https://doi.org/10.4081/vl.2024.12207

When lymphatics, the Devil and Maleficent melanoma meet

A narrative survey on the lymphogenous spread of metastasis

Vol. 13 (2024): Early Access
Published: 9 February 2024
lymphatics, lymph nodes, lymphatic system, melanoma, metastatic melanoma, metastatic spread, lymph node dissection, sentinel lymph node, lymphography
Abstract Views: 1115
PDF: 123
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Giancarlo Pansini
pgc@unife.it
https://orcid.org/0000-0002-8092-2704
Formerly, Clinical Associate Professor of Surgery at University of Ferrara’s School of Medicine; Consultant and Lead Clinician of Complex Cancer Surgery and Epatobiliary & Pancreatic Surgery, S. Anna Hospital, Ferrara, Italy.

The subject of lymphatics and cancer had been in the air for a lot of time. The Editor, Paolo Zamboni, came up at first with the idea of writing about this issue and was good enough to ask me to attempt this work after I provided him with images of mesenteric, intestinal and hepatic metastases from a young patient I treated for a malignant melanoma of the skin, in the last year of my surgical practice.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Crossref
Scopus
Google Scholar
Europe PMC
Pansini G. On the unlocked secrets of the lymphatics and lymphatic circulation. Veins and Lymphatics. 2023;12:12206. DOI: https://doi.org/10.4081/vl.2023.12206
Brautigan R. So the Wind Won’t Blow It All Away. New York, NY, USA: Delacorte Press/Seymour Lawrence; 1982.
Ariel IM. Malignant Melanoma. New York, NY, USA: Appleton-Century-Crofts; 1981.
Pansini R, Portaluppi F, Pansini GC. Trattato di Oncologia Cardiaca. Padova, Italy: Piccin Nuova Libraria; 1999.
Balinski AM, Vasbinder AL, Kerndt CC. Metastatic Melanoma of The Heart: Retrospective Cohort Study and Systematic Review of Prevalence, Clinical Characteristics, and Outcomes. Cancer Med. 2023;12:2356-67. DOI: https://doi.org/10.1002/cam4.5058
North JP, Bastian BC, Lazar AJ. In: McKee’s Pathology of the Skin, With Clinical Correlation. 5th Edition. London, UK: Elsevier Ltd, 2020.
NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). Melanoma: Cutaneous|Version 2.2023 — March 10, 2023. Available from: https://www.nccn.org/guidelines/category_1
ECIS – European Cancer Information System. Skin Melanoma Burden in EU-27. Available from: https://ecis.jrc.ec.europa.eu
Bucchi L, Mancini S, Zamagni F, et al. Patient Presentation, Skin Biopsy Utilization and Cutaneous Malignant Melanoma Incidence and Mortality in Northern Italy: Trends and Correlations. J Eur Acad Dermatol Venereol. 2023;37:1-10. DOI: https://doi.org/10.1111/jdv.18635
Zamagni F, Bucchi L, Mancini S, et al. The Relative Contribution of The Decreasing Trend in Tumour Thickness to the 2010s Increase in Net Survival from Cutaneous Malignant Melanoma in Italy: A Population-Based Investigation. British Journal of Dermatology. 2022;187:52-63. DOI: https://doi.org/10.1111/bjd.21051
Bucchi L, Mancini S, Crocetti E, et al. Mid-term trends and recent birth-cohort-dependent changes in incidence rates of cutaneous malignant melanoma in Italy. Int J Cancer. 2021;148:835-44. DOI: https://doi.org/10.1002/ijc.33259
Ascierto PA. In: I Numeri del Cancro in Italia-Rapporto 2022. 12a Ed.| Italian Cancer Figures-Report 2022, 12th Ed. 2022.
Marx V. Tracking Metastasis and Tricking Cancer. Nature. 2013;494:131-6. DOI: https://doi.org/10.1038/494131a
Lee JE. Factors Associated with Melanoma Incidence and Prognosis. Semin Sur Oncol. 1996;12:379-85. DOI: https://doi.org/10.1002/(SICI)1098-2388(199611/12)12:6<379::AID-SSU2>3.0.CO;2-7
Curti BD, Faries MB. Recent Advances in the Treatment of Melanoma. N Engl J Med. 2021;384;:2229-40. DOI: https://doi.org/10.1056/NEJMra2034861
Helvind NMN, Brinch-Møller Weitemeyer M, et al. Stage-Specific Risk of Recurrence and Death from Melanoma in Denmark, 2008-2021. A National Observational Cohort Study of 25 720 Patients with Stage IA to IV Melanoma. JAMA Dermatol. 2023;159:1213-22. DOI: https://doi.org/10.1001/jamadermatol.2023.3256
Calomarde-Rees L, Garcia-Calatayud R, Caballero CR, et al. Risk Factors for Lymphatic and Hematogenous Dissemination in Patients with Stages I to II Cutaneous Melanoma. JAMA Dermatol. 2019;155:679-87. DOI: https://doi.org/10.1001/jamadermatol.2019.0069
Batemi SB, Nguyen P, Eskander A, et al. Changes in Health Care Costs, Survival, and Time Toxicity in the Era of Immunotherapy and Targeted Systemic Therapy for Melanoma. JAMA Dermatol. 2023;159:1195-204. DOI: https://doi.org/10.1001/jamadermatol.2023.3179
Mukherjee S. The Emperor of All Maladies. A Biography of Cancer. London, UK: 4th Estate; 2011.
Haagensen CD. The Lymphatics in Cancer. Philadelphia, USA: WB Saunders Company; 1972.
Gray JH. The Relation of Lymphatic Vessels to the Spread of Cancer. Br J Surgery. 1939;26:462-95. DOI: https://doi.org/10.1002/bjs.18002610303
Ottaviani G. L’uso del Neoprene nella Iniezione dei Vasi Linfatici. Ateneo Parmense, 25:109, 1954.
Kinmonth JB. The Lymphatics. Disease, Lymphography and Surgery. London, UK: Edward Arnold; 1972.
Battezzati M, Donini I. The Lymphatic System. Padua and London: Piccin Medical Books; 1972.
Lamki LM, Logic JR. Defining Lymphatic Drainage Patterns with Cutaneous Lymphoscintigraphy. In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Aron A, Zavaleta C. Current and Developing Lymphatic Imaging Approaches for Elucidation of Functional Mechanisms and Disease Progression. Mol Imaging Biol. 2024;26:1-16. DOI: https://doi.org/10.1007/s11307-023-01827-4
AJCC Cancer Staging Manual, 8th Edition. Melanoma of the Skin. Cham, Switzerland: Springer International Publishing; 2017.
Mukherjee S. The Song of the Cell. London, UK: Bodley Head, 2022. 496 pp.
Barnett R. The Sick Rose. Disease and Art of Medical Illustration. London, UK: Thames & Hudson Ltd.; 2014.
Le Dran H.F. Traité des Operations de Chirurgie. Paris, 1742, and Bruxelles, Widow of Vase, 1774.
Virchow R. Cellularpathologie. 4th edn. Berlin, Germany: Hirschwald, 1858.
Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009;9:285-93. DOI: https://doi.org/10.1038/nrc2621
Paget S. The Distribution of Secondary Growths in Cancer of The Breast. Lancet. 1889;133:571-3. DOI: https://doi.org/10.1016/S0140-6736(00)49915-0
Talmage JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 2010;70:5649-69. DOI: https://doi.org/10.1158/0008-5472.CAN-10-1040
Beckhard AJ, Crane WD. Cancer, Cocaine and Courage. The Story of Dr. William Halsted. New York, USA: Julian Messner Inc. 1960.
Imber G. Genius on the Edge: The Bizarre Double Life of Dr. William Stewart Halsted. New York, NY, USA: Kaplan Publishing; 2010.
Menetrier P. Cancro. XIII Tomo in: Nuovo Trattato di Medicina Interna di Gilbert A e Thoinot L. Torino, Italy: Unione Tipografica Torinese; 1910.
Menetrier P. Cancer, Tome XIII Noveau Traitè de Mèdecine et Thèrapeutique. Paris, France: Baillièr; 1908.
Willis RA. The Spread of Tumours in the Human Body. London, UK: J.&A. Churchill; 1934.
Ewing J. Neoplastic diseases. 2th Ed. Philadelphia, USA: WB Saunders; 1934.
Time The Weekly Newsmagazine. Vol XVII, 2, Jan 12,1931.
Bland-Sutton J. Tumours, Innocent and Malignant. Their Clinical Characters and Appropriate Treatment. London, UK: Cassell and Company Ltd; 1917.
Taylor GW, Nathanson IT. Lymph Node Metastases. Incidence and Surgical Treatment in Neoplastic Disease. London, UK: Oxford University Press; 1942
Clark WH. Malignant melanoma as a paradigm for the study of cancer. In: Advances in the Biology and Clinical Management of Melanoma. Proceedings of the 35th Annual Clinical Conference and 42nd Annual Special Pathology Program, 1991 Nov 20-23, Houston, Texas, USA.
Rubin H. On The Nature of Enduring Modifications Induced in Cells and Organism. Am J Phisiol. 1990;258, L19-24. DOI: https://doi.org/10.1152/ajplung.1990.258.2.L19
Coso S, Bovay Epetrova TV. Pressing The Right Buttons: Signaling in Lymphangiogenesis. Blood. 2014;123:2614-24 . DOI: https://doi.org/10.1182/blood-2013-12-297317
Folkman J. Tumour angiogenesis: Therapeutic Implications. N Engl J Med. 1971;285:1182-6. DOI: https://doi.org/10.1056/NEJM197111182852108
Folkman J. Tumour angiogenesis. Adv Cancer Res. 1985;43:175-203. DOI: https://doi.org/10.1016/S0065-230X(08)60946-X
Fidler IJ, Kripke ML. Metastasis results from pre-existing variant cells within a malignant tumour. Science. 1977;197:893-5. DOI: https://doi.org/10.1126/science.887927
Fidler IJ. The biology of cancer metastasis or, 'you cannot fix it if you do not know how it works'. Bioessays. 1991;13:551-4. DOI: https://doi.org/10.1002/bies.950131010
Fidler IJ. The “seed and soil” hypothesis revisited. The Lancet Oncology. 2011;128:2527-35. DOI: https://doi.org/10.1002/ijc.26031
Spiric Z, Eri Z, Eric M. Significance of Vascular Endothelial Growth Factor (VEGF)-C and VEGF-D in the Progression of Cutaneous Melanoma. Int J Surg Pathol. 2015;23:629-37. DOI: https://doi.org/10.1177/1066896915583694
Qian J, Huang C, Zhu Z. NFE2L3 promotes tumour progression and predicts a poor prognosis of bladder cancer. Carcinogenesis. 2022;43,5:457-68. DOI: https://doi.org/10.1093/carcin/bgac006
Pepper MS. Lymphangiogenesis and Tumour Metastasis. Myth or Realty? Clinical Cancer Research. 2001;7:461-8.
Achen MG, McColl BK, Stacker SA. Focus on lymphangiogenesis in tumour metastasis. Cancer Cell. 2005;7:121-7. DOI: https://doi.org/10.1016/j.ccr.2005.01.017
Eccles SA, Welch D. Metastasis: Recent Discoveries and Novel Treatment Strategies. Lancet. 2007;19:1742-57. DOI: https://doi.org/10.1016/S0140-6736(07)60781-8
Christiansen A, Detmar M. Lymphangiogenesis and cancer. Genes Cancer. 2011;2:1146-58. DOI: https://doi.org/10.1177/1947601911423028
Stacher S, William SP, Karnezis T. et al. Lymphangiogenesis and Lymphatic Vessel Remodelling In Cancer. Nature Reviews Cancer. 2014;14:152-72. DOI: https://doi.org/10.1038/nrc3677
Grüner BM, Fendt SM. Cancer Cell Stock Up in Lymph Vessels to Survive. Nature. 2020;585:36-7. DOI: https://doi.org/10.1038/d41586-020-02383-5
Ubellacker JM, Tasdogan A, Ramesh V, et al. Lymph protects metastasizing melanoma cells from ferroptosis. Nature. 2020;585:113-8. DOI: https://doi.org/10.1038/s41586-020-2623-z
Suresh R, Ziemys A, Holder AM. Dissecting the Lymphatic System to Predict Melanoma Metastasis. Front Oncol. 220;27:576190.
Tuma RS. Mechanism of Metastasis: Theories Focus on Microenvironment, Host factors, Genes. News JNCI 2008;100:1752-4. DOI: https://doi.org/10.1093/jnci/djn456
Klein CA. Parallel Progression of Primary Tumours and Metastases. Nat Rev Cancer. 2009;9:302-12. DOI: https://doi.org/10.1038/nrc2627
Collins VP, Loeffler RK, Tivey H. Observations on Growth Rates of Human Tumours. Am J Roentenol Radium Ther Nucl Med. 1956;76:988-1000.
Gofrit ON, Gofrit B, Roditi Y, et al. Patterns of metastases progression - The linear parallel ratio. PloS One. 2022;17:1-13. DOI: https://doi.org/10.1371/journal.pone.0274942
Ulmer A. Immunomagnetic Enrichment, Genomic Characterization, and Prognostic Impact of Circulating Melanoma Cells. Clin Cancer Res. 2004;10:531-7. DOI: https://doi.org/10.1158/1078-0432.CCR-0424-03
Quintana E. Efficient Tumour Formation by Single Human Melanoma Cells. Nature. 2008;456:593-8. DOI: https://doi.org/10.1038/nature07567
Frost R. Collected Poems, Prose, & Plays. New York, NY, USA: The Library of America; 1995.
McCune WS, Letterman GS. Malignant Melanoma. Ten Years Results Following Excision and Regional Gland Resection. Ann Surg. 1955;141:901. DOI: https://doi.org/10.1097/00000658-195506000-00015
Singletary ES, Balch CM., Urist MM. Surgical Treatment of Primary Melanoma. In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Balch CM, Milton GW, Cascinelli N, et al. Elective Lymph Node Dissection. In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Singletary ES, Balch CM. Recurrent Regional Metastases and Their Management. In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Balch CM. The Role of Elective Lymph Node Dissection in Melanoma: Rationale, Results, and Controversies. In: Advances in the Biology and Clinical Management of Melanoma. Proceedings of the 35th Annual Clinical Conference and 42nd Annual Special Pathology Program, 1991 Nov 20-23, Houston, Texas, USA.
Milton GW, Shaw HM, McCarthy WH, et al. Prophylactic lymph node dissection in clinical stage I cutaneous malignant melanoma: results of surgical treatment in 1319 patients. Br J Surg. 1982;69:108-11. DOI: https://doi.org/10.1002/bjs.1800690217
Lotze MT. The Role of Lymph Node Dissection in The Treatment of Cancer. In: Rosenberg SA, Surgical Treatment of Metastatic Cancer. Philadelphia, USA: JB Lippincott Company; 1987.
Sutherland CM, Mather FJ. Prophylactic lymph node dissection for malignant melanoma: What to do while we wait. J. Surg. Oncol. 1992,51:1-4. DOI: https://doi.org/10.1002/jso.2930510103
Arié A, Yamamoto T. Lymphedema Secondary to Melanoma Treatments: Diagnosis, Evaluation, And Treatments. Glob Health Med. 2020;31;2:227-34. DOI: https://doi.org/10.35772/ghm.2020.01022
Slagelse C, Petersen KL, Dahl JB. Persistent Postoperative Pain and Sensory Changes Following Lymph Node Excision In Melanoma Patients: A Topical Review. Melanoma Res 2014:24:93-8. DOI: https://doi.org/10.1097/CMR.0000000000000041
Morton DL. Intraoperative Lymphatic Mapping and Selective Lymphoadenectomy for Detection of Regional Metastases. In: Advances in the Biology and Clinical Management of Melanoma. Proceedings of the 35th Annual Clinical Conference and 42nd Annual Special Pathology Program, 1991 Nov 20-23, Houston, Texas, USA.
Morton DL. Technical details of intraoperative lymphatic mapping for early-stage melanoma Arch Surg. 1992;127:392-9. DOI: https://doi.org/10.1001/archsurg.1992.01420040034005
Portinari M, Baldini G, Carcoforo P, et al. The long-term prognostic impact of sentinel lymph node biopsy in patients with primary cutaneous melanoma: a prospective study with 10-year follow-up. Ann Surg Treat Res. 2018;95:286-96. DOI: https://doi.org/10.4174/astr.2018.95.5.286
Tropea S, Del Fiore P, Maurichi A, et al. The role of sentinel node tumour burden in modeling the prognosis of melanoma patients with positive sentinel node biopsy: an Italian Melanoma Intergroup study (N = 2,086). BMC Cancer. 2022;22:610. DOI: https://doi.org/10.1186/s12885-022-09705-y
Faries MB, Thompson JF, Cochran AJ, et al. Completion Dissection or Observation for Sentinel-Node Metastasis in Melanoma. N Engl J Med. 2017;376:2211-22. DOI: https://doi.org/10.1056/NEJMoa1613210
Gassenmaier M, Eigentler TK, Keim U, et al. Serial or parallel metastasis of cutaneous melanoma? A study of the German Central Malignant Melanoma Registry. J Invest Dermatol. 2017;137:2570. DOI: https://doi.org/10.1016/j.jid.2017.07.006
El Sharouni M-A, Stodell MD, Ahmed T, et al. Sentinel node biopsy in patients with melanoma improves the accuracy of staging when added to clinicopathological features of the primary tumour. Ann Oncol. 2021;32:375-83. DOI: https://doi.org/10.1016/j.annonc.2020.11.015
Faries MB, Testori AAE, Gershenwald JE. Sentinel node biopsy for primary cutaneous melanoma. Ann Oncol. 2021;32:290-2. DOI: https://doi.org/10.1016/j.annonc.2021.01.007
Ames FC. Management of local and regional recurrence. In: Advances in the Biology and Clinical Management of Melanoma. Proceedings of the 35th Annual Clinical Conference and 42nd Annual Special Pathology Program, 1991 Nov 20-23, Houston, Texas, USA.
Davis NC, McLeod GR. The History of Melanoma from Hunter to Handley (1787-1908). In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Nicolson GL, Cavanaugh P, Hamada J-J, Menter D. Role of Cell Adhesion, Invasion, and Growth in Organ-Specific Melanoma Metastasis. In: Advances in the Biology and Clinical Management of Melanoma. Proceedings of the 35th Annual Clinical Conference and 42nd Annual Special Pathology Program, 1991 Nov 20-23, Houston, Texas, USA.
Fidler IJ. The Biology of Melanoma Metastasis. In: Balch CM, Houghton AN, Milton GW, Sober AJ, and Soong S-J’s Cutaneous Melanoma. 2nd Ed. Philadelphia, USA: JB Lippincott Company; 1992.
Bear HD. Malignant Melanoma. Seminars in Surgical Oncology. 1996;12:377-453. DOI: https://doi.org/10.1002/(SICI)1098-2388(199611/12)12:6<377::AID-SSU1>3.3.CO;2-4
Albino AP, Reed JA, McNutt NS. Malignant Melanoma. In: De Vita, Hellman, and Rosenberg’s Cancer Principles & Practice of Oncology. 5th ed. Philadelphia, USA: Lippincott-Raven; 1997.
Ribas A, Read P, Slingluff Jr CL. Malignant Melanoma. In: De Vita, Hellman, and Rosenberg’s Cancer Principles & Practice of Oncology. 11th ed. Philadelphia, USA: Wolters Kluwer; 2019.
Mabeta P. Paradigms of vascularization in melanoma: Clinical significance and potential for therapeutic targeting. Biomed Pharmacother. 2020;127:110135. DOI: https://doi.org/10.1016/j.biopha.2020.110135
Davis N. Cover quotations in: Kopf AW, Friedman RJ, Rigel DS (prepared by). The Many Faces of Malignant Melanoma. New York, NY, USA: The Skin Cancer Foundation, 1991.
Bernstein PL. Against the Gods. The Remarkable Story of Risk. New York, NY, USA: John Wiley & Sons, Inc; 1996.

How to Cite

Pansini, G. (2024). When lymphatics, the Devil and <i>Maleficent</i> melanoma meet: A narrative survey on the lymphogenous spread of metastasis. Veins and Lymphatics, 13. https://doi.org/10.4081/vl.2024.12207
Copyright (c) 2024 the Author(s) Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.