Clinical applications of a new through-the-scope ultrasound probe: prospective comparison with an ultrasound endoscope

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Clinical applications of a new through-the-scope ultrasound probe: prospective comparison with an ultrasound endoscope Amitabh Chak, MD Mimi Canto, MD, MHS Peter D. Stevens, MD Charles J. Lightdale, MD Frank Van de Mierop, MD Gregory Cooper, MD Bonnie J. Pollack, MD Michael V. Sivak, Jr., MD

Endoscopic ultrasonography (EUS) is a high-resolution imaging technique with applications that include staging of gastrointestinal malignancies, evaluation of gastrointestinal submucosal tumors, and diagnosis ofpancreaticobiliary diseases. 1EUS is usually performed with dedicated echoendoscopes. The oblique viewing optics combined with the added length and diameter of the transducer limit the endoscopic capabilities of these instruments. The large diameter of the transducer also makes it difficult for these instruments to traverse tight stenoses. Furthermore, dilation of stenotic esophageal tumors followed by EUS may increase the risk of perforation. 2 EUS requires a procedure separate from the initial endoscopy, adding to patient discomfort. Endoluminal ultrasonography can be performed in the gastrointestinal tract 3-9 and the pancreaticobiliary ductal system 1°-13 using high-frequency ultrasound catheters that are capable of being introduced through the accessory channel of standard diagnostic endoscopes (catheter-based endoscopic ultrasonography or C-EUS). Theoretically, C-EUS should be easier to perform than EUS because of the improved view and maneuverability of the endoscope. Catheters can

Received April 15, 1996. For revision August 21, 1996. Accepted October 16, 1996. From the Divisions of Gastroenterology at University Hospitals of Cleveland, Cleveland, Ohio, and Columbia-Presbyterian Medical Center, New York, New York. Presented in part at the annual meeting of the American Society for Gastrointestinal Endoscopy, May 1996, San Francisco, California (Gastrointest Endosc 1996;43:292). Reprint requests: Arnitabh Chak, MD, Gastroenterology, University Hospitals of Cleveland, 11100 Euclid Ave., Cleveland, OH 44106. 0016-5107/97/4503-029155.00 +0 GASTROINTESTINAL ENDOSCOPY Copyright © 1997 by the American Society for GastrointestinalEndoscopy 37/69/78665

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Figure 1. A, Ultrasound catheter with mechanically rotating transducer designed for passage through accessory channel of endoscopes. B, Probe-irrigation plug attached to accessory channel of endoscope showing catheter insertion into the channel. Luer Iock attachment on side can be connected to a water source for simultaneous irrigation. Water infusion can be controlled with stop-cock.

also be directed through tight stenoses and can be passed into the pancreaticobi]iary ductal system. Unfortunately, the clinical applicability of C-EUS has been limited to date because of inadequate imaging depth and poor resolution. The purpose of our study was to define clinical applications and technical limitations of a promising, newly developed highfrequency ultrasound catheter system by prospectively comparing it to EUS. MATERIALS AND METHODS

The Olympus Ultrasonic Probe Set MH-247 (Olympus America Inc., Melville, N.Y.) has been designed for use with the Olympus EU-M3 or EU-M20 ultrasound center. Two high-frequency catheters with mechanically rotating transducers, UM-2R (12 MHz) and UM-3R (20 MHz), have been developed (Fig. lA). These catheters provide a B-mode 360 ° radial image GASTROINTESTINAL ENDOSCOPY 291

Table 1. Cause of lesions imaged with C-EUS and EUS in 43 patients Type No. Mucosal lesions* Esophageal Inflammatory polyp 1 Metaplastic nodule (Barrett's mucosa) 1 Inflammatory nodule (post esophagectomy) 1 Gastric Enlarged folds (gastritis) 2 Nonhealing ulcer 1 Duodenal Ampullary adenoma 2 Submucosal tumors Esophageal Leiomyoma 2 Mediastinal granuloma (histoplasmosis) 1 Achalasia 1 Gastric Leiomyoma 4 Varices 2 Spleen 1 Pancreatic rest 1 Duodenal Gastrinoma 1 Rectal Postpolypectomyscar 1 Esophageal malignancies Adenocarcinoma 8 Squamous cell carcinoma 5 Strictures Esophageal Peptic stricture 2 Biliary Primary sclerosing cholangitis 2 Pancreatic cancer 1 Chronic pancreatitis 1 Adenomatosis 1 Pancreatic Carcinoid 1 *Suspected submucosalinvolvement.

in a plane perpendicular to the direction of insertion. The working length of the catheters is 205 cm and they have an outer diameter of 2.4 mm, allowing easy passage through the accessory channel of standard diagnostic upper endoscopes, colonoscopes, and duodenoscopes. A probe-irrigation plug (Fig. 1B) designed for the system can be connected to the accessory channel of the endoscope allowing for the infusion ofdeaerated water through a side port while the catheter is in the channel. All patients with small mucosal lesions (suspected submucosal pathology), submucosal tumors (defined as intraluminal elevation in the wall of upper gastrointestinal tract covered by apparently normal mucosa), esophageal malignancies, esophageal strictures, and pancreatic or biliary strictures who were undergoing standard EUS were eligible for the study. The study was conducted simultaneously at two university 292 G A S T R O I N T E S T I N A L E N D O S C O P Y

hospitals (University Hospitals of Cleveland and Columbia-Presbyterian Medical Center) and was approved by the Institutional Review Board for H u m a n Investigation at both centers. Premedication with meperidine and midazolam was administered in a standard fashion for endoscopic procedures. C-EUS was performed at the completion of a diagnostic upper endoscopy in patients with mucosal lesions, esophageal cancers, or submucosal tumors. The water immersion method was used for acoustic coupling. To facilitate scanning in the esophagus, a small amount of water was periodically infused through the irrigation plug, and the patient was occasionally placed in a supine or prone position t o submerge the lesion. Patients with stenotic esophageal malignancies did not undergo dilation prior to performance ofEUS. C-EUS was performed with a diagnostic or therapeutic duodenoscope at the time of ERCP in patients with pancreatic or biliary strictures (pancreaticobiliary C-EUS performed at University Hospitals of Cleveland only). All malignant lesions were staged according to C-EUS findings prior to performance of EUS. All patients underwent EUS with the GF-UM20 ultrasound endoscope (Olympus) after C-EUS had been performed (except two patients in whom EUS was not technically feasible). Procedures were performed by five different endoscopists. All endoscopists had at least 2 years of experience in EUS. Parameters assessed after both studies were as follows: depth of penetration with C-EUS, number of sonographic layers seen when examining normal gastrointestinal wall with C-EUS, time taken to complete each procedure, image clarity with C-EUS compared to EUS, TNM staging of malignancy with C-EUS compared to EUS, adequacy of C-EUS imaging, ease of performing C-EUS compared with EUS, and preferred instrument (catheter probe versus echoendoscope) including reason for preference.

RESULTS Forty-three patients (mean age 61 years, 24 men) who met eligibility criteria were entered into the study. No procedure-related complications were noted. Lesions that were imaged are listed in Table 1. Twenty-two patients had lesions in the esophagus (13 malignancies, 4 submucosal tumors, 3 mucosal lesions, 2 benign peptic strictures); 11 patients had gastric lesions (8 submucosal tumors, 3 mucosal lesions); 3 patients had duodenal tumors; 1 patient had a rectal lesion; and 6 patients had pancreaticobiliary strictures (5 biliary and 1 pancreatic). Twenty-three patients were imaged with the 12 MHz probe (UM-2R), 10 patients were imaged with the 20 MHz probe (UM3R), and 10 patients were imaged with both probes. Esophageal malignancies were always staged with the 12 MHz probe except for two cases (one case of VOLUME 45, NO. 3, 1997

Figure 2. C, The hypoechoic middle layer is thought to correspond to the muscularis. Portal vein (PV), hepatic artery (HA), cystic duct and (Cy) can be seen adjacent to the bile duct.

early cancer and one case when the 12 MHz probe was under repair). Technical considerations

Figure 2. Images of normal gastrointestinal wall obtained with ultrasound catheters. A, Esophageal wall imaged as five-layer structure at 12 MHz. B, Gastric wall imaged as five-layer structure at 20 MHz. Common bile duct imaged as a three-layer structure at 12 MHz with catheter positioned in the duct. VOLUME 45, NO. 3, 1997

Mean imaging depth with the 12 MHz probe was 2.9 cm (range, 1.7 to 4.1 cm) and with the 20 MHz probe was 1.8 cm (range, 0.9 to 2.7 cm). The wall of the gastrointestina] tract (see Fig. 2 for representative images) was generally imaged as a five-layer structure with the 12 MHz probe, except in one case where the gastric wall was resolved into seven layers (muscularis propria split into three layers). The wall of the gastrointestinal tract was also imaged as a five-layer structure with the 20 MHz probe, except in three cases where it was resolved into seven layers (muscularis propria split into three layers). The normal bile duct was always resolved into a three-layer structure (Fig. 2C) at both frequencies. Image clarity with the probes was rated better than EUS in 6 of 21 (29%) esophageal examinations, 7 of 11 (63%) gastric examinations, and 4 of 6 (67%) pancreaticobiliary examinations. Poor image clarity with C-EUS in esophageal examinations was believed to be secondary to an inability to retain water in the esophagus. Catheter breakage occurred during 3 of the first 25 examinations. The catheter was subsequently modified to reduce frictional torque. Catheter breakage occurred in only 1 of 18 examinations following the modifications. C-EUS was rated as being relative]y easy to perform GASTROINTESTINAL ENDOSCOPY

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(little or no manipulation) in 37 of 43 (86%) patients, whereas EUS was rated as being relatively easy to performin 27 of 42 (64%) patients (p < 0.1). Mean time for performance of C-EUS when examining an esophageal or gastric lesion was 16.3 minutes, somewhat shorter than the mean time for examining a pancreatic or biliary stricture, which was 23.7 minutes (p < 0.1). Five biliary strictures and one pancreatic stricture were imaged. The ultrasound catheter was unable to traverse one biliary stricture and one pancreatic stricture. C-EUS was preferred to EUS in three of the four (75%) patients with traversable strictures because C-EUS provided a clearer image and was easier to perform. Because the location of the transducer could be determined by fluoroscopy, the C-EUS image could be precisely correlated with the radiographic stricture. C-EUS did not provide an adequate image in the two patients with nontraversable strictures. C-EUS was performed in 22 patients with mucosal lesions or submucosal tumors. Fourteen of these patients (64%) had lesions smaller than I cm. Overall, C-EUS was preferred to EUS in 14 of 22 (64%) patients. C-EUS was preferred to EUS in 10 of 14 (71%) patients with lesions smaller than 1 cm and in 4 of 8 (50%) patients with lesions larger than 1 cm. This difference did not reach statistical siguificance. Reasons for C-EUS preference were as follows: reliability and ease of endoscopical]y directed placement of probe on small lesions (9 patients), convenience of performing C-EUS during diagnostic endoscopy (3 patients), and inabi]ity to introduce the GF-UM20 echoendoscope (2 patients). EUS was preferred in 7 of 22 (32%) patients with mucosal lesions or submucosal tumors because of poor acoustic contact with the catherer (3 patients), large lesion (2 patients), and C-EUS equipment failure (2 patients). C-EUS had a higher image clarity than EUS in 10 of the 14 patients in whom C-EUS was preferred, whereas EUS had a higher image clarity than C-EUS in 5 of the 7 patients in whom EUS was preferred. Esophageal cancers were staged in 13 patients whose EUS staging was as follows: 3 patients with T1N0, 1 patient with T2N0, 1 patient with T3N0, 5 patients with T3N1, and 3 patients with T4N1 cancers. One patient had a tumor that could not be traversed by the EUS endoscope but could be traversed by the diaguostic endoscope, and 2 patients had cancers that could not be traversed by either instrument. C-EUS was performed in the latter 2 patients by blind passage of the catheter through the stenotic tumor. The celiac axis could not be imaged with the catheter under these circumstances. C-EUS did not provide any additional information in these 3 patients who had esophageal cancers that were incompletely staged by EUS. Two patients whose tumors were T4 by EUS (one with pleural invasion and one with aor294

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tic invasion) were judged to be T3 and T2 by C-EUS, and one patient judged T3 by EUS was judged to be T2 by C-EUS. Two patients staged as N1 by EUS would have been staged as NO by C-EUS because a lymph node adherent to a bulky tumor in the distal esophagus, and a lymph node proximal to a tumor in the upper esophagus, was not imaged during C-EUS. Thus, compared to EUS, C-EUS imaging would have resulted in a lower staging of esophageal maliguancy in 5 of 13 (38%) patients. Surgical correlation was not available in the majority of patients. EUS was preferred to C-EUS in 12 of 13 (92%) patients because CEUS did not provide an adequate image of the extraluminal tumor margin. Detection of lymph nodes was also more difficult with C-EUS. C-EUS was preferred to EUS in 1 patient who had a superficial malignancy because the catheter could be placed more reliably on top of the small nodules, and the image was very clear. DISCUSSION Endoluminal ultrasonography using echoendoscopes has become an accepted diaguostic modality with several established gastrointestinal applications. 1 Catheter-type ultrasound probes, however, have remained experimental because oflimited imaging depth and resolution. The development of improved slimmer probes raises the hope that catheter ultrasonography (C-EUS) will be a useful adjunct to EUS. We found that C-EUS is relatively easy to perform. These new, slimmer probes offer the convenience of performing intraluminal ultrasonography during diagnostic endoscopic procedures. C-EUS also promises to be less expensive than EUS. To define applications of C-EUS it is necessary to compare it to EUS in situations where C-EUS may be potentially useful. We found that C-EUS was as good as or better than EUS at evaluating mucosal lesions and submucosal tumors, particularly lesions that were less than 1 cm in size. The transducer could be positioned adjacent to the lesion under direct visualization and C-EUS could be performed conveniently during diagnostic endoscopy. On the other hand, advanced esophageal malignancies were not staged reliably with C-EUS. Although surgica] staging was not available on a majority of these patients, we believed that because of its known accuracy EUS was a valid comparative standard. Compared to EUS, C-EUS understaged esophageal tumors in 3 of 13 (23%) patients because it was unable to image the extralumina] border adequately. C-EUS also failed to detect lymph nodes that were detected by EUS in 2 of 13 (15%) patients. Other reports 4, 6-s indicate that C-EUS is well suited for staging early maliguancies, specifically gastric cancers. We studied only one patient with an early esophageal malignancy and found that C-EUS provided a better image than VOLUME 45, NO. 3, 1997

E U S in t h a t patient. The clinical utility of C-EUS in e v a l u a t i n g early esophagea] malignancies bears furt h e r investigation. C e r t a i n problems are still p r e s e n t w i t h the perform a n c e of C-EUS. Because of the h i g h e r f r e q u e n c y of the probes the imaging d e p t h of these c a t h e t e r s is limited (2.9 cm at 12 MHz, 1.8 cm at 20 MHz). This is not unexpected. Although resolution of these catheters is rauch b e t t e r t h a n earlier c a t h e t e r s (Olympus UM-lW), f u r t h e r d e v e l o p m e n t s such as a n inflatable balloon s y s t e m are n e e d e d to improve image clarity further. High-resolution endoluminal ultrasonograp h y at frequencies of 15 to 20 MHz has been reported 6, s as showing a seven to nine l a y e r s t r u c t u r e w h e n imaging the g a s t r o i n t e s t i n a l wall. T h e s e reports suggest t h a t the m u s c u l a r i s mucosae can be resolved at these frequencies, a n d such resolution is proposed as being i m p o r t a n t in guiding t h e r a p y of e a r l y gastric cancer. 6 We d e m o n s t r a t e d seven layers only in a limited n u m b e r of patients, and were u n a b l e to consist e n t l y resolve the m u s c u l a r i s mucosae. The lack of f u r t h e r resolution at h i g h e r frequencies m a y h a v e been caused by an inability to always image the wall at the focal zone of the catheter. A good image was p a r t i c u l a r l y difficult to obtain in the esophagus because the esophagus does not r e t a i n w a t e r well and large a m o u n t s of w a t e r c a n n o t be infused safely. Ano t h e r problem we e n c o u n t e r e d was the inability to t r a v e r s e certain pancreaticobiliary strictures with the catheter, despite the decreased d i a m e t e r of these probes. Probes specifically designed for i n t r a d u c t a l use (probes t h a t can be passed over guide wires or even s l i m m e r probes) m a y be n e e d e d for imaging the pancreaticobiliary s y s t e m reliably. This p r e l i m i n a r y investigation indicates t h a t these new u l t r a s o u n d c a t h e t e r s h a v e potential clinical applications. T h e y are convenient a n d easy to use. T h e y can provide a clear image. The c a t h e t e r s will probably be most useful in e v a l u a t i n g small mucosal or submucosal t u m o r s and early cancers. In t h e i r c u r r e n t form

t h e y will not be a n a d e q u a t e s u b s t i t u t e for E U S in staging n o n t r a v e r s a b l e malignancies. T h e y h a v e potential diagnostic applications in e v a l u a t i n g pancreatic a n d biliary strictures. C e r t a i n technical difficulties t h a t are still p r e s e n t with the use o f t h i s new, improved C-EUS s y s t e m will hopefully be solved with f u t u r e modifications.

Laparoscopic biliary guide wire: a simplified approach to choledocholithiasis

M a n a g e m e n t of choledocholithiasis d u r i n g laparoscopic cholecystectomy r e m a i n s a continuing challenge. M a n y innovative a n d effective approaches h a v e been developed, each with its own a d v a n t a g e s a n d limitations. We h a v e developed a technique t h a t is technically simple and, once accomplished, should ensure successful extraction ofstones. A t r a n s a b d o m i n a l guide wire is laparoscopically i n s e r t e d t h r o u g h the cystic duct, c o m m o n duct, and into the d u o d e n u m w h e r e it is r e t r i e v e d by esophagogastroduodenoscopy (EGD). Rendezvous E R C P 1-4 over the guide wire with endoscopic s p h i n c t e r o t o m y (ES) a n d stone remova] is p e r f o r m e d after surgery. The biliary guide wire renders the E R C P - s p h i n c t e r o t o m y technically easy and reliable.

Thomas R. Huntington, MD Theodore W. Bohlman, MD Received April 4, 1996. For revision July 15, 1996. Accepted October 1, 1996. From the Departments of Surgery and Gastroenterology, St. Luke's Regional Medical Center, Boise, Idaho. Reprint requests: Thomas Huntington, MD, 222 N. 2nd St., Suite 107, Boise, ID 83702. 0016-5107/97/4503-029555.00 + 0 GASTROINTESTINAL ENDOSCOPY Copyright © 1997 by the American Society for Gastrointestinal Endoscopy 37/69/78663

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