Surg Clin N Am 84 (2004) 10851111

Intraoperative ultrasound
Junji Machi, MD, PhD*, Andrew J. Oishi, MD, Nancy L. Furumoto, MD, Robert H. Oishi, MD
Department of Surgery, University of Hawaii, John A. Burns School of Medicine and Kuakini Medical Center, 405 N. Kuakini St., Suite 601, Honolulu, HI 96817, USA

Although surgeons are currently using ultrasound in a variety of surgical settings such as the oce, the bedside, the emergency room, and the intensive care unit, one of the earliest surgeon-performed ultrasound examinations in the United States was in the operating room. Dr. Bernard Sigel, a general surgeon and a pioneer of intraoperative ultrasound (IOUS), introduced this modality during surgery in 1979 for intraoperative diagnosis of biliary calculi [1]. In the early 1980s, IOUS was employed during neurosurgery, endocrine surgery, and cardiovascular surgery [27]. Since 1980, the Sigel group has expanded the application of IOUS to various elds including hepatobiliary, pancreatic, and other abdominal surgery [813]. Although the benets of IOUS were clearly reported, gaining acceptance of IOUS among surgeons was slow in the 1980s. However, by the mid-1990s, many surgeons recognized the value of IOUS during surgical procedures, and with the availability of various types of IOUS and laparoscopic ultrasound probes, the use of ultrasound has become more widespread during a variety of operations. In certain operations such as hepatectomy, IOUS is presently considered as an essential modality. In this article, we present an overview of IOUS by reviewing our experience [819] and the literature. Instrumentation, techniques, indications, clinical applications, advantages, and disadvantages are described. The application of IOUS in open abdominal surgery is emphasized, although applications in other surgical elds are briey summarized. The future perspective of IOUS is also discussed. Although laparoscopic ultrasound during laparoscopic procedures is one form of IOUS, we discuss the use of IOUS during open procedures in this article.

Supported by Surgical Education, Inc. * Corresponding author. E-mail address: j.machi@surgedinc.org (J. Machi). 0039-6109/04/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.suc.2004.04.001

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Instrumentation B-mode ultrasound with high-frequency transducers, the so-called small parts scanner, is used for IOUS [14,2025]. Color or power Doppler imaging is sometimes valuable to distinguish blood vessels from other structures or to identify small vessels; however, the majority of IOUS examinations can be performed with B-mode ultrasound. Although ultrasound at higher frequencies penetrates less deeply, it provides images of greater resolution; this is a favorable trade-off for IOUS, which usually requires sound penetration of less than 10 cm without the need for penetrating the abdominal wall. Transducer frequencies range from 5 to 10 MHz, with 7 to 8 MHz most frequently used for IOUS. With such high frequencies, even small lesions, such as 1-mm calculi, 2-mm cysts, 1- to 2-mm vascular defects, and 3- to 5-mm tumors, can be detected. Transducer types for IOUS include linear array, curvilinear array (convex), and phased array (sector). The size and shape of the ultrasound probe are important features for IOUS scanning. The probe should be small enough to be manipulated in a small or narrow operative eld. There are two principal shapes of probes: a at T- or I-shaped probe (mostly side viewing) and a cylindrical pencil-like probe (mostly end viewing). The at probe usually has a wider footprint (3 to 6 cm) and provides a wide neareld image. This probe is suitable for scanning relatively large, at organs, such as the liver, pancreas, and gastrointestinal tract. The cylindrical probe is useful for scanning small target organs or structures, such as the extrahepatic bile duct that are located deep in the operative eld. IOUS probes can be cold-gas sterilized or used with a sterile cover. Gas sterilization requires aeration, and thus the probe can be used only once a day. Although the use of a cover is cumbersome, one probe can be repeatedly used. Recently, a low-temperature chemical sterilization (eg, Steris, Sterrad), which is completed in 60 minutes, has become available, and some IOUS probes are amenable to this method.

Techniques IOUS can be performed at any time during the operation and, if necessary, can be repeated as often as necessary [1425]. Most commonly, IOUS is performed early in the course of operation to acquire new intraoperative information. IOUS is also frequently used during operative procedures for guidance or assistance. After a procedure is nished but before closure, IOUS can be repeated as a completion examination. The two basic scanning techniques for IOUS are contact scanning and probe-stando scanning. In contact scanning, the probe is placed directly on the tissue or organ surface in a manner similar to transcutaneous ultrasound. In probe-stando scanning, the probe is positioned 1 to 2 cm away from the surface of the structure. The probe-stando technique uses saline immersion

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of the probe, which is unique to IOUS. Because ultrasound resolution nearest to the probe is poor, the distance from the probe to the area of interest determines the choice of scanning technique. For example, contact scanning is chosen for the examination of the interior of organs such as the liver and the pancreas, or for examination of target lesions located deep in the tissue (away from the probe). Probe-stando scanning is essential for examination of the surface area of organs or for examination of supercial structures, such as the supercially located bile duct. Another useful IOUS scanning technique is compression scanning, in which the tissue is intentionally compressed by the probe. This method helps to displace air in tissue spaces and air in the gastrointestinal tract lumen. Compression can be also used to distinguish arteries from veins. For complete evaluation, the organ should be systematically and thoroughly scannednot only the area of interest, but the entire organ. Although the scanning method varies in dierent organs, it is generally important to obtain longitudinal and transverse views and, at times, oblique views of the target organ. In addition, IOUS scanning should be performed from various positions and directions using various probe manipulation techniques, including sliding, rotating, and angulating (tilting, rocking) of the probe. By imaging the organ or the lesion with multiple views in twodimensional real time, three-dimensional information can be obtained. During examination of malignant tumors, close attention should be paid to surrounding structures as well. In particular, the major blood vessels should be followed and their relationship to the tumor evaluated. IOUS can be completed within a relatively short period. For example, screening of liver metastasis during laparotomy can be performed in 5 minutes. Precise IOUS evaluation of the extent of a malignant tumor may require 10 to 15 minutes. Indications There are four main general indications for IOUS: (1) acquisition of new information not otherwise available, (2) as a complement to or replacement for intraoperative radiography, (3) conrmation of completion of operation, and (4) guidance of surgical procedures [821]. IOUS is indicated to acquire new information that is not available during preoperative studies or standard intraoperative exploration. This includes new diagnosis of diseases, localization or exclusion of previously suspected lesions, and identication of pertinent anatomic information. IOUS is used for assessment of the extent of malignant tumors or cancer staging. For example, liver metastasis, lymph node involvement, and vascular invasion of cancers can be generally diagnosed more accurately than by routine preoperative studies. The liver can be screened for occult metastasis. Precise localization of lesions such as intrahepatic lesions, pancreatic tumors, or other nonpalpable intraabdominal disease is possible with IOUS. Preoperatively

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or intraoperatively suspected lesions may be quickly excluded by IOUS. Anatomic structures including blood vessels can be delineated before surgical tissue dissection. By providing various new information, IOUS helps to select the best approach to lesions or the most appropriate operation. As a complement to or replacement for conventional intraoperative radiography, IOUS is indicated during hepatobiliary, pancreatic, or vascular surgery. During open cholecystectomy, IOUS has demonstrated equal or superior accuracy in the screening of the bile duct for calculi compared with intraoperative cholangiography. Because contrast injection is not needed, IOUS is much simpler, quicker, and safer than intraoperative contrast radiography such as cholangiography or pancreatography. Thus, IOUS can be a rst-choice imaging method during biliary surgery. Likewise, during vascular surgery, IOUS has exhibited equal or superior accuracy in detecting vascular defects such as intimal aps or thrombi compared with intraoperative arteriography. IOUS is employed to conrm the completion of certain operations, mainly to assess excision of lesions or to discover surgical technical problems. Conrmation of complete resection of tumors in organs such as the liver, pancreas, brain, or breast can be done with IOUS. In certain instances, scanning of an excised tissue specimen in a water bath in the operating room is also a useful test to ensure the lesion as being completely excised. IOUS can be used to conrm complete removal of biliary or pancreatic calculi and extraction of foreign bodies. Technical errors after cardiac surgery or vascular reconstructive surgery can be detected by IOUS and thereby corrected immediately. After organ transplantation, IOUS may be used to examine vascular anastomotic sites and to evaluate adequate blood ow to the organ. In addition to providing diagnostic information, IOUS is indicated to help guide therapeutic procedures. Two types of intraoperative procedures are guided by IOUS: (1) intraoperative needle, cannula, or probe placement; and (2) surgical tissue dissection. IOUS-guided needle placement is similar to interventional radiology performed percutaneously, and aids intraoperative biopsy of tissues, aspiration of uids, injection of agents, or introduction of catheters. Cannula or probe placement for thermal ablation or cryoablation of tumors can be appropriately guided by IOUS. Tissue dissection is guided by IOUS for incision or resection of organs, especially solid organs such as the liver, pancreas, brain, or breast. For example, anatomic resection of the liver is precisely guided by IOUS. Various surgical procedures guided by IOUS are safer, quicker, and more accurate than those performed under inspection and palpation alone. The capability to guide procedures is a unique feature of IOUS for which intraoperative radiology cannot be substituted. Multiple indications for IOUS may be present during a single operation. For example, during hepatic surgery, IOUS is initially indicated to obtain new information, such as a nal cancer staging, then to guide biopsy and hepatectomy, and nally to conrm complete resection of lesions and to exclude intraoperative complications.

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Clinical applications Liver IOUS is indispensable during hepatic surgery for detection and localization of various hepatic lesions and for guidance of surgical procedures [15 19,2645]. During laparotomy for other intraabdominal malignancy, IOUS is also performed for screening for liver metastasis [4656]. Hepatocellular carcinoma, especially when associated with cirrhosis, is often not visible or palpable during laparotomy, even when the tumor is discovered by preoperative imaging methods. Hepatocellular carcinoma smaller than 5 cm in cirrhotic liver cannot be detected by inspection and palpation in approximately 50% of patients. IOUS can readily localize such a tumor. Precise tumor localization is crucial to select the type of hepatectomy. IOUS demonstrates the relation of the tumor to the portal vein and hepatic vein branches, and thereby accurately determines the segment/subsegment containing the tumor. In addition to the main hepatocellular carcinoma, its spread, including intrahepatic metastases (daughter nodules), and tumor thrombi in the portal and hepatic veins and in the bile duct can be more accurately diagnosed by IOUS than by preoperative studies (Fig. 1). Provision of anatomic and diagnostic information has made IOUS a standard tool during operation for hepatocellular carcinoma to determine resectability and to select the most appropriate operation (Fig. 2). IOUS information is an essential component (along with the patients liver function) in the nal decision on the possibility for and the extent of hepatectomy, that is, limited or wedge resection, subsegmentectomy, segmentectomy, or lobectomy. Other malignant tumors such as cholangiocarcinomas and metastatic liver tumors are similarly evaluated by IOUS. Furthermore,

Fig. 1. Tumor thrombus detected by intraoperative ultrasound (IOUS). A 6-cm hepatocellular carcinoma was in segment 8 (anteriorsuperior segment). During laparotomy, IOUS detected a tumor thrombus (TT) of the tumor (T), extending (arrow) from the segment 8 portal vein branch (PV8) into the anterior branch of the right portal vein (ARPV).

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Fig. 2. Hepatocellular carcinoma with its relation to intrahepatic blood vessels. A tumor (T) was located at the bifurcation of the anterior right portal vein (ARPV), invading the segment 8 branch (arrows). Based on the intraoperative ultrasound (IOUS) ndings, the anterior right portal vein was ligated and anterior segmentectomy was performed. RHV, right hepatic vein branches.

benign lesions such as liver cysts, abscesses, hemangiomas, and intrahepatic calculi, which may not be identiable by inspection and palpation, are precisely localized or detected by IOUS. On the basis of IOUS ndings, decisions for surgical procedures initially planned based on preoperative studies and standard surgical exploration have been frequently altered. Several reports have shown that surgical management of hepatic tumors has been changed by the use of IOUS in 30% to 50% of operations [19,2729,3133]. Because of the high incidence of liver metastases, screening of the liver is important for many malignant abdominal tumors, particularly for colorectal cancer. Liver metastases less than 1 cm are often not recognized by preoperative imaging methods. Deep-seated liver tumors cannot be palpated by a surgeon. IOUS has been shown to be more accurate in diagnosing liver metastases than traditional screening methods including percutaneous ultrasound, conventional computed tomography, and surgical exploration [4656]. Tumors as small as 3 to 5 mm can be detected by IOUS (Fig. 3). Both sensitivity and specicity of IOUS in detecting liver metastases from colorectal cancers are higher than 90%, and thus IOUS is an effective screening test. The routine use of IOUS during colorectal cancer surgery has diagnosed preoperatively unknown, nonpalpable, occult liver metastases in 5% to 10% of operations [4652]. Although IOUS is more accurate than traditional screening methods, the routine use of IOUS in all patients with colorectal cancer may not be costeective. In this era of cost containment, IOUS screening of the liver is recommended for locally advanced cancers (eg, T3 or T4 tumors and clinically positive lymph node metastases), for questionable or suspected liver tumors by preoperative studies, or for recurrent colorectal cancers (Fig. 4). During laparotomy for malignancy other than colorectal cancer,

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Fig. 3. Multiple liver metastases from a colon cancer. A 3-cm tumor (T) was known preoperatively. Intraoperative ultrasound (IOUS) detected several occult tumors: a 5-mm tumor (long arrow) and a 2-mm tumor (short arrow) are demonstrated.

IOUS can be also performed for screening for liver metastasis. Such malignant tumors include other gastrointestinal cancers, hepatobiliary and pancreatic cancers, retroperitoneal tumors, and gynecologic cancers. Especially when the presence of liver metastasis may alter the surgical procedures (eg, biliary or pancreatic cancers), IOUS screening is strongly recommended. Various surgical procedures of the liver can be guided by IOUS. Nonpalpable lesions located deep in the liver parenchyma can be biopsied or aspirated under IOUS imaging (Fig. 5). A needle can be inserted into intrahepatic bile ducts under IOUS guidance for aspiration or for

Fig. 4. Exclusion of liver metastasis. Preoperative computed tomography showed a possible metastatic liver tumor in a patient with rectal cancer. During laparotomy, a lesion was palpated under the surface of the liver, but whether it was solid or cystic could not be determined by palpation alone. Intraoperative ultrasound (IOUS) promptly demonstrated the lesion to be a cyst (C), avoiding a biopsy or resection. An arrow indicates the surgeons nger.

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Fig. 5. Intraoperative ultrasound (IOUS)-guided open liver biopsy. A tumor (T) was located deep in segment 7 (posteriorsuperior segment). IOUS precisely guided a biopsy needle into the tumor (arrows).

catheterization. Nonresectional local treatment of liver tumors has been recently introduced with the aid of open IOUS as well as transabdominal or laparoscopic ultrasound. IOUS precisely guides a cannula or probe into the tumor and monitors the process during thermal ablation or cryoablation. Particularly, the use of ultrasound-guided radiofrequency thermal ablation is becoming increasingly popular as its safety and local control efcacy have been demonstrated for both primary and metastatic liver tumors (Fig. 6) [57,58]. IOUS-guided techniques greatly facilitate the performance of hepatic resection, in particular, anatomic hepatectomy. Because interior anatomy of the liver, including intrahepatic vessels, is clearly delineated, hepatic resection can be performed more safely and in a more anatomically oriented fashion. In addition to the initial planning, the resectional process can be monitored by the repeated use of IOUS because the resection line is displayed in relation to the lesion and blood vessels. With the introduction of IOUS guidance techniques, unique hepatic resections such as IOUSguided systematic subsegmentectomy for hepatocellular carcinoma have been developed [26,30,35,42]. Given the overwhelming advantages, IOUS is considered as an essential adjunct, and hepatic surgery should not be conducted without IOUS. Biliary system The majority of simple cholecystectomies for calculous cholecystitis are currently performed laparoscopically. On the other hand, open biliary surgery is needed in more dicult situations or for more complex diseases. IOUS of the biliary tract is performed during laparotomy for diagnosis of gallbladder calculi, screening for bile duct calculi, localization of obscured or anomalous bile ducts, evaluation of biliary tumors, and guidance of biliary procedures [10,11,1618,5964].

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Fig. 6. Open intraoperative ultrasound (IOUS)-guided radiofrequency thermal ablation. (A) A metastatic tumor (T) was localized by IOUS in segment 6 (posteriorinferior segment). (B) A cannula was inserted into the tumor under the guidance of IOUS. (C) During radiofrequency ablation, the ablated lesion (A) became hyperechoic.

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IOUS is highly accurate in diagnosing biliary calculi, and calculi as small as 1 mm can be detected. Because diagnosis of gallbladder calculi is usually made preoperatively, it is not frequently needed during laparotomy. However, when preoperative studies are not performed or are not conclusive, IOUS can be used to quickly diagnose or exclude gallbladder calculi. The primary use of IOUS during cholecystectomy for calculous disease is for screening of the bile duct for calculi. Although intraoperative cholangiography has been the gold standard examination for this purpose, two large clinical studies performed during open cholecystectomies in 1980s demonstrated excellent accuracy of IOUS, comparable or even superior to intraoperative cholangiography, for diagnosing bile duct calculi [10,61]. The sensitivity of IOUS is more than 90% to 95% and the specicity is 98% to 99%. Therefore, IOUS is a suitable screening method for bile duct calculi. The accuracy of open IOUS in screening bile duct calculi is applicable to that of laparoscopic ultrasound, which can be used during current laparoscopic cholecystectomy. IOUS is also accurate to evaluate intrahepatic bile duct calculi, particularly their extent in the biliary tree, intraoperatively (Fig. 7). Adhesions due to previous operations, dense inammation due to acute cholecystitis or pancreatitis, or advanced tumors can distort the anatomy and obscure the extrahepatic bile ducts and surrounding structures. Surgical tissue dissection in such instances is often time consuming and risky. IOUS can quickly and precisely localize the ducts before tissue dissection. The size of the ducts can be accurately measured. Intraoperative color Doppler imaging is useful to readily distinguish vascular structures from the ducts, particularly when the anatomy is unclear. Needle placement into the bile duct can be guided by IOUS if intraoperative cholangiography is needed. Anomalies or variations of bile ducts or associated vascular structures can be also identied during laparotomy by IOUS (Fig. 8).

Fig. 7. Multiple intrahepatic bile duct calculi. A patient had recurrent episodes of cholangitis associated with bile duct calculi. Intraoperative ultrasound (IOUS) was performed to determine the extent of intrahepatic bile duct involvement; this shows multiple calculi (arrows) with shadowing (s) in bile ducts of segment 3 (left lateralinferior segment).

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Fig. 8. Replaced right hepatic artery identied by intraoperative ultrasound (IOUS). The replaced right hepatic artery (RRHA) originated from the superior mesenteric artery (SMA). Arrows indicate the course of this artery behind the portal vein (PV) and the pancreas (P). D, duodenum.

For evaluation of malignant biliary tumors, including gallbladder cancer and bile duct cancer, IOUS provides accurate assessment of direct invasion of tumor into the liver parenchyma or to blood vessels such as the portal vein and hepatic artery (Fig. 9). Metastasis to the liver and lymph nodes can be examined. These IOUS ndings help to determine the extent and the resectability of these biliary cancers. IOUS provides useful guidance for biopsy of biliary tumors, aspiration or catheterization of intrahepatic bile ducts, and assistance in obtaining free margin when tumor resection is performed, especially in combination with hepatic resection. IOUS can sometimes identify gallbladder polyps as small as 1 to 2 mm that are unknown preoperatively.

Fig. 9. Portal vein tumor thrombus caused by gallbladder cancer. A gallbladder cancer metastasized to hilar and hepatoduodenal lymph nodes (LN) and caused tumor thrombus (Th) in the portal vein (PV). These intraoperative ultrasound (IOUS) ndings suggested unresectable features of this cancer. VC , vena cava.

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Although intraoperative cholangiography has been the most widely used imaging modality during biliary surgery, it has certain disadvantages, such as complications associated with bile duct cannulation or adverse eects from contrast material and irradiation. It often takes 10 to15 minutes from duct cannulation to radiograph reading, and sometimes a second or third cholangiography is required to obtain optimal images. On the other hand, IOUS is inherently safer, requiring no contrast injection. IOUS is quicker, and screening for bile duct calculi is usually completed within 5 minutes during open cholecystectomy. IOUS does have limitations compared with intraoperative cholangiography, however, including inability to display the entire biliary ductal system simultaneously, diculty in assessing biliary stula, biliary stricture and bile duct injury, and inability to evaluate duct duodenal patency. Because both intraoperative imaging methods possess advantages and disadvantages, the two methods should be used in a complementary fashion. For screening of the bile duct for calculi during cholecystectomy for gallstones, IOUS can be employed as a rst-choice screening method because of its advantages. If IOUS is denitely negative or positive for bile duct calculi, intraoperative cholangiography is not required. When IOUS ndings are equivocal or inconclusive, cholangiography should be performed. During laparotomy for more dicult and complex conditions such as inammatory or neoplastic biliary diseases, the appropriate use of both methods is important. In the majority of complicated biliary operations, cholangiographic information is available preoperatively; in such instances, only IOUS may be needed intraoperatively. Pancreas Accurate diagnosis or localization of pancreatic diseases is not always possible until the time of operation despite use of various preoperative imaging studies. During operations, radiography (ie, pancreatography) has a limited value, and its utility is uncommon. On the other hand, IOUS can provide useful information during various pancreatic operations. IOUS is performed for evaluation of the complications of pancreatitis, evaluation of pancreatic cancer and other pancreatic lesions, localization of islet cell tumors, and guidance of pancreatic procedures [12,1519,63,6579]. Pseudocyst, pancreatic duct dilation, abscess, bile duct stenosis, and portal or splenic vein thrombosis are complications of pancreatitis. IOUS frequently oers imaging information for diagnosing, localizing, or excluding these complications, especially during surgery for chronic pancreatitis, thereby decreasing the need for exploratory tissue dissection and the operating time. Preoperatively unrecognized small pseudocysts or abscesses may be diagnosed; IOUS often detects more cysts in addition to previously diagnosed ones. The presence or absence of pancreatic duct dilation is readily diagnosed by IOUS. Precise localization of pseudocysts or dilated ducts by IOUS is helpful because they can be dicult to visualize or palpate

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due to dense inammation. Our study has shown that, based on the IOUS ndings, surgical procedures for chronic pancreatitis (drainage versus resection) or drainage sites have been altered in 15% to 20% of operations [18,63]. During operations for pancreatic cancer, IOUS helps to determine the stage and resectability before tissue dissection, usually immediately after laparotomy. Tumor invasion, particularly in the portal venous system, and metastasis to the liver and lymph nodes can be assessed (Fig. 10). IOUS is generally more accurate in diagnosing portal vein invasion of pancreatic cancer than preoperative imaging studies including computed tomography and arteriography [12,18,63,65,69,71]. Nonpalpable liver metastases may be detected by IOUS, thus changing the surgical procedure to be performed. Currently, prelaparotomy laparoscopy with laparoscopic ultrasound has been gaining popularity; in such a circumstance, laparoscopic ultrasound

Fig. 10. Vascular invasion of pancreatic head cancer. (A) A large pancreatic tumor (T) was displacing and invading the portal vein (PV) and the superior mesenteric vein (SMV). VC, vena cava. (B) The same tumor (T) was surrounding and involving the superior mesenteric artery (arrow). These intraoperative ultrasound (IOUS) ndings suggested unresectability of the tumor. SMV, superior mesenteric vein; VC, vena cava; Ao, aorta.

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can provide information similar to open IOUS to determine the resectability of pancreatic cancer. At times, a small cancer causing obstructive jaundice that is not visualized preoperatively can be delineated by IOUS in the pancreatic head or periampullary region. Other pancreatic tumors or lesions, such as cystic neoplasms of the pancreas, are also evaluated by IOUS during operation (Fig. 11). IOUS has been proven to be one of the most accurate modalities in diagnosing, excluding, and localizing islet cell tumors such as insulinoma and gastrinoma [12,7379]. A characteristic hypoechoic feature of islet cell tumors makes IOUS possible to delineate tumors as small as 3 mm to 4 mm in size. When a nodule is palpated during operation, IOUS can conrm or exclude it as an islet cell tumor. When a tumor is not palpated, IOUS is especially useful for localization. IOUS is more effective for insulinoma than for gastrinoma because insulinoma is usually located within the pancreatic parenchyma while gastrinoma is often extrapancreatic. The detectability of insulinoma by IOUS has been reported to be 83% to 100% [73,74,77]. The IOUS detectability of intrapancreatic gastrinoma was 95%, whereas that of extrapancreatic gastrinoma was 58%. Various pancreatic procedures can be guided by IOUS in a manner similar to hepatic procedures. Needle placement is guided by IOUS for biopsy of tumors or aspiration of cystic lesions. During internal drainage of dilated pancreatic ducts by pancreaticojejunostomy for chronic pancreatitis, the ducts are opened quickly and safely under IOUS guidance [67]. Opening of small pseudocysts can also be assisted. For small nonpalpable islet cell tumors or other benign lesions, enucleation after localization is facilitated by IOUS guidance.

Fig. 11. Mucinous cystadenoma of the pancreas. Intraoperative ultrasound (IOUS) demonstrated a complex multicystic lesion (C) in the body of the pancreas with its relation to the splenic artery (SA) and splenic vein (SV). IOUS also showed its relation to the main pancreatic duct, facilitating enucleation of this lesion (cystadenoma).

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Other abdomen and retroperitoneum Other diseases for which IOUS is used during laparotomy include, but are not limited to, gastrointestinal tumors, other abdominal or retroperitoneal tumors, abdominal abscesses, and splenic diseases. The stage of gastrointestinal malignancy can be evaluated by IOUS [80 82]. On high-frequency IOUS, the gastrointestinal wall shows a layered appearance (usually ve layers), which corresponds well with the histologic structure. The depth and the lateral extent of tumor invasion of malignancy such as gastric cancer are determined by IOUS. Tumor invasion to adjacent structures, including vascular invasion, can be assessed. The liver and regional lymph nodes are examined for metastasis. In the same manner, other malignancy such as retroperitoneal tumors, abdominal lymphoma, and gynecologic tumors such as ovarian cancer are staged by IOUS (Fig. 12). IOUS information helps to determine the curability and resectability of these tumors. Particularly, for recurrent abdominal or retroperitoneal cancers in which tissue dissection is difcult due to adhesions, IOUS is frequently helpful for biopsy or resection (Fig. 13). Although most abdominal abscesses are treated by percutaneous drainage, open surgical drainage is needed when percutaneous methods are unsuccessful or impractical. During laparotomy, surgical exploration and dissection is often dicult due to inammation. IOUS can help in quickly localizing abscesses, guiding a needle for aspiration, and facilitating adequate drainage [13]. IOUS can be used to evaluate splenic lesions, although not so frequently. The main indications for IOUS are: (1) to evaluate splenic lesions (eg, cystic versus solid), which are suspected by preoperative imaging methods; (2) to guide aspiration or biopsy; and (3) to stage tumors when splenectomy is

Fig. 12. Abdominal carcinoid tumor. A patient with ileal carcinoid tumor had metastatic disease. During laparotomy for palliation, intraoperative ultrasound (IOUS) localized and detected multiple retroperitoneal and intraperitoneal metastatic lymph nodes (N). PV, portal vein; SMA, superior mesenteric artery; VC, vena cava.

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Fig. 13. Recurrent pelvic lymphoma. A patient with a history of abdominal lymphoma had a recurrent pelvic tumor. Intraoperative ultrasound (IOUS) with color Doppler imaging demonstrated the relation of the tumor (T) to the iliac artery (A) and vein (V) branches and to the ureter with a stent (arrow). This nding helped intraoperative biopsy, avoiding injuries to these structures.

performed for malignant diseases. IOUS is also valuable for quick localization of accessory spleens when accessory splenectomy is planned, particularly for small nonpalpable spleens. Endocrine system IOUS of the endocrine system is performed for localization and assistance of resection of endocrine tumors, particularly pancreatic islet cell tumors, parathyroid tumors, and adrenal tumors [7379,83,84]. For malignant endocrine tumors, IOUS is also used to help in tumor staging. IOUS can be useful to identify parathyroid adenomas or hyperplasia during operation for hyperparathyroidism. In particular, IOUS is valuable to detect parathyroid glands in abnormal locations such as intrathyroidal tumor or to localize them during reoperation for recurrent hyperparathyroidism in which tissue dissection is often dicult. It was reported that IOUS accurately detected 33 of 41 tumors (80%) during 39 reoperations for hyperparathyroidism [84]. Although not frequently indicated, IOUS can be performed during initial operations or reoperations for thyroid cancer, mainly for evaluation of local extension and lymph nodes, for examination of the contralateral lobe, and for localization of recurrent thyroid cancer [85,86]. Adrenal operations are mostly performed laparoscopically at present, in which laparoscopic ultrasound can be used. When open surgery is performed, IOUS may be used to evaluate adrenal lesions (eg, cystic versus solid), to quickly localize small adrenal tumors such as functioning adenomas, and to stage and determine resectability in case of malignant adrenal tumors. IOUS-guided ablation of functioning metastatic endocrine tumors such as liver metastases of adrenal tumors or gastrinomas is benecial for the purpose of symptomatic palliation.

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Cardiovascular system IOUS of the cardiovascular system is performed for prereconstruction evaluation of peripheral vascular abnormalities, postreconstruction detection of vascular defects, and assessment of the completion of open-heart operations [7,16,18,8796]. When the results of preoperative vascular studies are not sucient or are inconclusive, IOUS can be used to delineate and evaluate vascular abnormalities before the opening of blood vessels. However, IOUS is used mainly to examine the vascular reconstruction sites as a completion examination. After vascular reconstruction, intraoperative arteriography has been widely employed to detect or exclude vascular defects (or technical errors) such as intimal aps, thrombi, and strictures, which may cause postoperative complications (ie, thrombosis or graft occlusion). Studies have demonstrated that IOUS is equal to or superior to intraoperative arteriography in identifying such defects, with a sensitivity of 93% and a specicity of 98% [7,89]. In addition, IOUS can be used repeatedly during the operation. The size or magnitude of detected vascular defects is more precisely estimated with IOUS. Therefore, IOUS can be a rst-choice screening method to examine vascular reconstruction sites. Particularly during carotid endarterectomy, IOUS is the only safe imaging method because of the risk associated with intraoperative carotid arteriography [87,91,92]. Intraoperative arteriography should be performed selectively, for example, to evaluate critical distal anastomotic sites or to delineate the distal arterial bed. In vascular surgery requiring laparotomy, such as renal and mesenteric bypass operations or porto-systemic shunts, IOUS is particularly useful because intraoperative arteriography is difcult in abdominal vessels. During open-heart operations for valvular or congenital heart diseases, the completion of cardiac procedures can be assessed with IOUS [9396]. Intraoperative transesophageal echography using color Doppler imaging has become a valuable tool during cardiac surgery because of the provision of dynamic blood ow information as well as anatomic abnormalities. This technique has greatly facilitated cardiac surgery by making it possible to assess the postreconstruction effectiveness of repair immediately, and has reduced the occurrence of early postoperative problems requiring second operations. During coronary artery bypass graft operations, IOUS can be used directly (epicardially) in the operative eld, mainly for examination of anastomotic sites after reconstruction. Neurologic system IOUS of the brain and spinal cord was one of the major applications of IOUS that became popular in 1980s [9799]. IOUS is performed mainly for localization and assessment of brain and spinal cord lesions and for guidance of neurosurgic procedures, particularly for needle and catheter placement and for resection of lesions [97101]. Lesions for which IOUS has

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been used during neurosurgery include brain and spinal cord tumors; cystic lesions, such as brain cysts, hematomas, abscesses, and syringomyelias; vascular abnormalities, such as arteriovenous malformations and aneurysms; hydrocephalus, disc hernias, and foreign bodies. In particular, IOUS localization and needle guidance for invisible subcortical lesions is useful, and is simpler and quicker than a stereotactic computed tomography method. Urologic system Although IOUS is not as frequently performed during open urologic procedures, it can be used to assist surgical removal of renal stones when open surgery is needed for nephrolithotomy [102,103]; IOUS helps in localizing intrarenal stones, in guiding stone removal, and in conrming completeness of stone removal. IOUS also can be performed during renal tumor operations for localization of nonpalpable small tumors, for detecting or excluding satellite lesions, or for detecting venous (renal vein and vena cava) tumor thrombi [104]. When partial nephrectomy is indicated to preserve renal function, IOUS evaluation of a renal tumor is of particular value [105]. Lung and mediastinum IOUS may be performed during operations for malignant tumors of the lung and mediastinum, particularly lung cancer, to evaluate cardiovascular invasion and lymph node and liver metastasis [106]. IOUS can be performed immediately after thoracotomy, and provides imaging information that is useful in selecting the type of surgical procedure (eg, lobectomy versus pneumonectomy) and in avoiding unnecessary extensive tissue dissection. Breast As breast surgeons are becoming more familiar, experienced, and facile with the use of ultrasound examinations in the oce, intraoperative use of ultrasound has been increasing during excision of breast tumors [107110]. For nonpalpable breast lesions, IOUS is more convenient and quicker than preoperative needle localization methods. After localization, repeated IOUS can assist resection of breast lesions with adequate margins. After resection, the specimen can be scanned in a water bath as a completion examination to conrm that the lesion has been completely excised (Fig. 14). Transplantation In addition to preoperative and postoperative evaluation of organ transplantation, ultrasound can be used intraoperatively during transplantation of various organs, including liver, kidney, pancreas, and heart transplantation. IOUS is mainly performed for assessment of vascular

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Fig. 14. Intraoperative ultrasound (IOUS)-guided lumpectomy of breast cancer. (A) A nonpalpable breast cancer (T), 6.5 8.1 mm, was localized by IOUS. Using and repeating IOUS as a guide, lumpectomy was performed. (B) The scanning of the resected specimen in a water bath (W) in the operating room showed complete excision of the tumor (T) with adequate margins.

anastomosis, diagnosis of intraoperative complications, and evaluation of adequacy of blood ow in the transplanted organ, especially using intraoperative color Doppler imaging. IOUS can also be used during hepatic resection to obtain liver graft from a living donor [111]. Foreign body Foreign-body extraction is often dicult and time consuming. Metal fragments, glass, wood, bone, and even medical instruments can be situated for the most part in the extremities and body wall but, occasionally, are located in internal organs. Radiologic studies are important as an initial tool in diagnosing foreign bodies. However, during extraction operations, nonpalpable foreign bodies are dicult to localize in the operative eld, even with the use of intraoperative radiography or uoroscopy. IOUS is an optimal method for precise and quick localization of foreign bodies,

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including radiographically nonopaque ones, because the ultrasound probe is placed directly on the tissue surface and real-time monitoring can be performed. An exploratory needle can be introduced toward the foreign body, and thus, extraction is facilitated under IOUS guidance. Advantages and disadvantages Although relatively new compared with intraoperative radiography, IOUS has a number of advantages, including safety, speed, high accuracy, more imaging information, wider applicability, and ability to guide procedures [8 21]. Because of its safety and ease of use, IOUS can be used repeatedly during the course of an operation. The results of IOUS scanning are obtained immediately because of the real-time feature of ultrasound imaging. Once learned, IOUS is completed within a short period of time. Screening of the liver for metastasis or the bile duct for calculi takes less than 5 minutes. Staging of cancer may require 10 to 15 minutes; however, IOUS information will eventually reduce unnecessary tissue dissection and the operating time. IOUS is more accurate in diagnosing certain lesions compared with preoperative imaging studies, intraoperative contrast radiography, and even surgical exploration. IOUS provides multiplanar images from various directions in real time, and thus the size and shape of target lesions are assessed more precisely. Imaging information of structures around target lesions, such as vascular systems, is also obtained. For example, a knowledge of vascular anatomy in reference to lesions obtained by IOUS during laparotomy is of great value for hepatobiliary or pancreatic surgery. IOUS is more widely applicable to various diseases and organs than intraoperative radiography. Procedure-guiding ability of IOUS in the operative eld cannot be achieved by intraoperative radiology. There are many procedures that cannot be performed without IOUS guidance; for example, biopsy of nonpalpable deep-seated lesions or certain anatomic resections of the liver. Color and power Doppler imagings are the latest modality of ultrasound, and exhibit blood ow in color within B-mode images. Blood ow information is obtained in addition to anatomic information. The use of color or power Doppler displays occasionally makes IOUS image interpretation quicker because of easier recognition of vascular structures. Disadvantages of IOUS include limitations in certain imaging or diagnostic abilities, need for specic instruments, and prolonged learning curve. There are limitations in detectability of small lesions and delineation of small ductal structures. Tumors smaller than 3 to 5 mm in size are not detectable even with high-resolution ultrasound. Even certain larger tumors are dicult to detect when they are isoechoic to surrounding tissue. Because of its limitations, IOUS should not be used to entirely replace other intraoperative diagnostic methods; complete surgical exploration by inspection and palpation and appropriate use of intraoperative radiography are always important. Special instruments, in particular small probes with high-frequency

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transducers, are required for IOUS; these IOUS instruments are presently available from several manufacturers. Ultrasound examination is highly operator-dependent, and this is related to the learning curve. The learning curve diers depending on the purpose of IOUS and the target organs or lesions. This learning issue will be solved if the surgeon realizes the value of IOUS and becomes interested enough in performing IOUS by himself or herself. Perspective The future uses of IOUS will be brought about by a combination of surgeons experience with ultrasound and technologic advances. Some predictable issues concerning IOUS include expansion of its applications, improvement in instrumentation, and incorporation of new ultrasound technology. The use of IOUS by surgeons will steadily increase, along with more formal training in ultrasound for surgeons. Having competent surgeons performing IOUS and having IOUS instruments always available in the operating room will permit IOUS to become an everyday tool for acquiring intraoperative information; it will allow surgeons to see in new dimension. Applications of IOUS to new elds will be also widened. This is particularly true in the use of laparoscopic ultrasound because of ongoing broader applications of laparoscopic or minimally invasive operations. Laparoscopic ultrasound is one form of IOUS, and basically it employs the same ultrasound technology. The basic ultrasound physics, images, advantages, and disadvantages of IOUS are applicable to laparoscopic ultrasound, although the method of access diers. Laparoscopic ultrasound is technically more demanding. Therefore, it is recommended for the surgeon who is interested in using laparoscopic ultrasound to learn IOUS during laparotomy. The introduction of new ultrasound technologies will lead to further improvement in resolution and deeper sound penetration of IOUS. New probes and more user-friendly scanners for surgeons are being developed. New ultrasound technologic developments, such as harmonic imaging with contrast agents, will improve the intraoperative use of color or power Doppler imaging. The renement of three-dimensional (3D) images will simplify IOUS for planning and guiding tumor ablation or organ resections, such as hepatectomy. Anatomic and pathologic information provided by 3D IOUS will enable a quicker and more assured IOUS-guided surgical procedures. 3D images may increase the diagnostic condence of the surgeons, which is often an obstacle for the broader applications of IOUS. Advances in various other medical or nonmedical technologies will continuously inuence or alter surgical procedures and imaging methods including IOUS. Less and less invasive surgery with smaller access sites will keep surgeons hands further away from organs, thus requiring more image guidance as seen in minimally invasive and percutaneous image-guided

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procedures. Therefore, there will be a less distinctive border between IOUS and percutaneous interventional ultrasound. Virtual reality technology will continually advance so that more realistic simulation of IOUS examinations, as well as surgical procedures, will be available. Computer-based ultrasound simulators will greatly help future education and training in IOUS. As technology is evolving, new advances in procedures and imaging methods including IOUS must be carefully assessed to dene its emerging role and cost-eectiveness for improving surgical practice of the future. Summary Instrumentation, techniques, indications, clinical applications, advantages, disadvantages, and future perspective of IOUS are described. IOUS is useful not only to acquire new diagnostic information but also to guide or assist therapeutic procedures. IOUS is commonly performed during hepatobiliary, pancreatic, endocrine, cardiovascular, and neurologic surgery; however, its applications are expanding to other surgical elds. Advantages of IOUS, including safety, speed, high accuracy, comprehensive anatomic information, and real-time guidance capability outweigh its disadvantages, such as specic equipment requirement and slow learning curve. The appropriate use of IOUS can have a marked impact on intraoperative management, including improved decision making; reduction in surgical tissue dissection, operating time, and complications; and development of new procedures. The use of IOUS by surgeons is expected to increase along with more formal training and experience in ultrasound for surgeons. With advances in ultrasound equipment and technology, the ability and the type of IOUS will be improving and altering in the future, as seen in current laparoscopic ultrasound, which is one form of IOUS. References
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