AJR InPractice
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Berton, F.
Right arrow Articles by Wilson, S. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Berton, F.
Right arrow Articles by Wilson, S. R.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?
Hotlight (NEW!)
Right arrow
What's Hotlight?
DOI:10.2214/AJR.07.3188
AJR 2008; 190:1495-1504
© American Roentgen Ray Society


Review

Perspective on the Role of Transrectal and Transvaginal Sonography of Tumors of the Rectum and Anal Canal

Francesca Berton1,2, Giada Gola1,3 and Stephanie R. Wilson1,4

1 Section of Ultrasound, Department of Medical Imaging, Toronto General Hospital, University of Toronto, Toronto, ON, Canada.
2 Present address: Institute of Radiology, IRCCS San Matteo Hospital, University of Pavia, Pavia Italy.
3 Present address: Serves di Radiologia, Ospedale Civile di Voghera, Voghera, Pavia, Italy.
4 Department of Diagnostic Imaging, Foothills Medical Centre, 1403 29 St. NW, Calgary, AB, Canada T2N 2T9.

Received January 29, 2007; accepted after revision December 27, 2007.

 
Address correspondence to S. R. Wilson (stephanie.wilson{at}calgaryhealthregion.ca).

S. R. Wilson acts as an advisor on sonography to Philips Medical Systems.


Abstract
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
OBJECTIVE. Intestinal sonography is characterized by excellent resolution of the multiple layers of the intestinal wall and sensitive depiction of the degree of invasion of rectal tumors. Traditional transrectal sonography has been enhanced by the addition of transvaginal scanning for women and by advances in transducer technology. Our purpose is to describe the current status of sonography in the evaluation of rectal and anal tumors and in the staging of rectal cancer.

CONCLUSION. Endorectal and transanal sonography are fast, minimally invasive techniques that can be performed with portable equipment and yield rapidly interpreted images. They are considered the reference standard for the preoperative staging of rectal and anal cancers and have relatively high accuracy in categorization of tumors and nodes in TNM staging.

Keywords: anal cancer • Doppler imaging • rectal cancer • rectal tumors • staging • transrectal sonography • transvaginal sonography


Introduction
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
Sonography of the rectum can be performed with an echoendoscope, which is a sonographic crystal array attached to an endoscopic device suitable for study of the lower gastrointestinal tract, or with an endorectal sonographic probe, which comprises a rigid probe and a fixed sonographic crystal array. Examinations with the devices yield similar information related to pathologic changes in the rectum. Endorectal sonography was introduced to clinical practice in 1983 and has been successfully developed for evaluation of both the prostate and the rectum. The prostate gland, which maintains a constant orientation and relation to the rectum, is easily and consistently evaluated with transrectal sonography. Scanning of the rectum is challenging with a probe positioned within the rectum because retained fecal material may be present, rectal lesions can be mobile or large, and general orientation is difficult.

To facilitate study of the rectal wall, a rotating mechanical crystal was introduced for transrectal sonography. Positioned within the rectal lumen and surrounded by a fluid-filled condom or balloon, the device gives a 360° axial view of the rectal wall and surrounding soft tissues. Reports of studies performed with such a transducer compose most of the early literature on the technique of transrectal sonography [1, 2]. Although these rotating crystals are durable and popular, the technique has potential mechanical problems related to jamming of the mechanism, entanglement of the inflated balloon, and poor resolution because of reduction in the effective aperture of a rotating crystal.

A number of changes in our scanning techniques over the last decade have transformed our ability to study diseases of the rectum and anal canal with sonography. These changes include introduction of biplane capability on a single transrectal sonographic probe of a high-end sonographic system, which allows placement of two transducer arrays. The probes provide state-of-the-art resolution and have sensitive Doppler capability, enabling acquisition of useful information about tumor structure and vascularity (Figs. 1A, 1B and 2A, 2B), which enhances the familiar gray-scale transrectal sonographic technology.


Figure 1
View larger version (153K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 1A 71-year-old woman with biopsy-proven tubulovillous adenoma who has undergone unsuccessful transrectal sonography. Images show advantages of biplane transducer technology, use of sodium phosphate enema, addition of color Doppler, and transvaginal scanning. Axial transrectal sonographic image shows soft mass on left wall of rectum outlined by fluid in rectum from sodium phosphate enema and evident on real-time examination.

 

Figure 2
View larger version (120K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 1B 71-year-old woman with biopsy-proven tubulovillous adenoma who has undergone unsuccessful transrectal sonography. Images show advantages of biplane transducer technology, use of sodium phosphate enema, addition of color Doppler, and transvaginal scanning. Color transrectal sonographic image confirms presence of lesion.

 

Figure 3
View larger version (158K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 2A 62-year-old woman with very small T1 rectal lesion. Images show advantages of biplane transducer technology, use of sodium phosphate enema, addition of color Doppler, and transvaginal scan. After normal findings on transrectal sonography, axial sonographic image of rectum obtained with transvaginal probe shows subtle superficial hypoechoic mass on left anterolateral wall. Submucosa and muscularis propria are intact.

 

Figure 4
View larger version (110K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 2B 62-year-old woman with very small T1 rectal lesion. Images show advantages of biplane transducer technology, use of sodium phosphate enema, addition of color Doppler, and transvaginal scan. Color Doppler image confirms vascularity of lesion. Small superficial tumor can be difficult to find with transrectal sonography and other imaging techniques.

 
Staging of rectal cancer before selection of a treatment regimen is critical for identifying superficial tumors amenable to transanal excision and invasive lesions better managed with neoadjuvant chemoradiation therapy before surgery. The contrast and spatial resolution of state-of-the-art sonography enable visualization of the multiple layers of the rectal wall, making sonography an excellent choice for the staging of both superficial and invasive rectal tumors. Our purpose is to describe our experience with sonography in the evaluation of all tumors of the rectum and to highlight the advantages of a variety of transducers and techniques for optimizing results.


Anatomy of the Rectum and Anal Canal
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
The rectum is the terminal part of the large intestine. At the level of S3, it is in continuity with the sigmoid colon, and it ends at the anocutaneous line. The rectum can be divided in two parts: the pelvic rectum or rectal ampulla, which is a contractile reservoir, and the perineal rectum, or anal canal (Figs. 3A, 3B and 3C).


Figure 5
View larger version (51K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 3A Anatomy of rectum and anal canal. Coronal schematic shows caudal extent of rectum in anal canal. Thin black line in rectal wall, representing muscularis propria, becomes thicker black internal anal sphincter at anorectal junction. Fibers of levator ani muscle contribute to external sphincter.

 

Figure 6
View larger version (22K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 3B Anatomy of rectum and anal canal. Cross-sectional schematics show rectum (B) and anal canal (C).

 

Figure 7
View larger version (44K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 3C Anatomy of rectum and anal canal. Cross-sectional schematics show rectum (B) and anal canal (C).

 
Rectal Ampulla
The rectum at the level of the rectosigmoid flexure is in continuity with the sigmoid colon. Where it traverses the pelvic diaphragm, the rectum becomes the anal canal. The rectum starts at the sacral promontory and ends beyond the coccyx, having a length of 12-15 cm. The rectum occupies a presacral position and is surrounded by perirectal fat.

Anal Canal
The anal canal is surrounded by a double sphincter. The first component consists of a smooth-muscle layer called the internal anal sphincter and a thickening of the circular muscle layer of the rectum that surrounds the superior three fourths of the anal canal. The internal anal sphincter is controlled by the autonomic nervous system. The second component is a striated muscle layer called the external anal sphincter, which forms a ring around the anal canal in continuity in the superior aspect with the puborectalis and levator ani muscles. The external anal sphincter is supplied by the cerebrospinal nervous system. The anal canal begins at the anorectal line and ends at the anal verge, generally having a length of 3 or 4 cm. The anal lumen is divided into three parts: the colorectal zone with columnar mucosa, the transitional zone or pecten, and the cutaneous zone.

Blood Flow and Rectal Lymph Nodes
The blood supply of the rectum depends on many arteries that originate in the aorta and iliac and pudendal or inferior gluteal arteries. Lymphatic drainage is important to carcinomatous dissemination. The lymph vessels begin in the intramural lymphatic plexuses and drain to the pararectal lymph nodes in the perirectal fat. The collectors drain in three nodal sites: superior, middle, and inferior rectal nodes. The drainage ends in the iliac and periaortic lymph nodes. The inferior rectal nodes drain only the anal canal below the mucocutaneous junction to the superficial inguinal lymph nodes [3].


Sonographic Technique
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
Transrectal sonography is an accepted standard for the staging of known rectal cancer. It is not, however, an acceptable technique for screening the rectum for tumors. Therefore, actual acquisition of a scan is best directed at known rectal masses, although with sufficient effort, time, and meticulous technique, a survey of the rectum can be performed. The technique of transrectal sonography requires a learning curve for orientation of biplane probes and for identification of rectal tumors.

We recommend that before sonography is performed for assessment of a rectal tumor, all relevant clinical information about the tumor be obtained, including the method of detection (digital rectal examination or colonoscopy), biopsy confirmation, and size and location. Whether excisional biopsy of rectal polyps has been performed and a diagnosis of cancer made is critical information because the tumor may have been largely or completely removed at biopsy. Digital rectal examination is performed before transrectal sonography, and palpable masses are documented. In clinical practice, differentiation of a soft, compliant tubulovillous adenoma from a firmer and often fixed malignant rectal tumor at digital rectal examination is highly contributory to a successful transrectal sonographic examination.


Figure 8
View larger version (41K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 4A Normal layers of bowel wall. Schematic shows loop of bowel.

 


Figure 9
View larger version (101K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 4B Normal layers of bowel wall. Bowel wall in cross section (B) and long axis (C).On sonography wall consists of alternating layers of echogenicity and hypoechogenicity beginning on inside with echogenic layer that represents mucosal interface. Dominant echogenic layer is submucosa, and each hypoechoic layer contains muscle fibers.

 


Figure 10
View larger version (63K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 4C Normal layers of bowel wall. Bowel wall in cross section (B) and long axis (C).On sonography wall consists of alternating layers of echogenicity and hypoechogenicity beginning on inside with echogenic layer that represents mucosal interface. Dominant echogenic layer is submucosa, and each hypoechoic layer contains muscle fibers.

 
Transrectal sonography is well tolerated by most patients, is inexpensive, and is easily performed. Preparation for the procedure is minimal, requiring only a sodium phosphate (Fleet®, Fleet Laboratories) enema immediately before the examination to clean the rectum and to add fluid to the rectal lumen for outlining intraluminal masses (Figs. 1A and 1B). Endorectal sonography is performed with a hand-sheld probe, which is inserted into the rectum through the anal canal. We do not use probes that require an inflated fluid-filled balloon and instead use biplane probes inserted with only a clean condom covering the transducer head. We have used probes with a curved array coupled with a linear array, both on the same side of the transducer (HDI 5000, Philips Medical Systems), and with two curved arrays (Aplio, Toshiba), one on the end of the probe and the other on the transducer side for scanning in perpendicular planes. The minor disadvantages of the biplane probes, related to the lack of a complete axial view of the rectum and perirectal soft tissues, are more than alleviated by the superior imaging afforded by these transducers.

In examinations of women, we use transvaginal probes to study rectal and anal lesions when transrectal sonography is difficult or fails to stage the rectal tumor. The accuracy of this technique is equivalent to that of conventional transrectal sonography for staging of rectal cancer. Use of the transvaginal technique overcomes problems related to the presence of stenotic, large, very small, high, or very low tumors and enables more thorough evaluation of the rectovaginal septum [4]. Transvaginal scanning is performed with high-frequency (9- to 12-MHz) transducer arrays. Modification of the routine technique includes elevation of the examining hand to allow the end-fired probe to be directed posteriorly at the region of interest. The rectum is visualized in cross section or in the long axis depending on the orientation of the probe. Alternatively, a biplane probe with a convex and linear side-firing transducer can show the rectum well in the transvaginal approach. Still experimental are improved methods of studying the rectum and anal canal with 3D endorectal (endoanal) sonography [5].


Figure 11
View larger version (109K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 5 42-year-old man who has undergone successful excision of rectal carcinoid. Follow-up sagittal transrectal sonographic image obtained with biplane linear rectal probe shows five layers of normal rectal wall. Muscle layers are hypoechoic, and submucosa is dominant echogenic layer. Fluid is present within rectal lumen, which appears black. Perirectal fat appears echogenic or white.

 


Figure 12
View larger version (72K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 6 Schematic shows T component of TNM staging of rectal cancer. Tumors are red and exhibit progressively deeper invasion beginning at 10-o'clock position, where T superficial noninvasive lesion involves only superficial layers of intestinal wall. At 7-o'clock position, T1 lesion invades submucosa (yellow). At 5-o'clock position, T2 lesion invades muscularis propria (blue). At 2-o'clock position, T3 lesion exhibits full-thickness invasion through layers of rectal wall with invasion of surrounding perirectal fat. In directly anterior aspect (12-o'clock position), T4 lesion exhibits invasion of prostate gland.

 
Sonography of the Rectum
The sonographic appearance of the normal rectal wall is five layers of alternating hyperechogenicity and hypoechogenicity with the inner and outermost layers appearing echogenic. The sonographic layers correspond to the histologic layers of the intestinal wall (Figs. 4A, 4B and 4C) and are constant throughout the intestinal tract (Fig. 5). The muscular components of the wall appear hypoechoic, and the other tissues are echogenic.

Sonography of the Anal Canal
Variation of the wall layering of the rectum occurs in the anal canal in that the circular muscle layer of the muscularis propria becomes the internal anal sphincter at the anorectal junction. In the upper two thirds of the anal canal, the internal anal sphincter can be seen as a complete hypoechoic wide band. The lower anal canal can be recognized by the circumferential hyperechoic band of striated muscle, the external anal sphincter (Figs. 3A, 3B and 3C). All axial images are oriented by convention as if they are viewed from below with the anterior abdominal wall at the top of the image and the right side on the left side of the image. Therefore, the anterior rectal wall appears at the top of the image and the posterior wall appears at the bottom of the image. Sagittal images are viewed as if the patient's head is on the left side of the image.


Rectal Carcinoma
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
Clinical Features
Colorectal carcinoma is an extremely common disease with great social impact. It is one of the most common malignant tumors in the United States, Europe, and Japan, after lung and prostate cancer among men and lung and breast cancer among women. It is equally prevalent among men and women and usually occurs in later life (60-70 years). Fifty to sixty percent of the tumors are localized to the rectosigmoid region. The prognosis among patients with malignant tumors of the rectum is negatively affected by advanced stage at diagnosis; extramural spread of the tumor into the mesorectum; tumor involvement of the anal sphincter, levator ani muscle, or adjacent organs; and advanced nodal involvement. Optimal management of colorectal carcinoma is predicated on curative resection and thus the ability to achieve surgical clearance at the circumferential margins of resection. A 1-mm tumor-free margin is the minimum requirement [6, 7].

Transrectal Sonography and Rectal Cancer
Although there are both institutional and geographic preferences, transrectal sonography is a well-established method and is considered by many the reference standard for the preoperative assessment of rectal cancer. Transrectal sonography depicts rectal wall stratification and tumor extension within and through the rectal wall, especially for T1 and T2 lesions, for which it is more accurate than MRI and CT [8-11]. Used with MRI for identification of the mesorectal fascia in patients with invasive disease [12], transrectal sonography is an invaluable component of local staging of rectal cancer [13-15].

Accurate preoperative regional staging, based on the TNM system (Fig. 6), is essential for planning optimal therapy. Whereas a small and superficial tumor can be managed with transanal excision, more extensive resection is necessary for larger tumors and those involving the deeper layers of the rectal wall. With transmural wall invasion and tumor involvement of the perirectal fat, neoadjuvant chemoradiation before surgery is the accepted standard of care. The addition of MRI to evaluation of patients with this lesion enables precise identification of the mesorectal fascia because tumors that traverse this plane are unlikely to allow a satisfactory circumferential margin of resection. Trans rectal sonography can precisely depict sphincter infiltration. Although CT and MRI show neoplastic wall thickening, these examinations do not allow discrimination of involvement of individual layers for accurate staging of tumors that do not extend beyond the rectal wall [9].


Figure 13
View larger version (138K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 7A 42-year-old woman with small palpable mass on left anterior rectal wall found at digital rectal examination that proved to be T1 adenocarcinoma of rectum. Curved axial (A) and linear sagittal (B) transrectal sonographic images show superficial hypoechoic tumor with subtle involvement of echogenic submucosa.

 


Figure 14
View larger version (108K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 7B 42-year-old woman with small palpable mass on left anterior rectal wall found at digital rectal examination that proved to be T1 adenocarcinoma of rectum. Curved axial (A) and linear sagittal (B) transrectal sonographic images show superficial hypoechoic tumor with subtle involvement of echogenic submucosa.

 


Figure 15
View larger version (137K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 8 56-year-old man with early T3 rectal carcinoma imaged with biplane rectal probe. Axial transrectal sonographic image shows hypoechoic tumor that has destroyed submucosa and muscularis propria. Gross extension of tumor into perirectal fat is evident. Echogenic margins (arrows) of remaining submucosa are present on each side of invasive tumor.

 


Figure 16
View larger version (156K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 9 64-year-old man with extensive T3 mucinous rectal adenocarcinoma. Axial transrectal sonographic image shows destruction of submucosa, echogenic edge (arrow) of which is evident on right side of image. Enlarged round perirectal node shows a hypoechoic tumor deposit.

 
Sonographic evaluation of rectal tumors entails identification of a rectal mass or focal mural thickening and determination of its size, extent, and layer of origin. Superficial tumors are often isoechoic with the adjacent wall layers and may produce only a small bump on the mucosal surface. Invasive rectal carcinoma, by comparison, appears progressively more hypoechoic with increasing invasion, so a T3 lesion exhibits clear disruption of the underlying submucosa and muscularis propria with spikes of black or hypoechoic tumor extending into the perirectal fat. The T category in the locoregional spread of rectal cancer indicates the presence of infiltration of the mucosal and submucosal layers (Tis-T1) (Figs. 7A and 7B), of the muscularis propria (T2), of the perivisceral fat tissue with obliteration of the interface between muscle and perirectal fat (T3) (Figs. 8 and 9), and of the contiguous organs (T4) (Figs. 10 and 11). This categorization is fundamental for the surgeon because some lesions are managed with local excision or endoscopic ablation (Tis-T1), and other lesions are managed with more extensive surgery, such as anterior resection, abdominoperineal resection or pelvic exenteration, and partial sacral resection.


Figure 17
View larger version (151K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 10 57-year-old man with invasive rectal cancer. Axial transrectal sonographic image shows large anterior T4 invasive malignant tumor of rectum with destruction of all wall layers and extension into perirectal fat. Hypoechoic tumor is in intimate contact with posterior wall of prostate, seemingly pushing it forward. Prostate involvement suspected on transrectal sonography was confirmed on MRI.

 

Figure 18
View larger version (163K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 11 56-year-old woman with invasive rectal cancer who had undergone undocumented incomplete transanal excision of polyp 10 years previously. Transvaginal axial sonographic image shows hypoechoic solid lobulated mass in anovaginal septum appearing almost independent of rectal wall that represents incompletely excised polyp with malignant change and regrowth over long interval.

 
The presence of adenopathy (N category) in the perirectal space can influence prognosis and management because it is widely accepted that positive lymph node results justify the choice of radiation therapy and preoperative chemotherapy in the management of T2 and early T3 lesions. Lymph node size is a difficult consideration because small nodes can have microscopic tumor foci, and large nodes can be reactive. Nonetheless, we report all lymph nodes visualized on sonography, including their maximal dimension, because small normal nodes are infrequently seen. The likelihood of malignancy increases for nodes larger than 5 mm in diameter.

Gray-scale visualization of actual tumor deposits within lymph nodes is uncommon, and Doppler criteria for tumor differentiation have not proved reliable for us. Transrectal sonography, CT, and MRI all have been used for different roles in staging of primary rectal tumors. Findings on color Doppler sonography are useful because most tumors are highly vascular. Identification of a hypervascular focus assists in determination of tumor margins (Figs. 12A and 12B) and in identification of small and superficial tumors to confirm that the region of interest does represent a neoplasm [16-18] (Figs. 1A, 1B, 13A and 13B). Furthermore, it is helpful that fecal material never has color signal.


Figure 19
View larger version (132K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 12A 58-year-old man with T2 rectal cancer. This case illustrates contribution of color Doppler imaging to tumor differentiation. Axial transrectal sonographic image shows hypoechoic tumor. Destruction of submucosa is evident with involvement of muscularis propria on right side of image.

 

Figure 20
View larger version (115K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 12B 58-year-old man with T2 rectal cancer. This case illustrates contribution of color Doppler imaging to tumor differentiation. Color Doppler transrectal sonographic image at default setting shows typical hypervascularity. Color demarcates tumor from normal rectal wall on left side of image. Technique is helpful for tumor staging.

 

Figure 21
View larger version (169K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 13A 55-year-old man with small rectal adenocarcinoma originating in adenomatous polyp of posterior rectal wall. This case illustrates contribution of color Doppler imaging to tumor differentiation. Axial transrectal sonographic image shows isoechoic polypoid mass with broad base surrounded by fluid within rectal lumen. Mass involves submucosal layer only.

 

Figure 22
View larger version (131K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 13B 55-year-old man with small rectal adenocarcinoma originating in adenomatous polyp of posterior rectal wall. This case illustrates contribution of color Doppler imaging to tumor differentiation. Color Doppler image shows profuse vascularity and vascular stalk of polypoid mass.

 
Histology of Rectal Tumors
More than 90% of rectal carcinomas are adenocarcinomas. By definition, on sonography all of these tumors appear as masses that involve the superficial mucosal layer of the intestinal wall. Rectal carcinoma has many risk factors and a known premalignant lesion, rectal adenoma. There is a relatively long time course for malignant transformation from adenoma to carcinoma, and outcome is markedly improved by early detection of adenoma and early cancer [19] (Figs. 7A, 7B and 13A, 13B). The risk of cancer increases from almost zero for polyps smaller than 5-6 mm to 40-50% for polyps larger than 2 cm [20]. In a meta-analysis, Worrell et al. [21] found that among 258 rectal adenomas with negative findings at biopsy, 50 (81%) of 62 found to be focal invasive cancer at surgical histopathologic examination had been correctly predicted at transrectal sonography. Conversely, the stage of 12% of benign adenomas was increased on the basis of findings at transrectal sonography.

Tubulovillous adenoma is a distinct premalignant benign tumor that has a high likelihood of malignant change. With malignant conversion, this tumor forms a subset of rectal adenocarcinoma but has a more favorable prognosis. At sonography, these soft and compliant tumors are often sizable and manifest as dominant intraluminal masses. They are T0 lesions with an intact underlying submucosa and muscularis propria (Figs. 14A and 14B). Differentiation of tubulovillous adenoma from a T1 lesion is often difficult with sonography. In the past, we and others [22, 23] noticed a tendency toward overstaging these tumors at endosonography. We believe this tendency was related to compression of the soft tumor into the rectal wall by the inflated balloon covering the examining transducer. With the use of high-resolution biplane transducers with no inflated balloon for real-time evaluation, however, transrectal sonography can show an intraluminal soft and compressible mass with no invasion. We also have found that color Doppler sonography consistently shows tubulovillous adenoma with a vascular stalk to the tumor and vessels with a characteristic stellate configuration (Fig. 14A, 14B), which differs from the more chaotic vascular pattern of many invasive rectal cancers.


Figure 23
View larger version (180K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 14A 58-year-old woman with tubulovillous adenoma. This case illustrates contribution of color Doppler imaging to tumor differentiation. Axial transvaginal sonographic image shows mixed echogenic mass that seems to fill lumen of rectum. There is no evidence of invasive cancer.

 

Figure 24
View larger version (131K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 14B 58-year-old woman with tubulovillous adenoma. This case illustrates contribution of color Doppler imaging to tumor differentiation. Color Doppler image shows characteristic stellate vascularity frequently encountered with this pathologic condition.

 

In addition to the common adenocarcinoma of the rectum, histologic types of malignancy include mucinous varieties with a tendency to intralesional calcification, mucinous deposits within metastatic nodes (Fig. 9), and local involvement of adjacent organs [24]; carcinoids, which are endocrine neoplasms with relatively low levels of malignancy [25] that usually manifest as small, mobile, submucosal nodules or focal areas of submucosal thickening [26] with an incidence of metastasis that correlates with tumor size [27]; and rare primary squamous cell carcinoma [28, 29], which seems to be frequently locally invasive and involve regional lymphatic vessels. Lymphoma [30], which is rare, can occur as a primary lesion of the large intestine [31] or as part of a generalized malignant process involving the gastrointestinal tract with infiltration of the perirectal soft tissues. Involvement of the deeper layers of the intestinal wall is characteristic of lymphoma (Figs. 15A and 15B). Anorectal melanoma [32] is an extremely rare variety of rectal tumor but constitutes the third most common site of origin of this tumor after the skin and eye (Figs. 16A and 16B).


Figure 25
View larger version (119K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 15A 64-year-old man with rectal lymphoma and known disseminated lymphoma with gastrointestinal involvement. Axial transrectal sonographic image of posterior rectal wall shows mucosa and submucosal layers are intact, excluding possibility of adenocarcinoma. Hypoechoic tumor is extensive and involves deep layers of rectal wall with diffuse extension into perirectal fat evident as many hypoechoic bands.

 

Figure 26
View larger version (154K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 15B 64-year-old man with rectal lymphoma and known disseminated lymphoma with gastrointestinal involvement. Axial CT image through rectum shows diffuse wall thickening and infiltration of perirectal fat. Layers of involvement are not defined.

 

Figure 27
View larger version (165K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 16A 47-year-old woman with melanoma of anal canal who presented with tumor prolapsing from anal canal. Axial transrectal sonographic image of rectum immediately above anorectal junctions shows very black tumor.

 

Figure 28
View larger version (125K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 16B 47-year-old woman with melanoma of anal canal who presented with tumor prolapsing from anal canal. Color Doppler image shows tumor is highly vascular.

 
Gastrointestinal stromal tumor (GIST) is the most common mesenchymal tumor that originates in the alimentary tract. The most common source is the stomach, followed by small bowel. In rare instances, the tumor originates in the anorectal region, esophagus, colon, or appendix [33-36]. GIST accounts for 0.1-3.0% of all gastrointestinal neoplasms [37]. The tissue of origin is commonly the muscularis propria of the bowel wall (Fig. 17), and the size can be tiny to huge [38]. Seventy to eighty percent of GISTs are benign, but there is a continuum from benign to malignant. On sonography, a GIST appears as a hypoechoic, well-circumscribed, round mass with areas of necrosis, hemorrhage, and cystic change. Large tumors frequently extend into the ischiorectal fossa or vagina with juxtaposition to the genital organs of women or the prostate. Transrectal sonography is accurate for defining the submucosal origin of rectal GIST with an intact mucosa, depicting the rectal wall layers, and can be used to differentiate extramural lesions, extrinsic compression, vascular lesions, and solid tumor.

The limitations of transrectal sonography include those of studying stenosing and high lesions (Figs. 18A and 18B) in the proximal rectum (greater than 15 cm from the anal verge) and rectosigmoid junction. We have found the addition of transvaginal sonography a valuable adjunct for defining the local extension of stenosing tumors in women and have made the technique a complementary examination to transrectal sonography [4, 36-39]. Placement of high-frequency sonographic probes in the vagina often enables high-resolution assessment of all of the pelvic viscera, including the rectum, anal canal [40-42], peritoneum of the pelvic pouch, and the rectovaginal septum, without interference from bowel gas and adipose tissue.


Figure 30
View larger version (158K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 18A 60-year-old man with stenotic high T3 rectal carcinoma. Endorectal probe could not pass through stenotic lumen. Biplane capability of probe allowed accurate measurement and staging of tumor in all planes. Long-axis transrectal sonographic image obtained with end-fired component shows large circumferential rectal tumor.

 

Figure 31
View larger version (177K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 18B 60-year-old man with stenotic high T3 rectal carcinoma. Endorectal probe could not pass through stenotic lumen. Biplane capability of probe allowed accurate measurement and staging of tumor in all planes. Axial transrectal sonographic image shows residual strictured lumen represented by small amount of echogenic air. Wall is circumferentially thickened and hypoechoicwith no residual normal wall layers. Invasion of perirectal fat is evident.

 
A further limitation of transrectal sonography, related to limited soft-tissue resolution, is lack of depiction of the mesorectal fascia, the fine linear envelope surrounding the mesorectum (a distinct anatomic unit that comprises the rectum, perirectal fat, and superior hemorrhoidal vessels, nerves, and lymphatic vessels). Furthermore, identification of normal-sized lymph nodes with microscopic tumor invasion and differentiation of lymph nodes with tumor from those with reactive change is a problem on sonographic images [42], as it is on CT scans and MR images. It may not be possible to identify lymph nodes outside the range of the sonographic transducer because of the limited field of view and limited penetration with high-frequency probes [43]. Moreover, when the tumor is extremely small or the rectum is collapsed and compressed by a rigid transducer, it may be difficult to detect and assess the tumor completely. For acquisition of an optimal sonic window for rectal sonography, an adequate sonographic medium must be used. A water-filled balloon can be attached to the tip of the transducer at endoscopic sonography, or the rectal lumen can be directly filled with water [44]. In the first technique, the pressure of the balloon on the rectal wall can make it difficult to identify individual layers, so the second technique is preferred. It is also helpful in the evaluation of stenosing malignant tumors. We have found a simple sodium phosphate enema with retention of some of the enema fluid provides good contrast between the tumor and the luminal fluid in almost all cases.

The accuracy of transrectal sonography for tumor staging ranges between 67% and 97% with a median accuracy of 89% [45-48]. Akasu et al. [46] found similar accuracy in a study of 164 consecutively detected cases of rectal cancer and reported on 12 cases in which examinations were incomplete because of the presence of annular constricting tumors. The most important staging error is overstaging of T2 lesions as T3 lesions owing to the presence of spontaneous (desmoplastic) or iatrogenic inflammation, which appears hypoechoic at sonographic examination and mimics invasion where there is none [10, 11]. Overstaging results in overtreatment, usually because the patient receives radiation therapy when it was not warranted. Tubulovillous adenoma can be easily classified T1 rather than T0. Understaging can be caused by failure to detect microscopic cancerous infiltration because of the limits of resolution of the equipment.

In our experience with transrectal sonography and newer probe designs, we have had continued success with staging. Our success rate with transrectal sonography has improved because large, bulky, and low tumors and annular stenotic tumors can usually be accurately staged despite inability to pass the probe beyond the stenotic segment (Figs. 18A and 18B). Furthermore, in a study in which the subjects were women with histologically confirmed rectal cancer, transvaginal sonographic findings were accurate in 25 (83%) of 30 cases and led to understaging in two and overstaging in three of 30 cases [4]. In the same study, a blinded assessment of 45 cases of cancers with both transvaginal and transrectal sonography showed good agreement between readers and comparable accuracy for staging in adequate examinations with each technique [4].

Lymph node classification (N) with transrectal sonography is less precise than is tumor classification (T). It is more difficult to differentiate tumor within a node than to identify the depth of wall invasion. The accuracy of N categorization with transrectal sonography ranges between 65% and 83% [47, 48]. In comparison with normal oval lymph nodes, which may have a linear echogenic hilar streak, malignant perirectal lymph nodes tend to be closer to round, to be more hypoechoic, and to have a mixed echo pattern and therefore at transrectal sonography can be easily visualized within the echogenic perirectal fat. Actual tumor deposits within the perirectal nodes infrequently may be visualized as necrosis or deposits of mucin (Figs. 8 and 9).


Figure 29
View larger version (188K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 17 59-year-old woman with asymptomatic gastrointestinal stromal tumor found at routine physical examination. Transrectal sonographic image shows solid, well-defined, round mass arising from muscularis propria. Tumor is growing with submucosal pattern, and mucosal surface bulges into fluid-filled lumen.

 
Metastatic involvement of the rectal wall in ovarian cancer is common, although metastasis can come from a variety of tumors, including those in the upper gastrointestinal tract and pancreas, which are likely to produce drop metastasis in the pelvis. On sonography, these tumors do not exhibit a mucosal component and appear instead as a mass or thickening of the deep layers of the rectal wall.

Postoperative transrectal sonography may show (accuracy, 80%) anastomotic recurrence as a hypoechoic, irregularly shaped area in the anastomotic region that infiltrates the perirectal fat of the rectal wall next to the anastomosis. The addition of color and spectral Doppler techniques improves detection of recurrent rectal cancer. Our experience suggests that recurrence, like a primary tumor, is almost always hypervascular on color Doppler images and is characterized by chaotic vessels. Higher-velocity blood flow in the hemorrhoidal vessels of patients with recurrence than in those without recurrence has been reported [49]. The endosonographic appearance of a normal anastomosis is characterized by mixed-echotexture symmetric interruption of the typical structure of the wall. In the case of stapled anastomosis, small, localized, bright echoes appear at the anastomosis without producing a shadow behind them [50].


Anal and Perianal neoplasms
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
Perianal and anal neoplasms are uncommon, accounting for approximately 1-5% of all colorectal carcinomas. The peak incidence is in the seventh decade of life with a marked predominance among women. Most (80-90%) of the tumors are of squamous cell origin [51]. These tumors usually appear as a hard nodular mass or ulcerating lesion and less frequently as an exophytic mass. Sonography reveals a hypoechoic central mass that can involve the sphincters and invade deeply (Figs. 19A, 19B and 19C). The profuse vascularity is similar to that of rectal cancer [52]. The tumors spread to the locoregional lymph nodes and rarely have distant metastasis [53]. The TNM staging differs from that of rectal cancer in that tumor size rather than depth of invasion differentiates the T category (Table 1). Treatment is conservative: chemotherapy and radiation therapy.


Figure 32
View larger version (178K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 19A 62-year-old woman with cancer of anal canal. (Reprinted from [4]) Sagittal sonographic image of anal canal obtained with transvaginal probe shows focal hypoechoic mass in outer third of anterior wall of anal canal.

 

Figure 33
View larger version (180K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 19B 62-year-old woman with cancer of anal canal. (Reprinted from [4]) Axial sonographic image shows hypoechoic tumor involving mucosa, submucosa,and internal sphincter.

 

Figure 34
View larger version (126K):
[in this window]
[in a new window]
[as a PowerPoint slide]
 
Fig. 19C 62-year-old woman with cancer of anal canal. (Reprinted from [4]) Color Doppler image corresponding to B shows hypervascularity of tumor.

 

View this table:
[in this window]
[in a new window]

 
TABLE 1: TNM Staging of Anal Cancer

 


Summary
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 
Endorectal and transanal sonography are fast, minimally invasive techniques performed with portable equipment that yield rapidly interpretable images. These techniques are considered the reference standard for preoperative staging of rectal and anal cancers and have relatively high accuracy for T and N categorization. The images depict rectal wall stratification and tumor extension within and through the rectal wall, especially for T1 and T2 lesions, for which sonography is more accurate than MRI and CT, and can be used for precise evaluation of sphincter infiltration. Other tumors, such as GIST, lymphoma, and metastatic lesions, have characteristic appearances that differ from those of adenocarcinoma. Advances in transducer technology also have improved the transrectal sonographic depiction of tubulovillous adenoma. Use of these techniques avoids the overstaging that previously occurred and depicts the typical hypervascularity of rectal cancer. Transvaginal scanning is an excellent adjunct to transrectal sonography in the care of women.


Acknowledgments
 
We thank Gordana Popovich for the schematics.


References
Top
Abstract
Introduction
Anatomy of the Rectum...
Sonographic Technique
Rectal Carcinoma
Anal and Perianal neoplasms
Summary
References
 

  1. Lee F, Gray JM, McLeary RD, et al. Transrectal ultrasound in the diagnosis of prostate cancer: location, echogenicity, histopathology and staging. Prostate 1985;7 : 117-129[Medline]
  2. Rifkin MD, Kurtz AB, Choi HY, Goldberg BB. Endoscopic ultrasonic evaluation of the prostate using a transrectal probe: prospective evaluation and acoustic characterization. Radiology1983; 149:265 -271[Abstract/Free Full Text]
  3. Godlewski G, Prudhomme M. Embryology and anatomy of the anorectum: basis of surgery. Surg Clin North Am2000; 80:319 -343[CrossRef][Medline]
  4. Dhamanaskar KP, Thurston W, Wilson SR. Transvaginal sonography as an adjunct to endorectal sonography in the staging of rectal cancer in women. AJR 2006; 187:90 -98[Abstract/Free Full Text]
  5. Hunerbein M. Endorectal ultrasound in rectal cancer. Colorectal Dis 2003;5 : 402-405[CrossRef][Medline]
  6. Beets-Tan RG. MRI in rectal cancer: the T stage and circumferential resection margin. Colorectal Dis 2003;5 : 392-395[CrossRef][Medline]
  7. Bartram C, Brown G. Endorectal ultrasound and magnetic resonance imaging in rectal cancer staging. Gastroenterol Clin North Am 2002; 31:827 -839[CrossRef][Medline]
  8. Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stiker J. Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging—a metaanalysis. Radiology 2004;232 : 773-783[Abstract/Free Full Text]
  9. Torricelli P, Lo Russo S, Pecchi A, Luppi G, Cesinaro AM, Romagnoli R. Endorectal coil MRI in local staging of rectal cancer. Radiol Med 2002; 103:74 -83
  10. Heriot AG, Grundy A, Kumar D. Preoperative staging of rectal carcinoma. Br J Surg 1999;86 : 17-28[CrossRef][Medline]
  11. Sahani DV, Kalva SP, Hahn PF. Imaging of rectal cancer. Semin Radiat Oncol 2003;13 : 389-402[CrossRef][Medline]
  12. Rao SX, Zeng MS, Xu JM, et al. Assessment of T staging and mesorectal fascia status using high-resolution MRI in rectal cancer with rectal distention. World J Gastroenterol2007; 13:4141 -4146[Medline]
  13. LeBlanc JK. Imaging and management of rectal cancer. Nat Clin Pract Gastroenterol Hepatol 2007;4 : 665-676[Medline]
  14. Bianchi P, Ceriani C, Palmisano A, et al. A prospective comparison of endorectal ultrasound and pelvic magnetic resonance in the preoperative staging of rectal cancer. Ann Ital Chir2006; 77:41 -46[Medline]
  15. Lahaye MJ, Engelen SM, Nelemans PJ, et al. Imaging for predicting the risk factors—the circumferential resection margin and nodal disease—of local recurrence in rectal cancer: a meta-analysis. Semin Ultrasound CT MR 2005;26 : 259-268[CrossRef][Medline]
  16. Heneghan JP, Salem RR, Lange RC, Taylor KJ, Hammers LW. Transrectal sonography in staging rectal carcinoma: the role of gray-scale, color-flow, and Doppler imaging analysis. AJR 1997;169 : 1247-1252[Abstract/Free Full Text]
  17. Sudakoff GS, Quiroz F, Foley WD. Sonography of anorectal, rectal, and perirectal abnormalities. AJR 2002;179 : 131-136[Free Full Text]
  18. Alexander AA, Liu JB, Palazzo JP, et al. Endorectal color and duplex imaging of the normal rectal wall and rectal masses. J Ultrasound Med 1994; 13:509 -513[Abstract]
  19. Scholefield JH. Screening for colorectal cancer. Br Med Bull 2002; 64:75 -80[Abstract/Free Full Text]
  20. Pijl ME, Chaoui AS, Wahl RL, van Oostayen JA. Radiology of colorectal cancer. Eur J Cancer 2002;38 : 887-898[CrossRef][Medline]
  21. Worrell S, Horvath K, Blakemore T, Flum D. Endorectal ultrasound detection of focal carcinoma within rectal adenomas. Am J Surg 2004; 187:625 -629[CrossRef][Medline]
  22. Renzulli P, Maurer CA, Netzer P, Buchler MW. Surgical management of large sessile villous and tubulovillous adenomas of the lower rectum. Dig Surg 2004; 21:287 -292[CrossRef][Medline]
  23. Loy TS, Kaplan PA. Villous adenocarcinoma of the colon and rectum: a clinicopathologic study of 36 cases. Am J Surg Pathol 2004; 28:1460 -1465[CrossRef][Medline]
  24. Kim MJ, Park JS, Park SI, et al. Accuracy in differentiation of mucinous and nonmucinous rectal carcinoma on MR imaging. J Comput Assist Tomogr 2003; 27:48 -55[CrossRef][Medline]
  25. Soga J. Early-stage carcinoids of the gastrointestinal tract. Cancer 2005; 103:1587 -1595[CrossRef][Medline]
  26. Maeda K, Maruta M, Utsumi T, Sato H, Masumori K, Matsumoto M. Minimally invasive surgery for carcinoid tumors in the rectum. Biomed Pharmacother 2002;56 : 222s-226s[CrossRef]
  27. Modlin IM, Kidd M, Latich I, Zikusoka MN, Shapiro MD. Current status of gastrointestinal carcinoids. Gastroenterology 2005;128 : 1717-1751[CrossRef][Medline]
  28. Gelas T, Peyrat P, Francois Y, et al. Primary squamous-cell carcinoma of the rectum. Dis Colon Rectum2002; 45:1535 -1540[CrossRef][Medline]
  29. Balfour TW. Does squamous carcinoma of the colon exist? Br J Surg 1972;59 : 410-412[CrossRef][Medline]
  30. Bilsel Y, Balik E, Yamaner S, Bugra D. Clinical and therapeutic considerations of rectal lymphoma: a case report and literature review. World J Gastroenterol 2005;11 : 460-461[Medline]
  31. Takenaka R, Tomoda J, Sakata T, et al. Mucosa-associated lymphoid tissue lymphoma of the rectum that regressed spontaneously. J Gastroenterol Hepatol 2000;15 : 331-335[CrossRef][Medline]
  32. Kim KW, Ha HK, Kim AY, et al. Primary malignant melanoma of the rectum: CT findings in eight patients. Radiology2004; 232:181 -186[Abstract/Free Full Text]
  33. Lau S, Tam KF, Kam CK, et al. Imaging of gastrointestinal stromal tumor (GIST). Clin Radiol 2004;59 : 487-498[CrossRef][Medline]
  34. Lau S, Lui CY, Yeung YP, Lam HS, Mak KL. Gastrointestinal stromal tumor of rectum: a report of 2 cases. J Comput Assist Tomogr 2004; 27:609 -615[Medline]
  35. Miettinen M, El-Rifai WE, Sobin LH, Lasota J. Evaluation of malignancy and prognosis of gastrointestinal stromal tumors: a review. Hum Pathol 2002;33 : 478-483[CrossRef][Medline]
  36. Nasu K, Ueda T, Kai S, et al. Gastrointestinal stromal tumor arising in the rectovaginal septum. Int J Gynecol Cancer 2004; 14:373 -377[CrossRef][Medline]
  37. Burkill GJ, Badran M, Al-Muderis O, et al. Malignant gastrointestinal stromal tumor: distribution, imaging features, and pattern of metastatic spread. Radiology 2003;226 : 527-532[Abstract/Free Full Text]
  38. Levy AD, Remotti HE, Thompson WM, Sobin LH, Miettinen M. Gastrointestinal stromal tumors: radiologic features with pathologic correlation. RadioGraphics 2003;23 : 283-304[Abstract/Free Full Text]
  39. Rieger N, Tjandra J, Solomon M. Endoanal and endorectal ultrasound: applications in colorectal surgery. ANZ J Surg2004; 74:671 -675[CrossRef][Medline]
  40. Damani N, Wilson SR. Nongynecologic applications of transvaginal US. RadioGraphics 1999;19 : S179-S200[Medline]
  41. Stewart LK, McGee J, Wilson SR. Transperineal and transvaginal sonography of perianal inflammatory disease. AJR2001; 177:627 -632[Abstract/Free Full Text]
  42. Stewart LK, Wilson SR. Transvaginal sonography of the anal sphincter: reliable, or not? AJR 1999;173 : 179-185[Abstract/Free Full Text]
  43. Beets-Tan RG, Beets GL, Vliegen RF, et al. Accuracy of magnetic resonance imaging in prediction of tumor-free resection margin in rectal cancer surgery. Lancet 2001;357 : 497-504[CrossRef][Medline]
  44. Kim S, Lim HK, Lee SJ, et al. Depiction and local staging of rectal tumors: comparison of transrectal US before and after water instillation. Radiology 2004;231 : 117-122[Abstract/Free Full Text]
  45. Maier A, Fuchsjager M. Preoperative staging of rectal cancer. Eur J Radiol 2003;47 : 89-97[CrossRef][Medline]
  46. Akasu T, Sugihara K, Yoshihiro M, et al. Limitations and pitfalls of transrectal ultrasonography for staging of rectal cancer. Dis Colon Rectum 1997;40 [suppl 10]:S10 -S15[CrossRef][Medline]
  47. Siddiqui AA, Fayiga Y, Huerta S. The role of endoscopic ultrasound in the evaluation of rectal cancer. Int Semin Surg Oncol 2006; 3:36[CrossRef][Medline]
  48. Muthusamy VR, Chang KJ. Optimal methods for staging rectal cancer. Clin Cancer Res 2007;13 : 6877s-6884s[Abstract/Free Full Text]
  49. Ghigi G, Garcea D, Canini R, et al. Transrectal ultrasonography in the study of recurrences in patients surgically treated for rectal neoplasms. Radiol Med (Torino) 1995;90 : 56-61[Medline]
  50. Lohnert MS, Doniec JM, Henne-Bruns D. Effectiveness of endoluminal sonography in the identification of occult local rectal cancer recurrences. Dis Colon Rectum 2003;43 : 483-491[CrossRef]
  51. Moore HG, Guillem JG. Anal neoplasms. Surg Clin North Am 2002; 82:1233 -1251[CrossRef][Medline]
  52. Drudi FM, Giovagnorio F, Raffetto N, et al. Trans rectal ultrasound color Doppler in the evaluation of recurrence of anal canal cancer. Eur J Radiol 2003;47 : 142-148[CrossRef][Medline]
  53. Scherrer A, Reboul F, Martin D, Dupuy JC, Menu Y. CT of malignant anal canal tumors. RadioGraphics 1990;10 : 433-453[Abstract]

Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Berton, F.
Right arrow Articles by Wilson, S. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Berton, F.
Right arrow Articles by Wilson, S. R.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?
Hotlight (NEW!)
Right arrow
What's Hotlight?


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS