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Commemoration

Intraoperative Ultrasonography
History, Current State of the Art, and
Future Directions
Robert A. Kane, MD
Department of Radiology
Harvard Medical School
Beth Israel Deaconess Medical Center
Boston, Massachusetts USA

Abbreviations
CT, computed tomography; IOUS,
intraoperative ultrasonography; LUS,
laparoscopic ultrasonography; MRI,
magnetic resonance imaging

t is a privilege to contribute an article on intraoperative ultrasonography (IOUS) to the series of articles on the history of ultrasound in
commemoration of the 50-year anniversary of the American Institute
of Ultrasound in Medicine in 2005. On approaching my own 30th
anniversary in the practice of diagnostic radiology, it is amazing to reflect
back on the uses of A-mode, B-scanning on nonpersistent green fluorescent oscilloscopes, and bistable B-mode scanning as the first primitive
diagnostic ultrasonographic tools. Although IOUS began developing in
earnest in the late 1970s and early 1980s, after the development of gray
scale B-mode ultrasonography and especially after the development of
real-time imaging, early investigators were using the more primitive
tools as early as the 1960s.
One of the very first reports of IOUS was by Schlegel et al1 in 1961, who
used A-mode ultrasonography for the localization of renal calculi (Figure
1). A-mode was also reported as useful in detection of stones in the gallbladder and common duct in an article by Knight and Newell2 in 1963
and in another article by Eiseman et al3 in 1965. A-mode echoencephalography was also reported as useful in delineation of intracerebral
mass lesions in a study by Dyck et al4 in 1966. The inability to display tissue texture in A-mode or bi-stable B-scanning as well as the rather large,
bulky size of the equipment limited the more widespread use of IOUS. A
small direct-contact ophthalmic B-scanner was developed and proved
useful for B-scan ultrasonography during orbital surgery for tumors, as
reported by Purnell et al5 in 1973 (Figure 2), but very little further development was reported until the advent of real-time scanners and smaller,
more portable equipment. One of the first reports of real-time B-mode
ultrasonographic scanning was by Sigel et al6 in 1982, which described
the use of ultrasonography for precise localization of renal calculi, thereby allowing for the use of smaller nephrotomy incisions, reduced operating room time, and determination that all stone fragments were removed
before completion of the procedure.
My own experience with IOUS began rather inadvertently in 1983,
when I received a call from a distraught surgeon in the operating room,
who could not find the intrahepatic abscess that we had shown on preoperative ultrasonography and computed tomography (CT) in a patient

2004 by the American Institute of Ultrasound in Medicine J Ultrasound Med 2004; 23:14071420 0278-4297/04/$3.50

History of Intraoperative Ultrasonography

Figure 1. A-mode sonogram of a renal calculus. The initial spike


labeled A represents the surface of the kidney; the spike labeled
B is a reflection from the calculus; and the small spike labeled C
is the posterior margin of the kidney. Reproduced with permission from Journal of Urology.1

Figure 2. A, Early contact B-scanner for intraoperative ophthalmic use. B, Intraoperative B-scan image of a retrobulbar
tumor. Reproduced with permission from Journal of Clinical
Ultrasound.5

with a history of intravenous drug use, acute


hemorrhagic cholecystitis, and an associated
liver abscess. Because by then we were very experienced with real-time ultrasonography, we
decided to bring our unit up into the operating
suite, cover the probe with a sterile sheath, and
have a look at the liver. It took less than a minute
to find the abscess and subsequently to direct a
needle into the abscess under real-time ultrasonographic guidance (Figure 3), much to the
appreciation of the surgeon. What struck us as
most compelling was the quality of the images
that were produced because all the noise-generating impediments of skin, subcutaneous fat,
bone, and gas were removed from our scanning
interface, and it became apparent that this was a
powerful imaging technique indeed. Because we
had an active hepatobiliary surgical group, we
began intraoperative ultrasonographic scanning
during planned surgical resections and soon
thereafter acquired specific intraoperative ultrasonic transducers, which were smaller in design
and able to be gas sterilized. It soon became

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Kane

apparent that IOUS was capable of showing 20%


to 30% more liver lesions than were predicted on
the basis of preoperative scanning with ultrasonography, CT, or magnetic resonance imaging
(MRI), and, indeed, most of these lesions could
not be palpated because of their small size of
1 cm or less (Figure 4). There were many reports
confirming this improved liver lesion detection
published in the 1980s.79 The impact of detection of these additional lesions was substantial,
resulting in a change in planned surgical procedures in more than 15% to 30% of cases in our
experience,10 as also reported by Parker et al.11
The pioneering breakthrough by Onik et al,12
demonstrating that ultrasonography could precisely show the margins of cryosurgical ablation
(Figure 5), led to a further proliferation of IOUS
for liver tumors. Cryosurgical tumor ablation
enabled the potential for curative treatment to
be offered to numbers of patients in whom
resection was technically impossible,13 and surgical-pathologic correlation studies confirmed
the accuracy of IOUS for determining complete
cryosurgical tumor ablation. The successful
results from a cryosurgical approach to tumor
ablation,14 in parallel with the use of ultrasono-

graphically guided ethanol injection for small


hepatoma ablation, have led to the extremely
robust and continually developing and expanding field of image-guided tumor ablation, which
is one of the most active areas of interventional
radiology today.
Another area of notable early success for IOUS
was in pancreatic imaging, as first reported by
Sigel et al15 in 1982, in which the utility of IOUS
during surgery for obstructive jaundice was
described in terms of detecting biliary dilatation,
the presence or absence of biliary stones, and the
pattern of obstruction of the duct, including
demonstration of a mass in the periampullary
region (Figure 6), as well as directing biopsy into
Figure 4. Six-millimeter colorectal hepatic metastasis (arrow)
not detected on preoperative imaging but seen only on IOUS.

Figure 3. Early intraoperative liver sonogram localizing a small


intrahepatic abscess with an ultrasonographically guided needle
placed into the abscess cavity for subsequent surgical drainage.
The needle tip can be seen, as indicated by the caret.

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History of Intraoperative Ultrasonography

such a pancreatic mass. With technical advancements, particularly in abdominal CT, detection of
pancreatic masses was improved considerably,
but Machi et al16 showed an additional role for
IOUS in assessment of the resectability of pancreatic cancers by assessing the presence of
extrapancreatic spread, invasion or occlusion of
the portal venous system, or the presence of hepatic metastases, all of which would render a
patient unresectable.
Detection of small pancreatic islet cell tumors
was a diagnostic imaging dilemma in the 1980s,
with multiple imaging modalities being used,
including highly interventional techniques such
as superselective angiography and portal venous
sampling methods. Rifkin and Weiss17 reported
success with intraoperative ultrasonographic
detection of nonpalpable pancreatic masses,
including islet cell tumors. Gorman et al18
demonstrated marked success with detection of
insulinomas, and this was confirmed by others
with consistent success, for a localization rate of
85% to 95%. Other types of islet cell tumors are
more rare, and the experience is more limited
and probably more difficult, particularly with
gastrinomas, which are frequently multiple, are

often extrapancreatic in location, and may also


frequently involve contiguous lymph nodes.
Some authors, including Sigel et al,19 have
advocated the use of IOUS for surgical treatment
of chronic pancreatitis, including localization of
pseudocysts or dilated pancreatic ducts for surgical drainage. This has not become as widely used
as in detection of occult pancreatic tumors.
Although ultrasonography was used in the
1960s in biliary tract disease, widespread use
during open biliary surgical procedures has
been limited. Most of these reports indicated
that IOUS was at least as accurate as radiographic intraoperative cholangiography for the detection of choledocholithiasis,20 but the relatively
equivalent results did not lead to widespread
application of this technique until the advent of
laparoscopic cholecystectomy. The technical
challenges of laparoscopic cholangiography
have led to renewed enthusiasm for laparoscopic intraoperative techniques, as will be discussed
later.
Figure 6. Early IOUS pancreatic scan showing a tortuous dilated pancreatic duct (arrow) leading to a 1.5-cm mass in the head
of the pancreas.

Figure 5. Three IOUS images taken during a hepatic cryoablation of a colorectal


metastasis. The arrow in the left image indicates the cryoprobe in the center of the
metastasis. The middle image shows the growing ice ball, which has not yet
reached the margins of the tumor, as shown by the arrowheads. The right image
shows the tumor to be completely encompassed within the ice ball.

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Some centers have been strong advocates for


the use of IOUS in vascular bypass and
endarterectomy procedures to assess for immediate postsurgical complications, such as intimal
tears or flaps, thrombosis, and anastomotic
stenosis. Dougherty et al21 reported detection of
major abnormalities, which required immediate
surgical revision, on IOUS in 11% of 64 reconstructed renal arteries. Others reported similar
results when IOUS was used for intraoperative
evaluation of carotid endarterectomy procedures.22
Neurosurgical applications of IOUS were widely reported and important techniques in the
1980s. Rubin and Dohrmann23 were among the
first to emphasize the accuracy and ease of use of
IOUS in the localization and characterization of
intracranial masses, thereby helping guide surgical resections and minimize collateral damage to
surrounding brain tissue. In the 1980s, the
stereotactic frames that were developed for use
with CT were not widely available, and the ability
of ultrasonography to precisely define and locate
these tumors was invaluable. Fortunately, most
intracerebral masses, other than low-grade astrocytomas, usually had substantially increased
echogenicity in comparison with the surrounding brain. This was true of meningiomas,
Figure 7. Early IOUS brain image of a cystic astrocytoma showing the cystic components and nodular septations within the
tumor.

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glioblastomas, and most metastases and lymphomas. Acute brain edema, in fact, made many
of these lesions even more conspicuous by lowering the echogenicity of the surrounding brain tissue. Many lesions that appeared cystic on CT
were shown to be completely solid on ultrasonography, whereas truly cystic tumors, such as
cystic astrocytomas, could be extremely well
characterized by IOUS, with demonstration of
various septated fluid collections, areas of thick
septations, nodularity, or solid components
(Figure 7). This accurate depiction was important in helping guide complete resection or
decompression of cystic tumors.
Low-grade gliomas, however, were much more
difficult to detect, often being isoechoic with surrounding brain, requiring experience and sensitivity to subtle mass effects and distortion of
normal architecture for detection, as described
by Pasto and Rifkin.24 Although acute brain
edema lowers the echogenicity of brain
parenchyma, chronic edema can increase its
echogenicity, also making detection of subtle
lesions more difficult.
Real-time imaging also allowed precise placement of biopsy needles and drainage with shunt
catheters, as reported by several authors.25,26
During the early years of the acquired immunodeficiency syndrome (AIDS) epidemic, brain
biopsies were frequently performed to attempt
to distinguish neoplastic brain lesions such as
lymphoma from infectious lesions such as
Cryptococcus. Berger27 developed an ultrasonographically guided stereotactic device that could
be used through a minimal craniotomy site
slightly larger than a standard burr hole (Figure
8). This allowed quick and precise ultrasonographically guided biopsies to be performed
with minimal morbidity to these patients (Figure
9). It was quite gratifying to visit a patient the day
after a stereotactic ultrasonographically guided
brain biopsy and to see the patient awake, conversant, and ambulatory.
Most neurosurgeons now seem to prefer the CT
stereotactic frame guidance device or even more
sophisticated virtual reality systems with CT or
magnetic resonance images superimposed over
the surgical field. However, on occasion even
today, there is still a sometimes unplanned and
urgent call from the neurosurgical suite, because
the stereotactic frame has slipped or for some
other reason, resulting in uncertainty as to the
precise location of the target lesion. We have
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History of Intraoperative Ultrasonography

found the use of an endoluminal prostate probe


with a biopsy guidance device to be very satisfactory in these situations, allowing for scanning
through a small craniotomy defect and resulting
in excellent imaging of brain anatomy and detection of focal lesions, as well as allowing the ability
for real-time image-guided biopsies, drainages,
or shunt catheter placements (Figure 10).
Simultaneously with the intracranial applications of ultrasonography was the equally profound development of IOUS techniques for
spinal sonography, as first reported by Dohrmann
A

and Rubin.28 By having the laminectomy incision


site filled with degassed sterile saline, elegant
imaging of the spinal cord and surrounding structures could be obtained; the normal anatomy
was well defined by Quencer and Montalvo.29
Excellent imaging could be obtained with the
dura still intact, thus ensuring that the laminectomy site would be optimal for the proposed surgical procedure before incising the dura.30
Intraoperative ultrasonography allowed accurate distinction of intramedullary from intradural, extramedullary tumors. Most intramedullary
tumors were hyperechoic, as with brain tumors,
but some were more isoechoic and recognized
primarily by cord swelling and effacement or distortion of the central spinal canal.30,31 Many

Figure 8. Berger biopsy guidance system. A, Ring that screws


into the burr hole and central pivot with biopsy plug and needle in place. B, Intraoperative image shows the ultrasonic
probe in the pivot during scanning to determine the optimal
path for biopsy. C, The probe is then replaced with the biopsy
plug, and the brain biopsy needle is placed precisely into the
target lesion.

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Figure 9. A, Intraoperative scan through the Berger biopsy


device of a brain metastasis in a patient with lung cancer. The
distance to the center of the metastasis is marked by the caliper.
B, Imaging immediately after a biopsy showing the path of the
biopsy needle precisely entering the metastatic lesion.

spinal cord astrocytomas and ependymomas


have areas of cystic degeneration, and IOUS was
particularly important in guiding surgical biopsies to the solid components of these tumors,
thereby increasing the diagnostic yield and
decreasing the number of biopsies required for
diagnosis.
Intraoperative ultrasonography was also particularly useful in defining the extent of
extramedullary masses, particularly those that
were deep to the spinal cord.32 The planning of
surgical exploration was improved by the IOUS
information about tumor extent, the relationship of the tumor to the spinal cord, and adjacent nerve roots. Assessment of completeness of
the surgical excision was also an important function of spinal IOUS.
The definition of syringomyelia and its distinction from cystic degeneration of intramedullary
tumors was recognized early as an invaluable
contribution of IOUS.33 The septations and compartmentalizations of complex syringes can be
accurately depicted by IOUS, and this is of
paramount importance to ensure complete
drainage of a syrinx. Real-time guidance can be
readily provided to ensure that all compartments
of a complex syrinx are adequately drained
(Figure 11).

Figure 10. Recent IOUS image of a glioblastoma multiforme. Biopsy of this highly vascular tumor was safely performed using real-time guidance with an endoluminal probe. The path of the biopsy needle is indicated by the arrow.

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History of Intraoperative Ultrasonography

Intraoperative ultrasonography has also been


quite helpful in defining the extent of vascular
lesions in the cord, such as intramedullary or dural
arteriovenous malformations.34 Arteriovenous
Figure 11. Cervical cord syrinx. A, Calipers mark the distance
from the dorsal surface of the cord to the syrinx before shunt
placement. B, The shunt catheter can be seen entering the cord
and syrinx cavity (arrows). The syrinx has been completely
decompressed.

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malformations are poorly shown with gray scale


ultrasonography but are much more effectively
depicted with color flow and power Doppler imaging. Similarly, some spinal hemangioblastomas
can only be fully depicted by adding the information of color Doppler imaging to that of gray scale
ultrasonography.35
Spinal IOUS also plays an important role in other
areas of spinal surgery, including surgery for trauma, to help detect hematomas, foreign bodies, and
bone fragments and to guide evacuation or
removal of these. Similarly, when unstable spine
fractures require metal rod fixation, IOUS is quite
valuable in assessing the adequacy of cord
decompression.36
A somewhat more recent development in IOUS
has been the development of laparoscopic ultrasonography (LUS) devices, although, once again,
early investigators were reporting on the use of Amode laparoscopic transducers as early as 1964.37
As with open IOUS, real clinical utility required the
development of real-time gray scale ultrasonography and miniaturized transducers, which could
be mounted on a long shaft and be inserted
through standard laparoscopic 10- to 11-mmdiameter ports. The initial instruments developed
by Frank et al38 and Fornari et al39 were mounted
on completely rigid shafts, using either linear array
or rotating sector transducers. However, the limitations of a rigid system were soon apparent, and
manufacturers were able to develop flexible tip
transducers, which could both flex and extend in
one plane and move left to right in an orthogonal
plane, with the use of control systems similar to
those developed for endoscopy. Both linear array
and curvilinear sector probes were developed,
often with multiple frequencies, typically ranging
from 5 to 7.5 MHz, and also offering color flow and
power and pulsed Doppler imaging. The rapid
growth of laparoscopic cholecystectomy in the
late 1980s and 1990s led to great enthusiasm for
the use of LUS in assessment of the biliary tract, in
particular for choledocholithiasis. Liu et al40
demonstrated successful visualization of common duct stones by LUS, but a large series by
Jakimowicz41 showed that, whereas LUS yielded
excellent-quality images of the common bile duct,
unsuspected abmormalities were detected infrequently, in less than 4% of the patients. Therefore,
routine use of LUS at the time of laparoscopic
cholecystectomy is not indicated, but it may certainly play a role in more selective cases in which
evaluation of the biliary tract is required.
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In a prospective study, Hann et al42 demonstrated the utility of LUS in evaluating the resectability
of patients with pancreatic cancers, finding additional information in approximately one third of
cases and making changes in the surgical treatment in 17%. Evaluation of peripancreatic vasculature for tumor invasion and detection of
metastatic lymphadenopathy and metastatic liver
disease were able to be done by LUS in an attempt
to determine whether surgical resection was feasible and appropriate. Similar findings were also
reported by Bemelman et al,43 although with the
development of multidetector CT scanning and
much higher-speed, higher-quality MRI, preoperative evaluation of pancreatic cancer resectability
has become much more accurate.
Laparoscopic ultrasonography of the liver
afforded similar excellent resolution and highly
sensitive detection of small liver lesions, which
were frequently undetectable by preoperative
imaging in the 1990s. We reported finding additional liver tumors in 7 of 18 patients, with most
of the lesions ranging from 0.4 to 1.0 cm,44 a finding that was confirmed by John et al,45 who
reported detection of 33% more liver lesions with
LUS and also emphasized that the rate of successful resection increased from 48% to 93%
when patients underwent laparoscopy and LUS
before open resection. This indicated that
laparoscopy and LUS together were able to prevent many unnecessary open surgical procedures in patients who proved to be unresectable.
The superior resolution of LUS is also capable of
depicting other important findings that may
affect resectability, such as invasion of the portal
or hepatic veins. However, once again, the rapid
acquisition times with current, state-of-the-art
liver MRI or multidetector CT have so improved
detection of liver lesions that the pickup rate of
additional lesions by LUS or IOUS may be less
now than had been established in previously
published series.
As a result of the steadily improved capabilities of CT and MRI in preoperative imaging, the
current roles of IOUS and LUS have changed
from a primary emphasis on increased detection of disease to a more active role in guidance
of therapeutic interventions during surgery.
Intraoperative ultrasonography can be invaluable in helping to plan subsegmental liver
resections for primary or metastatic neoplasms
by precisely defining the tumor margins, particularly the deep margins, which may not be palJ Ultrasound Med 2004; 23:14071420

pable. Resection planes can be planned and


marked on the liver surface for deep wedge
resections or individual segmental resections.
Similarly, for living related adult split liver transplantation, the plane of resection for harvesting
of the right lobe of the liver from the donor can
be accurately defined in real time by localizing
the course of the middle hepatic vein and again
marking the resection plane on the liver surface
with electrocautery, surgical clips, or other means.
Many cancers have a predilection to spread
within the abdomen along the peritoneal surfaces of solid organs as well as in the leaves of the
mesentery and in the omentum. Frequently,
these deposits are too small for any preoperative
imaging to detect; hence, staging laparoscopy is
still advocated by many before committing to an
open surgical resection because the presence of
these small metastatic lesions would obviate any
attempt at surgical resection for a cure.
Laparoscopic ultrasonography has a role in evaluating small surface lesions because benign
entities such as small cysts, hemangiomas, and
biliary hamartomas could simulate the presence
of tiny metastatic lesions as seen through the
laparoscope. Laparoscopic ultrasonography
may also provide excellent guidance for transabdominal biopsy of suggestive lesions during
laparoscopy, when the specific histologic characteristics of a lesion would affect the decision of
whether to proceed with surgical intervention, as
shown in Figure 12. Similarly, both IOUS and,
increasingly now, LUS have proved effective in
guiding intraoperative tumor ablations using
cryoablation, radio frequency ablation, laser
energy, and other ablative procedures. Although
many, if not most, of these ablations can be successfully accomplished percutaneously with
image guidance, in many clinical settings, the
choice is made to perform the procedure intraoperatively, and in those settings, ultrasonographic guidance is essential for precise
placement of the ablation probes and for monitoring the ablation procedure to ensure complete and adequate treatment.
Intraoperative ultrasonographic guidance continues to have a very important role in neurosurgical interventional procedures, including
selection of optimal routes for real-time guided
brain biopsies, aspirations, drainages, and shunt
catheter placements. If a surgical resection is
planned, IOUS is often used to assess completeness of the resection (Figure 13).
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History of Intraoperative Ultrasonography

Figure 12. A, Laparoscopic image of a large pancreatic mass


with demonstration of the adjacent biliary stent. Because of a
clinical suspicion of lymphoma and failed CT-guided biopsies, a
laparoscopic biopsy was undertaken. B, Arrows indicate a reverberation artifact from the biopsy needle within the mass. This
proved to be a benign lymphoplasmacytic sclerosing pancreatitis.

Figure 13. Cystic glioma. A, The multiple septations and nodular elements of the tumor are clearly depicted. B, After surgical
resection, the resection site was filled with sterile saline, and
subsequent scanning showed no evidence of a residual tumor.

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In addition to the important and expanding


current uses of IOUS and LUS, there are some
exciting new developments, which may expand
the role of ultrasonography in the operating
room. Many authors have been enthusiastic
about the role of 3-dimensional ultrasonography
in facilitating ultrasonographically guided interventional ablative procedures, notably in
cryosurgery of the prostate.46 There has also
been some investigation of robot-assisted
3-dimensional transrectal ultrasonography as a
guidance mechanism for prostate brachytherapy to improve the accuracy of seed placement.47
Additional work is under way to develop a robotic system for assisting intraoperative ultrasonographically guided hepatic tumor ablation.48
Another new and exciting area of development
is the attempt to fuse LUS images with preoperative CT scans. By obtaining fiduciary markers
from fixed anatomic locations on the CT scan,
such as bony landmarks or origins of mesenteric

vasculature, the LUS image can be correlated to


the anatomy on the CT scan with electromagnetic tracking sensors. Therefore, with this system,
simultaneous displays of the laparoscopic
image, the LUS image, and the real-time rendering of the ultrasonographic image plane relative
to the vascular and bony anatomy can be
obtained.49 This allows for more rapid orientation and understanding of the anatomic plane of
the LUS image relative to surrounding structures
(Figure 14). A prototype system has been assembled and tested, showing improvement in orientation of the operator and increased confidence
in identifying surgical anatomic landmarks.50
Intraoperative and laparoscopic ultrasonography have become indispensable elements of
many surgical procedures. The continued
improvements in speed of data collection and
miniaturization will undoubtedly lead to even
more widespread applications. The future,
indeed, is bright for IOUS and LUS.

Figure 14. Virtual integration of CT and LUS. Three sets of images are shown, with the left images showing the laparoscopic view of the ultrasonic
probe, the middle images showing the LUS view at that site, and the right images showing the virtual integrated rendering of the plane of the ultrasonographic image relative to the bony and vascular landmarks.

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History of Intraoperative Ultrasonography

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