Exercise-Loaded Indocyanine Green Fluorescence Lymphangiography for Diagnosing Lymphedema

Kumiko Matsumoto; Akira Shinaoka; Kiyoshi Yamada; Yoshihiro Kimata

doi:10.1055/s-0038-1667366

Journal of Reconstructive Microsurgery, Table of Contents

J Reconstr Microsurg 2019; 35(02): 138-144
DOI: 10.1055/s-0038-1667366

Original Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Exercise-Loaded Indocyanine Green Fluorescence Lymphangiography for Diagnosing Lymphedema

Kumiko Matsumoto

¹Department of Plastic and Reconstructive Surgery, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan

,

Akira Shinaoka

¹Department of Plastic and Reconstructive Surgery, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan

²Department of Human Morphology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan

,

Kiyoshi Yamada

³Department of Plastic and Reconstructive Surgery, Okayama University Hospital, Okayama, Japan

,

Yoshihiro Kimata

¹Department of Plastic and Reconstructive Surgery, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan

› Author Affiliations

Abstract

Background Indocyanine green (ICG) fluorescence lymphography (ICGLG) that can visualize the lymphatic vessel and its flow noninvasively and dynamically was developed in 2007. It is frequently used to observe the function and pathway of the lymphatic vessels. ICGLG is simple and easy to perform, and it is useful for understanding the condition of the lymphatic system in real time. However, its protocol is not standardized. In addition, the lymphatic flow is enhanced by an exercise load such as walking. Till now, there is no report of exercise-loaded ICGLG. Therefore, we aimed to shorten the examination time and establish a standard ICGLG protocol.

Methods We examined 63 patients (126 lower limbs) who visited our clinic for lower extremity edema. We observed detailed images of exercise-loaded ICGLG and examined the changes in findings over time in affected legs classified according to the International Society of Lymphedema. After ICG was injected, the participants exercised for 30 minutes. We observed the farthest proximal point where any ICG could be observed and the appearance of dermal backflow (DB), which is a specific finding of lymphedema, every 5 minutes.

Results The proximal migration speed of ICG tended to slow as the disease stage worsened. For all disease stages, after 20 minutes of exercise, the DB appearance rate did not change further. The rates were 0% for legs with stage 0 lymphedema, 50% for legs with stage 1 lymphedema, and 100% for legs with stages 2a and 2b lymphedema.

Conclusion The appropriate exercise duration after ICG injection is 20 minutes. ICGLG is useful for screening for lymphedema.

Keywords

indocyanine green fluorescence lymphography - lymphedema - exercise-loaded

Full Text

References

References
1 Aldrich MB, Guilliod R, Fife CE. , et al. Lymphatic abnormalities in the normal contralateral arms of subjects with breast cancer-related lymphedema as assessed by near-infrared fluorescent imaging. Biomed Opt Express 2012; 3 (06) 1256-1265
2 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 (06) 652-655
3 Unno N, Inuzuka K, Suzuki M. , et al. Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema. J Vasc Surg 2007; 45 (05) 1016-1021
4 Chang DW, Masia J, Garza III R, Skoracki R, Neligan PC. Lymphedema: surgical and medical therapy. Plast Reconstr Surg 2016; 138 (3, Suppl): 209S-218S
5 Maegawa J, Mikami T, Yamamoto Y, Satake T, Kobayashi S. Types of lymphoscintigraphy and indications for lymphaticovenous anastomosis. Microsurgery 2010; 30 (06) 437-442
6 Partsch H. Practical aspects of indirect lymphography and lymphoscintigraphy. Lymphat Res Biol 2003; 1 (01) 71-73 , discussion 73–74
7 Akita S, Mitsukawa N, Kazama T. , et al. Comparison of lymphoscintigraphy and indocyanine green lymphography for the diagnosis of extremity lymphoedema. J Plast Reconstr Aesthet Surg 2013; 66 (06) 792-798
8 Chang DW, Suami H, Skoracki R. A prospective analysis of 100 consecutive lymphovenous bypass cases for treatment of extremity lymphedema. Plast Reconstr Surg 2013; 132 (05) 1305-1314
9 Yamamoto T, Iida T, Matsuda N. , et al. Indocyanine green (ICG)-enhanced lymphography for evaluation of facial lymphoedema. J Plast Reconstr Aesthet Surg 2011; 64 (11) 1541-1544
10 Yamamoto T, Matsuda N, Doi K. , et al. The earliest finding of indocyanine green lymphography in asymptomatic limbs of lower extremity lymphedema patients secondary to cancer treatment: the modified dermal backflow stage and concept of subclinical lymphedema. Plast Reconstr Surg 2011; 128 (04) 314e-321e
11 Unno N, Nishiyama M, Suzuki M. , et al. Quantitative lymph imaging for assessment of lymph function using indocyanine green fluorescence lymphography. Eur J Vasc Endovasc Surg 2008; 36 (02) 230-236
12 Witte CL, Witte MH, Unger EC. , et al. Advances in imaging of lymph flow disorders. Radiographics 2000; 20 (06) 1697-1719
13 Witte CL, Witte MH. Contrasting patterns of lymphatic and blood circulatory disorders. Lymphology 1987; 20 (04) 171-178
14 Tartaglione G, Pagan M, Morese R. , et al. Intradermal lymphoscintigraphy at rest and after exercise: a new technique for the functional assessment of the lymphatic system in patients with lymphoedema. Nucl Med Commun 2010; 31 (06) 547-551
15 Havas E, Parviainen T, Vuorela J, Toivanen J, Nikula T, Vihko V. Lymph flow dynamics in exercising human skeletal muscle as detected by scintography. J Physiol 1997; 504 (Pt 1): 233-239
16 Lane KN, Dolan LB, Worsley D, McKenzie DC. Upper extremity lymphatic function at rest and during exercise in breast cancer survivors with and without lymphedema compared with healthy controls. J Appl Physiol (1985) 2007; 103 (03) 917-925
17 Jensen MR, Simonsen L, Karlsmark T, Bülow J. Lymphoedema of the lower extremities--background, pathophysiology and diagnostic considerations. Clin Physiol Funct Imaging 2010; 30 (06) 389-398
18 Shinaoka A, Koshimune S, Yamada K. , et al. Accelerated lymph flow in early-stage secondary lymphedema detected by indocyanine green fluorescence lymphography. J Reconstr Microsurg 2017; 33 (08) 596-602
19 Yamada K, Shinaoka A, Kimata Y. Three-dimensional imaging of lymphatic system in lymphedema legs using interstitial computed tomography-lymphography. Acta Med Okayama 2017; 71 (02) 171-177
20 International Society of Lymphology. The diagnosis and treatment of peripheral lymphedema: 2013 Consensus Document of the International Society of Lymphology. Lymphology 2013; 46 (01) 1-11
21 Hassanein AH, Maclellan RA, Grant FD, Greene AK. Diagnostic accuracy of lymphoscintigraphy for lymphedema and analysis of false-negative tests. Plast Reconstr Surg Glob Open 2017; 5 (07) e1396
22 Schook CC, Mulliken JB, Fishman SJ, Alomari AI, Grant FD, Greene AK. Differential diagnosis of lower extremity enlargement in pediatric patients referred with a diagnosis of lymphedema. Plast Reconstr Surg 2011; 127 (04) 1571-1581
23 Yamamoto T, Narushima M, Yoshimatsu H. , et al. Indocyanine green velocity: lymph transportation capacity deterioration with progression of lymphedema. Ann Plast Surg 2013; 71 (05) 591-594
24 Baulieu F, Bourgeois P, Maruani A. , et al. Contributions of SPECT/CT imaging to the lymphoscintigraphic investigations of the lower limb lymphedema. Lymphology 2013; 46 (03) 106-119
25 Lohrmann C, Foeldi E, Langer M. Indirect magnetic resonance lymphangiography in patients with lymphedema preliminary results in humans. Eur J Radiol 2006; 59 (03) 401-406
26 Cambria RA, Gloviczki P, Naessens JM, Wahner HW. Noninvasive evaluation of the lymphatic system with lymphoscintigraphy: a prospective, semiquantitative analysis in 386 extremities. J Vasc Surg 1993; 18 (05) 773-782