clearer demon- ation (as opposed to CT, usually performed during in-
stration of its relationships to the delicate surrounding spiration), is more comparable with the patient’s
structures, lying behind the colon and stomach and in breathing status during the interventional procedure and
close contact with the duodenum, the portal vein and is therefore less associated with registration errors [12].
major arterial structures such as the aorta, the celiac The pancreas is a less mobile organ during breathing
axis, and the superior mesenteric artery. For this reason, and is therefore theoretically less affected by registration
fusion imaging can be an extremely useful tool to errors. However, visualization of the pancreas often re-
recognize and avoid damaging these structures during quires that pressure be applied with the probe on the
US-guided percutaneous procedures. It has been shown upper abdomen to displace the overlying hollow organs.
that performing drainage of pancreatic necrosis using This can change the relationships between abdominal
US fusion imaging is superior to classic B-mode US in structures, which can affect the matching between the
terms of safety, efficiency, and hospitalization length and US and CT/MR images.
costs [14]. US fusion imaging also allows better Finally, while fusion imaging is increasingly proving to
visualization of the “blind area” when it is not clearly be a promising technology, further randomized clinical
shown with normal B-mode US [15]. trials are needed to define its presumed superiority over
Clinical indications for fusion imaging of the pancreas cognitive fusion during image-guided procedures.
can therefore be summarized as guidance for biopsy and
drainage and percutaneous treatment of pancreatic can- Conclusion
cer such as radiofrequency ablation or irreversible US fusion imaging is a relatively novel technique in the
electroporation. abdominal US panorama. Its ability to exploit all the
Even in these circumstances, the use of fusion imaging strengths of multiple imaging methods used together in
in pancreatic disease is not well-described in the litera- real time makes it a tool of great value when performing
ture and requires further clinical studies to confirm its a percutaneous procedure. Increasing the confidence of
validity. the operator, it allows better visualization of the abdom-
inal structures and more precise planning of needle
Limitations of fusion imaging paths, avoiding delicate structures, minimizing radiation
One of the most challenging limitations affecting US fu- exposure, and so increasing safety and efficiency (and
sion imaging is the risk of mistargeting a lesion. In hep- decreasing cost) of these procedures.
atic ablation, mistargeting normally occurs in about 2%
of cases and is principally due to the small size of the le- Acknowledgements
This paper was prepared by Mirko D’Onofrio (Member of the ESR Ultrasound
sion or confusion with the surrounding pseudo lesions Subcommittee) and Alessandro Beleù, Department of Radiology, G.B. Rossi
such as regenerative nodules. Lesions located in subcap- Hospital – University of Verona, Verona, Italy – with the contribution from
sular or subphrenic areas, as well as lesions with poor Subcommittee Members Diana Gaitini, Jean-Michel Corréas and Adrian Brady
(Chair of the ESR Quality, Safety and Standards Committee). The paper was
conspicuity, can also be missed [9]. supported by the ESR Ultrasound Subcommittee led by Dirk Clevert (Chair of
Another limitation of US fusion imaging is the need to the ESR Ultrasound Subcommittee).
synchronize a static image from a CT or MR study with It was approved by the ESR Executive Council on November 15, 2018.
the breathing motion and changing position of the pa-
Authors’ contributions
tient, in particular when approaching a subdiaphrag- All authors read and approved the final manuscript.
matic organ such as the liver [10]. During the breathing
cycle, the movement of the liver is complex and includes
Publisher’s Note
translations and rotations. During breathing, the periph- Springer Nature remains neutral with regard to jurisdictional claims in published
eral regions of the liver move more widely than the maps and institutional affiliations.
European Society of Radiology (ESR) Insights into Imaging (2019) 10:6 Page 6 of 6
Received: 12 December 2018 Accepted: 3 January 2019
References
1. Maybody M, Stevenson C, Solomon SB (2013) Overview of navigation systems
in image-guided interventions. Tech Vasc Interv Radiol 16(3):136–143.
2. Lee MW, Lim HK, Kim YJ et al (2011) Percutaneous sonographically guided
radio frequency ablation of hepatocellular carcinoma: causes of
mistargeting and factors affecting the feasibility of a second ablation
session. J Ultrasound Med 30(5):607–615.
3. Lorentzen T, Nolsøe CP, Ewertsen C et al (2015) EFSUMB guidelines on
interventional ultrasound (INVUS), part I. general aspects (long version).
Ultraschall Med 36(5):E1-14.
4. Lee MW (2014) Fusion imaging of real-time ultrasonography with CT or MRI
for hepatic intervention. Ultrasonography 33(4):227–239.
5. Song KD, Lee MW, Rhim H, Cha DI, Chong Y, Lim HK (2013) Fusion imaging-
guided radiofrequency ablation for hepatocellular carcinomas not visible on
conventional ultrasound. AJR Am J Roentgenol 201(5):1141–1147.
6. Mauri G, Cova L, De Beni S et al (2015) Real-time US-CT/MRI image fusion
for guidance of thermal ablation of liver tumors undetectable with US:
results in 295 cases. Cardiovasc Intervent Radiol 38(1):143–151.
7. Lee MW, Rhim H, Cha DI, Kim YJ, Lim HK (2013) Planning US for
percutaneous radiofrequency ablation of small hepatocellular carcinomas
(1–3 cm): value of fusion imaging with conventional US and CT/MR images.
J Vasc Interv Radiol 24(7):958–965.
8. Min JH, Lee MW, Rhim H et al (2014) Local tumour progression after loco-
regional therapy of hepatocellular carcinomas: value of fusion imaging-
guided radiofrequency ablation. Clin Radiol 69(3):286–293.
9. Meloni MF, Smolock A, Cantisani V et al (2015) Contrast enhanced
ultrasound in the evaluation and percutaneous treatment of hepatic and
renal tumors. Eur J Radiol 84(9):1666–1674.
10. Gulati M, King KG, Gill IS, Pham V, Grant E, Duddalwar VA (2015) Contrast-
enhanced ultrasound (CEUS) of cystic and solid renal lesions: a review.
Abdom Imaging 40(6):1982–1996.
11. Rübenthaler J, Paprottka KJ, Marcon J, Reiser M, Clevert DA (2016) MRI and
contrast enhanced ultrasound (CEUS) image fusion of renal lesions. Clin
Hemorheol Microcirc 64(3):457–466.
12. Helck A, D'Anastasi M, Notohamiprodjo M et al (2012) Multimodality
imaging using ultrasound image fusion in renal lesions. Clin Hemorheol
Microcirc 50(1–2):79–89.
13. Qiu W, Sun X, Wei F, Wang G, Ye J, Lv G (2016) Clinical study of B-mode
ultrasound-guided retroperitoneal and abdominal catheter treatment of
severe acute pancreatitis. Minerva Chir 71(1):25–30.
14. Zhang H, Chen GY, Xiao L et al (2018) Ultrasonic/CT image fusion guidance
facilitating percutaneous catheter drainage in treatment of acute
pancreatitis complicated with infected walled-off necrosis. Pancreatology
18(6):635–641.
15. Sumi H, Itoh A, Kawashima H et al (2014) Preliminary study on evaluation of
the pancreatic tail observable limit of transabdominal ultrasonography
using a position sensor and CT-fusion image. Eur J Radiol 83(8):1324–1331.