J Reconstr Microsurg 2023; 39(02): 102-110
DOI: 10.1055/s-0042-1750824
Original Article

The Use of Ultrasound Imaging for Upper Extremity Lymphedema after Breast Cancer: A Systematic Review

Elena Canales-Lachén
1   Department of Radiology, University Hospital Ramón y Cajal, Madrid, Spain
,
Ángel Asunsolo
2   Department of Surgery, Medical and Social Science, Faculty of Medicine and Health Sciences, University of Alcalá, Alcalá de Henares, Madrid, Spain
3   Ramón y Cajal Health Research Institute (IRYCIS), Madrid, Spain
,
Oscar J. Manrique
4   Deparment of Plastic Surgery, University of Rochester Medical Center, Rochester, New York
,
Javier Blázquez
1   Department of Radiology, University Hospital Ramón y Cajal, Madrid, Spain
3   Ramón y Cajal Health Research Institute (IRYCIS), Madrid, Spain
,
Purificación Holguín
5   Department of Plastic Surgery, University Hospital Getafe, Madrid, Spain
,
2   Department of Surgery, Medical and Social Science, Faculty of Medicine and Health Sciences, University of Alcalá, Alcalá de Henares, Madrid, Spain
3   Ramón y Cajal Health Research Institute (IRYCIS), Madrid, Spain
5   Department of Plastic Surgery, University Hospital Getafe, Madrid, Spain
6   Department of Plastic, Hand and Reconstructive Surgery, BG Trauma Center Frankfurt am Main, Academic Hospital of the Goethe University Frankfurt am Main, Frankfurt am Main, Germany
› Institutsangaben

Abstract

Background The aim of this study was to analyze the different applications of ultrasound (US) in upper extremity lymphedema (UEL) after breast cancer.

Methods A systematic review of the literature was performed in line with the PRISMA statement using MEDLINE/PubMed databases from January 1970 to December 2021. Articles describing the application of US in patients with UEL after breast cancer were included. The quality of the study, the level of reproducibility, and the different applications and type of US technique were analyzed.

Results In total, 30 articles with 1,193 patients were included in the final review. Five different applications were found: (1) diagnosis of UEL (14 studies found a direct correlation between lymphedema and morphological and/or functional parameters); (2) staging/severity of UEL (9 studies found a direct correlation between the clinical stage and the soft-tissue stiffness/texture/thickness); (3) therapeutic assessment (3 studies found an improvement in the circulatory status or in the muscle/subcutaneous thickness after conservative treatments); (4) prognosis assessment of UEL (1 study found a correlation between the venous flow and the risk of UEL); and (5) surgical planning (3 studies determined the location of the lymphatic vessel for lymphovenous anastomosis [LVA] surgery).

Conclusion Morphological and functional parameters have been correlated with the diagnosis, stage, therapeutic effect, prognosis of UEL, and surgical planning of LVA.



Publikationsverlauf

Eingereicht: 31. August 2021

Angenommen: 23. April 2022

Artikel online veröffentlicht:
26. September 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 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
  • 2 O'Donnell Jr TF, Rasmussen JC, Sevick-Muraca EM. New diagnostic modalities in the evaluation of lymphedema. J Vasc Surg Venous Lymphat Disord 2017; 5 (02) 261-273
  • 3 Kerasnoudis A, Tsivgoulis G. Nerve ultrasound in peripheral neuropathies: a review. J Neuroimaging 2015; 25 (04) 528-538
  • 4 Kouvaraki MA, Shapiro SE, Fornage BD. et al. Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 2003; 134 (06) 946-954 , discussion 954–955
  • 5 Méndez W, Rodgers SE, Lew JI, Montano R, Solórzano CC. Role of surgeon-performed ultrasound in predicting malignancy in patients with indeterminate thyroid nodules. Ann Surg Oncol 2008; 15 (09) 2487-2492
  • 6 Lew JI, Solorzano CC. Use of ultrasound in the management of thyroid cancer. Oncologist 2010; 15 (03) 253-258
  • 7 Calabrese E, Zorzi F, Pallone F. Ultrasound of the small bowel in Crohn's disease. Int J Inflamm 2012; 2012: 964720
  • 8 Horsthuis K, Bipat S, Bennink RJ, Stoker J. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology 2008; 247 (01) 64-79
  • 9 Valette PJ, Rioux M, Pilleul F, Saurin JC, Fouque P, Henry L. Ultrasonography of chronic inflammatory bowel diseases. Eur Radiol 2001; 11 (10) 1859-1866
  • 10 Dilauro S, Crum-Cianflone NF. Ileitis: when it is not Crohn's disease. Curr Gastroenterol Rep 2010; 12 (04) 249-258
  • 11 Liberati A, Altman DG, Tetzlaff J. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 2009; 62 (10) e1-e34
  • 12 Tassenoy A, De Mey J, De Ridder F. et al. Postmastectomy lymphoedema: different patterns of fluid distribution visualised by ultrasound imaging compared with magnetic resonance imaging. Physiotherapy 2011; 97 (03) 234-243
  • 13 Rezende MS, Marsengo AL, Apolinário A, Ferreira VTK, Guirro ECO. Correlation between upper limb volume and arterial and venous blood flow velocity in lymphedema secondary to breast cancer treatment. J Manipulative Physiol Ther 2017; 40 (04) 241-245
  • 14 de Abreu Junior GF, Pitta GBB, Araújo M, de Araújo Castro A, de Azevedo Junior WF, Miranda Junior F. Ultrasonografic changes in the axillary vein of patients with lymphedema after mastectomy. Rev Col Bras Cir 2015; 42 (02) 81-92
  • 15 Nascimben Matheus C, Caldeira de Oliveira Guirro E. Change in blood flow velocity demonstrated by Doppler ultrasound in upper limb after axillary dissection surgery for the treatment of breast cancer. Breast Cancer Res Treat 2011; 127 (03) 697-704
  • 16 Martin KP, Földi I. Are hemodynamic factors important in arm lymphedema after treatment of breast cancer?. Lymphology 1996; 29 (04) 155-157
  • 17 Svensson WE, Mortimer PS, Tohno E, Cosgrove DO. Increased arterial inflow demonstrated by Doppler ultrasound in arm swelling following breast cancer treatment. Eur J Cancer 1994; 30A (05) 661-664
  • 18 Svensson WE, Mortimer PS, Tohno E, Cosgrove DO. Colour Doppler demonstrates venous flow abnormalities in breast cancer patients with chronic arm swelling. Eur J Cancer 1994; 30A (05) 657-660
  • 19 Svensson WE, Mortimer PS, Tohno E, Cosgrove DO, Badger C, al Murrani B. The use of colour Doppler to define venous abnormalities in the swollen arm following therapy for breast carcinoma. Clin Radiol 1991; 44 (04) 249-252
  • 20 Johnson KC, DeSarno M, Ashikaga T, Dee J, Henry SM. Ultrasound and clinical measures for lymphedema. Lymphat Res Biol 2016; 14 (01) 8-17
  • 21 Choi YH, Seo KS. Correlation among bioimpedance analysis, sonographic and circumferential measurement in assessment of breast cancer-related arm lymphedema. Lymphology 2014; 47 (03) 123-133
  • 22 Devoogdt N, Pans S, De Groef A. et al. Postoperative evolution of thickness and echogenicity of cutis and subcutis of patients with and without breast cancer-related lymphedema. Lymphat Res Biol 2014; 12 (01) 23-31
  • 23 Lim CY, Seo HG, Kim K, Chung SG, Seo KS. Measurement of lymphedema using ultrasonography with the compression method. Lymphology 2011; 44 (02) 72-81
  • 24 Mellor RH, Bush NL, Stanton AWB, Bamber JC, Levick JR, Mortimer PS. Dual-frequency ultrasound examination of skin and subcutis thickness in breast cancer-related lymphedema. Breast J 2004; 10 (06) 496-503
  • 25 Pain SJ, Vowler S, Purushotham AD. Axillary vein abnormalities contribute to development of lymphoedema after surgery for breast cancer. Br J Surg 2005; 92 (03) 311-315
  • 26 Ashikaga T, Burns D, O'Brien P, Schaberg KB, Huston D. Texture analysis of post breast cancer lymphedema ultrasound images obtained using a portable device–a pilot study. Lymphat Res Biol 2005; 3 (03) 147-155
  • 27 Balzarini A, Milella M, Civelli E, Sigari C, De Conno F. Ultrasonography of arm edema after axillary dissection for breast cancer: a preliminary study. Lymphology 2001; 34 (04) 152-155
  • 28 Tassenoy A, De Mey J, Stadnik T. et al. Histological findings compared with magnetic resonance and ultrasonographic imaging in irreversible postmastectomy lymphedema: a case study. Lymphat Res Biol 2009; 7 (03) 145-151
  • 29 Han NM, Cho YJ, Hwang JS, Kim HD, Cho GY. Usefulness of ultrasound examination in evaluation of breast cancer-related lymphedema. J Korean Acad Rehabil Med. 2011; 35: 101-109
  • 30 van der Veen P, Vermeiren K, Von Kemp K, Lamote J, Sacre R, Lievens P. A key to understanding postoperative lymphoedema: a study on the evolution and consistency of oedema of the arm using ultrasound imaging. Breast 2001; 10 (03) 225-230
  • 31 Mander A, Venosi S, Menegatti E. et al. Upper limb secondary lymphedema ultrasound mapping and characterization. Int Angiol 2019; 38 (04) 334-342
  • 32 Giray E, Yağcı İ. Interrater and intrarater reliability of subcutaneous echogenicity grade and subcutaneous echo-free space grade in breast cancer-related lymphedema. Lymphat Res Biol 2019; 17 (05) 518-524
  • 33 Tassenoy A, Vermeiren K, van der Veen P. et al. Demonstration of tissue alterations by ultrasonography, magnetic resonance imaging and spectroscopy, and histology in breast cancer patients without lymphedema after axillary node dissection. Lymphology 2006; 39 (03) 118-126
  • 34 Yang X, Torres M, Kirkpatrick S, Curran WJ, Liu T. Ultrasound 2D strain measurement for arm lymphedema using deformable registration: a feasibility study. PLoS One 2017; 12 (08) e0181250
  • 35 Bok S-K, Jeon Y, Hwang P-S. Ultrasonographic evaluation of the effects of progressive resistive exercise in breast cancer-related lymphedema. Lymphat Res Biol 2016; 14 (01) 18-24
  • 36 Fong SSM, Ng SSM, Luk WS. et al. Effects of qigong exercise on upper limb lymphedema and blood flow in survivors of breast cancer: a pilot study. Integr Cancer Ther 2014; 13 (01) 54-61
  • 37 Rezende MS, Marsengo AL, de Jesus Guirro RR, de Oliveira Guirro EC. Blood flow velocity in brachial and subclavian vessels immediately after compressive procedures for treatment of postcancer therapy lymphedema in breast cancer: a randomized blind clinical trial. Lymphat Res Biol 2017; 15 (01) 23-31
  • 38 Mihara M, Hara H, Kawakami Y. Ultrasonography for classifying lymphatic sclerosis types and deciding optimal sites for lymphatic-venous anastomosis in patients with lymphoedema. J Plast Reconstr Aesthet Surg 2018; 71 (09) 1274-1281
  • 39 Bianchi A, Visconti G, Hayashi A, Santoro A, Longo V, Salgarello M. Ultra-high frequency ultrasound imaging of lymphatic channels correlates with their histological features: a step forward in lymphatic surgery. J Plast Reconstr Aesthet Surg 2020; 73 (09) 1622-1629
  • 40 Mohos B, Czedik-Eysenberg M, Steinbacher J, Tinhofer I, Meng S, Tzou CJ. Long-term use of ultrasound for locating optimal LVA sites: a descriptive data analysis. J Reconstr Microsurg 2022; 38 (03) 238-244
  • 41 O'Donnell Jr TF, Pauker SG, Callow AD, Kelly JJ, McBride KJ, Korwin S. The relative value of carotid noninvasive testing as determined by receiver operator characteristic curves. Surgery 1980; 87 (01) 9-19
  • 42 Garza RM, Ooi ASH, Falk J, Chang DW. The relationship between clinical and indocyanine green staging in lymphedema. Lymphat Res Biol 2019; 17 (03) 329-333
  • 43 Maclellan RA, Zurakowski D, Voss S, Greene AK. Correlation between lymphedema disease severity and lymphoscintigraphic findings: a clinical-radiologic study. J Am Coll Surg 2017; 225 (03) 366-370
  • 44 Jensen MR, Simonsen L, Karlsmark T, Bülow J. The washout rate of a subcutaneous 99mTc-HSA depot in lower extremity lymphoedema. Clin Physiol Funct Imaging 2012; 32 (02) 126-132
  • 45 Donahue MJ, Donahue PCM, Rane S. et al. Assessment of lymphatic impairment and interstitial protein accumulation in patients with breast cancer treatment-related lymphedema using CEST MRI. Magn Reson Med 2016; 75 (01) 345-355
  • 46 Auvert JF, Vayssairat M. Volumetrics: an indispensable complementary test in lymphology [in French]. Rev Med Interne 2002; 23 (Suppl 3): 388s-390s
  • 47 Sharkey AR, King SW, Kuo RY, Bickerton SB, Ramsden AJ, Furniss D. Measuring limb volume: accuracy and reliability of tape measurement versus perometer measurement. Lymphat Res Biol 2018; 16 (02) 182-186
  • 48 Seward C, Skolny M, Brunelle C, Asdourian M, Salama L, Taghian AG. A comprehensive review of bioimpedance spectroscopy as a diagnostic tool for the detection and measurement of breast cancer-related lymphedema. J Surg Oncol 2016; 114 (05) 537-542
  • 49 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
  • 50 Lee JH, Chang DW. Surgical treatment of primary lymphedema. Lymphat Res Biol 2017; 15 (03) 220-226
  • 51 Smoot BJ, Wong JF, Dodd MJ. Comparison of diagnostic accuracy of clinical measures of breast cancer-related lymphedema: area under the curve. Arch Phys Med Rehabil 2011; 92 (04) 603-610
  • 52 Kim M, Shin KH, Jung S-Y. et al. Identification of prognostic risk factors for transient and persistent lymphedema after multimodal treatment for breast cancer. Cancer Res Treat 2016; 48 (04) 1330-1337
  • 53 Cho M-J, Kwon JG, Pak CJ, Suh HP, Hong JP. The role of duplex ultrasound in microsurgical reconstruction: review and technical considerations. J Reconstr Microsurg 2020; 36 (07) 514-521
  • 54 Ottawa Hospital Research Institute. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Cited August 19, 2019. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  • 55 Sterne JA, Hernán MA, Reeves BC. et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016; 355: i4919
  • 56 von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 2008; 61 (04) 344-349