Abstract
Lymphedema is a chronic and progressive disease characterized by fluid accumulation, causing tissue edema as a result of a compromised lymphatic system. Diagnostic ultrasound (DUS) is a method capable of assessing soft tissue characteristics that can be used reliably to diagnose lymphedema as well as for measuring tissue compliance in a clinical setting. This is a systematic review, aiming to evaluate articles that made use of DUS in management of lymphedema secondary to breast cancer. A total of 570 articles were selected, exported to the Rayyan QCRI review program, and then screened by two researchers. From this search, 25 articles were selected after the authors reached consensus and were catalogued as to their main results. Diagnostic ultrasound was identified as an advantageous method that is safe, minimally invasive, low cost, and radiation free and is useful for evaluating the efficacy of therapies used in lymphedema treatment.
Keywords:
ultrasonography; breast cancer lymphedema; breast neoplasms
Resumo
O linfedema é uma doença crônica e progressiva caracterizada pelo acúmulo de fluidos, provocando edema tecidual em decorrência de um sistema linfático comprometido. A ultrassonografia diagnóstica (USD) é um método capaz de avaliar as características dos tecidos moles, podendo ser utilizada de maneira confiável para o diagnóstico do linfedema, além de mensurar a complacência tecidual em um cenário clínico. Esta é uma revisão sistemática, objetivando avaliar artigos que fizessem o uso da USD na abordagem do linfedema secundário ao câncer de mama. Foram selecionados 565 artigos, que foram exportados para o programa de revisão Rayyan QCRI e, em seguida, triados por dois pesquisadores. Dessa busca, foram obtidos 25 artigos selecionados após consenso entre os autores e que foram catalogados quanto aos seus resultados principais. A USD foi identificada como um método vantajoso por ser seguro, pouco invasivo, de baixo custo, sem uso de radiação, além de ser útil para avaliar a eficácia de terapias no tratamento do linfedema.
Palavras-chave:
ultrassonografia; linfedema relacionado a câncer de mama; neoplasias da mama
INTRODUCTION
Lymphedema is a severe chronic and progressive disease characterized by a high concentration of fluids containing proteins in the interstitial space, caused by partial or total obstruction of lymphatic drainage, provoking tissue edema, and caused by an impaired lymphatic system. As lymphedema worsens, there is greater involvement of the subfascial lymphatic system than the epifascial lymphatic system. As lymphedema progresses, fibrocytes and/or adipocytes begin to proliferate in affected areas, causing structural changes in skin and subcutaneous tissues and increasing vulnerability to bacterial and fungal infections.11 Zeltzer AA, Anzarut A, Hamdi M. A Review of Lymphedema for the Hand and Upper-Extremity Surgeon. J Hand Surg Am. 2018;43(11):1016-25. http://dx.doi.org/10.1016/j.jhsa.2018.03.054. PMid:29789187.
http://dx.doi.org/10.1016/j.jhsa.2018.03...
2 Iker E, Mayfield CK, Gould DJ, Patel KM. Characterizing lower extremity lymphedema and lipedema with cutaneous ultrasonography and an objective computer-assisted measurement of dermal echogenicity. Lymphat Res Biol. 2019;17(5):525-30. http://dx.doi.org/10.1089/lrb.2017.0090. PMid:30615553.
http://dx.doi.org/10.1089/lrb.2017.0090...
-33 Jeon Y, Beom J, Ahn S, Bok SK. Ultrasonographic evaluation of breast cancer-related lymphedema. J Vis Exp. 2017;(119):e54996. http://dx.doi.org/10.3791/54996. PMid:28117779.
http://dx.doi.org/10.3791/54996...
One of the most important manifestations of lymphedema is lymphedema secondary to breast cancer (LSBC). Studies report that during the initial stages lymphedema presents clinically as upper limb edema in the area of the arm, shoulder, neck, or trunk ipsilateral to treatment, because of removal of local lymph nodes and lymph vessels, compromising the local lymphatic system and impairing lymphatic drainage. There may be increased protein content in the affected tissues, resulting in chronic inflammation, fibrosis, pain, limited amplitude of movement, and/or paresthesia, in addition to reduced immune function, increasing the risk of local inflammation and infections.44 Shah C, Vicini FA. Breast cancer-related arm lymphedema: incidence rates, diagnostic techniques, optimal management and risk reduction strategies. Int J Radiat Oncol Biol Phys. 2011;81(4):907-14. http://dx.doi.org/10.1016/j.ijrobp.2011.05.043. PMid:21945108.
http://dx.doi.org/10.1016/j.ijrobp.2011....
5 Bok SK, Jeon Y, Hwang PS. Ultrasonographic Evaluation of the Effects of Progressive Resistive Exercise in Breast Cancer-Related Lymphedema. Lymphat Res Biol. 2016;14(1):18-24. http://dx.doi.org/10.1089/lrb.2015.0021. PMid:26824517.
http://dx.doi.org/10.1089/lrb.2015.0021...
6 National Cancer Institute - NCI. Surveillance, Epidemiology, and End Results (SEER) Program. SEER*Stat database: incidence-SEER 9 regs research data with delay-adjustment, malignant only, based on the november 2018 submission. Bethesda: NCI; 2019.-77 Seo D, Lee S, Choi W. Comparison of real-time ultrasound imaging for manual lymphatic drainage on breast cancer-related lymphedema in individuals with breast cancer: a preliminary study. Phys Ther Rehabil Sci. 2020;9(1):43-8. http://dx.doi.org/10.14474/ptrs.2020.9.1.43.
http://dx.doi.org/10.14474/ptrs.2020.9.1...
It has been demonstrated that lymphedema progresses in the form of a vicious cycle, in which lymphatic stasis provokes development of chronic inflammation, involving uncontrolled macrophage and CD4 + cell response and accumulation of fat, which also promotes chronic inflammation through macrophage infiltration and activation, producing inflammatory cytokines which in turn provoke more lymphatic stasis, reducing lymphatic pumping and increasing capillary filtration.88 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(5):518-24. http://dx.doi.org/10.1089/lrb.2018.0053. PMid:30570358.
http://dx.doi.org/10.1089/lrb.2018.0053...
With the objective of improving patients’ quality of life, reducing their physical and psychological discomfort, it is essential to conduct a precise diagnosis of the problem to achieve better prognosis and support treatment planning. It has been shown that this diagnosis is not always easy to achieve and it is necessary to differentiate it from other pathologies with similar conditions to lymphedema, such as local edema and fibrosis of subcutaneous tissues. There are many tests that can be used with the objective of achieving more precise diagnostic results, including imaging exams undertaken with the objective of visualizing soft tissues, lymph vessels, and lymph nodes, and which constitute a method that can identify the pathophysiologic changes of lymphedema.99 Lee YL, Huang YL, Chu SY, et al. Characterization of limb lymphedema using the statistical analysis of ultrasound backscattering. Quant Imaging Med Surg. 2020;10(1):48-56. http://dx.doi.org/10.21037/qims.2019.10.12. PMid:31956528.
http://dx.doi.org/10.21037/qims.2019.10....
,1010 Chung SH, Kim KG. Design of lymphedema ultrasound phantom with 3D-printed patient-specific subcutaneous anatomy: a-mode analysis approach for early diagnosis. Phys Med. 2018;55:73-81. http://dx.doi.org/10.1016/j.ejmp.2018.10.019. PMid:30471822.
http://dx.doi.org/10.1016/j.ejmp.2018.10...
Diagnostic ultrasound (DUS) is one of the new methods of lymphedema assessment for evaluating limbs with edema. It is used to detect whether the etiology is entirely venous or if there is also a lymphatic abnormality (phlebolymphedema). Using DUS offers the advantages that it is a simple imaging exam that is noninvasive and readily available for visualizing blood vessels. Although enlarged lymph nodes can very often be seen, DUS cannot provide images of the lymphatic vasculature. However, the ultrasonographic characteristics of the tissue layers in the limb with edema offer important information about the etiology of the edema, with the advantage of enabling follow-up of treatment response, measuring the thickness of each limb tissue element before and after treatment.1111 O’Donnell TF Jr, Rasmussen JC, Sevick-Muraca EM. New diagnostic modalities in the evaluation of lymphedema. J Vasc Surg Venous Lymphat Disord. 2017;5(2):261-73. http://dx.doi.org/10.1016/j.jvsv.2016.10.083. PMid:28214496.
http://dx.doi.org/10.1016/j.jvsv.2016.10...
Diagnostic ultrasound can be used to assess and diagnose lymphedema in upper limbs, lower limbs, and genital organs and can offer differential diagnosis between several different pathologies that cause increased limb volume. Moreover, DUS is a relatively inexpensive method for examining the characteristics of soft tissues and can reliably be used for lymphedema diagnosis, since it enables assessment of the thickness of the skin and subcutaneous tissue and can measure tissue compliance in clinical settings.1212 Dylke ES, Benincasa Nakagawa H, Lin L, Clarke JL, Kilbreath SL. Reliability and diagnostic thresholds for ultrasound measurements of dermal thickness in breast lymphedema. Lymphat Res Biol. 2018;16(3):258-62. http://dx.doi.org/10.1089/lrb.2016.0067. PMid:28759331.
http://dx.doi.org/10.1089/lrb.2016.0067...
,1313 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(8):e0181250. http://dx.doi.org/10.1371/journal.pone.0181250. PMid:28854199.
http://dx.doi.org/10.1371/journal.pone.0...
Despite progress in treatment approaches for lymphedema, it remains necessary to conduct more studies to improve care. Scientific studies have demonstrated that lymphedema assessment methods lack consistency and rigor, requiring a more precise technique for diagnosis and follow-up, particularly for early detection and precise classification. Early diagnosis of lymphedema enables safe intervention, which can reverse development and enable more accurate management of treatment, since treatment depends on disease severity, making precise classification necessary.1313 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(8):e0181250. http://dx.doi.org/10.1371/journal.pone.0181250. PMid:28854199.
http://dx.doi.org/10.1371/journal.pone.0...
In view of the need to examine DUS as a resource for detection and monitoring of lymphedema, the objective of this study is to conduct a review of the subject, focusing on its use for measurement and examination of structural changes in affected limbs.
METHOD
This is a systematic literature review based on database searches for articles that deal with the use of ultrasound for LSBC. The study was conducted in accordance with the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) and was performed from January to December of 2022.1414 Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372(71):n71. http://dx.doi.org/10.1136/bmj.n71. PMid:33782057.
http://dx.doi.org/10.1136/bmj.n71...
Identification of potential studies for analysis employed a wide-ranging strategy involving cross-referencing of specific search terms. The review started by searching the contemporary literature in Brazilian and international articles indexed on databases such as PubMed, Lilacs, IBECS, MEDLINE, Cochrane Library, EMBASE, SciELO, and Google Scholar. Electronic searches were conducted using keywords such as lymphedema, ultrasound, breast cancer, and upper limb in both Portuguese and English. The descriptors employed were chosen taking into consideration their relevance for representation of the subject and their use in the specialist scientific literature. The keywords were taken from the Biblioteca Virtual em Saude (BVS), specifically the Descritores em Ciências de Saude (DECS), and from Medical Subject Headings (Mesh), and Emtree.
The objective of this review is to offer researchers contact with what has been written on this research subject, contributing to construction of knowledge about use of ultrasonography in LSBC. A descriptive, bibliographic study was conducted on the basis of scientific articles available over the internet via scientific databases. The historical review attempts to collect what has been written on the subject, improving knowledge about the subject.
The inclusion criteria defined as eligible articles published in Portuguese, English, or Spanish on the subject of the review describing cross-sectional or longitudinal studies or accuracy studies. No date limits were set because of the importance of the subject and the small number of articles published on it and also to offer a temporal description of articles published on the subject, the importance of which from a historical perspective justifies conducting the study. Literature reviews, systematic reviews, and articles that did not cover the subject were excluded.
The articles selected using the search strategies described were exported to Rayyan Qatar Computing Research Institute (Rayyan QCRI) review software for independent analysis by two researchers previously blinded for assessment of the articles. The Rayyan program was initially used to exclude duplicates, followed by screening by titles, abstracts, and full text. The analysis involved assessment of methodological quality, intervention proposals, and outcomes achieved. At the end of the analysis, any disagreements were solved through consensus between the researchers.1515 Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan—a web and mobile app for systematic reviews. Syst Rev. 2016;5(1):210. http://dx.doi.org/10.1186/s13643-016-0384-4. PMid:27919275.
http://dx.doi.org/10.1186/s13643-016-038...
All articles found were evaluated to identify those that directly dealt with the subject. During analysis of the articles, choices were made between thematic areas, analyzing content as well as titles, since the title is not always indicative of a study’s scope.
Each article selected underwent analytical reading, with integral and interpretative analysis of the text, followed by identification of its principal concepts and synthesis of its main ideas. The data identified were then organized in a table, in which the information was organized as follows: sample size, type of study, intervention implemented, main findings, whether the intervention was effective, and equipment specifications. This cataloging process was done to facilitate understanding of the articles analyzed in the study. Figure 1 shows the research development flowchart.
RESULTS
A total of 565 articles were selected from the databases, which, after screening and analysis, yielded 25 articles for cataloging. The results constitute the findings of evaluation of 25 articles selected by consensus between the authors. The flow diagram contained in the Methods section illustrates how these studies were selected.
The authors of all 25 articles published from 2004 to 2021 described the efficacy of DUS as a diagnostic method for lymphedema. Only one article, by Duyur Çakit et al.,1616 Duyur Çakıt B, Ayhan FF, Gümrük Aslan S, Genç H. The role of ultrasonography in follow-up of effectiveness of Complex Decongestive Therapy (CDT) in different subgroups of patients with breast cancer-related lymphoedema. Eur J Cancer Care. 2021;30(2):e13376. http://dx.doi.org/10.1111/ecc.13376. PMid:33219612.
http://dx.doi.org/10.1111/ecc.13376...
discussed relative efficacy, evaluating only a non-obese population with grade 2 LSBC.
Table 1 lists the principal points discussed in the articles.
Polat et al.2929 Polat AV, Ozturk M, Polat AK, Karabacak U, Bekci T, Murat N. Efficacy of ultrasound and shear wave elastography for the diagnosis of breast cancer-related lymphedema. J Ultrasound Med. 2020;39(4):795-803. http://dx.doi.org/10.1002/jum.15162. PMid:31705687.
http://dx.doi.org/10.1002/jum.15162...
and Iyigun et al.2727 Iyigun ZE, Duymaz T, Ilgun AS, et al. Preoperative lymphedema-related risk factors in early-stage breast cancer. Lymphat Res Biol. 2018;16(1):28-35. http://dx.doi.org/10.1089/lrb.2016.0045. PMid:28346852.
http://dx.doi.org/10.1089/lrb.2016.0045...
reported on possible time of diagnosis: considering DUS feasible in the latent stage, initial stages, and late stages. Additionally, Yang et al.2626 Yang EJ, Kim SY, Lee WH, Lim JY, Lee J. Diagnostic accuracy of clinical measures considering segmental tissue composition and volume changes of breast cancer-related lymphedema. Lymphat Res Biol. 2018;16(4):368-76. http://dx.doi.org/10.1089/lrb.2017.0047. PMid:29338541.
http://dx.doi.org/10.1089/lrb.2017.0047...
correlated echogenicity of ultrasonographic waves as a method for improving diagnosis of lymphedema.
Duyur Çakit et al.1616 Duyur Çakıt B, Ayhan FF, Gümrük Aslan S, Genç H. The role of ultrasonography in follow-up of effectiveness of Complex Decongestive Therapy (CDT) in different subgroups of patients with breast cancer-related lymphoedema. Eur J Cancer Care. 2021;30(2):e13376. http://dx.doi.org/10.1111/ecc.13376. PMid:33219612.
http://dx.doi.org/10.1111/ecc.13376...
discussed use of DUS for monitoring the efficacy of complex decongestive therapy in different subgroups and suggested the instrument’s relative efficacy, showing that non-obese and stage 2 patients with LSBC can be assessed with greater reliability.
The process of lymphedema formation involves increased activity of neutrophils, macrophages, and fibroblasts and inflammation and collagen deposition (fibrosis). According to Suehiro et al.,3030 Suehiro K, Morikage N, Yamashita O, et al. Skin and subcutaneous tissue ultrasonography features in breast cancer-related lymphedema. Ann Vasc Dis. 2016;9(4):312-6. http://dx.doi.org/10.3400/avd.oa.16-00086. PMid:28018504.
http://dx.doi.org/10.3400/avd.oa.16-0008...
DUS can be used to capture the increase in collagen and the increase in subcutaneous inflammation, while Kim et al.3333 Kim SY, Lee CH, Heo SJ, Moon MH. The clinical usefulness of lymphedema measurement technique using ultrasound. Lymphat Res Biol. 2021;19(4):340-6. http://dx.doi.org/10.1089/lrb.2019.0070. PMid:33404351.
http://dx.doi.org/10.1089/lrb.2019.0070...
showed that it is also possible to detect histological changes in addition to structural ones. Finally, Han et al.1818 Han N, Cho YJ, Hwang JS, Kim H, Cho G. Usefulness of Ultrasound Examination in Evaluation of Breast Cancer-Related Lymphedema. Ann Rehabil Med. 2011;35(1):101-9. describe fibrosis as a highly valuable ultrasonographic finding, in addition to the extent of edema.
Seven of the 25 selected articles from 2004 to 2022 considered use of DUS in conjunction with therapeutic techniques with the objective of demonstrating the progress or regression obtained during treatment. Seo et al.77 Seo D, Lee S, Choi W. Comparison of real-time ultrasound imaging for manual lymphatic drainage on breast cancer-related lymphedema in individuals with breast cancer: a preliminary study. Phys Ther Rehabil Sci. 2020;9(1):43-8. http://dx.doi.org/10.14474/ptrs.2020.9.1.43.
http://dx.doi.org/10.14474/ptrs.2020.9.1...
used manual lymph drainage (MLD) as lymphedema treatment method and reported the efficacy DUS during the process. Devoogdt et al.1919 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(1):23-31. http://dx.doi.org/10.1089/lrb.2013.0028. PMid:24502300.
http://dx.doi.org/10.1089/lrb.2013.0028...
suggested that another diagnostic method in conjunction is needed until there is more scientific evidence.
Elastography conducted using DUS is a method that can identify tissue rigidity, observing the presence of possible nodules, and is painless and minimally invasive. Four authors demonstrated the efficacy of elastography. Hashemi et al.2525 Hashemi HS, Fallone S, Boily M, Towers A, Kilgour RD, Rivaz H. Ultrasound elastography of breast cancer-related lymphedema. In: Proceedings of the 2018 IEEE 15th International Symposium on Biomedical Imaging (ISBI 2018); 2018; Washington, DC, USA. New York: IEEE; 2018. p. 1491-5. http://dx.doi.org/10.1109/ISBI.2018.8363855.
http://dx.doi.org/10.1109/ISBI.2018.8363...
showed the importance of the method not only for diagnosis, but also for staging LSBC. Hashemi et al.3131 Hashemi HS, Fallone S, Boily M, Towers A, Kilgour RD, Rivaz H. Assessment of mechanical properties of tissue in breast cancer-related lymphedema using ultrasound elastography. IEEE Trans Ultrason Ferroelectr Freq Control. 2019;66(3):541-50. http://dx.doi.org/10.1109/TUFFC.2018.2876056. PMid:30334756.
http://dx.doi.org/10.1109/TUFFC.2018.287...
described elastography as more sensitive than the pitting test.
The ultrasound systems employed varied in terms of model and frequency. Mellor et al.1717 Mellor RH, Bush NL, Stanton AW, Bamber JC, Levick JR, Mortimer PS. Dual-frequency ultrasound examination of skin and subcutis thickness in breast cancer-related lymphedema. Breast J. 2004;10(6):496-503. http://dx.doi.org/10.1111/j.1075-122X.2004.21458.x. PMid:15569205.
http://dx.doi.org/10.1111/j.1075-122X.20...
and Dai et al.2323 Dai M, Sato A, Maeba H, et al. Dermal structure in lymphedema patients with history of acute dermatolymphangioadenitis evaluated by histogram analysis of ultrasonography findings: a case-control study. Lymphat Res Biol. 2016;14(1):2-7. http://dx.doi.org/10.1089/lrb.2015.0020. PMid:26982711.
http://dx.doi.org/10.1089/lrb.2015.0020...
used a Dermascan (20 MHz) system. Four articles did not specify what equipment was used and Bok et al.55 Bok SK, Jeon Y, Hwang PS. Ultrasonographic Evaluation of the Effects of Progressive Resistive Exercise in Breast Cancer-Related Lymphedema. Lymphat Res Biol. 2016;14(1):18-24. http://dx.doi.org/10.1089/lrb.2015.0021. PMid:26824517.
http://dx.doi.org/10.1089/lrb.2015.0021...
and Hansdorfer-Korzon et al.2424 Hansdorfer-Korzon R, Teodorczyk J, Gruszecka A, Lass P. Are compression corsets beneficial for the treatment of breast cancer-related lymphedema? New opportunities in physiotherapy treatment: a preliminary report. OncoTargets Ther. 2016;9:2089-98. http://dx.doi.org/10.2147/OTT.S100120. PMid:27103835.
http://dx.doi.org/10.2147/OTT.S100120...
did not report the frequency employed. Han et al.1818 Han N, Cho YJ, Hwang JS, Kim H, Cho G. Usefulness of Ultrasound Examination in Evaluation of Breast Cancer-Related Lymphedema. Ann Rehabil Med. 2011;35(1):101-9. and Suehiro et al.2222 Suehiro K, Yamamoto S, Honda S, et al. Perioperative variations in indices derived from noninvasive assessments to detect postmastectomy lymphedema. J Vasc Surg Venous Lymphat Disord. 2019;7(4):562-9. http://dx.doi.org/10.1016/j.jvsv.2019.02.012. PMid:31203860.
http://dx.doi.org/10.1016/j.jvsv.2019.02...
used a Logiq model. None of the other instruments and frequencies coincided.
Patients and studies varied in many different ways and no pattern emerged. There were 11 cross-sectional studies, two cross-sectional accuracy studies, and one descriptive cross-sectional study, while there were 11 longitudinal prospective studies and just one longitudinal retrospective study. Han et al.1818 Han N, Cho YJ, Hwang JS, Kim H, Cho G. Usefulness of Ultrasound Examination in Evaluation of Breast Cancer-Related Lymphedema. Ann Rehabil Med. 2011;35(1):101-9. and Abreu et al.2020 Abreu GF Jr, Pitta GB, Araújo M, Castro A, Azevedo WF Jr, Miranda F Jr. Ultrasonografic changes in the axillary vein of patients with lymphedema after mastectomy. Rev Col Bras Cir. 2015;42(2):81-92. http://dx.doi.org/10.1590/0100-69912015002004. PMid:26176673.
http://dx.doi.org/10.1590/0100-699120150...
separated participants into two groups, the first comprising patients with LSBC and the second containing healthy patients, but they differed in terms of the number of patients in each group.
Figure 2 shows a schematic illustration of the difference between normal tissue and tissue with LSBC assessed by DUS.
Table 1 shows the evidence level of each article. This systematic review included experimental articles, the majority with 1b and 1c evidence levels, according to the Oxford Scale for levels of evidence. The majority of evidence available is level 1, and the procedure is recommended (recommendation grade A).
DISCUSSION
This study conducted a wide-ranging review of 25 scientific articles that documented use of DUS as a diagnostic method in lymphedema cases. There was consensus on the instrument’s efficacy for identifying edema in subcutaneous tissue.
Currently there is no specific tool for diagnosis in the initial stages, when symptoms have not yet emerged. The most popular tests for characterizing LSBC include the following: arm circumference measurement; Perometry, which assesses the volume of the affected arm compared with the unaffected arm; and bioimpedance, which tests resistance to painless electric currents passed through the arm.3535 Forte AJ, Huayllani MT, Boczar D, et al. The basics of ultrasound elastography for diagnosis, assessment, and staging breast cancer-related lymphedema: a systematic review of the literature. Gland Surg. 2020;9(2):589-95. http://dx.doi.org/10.21037/gs.2020.02.08. PMid:32420294.
http://dx.doi.org/10.21037/gs.2020.02.08...
Other imaging methods used to assess LSBC are computed tomography, magnetic resonance imaging, and indocyanine green lymphography; but they are not portable and they are more expensive.88 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(5):518-24. http://dx.doi.org/10.1089/lrb.2018.0053. PMid:30570358.
http://dx.doi.org/10.1089/lrb.2018.0053...
On the other hand, the lymphoscintigraphy imaging technique is considered the standard criterion for diagnosis of LSBC, using a radiotracer to show the lymphatic system and reveal the presence and caliber of the lymph vessels, lymph nodes, collaterals, and delayed radiotracer uptake. However, this method is not generally preferred because of the lack of a standard protocol, the invasivity of the procedure, and patient exposure to radiation.3535 Forte AJ, Huayllani MT, Boczar D, et al. The basics of ultrasound elastography for diagnosis, assessment, and staging breast cancer-related lymphedema: a systematic review of the literature. Gland Surg. 2020;9(2):589-95. http://dx.doi.org/10.21037/gs.2020.02.08. PMid:32420294.
http://dx.doi.org/10.21037/gs.2020.02.08...
Ultrasonography is a safe, easy, and inexpensive procedure for assessment of patients with LSBC. Changes include increased thickness of the dermis, changes from hypoechogenicity to hyperechogenicity in subcutaneous tissue, and fluid accumulation in the dermis, the interlobular space, and the superficial fascia. While these images can be difficult to detect in ultrasound images, they can provide a quantitative measurement of the thickness of cutaneous, fascial, and surrounding tissues for assessment of LSBC.3535 Forte AJ, Huayllani MT, Boczar D, et al. The basics of ultrasound elastography for diagnosis, assessment, and staging breast cancer-related lymphedema: a systematic review of the literature. Gland Surg. 2020;9(2):589-95. http://dx.doi.org/10.21037/gs.2020.02.08. PMid:32420294.
http://dx.doi.org/10.21037/gs.2020.02.08...
Diagnostic ultrasound can also be useful as an effective prognostic tool, since it can identify patients at risk of developing an incomplete pathological response. Use of this imaging technique can reduce the time spent undergoing several invasive diagnostic procedures and can also reduce the health care costs involved in the process.3636 Chen W, Fang LX, Chen HL, Zheng JH. Accuracy of ultrasound elastography for predicting breast cancer response to neoadjuvant chemotherapy: a systematic review and meta-analysis. World J Clin Cases. 2022;10(11):3436-48. http://dx.doi.org/10.12998/wjcc.v10.i11.3436. PMid:35611212.
http://dx.doi.org/10.12998/wjcc.v10.i11....
Morphological and functional parameters detected using DUS can be correlated with diagnosis, staging, prognosis, and clinical therapeutic efficacy in LSBC.3737 Canales-Lachén E, Asunsolo Á, Manrique OJ, Blázquez J, Holguín P, Maldonado AA. The use of ultrasound imaging for upper extremity lymphedema after breast cancer: a systematic review. J Reconstr Microsurg. 2023;39(2):102-10. http://dx.doi.org/10.1055/s-0042-1750824. PMid:36162421.
http://dx.doi.org/10.1055/s-0042-1750824...
Ultrasound is considered a simple and safe imaging exam for assessing the thickness of the skin and subcutaneous tissue and, because of this, has been studied for assessment of patients with lymphedema. In recent years, ultrasound elastography has been used to assess LSBC, but the parameters for evaluation, diagnosis, and staging of the disease are not yet well-defined.
Diagnostic ultrasound appears to be a method that offers advantages because it is safe, minimally invasive, practical, and inexpensive, it doesn’t use ionizing radiation, it can be used preoperatively, intraoperatively, and postoperatively, and it is useful for assessing the efficacy of lymphedema treatment. The disadvantages observed were the need for a skilled operator to perform the procedure, application of the correct pressure when conducting DUS, and the need for more studies of the subject.
Finally, in clinical practice, DUS appears to be a promising resource for objective measurement, classification, and follow-up of LSBC. The procedure is rapid, painless, practical, and minimally invasive for the patients and the equipment can be found in many medical care settings.
CONCLUSIONS
In view of the facts presented, it is understood that ultrasonography is a necessary instrument for assessment of cases of lymphedema secondary to breast cancer, since it has been shown to be effective in a more objective manner and is a resource that is feasible for diagnosis.
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How to cite: Rezende LF, Piloni JPM, Kempa VL, et al. Ultrasonography as an instrument to evaluate lymphedema secondary to breast cancer: systematic review. J Vasc Bras. 2023;22:e20220144. https://doi.org/10.1590/1677-5449.202201442
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Financial support: None.
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The study was carried out at Centro Universitário das Faculdades Associadas de Ensino (FAE), São João da Boa Vista, SP, Brazil.Ethics committee approval: Not applicable.
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Publication Dates
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Publication in this collection
18 Dec 2023 -
Date of issue
2023
History
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Received
16 June 2023 -
Accepted
02 Oct 2023