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Superficial and functional imaging of the tricipital lymphatic pathway: a modern reintroduction

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Abstract

Purpose

The tricipital, or Caplan’s, lymphatic pathway has been previously identified in cadavers and described as a potential compensatory pathway for lymphatic drainage of the upper extremity, as it may drain lymphatic fluid directly to the scapular lymph nodes, avoiding the axillary lymph node groups. The aim of this study was to map the anatomy of the tricipital pathway in vivo in patients without lymphatic disease.

Methods

A retrospective review was performed to identify patients with unilateral breast cancer undergoing preoperative Indocyanine green (ICG) lymphography prior to axillary lymph node dissection from May 2021 through January 2022. Exclusion criteria were evidence or known history of upper extremity lymphedema or non-linear channels visualized on ICG. Demographic, oncologic, and ICG imaging data were extracted from a Lymphatic Surgery Database. The primary outcome of this study was the presence and absence of the tricipital pathway. The secondary outcome was major anatomical variations among those with a tricipital pathway.

Results

Thirty patients underwent preoperative ICG lymphography in the study period. The tricipital pathway was visualized in the posterior upper arm in 90% of patients. In 63% of patients, the pathway had a functional connection to the forearm (long bundle variant) and in 27%, the pathway was isolated to the upper arm without a connection to the forearm (short bundle variant). In those with a long bundle, the contribution was predominantly from the posterior ulnar lymphosome. Anatomic destinations of the tricipital pathway included the deltotricipital groove and the medial upper arm channel, which drains to the axilla.

Conclusion

When present, the tricipital pathway coursed along the posterior upper arm with variability in its connections to the forearm distally, and the torso proximally. Long-term follow-up studies will help determine the significance of these anatomic variations in terms of individual risk of lymphedema after axillary nodal dissection.

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Data availability

The datasets generated during and/or analyzed during the current study are not publicly available due containment of protected health information but are available from the corresponding author on reasonable request.

References

  1. Tashiro K, Yamashita S, Koshima I, Miyamoto S (2017) Visualization of accessory lymphatic pathways in secondary upper extremity lymphedema using indocyanine green lymphography. Ann Plast Surg 79(4):393–396. https://doi.org/10.1097/SAP.0000000000001120

    Article  Google Scholar 

  2. Togawa K, Ma H, Sullivan-Halley J et al (2014) Risk factors for self-reported arm lymphedema among female breast cancer survivors: a prospective cohort study. Breast Cancer Res. https://doi.org/10.1186/s13058-014-0414-x

    Article  Google Scholar 

  3. Ridner SH, Dietrich MS, Stewart BR, Armer JM (2011) Body mass index and breast cancer treatment-related lymphedema. Support Care Cancer 19(6):853–857. https://doi.org/10.1007/s00520-011-1089-9

    Article  Google Scholar 

  4. Johnson AR, Kimball S, Epstein S et al (2019) Lymphedema incidence after axillary lymph node dissection quantifying the impact of radiation and the lymphatic microsurgical preventive healing approach. Ann Plast Surg 82(4S Suppl 3):S234–S241. https://doi.org/10.1097/SAP.0000000000001864

    Article  Google Scholar 

  5. Suami H, Taylor GI, Pan WR (2007) The lymphatic territories of the upper limb: anatomical study and clinical implications. Plast Reconstr Surg 119(6):1813–1822. https://doi.org/10.1097/01.prs.0000246516.64780.61

    Article  Google Scholar 

  6. Stouthandel MEJ, Veldeman L, van Hoof T (2019) Call for a multidisciplinary effort to map the lymphatic system with advanced medical imaging techniques: a review of the literature and suggestions for future anatomical research. Anat Rec 302(10):1681–1695. https://doi.org/10.1002/ar.24143

    Article  Google Scholar 

  7. Johnson AR, Bravo MG, James TA, Suami H, Lee BT, Singhal D (2020) The all but forgotten mascagni-sappey pathway: learning from immediate lymphatic reconstruction. J Reconstr Microsurg 36(1):028–031. https://doi.org/10.1055/s-0039-1694757

    Article  Google Scholar 

  8. Johnson AR, Granoff MD, Suami H, Lee BT, Singhal D (2020) Real-time visualization of the mascagni-sappey pathway utilizing ICG lymphography. Cancers (Basel). https://doi.org/10.3390/cancers12051195

    Article  Google Scholar 

  9. Granoff M, Pardo J, Shillue K, et al. Variable anatomy of the lateral upper arm lymphatic channel a potential anatomic risk factor for the development of breast cancer related lymphedema. Plast Reconstr Surg. (In Press)

  10. Leduc A, Caplan I, Leduc O (1993) Lymphatic drainage of the upper limb Substitution lymphatic pathways. European J Lymphol IV(13):11–18

    Google Scholar 

  11. Ciucci J (2004) Derivative lymphatic currents UL, Ciucci, JL-English. In: Linfedema Del Miembro Superior Postratamiento Del Cancer de Mama. Nayarit (Ed). 29

  12. Purushotham AD, Britton TMB, Klevesath MB, Chou P, Agbaje OF, Duffy SW (2007) Lymph node status and breast cancer-related lymphedema. Ann Surg 246(1):42–45. https://doi.org/10.1097/01.sla.0000259390.51203.7b

    Article  Google Scholar 

  13. Cintolesi V, Stanton AWB, Bains SK et al (2016) Constitutively enhanced lymphatic pumping in the upper limbs of women who later develop breast cancer-related lymphedema. Lymphat Res Biol 14(2):50–61. https://doi.org/10.1089/lrb.2016.0005

    Article  Google Scholar 

  14. Bains SK, Stanton AWB, Cintolesi V et al (2015) A constitutional predisposition to breast cancer-related lymphoedema and effect of axillary lymph node surgery on forearm muscle lymph flow. Breast 24(1):68–74. https://doi.org/10.1016/j.breast.2014.11.010

    Article  Google Scholar 

  15. Stanton AWB, Modi S, Bennett Britton TM et al (2009) Lymphatic drainage in the muscle and subcutis of the arm after breast cancer treatment. Breast Cancer Res Treat 117(3):549–557. https://doi.org/10.1007/s10549-008-0259-z

    Article  Google Scholar 

  16. Ciucci JL, Vadra GD, Sorocco J (1996) Investigación anatómica del drenaje linfático del miembro superior. Su importancia en la patología traumatológica. Rev Asoc Arg Ortop y Traumatol 62(4):544–571

    Google Scholar 

  17. Pissas A, Rzal K, Math M, el Nasser M, Dubois J (2002) Prevention of secondary lymphedema. Ann Ital Chir LXXIII 73(5):489–492

    Google Scholar 

  18. Medina-Rodríguez ME, de-la-Casa-Almeida M, Martel-Almeida E, Ojeda-Cárdenes A, Medrano-Sánchez EM (2019) Visualization of accessory lymphatic pathways, before and after manual drainage, in secondary upper limb lymphedema using indocyanine green lymphography. J Clin Med 8(11):1917. https://doi.org/10.3390/jcm8111917

    Article  Google Scholar 

  19. Latorre J, Ciucci JL, Rosendo A (2004) Anatomía del sistema linfático del miembro superior. Anales de Cirugía Cardíaca y Vascular 10(3):184–198

    Google Scholar 

  20. Giacalone G, Belgrado JP, Bourgeois P, Bracale P, Röh N, Moraine JJ (2011) A new dynamic imaging tool to study lymphoedema and associated treatments indexed in excerpta medica. European J Lymphol Related Probl 22(62):10–14

    Google Scholar 

  21. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)-A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42(2):377–381. https://doi.org/10.1016/j.jbi.2008.08.010

    Article  Google Scholar 

  22. Harris PA, Taylor R, Minor BL et al (2019) The REDCap consortium: Building an international community of software platform partners. J Biomed Inform. https://doi.org/10.1016/j.jbi.2019.103208

    Article  Google Scholar 

  23. Granoff M, Pardo J, Johnson AR et al (2022) The superficial and functional lymphatic anatomy of the upper extremity. Plast Reconstr Surg. https://doi.org/10.1097/PRS.0000000000009555

    Article  Google Scholar 

  24. Kubik S (1980) The role of the lateral upper arm bundle and the lymphatic watersheds in the formation of collateral pathways in lymphedema. Acta bio Acad Sci Hung 31(1–3):191–200

    Google Scholar 

  25. Yamamoto T, Narushima M, Yoshimatsu H et al (2014) Dynamic indocyanine green (ICG) lymphography for breast cancer-related arm lymphedema. Ann Plast Surg 73(6):706–709. https://doi.org/10.1097/SAP.0b013e318285875f

    Article  Google Scholar 

  26. Yamamoto T, Yamamoto N, Doi K et al (2011) Indocyanine green-enhanced lymphography for upper extremity lymphedema: a novel severity staging system using dermal backflow patterns. Plast Reconstr Surg 128(4):941–947. https://doi.org/10.1097/PRS.0b013e3182268cd9

    Article  Google Scholar 

  27. Woo KJ, Lee MK, Seong IH, Park JW (2022) Classification of superficial lymphatic pathways in the upper extremity and incidence of lymphatic obstruction according to the lymphatic pathways in patients with unilateral upper extremity lymphedema. J Plast Reconstr Aesthet Surg. https://doi.org/10.1016/j.bjps.2022.02.049

    Article  Google Scholar 

  28. Kim G, Smith MP, Donohoe KJ, Johnson AR, Singhal D, Tsai LL (2020) MRI staging of upper extremity secondary lymphedema: correlation with clinical measurements. Eur Radiol 30(8):4686–4694. https://doi.org/10.1007/s00330-020-06790-0

    Article  Google Scholar 

  29. Amore M, Tapia L, Mercado D, Pattarone G, Ciucci J (2016) Lymphedema: a general outline of its anatomical base. J Reconstr Microsurg 32(1):2–9. https://doi.org/10.1055/s-0035-1560038

    Article  Google Scholar 

  30. Johnson AR, Fleishman A, Granoff MD et al (2021) Evaluating the impact of immediate lymphatic reconstruction for the surgical prevention of lymphedema. Plast Reconstr Surg. https://doi.org/10.1097/PRS.0000000000007636

    Article  Google Scholar 

  31. Akita S, Nakamura R, Yamamoto N et al (2016) early detection of lymphatic disorder and treatment for lymphedema following breast cancer. Plast Reconstr Surg 138(2):192e–202e. https://doi.org/10.1097/PRS.0000000000002337

    Article  Google Scholar 

  32. Johnson AR, Granoff MD, Lee BT, Padera TP, Bouta EM, Singhal D (2019) The impact of taxane-based chemotherapy on the lymphatic system. Ann Plast Surg 82(S4 Suppl 3):S173–S178. https://doi.org/10.1097/SAP.0000000000001884

    Article  Google Scholar 

  33. Cariati M, Bains SK, Grootendorst MR et al (2015) Adjuvant taxanes and the development of breast cancer-related arm lymphoedema. Br J Surg 102(9):1071–1078. https://doi.org/10.1002/bjs.9846

    Article  Google Scholar 

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Acknowledgements

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Funding

This work was partially supported by the National Heart, Lung, and Blood Institute of the National Institutes of Health (https://www.nhlbi.nih.gov/) under Award Number R01HL157991 (received by author D.S.), and the 2022 JOBST Lymphatic Research Grant awarded by the Boston Lymphatic Symposium, Inc. (received by author R.F).

Author information

Authors and Affiliations

  1. Division of Plastic and Reconstructive Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA

    Rosie Friedman, Valeria P. Bustos, Jaime Pardo, Elizabeth Tillotson & Dhruv Singhal

  2. Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA

    Kevin Donohoe

  3. Department of Surgery, Tufts University Medical Center, Boston, MA, USA

    Abhishek Chatterjee

  4. University of Buenos Aires, Buenos Aires, Argentina

    José Luis Ciucci

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  1. Rosie Friedman
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by RF, VB, JP, ET, and DS. The first draft of the manuscript was written by RF and all authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Dhruv Singhal.

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Conflict of interest

The authors have no relevant financial or other non-financial interests to disclose.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Beth Israel Deaconess Medical Center Institutional review board, Protocol # 2021P000859.

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Supplementary Information

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Supplementary file1: Video, Supplementary Digital Content 1. A video of ICG lymphography images demonstrating the variation of forearm connectivity of the tricipital pathway, including the long bundle, short bundle, and no bundle.

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Friedman, R., Bustos, V.P., Pardo, J. et al. Superficial and functional imaging of the tricipital lymphatic pathway: a modern reintroduction. Breast Cancer Res Treat 197, 235–242 (2023). https://doi.org/10.1007/s10549-022-06777-z

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  • DOI: https://doi.org/10.1007/s10549-022-06777-z

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