Rectal cancer: Review with emphasis on MR imaging

Radiology

Volumn 232, Issue 2, 2004, Pages 335-346

  Beets Tan, Regina G H ^a   Beets, Geerard L ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CT; MR; Neoplasms; Rectum; Review

Indexed keywords

ANTINEOPLASTIC AGENT; FLUORODEOXYGLUCOSE; GADOLINIUM; SUPERPARAMAGNETIC IRON OXIDE;

ADVANCED CANCER; CANCER ADJUVANT THERAPY; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER GROWTH; CANCER INVASION; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER STAGING; CANCER SURGERY; CLINICAL TRIAL; COMPUTER ASSISTED EMISSION TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; DIAGNOSTIC ACCURACY; DIAGNOSTIC IMAGING; HIGH RISK PATIENT; HUMAN; LYMPH NODE METASTASIS; MEDICAL DECISION MAKING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT SELECTION; PELVIS LYMPHADENECTOMY; PHYSICAL EXAMINATION; PREOPERATIVE EVALUATION; PREOPERATIVE TREATMENT; PRIORITY JOURNAL; RANDOMIZATION; RECTUM CANCER; RECTUM RESECTION; RECTUM SURGERY; RECURRENCE RISK; REVIEW; SPIRAL COMPUTER ASSISTED TOMOGRAPHY; SURGICAL APPROACH; TRANSRECTAL ULTRASONOGRAPHY; TREATMENT INDICATION;

COMBINED MODALITY THERAPY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; NEOADJUVANT THERAPY; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; RADIOTHERAPY, ADJUVANT; RECTAL NEOPLASMS; RECTUM;

EID: 3242808840     PISSN: 00338419     EISSN: None     Source Type: Journal    
DOI: 10.1148/radiol.2322021326     Document Type: Review

References (111)

1. Sagar PM, Pemberton JH. Surgical management of locally recurrent rectal cancer. Br J Surg 1996; 83:293-304.
2. Adam IJ, Mohamdee MO, Martin IG, et al. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet 1994; 344:707-711.
3. Quirke P, Durdey P, Dixon MF, Williams NS. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection: histopathological study of lateral tumor spread and surgical excision. Lancet 1986; 2:996-999.
4. Minsky BD. Adjuvant radiation therapy for rectal cancer: is there finally an answer? (editorial). Lancet 2001; 358: 1285-1286.
5. Minsky BD. Role of adjuvant therapy in adenocarcinoma of the rectum. Semin Surg Oncol 1999; 17:189-198.
6. Improved survival with preoperative radiotherapy in resectable rectal cancer. Swedish Rectal Cancer Trial. N Engl J Med 1997; 336:980-987.
7. Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1986; 1:1479-1482.
8. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 2001; 345:638-646.
9. Adjuvant radiotherapy for rectal cancer: a systematic overview of 8,507 patients from 22 randomised trials. Colorectal Cancer Collaborative Group. Lancet 2001; 358:1291-1304.
10. Rifkin MD, Ehrlich SM, Marks G. Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology 1989; 170:319-322.
11. 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.
12. Glaser F, Schlag P, Herfarth C. Endorectal ultrasonography for the assessment of invasion of rectal tumors and lymph node involvement. Br J Surg 1990; 77: 883-887.
13. Katsura Y, Yamada K, Ishizawa T, Yoshinaka H, Shimazu H. Endorectal ultrasonography for the assessment of wall invasion and lymph node metastasis in rectal cancer. Dis Colon Rectum 1992; 35:362-368.
14. 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.
15. 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.
16. 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): S10-S15.
17. 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.
18. Lee P, Oyama K, Homer L, Sullivan E. Effects of endorectal ultrasonography in the surgical management of rectal adenomas and carcinomas. Am J Surg 1999; 177:388-391.
19. 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.
20. Genna M, Leopardi F, Valloncini E, Veraldi GF. Results of preoperative staging using endosonography in rectal cancer. Minerva Chir 2000; 55:409-414.
21. 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.
22. 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.
23. 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.
24. 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.
25. Marone P, Petrulio F, de Bellis M, Battista Rossi G, Tempesta A. Role of endoscopic ultrasonography in the staging of rectal cancer: a retrospective study of 63 patients. J Clin Gastroenterol 2000; 30: 420-424.
26. Maldjian C, Smith R, Kilger A, Schnall M, Ginsberg G, Kochman M. Endorectal surface coil MR imaging as a staging technique for rectal carcinoma: a comparison study to rectal endosonography. Abdom Imaging 2000; 25:75-80.
27. Akasu T, Kondo H, Moriya Y, et al. Endorectal ultrasonography and treatment of early stage rectal cancer. World J Surg 2000; 24:1061-1068.
28. Solomon MJ, McLeod RS. Endoluminal transrectal ultrasonography: accuracy, reliability, and validity. Dis Colon Rectum 1993; 36:200-205.
29. Enck P, Heyer T, Gantke B, et al. How reproducible are measures of the anal sphincter muscle diameter by endoanal ultrasound? Am J Gastroenterol 1997; 92:293-296.
30. Gold DM, Halligan S, Kmiot WA, Bartram CI. Intraobserver and interobserver agreement in anal endosonography. Br J Surg 1999; 86:371-375.
31. Solomon MJ, McLeod RS, Cohen EK, Simons ME, Wilson S. Reliability and validity studies of endoluminal ultrasonography for anorectal disorders. Dis Colon Rectum 1994; 37:546-551.
32. Thoeni RF, Moss AA, Schnyder P, Margulis AR. Detection and staging of primary rectal and rectosigmoid cancer by computed tomography. Radiology 1981; 141:135-138.
33. Zaunbauer W, Haertel M, Fuchs WA. Computed tomography in carcinoma of the rectum. Gastrointest Radiol 1981; 6:79-84.
34. van Waes PF, Koehler PR, Feldberg MA. Management of rectal carcinoma: impact of computed tomography. AJR Am J Roentgenol 1983; 140:1137-1142.
35. Grabbe E, Lierse W, Winkler R. The perirectal fascia: morphology and use in staging of rectal carcinoma. Radiology 1983; 149:241-246.
36. 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.
37. 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.
38. 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.
39. Cova M, Frezza F, Pozzi-Mucelli RS, et al. Computed tomography and magnetic resonance in the preoperative staging of the spread of rectal cancer: a correlation with the anatomicopathological aspects. Radiol Med (Torino) 1994; 87:82-89.
40. Shank B, Dershaw DD, Caravelli J, Barth J, Enker W. A prospective study of the accuracy of preoperative computed tomographic staging of patients with biopsy-proven rectal carcinoma. Dis Colon Rectum 1990; 33:285-290.
41. Zerhouni EA, Rutter C, Hamilton SR, et al. CT and MR imaging in the staging of colorectal carcinoma: report of the Radiology Diagnostic Oncology Group II. Radiology 1996; 200:443-451.
42. Thoeni RF. Colorectal cancer: radiologic staging. Radiol Clin North Am 1997; 35: 457-485.
43. Butch RJ, Stark DD, Wittenberg J, et al. Staging rectal cancer by MR and CT. AJR Am J Roentgenol 1986; 146:1155-1160.
44. Kwok H, Bissett IP, Hill GL. Preoperative staging of rectal cancer. Int J Colorectal Dis 2000; 15:9-20.
45. Guinet C, Buy JN, Ghossain MA, et al. Comparison of magnetic resonance imaging and computed tomography in the preoperative staging of rectal cancer. Arch Surg 1990; 125:385-388.
46. 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.
47. 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.
48. Vogl TJ, Pegios W, Hunerbein M, Mack MG, Schlag PM, Felix R. Use and applications of MRI techniques in the diagnosis and staging of rectal lesions. Recent Results Cancer Res 1998; 146:35-47.
49. Chan TW, Kressel HY, Milestone B, et al. Rectal carcinoma: staging at MR imaging with endorectal surface coil-work in progress. Radiology 1991; 181:461-467.
50. Schnall MD, Furth EE, Rosato EF, Kressel HY. Rectal tumor stage: correlation of endorectal MR imaging and pathologic findings. Radiology 1994; 190:709-714.
51. Indinnimeo M, Grasso RF, Cicchini C, et al. Endorectal magnetic resonance imaging in the preoperative staging of rectal tumors. Int Surg 1996; 81:419-422.
52. Zagoria RJ, Schlarb CA, Ott DJ, et al. Assessment of rectal tumor infiltration utilizing endorectal MR imaging and comparison with endoscopic rectal sonography. J Surg Oncol 1997; 64:312-317.
53. Pegios W, Vogl J, Mack MG, et al. MRI diagnosis and staging of rectal carcinoma. Abdom Imaging 1996; 21:211-218.
54. 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.
55. deSouza NM, Hall AS, Puni R, Gilderdale DJ Young IR, Kmiot WA. High resolution magnetic resonance imaging of the anal sphincter using a dedicated endoanal coil: comparison of magnetic resonance imaging with surgical findings. Dis Colon Rectum 1996; 39:926-934.
56. 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.
57. Beets-Tan RG, Beets GL, van der Hoop AG, et al. High-resolution magnetic resonance imaging of the anorectal region without an endocoil. Abdom Imaging 1999; 24:576-581; discussion 582-584.
58. Beets-Tan RG, Morren GL, Beets GL, et al. Measurement of anal sphincter muscles: endoanal US, endoanal MR imaging, or phased-array MR imaging? - a study with healthy volunteers. Radiology 2001; 220:81-89.
59. Beets-Tan RG, Beets GL, van der Hoop AG, et al. Preoperative MR imaging of anal fistulas: does it really help the surgeon? Radiology 2001; 218:75-84.
60. Brown G, Richards CJ, Newcombe RG, et al. Rectal carcinoma: thin-section MR imaging for staging in 28 patients. Radiology 1999; 211:215-222.
61. Blomqvist L, Machado M, Rubio C, et al. Rectal tumor staging: MR imaging using pelvic phased-array and endorectal coils vs endoscopic ultrasonography. Eur Radiol 2000; 10:653-660.
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.
63. de Lange EE, Fechner RE, Wanebo HJ. Suspected recurrent rectosigmoid carcinoma after abdominoperineal resection: MR imaging and histopathologic findings. Radiology 1989; 170:323-328.
64. 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.
65. Blomqvist L, Holm T, Rubio C, Hindmarsh T. Rectal tumors: MR imaging with endorectal and/or phased-array coils, and histopathological staging on giant sections - a comparative study. Acta Radiol 1997; 38:437-444.
66. 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.
67. Meyenberger C, Huch Boni RA, Bertschinger P, Zala GF, Klotz HP, Krestin GP. Endoscopic ultrasound and endorectal magnetic resonance imaging: a prospective, comparative study for preoperative staging and follow-up of rectal cancer. Endoscopy 1995; 27:469-479.
68. Nagtegaal ID, Marijnen CA, Kranenbarg EK, van De Velde CJ, van Krieken JH. Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma: not one millimeter but two millimeters is the limit. Am J Surg Pathol 2002; 26:350-357.
69. Wibe A, Rendedal PR, Svensson E, et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg 2002; 89:327-334.
70. Nelson H, Sargent DJ. Refining multimodal therapy for rectal cancer (editorial). N Engl J Med 2001; 345:690-692.
71. Radcliffe A, Brown G. Will MRI provide maps of lines of excision for rectal cancer? (editorial). Lancet 2001; 357:495-496.
72. Wiggers T, van de Velde CH. Reduction "by half:" the need for standardised surgical technique in studies of radiotherapy for rectal cancer (editorial). Eur J Surg 1999; 165:407-409.
73. Blomqvist L, Rubio C, Holm T, Machado M, Hindmarsh T. Rectal adenocarcinoma: assessment of tumor involvement of the lateral resection margin by MRI of resected specimen. Br J Radiol 1999; 72:18-23.
74. Brown G, Radcliffe AG, Newcombe RG, Dallimore NS, Bourne MW, Williams GT. Preoperative assessment of prognostic factors in rectal cancer using high-resolution magnetic resonance imaging. Br J Surg 2003; 90:355-364.
75. 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.
76. Poeze M, Houbiers JG, van de Velde CJ, Wobbes T, von Meyenfeldt MF. Radical resection of locally advanced colorectal cancer. Br J Surg 1995; 82:1386-1390.
77. Popovich MJ, Hricak H, Sugimura K, Stern JL. The role of MR imaging in determining surgical eligibility for pelvic exenteration. AJR Am J Roentgenol 1993; 160:525-531.
78. Moss AA. Imaging of colorectal carcinoma (editorial). Radiology 1989; 170: 308-310.
79. Beets-Tan RG, Beets GL, Borstlap AC, et al. Preoperative assessment of local tumor extent in advanced rectal cancer: CT or high-resolution MRI? Abdom Imaging 2000; 25:533-541.
80. Blomqvist L, Holm T, Nyren S, Svanstrom R, Ulvskog Y, Iselius L. MR imaging and computed tomography in patients with rectal tumors clinically judged as locally advanced. Clin Radiol 2002; 57:211-218.
81. Blomqvist L, Holm T, Goranson H, Jacobsson H, Ohlsen H, Larsson SA. MR imaging, CT and CEA scintigraphy in the diagnosis of local recurrence of rectal carcinoma. Acta Radiol 1996; 37: 779-784.
82. 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.
83. Horton KM, Abrams RA, Fishman EK. Spiral CT of colon cancer: imaging features and role in management. Radio-Graphics 2000; 20:419-430.
84. 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.
85. Harnsberger JR, Vernava VM 3rd, Longo WE. Radical abdominopelvic lymphadenectomy: historic perspective and current role in the surgical management of rectal cancer. Dis Colon Rectum 1994; 37:73-87.
86. Monig SP, Baldus SE, Zirbes TK, et al. Lymph node size and metastatic infiltration in colon cancer. Ann Surg Oncol 1999; 6:579-581.
87. Andreola S, Leo E, Belli F, et al. Manual dissection of adenocarcinoma of the lower third of the rectum specimens for detection of lymph node metastases smaller than 5 mm. Cancer 1996; 77: 607-612.
88. Bjelovic M, Kalezic V, Petrovic M, et al. Correlation of macroscopic and histological characteristics in the regional lymph nodes of patients with rectal and sigmoidal adenocarcinoma. Hepatogastroenterology 1998; 45:433-438.
89. Dworak O. Number and size of lymph nodes and node metastases in rectal carcinomas. Surg Endosc 1989; 3:96-99.
90. Moriya Y, Sugihara K, Akasu T, Fujita S. Importance of extended lymphadenectomy with lateral node dissection for advanced lower rectal cancer. World J Surg 1997; 21:728-732.
91. Jager GJ, Barentsz JO, Oosterhof GO, Witjes JA, Ruijs SJ. Pelvic adenopathy in prostatic and urinary bladder carcinoma: MR imaging with a three-dimensional T1-weighted magnetization-prepared-rapid gradient-echo sequence. AJR Am J Roentgenol 1996; 167:1503-1507.
92. Williams AD, Cousins C, Soutter WP, et al. Detection of pelvic lymph node metastases in gynecologic malignancy: a comparison of CT, MR imaging, and positron emission tomography. AJR Am J Roentgenol 2001; 177:343-348.
93. Carrington B. Lymph nodes. In: Husband JES, Reznek RH, eds. Imaging in oncology. Oxford, England: Dunitz, 1998.
94. Tio TL, Coene PP, van Delden OM, Tytgat GN. Colorectal carcinoma: preoperative TNM classification with endosonography. Radiology 1991; 179:165-170.
95. 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.
96. Balthazar EJ, Megibow AJ, Hulnick D, Naidich DP. Carcinoma of the colon: detection and preoperative staging by CT. AJR Am J Roentgenol 1988; 150:301-306.
97. Thompson WM, Halvorsen RA, Foster WL Jr, Roberts L, Gibbons R. Preoperative and postoperative CT staging of rectosigmoid carcinoma. AJR Am J Roentgenol 1986; 146:703-710.
98. 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.
99. 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.
100. 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.
101. 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.
102. Hung GU, Shiau YC, Tsai SC, Chao TH, Ho YJ, Kao CH. Value of 18F-fluoro-2-deoxyglucose positron emission tomography in the evaluation of recurrent colorectal cancer. Anticancer Res 2001; 21:1375-1378.
103. Imdahl A, Reinhardt MJ, Nitzsche EU, et al. Impact of 18F-FDG-positron emission tomography for decision making in colorectal cancer recurrences. Langenbecks Arch Surg 2000; 385:129-134.
104. Flamen P, Hoekstra OS, Homans F, et al. Unexplained rising carcinoembryonic antigen (CEA) in the postoperative surveillance of colorectal cancer: the utility of positron emission tomography (PET). Eur J Cancer 2001; 37:862-869.
105. Staib L, Schirrmeister H, Reske SN, Beger HG. Is (18)F-fluorodeoxyglucose positron emission tomography in recurrent colorectal cancer a contribution to surgical decision making? Am J Surg 2000; 180:1-5.
106. Arulampalam T, Costa D, Visvikis D, Boulos P, Taylor I, Ell P. The impact of FDG-PET on the management algorithm for recurrent colorectal cancer. Eur J Nucl Med 2001; 28:1758-1765.
107. Beets G, Penninckx F, Schiepers C, et al. Clinical value of whole-body positron emission tomography with [18F]fluorodeoxyglucose in recurrent colorectal cancer. Br J Surg 1994; 81:1666-1670.
108. 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.
109. 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.
110. Sigal R, Vogl T, Casselman J, et al. Lymph node metastases from head and neck squamous cell carcinoma: MR imaging with ultrasmall superparamagnetic iron oxide particles (Sinerem MR)-results of a phase-III multicenter clinical trial. Eur Radiol 2002; 12:1104-1113.
111. Vliegen RFA, Beets GL, Kessels AG, et al. Magnetic resonance imaging in staging rectal cancer: is gadolinium helpful? (abstr). Radiology 2002; 205(P):244.