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ENDORECTAL SONOGRAPHY FOR RECTAL CARCINOMA D. DAVID DERSHAW, M.D. Department of Medical Imaging Memorial Sloan-Kettering Cancer Center, New York, New York

IN ULTRASONOGRAPHY the closer a transducer can be placed to the area being scanned, the higher the frequency of sound that can be utilized. Higher frequency sound is less penetrating and therefore travels less far in tissue. Close proximity of the transducer to the area of interest eliminates the need for a deeply penetrating beam. Higher frequency sound also results in greater resolution; tissue detail, not discernible with a lower frequency sound wave, can be visualized. In rectal endosonography a sonographic transducer is introduced per rectum, placing the transducer in intimate contact with the rectal wall. Although first widely utilized to study prostatic lesions, this technique is also useful in evaluating rectal wall lesions. The earliest efforts to utilize endorectal scanning were during the mid1950s by Wild anld Reid who designed and produced three probes by which they were able to scan the rectum and to detect alteration in the normal tissue pattern caused by cancer.1 The first extensive utilization of this idea, however, was by Watanabe two decades later. Using a specifically designed chair, which contained an ultrasound probe that could be positioned in the rectum of a patient sitting in the chair, he conducted mass screening for early detection of prostate cancer.2 It was almost another decade before practical clinical application of this technique was reported by Alzin3 and Dragsted4 in evaluating patients with rectal carcinoma. The significance of the development of this technique was the possibility of improving preoperative staging in patients with rectal carcinoma. This disease develops in about 42,000 Americans annually,5 and to a great extent treatment is determined by the extent of tumor penetration. There is an increasing trend toward transanal excision of early rectal carcinoma and preservation of the sphincter in patients with smaller tumors.6 Transmural penetration of tumor, however, greatly increases the risk of nodal metastases Address for reprint requests: Department of Medical Imaging, Memorial Hospital, 1275 York Avenue, New York, NY 10021

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for which pelvic lymphadenectomy may be required in an attempt to cure these patients.7 More extensive surgery increases morbidity but offers a greater prospect of cure for patients with more extensive tumor. Accurate preoperative staging is necessary to choose the surgical procedure to be utilized. Unfortunately, accurate preoperative staging has been a significant problem. Digital rectal examination is highly subjective, and its accuracy varies with physician experience.' Computed tomography and magnetic resonance imaging have been disappointing in this situation.9-" Work with endorectal sonography was undertaken by various investigators to obtain better staging information in this setting. The efficacy of endorectal sonography for staging rectal carcinoma was acknowledged when this technique was included as a staging modality in the 1988 American Joint Committee on Cancer's Manual for Staging of Cancer. Endorectal sonography can be easily performed, usually with minimal patient discomfort. At our institution no preparation is required, although some authors prefer a cleansing enema. The patient may be scanned in the left lateral decubitus, supine, or lithotomy positions. At Memorial SloanKettering we always examine in the left lateral decubitus position. Digital rectal examination precedes sonographic study. This is utilized to determine the course of the rectum and the position of the rectal tumor. The transducer is covered by a fitted condom, lubricated before insertion into the rectum. If the patient complains of pain with rectal manipulation, an anesthetic lubricant is used. After insertion of the transducer into the rectum, the condom is insufflated with 40-70 ml of degassed water. This pushes away any gas between the transducer and the rectal wall. Intervening gas totally reflects sound and prevents any image being obtained. The water filled condom also displaces the transducer slightly away from the rectal wall, thereby placing the rectum within the range of focus of the transducer. Images are routinely obtained in radial and longitudinal axes. Scanning can usually be done of lesions within 13 cm of the anal sphincter, and requires 10- 15 minutes to perform. Circumferential cancers that narrow the rectal lumen may not always allow for passage of the transducer, and scanning of these lesions may be limited. However, these invariably seem to be transmural carcinomas, and their staging is rarely in question. When the rectum curves sharply posteriorly, it may be difficult to place the transducer against the posterior rectal wall, and lesions situated there may be difficult to scan. Complications of this technique have not been reported. Manipulation of tumor by the transducer often exacerbates tumor bleeding for a short period, Bull. N.Y. Acad. Med.

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Fig. 1. This 68-year-old woman has a posterior rectal wall adenocarcinoma that expands the superficial layers, i.e., mucosa and submucosa, (large arrows) of the rectal wall. The muscularis propria (small arrows) is spared.

but this is not of clinical significance. The possibility of perforation through tumor by a rigid probe is always a hazard, but if this has occurred during sonographic scanning, it has not been reported. Sonographic characteristics of the rectal wall have been well described. They consist of three hyperechoic layers separated by two hypoechoic layers. The first echogenic layer is due to the water filled condom. A hypoechoic layer is then seen and is due to the mucosa. An echogenic layer is then seen and is caused by either the submucosa or the mucosa-muscularis propria interface (Figure 1). A hypoechoic layer is then present and is the muscularis propria (Figure 2). An echogenic margin between this layer and perirectal fat defines the outermost layer of the rectal wall (Figure 3). 12 Lymph nodes appear as hypoechoic masses in perirectal fat (Figure 4). Rifkin has suggested that if these measure more than 3 mm they are suspicious for metastatic disease.9 The pattern, however, is not specific, and lymph nodes enlarged by inflammation may have an identical pattern.12 Normal lymph nodes are probably not visualized. Prominent draining veins are also hypoechoic, but their serpiginous configuration makes them readily identifiable. If there is any doubt as to their nature, Doppler interrogation can determine whether a venous signal is present. Studies of the efficacy of endorectal sonography in staging rectal carcinoma have examined its accuracy in evaluating three different findings: depth of mural penetration of tumor; presence of perirectal adenopathy; and adjacent organ involvement. In most series the depth of tumor penetration has examined by evaluating the presence or absence of perirectal fat infiltration, Vol. 68, No. 3, July 1992

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Fig. 2. This 61-year-old man has an anterior rectal wall carcinoma (arrows) seen as an area of thickening of the rectal wall in this transverse scan. Deep to the cancer and separate from it can be seen the two seminal vesicles (s) and the urine-filled bladder (u).

i.e., transmural disease. With newer technology the depth of tumor penetration within layers of the rectal wall is also being examined. One of the earliest studies was reported by Hildebrandt in Homburg, Germany in 1984.'3 Twenty-five patients were examined by sonography and digital rectal examination. Digital examination was -able to evaluate only 17 tumors and accurately staged 15 of these, overestimating depth of tumor in two. Sonography accurately staged 23 of 25 tumors, overstaging two. Six years later, after their earlier promising results, this same group reported a larger series of 163 patients.'3 For tumor extending through the rectal wall, the sensitivity of sonography was 98% with a specificity, i.e., the ability to predict tumors confined to the rectal wall, of 84%. The positive predictive value, i.e., the prediction of penetration through the rectal wall, was 84% with a negative predictive value, i.e., the prediction of tumors confined to the rectal wall, of 98%. The accuracy of this series was 87%. In this same series 113 patients could be evaluated for perirectal adenopathy with pathologic correlation with the surgical specimen. Only 50% of all lymph nodes found in the surgical specimen were sonographically visualized. Lymph node metastases were correctly predicted in 31 patients and missed in 12 patients. In another 46 patients echogenic lymph nodes were found sonographically and correctly called benign. Perirectal nodal metastases were incorrectly predicted in 12 patients. In this group the sensitivity for predicting local nodal metastases was 72% with an accuracy of 76%. Bull. N.Y. Acad. Med.

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Fig. 3. This scan through a posterior rectal wall carcinoma, 8.5 cm. from the anal verge, shows tumor with an irregular deep margin (arrows) extending into the perirectal fat, which is echogenic and appears white. This signifies transmural penetration of tumor.

Another early study was reported by DiCandio'4 in Pisa on 55 patients. Evaluation of transmural spread of tumor had four false-negatives and one false-positive for a sensitivity and specificity of 91 % and positive and negative predictive values of 97% and 71%. In examining lymph node involvement 11 true positives and 11 false negatives were present among the 22 patients with perinodal metastases. Beynon and colleagues'5 in Bristol assessed the local invasion of rectal cancer in 51 patients. Transmural penetration was predicted with a sensitivity of 97%, specificity of 92%, and a positive predictive value of 97%. In the United States Jochem et al.'6 at the Mayo Clinic evaluated penetration of tumor beyond the muscularis propria in 50 cases with accuracy of 80%, sensitivity of 92%, and specificity of 76%. In 19 patients in whom perirectal adenopathy was identified and surgical correlation was available, nine had true metastases and 1O had only reactive adenopathy. In another 20 patients with surgical correlation, no nodes were seen, and in one of these Vol. 68, No. 3, July 1992

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Fig. 4. A scan through a a lateral rectal wall carcinoma in this 56-year-old woman shows a focus of transmural penetration (black arrows) into perirectal fat and two enlarged lymph nodes (white arrows) in perirectal fat. This contain metastatic disease.

cases metastatic disease was present in two perirectal nodes, while in the remaining 19 no metastatic disease was found in the nodes. In this series the detection of metastatic disease in perirectal nodes had a sensitivity and specificity of 90% and 66%, positive and negative predictive values of 47% and 95%, and accuracy of 72%. Rifkin and Marks'7 at Jefferson in Philadelphia published an early series including 26 patients with rectal carcinoma studied by endorectal sonography. Perirectal tumor extension was present in seven of these cases, all correctly identified sonographically. In another two cases transmural penetration was falsely predicted. The sensitivity and specificity were 100% and 88% for detecting transrectal penetration. In these same patients extrarectal nodal metastases were present in seven patients. Sonography identified these in six, and there were false-negative scans in another two. A more extensive experience of these investigators with 102 patients resulted in less dramatic results than had been published in other series.9 The detection of transrectal tumor penetration had a specificity of 77%, sensitivity of 67%, positive predictive value of 73%, and negative predictive value of Bull. N.Y. Acad. Med.

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72%. In 26 of these patients perirectal nodal metastases were present, of which 13 were sonographically detected. The sensitivity and specificity for detecting positive nodes was 50% and 92% with positive and negative predictive values of 68% and 84%. In 81 of the patients in this study CT staging was also utilized, and endosonography was found to be superior both for staging the extent of mural disease and detecting perirectal adenopathy. At Memorial Sloan-Kettering Cancer Center 38 consecutive patients with known rectal carcinoma were scanned, including six who had had their tumors irradiated.'8 In the 32 nonirradiated patients, endosonography successfully staged disease confined to the rectal wall in 18 of 20 (90%) and transmural extension in six of 12 (50%). Sonographic detection of transmural extension had positive and negative predictive values of 74% and 25% with sensitivity and specificity of 50% and 90%. In this group 14 patients had metastatic disease in perirectal nodes, and these were sonographically detected in 12. There were two false-negative examinations and 11 true-negative studies. Detection of perinodal adenopathy by sonography had a sensitivity and specificity of 63% and 85% with a positive and negative predictive value of 86% and 61%. In comparison to staging by digital rectal examination done by experienced colorectal surgeons, endosonography was slightly superior because of its ability to detect perirectal adenopathy. In irradiated patients, tumor shrinkage with therapy could be documented sonographically in all patients. Because irradiation destroys normal tissue planes, tumors could not be accurately staged postradiation. However, the digital rectal examination was unable to assess tumor shrinkage because of radiation induced peritumoral inflammation so that endosonography was superior in this situation also. In six patients an attempt was made to evaluate the presence or absence of adjacent organ involvement. In one woman peritumoral fibrosis was mistakenly called tumor extension into the uterus and ovary. In another woman tumor extension into the cervix was correctly predicted. In four men with anterior rectal wall carcinomas tumor extension into the prostate in one and the absence of prostatic involvement in another three were accurately iden-

tified. One limitation of accurate staging of tumors by endorectal sonography is peritumor inflammation, which destroys tissues planes and causes overstaging of some tumors. Microscopic tumor penetration is beyond the resolution of sonography and will result in understaging of tumor. Failure to differentiate between nodal enlargement due to neoplasia and some inflammatory processes is a constant problem in medical imaging and plagues sonography as Vol. 68, No. 3, July 1992

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well as other modalities. Microscopic metastases are also beyond the resolution capabilities of sonography. However, the superiority of endosonography to other imaging techniques and possibly to digital rectal examination as performed by highly experienced examiners has given this study an important place in evaluating the local extent of rectal carcinomas. CONCLUSION

The capabilities of endorectal sonography for high resolution of tissue planes and textures enable this technique to define the extent of mural penetration of rectal carcinoma better than by other imaging modalities and at least as well as can be done by digital rectal examination. In irradiated tumors it is superior to other techniques in demonstrating alteration in tumor size. The ability accurately to predict adjacent organ involvement is promising but the experience here is limited. Perirectal adenopathy can be detected in many patients but the accuracy of endosonography in this setting is limited. However, the technique does appear to be superior to other available examinations in evaluating for perirectal nodal metastases preoperatively. These capabilities may make endorectal sonography the most accurate means available preoperatively to stage the local extent of tumor in patients with rectal carcinoma and to evaluate treatment response in patients whose tumors are being irradiated. REFERENCES 1. Wild, J.J., and Reid, J.M.: Diagnostic use of ultrasound. Br. J. Phys. Med. 11: 248-64, 1956. 2. Watanabe, H., Ieari, D., lanahashi, Y. Transrectal ultrasonotomography of the prostate. J. Urol. (Paris) 114: 734-39, 1975. 3. Alzin, H.H., Kohlberger, E., Schwaiger, R. and Alloussi, S. Valeur de l'echographic endorectal dans la chiurgie du rectum. Ann. Radiol. (Paris) 26: 334-36, 1983. 4. Dragsted, J. and Gammelgaard, J.: Endoluminal ultrasonic scanning in the evaluation of rectal cancer. Gastrointest. Radiol. 8: 367-69, 1983. 5. Silverberg, E.: Cancer statistics. CA 35: 19-35, 1985. 6. Steams, M.W., Jr., Sternberg, S.S., and DeCosse, J.J.: Local Treatment of Rectal Cancer. In: Large Bowel Cancer Clinical Surgery, Int. vol I, DeCosse, J.J., editor. London, Churchill Livingston, 1981, pp. 143-53. 7. Enker, W.E., Heilweil, M.L., Hertz, R.E.L., et al.: En bloc pelvic lymphadenectomy and sphincter preservation in the surgical management of rectal cancer. Ann. Surg. 203: 426-33, 1986. 8. Nichols, R.J., York, M.A., Morson, B.C., et al.: The clinical staging of rectal cancer. Br. J. Surg. 69: 404-09, 1982. 9. Rifkin, M.D., Ehrlich, S.M., and Marks, G.: Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology 170: 319-22, 1989. 10. Goshlin, H., Lerner, R.M., Gadeholt, B., et al.: CT staging of early rectal carcinoma. Gastrointest. Radiol. 12: 253-56, 1987. 11. Butch, R.J., Stark, D.D., Wittenberg, J., et al.: Staging of rectal cancer by MR and CT. Am. J. Radiol. 146:1155-60, 1986.

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12. Hildebrandt, U., Beynon, J., Feifel, G., et al.: Endorectal Sonography. In: Endosonography in Gastroenterology, Gynecology and Urology, Feifel, G., Hildebrandt, U., and Mortensen, N. J. Mc., editors. New York, Springer-Verlag, 1990, pp. 81-130. 13. Hildebrandt, U. and Feifel, G.: Preoperative staging of rectal cancer by intrarectal ultrasound. Dis. Colon Rectum 28: 42-46, 1985. 14. DiCandio, G., Mosca, F., Campatelli, A., et al.: Endosonographic staging of rectal carcinoma. Gastrointest. Radiol. 12: 289-95, 1987. 15. Beynon, J., Roe, A.M., Foy, D.M.A., et al.: Preoperative staging endoluminal ultrasound. J. R. Soc. Med. 80: 23-24, 1987. 16. Jochem, R.J., Reading, C.C., Dozois, R.R., et al.: Endorectal ultrasonographic staging of rectal carcinoma. Mayo Clin. Proc. 65: 1571-77, 1990. 17. Rifkin, M. and Marks, G.J.: Transrectal US as an adjunct in the diagnosis of rectal and extrarectal tumors. Radiology 157: 499-502, 1985. 18. Dershaw, D.D., Enker, W.E., Cohen, A.M., and Sigurdson, E.R.: Transrectal ultrasonography of rectal carcinoma. Cancer 66: 2336-40, 1990.

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411 ENDORECTAL SONOGRAPHY FOR RECTAL CARCINOMA D. DAVID DERSHAW, M.D. Department of Medical Imaging Memorial Sloan-Kettering Cancer Center, New York,...
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