Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Contrast-Enhanced MR Imaging of Lymph Nodes in Cancer Patients

  • Choi, Seung-Hong (Department of Radiology and the Clinical Research Institute, Seoul National University Hospital and the Institute of Radiation Medicine, Seoul National University College of Medicine) ;
  • Moon, Woo-Kyung (Department of Radiology and the Clinical Research Institute, Seoul National University Hospital and the Institute of Radiation Medicine, Seoul National University College of Medicine)
  • Received : 2010.01.18
  • Accepted : 2010.02.25
  • Published : 2010.08.01
⟨ Previous Next ⟩

Abstract

The accurate identification and characterization of lymph nodes by modern imaging modalities has important therapeutic and prognostic significance for patients with newly diagnosed cancers. The presence of nodal metastases limits the therapeutic options, and it generally indicates a worse prognosis for the patients with nodal metastases. Yet anatomic imaging (CT and MR imaging) is of limited value for depicting small metastatic deposits in normal-sized nodes, and nodal size is a poor criterion when there is no extracapsular extension or focal nodal necrosis to rely on for diagnosing nodal metastases. Thus, there is a need for functional methods that can be reliably used to identify small metastases. Contrast-enhanced MR imaging of lymph nodes is a non-invasive method for the analysis of the lymphatic system after the interstitial or intravenous administration of contrast media. Moreover, some lymphotrophic contrast media have been developed and used for detecting lymph node metastases, and this detection is independent of the nodal size. This article will review the basic principles, the imaging protocols, the interpretation and the accuracies of contrast-enhanced MR imaging of lymph nodes in patients with malignancies, and we also focus on the recent issues cited in the literature. In addition, we discuss the results of several pre-clinical studies and animal studies that were conducted in our institution.

Keywords

References

  1. King AD, Tse GM, Ahuja AT, Yuen EH, Vlantis AC, To EW, et al. Necrosis in metastatic neck nodes: diagnostic accuracy of CT, MR imaging, and US. Radiology 2004;230:720-726 https://doi.org/10.1148/radiol.2303030157
  2. Anzai Y, Brunberg JA, Lufkin RB. Imaging of nodal metastases in the head and neck. J Magn Reson Imaging 1997;7:774-783 https://doi.org/10.1002/jmri.1880070503
  3. Gershenwald JE, Thompson W, Mansfield PF, Lee JE, Colome MI, Tseng CH, et al. Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J Clin Oncol 1999;17:976-983 https://doi.org/10.1200/JCO.1999.17.3.976
  4. Laissy JP, Gay-Depassier P, Soyer P, Dombret MC, Murciano G, Sautet A, et al. Enlarged mediastinal lymph nodes in bronchogenic carcinoma: assessment with dynamic contrastenhanced MR imaging. Work in progress. Radiology 1994;191:263-267 https://doi.org/10.1148/radiology.191.1.8134585
  5. van den Brekel MW. Lymph node metastases: CT and MRI. Eur J Radiol 2000;33:230-238 https://doi.org/10.1016/S0720-048X(99)00145-X
  6. Davis GL. Sensitivity of frozen section examination of pelvic lymph nodes for metastatic prostate carcinoma. Cancer 1995;76:661-668 https://doi.org/10.1002/1097-0142(19950815)76:4<661::AID-CNCR2820760419>3.0.CO;2-S
  7. Torabi M, Aquino SL, Harisinghani MG. Current concepts in lymph node imaging. J Nucl Med 2004;45:1509-1518
  8. Moghimi SM, Bonnemain B. Subcutaneous and intravenous delivery of diagnostic agents to the lymphatic system: applications in lymphoscintigraphy and indirect lymphography. Adv Drug Deliv Rev 1999;37:295-312 https://doi.org/10.1016/S0169-409X(98)00099-4
  9. Puri SK, Fan CY, Hanna E. Significance of extracapsular lymph node metastases in patients with head and neck squamous cell carcinoma. Curr Opin Otolaryngol Head Neck Surg 2003;11:119-123 https://doi.org/10.1097/00020840-200304000-00010
  10. Kapucu LO, Meltzer CC, Townsend DW, Keenan RJ, Luketich JD. Fluorine-18-fluorodeoxyglucose uptake in pneumonia. J Nucl Med 1998;39:1267-1269
  11. Rennen HJ, Corstens FH, Oyen WJ, Boerman OC. New concepts in infection/inflammation imaging. Q J Nucl Med 2001;45:167-173
  12. Misselwitz B, Platzek J, Weinmann HJ. Early MR lymphography with gadofluorine M in rabbits. Radiology 2004;231:682-688 https://doi.org/10.1148/radiol.2313021000
  13. Misselwitz B. MR contrast agents in lymph node imaging. Eur J Radiol 2006;58:375-382 https://doi.org/10.1016/j.ejrad.2005.12.044
  14. Witte CL, Williams WH, Witte MH. Lymphatic imaging. Lymphology 1993;26:109-111
  15. Ruehm SG, Corot C, Debatin JF. Interstitial MR lymphography with a conventional extracellular gadolinium-based agent: assessment in rabbits. Radiology 2001;218:664-669 https://doi.org/10.1148/radiology.218.3.r01fe21664
  16. Lohrmann C, Foldi E, Bartholoma JP, Langer M. MR imaging of the lymphatic system: distribution and contrast enhancement of gadodiamide after intradermal injection. Lymphology 2006;39:156-163
  17. Misselwitz B, Sachse A. Interstitial MR lymphography using Gdcarrying liposomes. Acta Radiol Suppl 1997;412:51-55
  18. Weissleder R, Elizondo G, Josephson L, Compton CC, Fretz CJ, Stark DD, et al. Experimental lymph node metastases: enhanced detection with MR lymphography. Radiology 1989;171:835-839 https://doi.org/10.1148/radiology.171.3.2717761
  19. Harika L, Weissleder R, Poss K, Zimmer C, Papisov MI, Brady TJ. MR lymphography with a lymphotropic T1-type MR contrast agent: Gd-DTPA-PGM. Magn Reson Med 1995;33:88-92 https://doi.org/10.1002/mrm.1910330113
  20. Staatz G, Nolte-Ernsting CC, Bucker A, Misselwitz B, Grosskortenhaus S, Pfluger D, et al. Interstitial T1-weighted MR lymphography with use of the dendritic contrast agent Gadomer-17 in pigs. Rofo 2001;173:1131-1136 https://doi.org/10.1055/s-2001-18891
  21. Misselwitz B, Platzek J, Raduchel B, Oellinger JJ, Weinmann HJ. Gadofluorine 8: initial experience with a new contrast medium for interstitial MR lymphography. MAGMA 1999;8:190-195 https://doi.org/10.1007/BF02594598
  22. Staatz G, Nolte-Ernsting CC, Adam GB, Grosskortenhaus S, Misselwitz B, Bucker A, et al. Interstitial T1-weighted MR lymphography: lipophilic perfluorinated gadolinium chelates in pigs. Radiology 2001;220:129-134 https://doi.org/10.1148/radiology.220.1.r01jl04129
  23. Motoyama S, Ishiyama K, Maruyama K, Okuyama M, Sato Y, Hayashi K, et al. Preoperative mapping of lymphatic drainage from the tumor using ferumoxide-enhanced magnetic resonance imaging in clinical submucosal thoracic squamous cell esophageal cancer. Surgery 2007;141:736-747 https://doi.org/10.1016/j.surg.2007.01.032
  24. Bengele HH, Palmacci S, Rogers J, Jung CW, Crenshaw J, Josephson L. Biodistribution of an ultrasmall superparamagnetic iron oxide colloid, BMS 180549, by different routes of administration. Magn Reson Imaging 1994;12:433-442 https://doi.org/10.1016/0730-725X(94)92537-2
  25. Taupitz M, Wagner S, Hamm B. Contrast media for magnetic resonance tomographic lymph node diagnosis (MR lymphography). Radiologe 1996;36:134-140 https://doi.org/10.1007/s001170050050
  26. Vassallo P, Matei C, Heston WD, McLachlan SJ, Koutcher JA, Castellino RA. Characterization of reactive versus tumor-bearing lymph nodes with interstitial magnetic resonance lymphography in an animal model. Invest Radiol 1995;30:706-711 https://doi.org/10.1097/00004424-199512000-00003
  27. Weissleder R, Heautot JF, Schaffer BK, Nossiff N, Papisov MI, Bogdanov A Jr, et al. MR lymphography: study of a highefficiency lymphotrophic agent. Radiology 1994;191:225-230 https://doi.org/10.1148/radiology.191.1.8134576
  28. Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L. Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology 1990;175:489-493 https://doi.org/10.1148/radiology.175.2.2326474
  29. Suga K, Yuan Y, Ogasawara N, Okada M, Matsunaga N. Localization of breast sentinel lymph nodes by MR lymphography with a conventional gadolinium contrast agent. Preliminary observations in dogs and humans. Acta Radiol 2003;44:35-42 https://doi.org/10.1034/j.1600-0455.2003.00014.x
  30. Ruehm SG, Schroeder T, Debatin JF. Interstitial MR lymphography with gadoterate meglumine: initial experience in humans. Radiology 2001;220:816-821 https://doi.org/10.1148/radiol.2203010090
  31. Dimakakos E, Koureas A, Skiadas V, Kostapanagiotou G, Katsenis K, Arkadopoulos N, et al. Interstitial magnetic resonance lymphography with gadobutrol in rabbits and an initial experience in humans. Lymphology 2006;39:164-170
  32. Trubetskoy VS, Cannillo JA, Milshtein A, Wolf GL, Torchilin VP. Controlled delivery of Gd-containing liposomes to lymph nodes: surface modification may enhance MRI contrast properties. Magn Reson Imaging 1995;13:31-37 https://doi.org/10.1016/0730-725X(94)00083-F
  33. Harika L, Weissleder R, Poss K, Papisov MI. Macromolecular intravenous contrast agent for MR lymphography: characterization and efficacy studies. Radiology 1996;198:365-370 https://doi.org/10.1148/radiology.198.2.8596833
  34. Kobayashi H, Kawamoto S, Star RA, Waldmann TA, Tagaya Y, Brechbiel MW. Micro-magnetic resonance lymphangiography in mice using a novel dendrimer-based magnetic resonance imaging contrast agent. Cancer Res 2003;63:271-2764
  35. Kobayashi H, Kawamoto S, Sakai Y, Choyke PL, Star RA, Brechbiel MW, et al. Lymphatic drainage imaging of breast cancer in mice by micro-magnetic resonance lymphangiography using a nano-size paramagnetic contrast agent. J Natl Cancer Inst 2004;96:703-708 https://doi.org/10.1093/jnci/djh124
  36. Misselwitz B, Schmitt-Willich H, Michaelis M, Oellinger JJ. Interstitial magnetic resonance lymphography using a polymeric t1 contrast agent: initial experience with Gadomer-17. Invest Radiol 2002;37:146-151
  37. Desser TS, Rubin DL, Muller H, McIntire GL, Bacon ER, Hollister KR. Interstitial MR and CT lymphography with GddTPA- co-alpha, omega-diaminoPEG(1450) and Gd-dTPA-co- 1,6-diaminohexane polymers: preliminary experience. Acad Radiol 1999;6:112-118 https://doi.org/10.1016/S1076-6332(99)80490-5
  38. Herborn CU, Vogt FM, Lauenstein TC, Goyen M, Dirsch O, Corot C, et al. Assessment of normal, inflammatory, and tumorbearing lymph nodes with contrast-enhanced interstitial magnetic resonance lymphography: preliminary results in rabbits. J Magn Reson Imaging 2003;18:328-335 https://doi.org/10.1002/jmri.10357
  39. Herborn CU, Lauenstein TC, Vogt FM, Lauffer RB, Debatin JF, Ruehm SG. Interstitial MR lymphography with MS-325: characterization of normal and tumor-invaded lymph nodes in a rabbit model. AJR Am J Roentgenol 2002;179:1567-1572 https://doi.org/10.2214/ajr.179.6.1791567
  40. Choi SH, Han MH, Moon WK, Son KR, Won JK, Kim JH, et al. Cervical lymph node metastases: MR imaging of gadofluorine M and monocrystalline iron oxide nanoparticle-47 in a rabbit model of head and neck cancer. Radiology 2006;241:753-762 https://doi.org/10.1148/radiol.2413051979
  41. Cha JH, Moon WK, Cheon JE, Koh YH, Lee EH, Park SS, et al. Differentiation of hyperplastic from metastatic lymph nodes using a lymph node specific MR contrast agent gadofluroine M. J Korean Radiol Soc 2006;55:183-189 [Korean] https://doi.org/10.3348/jkrs.2006.55.2.183
  42. Harisinghani MG, Barentsz J, Hahn PF, Deserno WM, Tabatabaei S, van de Kaa CH, et al. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 2003;348:2491-2499 https://doi.org/10.1056/NEJMoa022749
  43. Choi SH, Moon WK, Hong JH, Son KR, Cho N, Kwon BJ, et al. Lymph node metastasis: ultrasmall superparamagnetic iron oxide-enhanced MR imaging versus PET/CT in a rabbit model. Radiology 2007;242:137-143 https://doi.org/10.1148/radiol.2421060093
  44. Weissleder R, Elizondo G, Wittenberg J, Lee AS, Josephson L, Brady TJ. Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology 1990;175:494-498 https://doi.org/10.1148/radiology.175.2.2326475
  45. Muhler A, Zhang X, Wang H, Lawaczeck R, Weinmann HJ. Investigation of mechanisms influencing the accumulation of ultrasmall superparamagnetic iron oxide particles in lymph nodes. Invest Radiol 1995;30:98-103 https://doi.org/10.1097/00004424-199502000-00006
  46. Bush CH, Mladinich CR, Montgomery WJ. Evaluation of an ultrasmall superparamagnetic iron oxide in MRI in a bone tumor model in rabbits. J Magn Reson Imaging 1997;7:579-584 https://doi.org/10.1002/jmri.1880070320
  47. Rogers JM, Jung CW, Lewis J, Groman EV. Use of USPIOinduced magnetic susceptibility artifacts to identify sentinel lymph nodes and lymphatic drainage patterns. I. Dependence of artifact size with subcutaneous Combidex dose in rats. Magn Reson Imaging 1998;16:917-923 https://doi.org/10.1016/S0730-725X(98)00090-3
  48. 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 https://doi.org/10.1007/s00261-001-0182-9
  49. Harisinghani MG, Dixon WT, Saksena MA, Brachtel E, Blezek DJ, Dhawale PJ, et al. MR lymphangiography: imaging strategies to optimize the imaging of lymph nodes with ferumoxtran- 10. Radiographics 2004;24:867-878 https://doi.org/10.1148/rg.243035190
  50. Safety Data from Study 38804-10: A phase III safety and efficacy study of combidex as a magnetic resonance imaging agent for the evaluation of lymph node disease, AMAG. Pharmaceuticals, Inc., Boston, MA, USA-498
  51. Islam T, Harisinghani MG. Overview of nanoparticle use in cancer imaging. Cancer Biomark 2009;5:61-67 https://doi.org/10.3233/CBM-2009-0578
  52. Will O, Purkayastha S, Chan C, Athanasiou T, Darzi AW, Gedroyc W, et al. Diagnostic precision of nanoparticle-enhanced MRI for lymph-node metastases: a meta-analysis. Lancet Oncol 2006;7:52-60 https://doi.org/10.1016/S1470-2045(05)70537-4
  53. Anzai Y, Piccoli CW, Outwater EK, Stanford W, Bluemke DA, Nurenberg P, et al. Evaluation of neck and body metastases to nodes with ferumoxtran 10-enhanced MR imaging: phase III safety and efficacy study. Radiology 2003;228:777-788 https://doi.org/10.1148/radiol.2283020872
  54. Saksena M, Harisinghani M, Hahn P, Kim J, Saokar A, King B, et al. Comparison of lymphotropic nanoparticle-enhanced MRI sequences in patients with various primary cancers. AJR Am J Roentgenol 2006;187:W582-W588 https://doi.org/10.2214/AJR.05.0873
  55. Narayanan P, Iyngkaran T, Sohaib SA, Reznek RH, Rockall AG. Pearls and pitfalls of MR lymphography in gynecologic malignancy. Radiographics 2009;29:1057-1069 https://doi.org/10.1148/rg.294085231
  56. Kimura K, Tanigawa N, Matsuki M, Nohara T, Iwamoto M, Sumiyoshi K, et al. High-resolution MR lymphography using ultrasmall superparamagnetic iron oxide (USPIO) in the evaluation of axillary lymph nodes in patients with early stage breast cancer: preliminary results. Breast Cancer 2009 [Epub ahead of print]
  57. Heesakkers RA, Futterer JJ, Hovels AM, van den Bosch HC, Scheenen TW, Hoogeveen YL, et al. Prostate cancer evaluated with ferumoxtran-10-enhanced T2*-weighted MR Imaging at 1.5 and 3.0 T: early experience. Radiology 2006;239:481-487 https://doi.org/10.1148/radiol.2392050411
  58. Choi SH, Kim KH, Moon WK, Kim HC, Cha JH, Paik JH, et al. Comparison of lymph node metastases assessment with the use of USPIO-enhanced MR imaging at 1.5 T versus 3.0 T in a rabbit model. J Magn Reson Imaging 2010;31:134-141 https://doi.org/10.1002/jmri.22020
  59. Lahaye MJ, Engelen SM, Kessels AG, de Bruine AP, von Meyenfeldt MF, van Engelshoven JM, et al. USPIO-enhanced MR imaging for nodal staging in patients with primary rectal cancer: predictive criteria. Radiology 2008;246:804-811 https://doi.org/10.1148/radiol.2463070221
  60. Lee AS, Weissleder R, Brady TJ, Wittenberg J. Lymph nodes: microstructural anatomy at MR imaging. Radiology 1991;178:519-522 https://doi.org/10.1148/radiology.178.2.1987619
  61. Koh DM, Brown G, Temple L, Raja A, Toomey P, Bett N, et al. Rectal cancer: mesorectal lymph nodes at MR imaging with USPIO versus histopathologic findings--initial observations. Radiology 2004;231:91-99 https://doi.org/10.1148/radiol.2311030142
  62. Anzai Y, Prince MR. Iron oxide-enhanced MR lymphography: the evaluation of cervical lymph node metastases in head and neck cancer. J Magn Reson Imaging 1997;7:75-81 https://doi.org/10.1002/jmri.1880070111
  63. Anzai Y, Blackwell KE, Hirschowitz SL, Rogers JW, Sato Y, Yuh WT, et al. Initial clinical experience with dextran-coated superparamagnetic iron oxide for detection of lymph node metastases in patients with head and neck cancer. Radiology 1994;192:709-715 https://doi.org/10.1148/radiology.192.3.7520182
  64. Bellin MF, Roy C, Kinkel K, Thoumas D, Zaim S, Vanel D, 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 https://doi.org/10.1148/radiology.207.3.9609907
  65. Sigal R, Vogl T, Casselman J, Moulin G, Veillon F, Hermans R, 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 https://doi.org/10.1007/s003300101130
  66. Stets C, Brandt S, Wallis F, Buchmann J, Gilbert FJ, Heywang- Ko brunner SH. Axillary lymph node metastases: a statistical analysis of various parameters in MRI with USPIO. J Magn Reson Imaging 2002;16:60-68 https://doi.org/10.1002/jmri.10134
  67. Mack MG, Balzer JO, Straub R, Eichler K, Vogl TJ. Superparamagnetic iron oxide-enhanced MR imaging of head and neck lymph nodes. Radiology 2002;222:239-244 https://doi.org/10.1148/radiol.2221010225
  68. Deserno WM, Harisinghani MG, Taupitz M, Jager GJ, Witjes JA, Mulders PF, et al. Urinary bladder cancer: preoperative nodal staging with ferumoxtran-10-enhanced MR imaging. Radiology 2004;233:449-456 https://doi.org/10.1148/radiol.2332031111
  69. Rockall AG, Sohaib SA, Harisinghani MG, Babar SA, Singh N, Jeyarajah AR, et al. Diagnostic performance of nanoparticleenhanced magnetic resonance imaging in the diagnosis of lymph node metastases in patients with endometrial and cervical cancer. J Clin Oncol 2005;23:2813-2821 https://doi.org/10.1200/JCO.2005.07.166
  70. Stadnik TW, Everaert H, Makkat S, Sacre R, Lamote J, Bourgain C. Breast imaging. Preoperative breast cancer staging: comparison of USPIO-enhanced MR imaging and 18Ffluorodeoxyglucose (FDC) positron emission tomography (PET) imaging for axillary lymph node staging--initial findings. Eur Radiol 2006;16:2153-2160 https://doi.org/10.1007/s00330-006-0276-4
  71. Memarsadeghi M, Riedl CC, Kaneider A, Galid A, Rudas M, Matzek W, et al. Axillary lymph node metastases in patients with breast carcinomas: assessment with nonenhanced versus uspio-enhanced MR imaging. Radiology 2006;241:367-377 https://doi.org/10.1148/radiol.2412050693
  72. Heesakkers RA, Ho vels AM, Jager GJ, van den Bosch HC, Witjes JA, Raat HP, et al. MRI with a lymph-node-specific contrast agent as an alternative to CT scan and lymph-node dissection in patients with prostate cancer: a prospective multicohort study. Lancet Oncol 2008;9:850-856 https://doi.org/10.1016/S1470-2045(08)70203-1
  73. Fischbein NJ, Noworolski SM, Henry RG, Kaplan MJ, Dillon WP, Nelson SJ. Assessment of metastatic cervical adenopathy using dynamic contrast-enhanced MR imaging. AJNR Am J Neuroradiol 2003;24:301-311
  74. Lee KC, Moon WK, Chung JW, Choi SH, Cho N, Cha JH, et al. Assessment of lymph node metastases by contrast-enhanced MR imaging in a head and neck cancer model. Korean J Radiol 2007;8:9-14 https://doi.org/10.3348/kjr.2007.8.1.9
  75. Murray AD, Staff RT, Redpath TW, Gilbert FJ, Ah-See AK, Brookes JA, et al. Dynamic contrast enhanced MRI of the axilla in women with breast cancer: comparison with pathology of excised nodes. Br J Radiol 2002;75:220-228 https://doi.org/10.1259/bjr.75.891.750220
  76. Luciani A, Dao TH, Lapeyre M, Schwarzinger M, Debaecque C, Lantieri L, et al. Simultaneous bilateral breast and high-resolution axillary MRI of patients with breast cancer: preliminary results. AJR Am J Roentgenol 2004;182:1059-1067 https://doi.org/10.2214/ajr.182.4.1821059

Cited by

  1. Imaging assessment of tumor response: past, present and future vol.7, pp.5, 2010, https://doi.org/10.2217/fon.11.38
  2. Comparison of Two Ultrasmall Superparamagnetic Iron Oxides on Cytotoxicity and MR Imaging of Tumors vol.2, pp.1, 2012, https://doi.org/10.7150/thno.3462
  3. Graphene oxide-Fe3O4 nanoparticle composite with high transverse proton relaxivity value for magnetic resonance imaging vol.117, pp.15, 2010, https://doi.org/10.1063/1.4918605
  4. International Multicenter Study on the Impact of Extracapsular Lymph Node Involvement in Primary Surgery Adenocarcinoma of the Esophagus on Overall Survival and Staging Systems vol.262, pp.5, 2010, https://doi.org/10.1097/sla.0000000000001463
  5. Lymph node staging using dedicated magnetic resonance contrast agents-the accumulation mechanism revisited vol.7, pp.2, 2010, https://doi.org/10.1002/wnan.1290
  6. Effects of ferumoxytol on quantitative PET measurements in simultaneous PET/MR whole-body imaging: a pilot study in a baboon model vol.2, pp.1, 2010, https://doi.org/10.1186/s40658-015-0109-0
  7. Fat-suppressed gadolinium-enhanced isotropic high-resolution 3D-GRE-T1WI for predicting small node metastases in patients with rectal cancer vol.18, pp.None, 2018, https://doi.org/10.1186/s40644-018-0153-9
  8. MR lymphography for sentinel lymph node detection in patients with oral cavity cancer: Preliminary clinical study vol.40, pp.7, 2010, https://doi.org/10.1002/hed.25167
  9. Role of Quantitative Dynamic Contrast-Enhanced MRI in Evaluating Regional Lymph Nodes With a Short-Axis Diameter of Less Than 5 mm in Rectal Cancer vol.212, pp.1, 2010, https://doi.org/10.2214/ajr.18.19866
  10. MRI of Rectal Cancer: Tumor Staging, Imaging Techniques, and Management vol.39, pp.2, 2019, https://doi.org/10.1148/rg.2019180114
  11. The mechanical responses of advecting cells in confined flow vol.14, pp.3, 2010, https://doi.org/10.1063/5.0005154
  12. New Developments in Imaging for Sentinel Lymph Node Biopsy in Early-Stage Oral Cavity Squamous Cell Carcinoma vol.12, pp.10, 2010, https://doi.org/10.3390/cancers12103055