Lymphoscintigraphy versus Indocyanine Green Lymphography—Which Should Be the Gold Standard for Lymphedema Imaging?
Abstract
:1. Introduction
2. Results
3. Discussion
4. Methods
4.1. Patient Population and Study Design
4.2. Indocyanine Green Lymphography
4.3. Lymphoscintigraphy
4.4. Data Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Executive, C. The Diagnosis and Treatment of Peripheral Lymphedema: 2016 Consensus Document of the International Society of Lymphology. Lymphology 2016, 49, 170–184. [Google Scholar]
- Partsch, H. Assessment of abnormal lymph drainage for the diagnosis of lymphedema by isotopic lymphangiography and by indirect lymphography. Clin. Dermatol. 1995, 13, 445–450. [Google Scholar] [CrossRef]
- Weissleder, H.; Weissleder, R. Lymphedema: Evaluation of qualitative and quantitative lymphoscintigraphy in 238 patients. Radiology 1988, 167, 729–735. [Google Scholar] [CrossRef] [PubMed]
- Ogata, F.; Azuma, R.; Kikuchi, M.; Koshima, I.; Morimoto, Y. Novel lymphography using indocyanine green dye for near-infrared fluorescence labeling. Ann. Plast. Surg. 2007, 58, 652–655. [Google Scholar] [CrossRef] [PubMed]
- Bae, J.S.; Yoo, R.E.; Choi, S.H.; Park, S.O.; Chang, H.; Suh, M.; Cheon, G.J. Evaluation of lymphedema in upper extremities by MR lymphangiography: Comparison with lymphoscintigraphy. Magn. Reson. Imaging 2018, 49, 63–70. [Google Scholar] [CrossRef]
- Mazzei, F.G.; Gentili, F.; Guerrini, S.; Cioffi Squitieri, N.; Guerrieri, D.; Gennaro, P.; Scialpi, M.; Volterrani, L.; Mazzei, M.A. MR Lymphangiography: A Practical Guide to Perform It and a Brief Review of the Literature from a Technical Point of View. BioMed Res. Int. 2017, 2017, 2598358. [Google Scholar] [CrossRef]
- Cellina, M.; Oliva, G.; Menozzi, A.; Soresina, M.; Martinenghi, C.; Gibelli, D. Non-contrast Magnetic Resonance Lymphangiography: An emerging technique for the study of lymphedema. Clin. Imaging 2019, 53, 126–133. [Google Scholar] [CrossRef]
- Guerrini, S.; Gentili, F.; Mazzei, F.G.; Gennaro, P.; Volterrani, L.; Mazzei, M.A. Magnetic resonance lymphangiography: With or without contrast? Diagn Interv. Radiol. 2020, 26, 587–595. [Google Scholar] [CrossRef] [PubMed]
- Ogata, F.; Narushima, M.; Mihara, M.; Azuma, R.; Morimoto, Y.; Koshima, I. Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema. Ann. Plast. Surg. 2007, 59, 180–184. [Google Scholar] [CrossRef]
- Mihara, M.; Hara, H.; Narushima, M.; Todokoro, T.; Iida, T.; Ohtsu, H.; Murai, N.; Koshima, I. Indocyanine green lymphography is superior to lymphoscintigraphy in imaging diagnosis of secondary lymphedema of the lower limbs. J. Vasc. Surg. Venous Lymphat. Disord. 2013, 1, 194–201. [Google Scholar] [CrossRef]
- Yoon, J.A.; Shin, M.J.; Kim, J.H. Indocyanine Green Lymphography and Lymphoscintigraphy Severity Stage Showed Strong Correlation in Lower Limb Lymphedema. Lymphat. Res. Biol. 2021, 19, 80–85. [Google Scholar] [CrossRef]
- Yoon, J.A.; Shin, M.J.; Shin, Y.B.; Kim, K.; Park, H.; Kang, T.; Kong, I.J.; Kim, H.; Park, M.S.; Kim, J.H. Correlation of ICG lymphography and lymphoscintigraphy severity stage in secondary upper limb lymphedema. J. Plast. Reconstr. Aesthet. Surg. 2020, 73, 1982–1988. [Google Scholar] [CrossRef]
- Polomska, A.K.; Proulx, S.T. Imaging technology of the lymphatic system. Adv. Drug Deliv. Rev. 2021, 170, 294–311. [Google Scholar] [CrossRef]
- Sadeghi, R.; Forghani, M.N.; Memar, B.; Rajabi Mashhadi, M.T.; Dabbagh Kakhki, V.R.; Abdollahi, A.; Zakavi, S.R. How long the lymphoscintigraphy imaging should be continued for sentinel lymph node mapping? Ann. Nucl. Med. 2009, 23, 507–510. [Google Scholar] [CrossRef]
- Villa, G.; Campisi, C.C.; Ryan, M.; Boccardo, F.; Di Summa, P.; Frascio, M.; Sambuceti, G.; Campisi, C. Procedural Recommendations for Lymphoscintigraphy in the Diagnosis of Peripheral Lymphedema: The Genoa Protocol. Nucl. Med. Mol. Imaging 2019, 53, 47–56. [Google Scholar] [CrossRef]
- Gloviczki, P.; Calcagno, D.; Schirger, A.; Pairolero, P.C.; Cherry, K.J.; Hallett, J.W.; Wahner, H.W. Noninvasive evaluation of the swollen extremity: Experiences with 190 lymphoscintigraphic examinations. J. Vasc. Surg. 1989, 9, 683–689. [Google Scholar] [CrossRef]
- Szuba, A.; Shin, W.S.; Strauss, H.W.; Rockson, S. The third circulation: Radionuclide lymphoscintigraphy in the evaluation of lymphedema. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2003, 44, 43–57. [Google Scholar]
- Chen, W.F.; McNurlen, M.; Ding, J.; Bowen, M. Vascularized lymph vessel transfer for extremity lymphedema-is transfer of lymph node still necessary? Int. Microsurg. J. 2019, 3, 1. [Google Scholar] [CrossRef]
- Chen, W.F.; Bowen, M.; Ding, J.J.I.M.J. Immediate limb compression following supermicrosurgical lymphaticovenular anastomosis–is it helpful or harmful? Int. Microsurg. J. 2018, 2, 1. [Google Scholar] [CrossRef]
- Imai, H.; Yoshida, S.; Mese, T.; Roh, S.; Fujita, A.; Sasaki, A.; Nagamatsu, S.; Koshima, I. Correlation between Lymphatic Surgery Outcome and Lymphatic Image-Staging or Clinical Severity in Patients with Lymphedema. J. Clin. Med. 2022, 11, 4979. [Google Scholar] [CrossRef]
- Liu, M.; Liu, S.; Zhao, Q.; Cui, Y.; Chen, J.; Wang, S. Using the Indocyanine Green (ICG) Lymphography to Screen Breast Cancer Patients at High Risk for Lymphedema. Diagnostics 2022, 12, 983. [Google Scholar] [CrossRef]
- 22. Early Detection of Breast Cancer-Related Lymphedema: Accuracy of Indocyanine Green Lymphography Compared with Bioimpedance Spectroscopy and Subclinical Lymphedema Symptoms. Lymphat. Res. Biol. 2023; ahead of print. [CrossRef]
- Aldrich, M.B.; Rasmussen, J.C.; DeSnyder, S.M.; Woodward, W.A.; Chan, W.; Sevick-Muraca, E.M.; Mittendorf, E.A.; Smith, B.D.; Stauder, M.C.; Strom, E.A.; et al. Prediction of breast cancer-related lymphedema by dermal backflow detected with near-infrared fluorescence lymphatic imaging. Breast Cancer Res. Treat 2022, 195, 33–41. [Google Scholar] [CrossRef]
- Chen, W.F.; Qin, E.S.; Bowen, M.J.; Little, A.S.; Lensing, J.N. Exercise-enhanced ICG lymphography: A fast approach to diagnosis and staging of lymphedema. Int. Microsurg. J. 2021, 5, 2. [Google Scholar] [CrossRef]
- Ebrahim, M.; Savitcheva, I.; Axelsson, R. Reliability of a Scoring System for Qualitative Evaluation of Lymphoscintigraphy of the Lower Extremities. J. Nucl. Med. Technol. 2017, 45, 219–224. [Google Scholar] [CrossRef]
- Akita, S.; Mitsukawa, N.; Kazama, T.; Kuriyama, M.; Kubota, Y.; Omori, N.; Koizumi, T.; Kosaka, K.; Uno, T.; Satoh, K. Comparison of lymphoscintigraphy and indocyanine green lymphography for the diagnosis of extremity lymphoedema. J. Plast. Reconstr. Aesthetic Surg. JPRAS 2013, 66, 792–798. [Google Scholar] [CrossRef]
- The diagnosis and treatment of peripheral lymphedema: 2020 Consensus Document of the International Society of Lymphology. Lymphology 2020, 53, 3–19.
- Unno, N.; Nishiyama, M.; Suzuki, M.; Yamamoto, N.; Inuzuka, K.; Sagara, D.; Tanaka, H.; Konno, H. Quantitative lymph imaging for assessment of lymph function using indocyanine green fluorescence lymphography. Eur. J. Vasc. Endovasc. Surg. 2008, 36, 230–236. [Google Scholar] [CrossRef]
Demographic | Value † |
---|---|
Age (Years) | 49 ± 15.55 |
Sex | |
Male | 5 (22) |
Female | 18 (78) |
BMI (Kg/m2) | 26 ± 5.47 |
Symptoms Location | |
Right Upper Extremity | 2 |
Left Upper Extremity | 1 |
Bilateral Upper Extremity | 1 |
Left Lower Extremity | 7 |
Right Lower Extremity | 3 |
Bilateral Lower Extremity | 11 |
History of Cellulitis | |
Present | 4 (17) |
Absent | 19 (83) |
Age of Onset (Years) | 39 ± 19.23 |
Lymphedema Duration (Years) | 11 ± 11.38 |
Lymphedema Family History | |
Positive | 0 (0) |
Negative | 23 (100) |
Lymphedema Type | |
Primary Lymphedema | 15 (65) |
Secondary Lymphedema | 8 (35) |
Lymphedema Type | Patients | Limbs | Symptomatic Limbs | LSG + | ICG + | p Value | Asymptomatic Limbs | LSG + | ICG + | p Value |
---|---|---|---|---|---|---|---|---|---|---|
Primary | 15 (65%) | 33 (66%) | 25 | 16 (64%) | 25 (100%) | <0.01 | 8 | 1 (12.5%) | 5 (63%) | <0.01 |
Secondary | 8 (35%) | 17 (34%) | 12 | 10 (83%) | 12 (100%) | <0.01 | 5 | 0 (0%) | 3 (60%) | <0.01 |
Total | 23 | 50 | 37 | 26/37 (70%) | 37/37 (100%) | <0.01 | 13 | 1/13 (8%) | 8/13 (62%) | <0.01 |
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Figueroa, B.A.; Lammers, J.D.; Al-Malak, M.; Pandey, S.; Chen, W.F. Lymphoscintigraphy versus Indocyanine Green Lymphography—Which Should Be the Gold Standard for Lymphedema Imaging? Lymphatics 2023, 1, 25-33. https://doi.org/10.3390/lymphatics1010004
Figueroa BA, Lammers JD, Al-Malak M, Pandey S, Chen WF. Lymphoscintigraphy versus Indocyanine Green Lymphography—Which Should Be the Gold Standard for Lymphedema Imaging? Lymphatics. 2023; 1(1):25-33. https://doi.org/10.3390/lymphatics1010004
Chicago/Turabian StyleFigueroa, Brian A., Jacob D. Lammers, Mazen Al-Malak, Sonia Pandey, and Wei F. Chen. 2023. "Lymphoscintigraphy versus Indocyanine Green Lymphography—Which Should Be the Gold Standard for Lymphedema Imaging?" Lymphatics 1, no. 1: 25-33. https://doi.org/10.3390/lymphatics1010004