Skip to main content
Top
Published in: European Radiology 8/2004

01-08-2004 | Oncology

Imaging the lymphatic system: possibilities and clinical applications

Authors: Olivier Clément, Alain Luciani

Published in: European Radiology | Issue 8/2004

Login to get access

Abstract

The lymphatic system is anatomically complex and difficult to image. Lymph ducts are responsible for the drainage of part of the body’s interstitial fluid. Lymph nodes account for the enrichment of lymph fluid, and can be involved in a large variety of diseases, especially cancer. For a long time, lymphatic imaging was limited to the sole use of conventional lymphography involving invasive procedures and patient discomfort. New contrast agents and techniques in ultrasound, nuclear medicine, and MR imaging are now available for imaging of both the lymphatic vessels and the lymph nodes. The objective of this review is to discuss the different imaging modalities of the lymphatic system, with a special focus on the new possibilities of lymphatic imaging including enhanced MR lymphography, sentinel node and positron emission tomography imaging, and contrast-enhanced ultrasound.
Literature
1.
go back to reference Witte CL, Witte MH, Unger EC et al (2000) Advances in imaging of lymph flow disorders. Radiographics 20:1697–1719PubMed Witte CL, Witte MH, Unger EC et al (2000) Advances in imaging of lymph flow disorders. Radiographics 20:1697–1719PubMed
2.
go back to reference Picard J-D (1995) Lymphatic circulation. S.I.A., Lavaur, France Picard J-D (1995) Lymphatic circulation. S.I.A., Lavaur, France
4.
go back to reference Moghimi SM, Bonnemain B (1999) Subcutaneous and intravenous delivery of diagnostic agents to the lymphatic system: applications in lymphoscintigraphy and indirect lymphography. Adv Drug Deliv Rev 37:295–312CrossRefPubMed Moghimi SM, Bonnemain B (1999) Subcutaneous and intravenous delivery of diagnostic agents to the lymphatic system: applications in lymphoscintigraphy and indirect lymphography. Adv Drug Deliv Rev 37:295–312CrossRefPubMed
5.
go back to reference Weissleder H, Weissleder R (1988) Lymphedema: evaluation of qualitative and quantitative lymphoscintigraphy in 238 patients. Radiology 167:729–735PubMed Weissleder H, Weissleder R (1988) Lymphedema: evaluation of qualitative and quantitative lymphoscintigraphy in 238 patients. Radiology 167:729–735PubMed
6.
go back to reference Witte CL, Witte MH (1999) Diagnostic and interventional imaging of lymphatic disorders. Int Angiol 18:25–30PubMed Witte CL, Witte MH (1999) Diagnostic and interventional imaging of lymphatic disorders. Int Angiol 18:25–30PubMed
7.
go back to reference Weissleder R, Elizondo G, Josephson L et al (1989) Experimental lymph node metastases: enhanced detection with MR lymphography. Radiology 171:835–839PubMed Weissleder R, Elizondo G, Josephson L et al (1989) Experimental lymph node metastases: enhanced detection with MR lymphography. Radiology 171:835–839PubMed
8.
go back to reference Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L (1990) Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology 175:489–493PubMed Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L (1990) Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology 175:489–493PubMed
9.
go back to reference Jung CW (1995) Surface properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging 13:675–691CrossRefPubMed Jung CW (1995) Surface properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging 13:675–691CrossRefPubMed
10.
go back to reference Jung CW, Jacobs P (1995) Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging 13:661–674CrossRefPubMed Jung CW, Jacobs P (1995) Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging 13:661–674CrossRefPubMed
11.
go back to reference Weissleder R, Elizondo G, Wittenberg J, Lee AS, Josephson L, Brady TJ (1990) Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology 175:494–498PubMed Weissleder R, Elizondo G, Wittenberg J, Lee AS, Josephson L, Brady TJ (1990) Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology 175:494–498PubMed
12.
go back to reference Clement O, Rety F, Cuenod CA et al (1998) MR lymphography: evidence of extravasation of superparamagnetic nanoparticles into the lymph. Acad Radiol 5:S170–S172 (discussion S183–S174)PubMed Clement O, Rety F, Cuenod CA et al (1998) MR lymphography: evidence of extravasation of superparamagnetic nanoparticles into the lymph. Acad Radiol 5:S170–S172 (discussion S183–S174)PubMed
13.
go back to reference Rety F, Clement O, Siauve N et al (2000) MR lymphography using iron oxide nanoparticles in rats: pharmacokinetics in the lymphatic system after intravenous injection. J Magn Reson Imaging 12:734–739 Rety F, Clement O, Siauve N et al (2000) MR lymphography using iron oxide nanoparticles in rats: pharmacokinetics in the lymphatic system after intravenous injection. J Magn Reson Imaging 12:734–739
14.
go back to reference Vassallo P, Matei C, Heston WD, McLachlan SJ, Koutcher JA, Castellino RA (1994) AMI-227-enhanced MR lymphography: usefulness for differentiating reactive from tumor-bearing lymph nodes. Radiology 193:501–506PubMed Vassallo P, Matei C, Heston WD, McLachlan SJ, Koutcher JA, Castellino RA (1994) AMI-227-enhanced MR lymphography: usefulness for differentiating reactive from tumor-bearing lymph nodes. Radiology 193:501–506PubMed
15.
go back to reference Guimaraes R, Clement O, Bittoun J, Carnot F, Frija G (1994) MR lymphography with superparamagnetic iron nanoparticles in rats: pathologic basis for contrast enhancement. Am J Roentgenol 162:201–207 Guimaraes R, Clement O, Bittoun J, Carnot F, Frija G (1994) MR lymphography with superparamagnetic iron nanoparticles in rats: pathologic basis for contrast enhancement. Am J Roentgenol 162:201–207
16.
go back to reference Hayashi S, Miyazaki M (1999) Thoracic duct: visualization at nonenhanced MR lymphography—initial experience. Radiology 212:598–600PubMed Hayashi S, Miyazaki M (1999) Thoracic duct: visualization at nonenhanced MR lymphography—initial experience. Radiology 212:598–600PubMed
17.
go back to reference Harika L, Weissleder R, Poss K, Zimmer C, Papisov MI, Brady TJ (1995) MR lymphography with a lymphotropic T1-type MR contrast agent: Gd-DTPA-PGM. Magn Reson Med 33:88–92PubMed Harika L, Weissleder R, Poss K, Zimmer C, Papisov MI, Brady TJ (1995) MR lymphography with a lymphotropic T1-type MR contrast agent: Gd-DTPA-PGM. Magn Reson Med 33:88–92PubMed
18.
go back to reference Staatz G, Nolte-Ernsting CC, Adam GB et al (2001) Interstitial T1-weighted MR lymphography: lipophilic perfluorinated gadolinium chelates in pigs. Radiology 220:129–134PubMed Staatz G, Nolte-Ernsting CC, Adam GB et al (2001) Interstitial T1-weighted MR lymphography: lipophilic perfluorinated gadolinium chelates in pigs. Radiology 220:129–134PubMed
19.
go back to reference Misselwitz B, Schmitt-Willich H, Michaelis M, Oellinger JJ (2002) Interstitial magnetic resonance lymphography using a polymeric t1 contrast agent: initial experience with Gadomer-17. Invest Radiol 37:146–151CrossRefPubMed Misselwitz B, Schmitt-Willich H, Michaelis M, Oellinger JJ (2002) Interstitial magnetic resonance lymphography using a polymeric t1 contrast agent: initial experience with Gadomer-17. Invest Radiol 37:146–151CrossRefPubMed
20.
go back to reference Ruehm SG, Corot C, Debatin JF (2001) Interstitial MR lymphography with a conventional extracellular gadolinium-based agent: assessment in rabbits. Radiology 218:664–669PubMed Ruehm SG, Corot C, Debatin JF (2001) Interstitial MR lymphography with a conventional extracellular gadolinium-based agent: assessment in rabbits. Radiology 218:664–669PubMed
21.
go back to reference Bellin MF, Vasile M, Morel-Precetti S (2003) Currently used non-specific extracellular MR contrast media. Eur Radiol 12:2688–2698 Bellin MF, Vasile M, Morel-Precetti S (2003) Currently used non-specific extracellular MR contrast media. Eur Radiol 12:2688–2698
22.
go back to reference Ruehm SG, Schroeder T, Debatin JF (2001) Interstitial MR lymphography with gadoterate meglumine: initial experience in humans. Radiology 220:816–821PubMed Ruehm SG, Schroeder T, Debatin JF (2001) Interstitial MR lymphography with gadoterate meglumine: initial experience in humans. Radiology 220:816–821PubMed
23.
go back to reference Moskovic E, Fernando I, Blake P, Parsons C (1991) Lymphography—current role in oncology. Br J Radiol 64:422–427PubMed Moskovic E, Fernando I, Blake P, Parsons C (1991) Lymphography—current role in oncology. Br J Radiol 64:422–427PubMed
24.
go back to reference Cserni G (1999) Metastases in axillary sentinel lymph nodes in breast cancer as detected by intensive histopathological work up. J Clin Pathol 52:922–924PubMed Cserni G (1999) Metastases in axillary sentinel lymph nodes in breast cancer as detected by intensive histopathological work up. J Clin Pathol 52:922–924PubMed
25.
go back to reference Dowlatshahi K, Fan M, Snider HC, HabibFA (1997) Lymph node micrometastases from breast carcinoma: reviewing the dilemma. Cancer 80:1188–1197CrossRefPubMed Dowlatshahi K, Fan M, Snider HC, HabibFA (1997) Lymph node micrometastases from breast carcinoma: reviewing the dilemma. Cancer 80:1188–1197CrossRefPubMed
26.
go back to reference Uematsu T, Sano M, Homma K (2001) In vitro high-resolution helical CT of small axillary lymph nodes in patients with breast cancer: correlation of CT and histology. Am J Roentgenol 176:1069–1074 Uematsu T, Sano M, Homma K (2001) In vitro high-resolution helical CT of small axillary lymph nodes in patients with breast cancer: correlation of CT and histology. Am J Roentgenol 176:1069–1074
27.
go back to reference Mumtaz H, Hall-Craggs MA, Davidson T et al (1997) Staging of symptomatic primary breast cancer with MR imaging. Am J Roentgenol 169:417–424 Mumtaz H, Hall-Craggs MA, Davidson T et al (1997) Staging of symptomatic primary breast cancer with MR imaging. Am J Roentgenol 169:417–424
28.
go back to reference Konyer NB, Ramsay EA, Bronskill MJ, Plewes DB (2002) Comparison of MR imaging breast coils. Radiology 222:830–834PubMed Konyer NB, Ramsay EA, Bronskill MJ, Plewes DB (2002) Comparison of MR imaging breast coils. Radiology 222:830–834PubMed
29.
go back to reference Luciani A, Dao TH, Lapeyre M et al (2004) Simultaneous bilateral breast and high-resolution axillary MRI of patients with breast cancer: preliminary results. Am J Roentgenol (in press) Luciani A, Dao TH, Lapeyre M et al (2004) Simultaneous bilateral breast and high-resolution axillary MRI of patients with breast cancer: preliminary results. Am J Roentgenol (in press)
30.
go back to reference Morton DL, Wen DR, Wong JH et al (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127:392–399PubMed Morton DL, Wen DR, Wong JH et al (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127:392–399PubMed
31.
go back to reference Krag DN (1999) The sentinel node for staging breast cancer: current review. Breast Cancer 6:233–236PubMed Krag DN (1999) The sentinel node for staging breast cancer: current review. Breast Cancer 6:233–236PubMed
32.
go back to reference Whitworth P, McMasters KM, Tafra L, Edwards MJ (2000) State-of-the-art lymph node staging for breast cancer in the year 2000. Am J Surg 180:262–267CrossRefPubMed Whitworth P, McMasters KM, Tafra L, Edwards MJ (2000) State-of-the-art lymph node staging for breast cancer in the year 2000. Am J Surg 180:262–267CrossRefPubMed
33.
go back to reference Wisner ER, Katzberg RW, Koblik PD et al (1995) Indirect computed tomography lymphography of subdiaphragmatic lymph nodes using iodinated nanoparticles in normal dogs. Acad Radiol 2:405–412PubMed Wisner ER, Katzberg RW, Koblik PD et al (1995) Indirect computed tomography lymphography of subdiaphragmatic lymph nodes using iodinated nanoparticles in normal dogs. Acad Radiol 2:405–412PubMed
34.
go back to reference McIntire GL, Bacon ER, Illig KJ et al (2000) Time course of nodal enhancement with CT X-ray nanoparticle contrast agents: effect of particle size and chemical structure. Invest Radiol 35:91–96CrossRefPubMed McIntire GL, Bacon ER, Illig KJ et al (2000) Time course of nodal enhancement with CT X-ray nanoparticle contrast agents: effect of particle size and chemical structure. Invest Radiol 35:91–96CrossRefPubMed
35.
go back to reference Bellin MF, Roy C, Kinkel K et al (1998) Lymph node metastases: safety and effectiveness of MR imaging with ultrasmall superparamagnetic iron oxide particles—initial clinical experience. Radiology 207:799–808PubMed Bellin MF, Roy C, Kinkel K et al (1998) Lymph node metastases: safety and effectiveness of MR imaging with ultrasmall superparamagnetic iron oxide particles—initial clinical experience. Radiology 207:799–808PubMed
36.
go back to reference Sigal R, Vogl T, Casselman J et al (2002) 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 12:1104–1113CrossRefPubMed Sigal R, Vogl T, Casselman J et al (2002) 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 12:1104–1113CrossRefPubMed
37.
go back to reference Harisinghani MG, Barentsz J, Hahn PF et al (2003) Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 348:2491–2499CrossRefPubMed Harisinghani MG, Barentsz J, Hahn PF et al (2003) Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 348:2491–2499CrossRefPubMed
38.
go back to reference Michel SC, Keller TM, Frohlich JM et al (2002) Preoperative breast cancer staging: MR imaging of the axilla with ultrasmall superparamagnetic iron oxide enhancement. Radiology 225:527–536PubMed Michel SC, Keller TM, Frohlich JM et al (2002) Preoperative breast cancer staging: MR imaging of the axilla with ultrasmall superparamagnetic iron oxide enhancement. Radiology 225:527–536PubMed
39.
go back to reference Harisinghani MG, Saini S, Slater GJ, Schnall MD, Rifkin MD (1997) MR imaging of pelvic lymph nodes in primary pelvic carcinoma with ultrasmall superparamagnetic iron oxide (Combidex): preliminary observations. J Magn Reson Imaging 7:161–163PubMed Harisinghani MG, Saini S, Slater GJ, Schnall MD, Rifkin MD (1997) MR imaging of pelvic lymph nodes in primary pelvic carcinoma with ultrasmall superparamagnetic iron oxide (Combidex): preliminary observations. J Magn Reson Imaging 7:161–163PubMed
40.
go back to reference Williams AD, Cousins C, Soutter WP et al (2001) Detection of pelvic lymph node metastases in gynecologic malignancy: a comparison of CT, MR imaging, and positron emission tomography. Am J Roentgenol 177:343–348 Williams AD, Cousins C, Soutter WP et al (2001) Detection of pelvic lymph node metastases in gynecologic malignancy: a comparison of CT, MR imaging, and positron emission tomography. Am J Roentgenol 177:343–348
41.
go back to reference Hong SP, Hahn JS, Lee JD, Bae SW, Youn MJ (2003) 18F-Fluorodeoxyglucose-positron emission tomography in the staging of malignant lymphoma compared with CT and 67 Ga Scan. Yonsei Med J 44:779–786PubMed Hong SP, Hahn JS, Lee JD, Bae SW, Youn MJ (2003) 18F-Fluorodeoxyglucose-positron emission tomography in the staging of malignant lymphoma compared with CT and 67 Ga Scan. Yonsei Med J 44:779–786PubMed
42.
go back to reference Friedberg JW, Chengazi V (2003) PET scans in the staging of lymphoma: current status. Oncologist 8:438–447PubMed Friedberg JW, Chengazi V (2003) PET scans in the staging of lymphoma: current status. Oncologist 8:438–447PubMed
43.
go back to reference Barranger E, Grahek D, Antoine M, Montravers F, Talbot JN, Uzan S (2003) Evaluation of fluorodeoxyglucose positron emission tomography in the detection of axillary lymph node metastases in patients with early-stage breast cancer. Ann Surg Oncol 10:622–627CrossRefPubMed Barranger E, Grahek D, Antoine M, Montravers F, Talbot JN, Uzan S (2003) Evaluation of fluorodeoxyglucose positron emission tomography in the detection of axillary lymph node metastases in patients with early-stage breast cancer. Ann Surg Oncol 10:622–627CrossRefPubMed
44.
go back to reference Eubank WB, Mankoff DA, Takasugi J et al (2001) 18fluorodeoxyglucose positron emission tomography to detect mediastinal or internal mammary metastases in breast cancer. J Clin Oncol 19:3516–3523PubMed Eubank WB, Mankoff DA, Takasugi J et al (2001) 18fluorodeoxyglucose positron emission tomography to detect mediastinal or internal mammary metastases in breast cancer. J Clin Oncol 19:3516–3523PubMed
45.
go back to reference Lin WC, Hung YC, Yeh LS, Kao CH, Yen RF, Shen YY (2003) Usefulness of (18)F-fluorodeoxyglucose positron emission tomography to detect para-aortic lymph nodal metastasis in advanced cervical cancer with negative computed tomography findings. Gynecol Oncol 89:73–76CrossRefPubMed Lin WC, Hung YC, Yeh LS, Kao CH, Yen RF, Shen YY (2003) Usefulness of (18)F-fluorodeoxyglucose positron emission tomography to detect para-aortic lymph nodal metastasis in advanced cervical cancer with negative computed tomography findings. Gynecol Oncol 89:73–76CrossRefPubMed
46.
go back to reference Antoch G, Stattaus J, Nemat AT et al (2003) Non-small cell lung cancer: dual-modality PET/CT in preoperative staging. Radiology 229:526–533PubMed Antoch G, Stattaus J, Nemat AT et al (2003) Non-small cell lung cancer: dual-modality PET/CT in preoperative staging. Radiology 229:526–533PubMed
47.
go back to reference Picchio M, Messa C, Landoni C et al (2003) Value of [11C]choline-positron emission tomography for re-staging prostate cancer: a comparison with [18F]fluorodeoxyglucose-positron emission tomography. J Urol 169:1337–1340PubMed Picchio M, Messa C, Landoni C et al (2003) Value of [11C]choline-positron emission tomography for re-staging prostate cancer: a comparison with [18F]fluorodeoxyglucose-positron emission tomography. J Urol 169:1337–1340PubMed
48.
go back to reference Vassallo P, Wernecke K, Roos N, Peters PE (1992) Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology 183:215–220PubMed Vassallo P, Wernecke K, Roos N, Peters PE (1992) Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology 183:215–220PubMed
49.
go back to reference Tregnaghi A, De Candia A, Calderone M et al (1997) Ultrasonographic evaluation of superficial lymph node metastases in melanoma. Eur J Radiol 24:216–221CrossRefPubMed Tregnaghi A, De Candia A, Calderone M et al (1997) Ultrasonographic evaluation of superficial lymph node metastases in melanoma. Eur J Radiol 24:216–221CrossRefPubMed
50.
go back to reference Steinkamp HJ, Wissgott C, Rademaker J, Felix R (2002) Current status of power Doppler and color Doppler sonography in the differential diagnosis of lymph node lesions. Eur Radiol 12:1785–1793CrossRefPubMed Steinkamp HJ, Wissgott C, Rademaker J, Felix R (2002) Current status of power Doppler and color Doppler sonography in the differential diagnosis of lymph node lesions. Eur Radiol 12:1785–1793CrossRefPubMed
51.
go back to reference Moritz JD, Ludwig A, Oestmann JW (2000) Contrast-enhanced color Doppler sonography for evaluation of enlarged cervical lymph nodes in head and neck tumors. Am J Roentgenol 174:1279–1284 Moritz JD, Ludwig A, Oestmann JW (2000) Contrast-enhanced color Doppler sonography for evaluation of enlarged cervical lymph nodes in head and neck tumors. Am J Roentgenol 174:1279–1284
52.
go back to reference Yang WT, Metreweli C, Lam PK, Chang J (2001) Benign and malignant breast masses and axillary nodes: evaluation with echo-enhanced color power Doppler US. Radiology 220:795–802PubMed Yang WT, Metreweli C, Lam PK, Chang J (2001) Benign and malignant breast masses and axillary nodes: evaluation with echo-enhanced color power Doppler US. Radiology 220:795–802PubMed
53.
go back to reference Schmid-Wendtner MH, Partscht K, Korting HC, Volkenandt M (2002) Improved differentiation of benign and malignant lymphadenopathy in patients with cutaneous melanoma by contrast-enhanced color Doppler sonography. Arch Dermatol 138:491–497CrossRefPubMed Schmid-Wendtner MH, Partscht K, Korting HC, Volkenandt M (2002) Improved differentiation of benign and malignant lymphadenopathy in patients with cutaneous melanoma by contrast-enhanced color Doppler sonography. Arch Dermatol 138:491–497CrossRefPubMed
54.
go back to reference Wisner ER, Ferrara KW, Short RE, Ottoboni TB, Gabe JD, Patel D (2003) Sentinel node detection using contrast-enhanced power Doppler ultrasound lymphography. Invest Radiol 38:358–365CrossRefPubMed Wisner ER, Ferrara KW, Short RE, Ottoboni TB, Gabe JD, Patel D (2003) Sentinel node detection using contrast-enhanced power Doppler ultrasound lymphography. Invest Radiol 38:358–365CrossRefPubMed
Metadata
Title
Imaging the lymphatic system: possibilities and clinical applications
Authors
Olivier Clément
Alain Luciani
Publication date
01-08-2004
Publisher
Springer-Verlag
Published in
European Radiology / Issue 8/2004
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-004-2265-9

Other articles of this Issue 8/2004

European Radiology 8/2004 Go to the issue

Book Reviews

Recent literature