Computed tomography colonography in preoperative evaluation of colorectal cancer

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1 POLSKI PRZEGLĄD CHIRURGICZNY 2010, 82, 8, /v O R I G I N A L P A P E R S Computed tomography colonography in preoperative evaluation of colorectal cancer Małgorzata Rudzińska 1, Janusz Rudziński 2, Robert Szyca 3,4, Krzysztof Leksowski 3,4 Department of Radiology 1 Kierownik: ppłk lek. med. C. Wałęsa (Department of Gastroenterology 2 Kierownik: dr n. med. J. Rudziński Department of General Surgery 3 Kierownik: dr hab. K. Leksowski, prof. UMK 10 th Military Clinical Hospital in Bydgoszcz Chair of Public Health, Collegium Medicum of Nicolas Copernicus University 4 Kierownik: dr hab. K. Leksowski, prof. UMK Computed tomographic colonography (CTC) has the potential to become an accepted technique for detecting of colorectal cancer. The aim of the study was to evaluate usefulness of CTC in preoperative evaluation of colorectal tumors and the regions of colon endoscopically unavailable. Material and methods. A total of 49 patients with colorectal tumors identified at conventional colonoscopy were included. In all these patients CTC was performed and results were compared with colonoscopy. In addition in CTC infiltration of surrounding tissues, organs, lymph nodes and liver were assessed. Findings were compared with contrast-enhanced CT of abdomen. Results. Colonoscopy was completed to the caecum in 24 (48.9%) patients. CTC failed only in one patient. CTC was congruent with colonoscopy in evaluation of tumor location and morphological type. In CTC two additional tumors were found proximately to occlusive masses, it is in endoscopically unavailable regions. Sensitivity and specificity of CTC comparing to CT in diagnosis of fat tissue infiltration and surrounding organs infiltration at the site of tumor were 95.5% / 50% and 100% / 86.9% respectively. Concordance of results in evaluation of lymph nodes was 93.9% while sensitivity and specificity for CTC was 84.6% and 100% respectively. Concordance of evaluation of liver metastases was 78.8%, while sensitivity and specificity for CTC was 61.5% and 90% respectively. Conclusions. CTC is a useful method in diagnostics of colorectal tumors. It allows to diagnose tumor, determine local tumor staging and detect synchronous lesions in endoscopically unavailable regions. Key words: colonoscopy, computed tomography, tumor of colon, diagnostics Conventional colonoscopy is still considered the gold standard for the detection of colorectal neoplasm as highly sensitive and specific diagnostic method. However it fails to show the entire colon in % examinations because of technical reasons as well as patient s intolerance (1). From among newest radiologic modalities promising methods are CT colonography (CTC), MR colonography and PET colonography. Effectiveness of these techniques in the detection and evaluation of large bowel tumours, as well as in clinical staging, are currently undergoing vigorous research (2, 3, 4). The purpose of this study was to assess the usefulness of CTC in preoperative evaluation

2 450 M. Rudzińska et al. of colorectal tumors and the entire bowel including regions endoscopically unavailable. Material and methods This prospective study recruited 49 consecutive patients (31 men, 18 women, ages 24 to 88 years; median age: 70 years) with colorectal tumors identified at conventional colonoscopy. All these patients were referred for CTC and contrast-enhanced CT of abdomen additionally in 33 (67.3%) patients was performed. CTC was performed with 64-slice row CT (Siemens Sensation Cardiac 64, Siemens, Germany). Acquired CT data were transferred to a workstation Leonardo equipped with software (Software Version syngo CT 2006A, Siemens) adjusted to CTC evaluation. For interpretation of the results of examination threedimensional volume rendering technique (VRT) reconstructions, three-dimensional endoluminal fly-through views and two-dimensional multiplanar reformatted images (MPR) were used. Both supine and prone image data sets were evaluated. CTDI vol amounted 3.9 mgy in supine and 2.3 mgy in prone and effective dose for average man or woman amounted adequately: 2.40 msv or 3.71 msv in supine and 1.44 msv or 2.23 msv in prone. All CTC images were interpreted by the same radiologist. Except colorectal findings regional lymph nodes, liver as well others organs were assessed and correlated with contrast-enhanced CT of abdomen. The adequacy of bowel cleasing was evaluated both in colonoscopy and CT colonography using 5-point scale, where 1 meant inadequate and 5 optimal bowel preparation. 4 and 5 point were considered as well bowel cleansing. Each patient subjectively assessed tolerancy of colonoscopy and CT colonography in 5-point scale, where 1 meant total intolerance and 5 very good tolerancy. In statistical analysis following tests were used: two fraction test, F Snedecor s test, z-test, t-student s test and Cochran-Cox s test. p values < 0.05 were considered significant. Results Results of comparison between colonoscopy and CTC are presented in tab. 1. In 24 (48.9%) patients colonoscopy was complete while in 25 (51.1%) patients examina- tion of entire colon was impossible because of obstructive or occlusive masses. In CTC visualization of the entire colon was obtained in 44 (89.8%) patients. Incomplete examination because of inadequate bowel distention was in 5 (10.2%) patients in CTC and was caused by difficulties in air holding or occlusive tumor. In one patient CTC failed because of completely collapsed colon and no possibility of it s evaluation. Therefore 48 patients were included to analysis in this group. In supine the worst cleansed bowel segments were: rectum and sigmoid colon / rectal junction. However the same segments were well-visualized in prone because residual fluid and feces moved to sigmoid and descending colon. Whilst in prone the worst cleansed and distended was transverse colon, well-visualized in supine. Evaluation of tumor size and volume in occlusive tumors during colonoscopy were impossible. CTC was congruent with colonoscopy in evaluation of morphological type of tumor. In colonoscopy untypical colon topography concerned dolichosigmoid. Whilst in CTC elongation of transverse colon, descending colon or dolichocolon were stated. Besides segmental sharp bending of descending colon, shortening of ascending colon, loop of ascending colon and high position of coecum. In CTC two additional tumors were found proximately to occlusive masses, it is in endoscopically unavailable regions. In one patient with occlusive tumor in transverse colon, the second large lesion (size: 7x6.5x6 cm) was found in caecum and confirmed in contrast-enhanced CT of abdomen. Congruence of CTC and contract enhanced CT in evaluation of infiltration of fat tissue was 78.8%. Among disagreements false positive results in CTC were stated in 5 (15.2%) of patients. In one patient (3%) result was false negative. While congruence both examinations in evaluation of surrounding organs infiltration was 87.9% and divergence of results concerned also overinterpretation of CTC results. Sensitivity of CTC in comparison with CT in diagnosis of infiltration of fat tissue and surrounding organs was 95.5% and 100% and specificity 50% and 86.9% respectively. In evaluation of lymph nodes criterion of > than 1 cm was assumed. Congruence in evaluation of enlarged lymph nodes was 93.9%. In 2 (6.1%) patients lymph nodes were not showed in CTC whilst were visible in CT. Sensitivity in

3 Computed tomography colonography in preoperative evaluation of colorectal cancer 451 Table 1. Results of comparison between colonoscopy and CT colonography Colonoscopy CT colonography p Time of examination (SD) 3-25 min (15) min (61) < 0,05 Bowel cleansing (mean) 3,70-5 (4,66) 2,80-5 (4,29) =0,001 Occlusive tumour 25/49 (51%) 3/49 (6,1%) <0,0001 Tumour size evaluation (1-2 diameters) 29/49 (59,2%) 48/48 (100%) <0,0001 Tumour volume (3 diameters) 15/49 (30,6%) 48/48 (100%) <0,0001 Wall thickening evaluation 0/49 (0%) 48/48 (100%) <0,0001 Tolerance of examination (mean) 2-5 (3,51) 3-5 (4,23) < 0,0001 Untypical colon topography 5/49 (10,2%) 24/49 (49%) < 0,0001 Infiltrating tumour 30/49 (61,2%) 30/48 (61,2%) = 1 Polypoid tumour 19/49 (38,8%) 18/48 (36,8%) = 0,83 Synchronic polyps <0,0001 Synchronic tumours 4 (8,2%) 6 (12,2%) - evaluation of enlarged lymph nodes for CTC was 84.6% and specificity 100%. Congruence of results in evaluation of liver metastases were in 26 (78.8%) patients. In 5 (15.2%) patients liver metastases seen in Ct was not seen in CTC, whereas lesions suspected as metastases in CTC were evaluated in CT as cysts. Sensitivity and specificity of CTC in evaluation of liver metastases in our patients were 61.5% and 90% respectively. A comparison of results of CTC and CT is presented in tab. 2. Discussion Till recently there is a few studies assessing diagnostic value of CTC in complex preoperative evaluation of patients suffering from large bowel tumors, and this method did not find at present proper place in clinical diagnostics (4-9). The main reason of this situation is variety of results from different centers (10-17). Many doubt are connected with kind of the reference standard for comparison of results. In most centers the reference standard is colonoscopy, in some results of histopathological and intraoperative examinations, in individual double-contrast enema images (5, 7, 18, 19, 20). Necessity of introduction precise standards suggest many authors (8, 12, 21). Working Group on Virtual Colonoscopy suggested introduction of a uniform system of performing and interpreting the study, known as C-RADS (CT Colonography Reporting and Data System), modeling on the BI-RADS system (Brest Imaging Reporting and Data System) currently used in mammography (21) It seems to that reaching a consensus concerning methodology of examination and introduction of uniform study protocol might contribute to similar and comparable results (5, 12, 15, 21). According to radiologists evaluating examination proper bowel cleansing plays important role in assessing of results of CTC (12, 15, 16). Poor preparation of bowel is the most common cause of diagnostic errors (7, 14, 16, 22). Because of this, examination should be performed in two positions of patients. Contrary to CTC liquid content or fecal debris did not make a big problem during interpretation of results of colonoscopy. Consequently better bowel cleansing is necessary for CTC. The time of examination was longer in CTC then in colonoscopy especially relating to interpretation part of the examination which is the longer the more lesions are in the large intestine. Increasing radiologists experience evaluating examination is also very important Table 2. Results of comparison between CT colonography and contrast-enhanced CT of abdomen CT colonography Contrast-enhanced CT p Fat tissue infiltration at the site of tumour 26/33 (78,8%) 20/33 (60,6%) 0,1 Surrounding organs infiltration at the site of tumour 12/33 (36,4%) 9/33 (27,3%) 0,43 Presence of enlarged ( 10 mm) abdominal and pelvic 11/33 (33,3%) 13/33 (39,4%) 0,61 lymph nodes Liver metastases 10/33 (30,3%) 13/33 (39,4%)

4 452 M. Rudzińska et al. (6, 14, 23). In our study CTC was congruent with colonoscopy in evaluation of tumor location but evaluation of location was more precise in CTC. In colonoscopy anatomic variation and the absence of fixed internal landmarks make it difficult to localize the tumor accurately and may be a cause of false results (1, 7, 24, 25). Volume reendering technique (VRT) enable a spatial, 3D imaging of large bowel provides images of bowel cast, similar to single or double-contrast enema images and enables assessment of localization of the tumor. Many authors similarly like in our study subsequently confirmed the effectiveness of CTC in detecting lesions located above the tumor and inaccessible on colonoscopy in spite of that in this examination it is difficult to avoid mistakes related to poor preparation and/or inadequate distension of bowel (7, 24, 25, 26). Improvements in CT technology and acquired radiologists experience help to reduce false results. Preoperative evaluation of the entire colon in patients with occluding colorectal cancer is widely recommended. Firstly, occluding tumors are located mainly in distal segments of large bowel thus the greater part of intestine is inaccessible for preoperative evaluation. Secondly, synchronous tumors are found more frequently in patients with occlusive tumors. Thirdly, it is difficult to evaluate intraoperatively the part of large bowel above the tumor because of bad cleansing and distension of the colon. Fenlon was the first to use CTC in patients with large bowel occluded by tumor to assess bowel segments proximal to the lesion (13). Synchronous tumors in this patients influenced frequently surgical conduct as the extent of the resection. Effectiveness of CTC in the evaluation of entire colon in case of incomplete colonoscopy has been confirmed by many authors (2, 4, 7, 8, 15, 24, 26, 27, 28). Preoperative precise evaluation of local infiltration, metastases to regional lymph nodes and distant organs is essential for the planning of optimal therapy (5, 13, 24, 26). Traditional colonoscopy does not able clinical staging. At present, this is done using spiral biphasic computed tomography encompassing abdominal cavity and pelvis (27, 29). The use on CTC of 2D reconstruction in any plane enable determination of both tumor size, thickening of bowel wall, degree of lumen stenosis, outline of external surface of bowel wall and relation to adjacent structures (2, 5, 7, 9, 25, 26, 30). Amin was the first who described the use of contrast-enhanced CTC in the detection and staging of colorectal cancer in few patients, presenting high accuracy in comparison with histopathological and intraoperative results (30). In CTC it is not possible to avoid false diagnosis (5, 7, 24, 26). Till now contrast-enhanced CT is necessary for the evaluation of adipose tissue and surrounding organs infiltration. Contrast-enhanced CTC enables simultaneous evaluation of abdominal organs, obviating the need for an additional classic computed tomography (5, 7, 13, 15). In our study we have shown that CT colonography is useful method in diagnostics of colorectal tumors. It allows both to determine local tumor staging and detect synchronous lesions in large bowel including endoscopically unavailable regions. CTC is not able to completely replace colonoscopy but it has the potential to become an alternative method. Further multicenter randomized studies are necessary to determine the role of CT colonography in colorectal tumor diagnostics. references 1. Hanson ME, Pickhardt PJ, Kim DH et al.: Anatomic factors predictive of incomplete colonoscopy based on findings at CT colonography. AJR Am J Roentgenol 2007; 189: Haykir R, Karakose S, Karabacakoglu A et al.: Three-dimensional MR and axial CT colonography versus conventional colonoscopy for detection of colon pathologies. World J Gastroenterol 2006; 12: Haykir R, Karakose S, Karabacakoglu A et al.: Detection of colonic masses with MR colonography. Turk J Gastroenterol 2006; 17: Morrin MM, Farrell RJ, Raptopoulos V et al.: Role of virtual computed tomographic colonography in patients with colorectal cancers and obstructing colorectal lesions. Dis Colon Rectum 2000; 43: Filippone A, Ambrosini R, Fuschi M et al.: Preoperative T and N staging of colorectal cancer: accuracy of contrast-enhanced multi-detector row CT colonography initial experience. Radiology 2004; 231: van DJ, Cotton P, Johnson CD et al.: AGA future trends report: CT colonography. Gastroenterology 2004; 127:

5 Computed tomography colonography in preoperative evaluation of colorectal cancer Chung DJ, Huh KC, Choi WJ et al.: CT colonography using 16-MDCT in the evaluation of colorectal cancer. AJR Am J Roentgenol 2005; 184: Anonymous Position of the American Gastroenterological Association (AGA) Institute on computed tomographic colonography. Gastroenterology 2006; 131: Utano K, Endo K, Togashi K et al.: Preoperative T staging of colorectal cancer by CT colonography. Dis Colon Rectum 2008; 51: Halligan S, Altman DG, Taylor SA et al.: CT colonography in the detection of colorectal polyps and cancer: systematic review, meta-analysis, and proposed minimum data set for study level reporting. Radiology 2005; 237: Mulhall BP, Veerappan GR, Jackson JL: Metaanalysis: computed tomographic colonography. Ann Intern Med 2005; 142: Pickhardt PJ, Choi JR, Hwang I et al.: Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 2003; 349: Fenlon HM, McAneny DB, Nunes DP et al.: Occlusive colon carcinoma: virtual colonoscopy in the preoperative evaluation of the proximal colon. Radiology 1999; 210: Doshi T, Rusinak D, Halvorsen RA et al.: CT colonography: false-negative interpretations. Radiology 2007; 244: Hoppe H, Netzer P, Spreng A et al.: Prospective comparison of contrast enhanced CT colonography and conventional colonoscopy for detection of colorectal neoplasms in a single institutional study using second-look colonoscopy with discrepant results. Am J Gastroenterol 2004; 99: van Gelder RE, Nio CY, Florie J et al.: Computed tomographic colonography compared with colonoscopy in patients at increased risk for colorectal cancer. Gastroenterology 2004; 127: Rockey DC, Paulson E, Niedzwiecki D et al.: Analysis of air contrast barium enema, computed tomographic colonography, and colonoscopy: prospective comparison. Lancet 2005; 365: Fenlon HM, Nunes DP, Schroy PC et al.: A comparison of virtual and conventional colonoscopy for the detection of colorectal polyps. N Engl J Med 1999; 341: Iannaccone R, Laghi A, Catalano C et al.: Feasibility of ultra-low-dose multislice CT colonography for the detection of colorectal lesions: preliminary experience. Eur Radiol 2003; 13: Gluecker TM, Johnson CD, Harmsen WS et al.: Colorectal cancer screening with CT colonography, colonoscopy, and double-contrast barium enema examination: prospective assessment of patient perceptions and preferences. Radiology 2003; 227: Zalis ME, Barish MA, Choi JR et al.: CT colonography reporting and data system: a consensus proposal. Radiology 2005; 236: Mang T, Maier A, Plank C et al.: Pitfalls in multi-detector row CT colonography: a systematic approach. Radiographics 2007; 27: Burling D, Halligan S, Altman DG et al.: CT colonography interpretation times: effect of reader experience, fatigue, and scan findings in a multicentre setting. Eur Radiol 2006; Mainenti PP, Cirillo LC, Camera L et al.: Accuracy of single phase contrast enhanced multidetector CT colonography in the preoperative staging of colorectal cancer. Eur J Radiol 2006; 60: Silva AC, Vens EA, Hara AK et al.: Evaluation of benign and malignant rectal lesions with CT colonography and endoscopic correlation. Radiographics 2006; 26: Kim JH, Kim WH, Kim TI et al.: Incomplete colonoscopy in patients with occlusive colorectal cancer: usefulness of CT colonography according to tumor location. Yonsei Med J 2007; 48: Prokop M, Galanski M, van der Molen AJ et al.: Spiralna i wielorzędowa tomografia komputerowa człowieka. Medipage 2007; 47-83, , , , Smith CS, Fenlon HM: Virtual colonoscopy. Best Pract Res Clin Gastroenterol 2002; 16: Pruszyński B: Radiologia diagnostyka obrazowa, RTG, TK, USG, MR i medycyna nuklearna. PZWL, Warszawa 2005; 65-68, Amin Z, Boulos PB, Lees WR: Technical report: spiral CT pneumocolon for suspected colonic neoplasms. Clin Radiol 1996; 51: Received: r. Adress correspondence: Bydgoszcz, ul. Powstańców Warszawy 5

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