Endoscopic Ultrasound-Guided Transrectal Biopsies of Pelvic Tumors

Original Articles

Endoscopic Ultrasound–Guided Transrectal Biopsies of Pelvic Tumors

Marco Sailer, M.D., Dieter Bussen, M.D., Martin Fein, M.D., Stephan Freys, M.D., Sebastian E. Debus, M.D., Arnulf Thiede, M.D., Karl-Hermann Fuchs, M.D.

The aim of this study was to evaluate the feasibility, safety, and diagnostic accuracy of endorectal ultrasound–guided biopsies in patients with extrarectal lesions. Data from all patients with suspicious pelvic pathology who underwent endorectal ultrasound–guided biopsies were collected prospectively. To evaluate the accuracy of the diagnosis, all patients with benign histology but primary suspicion of a malignant lesion were followed up for at least 12 months. A total of 48 patients whose median age was 66 years were evaluated. Apart from one postbiopsy hemorrhage, which was managed conservatively, no other complications were encountered. Sufficient tissue was removed to allow histologic examination in all cases. A large variety of diagnoses including primary and secondary malignancies (n 25) as well as benign pathologies (n 23) could be established. There were no false positive but three false negative histologies in patients with proven local recurrence of a malignant tumor during the follow-up period. This results in a sensitivity of 88%, specificity of 100%, positive predictive value of 100%, and negative predictive value of 89%. It is concluded that endoscopic ultrasound–guided transrectal biopsy is a safe method with a high diagnostic accuracy in the assessment of pelvic tumors. ( J GASTROINTEST SURG 2002;6:342–346.) © 2002 The Society for Surgery of the Alimentary Tract, Inc.

KEY WORDS: Endorectal ultrasound, transrectal biopsy, pelvic tumor

Endorectal ultrasound (ERUS) is a well-estab- PATIENTS AND METHODS lished imaging technique for the evaluation of an- orectal diseases, most notably in the preoperative During a study period of 7 years, we prospectively staging of rectal cancer.1 Furthermore, ERUS has collected data from all patients undergoing ERUS at also gained acceptance in the evaluation of anal our institution. Patients with suspicious or unclear sphincter morphology in fecal incontinence,2,3 in pa- extrarectal pelvic pathology who underwent ERUS- tients presenting with perianal sepsis,4,5 and in the guided biopsies were included in the present study. staging and follow-up of anal carcinoma.6,7 Because After informed consent was obtained, patients were of its high resolution, ERUS is also useful in the as- prepared for the procedure with an orthograde sessment of perirectal pathology if the lesions are bowel lavage and local (i.e., intrarectal) application within the reach of the ultrasound probe, which— of an antiseptic solution immediately before the ex- depending on the frequency—is generally in the amination. Patients routinely received a single dose range of 6 to 8 cm.8 Whereas there is an extensive of intravenous antibiotic prophylaxis with metro- body of literature dealing with perirectal absces- nidazole and cefotiam. Sedation with intravenous ses4,8–10 or lymph node involvement in rectal carcino- midazolam was necessary in only three patients. mas,1,11–14 there are only a few reports of application The procedure was carried out with patients in of ERUS for nonprostatic, nongynecologic pelvic dis- the lithotomy position using a rotating scanner ease in general,8,9,15,16 and ERUS-guided biopsy of (Combison 310, Kretz Co., Zipf, Austria) with a these lesions in particular.8,17 The aim of this study special biopsy aid that allows precise positioning of was, therefore, to evaluate the feasibility, safety, and the biopsy needle under constant ultrasound control. diagnostic accuracy of ERUS-guided biopsies in pa- The rectal probe measures 16 cm in length, with a tients presenting with extrarectal pelvic lesions. head diameter of 21 mm. During the examination

Presented at the Forty-Second Annual Meeting of The Society for Surgery of the Alimentary Tract, Atlanta, Georgia, May 20–23, 2001 (poster presentation). From the Department of Surgery (M.S., D.B., M.F., S.F., S.E.D., A.T., K.-H.F.), University School of Medicine, Wuerzburg, Germany. Reprint requests: Marco Sailer, M.D., Department of Surgery, University of Wuerzburg, Josef-Schneider-Str. 2, 97080 Wuerzburg, Germany. e-mail: [email protected]

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the frequency of the bifocal probe can be switched RESULTS from 7.5 to 5 MHz, thus allowing assessment of ex- A total of 48 patients (30 men) who had a me- trarectal pathology with a maximum tissue penetra- dian age of 66 years (range 18 to 87 years) under- tion of 7 cm. Resolution for both frequencies is less went ERUS-guided transrectal biopsy. In all patients than 1 mm. The transducer rotates at a speed of 12 the indication for the procedure was a suspicion of cycles per second, generating a 360-degree real-time either metastatic disease (n 31) or a primary tumor image. The beams can be emitted longitudinally of unknown etiology (n 17). In almost all cases producing a 100-degree sector or transversely (360- (91%) there had been additional imaging (CT scan degree image) in reference to the longitudinal axis of and/or MRI) before the ERUS. the rectum. A special biopsy software program acti- With regard to localization, size, and sonographic vates a small square in the transverse plane (Fig. 1) appearance of the lesions, a wide range was observed. and a dotted line in the longitudinal plane (Fig. 2) on Tumor localization varied from 4 to 16 cm measured the monitor, allowing exact visualization of the bi- from the anal verge, and the position with regard to opsy target and needle tract, respectively. the rectal axis was anterior in 19%, posterior in 44%, Using the TRU-CUT principle, a high-speed lateral in 25%, and circular in the remaining 12%. biopsy needle (Magnum, Bard/Angiomed Co., Karls- Most lesions (73%) were within 2.0 cm of the rectal ruhe, Germany) is fired once the target has been pre- wall. The median size of the lesions measured 26 cisely visualized, both transversely and longitudi- mm (range 7 to 64 mm). Most tumors (61%) were nally. The core biopsy needle measures 18 gauge and hypoechoic (Fig. 3), whereas an echo-mixed (Fig. 4) is 20 cm long, providing a specimen length of 19 mm or hyperechoic (Fig. 5) pattern was noted in 17% with a 0.9 mm diameter. All specimens were sent for and 22%, respectively. Compared with benign histologic examination. To evaluate the diagnostic changes, lesions that proved malignant on histo- accuracy, all patients with benign histology but pri- pathologic examination appeared hypoechoic more mary suspicion of a malignant lesion were followed frequently (39% vs. 84%). up for a minimum of 12 months. Sensitivity, specific- Apart from one postbiopsy hemorrhage, which was ity, and positive and negative predictive values were managed conservatively with no transfusion require- calculated. ment, no other complications were encountered. Suf- ficient tissue was removed to allow a histologic examination in all cases. A large variety of diagnoses

Fig. 1. Hypoechoic extramucosal lesion in the anterior position measuring 20 10 mm (arrows). The small square indi- cates the biopsy target. Histologic examination revealed a re- Fig. 2. The hyperechoic biopsy needle is clearly visible in the current adenocarcinoma following low anterior resection for longitudinal plane. The biopsy tract is along the dotted line. rectal cancer 9 months previously. The distance between two dots equals 1 cm.

Journal of 344 Sailer et al. Gastrointestinal Surgery

Fig. 3. A large hypoechoic tumor (34 65 mm) is seen in the Fig. 5. This 63-year-old patient had undergone radical pros- right lateral position localized 12 cm from the anal verge (ar- tatectomy for cancer 6 months earlier. Anteriorly, the pros- rows). Histologic examination showed an epidermoid cyst. tatic compartment is seen as an echo-free area. This patient presented with a palpable tumor on rectal digital examination. On transrectal biopsy, this hyperechoic lesion (arrows), which measured 47 22 mm, proved to be a lymph node metastasis. including primary and secondary malignancies (Table 1), as well as benign pathologies (Table 2), could be established. There were no false positive but three cases in which only one or two aspirations were per- false negative histologies in patients with proven local formed. This results in a sensitivity of 88%, specificity recurrence of a malignant tumor during the follow-up of 100%, positive predictive value of 100%, and nega- period. All three patients were among the first 15 tive predictive value of 89%. Subsequently, as a result of these negative biopsies, at least five specimens were removed from every patient. Since then no false negative results have been encountered.

DISCUSSION The diagnostic workup of pelvic tumors can occa- sionally be laborious. When using imaging techniques such as CT scan and/or MRI in patients with a history

Table 1. Histologic diagnosis of ultrasound-guided transrectal biopsy in patients with malignant histology (n 25)

Histology n

Adenocarcinoma 10 Squamous cell carcinoma 5 Prostate cancer 4 Malignant melanoma 2 Adenosquamous carcinoma 1 Signet ring carcinoma 1 Fig. 4. Transrectal biopsy of this presacral echomixed tumor Neuroendocrine tumor 1 (45 22 mm) disclosed an adenosquamous carcinoma of un- Undifferentiated carcinoma 1 25 known origin. Total

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Table 2. Histologic diagnosis of ultrasound-guided The use of ERUS-guided biopsy of the prostate transrectal biopsy in patients with benign histology gland is a well-established method in urology and (n 23) has gained widespread acceptance in routine practice.19 Well-documented studies including several Histology n thousand patients have shown the safety and efficacy Connective/fatty tissue 6 of this procedure with little patient discomfort and Scar tissue 5 very low morbidity.20 Infection, albeit a rare event, is Chronic inflammation 4 probably the most serious complication and the ad- Nonspecific inflammation 5 ministration of a prophylactic antibiotic is generally Necrosis 1 recommended.19–21 Because the perirectal tissue is Leiomyoma 1 not as well vascularized and contained as the pros- Colitis cystica profunda 1 tate, it was thought that a more thorough prepara- Total 23 tion, including a complete bowel lavage, was war- ranted. Furthermore, our present regimen includes of a pelvic malignancy, for example, rectal, prostate, or a second-generation cephalosporin as well as a po- cervical cancer, it is often difficult to differentiate be- tent antianaerobic coverage with metronidazole. tween scar tissue and recurrent tumor, particularly if Whereas hematuria is a common complication fol- the space-occupying lesion is small and tumor markers lowing prostatic needle biopsy and can occur in up to are only slightly raised if at all. With the advent of 58%,22 other hemorrhagic events such as rectal positron emission tomography (PET), these lesions bleeding are generally encountered in only a small can be further divided into those with and those with- percentage.23 However, rates as high as 37% have out uptake of the marker used, which is usually 2-[18F] been published.22 As with any other invasive proce- fluoro-2-deoxy-D-glucose.18 However, to conclu- dure, it seems prudent not to perform ERUS-guided sively decide on further therapeutic strategies, which transrectal biopsy in patients taking anticoagulant or might range from palliative conservative measures to thrombolytic medication. If a biopsy is nevertheless major surgery such as multivisceral resection, a definite needed, medication should either be discontinued, if histologic diagnosis needs to be established. The same possible, or the patient should be monitored on an holds true for patients with no previous history who in-patient basis. present with a symptomatic or incidental pelvic tumor There are only a few studies in the nonurologic, that cannot be clearly classified by means of either im- nongynecologic literature dealing with transrectal aging, laboratory investigations, or follow-up exami- biopsy of pelvic masses. Apart from anecdotal re- nations, as directed by the respective specialists ( i.e., ports of small patient cohorts, 8,16,17,24 there are two urologist, gynecologist, or colorectal surgeon). articles describing transrectal ultrasound-guided bi- Percutaneous biopsies assisted by either CT or ab- opsies in larger series of patients with suspected re- dominal ultrasound imaging have several limitations. currence of rectal carcinoma. Hünerbein et al.25 The distance from the surface to the lesion can be con- report 30 patients who underwent transrectal ERUS- siderable, which renders precise puncture difficult if guided biopsies during tumor follow-up. They found not impossible. Tumors can be obscured by anatomic 10 patients with malignant histologies, whereas the structures such as the uterus, adnexa, or bowel. Fur- remaining patients had no evidence of recurrent dis- thermore, patient discomfort and the risk of intraperi- ease during a follow-up period of 7 months. No toneal infection should also be kept in mind when this complications were encountered. Löhnert et al.26 type of approach is used. Transrectal ultrasound over- used a transperineal approach under local anesthesia comes most of these restrictions and, most important, in 111 patients with suspicious masses following low spatial resolution is considerably better compared with anterior resection for rectal cancer. In 52 patients lo- all other imaging techniques including PET. There- cal recurrence was shown on histologic examination. fore ERUS is able to potentially detect lesions at a Potentially curative salvage surgery was possible in stage where conventional diagnostic tools would fail to 31 patients, 25 of whom had been diagnosed by do so. In our series only 13 tumors (27%) were easily ERUS alone (81% of all curatively resected patients palpable by rectal examination. Theoretically these tu- with local recurrence). There were no false positive mors could have been approached by simple digitally or negative results. In both of these papers, the total guided transrectal needle biopsy. However, ERUS number of biopsies retrieved from each patient is not provides biplanar imaging with very precise target lo- mentioned. However, taking into consideration our calization and needle monitoring. Lesions can be biop- three false negative histologies, all from the early pe- sied under visual control rendering the procedure riod of the study where only one or two aspirations more controlled and consequently safer. were performed, we would now recommend obtain-

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