Transrectal ultrasonography (TRUS) has been widely accepted as a popular imaging modality for evaluating the lower rectum, anal sphincters, and pelvic floor in patients with various anorectal diseases. It provides excellent visualization of the layers of the rectal wall and of the anatomy of the anal canal. TRUS is an accurate tool for the staging of primary rectal cancer, especially for early stages. Although magnetic resonance imaging is a modality complementary to TRUS with advantages for evaluating the mesorectum, external sphincter, and deep pelvic inflammation, three-dimensional ultrasonography improves the detection and characterization of perianal fistulas and therefore plays a crucial role in optimal treatment planning. The operator should be familiar with the anatomy of the rectum and pelvic structures relevant to the preoperative evaluation of rectal cancer and other anal canal diseases, and should have technical proficiency in the use of TRUS combined with an awareness of its limitations compared to magnetic resonance imaging.
Transrectal ultrasonography (TRUS) has been widely accepted as a popular imaging modality for evaluating the lower rectum, anal sphincter, and pelvic floor in patients with various anorectal diseases . Exact knowledge of the normal ultrasonographic (US) anatomy of the rectal wall and anal canal provides an important foundation for identifying abnormalities. Preoperative staging of rectal cancer is an important factor in determining optimal treatment and requires accurate diagnostic tools for clinical use. TRUS is a safe imaging modality for the evaluation of tumor invasion and lymph node metastasis in patients with rectal cancer. When performing the procedure, it is crucial to be aware of how signs of anorectal disease appear in ultrasonogram and the proper indications and limitations of the technique. Although TRUS has several limitations in the evaluation of rectal cancer and perianal fistulas, improved US transducers with three-dimensional (3D) equipment provide a better depiction of the anatomic relationship between the rectal wall and anal canal [2,3]. Radiologists should understand the advantages and disadvantages of TRUS compared with magnetic resonance imaging (MRI) for the accurate assessment of anorectal diseases. An overview is herein provided of the anatomy of the rectum and pelvic structures relevant to the preoperative evaluation of rectal cancer and diseases of the anal canal along with a review of the techniques, applications, and limitations of TRUS compared to MRI.
Technique and Preparation
TRUS is operator-dependent like other US examinations. For an accurate exam, the rectum should be cleansed thoroughly to avoid artifacts. Patients are given a routine cleansing enema two hours before the examination. It is very important that the rectum is clear and empty before the examination because image quality can be impaired by residual stool or air. Sedation is not necessary before the procedure, and the examination is usually performed with the patient placed in the left lateral decubitus position, in the kneechest position. A digital rectal examination should be performed to identify the lesion size, location, and the mobility of the tumor before the operator inserts the probe into the rectum. For optimal distension of the rectum, a water-filled balloon (usually 30-60 mL water instillation) should be inserted with an appropriate degree of contact with the rectal wall . When the probe is placed into the rectum, it is aligned in standard orientation, in which the anterior anatomical structures are at the uppermost or 12 o’clock side of the image, the patient’s left side is at 3 o’clock, the patient’s posterior side is at 6 o’clock, and the patient’s right side is at 9 o’clock. Then the probe is slowly withdrawn to the anal canal until the hyperechoic puborectalis muscle is seen. Images of the anal canal are taken at the upper, middle, and lower levels. Ideally, all five layers of the rectum should be clearly visible (Fig. 1).
In order to obtain high-quality images of the anal canal and the rectal wall layers, the equipment used must meet certain specifications. The transrectal probe mechanically rotates 360° with a variable ultrasound frequency of 5-15 MHz, depending on the lesions under investigation [5-7]. Higher frequencies provide better resolution with clear definition of the rectal wall layers, whereas lower frequencies are essential for the assessment of enlarged lymph nodes and perirectal tissue. In the 3D acquisition system, the probe automatically moves inward and outward over a distance of 6 cm . Stored data can be reviewed at any time, and it is possible to select any axis for visualization, allowing the operator to obtain the most information from the data (Fig. 2). The 3D image acquisition is automated and the moving parts inside the probe do not touch the patient.
To evaluate an entire lesion, the probe should be inserted above the lesion of interest as carefully as possible and then withdrawn with the probe kept at the center of the rectal lumen. All critical points of the tumor should be recorded, along with surrounding lesions from the anal verge to the upper rectum. Careful examination of the entire rectum below and above the lesion is also an essential component of the procedure. The operator should pay particular attention to the perirectal area in order to identify enlarged lymph nodes. Using a water balloon as a sonic window has the potential disadvantage of not clearly delineating the mesorectum, perirectal lymph nodes, and the rectal wall. The use of 3D data reconstruction can compensate for this potential disadvantage.
Normal US Anatomy of the Rectum and Anal Canal
The rectal wall is composed of five layers that can be clearly visualized by TRUS. The innermost hyperechoic line shows the interface of the balloon and the mucosal surface of the rectal wall. The inner hypoechoic layer represents the mucosa and muscularis mucosa, followed by a slightly thicker hyperechoic submucosal layer. The outer hypoechoic layer represents the muscularis propria, and the outermost hyperechoic layer corresponds to the perirectal fatty tissue (Fig. 3) [1,2]. When staging rectal cancer with TRUS, the operator must make every effort to image all five layers clearly at all points of the tumor because tumor infiltration can differ significantly along the body of the tumor. The thickness and continuity of the rectal wall layers should be carefully evaluated; for advanced cancer located in the anterior rectal wall, it is essential to determine the degree of invasion of adjacent organs. The operator must also focus on the mesorectum and surrounding tissues to evaluate possible lymph node involvement.
The anal canal is usually divided into three levels during the examination (Fig. 4). The puborectalis muscle is easily seen and appears as a U-shaped echogenic band (sometimes described as a horseshoe sling) in the upper anal canal. When retracting the probe, this hyperechoic band closes anteriorly and forms the external anal sphincter. The internal anal sphincter displays a band of maximum thickness anteriorly in the middle anal canal, in combination with the external anal sphincter ring . The external anal sphincter is usually hyperechoic, broad, and lies immediately outside the internal anal sphincter. In the lower anal canal, the internal anal sphincter terminates and the subcutaneous external anal sphincter is present . The internal anal sphincter increases in thickness and echogenicity with age . 3D TRUS also provides anatomic details of perianal spaces that are located in the intersphincteric space between the internal and external anal sphincters: the pyramid-shaped ischioanal space surrounds the anal canal, and the supralevator space is located superior to the levator ani muscle (Fig. 5).
Staging of Rectal Cancer
Preoperative rectal tumor staging includes factors such as the depth of tumor invasion, lymph node involvement, and metastasis (TNM staging), as well as extramural venous invasion and the presence of circumferential resection margin involvement . For the local tumor staging of rectal cancer, TRUS and MRI each have distinct advantages and disadvantages (Table 1).
Tumor Depth (T Staging)
Tumor depth is an important factor for planning the treatment of both early and locally advanced cancer abutting the mesorectum. Rectal cancer appears on TRUS as a hypoechoic lesion interrupting the normal rectal layers. A T1 cancer is confined to the submucosa (Fig. 6). Thickening of the muscularis propria and/or the extension of the hyperechoic tumor into the muscularis propria indicate T2 cancer (Fig. 7). Most early cancer can be treated with surgery alone, such as transanal endoscopic excision or total mesorectal excision . If the tumor disrupts the muscularis propria and breaches the hyperechoic perirectal fat, it is a T3 tumor (Fig. 8), while T4 cancer involves adjacent organs or the pelvic side wall. TRUS is capable of identifying involvement of the vagina, uterus, urinary bladder, prostate gland, and seminal vesicles.
TRUS has 69%-94% accuracy for the T staging of rectal cancer . A meta-analysis showed that TRUS provided more accurate data than computed tomography or MRI in the evaluation of local tumor invasion in rectal cancer patients . Another meta-analysis including 5,039 patients from 42 different studies between 1980 and 2008 reported that the sensitivity and specificity of TRUS for the T staging of rectal cancers were as follows: T1, 87.8% and 98.3%; T2, 80.5% and 95.6%; T3, 96.4% and 90.6%; and T4, 95.4% and 98.3%, respectively . TRUS may be accurate in distinguishing early lesions from more advanced stage lesions with a sensitivity and specificity of 96% and 85%, respectively . For superficial rectal cancers, the accuracy of T staging has been shown to range from 69% to 97% . The recently updated 3D US system, which enables volumetric evaluation with better anatomic planes for adjacent structures, further enhanced the diagnostic capabilities of TRUS, resulting in reported T staging sensitivities of 92.8% for T1, 93.1% for T2, 91.6% for T3, and 100% for T4 .
The accuracy rate of TRUS varies according to different tumor stages. TRUS identifies the depth of tumor invasion less accurately for T2 rectal cancer lesions than for early T1 lesions or advanced T3 and T4 lesions, due to a tendency toward overstaging . A prospective multicenter study demonstrated that the accuracy of TRUS for all T stages was 65.8%, which was lower than previous data had indicated; the moderate experience of the investigators was proposed to be the major reason for this discrepancy . Variable interobserver agreement has also been noted, with experienced operators reporting higher accuracy. In this study, a sensitivity of 74.9% was observed in the detection of T3 tumors, which was the highest reported sensitivity . Staging tumors with stenosis can be difficult if the scope cannot pass through the narrow segment. In such cases, a flexible probe can be used .
TRUS is more accurate than computed tomography or MRI in evaluating the depth of tumor invasion, especially in the early stages of T1 and T2 tumors, because of its ability to clearly depict the layers of the rectal wall [2,18]. The overall T staging accuracy of TRUS has been reported as 80%-95%, compared to 75%-85% for MRI [1,15,18,19]. MRI has been shown to be the most accurate imaging modality for local rectal cancer staging, particularly in advanced T3 and T4 tumors [4,20]. Although it has difficulties distinguishing between T1 and T2 tumors, MRI is more accurate in staging T4 tumors involving adjacent organs [4,21-23]. Compared to MRI, TRUS has the advantages of being less costly and readily used in the office, and offering real-time imaging .
Nodal Metastasis (N Staging)
Assessing the nodal stage is also essential in treatment planning, given the necessity of evaluating possible neoadjuvant treatment and determining the extent of nodal excision . Abnormal lymph nodes are defined by size and echotexture; however, several challenges exist in the accurate US detection of lymph node involvement. Lymph nodes that are larger than 3 mm, uniformly hypoechoic, and round are considered to be metastatic lymph nodes. These criteria are neither sensitive nor specific, because reactive lymph nodes can be enlarged and small nodes may have microscopic malignant foci . A meta-analysis of 35 studies from 1966 to 2008 demonstrated that the overall sensitivity and sensitivity of TRUS in the diagnosis of lymph node involvement were 73.2% and 75.8%, respectively . TRUS showed a moderate diagnostic capability, but improved diagnostic criteria are needed. Those using MRI encounter similar difficulties when it is used to evaluate whether lymph nodes are malignant. Using only the size criterion may lead to considerable overstaging and thus overtreatment, as reactive lymph nodes may be mistakenly diagnosed as malignant . The addition of other imaging features allowing the visualization of the nodal border, contour, and heterogeneous signal intensities increased the sensitivity and specificity to 85% and 97%, respectively . A meta-analysis including 21 studies showed that the sensitivity and specificity of MRI in detecting lymph node involvement were 77% and 71%, respectively . This result indicates that the current capability of MRI to detect metastatic lymph nodes accurately is limited [12,28].
TRUS detects lymph node metastasis more accurately than MRI due to its higher anatomical resolution . It can easily define nodes as small as 3 mm in diameter. However, an inherent limitation of TRUS is its limited field of view, which makes it impossible to evaluate lymph nodes outside of the US range . In contrast, MRI can visualize the iliac and retroperitoneal lymph nodes . Recently updated 3D TRUS with multi-planar display and better resolution has improved N-staging accuracy rates compared to conventional two-dimensional (2D) US ; however, even with current TRUS and MRI techniques, evaluating lymph nodes for malignancy has remained a challenge .
Mesorectal Fascia (Circumferential Resection Margin Involvement)
Involvement of the circumferential resection margin is one of the most important predictors of local recurrence in rectal cancer patients who are treated with total mesorectal excision [4,31]. TRUS can identify the circumferential resection margin at the level of the seminal vesicle, prostate, and vagina; however, it cannot accurately depict the mesorectal fascia, especially in the posterior aspect . A recent meta-analysis has found that MRI has a sensitivity of 77% and specificity of 94% in predicting circumferential resection margin involvement . One study has reported a strong correlation between TRUS and MRI in predicting circumferential resection margin involvement in 52 rectal cancer patients ; however, MRI remains preferable to TRUS for evaluating the relationship of a tumor to the mesorectal fascia.
Assessment of Anal Canal Disease
Perianal fistulas are caused by various inflammatory diseases including Crohn disease, pelvic infection, diverticulitis, and tuberculosis, as well as by pelvic malignancy, trauma, or radiation therapy . Fistulas are believed to form most commonly secondary to impaired drainage of the anal glands, which is known as the cryptoglandular hypothesis (Fig. 9) . Perianal fistulas have been divided into inter-, trans-, extra-, and suprasphincteric types by Parks et al. . The treatment of perianal fistulas is primarily surgical and includes a fistulotomy or fistulectomy of the tracts combined with abscess drainage . The major role of imaging modalities in evaluating perianal fistulas is identifying the anatomic relationship of the fistula and demonstrating the extent of inflammation, internal opening, and fluid collection . To reduce the rate of disease recurrence and postoperative fecal incontinence, it is important to evaluate the anatomic details of the fistulas and the presence of anal sphincter defects before therapy .
Perianal fistulas appear as hypoechoic tracts or focal soft tissue lesions within anal wall structures (Video clips 1, 2). Abscesses may contain internal gas or hyperechoic debris, and fistulas show a narrow and irregular path on TRUS (Figs. 10, 11, Video clip 3). Depending on the internal composition or stage of inflammation, the primary fistula tract appears as variable echogenic fluid with a thickened wall (Fig. 12). Compared to an active anal fistula containing fluid-like material, inactive fistulas are tubular fibrotic bands without fluid content. The fistula tract extends through the perianal spaces while crossing the subepithelium, internal, or external sphincter . TRUS provides excellent imaging of the rectal wall layers and anal sphincter, and therefore is excellent at visualizing intersphincteric fistulas and their relationship to the anal canal [1,33]. TRUS with a high frequency transducer (81%) has been shown to be more accurate than digital examination (61%) in 108 primary fistula tracts . A meta-analysis reported the sensitivity and specificity of TRUS in the detection of fistulas as 0.87 (95% confidence interval, 0.70 to 0.95) and 0.43 (95% confidence interval, 0.21 to 0.69) . High-resolution 3D US is potentially a useful tool for accurately assessing fistula tracts. The operator can trace the tract by reconstructing all necessary planes from the US images. 3D imaging has improved the accuracy to 98.5% for primary tracts and 96.4% for secondary tracts, compared to accuracies of 83.3% and 87.9%, respectively, for 2D imaging .
MRI is considered to be an accurate modality for depicting primary tracts, showing 87% sensitivity and 69% specificity in a recent meta-analysis . Several comparison studies of TRUS and MRI have shown conflicting results. Both hydrogen peroxideenhanced 3D TRUS and endoanal MRI showed good agreement in the evaluation of perianal fistulas, particularly in the identification of primary fistulas and the location of the internal opening; both modalities agreed well with surgical findings [41,42]. Regarding the identification of intersphincteric fistulas, a meta-analysis reported that MRI and TRUS showed sensitivities of 88%-95% and 50%-79% and specificities of 92%-100% and 84%-100%, respectively . This study suggests that MRI and TRUS have similar sensitivities, but that MRI has a better specificity for the identification of fistulas. The advantage of TRUS is that it provides accurate visualization when the tract is close to the probe, but structures further from the probe are visualized less clearly. An inconvenient aspect of TRUS is its limited field of view and inability to accurately delineate anatomic spaces outside the external anal sphincter . MRI offers a wider field of view and is better for assessing complex tracts, lateral extension into the perianal space, and fistulas crossing the levator ani muscle .
The most common malignancy of the anal canal is squamous cell carcinoma. These tumors are technically easier to image than rectal cancer due to their location in the anal canal and the fact that they do not necessarily needs rectal distention. TRUS can accurately detect the depth of anal cancer into the sphincters with a focus on tumor penetration , which is important because the depth of penetration is more closely associated with the prognosis of patients receiving chemoradiation therapy than the size of the lesion. Anal cancer appears as a hypoechoic mass infiltrating the anal sphincter (Fig. 13). TRUS and MRI appear to be comparable modalities for the staging of anal cancer . TRUS may be superior for the detection of superficial small anal cancers and is therefore recommended for T staging. However, for lymph node staging, TRUS should be supplemented by MRI because US has a limited field of view [2,44].
Sphincter injury is the most common cause of fecal incontinence, and frequently occurs as the consequence of birth trauma, anorectal surgery, or other accidental injuries. Birth trauma results in tears in the anal sphincter, especially the external sphincter, and laceration of the sphincter. TRUS provides accurate images of the anal sphincter and surrounding tissues and can show breaks in the hypoechoic internal anal sphincter or interruption of the external anal sphincter. Discontinuity of the external anal sphincter indicates the presence of a tear (Fig. 14). It has been reported that the accuracy of TRUS in diagnosing sphincter disruption approaches 95% .
TRUS provides excellent visualization of the layers of the rectal wall. It is an accurate and useful tool for staging primary rectal cancer and determining rectal wall integrity. It is a fast and minimally invasive technique performed with portable equipment. TRUS can also accurately assess the anal sphincter and provide critical information helpful for planning the appropriate treatment of perianal fistulas and fecal incontinence. TRUS is better than MRI for the evaluation of superficial tumors, whereas MRI provides a better visualization of locally advanced or stenosing cancers. TRUS is comparable to MRI in the staging of perirectal lymph nodes. Although TRUS is limited in the evaluation of the circumferential resection margin due to its small field of view, 3D TRUS can improve the accuracy of diagnoses of anorectal diseases and therefore should have an expanded role in the management of patients with anorectal diseases.
2. Saranovic D, Barisic G, Krivokapic Z, Masulovic D, Djuric-Stefanovic A. Endoanal ultrasound evaluation of anorectal diseases and disorders: technique, indications, results and limitations. Eur J Radiol 2007;61:480–489.
3. Saftoiu A, Gheonea DI. Tridimensional (3D) endoscopic ultrasound: a pictorial review. J Gastrointestin Liver Dis 2009;18:501–505.
4. Samdani T, Garcia-Aguilar J. Imaging in rectal cancer: magnetic resonance imaging versus endorectal ultrasonography. Surg Oncol Clin N Am 2014;23:59–77.
5. Cartana ET, Parvu D, Saftoiu A. Endoscopic ultrasound: current role and future perspectives in managing rectal cancer patients. J Gastrointestin Liver Dis 2011;20:407–413.
6. Bhutani MS. Recent developments in the role of endoscopic ultrasonography in diseases of the colon and rectum. Curr Opin Gastroenterol 2007;23:67–73.
7. Rovera F, Dionigi G, Boni L, Cutaia S, Diurni M, Dionigi R. The role of EUS and MRI in rectal cancer staging. Surg Oncol 2007;16 Suppl 1:S51–S52.
8. Felt-Bersma RJ. Endoanal ultrasound in perianal fistulas and abscesses. Dig Liver Dis 2006;38:537–543.
9. Chand M, Brown G. Pre-operative staging of rectal cancer: MRI or ultrasound? Semin Colon Rectal Surg 2013;24:114–118.
10. Van Cutsem E, Dicato M, Haustermans K, Arber N, Bosset JF, Cunningham D, et al. The diagnosis and management of rectal cancer: expert discussion and recommendations derived from the 9th World Congress on Gastrointestinal Cancer, Barcelona, 2007. Ann Oncol 2008;19 Suppl 6:vi1–vi8.
11. Krajewski KM, Kane RA. Ultrasound staging of rectal cancer. Semin Ultrasound CT MR 2008;29:427–432.
12. Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker 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.
13. Puli SR, Bechtold ML, Reddy JB, Choudhary A, Antillon MR, Brugge WR. How good is endoscopic ultrasound in differentiating various T stages of rectal cancer? Meta-analysis and systematic review. Ann Surg Oncol 2009;16:254–265.
14. Zorcolo L, Fantola G, Cabras F, Marongiu L, D'Alia G, Casula G. Preoperative staging of patients with rectal tumors suitable for transanal endoscopic microsurgery (TEM): comparison of endorectal ultrasound and histopathologic findings. Surg Endosc 2009;23:1384–1389.
15. Kav T, Bayraktar Y. How useful is rectal endosonography in the staging of rectal cancer? World J Gastroenterol 2010;16:691–697.
16. Kolev NY, Tonev AY, Ignatov VL, Zlatarov AK, Bojkov VM, Kirilova TD, et al. The role of 3-d endorectal ultrasound in rectal cancer: our experience. Int Surg 2014;99:106–111.
17. Ptok H, Marusch F, Meyer F, Wendling P, Wenisch HJ, Sendt W, et al. Feasibility and accuracy of TRUS in the pre-treatment staging for rectal carcinoma in general practice. Eur J Surg Oncol 2006;32:420–425.
18. Wang Y, Zhou CW, Hao YZ, Li L, Liu SM, Feng XL, et al. Improvement in T-staging of rectal carcinoma: using a novel endorectal ultrasonography technique with sterile coupling gel filling the rectum. Ultrasound Med Biol 2012;38:574–579.
19. Liu ZL, Zhou T, Liang XB, Ma JJ, Zhang GJ. Learning curve of endorectal ultrasonography in preoperative staging of rectal carcinoma. Mol Clin Oncol 2014;2:1085–1090.
20. MERCURY Study Group. Diagnostic accuracy of preoperative magnetic resonance imaging in predicting curative resection of rectal cancer: prospective observational study. BMJ 2006;333:779.
21. Battersby NJ, Moran B, Yu S, Tekkis P, Brown G. MR imaging for rectal cancer: the role in staging the primary and response to neoadjuvant therapy. Expert Rev Gastroenterol Hepatol 2014;8:703–719.
22. Huang Z, Chu L, Zhao R, Wang H. Meta-analysis of diagnostic accuracy of magnetic resonance in restaging of rectal cancer after preoperative chemoradiotherapy. Zhonghua Wei Chang Wai Ke Za Zhi 2014;17:258–263.
23. Intven M, Reerink O, Philippens ME. Dynamic contrast enhanced MR imaging for rectal cancer response assessment after neoadjuvant chemoradiation. J Magn Reson Imaging 2014 Aug 14 [Epub]. http://dx.doi.org/10.1002/jmri.24718.
24. Beets GL, Beets-Tan RG. Pretherapy imaging of rectal cancers: ERUS or MRI? Surg Oncol Clin N Am 2010;19:733–741.
25. Puli SR, Reddy JB, Bechtold ML, Choudhary A, Antillon MR, Brugge WR. Accuracy of endoscopic ultrasound to diagnose nodal invasion by rectal cancers: a meta-analysis and systematic review. Ann Surg Oncol 2009;16:1255–1265.
26. Brown G, Richards CJ, Bourne MW, Newcombe RG, Radcliffe AG, Dallimore NS, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology 2003;227:371–377.
27. Al-Sukhni E, Milot L, Fruitman M, Beyene J, Victor JC, Schmocker S, et al. Diagnostic accuracy of MRI for assessment of T category, lymph node metastases, and circumferential resection margin involvement in patients with rectal cancer: a systematic review and meta-analysis. Ann Surg Oncol 2012;19:2212–2223.
28. Lahaye MJ, Engelen SM, Nelemans PJ, Beets GL, van de Velde CJ, van Engelshoven JM, 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.
29. Heo SH, Kim JW, Shin SS, Jeong YY, Kang HK. Multimodal imaging evaluation in staging of rectal cancer. World J Gastroenterol 2014;20:4244–4255.
30. Kim JC, Kim HC, Yu CS, Han KR, Kim JR, Lee KH, et al. Efficacy of 3-dimensional endorectal ultrasonography compared with conventional ultrasonography and computed tomography in preoperative rectal cancer staging. Am J Surg 2006;192:89–97.
31. Brown G, Richards CJ, Newcombe RG, Dallimore NS, Radcliffe AG, Carey DP, et al. Rectal carcinoma: thin-section MR imaging for staging in 28 patients. Radiology 1999;211:215–222.
32. Phang PT, Gollub MJ, Loh BD, Nash GM, Temple LK, Paty PB, et al. Accuracy of endorectal ultrasound for measurement of the closest predicted radial mesorectal margin for rectal cancer. Dis Colon Rectum 2012;55:59–64.
33. de Miguel Criado J, del Salto LG, Rivas PF, del Hoyo LF, Velasco LG, de las Vacas MI, et al. MR imaging evaluation of perianal fistulas: spectrum of imaging features. Radiographics 2012;32:175–194.
34. Sainio P. Fistula-in-ano in a defined population. Incidence and epidemiological aspects. Ann Chir Gynaecol 1984;73:219–224.
36. O'Malley RB, Al-Hawary MM, Kaza RK, Wasnik AP, Liu PS, Hussain HK. Rectal imaging: part 2, Perianal fistula evaluation on pelvic MRI: what the radiologist needs to know. AJR Am J Roentgenol 2012;199:W43–W53.
37. Santoro GA, Fortling B. The advantages of volume rendering in three-dimensional endosonography of the anorectum. Dis Colon Rectum 2007;50:359–368.
38. Buchanan GN, Halligan S, Bartram CI, Williams AB, Tarroni D, Cohen CR. Clinical examination, endosonography, and MR imaging in preoperative assessment of fistula in ano: comparison with outcome-based reference standard. Radiology 2004;233:674–681.
39. Siddiqui MR, Ashrafian H, Tozer P, Daulatzai N, Burling D, Hart A, et al. A diagnostic accuracy meta-analysis of endoanal ultrasound and MRI for perianal fistula assessment. Dis Colon Rectum 2012;55:576–585.
40. Ratto C, Grillo E, Parello A, Costamagna G, Doglietto GB. Endoanal ultrasound-guided surgery for anal fistula. Endoscopy 2005;37:722–728.
41. West RL, Zimmerman DD, Dwarkasing S, Hussain SM, Hop WC, Schouten WR, et al. Prospective comparison of hydrogen peroxideenhanced three-dimensional endoanal ultrasonography and endoanal magnetic resonance imaging of perianal fistulas. Dis Colon Rectum 2003;46:1407–1415.
42. West RL, Dwarkasing S, Felt-Bersma RJ, Schouten WR, Hop WC, Hussain SM, et al. Hydrogen peroxide-enhanced three-dimensional endoanal ultrasonography and endoanal magnetic resonance imaging in evaluating perianal fistulas: agreement and patient preference. Eur J Gastroenterol Hepatol 2004;16:1319–1324.
43. Hunerbein M, Pegios W, Rau B, Vogl TJ, Felix R, Schlag PM. Prospective comparison of endorectal ultrasound, threedimensional endorectal ultrasound, and endorectal MRI in the preoperative evaluation of rectal tumors: preliminary results. Surg Endosc 2000;14:1005–1009.
44. Otto SD, Lee L, Buhr HJ, Frericks B, Hocht S, Kroesen AJ. Staging anal cancer: prospective comparison of transanal endoscopic ultrasound and magnetic resonance imaging. J Gastrointest Surg 2009;13:1292–1298.