Evidence-based Practice

Rectal Cancer: Local Staging and Assessment of Lymph Node Involvement with Endoluminal US, CT, and MR Imaging—A Meta-Analysis

Abstract

PURPOSE: To perform a meta-analysis to compare endoluminal ultrasonography (US), computed tomography (CT), and magnetic resonance (MR) imaging in rectal cancer staging.

MATERIALS AND METHODS: Relevant articles published between 1985 and 2002 were included if more than 20 patients were studied, histopathologic findings were the reference standard, and data were presented for 2 × 2 tables; articles were excluded if data were reported elsewhere in more detail. Two reviewers independently extracted data on study characteristics and results. Bivariate random-effects approach was used to obtain summary estimates of sensitivity and specificity for invasion of muscularis propria, perirectal tissue, and adjacent organs and for lymph node involvement. Summary receiver operating characteristic (ROC) curves were fitted for perirectal tissue invasion and lymph node involvement.

RESULTS: Ninety articles fulfilled all inclusion criteria. For muscularis propria invasion, US and MR imaging had similar sensitivities; specificity of US (86% [95% confidence interval {CI}: 80, 90]) was significantly higher than that of MR imaging (69% [95% CI: 52, 82]) (P = .02). For perirectal tissue invasion, sensitivity of US (90% [95% CI: 88, 92]) was significantly higher than that of CT (79% [95% CI: 74, 84]) (P < .001) and MR imaging (82% [95% CI: 74, 87]) (P = .003); specificities were comparable. For adjacent organ invasion and lymph node involvement, estimates for US, CT, and MR imaging were comparable. Summary ROC curve for US of perirectal tissue invasion showed better diagnostic accuracy than that of CT and MR imaging. Summary ROC curves for lymph node involvement showed no differences in accuracy.

CONCLUSION: For local invasion, endoluminal US was most accurate and can be helpful in screening patients for available therapeutic strategies.

References

1 Harrison JC, Dean PJ, el Zeky F, Vander ZR. From Dukes through Jass: pathological prognostic indicators in rectal cancer. Hum Pathol 1994; 25:498-505. Crossref, Medline, Google Scholar
2 Jass JR, Love SB. Prognostic value of direct spread in Dukes’ C cases of rectal cancer. Dis Colon Rectum 1989; 32:477-480. Crossref, Medline, Google Scholar
3 Tang R, Wang JY, Chen JS, et al. Survival impact of lymph node metastasis in TNM stage III carcinoma of the colon and rectum. J Am Coll Surg 1995; 180:705-712. Medline, Google Scholar
4 Willett CG, Badizadegan K, Ancukiewicz M, Shellito PC. Prognostic factors in stage T3N0 rectal cancer: do all patients require postoperative pelvic irradiation and chemotherapy? Dis Colon Rectum 1999; 42:167-173. Crossref, Medline, Google Scholar
5 Wolmark N, Fisher B, Wieand HS. The prognostic value of the modifications of the Dukes’ C class of colorectal cancer. Ann Surg 1986; 203:115-122. Crossref, Medline, Google Scholar
6 Akasu T, Kondo H, Moriya Y, et al. Endorectal ultrasonography and treatment of early stage rectal cancer. World J Surg 2000; 24:1061-1068. Crossref, Medline, Google Scholar
7 Blair S, Ellenhorn JD. Transanal excision for low rectal cancers is curative in early-stage disease with favorable histology. Am Surg 2000; 66:817-820. Medline, Google Scholar
8 Gao JD, Shao YF, Bi JJ, Shi SS, Liang J, Hu YH. Local excision carcinoma in early stage. World J Gastroenterol 2003; 9:871-873. Crossref, Medline, Google Scholar
9 Langer C, Liersch T, Markus P, et al. Transanal endoscopic microsurgery (TEM) for minimally invasive resection of rectal adenomas and “low-risk” carcinomas (uT1, G1–2). Z Gastroenterol 2002; 40:67-72. Crossref, Medline, Google Scholar
10 Chen ET, Mohiuddin M, Brodovsky H, Fishbein G, Marks G. Downstaging of advanced rectal cancer following combined preoperative chemotherapy and high dose radiation. Int J Radiat Oncol Biol Phys 1994; 30:169-175. Crossref, Medline, Google Scholar
11 Kaminsky-Forrett MC, Conroy T, Luporsi E, et al. Prognostic implications of downstaging following preoperative radiation therapy for operable T3–T4 rectal cancer. Int J Radiat Oncol Biol Phys 1998; 42:935-941. Crossref, Medline, Google Scholar
12 Rau B, Wust P, Hohenberger P, et al. Preoperative hyperthermia combined with radiochemo therapy in locally advanced rectal cancer: a phase II clinical trial. Ann Surg 1998; 227:380-389. Crossref, Medline, Google Scholar
13 Hermanek P, Hermanek P, Hohenberger W, Klimpfinger M, Kockerling F, Papadopoulos T. The pathological assessment of mesorectal excision: implications for further treatment and quality management. Int J Colorectal Dis 2003; 18:335-341. Crossref, Medline, Google Scholar
14 Nagtegaal ID, van Krieken JH. The role of pathologists in the quality control of diagnosis and treatment of rectal cancer: an overview. Eur J Cancer 2002; 38:964-972. Crossref, Medline, Google Scholar
15 Wiggers T, van de Velde CJ. The circumferential margin in rectal cancer: recommendations based on the Dutch Total Mesorectal Excision Study. Eur J Cancer 2002; 38:973-976. Crossref, Medline, Google Scholar
16 Gualdi GF, Casciani E, Guadalaxara A, d’Orta C, Polettini E, Pappalardo G. Local staging of rectal cancer with transrectal ultrasound and endorectal magnetic resonance imaging: comparison with histologic findings. Dis Colon Rectum 2000; 43:338-345. Crossref, Medline, Google Scholar
17 Hunerbein M, Pegios W, Rau B, Vogl TJ, Felix R, Schlag PM. Prospective comparison of endorectal ultrasound, three-dimensional endorectal ultrasound, and endorectal MRI in the preoperative evaluation of rectal tumors: preliminary results. Surg Endosc 2000; 14:1005-1009. Crossref, Medline, Google Scholar
18 Chiesura-Corona M, Muzzio PC, Giust G, Zuliani M, Pucciarelli S, Toppan P. Rectal cancer: CT local staging with histopathologic correlation. Abdom Imaging 2001; 26:134-138. Crossref, Medline, Google Scholar
19 Matsuoka H, Nakamura A, Masaki T, et al. Preoperative staging by multidetector-row computed tomography in patients with rectal carcinoma. Am J Surg 2002; 184:131-135. Crossref, Medline, Google Scholar
20 Blomqvist L, Machado M, Rubio C, et al. Rectal tumour staging: MR imaging using pelvic phased-array and endorectal coils vs endoscopic ultrasonography. Eur Radiol 2000; 10:653-660. Crossref, Medline, Google Scholar
21 Kinkel K, Lu Y, Both M, Warren RS, Thoeni RF. Detection of hepatic metastases from cancers of the gastrointestinal tract by using noninvasive imaging methods (US, CT, MR imaging, PET): a meta-analysis. Radiology 2002; 224:748-756. Link, Google Scholar
22 Oei EH, Nikken JJ, Verstijnen AC, Ginai AZ, Myriam Hunink MG. MR imaging of the menisci and cruciate ligaments: a systematic review. Radiology 2003; 226:837-848. Link, Google Scholar
23 Deville WL, Bezemer PD, Bouter LM. Publications on diagnostic test evaluation in family medicine journals: an optimal search strategy. J Clin Epidemiol 2000; 53:65-69. Crossref, Medline, Google Scholar
24 Van Houwelingen HC, Zwinderman KH, Stijnen T. A bivariate approach to meta-analysis. Stat Med 1993; 12:2273-2284. Crossref, Medline, Google Scholar
25 Van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 2002; 21:589-624. Crossref, Medline, Google Scholar
26 Rao CR. Linear statistical inference and its applications 2nd ed. New York, NY: Wiley, 1973; 417-420. Google Scholar
27 Liang KY, Zeger SL. Regression analysis for correlated data. Annu Rev Public Health 1993; 14:43-68. Crossref, Medline, Google Scholar
28 Hildebrandt U, Feifel G. Preoperative staging of rectal cancer by intrarectal ultrasound. Dis Colon Rectum 1985; 28:42-46. Crossref, Medline, Google Scholar
29 Konishi F, Muto T, Takahashi H, Itoh K, Kanazawa K, Morioka Y. Transrectal ultrasonography for the assessment of invasion of rectal carcinoma. Dis Colon Rectum 1985; 28:889-894. Crossref, Medline, Google Scholar
30 Beynon J, Foy DM, Roe AM, Temple LN, Mortensen NJ. Endoluminal ultrasound in the assessment of local invasion in rectal cancer. Br J Surg 1986; 73:474-477. Crossref, Medline, Google Scholar
31 Kramann B, Hildebrandt U. Computed tomography versus endosonography in the staging of rectal carcinoma: a comparative study. Int J Colorectal Dis 1986; 1:216-218. Crossref, Medline, Google Scholar
32 Feifel G, Hildebrandt U, Dhom G. Assessment of depth of invasion in rectal cancer by endosonography. Endoscopy 1987; 19:64-67. Crossref, Medline, Google Scholar
33 Glaser F, Schlag P, Herfarth C. Endorectal ultrasonography for the assessment of invasion of rectal tumours and lymph node involvement. Br J Surg 1990; 77:883-887. Crossref, Medline, Google Scholar
34 Orrom WJ, Wong WD, Rothenberger DA, Jensen LL, Goldberg SM. Endorectal ultrasound in the preoperative staging of rectal tumors: a learning experience. Dis Colon Rectum 1990; 33:654-659. Crossref, Medline, Google Scholar
35 Napoleon B, Pujol B, Berger F, Valette PJ, Gerard JP, Souquet JC. Accuracy of endosonography in the staging of rectal cancer treated by radiotherapy. Br J Surg 1991; 78:785-788. Crossref, Medline, Google Scholar
36 Boyce GA, Sivak MV, Jr, Lavery IC, et al. Endoscopic ultrasound in the pre-operative staging of rectal carcinoma. Gastrointest Endosc 1992; 38:468-471. Crossref, Medline, Google Scholar
37 Derksen EJ, Cuesta MA, Meijer S. Intraluminal ultrasound of rectal tumours: a prerequisite in decision making. Surg Oncol 1992; 1:193-198. Crossref, Medline, Google Scholar
38 Herzog U, von Flue M, Tondelli P, Schuppisser JP. How accurate is endorectal ultrasound in the preoperative staging of rectal cancer? Dis Colon Rectum 1993; 36:127-134. Crossref, Medline, Google Scholar
39 Houvenaeghel G, Delpero JR, Giovannini M, et al. Staging of rectal cancer: a prospective study of digital examination and endosonography before and after preoperative radiotherapy. Acta Chir Belg 1993; 93:164-168. Medline, Google Scholar
40 Hulsmans FJ, Tio TL, Fockens P, Bosma A, Tytgat GN. Assessment of tumor infiltration depth in rectal cancer with transrectal sonography: caution is necessary. Radiology 1994; 190:715-720. Link, Google Scholar
41 Kim NK, Choi JS, Sohn SK, Min JS. Transrectal ultrasonography in preoperative staging of rectal cancer. Yonsei Med J 1994; 35:396-403. Crossref, Medline, Google Scholar
42 Rafaelsen SR, Kronborg O, Fenger C. Digital rectal examination and transrectal ultrasonography in staging of rectal cancer: a prospective, blind study. Acta Radiol 1994; 35:300-304. Crossref, Medline, Google Scholar
43 Adams WJ, Wong WD. Endorectal ultrasonic detection of malignancy within rectal villous lesions. Dis Colon Rectum 1995; 38:1093-1096. Crossref, Medline, Google Scholar
44 Fedyaev EB, Volkova EA, Kuznetsova EE. Transrectal and transvaginal ultrasonography in the preoperative staging of rectal carcinoma. Eur J Radiol 1995; 20:35-38. Crossref, Medline, Google Scholar
45 Starck M, Bohe M, Fork FT, Lindstrom C, Sjoberg S. Endoluminal ultrasound and low-field magnetic resonance imaging are superior to clinical examination in the preoperative staging of rectal cancer. Eur J Surg 1995; 161:841-845. Medline, Google Scholar
46 Kaneko K, Boku N, Hosokawa K, et al. Diagnostic utility of endoscopic ultrasonography for preoperative rectal cancer staging estimation. Jpn J Clin Oncol 1996; 26:30-35. Crossref, Medline, Google Scholar
47 Nielsen MB, Qvitzau S, Pedersen JF, Christiansen J. Endosonography for preoperative staging of rectal tumours. Acta Radiol 1996; 37:799-803. Crossref, Medline, Google Scholar
48 Akasu T, Sugihara K, Moriya Y, Fujita S. Limitations and pitfalls of transrectal ultrasonography for staging of rectal cancer. Dis Colon Rectum 1997; 40(suppl 10):S10-S15. Crossref, Medline, Google Scholar
49 Hunerbein M, Schlag PM. Three-dimensional endosonography for staging of rectal cancer. Ann Surg 1997; 225:432-438. Crossref, Medline, Google Scholar
50 Maier AG, Barton PP, Neuhold NR, Herbst F, Teleky BK, Lechner GL. Peritumoral tissue reaction at transrectal US as a possible cause of overstaging in rectal cancer: histopathologic correlation. Radiology 1997; 203:785-789. Link, Google Scholar
51 Sailer M, Leppert R, Kraemer M, Fuchs KH, Thiede A. The value of endorectal ultrasound in the assessment of adenomas, T1- and T2-carcinomas. Int J Colorectal Dis 1997; 12:214-219. Crossref, Medline, Google Scholar
52 Massari M, De Simone M, Cioffi U, Rosso L, Chiarelli M, Gabrielli F. Value and limits of endorectal ultrasonography for preoperative staging of rectal carcinoma. Surg Laparosc Endosc 1998; 8:438-444. Crossref, Medline, Google Scholar
53 Akahoshi K, Kondoh A, Nagaie T, et al. Preoperative staging of rectal cancer using a 7.5 MHz front-loading US probe. Gastrointest Endosc 2000; 52:529-534. Crossref, Medline, Google Scholar
54 Carmody BJ, Otchy DP. Learning curve of transrectal ultrasound. Dis Colon Rectum 2000; 43:193-197. Crossref, Medline, Google Scholar
55 Kim JC, Cho YK, Kim SY, Park SK, Lee MG. Comparative study of three-dimensional and conventional endorectal ultrasonography used in rectal cancer staging. Surg Endosc 2002; 16:1280- 1285. Crossref, Medline, Google Scholar
56 Steele SR, Martin MJ, Place RJ. Flexible endorectal ultrasound for predicting pathologic stage of rectal cancers. Am J Surg 2002; 184:126-130. Crossref, Medline, Google Scholar
57 Garcia-Aguilar J, Pollack J, Lee SH, et al. Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum 2002; 45:10-15. Crossref, Medline, Google Scholar
58 Okizuka H, Sugimura K, Ishida T. Preoperative local staging of rectal carcinoma with MR imaging and a rectal balloon. J Magn Reson Imaging 1993; 3:329-335. Crossref, Medline, Google Scholar
59 Schnall MD, Furth EE, Rosato EF, Kressel HY. Rectal tumor stage: correlation of endorectal MR imaging and pathologic findings. Radiology 1994; 190:709-714. Link, Google Scholar
60 Okizuka H, Sugimura K, Yoshizako T, Kaji Y, Wada A. Rectal carcinoma: prospective comparison of conventional and gadopentetate dimeglumine enhanced fat-suppressed MR imaging. J Magn Reson Imaging 1996; 6:465-471. Crossref, Medline, Google Scholar
61 Pegios W, Vogl J, Mack MG, et al. MRI diagnosis and staging of rectal carcinoma. Abdom Imaging 1996; 21:211-218. Crossref, Medline, Google Scholar
62 Hadfield MB, Nicholson AA, MacDonald AW, et al. Preoperative staging of rectal carcinoma by magnetic resonance imaging with a pelvic phased-array coil. Br J Surg 1997; 84:529-531. Crossref, Medline, Google Scholar
63 Vogl TJ, Pegios W, Mack MG, et al. Accuracy of staging rectal tumors with contrast-enhanced transrectal MR imaging. AJR Am J Roentgenol 1997; 168:1427-1434. Crossref, Medline, Google Scholar
64 Drew PJ, Farouk R, Turnbull LW, Ward SC, Hartley JE, Monson JR. Preoperative magnetic resonance staging of rectal cancer with an endorectal coil and dynamic gadolinium enhancement. Br J Surg 1999; 86:250-254. Crossref, Medline, Google Scholar
65 Kim NK, Kim MJ, Park JK, Park SI, Min JS. Preoperative staging of rectal cancer with MRI: accuracy and clinical usefulness. Ann Surg Oncol 2000; 7:732-737. Crossref, Medline, Google Scholar
66 Beynon J, Mortensen NJ, Foy DM, Channer JL, Virjee J, Goddard P. Pre-operative assessment of local invasion in rectal cancer: digital examination, endoluminal sonography or computed tomography? Br J Surg 1986; 73:1015-1017. Crossref, Medline, Google Scholar
67 Rifkin MD, Wechsler RJ. A comparison of computed tomography and endorectal ultrasound in staging rectal cancer. Int J Colorectal Dis 1986; 1:219-223. Crossref, Medline, Google Scholar
68 Saitoh N, Okui K, Sarashina H, Suzuki M, Arai T, Nunomura M. Evaluation of echographic diagnosis of rectal cancer using intrarectal ultrasonic examination. Dis Colon Rectum 1986; 29:234-242. Crossref, Medline, Google Scholar
69 Alessi G, Giuliani A, Risi D, Meli C, Schillaci A, Stipa S. Intrarectal ultrasonography in the preoperative staging of rectal cancer. Ital J Surg Sci 1987; 17:239-244. Medline, Google Scholar
70 Beynon J, Roe AM, Foy DM, Channer JL, Virjee J, Mortensen NJ. Preoperative staging of local invasion in rectal cancer using endoluminal ultrasound. J R Soc Med 1987; 80:23-24. Crossref, Medline, Google Scholar
71 Di Candio G, Mosca F, Campatelli A, Cei A, Ferrari M, Basolo F. Endosonographic staging of rectal carcinoma. Gastrointest Radiol 1987; 12:289-295. Crossref, Medline, Google Scholar
72 Holdsworth PJ, Johnston D, Chalmers AG, et al. Endoluminal ultrasound and computed tomography in the staging of rectal cancer. Br J Surg 1988; 75:1019-1022. Crossref, Medline, Google Scholar
73 Salo JO, Mecklin JP, Jarvinen H, Lehtonen T. Endo-ultrasonography for preoperative staging of rectal cancer. Ann Chir Gynaecol 1988; 77:57-60. Medline, Google Scholar
74 Rifkin MD, Ehrlich SM, Marks G. Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology 1989; 170:319-322. Link, Google Scholar
75 Rotte KH, Kluhs L, Kleinau H, Kriedemann E. Computed tomography and endosonography in the preoperative staging of rectal carcinoma. Eur J Radiol 1989; 9:187-190. Medline, Google Scholar
76 Dershaw DD, Enker WE, Cohen AM, Sigurdson ER. Transrectal ultrasonography of rectal carcinoma. Cancer 1990; 66:2336-2340. Crossref, Medline, Google Scholar
77 Jochem RJ, Reading CC, Dozois RR, Carpenter HA, Wolff BG, Charboneau JW. Endorectal ultrasonographic staging of rectal carcinoma. Mayo Clin Proc 1990; 65:1571-1577. Crossref, Medline, Google Scholar
78 Goldman S, Arvidsson H, Norming U, Lagerstedt U, Magnusson I, Frisell J. Transrectal ultrasound and computed tomography in preoperative staging of lower rectal adenocarcinoma. Gastrointest Radiol 1991; 16:259-263. Crossref, Medline, Google Scholar
79 Lindmark G, Elvin A, Pahlman L, Glimelius B. The value of endosonography in preoperative staging of rectal cancer. Int J Colorectal Dis 1992; 7:162-166. Crossref, Medline, Google Scholar
80 Scialpi M, Andreatta R, Agugiaro S, Zottele F, Niccolini M, Dalla PF. Rectal carcinoma: preoperative staging and detection of postoperative local recurrence with transrectal and transvaginal ultrasound. Abdom Imaging 1993; 18:381-389. Crossref, Medline, Google Scholar
81 Nielsen MB, Pedersen JF, Christiansen J. Rectal endosonography in the evaluation of stenotic rectal tumors. Dis Colon Rectum 1993; 36:275-279. Crossref, Medline, Google Scholar
82 Thaler W, Watzka S, Martin F, et al. Preoperative staging of rectal cancer by endoluminal ultrasound vs. magnetic resonance imaging: preliminary results of a prospective, comparative study. Dis Colon Rectum 1994; 37:1189-1193. Google Scholar
83 Barbaro B, Valentini V, Manfredi R. Combined modality staging of high risk rectal cancer. Rays 1995; 20:165-181. Medline, Google Scholar
84 Osti MF, Padovan FS, Pirolli C, et al. Comparison between transrectal ultrasonography and computed tomography with rectal inflation of gas in preoperative staging of lower rectal cancer. Eur Radiol 1997; 7:26-30. Crossref, Medline, Google Scholar
85 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 Am J Roentgenol 1997; 169:1247-1252. Crossref, Medline, Google Scholar
86 Lindmark GE, Kraaz WG, Elvin PA, Glimelius BL. Rectal cancer: evaluation of staging with endosonography. Radiology 1997; 204:533-538. Link, Google Scholar
87 Barbaro B, Schulsinger A, Valentini V, Marano P, Rotman M. The accuracy of transrectal ultrasound in predicting the pathological stage of low-lying rectal cancer after preoperative chemoradiation therapy. Int J Radiat Oncol Biol Phys 1999; 43:1043-1047. Crossref, Medline, Google Scholar
88 Adams DR, Blatchford GJ, Lin KM, Ternent CA, Thorson AG, Christensen MA. Use of preoperative ultrasound staging for treatment of rectal cancer. Dis Colon Rectum 1999; 42:159-166. Crossref, Medline, Google Scholar
89 Harewood GC, Wiersema MJ, Nelson H, et al. A prospective, blinded assessment of the impact of preoperative staging on the management of rectal cancer. Gastroenterology 2002; 123:24-32. Crossref, Medline, Google Scholar
90 Netri G, Coco C, Valentini V, et al. Clinical staging of rectal cancer: results of a prospective continuing study. Ital J Surg Sci 1985; 15:169-174. Medline, Google Scholar
91 Thompson WM, Halvorsen RA, Foster WL, Roberts L, Gibbons R. Preoperative and postoperative CT staging of rectosigmoid carcinoma. AJR Am J Roentgenol 1986; 146:703-710. Crossref, Medline, Google Scholar
92 Cellini N, Coco C, Maresca G, et al. Clinical staging of rectal cancer: a study on 126 patients. Rays 1986; 11:69-79. Google Scholar
93 Angelelli G, Macarini L, Lupo L, Caputi-Jambrenghi O, Pannarale O, Memeo V. Rectal carcinoma: CT staging with water as contrast medium. Radiology 1990; 177:511-514. Link, Google Scholar
94 Civelli EM, Gallino G, Mariani L, et al. Double-contrast barium enema and computerised tomography in the pre-operative evaluation of rectal carcinoma: are they still useful diagnostic procedures? Tumori 2000; 86:389-392. Crossref, Medline, Google Scholar
95 Gagliardi G, Bayar S, Smith R, Salem RR. Preoperative staging of rectal cancer using magnetic resonance imaging with external phase-arrayed coils. Arch Surg 2002; 137:447-451. Crossref, Medline, Google Scholar
96 Murano A, Sasaki F, Kido C, et al. Endoscopic MRI using 3D-spoiled GRASS (SPGR) sequence for local staging of rectal carcinoma. J Comput Assist Tomogr 1995; 19:586-591. Crossref, Medline, Google Scholar
97 Scialpi M, Rotondo A, Angelelli G. Water enema transvaginal ultrasound for local staging of stenotic rectal carcinoma. Abdom Imaging 1999; 24:132-136. Crossref, Medline, Google Scholar
98 Lupo L, Angelelli G, Pannarale O, Altomare D, Macarini L, Memeo V. Improved accuracy of computed tomography in local staging of rectal cancer using water enema. Int J Colorectal Dis 1996; 11:60-64. Crossref, Medline, Google Scholar
99 Zainea GG, Lee F, McLeary RD, Siders DB, Thieme ET. Transrectal ultrasonography in the evaluation of rectal and extrarectal disease. Surg Gynecol Obstet 1989; 169:153-156. Medline, Google Scholar
100 Beynon J, Mortensen NJ, Foy DM, Channer JL, Rigby H, Virjee J. Preoperative assessment of mesorectal lymph node involvement in rectal cancer. Br J Surg 1989; 76:276-279. Crossref, Medline, Google Scholar
101 Hildebrandt U, Klein T, Feifel G, Schwarz HP, Koch B, Schmitt RM. Endosonography of pararectal lymph nodes: in vitro and in vivo evaluation. Dis Colon Rectum 1990; 33:863-868. Crossref, Medline, Google Scholar
102 Milsom JW, Graffner H. Intrarectal ultrasonography in rectal cancer staging and in the evaluation of pelvic disease: clinical uses of intrarectal ultrasound. Ann Surg 1990; 212:602-606. Crossref, Medline, Google Scholar
103 Konishi F, Ugajin H, Ito K, Kanazawa K. Endorectal ultrasonography with a 7.5 MHz linear array scanner for the assessment of invasion of rectal carcinoma. Int J Colorectal Dis 1990; 5:15-20. Crossref, Medline, Google Scholar
104 Milsom JW, Lavery IC, Stolfi VM, et al. The expanding utility of endoluminal ultrasonography in the management of rectal cancer. Surgery 1992; 112:832- 840. Medline, Google Scholar
105 Spinelli P, Schiavo M, Meroni E, et al. Results of EUS in detecting perirectal lymph node metastases of rectal cancer: the pathologist makes the difference. Gastrointest Endosc 1999; 49:754-758. Crossref, Medline, Google Scholar
106 Kim NK, Kim MJ, Yun SH, Sohn SK, Min JS. Comparative study of transrectal ultrasonography, pelvic computerized tomography, and magnetic resonance imaging in preoperative staging of rectal cancer. Dis Colon Rectum 1999; 42:770-775. Crossref, Medline, Google Scholar
107 Tada M, Endo M. Ultrasonographic examination for lateral lymphatic spread and local recurrence of rectal cancer: preoperative detection and evaluation. Dis Colon Rectum 1995; 38:1047-1052. Crossref, Medline, Google Scholar
108 Hodgman CG, MacCarty RL, Wolff BG, et al. Preoperative staging of rectal carcinoma by computed tomography and 0.15T magnetic resonance imaging. Preliminary report. Dis Colon Rectum 1986; 29:446-450. Crossref, Medline, Google Scholar
109 de Lange EE, Fechner RE, Edge SB, Spaulding CA. Preoperative staging of rectal carcinoma with MR imaging: surgical and histopathologic correlation. Radiology 1990; 176:623-628. Link, Google Scholar
110 McNicholas MM, Joyce WP, Dolan J, Gibney RG, MacErlaine DP, Hyland J. Magnetic resonance imaging of rectal carcinoma: a prospective study. Br J Surg 1994; 81:911-914. Crossref, Medline, Google Scholar
111 Lijmer JG, Mol BW, Heisterkamp S, et al. Empirical evidence of design-related bias in studies of diagnostic tests. JAMA 1999; 282:1061-1066. Crossref, Medline, Google Scholar
112 Littenberg B, Moses LE. Estimating diagnostic accuracy from multiple conflicting reports: a new meta-analytic method. Med Decis Making 1993; 13:313-321. Crossref, Medline, Google Scholar
113 Rutter CM, Gatsonis CA. A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat Med 2001; 20:2865-2884. Crossref, Medline, Google Scholar
114 Abdel-Nabi H, Doerr RJ, Lamonica DM, et al. Staging of primary colorectal carcinomas with fluorine-18 fluorodeoxyglucose whole-body PET: correlation with histopathologic and CT findings. Radiology 1998; 206:755-760. Link, Google Scholar
115 Falk PM, Gupta NC, Thorson AG, et al. Positron emission tomography for preoperative staging of colorectal carcinoma. Dis Colon Rectum 1994; 37:153-156. Crossref, Medline, Google Scholar
116 Gupta NC, Falk PM, Frank AL, Thorson AM, Frick MP, Bowman B. Pre-operative staging of colorectal carcinoma using positron emission tomography. Nebr Med J 1993; 78:30-35. Medline, Google Scholar
117 Kwok H, Bissett IP, Hill GL. Preoperative staging of rectal cancer. Int J Colorectal Dis 2000; 15:9-20. Crossref, Medline, Google Scholar
118 Bellin MF, Lebleu L, Meric JB. Evaluation of retroperitoneal and pelvic lymph node metastases with MRI and MR lymphangiography. Abdom Imaging 2003; 28:155-163. Crossref, Medline, Google Scholar
119 Bellin MF, Roy C, Kinkel K, et al. Lymph node metastases: safety and effectiveness of MR imaging with ultrasmall superparamagnetic iron oxide particles—initial clinical experience. Radiology 1998; 207:799-808. Link, Google Scholar
120 Harisinghani MG, Saini S, Weissleder R, et al. MR lymphangiography using ultrasmall superparamagnetic iron oxide in patients with primary abdominal and pelvic malignancies: radiographic-pathologic correlation. AJR Am J Roentgenol 1999; 172:1347-1351. Crossref, Medline, Google Scholar
121 Hudgins PA, Anzai Y, Morris MR, Lucas MA. Ferumoxtran-10, a superparamagnetic iron oxide as a magnetic resonance enhancement agent for imaging lymph nodes: a phase 2 dose study. AJNR Am J Neuroradiol 2002; 23:649-656. Medline, Google Scholar
122 McCauley TR, Rifkin MD, Ledet CA. Pelvic lymph node visualization with MR imaging using local administration of ultra-small superparamagnetic iron oxide contrast. J Magn Reson Imaging 2002; 15:492-497. Crossref, Medline, Google Scholar
123 Laghi A, Iannaccone R, Trenna S, et al. Multislice spiral CT colonography in the evaluation of colorectal neoplasms. Radiol Med (Torino) 2002; 104:394-403. Medline, Google Scholar
124 Vogl TJ, Luboldt W, Herzog C, Hammerstingl R. Contrast-enhanced multislice CT in detection and evaluation of abdominal neoplasms. Radiologe 2002; 42:646-654. [German]. Crossref, Medline, Google Scholar
125 Beets-Tan RG, Beets GL, Vliegen RF, et al. Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery. Lancet 2001; 357:497-504. Crossref, Medline, Google Scholar
126 Bissett IP, Fernando CC, Hough DM, et al. Identification of the fascia propria by magnetic resonance imaging and its relevance to preoperative assessment of rectal cancer. Dis Colon Rectum 2001; 44:259-265. Crossref, Medline, Google Scholar
127 Brown G, Richards CJ, Newcombe RG, et al. Rectal carcinoma: thin-section MR imaging for staging in 28 patients. Radiology 1999; 211:215-222. Link, Google Scholar

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Vol. 232, No. 3

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