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Operative ultrasound in general surgery
Operative
Ultrasound
Junji Machi, MD, PhD, Bernard
BACKGROUND: Since the introduction of real-time B-mode ultrasound during surgery almost 20 years ago, the use of operative ultrasound (OUS) has gradually expanded to a variety of surgical fields. METHODS: A review of the history, technology, and specific applications of OUS in general surgery is presented with our clinical results of over 2300 operations. RESULTS: The benefits provided by OUS are the acquisition of new information not otherwise available, complement to or replacement for operative radiography, confirmation of satisfactory completion of an operation, and guidance of surgical procedures. OUS possesses many advantages as an intraoperative tool, including safety, speed, unique imaging information, wide applicability, high accuracy and procedure guidance capability. CONCLUSION: OUS is gaining wider acceptance in hepatobiliary, pancreatic, endocrine, and vascular surgery. Newer OUS modalities-color Doppler imaging and laparoscopic ultrasound-potentially may widen the applications of OUS in general surgery. Am J Sot-g. 1996;172:15-20.
T
he use of ultrasound during surgery-operative ultrasound (OUS) -has expanded to a variety of surgical fields. Our experience with OUS started at the University of Illinois during the chairmanship of Lloyd Nyhus in the Department of Surgery. Dr. Nyhus strongly encouraged its application to general surgery. Since then, we have performed OUS during more than 2800 operations, including over 2300 general surgical operations, at the University of Illinois, Kurume University (Japan), Medical College of Pennsylvania, and Mercy Hospital of Pittsburgh.ld4 Based on our experience and a literature review of OUS, we summarize the history, technology, and specific applications of OUS in general surgery.
HISTORY While operative radiography such as operative cholangiography started in the 193Os, the use of OUS did not occur until the early 1960s. Diagnostic medical ultrasound was just getting started after World War II and was relatively primitive by today’s standards. The early OUS scanning was mostly with A-mode imaging, which presented as blips on From the Department of Surgery, Medical College of Pennsylvania, Philadelphia, Pennsylvania. Requests for reprints should be addressed to Bernard Sigel, MD, Medical College of Pennsylvania, Department of Surgery, 3300 Henry Avenue, Philadelphia, Pennsylvania 19129.
0 1996 by Excerpta All rights reserved.
Medica,
Inc.
in General Sigel, MD,
Philadelphia,
Surgery
Pennsylvania
a monitor screen. Schlegel first employed A-mode OUS to locate renal calculi in 1961.5 Hayashl in 1962, Knight in 1963, and Eiseman in 1965 applied this A-mode method to detect bile duct calculi at operation.‘,‘,” In the 196Os, OUS was also attempted during neurosurgery to locate cerebral mass lesions.’ However, A-mode or early B-mode imaging did not lead to widespread use of OUS because it was not easily performed or interpreted. The more recent development of real-time B-mode imaging, particularly high-frequency high-resolution ultrasound, rekindled interest in OUS in the late 1970s. The first applications of real-time B-mode OUS were reported by Cook for localizing renal calculi in 1977,’ by Makuuchi for detecting hepatic tumors in 1979,’ and Lane and Sigel for diagnosing biliary calculi in 1979.“~” In the United States, cylindrical sector probes were employed during operation at that time, whereas flat linear-array probes were developed in Japan by Makuuchi in 1979, mainly for OUS scanning of the liver.” In the early 198Os, B-mode OUS was introduced to various surgical fields: by Rubin, Dohrmann, and Shkolnik during neurosurgery in 1980 and 1981, “,” by Sigel and Lane during endocrine surgery (parathyroid, islet cell tumors) in 1981 and 1982,‘4,” and by Sahn during cardiac surgery in 1982.16 We also used OUS extensively during pancreatic and vascular surgery at that time. Over the past 15 years, high-resolution real-time B-mode ultrasound has been used to examine small and superficial structures (eg, breast, thyroid, parathyroid and superficial blood vessels) and has become the standard equipment for OUS. A newer modality, color Doppler imaging, was also introduced during cardiac surgery, first by Takamoto in 1985.17 We have applied color Doppler imaging to vascular and general surgery OUS.‘,‘s With the advent of laparoscopic procedures, laparoscopic or intracorporeal ultrasound has generated new interest. Laparoscopic ultrasound was originally developed for examining intra-abdominal diseases in the mid-1980s.” More recently, rigid and flexible laparoscopic probes, passing through 10 mm trocars, were developed for delineation of the biliary tract, liver, pancreas, and other abdominal organs.‘“-~” The application of laparoscopic ultrasound is likely to increase with the more frequent use of diagnostic laparoscopic examinations.
TECHNOLOGY The most suitable and most frequently used instruments for OUS are real-time B-mode ultrasound scanners with high-frequency transducers.‘,’ Higher frequencies result in increased resolution, but decreased depth of penetration. Consequently, there needs to he
5.00
15
OPERATIVE
TABLE
ULTRASOUND
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SIGEL
!
I Comparison
of Screening
Methods
Preoperative Ultrasound Sensitivity Specificity Predictability of a positive Predictability of a negative Overall accuracy
in Diagnosing
40.8% 95.8% 87.0% 70.2% 73.4%
test test
Liver
Metastasis
Preoperative Computed Tomography 49.0% 94.4% 85.7% 72.9% 75.9%
from
Colorectal
Carcinoma
Surgical Exploration
Operative Ultrasound
66.0% 89.3% 80.8% 79.2% 79.8%
93.8% 94.4% 92.0% 95.7% 94.2%
P-value <0.0001* <0.05** <0.0001’ <0.0001*
+ Operatwe ultrasound versus each of the other three procedures. ‘* Operative ultrasound versus surgical exploration.
sufficient during OUS examination. With high-frequency high-resolution ultrasound, small lesions including 1 mm biliary stones, 3 to 4 mm tumors, 1 to 2 mm cysts, and 1 to 2 mm vascular defects can be detected. The size of ultrasound probes should he small enough to be manipulated in operative fields, which at times are limited in space. The shape of the probe is an important feature for OUS scanning. There are two fundamental shapes, flat and cylindrical. A flat T- or I-shaped side-viewing prohe with linear-array transducers is appropriate for scanning of relatively large organs such as the liver, pancreas, and kidney. Flat probes are essential for examining the liver under the abdominal wall or the diaphragm. A pencil-like cylindrical front-viewing probe with sector images is suitable for scanning of small organs or structures deep in the operative field, such as the extrahepatic bile duct or Hood vessels. Laparoscopic ultrasound is the latest mode of OUS. It is basically real-time B-mode ultrasound, mostly using lineararray transducers. The transducers are mounted at or near the tip of a long shaft, which is 10 mm in diameter. Currently flexible probes are available in addition to rigid probes. With the laparoscopic ultrasound probe, complete examination of the extrahepatic bile duct is possible during laparoscopic cholecystectomy.‘O’? The intrahepatic bile duct can also he imqed by placing the probe over the liver surface. Laparoscopic ultrasound has recently been introduced for evaluating the liver and pancreas during exploratory laparoscopy, especially in determining the stage and the resectability of malignant turnors.“~” Color Doppler imaging exhibits blood flow by real-time color mapping on conventional B-mode images.‘.‘.“.‘” With current color Doppler scanners, blood flow with a velocity as slow as 4 to 5 mm/set can he displayed in color. The color, either red or blue, corresponds to the direction of flow in relation to the transducer. As the flow increases in velocity, the color becomes brighter or whiter. In our experience, color Doppler has offered additional useful information in addition to anatomical information provided by B-mode imaging during general and vascular surgery.3,‘h Benefits of color Doppler imaging during general surgery include detection and localization of small blood vessels that are difficult to identify by B-mode alone, distinguishing blood vessels from other hyperechoic areas such as ducts and tissue spaces, determining the relation of tumors to vascular structures such as vascular invasion by carcinoma, appraising blood flow to organs after surgical procedures, and improving needle localization for guidance. Color Doppler imaging has also been adapted to laparoscopic ultrasound 16
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probes. During laparoscopic OUS scanning, color Doppler imaging is particularly useful to rapidly distinguish bile ducts from vessels such as the hepatic artery.
SPECIFIC APPLICATIONS Use of OUS during liver, hiliary, pancreatic, endocrine, and vascular surgery varies and each of these specific applications is briefly reviewed. Liver For both primary and metastatic liver tumors, OUS is indicated to determine resectability and to select the type of operation needed. OUS screening is also performed for metastatic tumors, particularly from colorectal carcinoma. When hepatic resection is performed, OUS is used for guidance of tissue dissection.‘m4,‘4m’” OUS provides valuable informr-ltion that is not obtained by preoperative studies and intraoperative exploratory inspection and palpation of the liver. OUS can localize nonpalpable tumors, eg, small hepatocellular carcinoma in cirrhotic liver. Extention of malignant tumors to the intrahepatic portal or hepatic vems and the presence of tumor thromhi or intrahepatic metastases is more accurately delineated. Based on OUS, which can be performed immediately after laparotomy, resectahility can be assessecl, and the most appropriate resectional procedure can he selected. Cysts and abscesses can he Jetected and localized. In our experience, OUS provided useful information during 112 of 126 hepatic operations (88.9%).’ 4 On the basis of OUS findings, decisions for surgical procedures initially proposed on the basis of preoperative studies and surgical exploration were altered in 48 of 126 operations (38.1%). Several other reports demonstrated that surgical management of hepatic tumors had been changed in 30% to 50% of operations by using OUS.‘“,” One recent study by John using laparoscopic exploration of 50 hepatic tumors revealed that laparoscopic ultrasound identified tumors not visible by laparoscopy in 33% and provided staging infor, mation in addition to that derived from laparoscopy alone in 42%.” OUS is more accurate than conventional preoperative imaging methods and surgical inspection and palpation in screening for liver metastasis. In our study of 250 patients with colorectal carcinomas, screening OUS detected otherwise unrecognized liver metastases in 25 patients ( 10.0%).4,‘” These metastases were 4 X 4 mm to 15 X 18 mm in size and were nonpalpable. On the basis of lesions found, OUS was significantly superior to other methods in JULY
1996
/ OPERATIVE TABLE
IN SURGERY/MACH1
from
Carcinoma
AND
SIGEL
II Operative
Author
ULTRASOUND
(Year)
Ultrasound Number
Machi (1987) Boldrini (1987) Russo (1989) Olsen (1990) Machi (1991) Stadler (1991) Charnley (1991) Stone (1994) * Number ‘* Number
of patients
TABLE
Ill
of paknts
in Diagnosing
(Screening)
Liver
Diagnosis ous*
of Patients 84 86 70 213 189 85 99 56
10 3 5 21 18 12 9 3
of Two
Screening Machi
test test
Followup
6-24 18-54
by other
in Diagnosing
months
92.4% 99.3% 94.8%* 99.0% 98.5%
84.4% 95.5% 71.7%* 97.9% 94.2%
Biliary Tract During hiliary tract operations OUS is indicated to diagnose previously unknown gallbladder calculi, evaluate biliary tumors, localize obscured bile ducts, and screen for bile duct calculi.‘. 4.15.3h OUS can diagnose gallbladder calculi as small as 1 mm and gallbladder polyps 1 to 2 mm in size. During intraoperative examination of gallbladder and bile duct carcinomas, OUS can more precisely assess tumor invasion of the liver parenchyma, involvement of the portal vein and hepatic artery, and metastasis to the lymph nodes and liver. The
3/60
(37) months
20/l 51 (13.2%)
8/47
tests or mefaslasis
Bile Duct
(5.0%)
occured
during
(17.0%)
foilowup
periods
Stones Jakimowicz
Operative Cholangiography
terms of the sensitivity, predictability of a negative test and overall accuracy (Table I). Others have confirmed our findings that routine OUS can detect so-called “occult” metastasis in approximately 5 to 10% of operations as sum‘. in Table II.‘nm3’ mari-ed A unique feature of OUS is its ability to directly guide surgical procedures on the liver. OUS guidance is used either in needle placement or for hepatic tissue dissection.3,4 Needle placement facilitates biopsy, especially of nonpalpable lesions, aspiration of cavitary lesions, injection of agents or contrasts, and catheterization of bile ducts. Local nonresectional treatment of hepatic tumors such as cryosurgery can also be guided hy OUS. Needle guidance can also he performed during laparoscopic ultrasound. OUS guidance has directed anatomic resections of segments and subsegments. New hepatic resectional procedures such as OUS-guided systematic suhsegmentectomy have heen developed.‘5 During 89 hepatic resections, we have used OUS guidance techniques in 67 operations (75.3%).
False-Negative ous** (%)
(median)
(23 months)
ultrasound. was diagnosed
Methods
Colorectal
and Sigel
Operative Ultrasound Sensitivity Specificity Predictability of a positive Predictability of a negative Overall Accuracy
Metastasis by
(11.9%) (3.5%) (7.1%) (9.9%) (9.5%) (14.1%) (9.1%) (5.4%)
who had metastasis which was diagnosed on/y by operatwe in whom operatwe ultrasound was negative, but metastasis
Comparison
only (%)
Operative Ultrasound
Operative Cholangiography
93.7% 98.8% 96.3% 97.9% 97.5%
86.1% 95.6% 86.9% 95.3% 94.4%
extrahepatic bile duct may be ohscured by adhesion from previous surgery, inflammation, or tumors; these distort the anatomy, and increase the chance of bile duct injuries. In such situations, bile ducts can be quickly localized by OUS, especially with color Doppler imaging, which readily distinguishes blood vessels from bile ducts. During 73 operations for benign and malignant Mary diseases, OUS was considered useful in 60 operations (82.2X).‘.’ The major use of OUS has heen for screening of bile duct calculi at the titne of cholecystectomy. Before the era of laparoscopic cholecystectomy, we evaluated the accuracy of OUS by comparing it with operative cholangiography.‘-4,35 OUS was performed during 666 operations, while operative cholangiography was performed during 401 operations. There were 6 operations in pregnant women and 12 operations in patients with contrast allergy, in which cholangiography was avoided. Technically unsuccessful results were encountered in 1.2% for OUS versus 5.5% for operative cholangiography. The two teats were comparable in terms of the sensitivity, specificity, and predictability of a negative test and overall accuracy, whereas OUS was significantly superior in the predictability of a positive test (Table III ). Common hilt duct exploration was performed in 86 operations (12.9%). and the Me duct stones were detected in 77 operations, with a positive hile duct exploration rate of 89.5%. A similar result in the accuracy of OUS compared to cholangiography was reported in Jakimowicz’s study of 491 patients’” (Table III). Our preliminary experience of laparoscoplc ultrasound during 25 laparoscopic cholecystectomies showed that the findings of ultrasound concurred with those of cholangiography.‘@ In
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addition, laparoscopic ultrasound was completed in examining the bile duct in a shorter period of time than operative cholangiography (9.7 2 4.6 minutes versus 17.9 -f 8.9 minutes) (mean -C standard deviation) The feasibility of laparoscopic ultrasound during cholecystectomy has been reported by others.z2
AND
SIGEL
TABLE IV Comparison
of Preoperative Portal Vein
Sensitivity Specificity Predictability of a positive test Predictability of a negative test Overall accuracy
Studies Invasion
and Operative of Pancreatic
Ultrasound Carcinoma
Preoperative Studies
Operative Ultrasound
76.5% 54.5%
94.1% 86.4%
56.5%
84.2%
in Diagnosing
P-value P < 0.05
95.0% 75.0% Pancreas 64.1% 89.7% P < 0.01 OUS is indicated during pancreatic operations for diagnosing or defining Reproduced with permission from reference 6. complications of pancreatitis and evaluating pancreatic carcinoma.‘-4,3’ Pancreatic surgical procedures can also he guided by OUS. Localizing islet cell tumors by OUS will he has been during operations for pancreatic islet cell tumors discussed in the section dealing with endocrine operations. and parathyroid tumors. ‘-‘,“,” Pancreatitis causes multiple complications such as panDespite various imaging modalities currently availahle, creatic duct dilatation, pseudocyst, abscess, and distal bile more than one half of insulinomas and gastrinomas cannot duct stenosis. OUS helps to detect, localize, or exclude he delineated preoperatively. Furthermore, small islet cell these complications during operations, thereby reducing the tumors may not be palpable at operation. On OUS examneed for exploratory dissection. Nonpalpable pancreatic ination, islet cell tumors are almost always hypoechoic comducts and even small cysts are readily localized by OUS. At pared to pancreatic parenchyma. With high-resolution Btimes, previously unknown cysts and abscesses are diagmode ultrasound, tumors as small as 3 to 4 mm can he nosed. Preoperatively or intraoperatively suspected dilated detected. OUS is more effective for finding and localizing ducts or cysts may he excluded by OUS. In 169 operations insulinomas than for gastrinomas because insulinomas are for pancreatitis ( 150 operations for chronic pancreatitis and usually situated within the pancreas. Extrapancreatic gas19 operations for acute pancreatitis), OUS was used and trinomas arc more difficult to localize with OUS. Norton provided useful information in 124 operations ( 73.3%).3,4,‘7 and others reported the detectability of insulinomas by On the basis of OUS findings, the type of procedure ultiOUS to he 83% to loo%.” The detectability of pancreatic mately used was changed from the initially planned progastrinomas by OUS was 95% compared to 58% for extracedure in 25 operations (16.7%) for chronic pancreatitis. pancreatic gastrinomas. In our experience with 8 islet cell The stage and resectability of pancreatic carcinoma can tumors (5 insulinomas and 3 gastrinomas), OUS helped to be determined by OUS early during the course of operation. localize or exclude multiple tumors in 7 operations OUS provides information regarding tumor extension in( 87.5%).L,4 cluding vascular invasion, and lymph node and liver meImaging studies are usually not needed during operations tastasis. The accuracy of OUS in diagnosing portal vein for hyperparathyroidism. The exception to this observation tumor invasion was compared to preoperative studies that is reoperation for parathyroid tumors. Parathyroid adenoincluded computed tomography, percutaneous ultrasound, mas and hyperplasia exhibit hypoechogenicity compared to or angiography in 39 operations.4 The final diagnosis was surrounding tissue on OUS. OUS can be performed before made by surgical exploration, often with histologic confirextensive tissue dissection, and help localize parathyroid mation, that demonstrated portal vein invasion in 22 optumors. In 39 rcoperations for hyperparathyroidism reported erations. For determining portal vein invasion, OUS was by Kern, 33 of 41 tumors (80%) were accurately detected significantly superior to the combination of preoperative and localized by OUS.“’ The sensitivity of OUS was 85%, studies in terms of the specificity and overall accuracy (Tawhich was superior to that of preoperative computed toble IV In a total of 68 operations for pancreatic carcinoma, mography, ultrasound, and Technetium-thallium scan. TuOUS was considered useful in 49 operations (72.1%). Simmors at aberrant locations such as undescended adenomas ilar benefits of OUS were reported in other studies. Lapawere imaged accurately, and all intrathyroidal adenomas roscopic ultrasound has recently been reported for evaluwere detected. In our experience of 18 operations for ating pancreatic carcinoma.” parathyroid tumors, OUS accurately localized tumors in 10 OUS can guide various pancreatic procedures in a manner operations (56%) .‘,’ similar to hepatic procedures. OUS guidance is particularly useful for opening nonpalpable pancreatic ducts or pseuBlood Vessels docysts. ‘.’ These OUS-gu ided procedures are safer and When information of preoperatilre imaging studies is not quicker than blind procedures because it decreases the sufficient, OUS can he used hefore vascular reconstruction chances of complications such as vascular or ductal injuries. to examine native blood vessels if needed. However, the main indicatton of OUS is post-reconstruction evaluation Endocrine of vessel. ’ m4,4CAfter vascular reconstruction but before OUS during endocrine surgery is indicated for diagnosing, wound closure, vascular defects such as intimal flaps, localizing, and excluding endocrine tumors. Although OUS thromhi, and strictures that may cause postoperative comcan be used for thyroid and adrenal tumors, its major use plications may he detected and repaired if clinically signif-
18
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) OPERATIVE TABLE
V Comparison of Two Postreconstruction
Sensitivity Specificity Predictability of a positive Predictability of a negative Overall accuracy Reproduced
with permwon
Methods in Diagnosing of Vascular Defects
test test
from
reference
Operative Ultrasound
Operative Atteriography
93.1% 97.8% 87.1% 98.9% 97.2%
93.1% 94.5% 73.0% 98.9% 94.3%
2.
icant. Experimental and clinical studies have demonstrated that OUS is as accurate as operative arteriography in detecting these defects.lm4 In our studies of 519 vascular operations including 153 carotid endarterectomies, vascular defects were detected by OUS in 155 operations (29.9%).*x3 Of these, defects in 48 operations (9.3%) were judged to be likely to endanger patency of vascular reconstruction, and were repaired. OUS showed accuracy equal to contrast arteriography in the diagnosis of vascular defects (Table V). A similar result was reported by Lane in using OUS for carotid endarterectomy.4@ Furthermore, OUS was quicker, usually requiring less than 5 minutes for examination. Therefore, we consider OUS to be the first-choice test to examine vascular reconstruction sites. Operative color Doppler imaging that provides additional blood flow information may enhance the efficacy of OUS *,’ B 17 using OUS routinely, operative arteriography can be used more selectively when OUS results are not conclusive or when the distal vascular tree needs to be evaluated.
REFERENCES 1. Sigel B. Operative Ultrasonogru~hy. 2nd ed. New York: Raven Press. 1988. 2. Machi J. Operatiwe Ultrasono~uphr-Fundamentals and Clinical Applications. (In Japanese), Tokyo: Life Science, 1987. 3. Machi J, Sigel B. Intraoperative ultrasonography. Radiolo Clin NA. 1992;30:1085-1103. 4. Machi J, Sigel B, Zaren HA, et al. Operative ultrasonography during hepatobiliary and pancreatic surgery. World ./ Surg. 1993; 17:640-646. 5. Schlegel JU, Diggdon I’, Cuellar J. The use of ultrasound for localizing renal calculi. J Ural. 1961;86:367-369. 6. Eiseman 8, Greenlaw RH, Gallagher JQ. Localization of common duct stones by ultrasound. Arch Surg. 1965;91:195-199. 7. Tanaka K, Ito K, Wagai T. The localization of brain tumors by ultrasonic techniques. A clinical review of 111 cases. J Neurosurg. 1965;23:135-147. 8. Cook JH, Lytton B. lntraoperative localization of renal calcuh during nephrolithotomy by ultrasound scanning. J L’rol. 1977;117:543-546. 9. Makuuchi M, Hasagawa H, Yamasaki S. Newly devised intraoperative probe. Image technology and information display. Medical. 1979;11:1167-1168. 10. Lane RJ, Cracker EF. Operative ultrasonic bile duct scanning. Aust NZJ Surg. 1979;49:454-458. 11. Sigel B, Spigos DG, Donahue PE, et al. Intraoperative ultrasonic visualization of biliary calculi. Curr Surg. 1979;36:158-159. 12. Rubin JM, Mirfakhraee M, Duda EE, et al. Intraoperative ultrasound examination of the brain. Radiology. 1980;137:831-832. THE
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13. Shkolnik A, McLane DC. Intraoprrative real-time ultrasonic guidance of ventricular shunt placement in Infant. Radiolog)l. 1981;141:515-517. 14. Sigel B, Draft AR, Nyhus LM. et al. Identification of a paraby operative ultra\onugraphy. Arch Surg. thyroid adenoma 1981;116:?34-235. 15. Lane RJ, Coupland GA. Operative ultrasonic features of insulinomas. Am J Surg. 1982;144:585-587. 16. Sahn DJ, Barratt-Boyes BG, Graham K, et al. Ultrasonic imaging of the coronary arteries in open-chest humans: evaluation of coronary atherosclerotic lesions during cardiac surgery. Circulation. 1982;66:1034-1044. 17. Takamoto, S, Kyo, S, Adachi, H, et al. Intraoperative color flow mapping by real-time two-dimensional Doppler echocardiography for evaluation of valvular and congenital heart disease and vascular disease. J Thorac Curdiovasc Surg. 1985;90:802-812. 18. Machi J, Sigel B, Kurohiji T, et al. Operative color Doppler imaging for general surgery. J L~ltn~sound Med. 1993;12:455-461. 19. Ohta Y, Fujlwara K, Sato Y, et al. New ultrasound laparoscope for diagnosis of intraahdominal dise,\ses. Gnstromtest En&c. 1983;29:289-294. 20. Machi J, Sigel B, Zaren HA, et al. Technique of ultrasound examination during laparoscopic cholecystectomy. Surg Endosc. 1993;7:544-549. 21. Muruglah M, Paterson-Brown S, WI&or JA, et al. Early experlence of laparoscopic ultrasonography m the management of pancreatic carcinoma. Surg Endosc. 1991;7:177-181. 22. Stiegmann G’v’, McIntyre RC, Pearlm,m NW. Laparoscopic intracorporeal ultrasound. An alternative to cholangiography? Surg E&XC. 1994;8:167-172. 23. John TG, Greig JD, Croshie JL, et nl. Superior staging of liver tumors with laparoscopy and laparoscopic ultrasound. Ann Surg. 1994;220:711-719. 24. Castaing D, Emond J, Kunstlinyer F, Bismuth H. Utility of operative ultrasound in the surgical management of liver tumors. Ann Surg. 1986;204:600-605. 25. Makuuchi M, Hasegawa H, Yamasaki S, et al. The use of operative ultrasound as an aid to liver resection in patients with hepatocellular carcinoma. World J Surg. 1987;11:615-621. 26. Ritkin MD, Rosato FE, Branch HM, et al. lntraoperative ultrasound of the liver. An important adjunctive tool for decision makmg in the operatmg room. Ann StLrg. 1987;205:466-472. 27. Parker GA, Lawrence W, Jr Ho&y JS, et al. Intraoperative ultrasound of the liver affects operative drcismn tnaking. Ann Surg. 1989;209:569-577. 28. Machi J, Isomoto H, Kurohiji T, er al. Accuracy of intraoperative ultrasonography in diagnosing liver metastasis from colorectal cancer: evaluation with postoperative follow-up results. World J Surg. 1991;15:551-557. 29. Boldrini G, Gaetdno AM, Giovannmi I, et al. The systematic use of operative ultrasound for detection of hver metastases during colorectal surgery. World] Surg. 1987;11:622-627. 30. Russo A, Sparacino G, Plaja S. et al. Role of intraoperative ultrasound in the screening of liver metastases from colorectal carcinoma: initial experiences. J Surg On&. 1989;42:249-255. 3 1. Olsen AK. Inrraoperative uItrasonography and the detection of liver metastases in patients with colorectal cancer. Br J Surg. 1990;77:998-999. 32. Stadler J, Holscher AH, Adolf J. Intraoperative ultrasonographic detectlon of occult liver metastases in colorectal cancer. Surg Endosc. 1991;5:36-40. 33. Charnley RM, Morris DL, Dennison AR, et al. Detection of colorectal liver metastases using intraoperative ultrasonography. Br J Surg. 1991;78:45-48. 34. Stone MD. Kane R, Jr Bathe A, et al. Intraoperative ultrasound imaging of the liver at the time of colorectal cancer resection. Arch Surg. 1994;129:43 l-436.
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35. Sigel B, Machi J, Beitler JC, et al. Comparative accuracy of operative ultrasonography ,rnd cholanpiography in detecting common duct calculi. Sur‘Tuy. 1983;94:71 i-720. 16. Jakimowicz JJ, Rutten H, Jurgens PJ, Carol EJ. Comparison of operattve ultrasonography and radiography in screening of the cornmon hde duct for calculi. World ] Surg. 1987; 11:628-634. 37. Sqyl B, Machi J, Ramos JR, et al. The role of imaging ultrasound during pancreatic surgery. Ann Surg. 1984;2@0:486-493. 38. Zeiger MA, Shawker TH, Norton JA. Use of intraoperative
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--F World J surg. ultrasono~raphy to locahze ihlet cell tumors. 1993;17:448-454. 39. Kern KA, Shawker TH, D ~~ppman JL, et nl. The use of highresolution ultrasound to locate parathyroid tumor:, during reoperatians for primary hypcrp”‘“thyr~)i~lihlrl. World J Surg. 1987;l 1:579585. 40. Lane RJ. Ackroyd N, Applehq M, ( ;r,lham J. The application of operative ultrasound immediately f;&wm~ cxotid endarterectomy. World 1 Surg. 1987;11:593-597.
JULY
1996
Ultrasound
Junji Machi, MD, PhD, Bernard
BACKGROUND: Since the introduction of real-time B-mode ultrasound during surgery almost 20 years ago, the use of operative ultrasound (OUS) has gradually expanded to a variety of surgical fields. METHODS: A review of the history, technology, and specific applications of OUS in general surgery is presented with our clinical results of over 2300 operations. RESULTS: The benefits provided by OUS are the acquisition of new information not otherwise available, complement to or replacement for operative radiography, confirmation of satisfactory completion of an operation, and guidance of surgical procedures. OUS possesses many advantages as an intraoperative tool, including safety, speed, unique imaging information, wide applicability, high accuracy and procedure guidance capability. CONCLUSION: OUS is gaining wider acceptance in hepatobiliary, pancreatic, endocrine, and vascular surgery. Newer OUS modalities-color Doppler imaging and laparoscopic ultrasound-potentially may widen the applications of OUS in general surgery. Am J Sot-g. 1996;172:15-20.
T
he use of ultrasound during surgery-operative ultrasound (OUS) -has expanded to a variety of surgical fields. Our experience with OUS started at the University of Illinois during the chairmanship of Lloyd Nyhus in the Department of Surgery. Dr. Nyhus strongly encouraged its application to general surgery. Since then, we have performed OUS during more than 2800 operations, including over 2300 general surgical operations, at the University of Illinois, Kurume University (Japan), Medical College of Pennsylvania, and Mercy Hospital of Pittsburgh.ld4 Based on our experience and a literature review of OUS, we summarize the history, technology, and specific applications of OUS in general surgery.
HISTORY While operative radiography such as operative cholangiography started in the 193Os, the use of OUS did not occur until the early 1960s. Diagnostic medical ultrasound was just getting started after World War II and was relatively primitive by today’s standards. The early OUS scanning was mostly with A-mode imaging, which presented as blips on From the Department of Surgery, Medical College of Pennsylvania, Philadelphia, Pennsylvania. Requests for reprints should be addressed to Bernard Sigel, MD, Medical College of Pennsylvania, Department of Surgery, 3300 Henry Avenue, Philadelphia, Pennsylvania 19129.
0 1996 by Excerpta All rights reserved.
Medica,
Inc.
in General Sigel, MD,
Philadelphia,
Surgery
Pennsylvania
a monitor screen. Schlegel first employed A-mode OUS to locate renal calculi in 1961.5 Hayashl in 1962, Knight in 1963, and Eiseman in 1965 applied this A-mode method to detect bile duct calculi at operation.‘,‘,” In the 196Os, OUS was also attempted during neurosurgery to locate cerebral mass lesions.’ However, A-mode or early B-mode imaging did not lead to widespread use of OUS because it was not easily performed or interpreted. The more recent development of real-time B-mode imaging, particularly high-frequency high-resolution ultrasound, rekindled interest in OUS in the late 1970s. The first applications of real-time B-mode OUS were reported by Cook for localizing renal calculi in 1977,’ by Makuuchi for detecting hepatic tumors in 1979,’ and Lane and Sigel for diagnosing biliary calculi in 1979.“~” In the United States, cylindrical sector probes were employed during operation at that time, whereas flat linear-array probes were developed in Japan by Makuuchi in 1979, mainly for OUS scanning of the liver.” In the early 198Os, B-mode OUS was introduced to various surgical fields: by Rubin, Dohrmann, and Shkolnik during neurosurgery in 1980 and 1981, “,” by Sigel and Lane during endocrine surgery (parathyroid, islet cell tumors) in 1981 and 1982,‘4,” and by Sahn during cardiac surgery in 1982.16 We also used OUS extensively during pancreatic and vascular surgery at that time. Over the past 15 years, high-resolution real-time B-mode ultrasound has been used to examine small and superficial structures (eg, breast, thyroid, parathyroid and superficial blood vessels) and has become the standard equipment for OUS. A newer modality, color Doppler imaging, was also introduced during cardiac surgery, first by Takamoto in 1985.17 We have applied color Doppler imaging to vascular and general surgery OUS.‘,‘s With the advent of laparoscopic procedures, laparoscopic or intracorporeal ultrasound has generated new interest. Laparoscopic ultrasound was originally developed for examining intra-abdominal diseases in the mid-1980s.” More recently, rigid and flexible laparoscopic probes, passing through 10 mm trocars, were developed for delineation of the biliary tract, liver, pancreas, and other abdominal organs.‘“-~” The application of laparoscopic ultrasound is likely to increase with the more frequent use of diagnostic laparoscopic examinations.
TECHNOLOGY The most suitable and most frequently used instruments for OUS are real-time B-mode ultrasound scanners with high-frequency transducers.‘,’ Higher frequencies result in increased resolution, but decreased depth of penetration. Consequently, there needs to he
5.00
15
OPERATIVE
TABLE
ULTRASOUND
IN SURGERY/MACH1
AND
SIGEL
!
I Comparison
of Screening
Methods
Preoperative Ultrasound Sensitivity Specificity Predictability of a positive Predictability of a negative Overall accuracy
in Diagnosing
40.8% 95.8% 87.0% 70.2% 73.4%
test test
Liver
Metastasis
Preoperative Computed Tomography 49.0% 94.4% 85.7% 72.9% 75.9%
from
Colorectal
Carcinoma
Surgical Exploration
Operative Ultrasound
66.0% 89.3% 80.8% 79.2% 79.8%
93.8% 94.4% 92.0% 95.7% 94.2%
P-value <0.0001* <0.05** <0.0001’ <0.0001*
+ Operatwe ultrasound versus each of the other three procedures. ‘* Operative ultrasound versus surgical exploration.
sufficient during OUS examination. With high-frequency high-resolution ultrasound, small lesions including 1 mm biliary stones, 3 to 4 mm tumors, 1 to 2 mm cysts, and 1 to 2 mm vascular defects can be detected. The size of ultrasound probes should he small enough to be manipulated in operative fields, which at times are limited in space. The shape of the probe is an important feature for OUS scanning. There are two fundamental shapes, flat and cylindrical. A flat T- or I-shaped side-viewing prohe with linear-array transducers is appropriate for scanning of relatively large organs such as the liver, pancreas, and kidney. Flat probes are essential for examining the liver under the abdominal wall or the diaphragm. A pencil-like cylindrical front-viewing probe with sector images is suitable for scanning of small organs or structures deep in the operative field, such as the extrahepatic bile duct or Hood vessels. Laparoscopic ultrasound is the latest mode of OUS. It is basically real-time B-mode ultrasound, mostly using lineararray transducers. The transducers are mounted at or near the tip of a long shaft, which is 10 mm in diameter. Currently flexible probes are available in addition to rigid probes. With the laparoscopic ultrasound probe, complete examination of the extrahepatic bile duct is possible during laparoscopic cholecystectomy.‘O’? The intrahepatic bile duct can also he imqed by placing the probe over the liver surface. Laparoscopic ultrasound has recently been introduced for evaluating the liver and pancreas during exploratory laparoscopy, especially in determining the stage and the resectability of malignant turnors.“~” Color Doppler imaging exhibits blood flow by real-time color mapping on conventional B-mode images.‘.‘.“.‘” With current color Doppler scanners, blood flow with a velocity as slow as 4 to 5 mm/set can he displayed in color. The color, either red or blue, corresponds to the direction of flow in relation to the transducer. As the flow increases in velocity, the color becomes brighter or whiter. In our experience, color Doppler has offered additional useful information in addition to anatomical information provided by B-mode imaging during general and vascular surgery.3,‘h Benefits of color Doppler imaging during general surgery include detection and localization of small blood vessels that are difficult to identify by B-mode alone, distinguishing blood vessels from other hyperechoic areas such as ducts and tissue spaces, determining the relation of tumors to vascular structures such as vascular invasion by carcinoma, appraising blood flow to organs after surgical procedures, and improving needle localization for guidance. Color Doppler imaging has also been adapted to laparoscopic ultrasound 16
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probes. During laparoscopic OUS scanning, color Doppler imaging is particularly useful to rapidly distinguish bile ducts from vessels such as the hepatic artery.
SPECIFIC APPLICATIONS Use of OUS during liver, hiliary, pancreatic, endocrine, and vascular surgery varies and each of these specific applications is briefly reviewed. Liver For both primary and metastatic liver tumors, OUS is indicated to determine resectability and to select the type of operation needed. OUS screening is also performed for metastatic tumors, particularly from colorectal carcinoma. When hepatic resection is performed, OUS is used for guidance of tissue dissection.‘m4,‘4m’” OUS provides valuable informr-ltion that is not obtained by preoperative studies and intraoperative exploratory inspection and palpation of the liver. OUS can localize nonpalpable tumors, eg, small hepatocellular carcinoma in cirrhotic liver. Extention of malignant tumors to the intrahepatic portal or hepatic vems and the presence of tumor thromhi or intrahepatic metastases is more accurately delineated. Based on OUS, which can be performed immediately after laparotomy, resectahility can be assessecl, and the most appropriate resectional procedure can he selected. Cysts and abscesses can he Jetected and localized. In our experience, OUS provided useful information during 112 of 126 hepatic operations (88.9%).’ 4 On the basis of OUS findings, decisions for surgical procedures initially proposed on the basis of preoperative studies and surgical exploration were altered in 48 of 126 operations (38.1%). Several other reports demonstrated that surgical management of hepatic tumors had been changed in 30% to 50% of operations by using OUS.‘“,” One recent study by John using laparoscopic exploration of 50 hepatic tumors revealed that laparoscopic ultrasound identified tumors not visible by laparoscopy in 33% and provided staging infor, mation in addition to that derived from laparoscopy alone in 42%.” OUS is more accurate than conventional preoperative imaging methods and surgical inspection and palpation in screening for liver metastasis. In our study of 250 patients with colorectal carcinomas, screening OUS detected otherwise unrecognized liver metastases in 25 patients ( 10.0%).4,‘” These metastases were 4 X 4 mm to 15 X 18 mm in size and were nonpalpable. On the basis of lesions found, OUS was significantly superior to other methods in JULY
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/ OPERATIVE TABLE
IN SURGERY/MACH1
from
Carcinoma
AND
SIGEL
II Operative
Author
ULTRASOUND
(Year)
Ultrasound Number
Machi (1987) Boldrini (1987) Russo (1989) Olsen (1990) Machi (1991) Stadler (1991) Charnley (1991) Stone (1994) * Number ‘* Number
of patients
TABLE
Ill
of paknts
in Diagnosing
(Screening)
Liver
Diagnosis ous*
of Patients 84 86 70 213 189 85 99 56
10 3 5 21 18 12 9 3
of Two
Screening Machi
test test
Followup
6-24 18-54
by other
in Diagnosing
months
92.4% 99.3% 94.8%* 99.0% 98.5%
84.4% 95.5% 71.7%* 97.9% 94.2%
Biliary Tract During hiliary tract operations OUS is indicated to diagnose previously unknown gallbladder calculi, evaluate biliary tumors, localize obscured bile ducts, and screen for bile duct calculi.‘. 4.15.3h OUS can diagnose gallbladder calculi as small as 1 mm and gallbladder polyps 1 to 2 mm in size. During intraoperative examination of gallbladder and bile duct carcinomas, OUS can more precisely assess tumor invasion of the liver parenchyma, involvement of the portal vein and hepatic artery, and metastasis to the lymph nodes and liver. The
3/60
(37) months
20/l 51 (13.2%)
8/47
tests or mefaslasis
Bile Duct
(5.0%)
occured
during
(17.0%)
foilowup
periods
Stones Jakimowicz
Operative Cholangiography
terms of the sensitivity, predictability of a negative test and overall accuracy (Table I). Others have confirmed our findings that routine OUS can detect so-called “occult” metastasis in approximately 5 to 10% of operations as sum‘. in Table II.‘nm3’ mari-ed A unique feature of OUS is its ability to directly guide surgical procedures on the liver. OUS guidance is used either in needle placement or for hepatic tissue dissection.3,4 Needle placement facilitates biopsy, especially of nonpalpable lesions, aspiration of cavitary lesions, injection of agents or contrasts, and catheterization of bile ducts. Local nonresectional treatment of hepatic tumors such as cryosurgery can also be guided hy OUS. Needle guidance can also he performed during laparoscopic ultrasound. OUS guidance has directed anatomic resections of segments and subsegments. New hepatic resectional procedures such as OUS-guided systematic suhsegmentectomy have heen developed.‘5 During 89 hepatic resections, we have used OUS guidance techniques in 67 operations (75.3%).
False-Negative ous** (%)
(median)
(23 months)
ultrasound. was diagnosed
Methods
Colorectal
and Sigel
Operative Ultrasound Sensitivity Specificity Predictability of a positive Predictability of a negative Overall Accuracy
Metastasis by
(11.9%) (3.5%) (7.1%) (9.9%) (9.5%) (14.1%) (9.1%) (5.4%)
who had metastasis which was diagnosed on/y by operatwe in whom operatwe ultrasound was negative, but metastasis
Comparison
only (%)
Operative Ultrasound
Operative Cholangiography
93.7% 98.8% 96.3% 97.9% 97.5%
86.1% 95.6% 86.9% 95.3% 94.4%
extrahepatic bile duct may be ohscured by adhesion from previous surgery, inflammation, or tumors; these distort the anatomy, and increase the chance of bile duct injuries. In such situations, bile ducts can be quickly localized by OUS, especially with color Doppler imaging, which readily distinguishes blood vessels from bile ducts. During 73 operations for benign and malignant Mary diseases, OUS was considered useful in 60 operations (82.2X).‘.’ The major use of OUS has heen for screening of bile duct calculi at the titne of cholecystectomy. Before the era of laparoscopic cholecystectomy, we evaluated the accuracy of OUS by comparing it with operative cholangiography.‘-4,35 OUS was performed during 666 operations, while operative cholangiography was performed during 401 operations. There were 6 operations in pregnant women and 12 operations in patients with contrast allergy, in which cholangiography was avoided. Technically unsuccessful results were encountered in 1.2% for OUS versus 5.5% for operative cholangiography. The two teats were comparable in terms of the sensitivity, specificity, and predictability of a negative test and overall accuracy, whereas OUS was significantly superior in the predictability of a positive test (Table III ). Common hilt duct exploration was performed in 86 operations (12.9%). and the Me duct stones were detected in 77 operations, with a positive hile duct exploration rate of 89.5%. A similar result in the accuracy of OUS compared to cholangiography was reported in Jakimowicz’s study of 491 patients’” (Table III). Our preliminary experience of laparoscoplc ultrasound during 25 laparoscopic cholecystectomies showed that the findings of ultrasound concurred with those of cholangiography.‘@ In
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addition, laparoscopic ultrasound was completed in examining the bile duct in a shorter period of time than operative cholangiography (9.7 2 4.6 minutes versus 17.9 -f 8.9 minutes) (mean -C standard deviation) The feasibility of laparoscopic ultrasound during cholecystectomy has been reported by others.z2
AND
SIGEL
TABLE IV Comparison
of Preoperative Portal Vein
Sensitivity Specificity Predictability of a positive test Predictability of a negative test Overall accuracy
Studies Invasion
and Operative of Pancreatic
Ultrasound Carcinoma
Preoperative Studies
Operative Ultrasound
76.5% 54.5%
94.1% 86.4%
56.5%
84.2%
in Diagnosing
P-value P < 0.05
95.0% 75.0% Pancreas 64.1% 89.7% P < 0.01 OUS is indicated during pancreatic operations for diagnosing or defining Reproduced with permission from reference 6. complications of pancreatitis and evaluating pancreatic carcinoma.‘-4,3’ Pancreatic surgical procedures can also he guided by OUS. Localizing islet cell tumors by OUS will he has been during operations for pancreatic islet cell tumors discussed in the section dealing with endocrine operations. and parathyroid tumors. ‘-‘,“,” Pancreatitis causes multiple complications such as panDespite various imaging modalities currently availahle, creatic duct dilatation, pseudocyst, abscess, and distal bile more than one half of insulinomas and gastrinomas cannot duct stenosis. OUS helps to detect, localize, or exclude he delineated preoperatively. Furthermore, small islet cell these complications during operations, thereby reducing the tumors may not be palpable at operation. On OUS examneed for exploratory dissection. Nonpalpable pancreatic ination, islet cell tumors are almost always hypoechoic comducts and even small cysts are readily localized by OUS. At pared to pancreatic parenchyma. With high-resolution Btimes, previously unknown cysts and abscesses are diagmode ultrasound, tumors as small as 3 to 4 mm can he nosed. Preoperatively or intraoperatively suspected dilated detected. OUS is more effective for finding and localizing ducts or cysts may he excluded by OUS. In 169 operations insulinomas than for gastrinomas because insulinomas are for pancreatitis ( 150 operations for chronic pancreatitis and usually situated within the pancreas. Extrapancreatic gas19 operations for acute pancreatitis), OUS was used and trinomas arc more difficult to localize with OUS. Norton provided useful information in 124 operations ( 73.3%).3,4,‘7 and others reported the detectability of insulinomas by On the basis of OUS findings, the type of procedure ultiOUS to he 83% to loo%.” The detectability of pancreatic mately used was changed from the initially planned progastrinomas by OUS was 95% compared to 58% for extracedure in 25 operations (16.7%) for chronic pancreatitis. pancreatic gastrinomas. In our experience with 8 islet cell The stage and resectability of pancreatic carcinoma can tumors (5 insulinomas and 3 gastrinomas), OUS helped to be determined by OUS early during the course of operation. localize or exclude multiple tumors in 7 operations OUS provides information regarding tumor extension in( 87.5%).L,4 cluding vascular invasion, and lymph node and liver meImaging studies are usually not needed during operations tastasis. The accuracy of OUS in diagnosing portal vein for hyperparathyroidism. The exception to this observation tumor invasion was compared to preoperative studies that is reoperation for parathyroid tumors. Parathyroid adenoincluded computed tomography, percutaneous ultrasound, mas and hyperplasia exhibit hypoechogenicity compared to or angiography in 39 operations.4 The final diagnosis was surrounding tissue on OUS. OUS can be performed before made by surgical exploration, often with histologic confirextensive tissue dissection, and help localize parathyroid mation, that demonstrated portal vein invasion in 22 optumors. In 39 rcoperations for hyperparathyroidism reported erations. For determining portal vein invasion, OUS was by Kern, 33 of 41 tumors (80%) were accurately detected significantly superior to the combination of preoperative and localized by OUS.“’ The sensitivity of OUS was 85%, studies in terms of the specificity and overall accuracy (Tawhich was superior to that of preoperative computed toble IV In a total of 68 operations for pancreatic carcinoma, mography, ultrasound, and Technetium-thallium scan. TuOUS was considered useful in 49 operations (72.1%). Simmors at aberrant locations such as undescended adenomas ilar benefits of OUS were reported in other studies. Lapawere imaged accurately, and all intrathyroidal adenomas roscopic ultrasound has recently been reported for evaluwere detected. In our experience of 18 operations for ating pancreatic carcinoma.” parathyroid tumors, OUS accurately localized tumors in 10 OUS can guide various pancreatic procedures in a manner operations (56%) .‘,’ similar to hepatic procedures. OUS guidance is particularly useful for opening nonpalpable pancreatic ducts or pseuBlood Vessels docysts. ‘.’ These OUS-gu ided procedures are safer and When information of preoperatilre imaging studies is not quicker than blind procedures because it decreases the sufficient, OUS can he used hefore vascular reconstruction chances of complications such as vascular or ductal injuries. to examine native blood vessels if needed. However, the main indicatton of OUS is post-reconstruction evaluation Endocrine of vessel. ’ m4,4CAfter vascular reconstruction but before OUS during endocrine surgery is indicated for diagnosing, wound closure, vascular defects such as intimal flaps, localizing, and excluding endocrine tumors. Although OUS thromhi, and strictures that may cause postoperative comcan be used for thyroid and adrenal tumors, its major use plications may he detected and repaired if clinically signif-
18
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) OPERATIVE TABLE
V Comparison of Two Postreconstruction
Sensitivity Specificity Predictability of a positive Predictability of a negative Overall accuracy Reproduced
with permwon
Methods in Diagnosing of Vascular Defects
test test
from
reference
Operative Ultrasound
Operative Atteriography
93.1% 97.8% 87.1% 98.9% 97.2%
93.1% 94.5% 73.0% 98.9% 94.3%
2.
icant. Experimental and clinical studies have demonstrated that OUS is as accurate as operative arteriography in detecting these defects.lm4 In our studies of 519 vascular operations including 153 carotid endarterectomies, vascular defects were detected by OUS in 155 operations (29.9%).*x3 Of these, defects in 48 operations (9.3%) were judged to be likely to endanger patency of vascular reconstruction, and were repaired. OUS showed accuracy equal to contrast arteriography in the diagnosis of vascular defects (Table V). A similar result was reported by Lane in using OUS for carotid endarterectomy.4@ Furthermore, OUS was quicker, usually requiring less than 5 minutes for examination. Therefore, we consider OUS to be the first-choice test to examine vascular reconstruction sites. Operative color Doppler imaging that provides additional blood flow information may enhance the efficacy of OUS *,’ B 17 using OUS routinely, operative arteriography can be used more selectively when OUS results are not conclusive or when the distal vascular tree needs to be evaluated.
REFERENCES 1. Sigel B. Operative Ultrasonogru~hy. 2nd ed. New York: Raven Press. 1988. 2. Machi J. Operatiwe Ultrasono~uphr-Fundamentals and Clinical Applications. (In Japanese), Tokyo: Life Science, 1987. 3. Machi J, Sigel B. Intraoperative ultrasonography. Radiolo Clin NA. 1992;30:1085-1103. 4. Machi J, Sigel B, Zaren HA, et al. Operative ultrasonography during hepatobiliary and pancreatic surgery. World ./ Surg. 1993; 17:640-646. 5. Schlegel JU, Diggdon I’, Cuellar J. The use of ultrasound for localizing renal calculi. J Ural. 1961;86:367-369. 6. Eiseman 8, Greenlaw RH, Gallagher JQ. Localization of common duct stones by ultrasound. Arch Surg. 1965;91:195-199. 7. Tanaka K, Ito K, Wagai T. The localization of brain tumors by ultrasonic techniques. A clinical review of 111 cases. J Neurosurg. 1965;23:135-147. 8. Cook JH, Lytton B. lntraoperative localization of renal calcuh during nephrolithotomy by ultrasound scanning. J L’rol. 1977;117:543-546. 9. Makuuchi M, Hasagawa H, Yamasaki S. Newly devised intraoperative probe. Image technology and information display. Medical. 1979;11:1167-1168. 10. Lane RJ, Cracker EF. Operative ultrasonic bile duct scanning. Aust NZJ Surg. 1979;49:454-458. 11. Sigel B, Spigos DG, Donahue PE, et al. Intraoperative ultrasonic visualization of biliary calculi. Curr Surg. 1979;36:158-159. 12. Rubin JM, Mirfakhraee M, Duda EE, et al. Intraoperative ultrasound examination of the brain. Radiology. 1980;137:831-832. THE
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13. Shkolnik A, McLane DC. Intraoprrative real-time ultrasonic guidance of ventricular shunt placement in Infant. Radiolog)l. 1981;141:515-517. 14. Sigel B, Draft AR, Nyhus LM. et al. Identification of a paraby operative ultra\onugraphy. Arch Surg. thyroid adenoma 1981;116:?34-235. 15. Lane RJ, Coupland GA. Operative ultrasonic features of insulinomas. Am J Surg. 1982;144:585-587. 16. Sahn DJ, Barratt-Boyes BG, Graham K, et al. Ultrasonic imaging of the coronary arteries in open-chest humans: evaluation of coronary atherosclerotic lesions during cardiac surgery. Circulation. 1982;66:1034-1044. 17. Takamoto, S, Kyo, S, Adachi, H, et al. Intraoperative color flow mapping by real-time two-dimensional Doppler echocardiography for evaluation of valvular and congenital heart disease and vascular disease. J Thorac Curdiovasc Surg. 1985;90:802-812. 18. Machi J, Sigel B, Kurohiji T, et al. Operative color Doppler imaging for general surgery. J L~ltn~sound Med. 1993;12:455-461. 19. Ohta Y, Fujlwara K, Sato Y, et al. New ultrasound laparoscope for diagnosis of intraahdominal dise,\ses. Gnstromtest En&c. 1983;29:289-294. 20. Machi J, Sigel B, Zaren HA, et al. Technique of ultrasound examination during laparoscopic cholecystectomy. Surg Endosc. 1993;7:544-549. 21. Muruglah M, Paterson-Brown S, WI&or JA, et al. Early experlence of laparoscopic ultrasonography m the management of pancreatic carcinoma. Surg Endosc. 1991;7:177-181. 22. Stiegmann G’v’, McIntyre RC, Pearlm,m NW. Laparoscopic intracorporeal ultrasound. An alternative to cholangiography? Surg E&XC. 1994;8:167-172. 23. John TG, Greig JD, Croshie JL, et nl. Superior staging of liver tumors with laparoscopy and laparoscopic ultrasound. Ann Surg. 1994;220:711-719. 24. Castaing D, Emond J, Kunstlinyer F, Bismuth H. Utility of operative ultrasound in the surgical management of liver tumors. Ann Surg. 1986;204:600-605. 25. Makuuchi M, Hasegawa H, Yamasaki S, et al. The use of operative ultrasound as an aid to liver resection in patients with hepatocellular carcinoma. World J Surg. 1987;11:615-621. 26. Ritkin MD, Rosato FE, Branch HM, et al. lntraoperative ultrasound of the liver. An important adjunctive tool for decision makmg in the operatmg room. Ann StLrg. 1987;205:466-472. 27. Parker GA, Lawrence W, Jr Ho&y JS, et al. Intraoperative ultrasound of the liver affects operative drcismn tnaking. Ann Surg. 1989;209:569-577. 28. Machi J, Isomoto H, Kurohiji T, er al. Accuracy of intraoperative ultrasonography in diagnosing liver metastasis from colorectal cancer: evaluation with postoperative follow-up results. World J Surg. 1991;15:551-557. 29. Boldrini G, Gaetdno AM, Giovannmi I, et al. The systematic use of operative ultrasound for detection of hver metastases during colorectal surgery. World] Surg. 1987;11:622-627. 30. Russo A, Sparacino G, Plaja S. et al. Role of intraoperative ultrasound in the screening of liver metastases from colorectal carcinoma: initial experiences. J Surg On&. 1989;42:249-255. 3 1. Olsen AK. Inrraoperative uItrasonography and the detection of liver metastases in patients with colorectal cancer. Br J Surg. 1990;77:998-999. 32. Stadler J, Holscher AH, Adolf J. Intraoperative ultrasonographic detectlon of occult liver metastases in colorectal cancer. Surg Endosc. 1991;5:36-40. 33. Charnley RM, Morris DL, Dennison AR, et al. Detection of colorectal liver metastases using intraoperative ultrasonography. Br J Surg. 1991;78:45-48. 34. Stone MD. Kane R, Jr Bathe A, et al. Intraoperative ultrasound imaging of the liver at the time of colorectal cancer resection. Arch Surg. 1994;129:43 l-436.
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35. Sigel B, Machi J, Beitler JC, et al. Comparative accuracy of operative ultrasonography ,rnd cholanpiography in detecting common duct calculi. Sur‘Tuy. 1983;94:71 i-720. 16. Jakimowicz JJ, Rutten H, Jurgens PJ, Carol EJ. Comparison of operattve ultrasonography and radiography in screening of the cornmon hde duct for calculi. World ] Surg. 1987; 11:628-634. 37. Sqyl B, Machi J, Ramos JR, et al. The role of imaging ultrasound during pancreatic surgery. Ann Surg. 1984;2@0:486-493. 38. Zeiger MA, Shawker TH, Norton JA. Use of intraoperative
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--F World J surg. ultrasono~raphy to locahze ihlet cell tumors. 1993;17:448-454. 39. Kern KA, Shawker TH, D ~~ppman JL, et nl. The use of highresolution ultrasound to locate parathyroid tumor:, during reoperatians for primary hypcrp”‘“thyr~)i~lihlrl. World J Surg. 1987;l 1:579585. 40. Lane RJ. Ackroyd N, Applehq M, ( ;r,lham J. The application of operative ultrasound immediately f;&wm~ cxotid endarterectomy. World 1 Surg. 1987;11:593-597.
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