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J Reconstr Microsurg 2024; 40(03): 177-185
DOI: 10.1055/a-2102-0261
Original Article

Association between Bioimpedance Spectroscopy and Magnetic Resonance Lymphangiography in the Diagnosis and Assessment of Lymphedema

Kaamya Varagur 
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Anup S. Shetty
2   Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, Missouri
,
Karim Saoud
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Esther Ochoa
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Rachel Skladman
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Gary B. Skolnick
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Justin M. Sacks
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
,
Joani M. Christensen
1   Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri
› Author Affiliations Funding This study was supported by the Washington University School of Medicine Yearlong Research Scholars Grant from the DeNardo Education & Research Foundation.
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Abstract

Background This study assesses associations between bioimpedance spectroscopy (BIS) and magnetic resonance lymphangiography (MRL) in the staging and assessment of lymphedema.

Methods Adults who received MRL and BIS between 2020 and 2022 were included. We collected fluid, fat, and lymphedema severity ratings, and measured fluid stripe thickness, subcutaneous fat width, and lymphatic diameter on MRL. BIS lymphedema index (L-Dex) scores were collected from patient charts. We assessed sensitivity and specificity of L-Dex scores to detect MRL-identified lymphedema, and examined associations between L-Dex scores and MRL imaging measures.

Results Forty-eight limbs across 40 patients were included. L-Dex scores had 72.5% sensitivity and 87.5% specificity for detecting MRL-defined lymphedema, with a 96.7% estimated positive predictive value and 38.9% negative predictive value. L-Dex scores were associated with MRL fluid and fat content scores (p ≤ 0.05), and lymphedema severity (p = 0.01), with better discrimination between fluid than fat content levels on pairwise analysis, and poor discrimination between adjacent severity levels. L-Dex scores were correlated with distal and proximal limb fluid stripe thickness (distal: rho = 0.57, p < 0.01; proximal: rho = 0.58, p < 0.01), partially correlated with distal subcutaneous fat thickness when accounting for body mass index (rho = 0.34, p = 0.02), and were not correlated with lymphatic diameter (p = 0.25).

Conclusion L-Dex scores have high sensitivity, specificity, and positive predictive value for the identification of MRL-detected lymphedema. L-Dex has difficulty distinguishing between adjacent severity levels of lymphedema and a high false negative rate, explained in part by reduced discrimination between levels of fat accumulation.

Keywords

MR lymphangiography - bioimpedance spectroscopy - lymphedema - diagnostic imaging - lymphedema staging

Institutional Review Board Approval

This study was approved by the Washington University School of Medicine Institutional Review Board (IRB ID: 202209002).


Presentations

Presented at the Plastic Surgery Research Council (PSRC) Meeting, April 13–16, 2023, Cleveland, OH.


Financial Disclosure

K.V., K.S., R.S., E.O., A.S.S., and J.M.C. have nothing to disclose. J.M.S. is a co-founder and equity holder of LifeSprout, and a consultant for 3M. None of the authors has a financial interest in any of the products, devices, or drugs mentioned in this manuscript. No funding was received for this article.




Publication History

Received: 04 March 2023

Accepted: 23 May 2023

Accepted Manuscript online:
26 May 2023

Article published online:
05 July 2023

© 2023. Thieme. All rights reserved.

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  • References

  • 1 Grada AA, Phillips TJ. Lymphedema: pathophysiology and clinical manifestations. J Am Acad Dermatol 2017; 77 (06) 1009-1020
    CrossrefPubMedGoogle Scholar
  • 2 Rockson SG, Rivera KK. Estimating the population burden of lymphedema. Ann N Y Acad Sci 2008; 1131: 147-154
    CrossrefPubMedGoogle Scholar
  • 3 Földi M, Földi E, Strössenreuther RHK, Kubik S, Asmussen PD, Biotext LLC. Földi's Textbook of Lymphology: For Physicians and Lymphedema Therapists. Amsterdam, Netherlands: Urban & Fischer; 2012
    Google Scholar
  • 4 Greene AK, Slavin SA, Brorson H. SpringerLink. Lymphedema: Presentation, Diagnosis, and Treatment. 1st ed.. Springer International Publishing: Switzerland: Springer; 2015
    CrossrefGoogle Scholar
  • 5 Hayes S, Di Sipio T, Rye S. et al. Prevalence and prognostic significance of secondary lymphedema following breast cancer. Lymphat Res Biol 2011; 9 (03) 135-141
    CrossrefPubMedGoogle Scholar
  • 6 Hidding JT, Viehoff PB, Beurskens CH, van Laarhoven HW, Nijhuis-van der Sanden MW, van der Wees PJ. Measurement properties of instruments for measuring of lymphedema: systematic review. Phys Ther 2016; 96 (12) 1965-1981
    CrossrefPubMedGoogle Scholar
  • 7 Ward LC, Koelmeyer LA, Moloney E. Staging breast cancer-related lymphedema with bioimpedance spectroscopy. Lymphat Res Biol 2022; 20 (04) 398-408
    CrossrefPubMedGoogle Scholar
  • 8 Forte AJ, Huayllani MT, Boczar D. et al. Use of bioimpedance spectroscopy for prospective surveillance and early diagnosis of breast cancer-related lymphedema. Breast Dis 2021; 40 (02) 85-93
    CrossrefPubMedGoogle Scholar
  • 9 Sutherland A, Wagner JL, Korentager S. et al. Is bioimpedance spectroscopy a useful tool for objectively assessing lymphovenous bypass surgical outcomes in breast cancer-related lymphedema?. Breast Cancer Res Treat 2021; 186 (01) 1-6
    CrossrefPubMedGoogle Scholar
  • 10 Ridner SH, Dietrich MS, Cowher MS. et al. A randomized trial evaluating bioimpedance spectroscopy versus tape measurement for the prevention of lymphedema following treatment for breast cancer: interim analysis. Ann Surg Oncol 2019; 26 (10) 3250-3259
    CrossrefPubMedGoogle Scholar
  • 11 Coroneos CJ, Wong FC, DeSnyder SM, Shaitelman SF, Schaverien MV. Correlation of L-Dex bioimpedance spectroscopy with limb volume and lymphatic function in lymphedema. Lymphat Res Biol 2019; 17 (03) 301-307
    CrossrefPubMedGoogle Scholar
  • 12 Neligan PC, Kung TA, Maki JH. MR lymphangiography in the treatment of lymphedema. J Surg Oncol 2017; 115 (01) 18-22
    CrossrefPubMedGoogle Scholar
  • 13 Bae JS, Yoo RE, Choi SH. et al. Evaluation of lymphedema in upper extremities by MR lymphangiography: comparison with lymphoscintigraphy. Magn Reson Imaging 2018; 49: 63-70
    CrossrefPubMedGoogle Scholar
  • 14 Notohamiprodjo M, Weiss M, Baumeister RG. et al. MR lymphangiography at 3.0 T: correlation with lymphoscintigraphy. Radiology 2012; 264 (01) 78-87
    CrossrefPubMedGoogle Scholar
  • 15 Kim HB, Jung SS, Cho MJ. et al. Comparative analysis of preoperative high frequency color Doppler ultrasound versus MR lymphangiography versus ICG lymphography of lymphatic vessels in lymphovenous anastomosis. J Reconstr Microsurg 2023; 39 (02) 92-101
    Article in Thieme ConnectPubMedGoogle Scholar
  • 16 Yasunaga Y, Kinjo Y, Nakajima Y. et al. Impact of magnetic resonance lymphography on lymphaticolvenular anastomosis for lower-limb lymphedema. J Reconstr Microsurg 2022; 38 (02) 121-128
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Guerrini S, Gentili F, Mazzei FG, Gennaro P, Volterrani L, Mazzei MA. Magnetic resonance lymphangiography: with or without contrast?. Diagn Interv Radiol 2020; 26 (06) 587-595
    CrossrefPubMedGoogle Scholar
  • 18 Ward LC, Czerniec S, Kilbreath SL. Operational equivalence of bioimpedance indices and perometry for the assessment of unilateral arm lymphedema. Lymphat Res Biol 2009; 7 (02) 81-85
    CrossrefPubMedGoogle Scholar
  • 19 Barrio AV, Eaton A, Frazier TG. A prospective validation study of bioimpedance with volume displacement in early-stage breast cancer patients at risk for lymphedema. Ann Surg Oncol 2015; 22 (0 3, Suppl 3): S370-S375
    CrossrefPubMedGoogle Scholar
  • 20 Fu MR, Cleland CM, Guth AA. et al. L-Dex ratio in detecting breast cancer-related lymphedema: reliability, sensitivity, and specificity. Lymphology 2013; 46 (02) 85-96
    PubMedGoogle Scholar
  • 21 ImpediMed. L-Dex® Score. Accessed June 10, 2023 at: https://www.impedimed.com/resources/l-dex-score/#:~:text=The%20L%2DDex%20score%20represents,compared%20to%20an%20unaffected%20limb
    PubMedGoogle Scholar
  • 22 Dayan JH, Wiser I, Verma R. et al. Regional patterns of fluid and fat accumulation in patients with lower extremity lymphedema using magnetic resonance angiography. Plast Reconstr Surg 2020; 145 (02) 555-563
    CrossrefPubMedGoogle Scholar
  • 23 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2021 . Accessed June 10, 2023 at: https://www.R-Project.Org/
    PubMedGoogle Scholar
  • 24 Power M, Fell G, Wright M. Principles for high-quality, high-value testing. Evid Based Med 2013; 18 (01) 5-10
    CrossrefPubMedGoogle Scholar
  • 25 DiSipio T, Rye S, Newman B, Hayes S. Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol 2013; 14 (06) 500-515
    CrossrefPubMedGoogle Scholar
  • 26 Hayes SC, Janda M, Ward LC. et al. Lymphedema following gynecological cancer: results from a prospective, longitudinal cohort study on prevalence, incidence and risk factors. Gynecol Oncol 2017; 146 (03) 623-629
    CrossrefPubMedGoogle Scholar
  • 27 Ward L, Kilbreath S, Cornish B. Bioelectrical impedance analysis for early detection of lymphedema. . In: Weissleder H, Schuchhardt C. eds. Lymphedema Diagnosis and Therapy. Germany: Viavital Verlag GmbH; 2008: 502-517
    Google Scholar
  • 28 Forte AJ, Huayllani MT, Boczar D. et al. Bioimpedance spectroscopy for assessment of breast cancer-related lymphedema: a systematic review. Plast Surg Nurs 2020; 40 (02) 86-90
    CrossrefPubMedGoogle Scholar
  • 29 Rockson SG. Advances in lymphedema. Circ Res 2021; 128 (12) 2003-2016
    CrossrefPubMedGoogle Scholar
  • 30 Suehiro K, Morikage N, Harada T. et al. Application of the L-Dex score for the assessment of bilateral leg edema. Lymphat Res Biol 2018; 16 (01) 65-68
    CrossrefPubMedGoogle Scholar
  • 31 Son WC, Kwon JG, Hong JP. et al. Clinical utility of bioelectrical impedance analysis parameters for evaluating patients with lower limb lymphedema after lymphovenous anastomosis. J Reconstr Microsurg 2023; 39 (03) 171-178
    Article in Thieme ConnectPubMedGoogle Scholar
  • 32 Laidley A, Anglin B. The impact of L-Dex(®) measurements in assessing breast cancer-related lymphedema as part of routine clinical practice. Front Oncol 2016; 6: 192
    CrossrefPubMedGoogle Scholar
  • 33 Ward LC. Bioelectrical impedance analysis: proven utility in lymphedema risk assessment and therapeutic monitoring. Lymphat Res Biol 2006; 4 (01) 51-56
    CrossrefPubMedGoogle Scholar
  • 34 Dylke ES, Schembri GP, Bailey DL. et al. Diagnosis of upper limb lymphedema: development of an evidence-based approach. Acta Oncol 2016; 55 (12) 1477-1483
    CrossrefPubMedGoogle Scholar
  • 35 Svensson BJ, Dylke ES, Ward LC, Kilbreath SL. Segmental impedance thresholds for early detection of unilateral upper limb swelling. Lymphat Res Biol 2015; 13 (04) 253-259
    CrossrefPubMedGoogle Scholar
  • 36 Kim G, Adondakis M, Smith MP, Singhal D, Tsai LL. Rate of incidental edema in the contralateral arm of patients with unilateral postsurgical secondary upper extremity lymphedema. Lymphat Res Biol 2023; 21 (02) 111-117
    CrossrefPubMedGoogle Scholar