Professional Documents
Culture Documents
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
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
1408
Kane
1409
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
1410
Kane
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
1411
1412
Kane
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.
1413
1414
Kane
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
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.
1416
Kane
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.
1417
References
1.
Schlegel JU, Diggdon P, Cuellar J. The use of ultrasound for localizing renal calculi. J Urol 1961;
86:367369.
2.
3.
4.
Dyck P, Surze T, Barrows HS. Intraoperative ultrasonic encephalography of cerebral mass lesions. Bull Los
Angeles Neurol Soc 1966; 31:114124.
5.
Purnell EW, Cappaert WE, Sokollu A. B-scan ultrasonography during orbital surgery. J Clin Ultrasound
1973; 1:3235.
6.
7.
8.
9.
10. Kane RA, Hughes LA, Cua EJ, Steele GD, Jenkins RL,
Cady B. The impact of intraoperative ultrasonography on surgery for liver neoplasms. J Ultrasound
Med 1994; 13:16.
11. Parker GA, Lawrence W Jr, Horsley J III, et al.
Intraoperative hepatic ultrasound of the liver affects
operative decision making. Ann Surg 1989;
209:569577.
12. Onik G, Kane RA, Steele G, et al. Monitoring hepatic cryosurgery with sonography. AJR Am J
Roentgenol 1986; 147:665669.
13. Ravikumar TS, Kane R, Cady B, Jenkins R, Clouse M,
Steele G Jr. A 5-year study of cryosurgery in the
treatment of liver tumors. Arch Surg 1991;
126:15201524.
1418
23. Rubin JM, Dohrmann GJ. Intraoperative neurosurgical ultrasound in the localization and characterization of intracranial masses. Radiology 1983;
148:519524.
24. Pasto ME, Rifkin MD. Intraoperative ultrasound
examination of the brain: possible pitfalls in diagnosis and biopsy guidance. J Ultrasound Med 1984;
3:245249.
25. Shkolnik A, McLone DG. Intraoperative real-time
ultrasonic guidance of ventricular shunt placement
in infants. Radiology 1981; 141:515517.
26. Enzmann DR, Irwin KM, Marshall WH, Silverberg
GD, Britt RH, Hanbery JW. Intraoperative sonogra-
Kane
40. Liu JB, Feld RI, Goldberg BB, et al. Laparoscopic gray
scale and color Doppler US: preliminary animal and
clinical studies. Radiology 1995; 194:851857.
1419
1420