DOI QR코드

DOI QR Code

Comprehensive Evaluation of the Current Knowledge on Breast Implant Associated-Anaplastic Large Cell Lymphoma

  • Yoo, Hyokyung (Department of Plastic and Reconstructive Surgery, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Park, Ji-Ung (Department of Plastic and Reconstructive Surgery, Seoul National University Boramae Hospital, Seoul National University College of Medicine) ;
  • Chang, Hak (Department of Plastic and Reconstructive Surgery, Seoul National University Hospital, Seoul National University College of Medicine)
  • Published : 2022.03.15

Abstract

Breast implant-associated anaplastic large cell lymphoma (BIA-ALCL) is a recently spotlighted T-cell origin non-Hodgkin's lymphoma with an increasing incidence of over 800 cases and 33 deaths reported worldwide. Development of BIA-ALCL is likely a complex process involving many factors, such as the textured implant surface, bacterial biofilm growth, immune response, and patient genetics. As the incidence of BIA-ALCL is expected to increase, it is important for all surgeons and physicians to be aware of this disease entity and acquire thorough knowledge of current evidence-based guidelines and recommendations. Early detection, accurate diagnosis, and appropriate treatment are the foundations of current care.

Keywords

References

  1. Ghosh T, Duncavage E, Mehta-Shah N, McGuire PA, Tenenbaum M, Myckatyn TM. A cautionary tale and update on breast implant-associated anaplastic large cell lymphoma (BIA-ALCL). Aesthet Surg J 2020;40(12):1288-1300 https://doi.org/10.1093/asj/sjz377
  2. Keech JA Jr, Creech BJ. Anaplastic T-cell lymphoma in proximity to a saline-filled breast implant. Plast Reconstr Surg 1997;100(02):554-555 https://doi.org/10.1097/00006534-199708000-00064
  3. Taylor CR, Siddiqi IN, Brody GS. Anaplastic large cell lymphoma occurring in association with breast implants: review of pathologic and immunohistochemical features in 103 cases. Appl Immunohistochem Mol Morphol 2013;21(01):13-20 https://doi.org/10.1097/PAI.0b013e318266476c
  4. Laurent C, Delas A, Gaulard P, et al. Breast implant-associated anaplastic large cell lymphoma: two distinct clinicopathological variants with different outcomes. Ann Oncol 2016;27(02):306-314 https://doi.org/10.1093/annonc/mdv575
  5. Duvic M, Moore D, Menter A, Vonderheid EC. Cutaneous T-cell lymphoma in association with silicone breast implants. J Am Acad Dermatol 1995;32(06):939-942 https://doi.org/10.1016/0190-9622(95)91328-9
  6. Ramos-Gallardo G, Cuenca-Pardo J, Rodriguez-Olivares E, et al. Breast implant and anaplastic large cell lymphoma meta-analysis. J Invest Surg 2017;30(01):56-65 https://doi.org/10.1080/08941939.2016.1215576
  7. George EV, Pharm J, Houston C, et al. Breast implant-associated ALK-negative anaplastic large cell lymphoma: a case report and discussion of possible pathogenesis. Int J Clin Exp Pathol 2013;6(08):1631-1642
  8. Lazzeri D, Agostini T, Bocci G, et al. ALK-1-negative anaplastic large cell lymphoma associated with breast implants: a new clinical entity. Clin Breast Cancer 2011;11(05):283-296 https://doi.org/10.1016/j.clbc.2011.03.020
  9. Eaves F III, Nahai F. Anaplastic large cell lymphoma and breast implants: FDA report. Aesthet Surg J 2011;31(04):467-468 https://doi.org/10.1177/1090820X11407872
  10. Kim IK, Hong KY, Lee CK, et al. Analysis of the molecular signature of breast implant-associated anaplastic large cell lymphoma in an Asian patient. Aesthet Surg J 2021;41(05):NP214-NP222 https://doi.org/10.1093/asj/sjaa398
  11. Yoon ES. Current status of breast implant-associated anaplastic large cell lymphoma in South Korea. J Korean Med Assoc 2021;64:5-9 https://doi.org/10.5124/jkma.2021.64.1.5
  12. DeCoster RC, Lynch EB, Bonaroti AR, et al. Breast implant-associated anaplastic large cell lymphoma: an evidence-based systematic review. Ann Surg 2021;273(03):449-458 https://doi.org/10.1097/SLA.0000000000004365
  13. Marra A, Viale G, Pileri SA, et al. Breast implant-associated anaplastic large cell lymphoma: a comprehensive review. Cancer Treat Rev 2020;84:101963 https://doi.org/10.1016/j.ctrv.2020.101963
  14. Collett DJ, Rakhorst H, Lennox P, Magnusson M, Cooter R, Deva AK. Current risk estimate of breast implant-associated anaplastic large cell lymphoma in textured breast implants. Plast Reconstr Surg 2019;143(3S A Review of Breast Implant-Associated Anaplastic Large Cell Lymphoma):30S-40S https://doi.org/10.1097/PRS.0000000000005567
  15. McCarthy CM, Loyo-Berrios N, Qureshi AA, et al. Patient registry and outcomes for breast implants and anaplastic large cell lymphoma etiology and epidemiology (PROFILE): initial report of findings, 2012-2018. Plast Reconstr Surg 2019;143(3S A Review of Breast Implant-Associated Anaplastic Large Cell Lymphoma):65S-73S https://doi.org/10.1097/PRS.0000000000005571
  16. Doren EL, Miranda RN, Selber JC, et al. U.S. Epidemiology of breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2017;139(05):1042-1050 https://doi.org/10.1097/PRS.0000000000003282
  17. Jacombs A, Tahir S, Hu H, et al. In vitro and in vivo investigation of the influence of implant surface on the formation of bacterial biofilm in mammary implants. Plast Reconstr Surg 2014;133(04):471e-480e https://doi.org/10.1097/PRS.0000000000000020
  18. Wang F, Meng W, Wang B, Qiao L. Helicobacter pylori-induced gastric inflammation and gastric cancer. Cancer Lett 2014;345(02):196-202 https://doi.org/10.1016/j.canlet.2013.08.016
  19. Brody GS. The case against biofilm as the primary initiator of breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2016;137(04):766e-767e https://doi.org/10.1097/01.prs.0000480003.80422.03
  20. Clemens MW, McGuire PA. Discussion: a prospective approach to inform and treat 1340 patients at risk for BIA-ALCL. Plast Reconstr Surg 2019;144(01):57-59 https://doi.org/10.1097/PRS.0000000000005756
  21. TGA update on rare cancer associated with breast implants. Therapeutic Goods Administration. 2016; c2021. Available at: https://www.tga.gov.au/node/733726
  22. de Boer M, van Leeuwen FE, Hauptmann M, et al. Breast implants and the risk of anaplastic large-cell lymphoma in the breast. JAMA Oncol 2018;4(03):335-341 https://doi.org/10.1001/jamaoncol.2017.4510
  23. Loch-Wilkinson A, Beath KJ, Knight RJW, et al. Breast implant-associated anaplastic large cell lymphoma in Australia and New Zealand: high-surface-area textured implants are associated with increased risk. Plast Reconstr Surg 2017;140(04):645-654 https://doi.org/10.1097/PRS.0000000000003654
  24. Lee JH. Breast implant-associated anaplastic large-cell lymphoma (BIA-ALCL). Yeungnam Univ J Med 2021;38(03):175-182 https://doi.org/10.12701/yujm.2020.00801
  25. Ashley FL. Further studies on the natural-Y breast prosthesis. Plast Reconstr Surg 1972;49(04):414-419 https://doi.org/10.1097/00006534-197204000-00009
  26. O'Shaughnessy K. Evolution and update on current devices for prosthetic breast reconstruction. Gland Surg 2015;4(02):97-110 https://doi.org/10.3978/j.issn.2227-684X.2015.03.09
  27. Henderson PW, Nash D, Laskowski M, Grant RT. Objective comparison of commercially available breast implant devices. Aesthetic Plast Surg 2015;39(05):724-732 https://doi.org/10.1007/s00266-015-0537-1
  28. Brody GS, Deapen D, Taylor CR, et al. Anaplastic large cell lymphoma occurring in women with breast implants: analysis of 173 cases. Plast Reconstr Surg 2015;135(03):695-705 https://doi.org/10.1097/PRS.0000000000001033
  29. de Jong D, Vasmel WL, de Boer JP, et al. Anaplastic large-cell lymphoma in women with breast implants. JAMA 2008;300(17):2030-2035 https://doi.org/10.1001/jama.2008.585
  30. Clemens MW. BIA-ALCL Resources: by the numbers, and what they mean. c2021. Available at: https://www.plasticsurgery.-org/for-medical-professionals/health-policy/bia-alcl-physician--resources/by-the-numbers
  31. Calobrace MB, Schwartz MR, Zeidler KR, Pittman TA, Cohen R, Stevens WG. Long-term safety of textured and smooth breast implants. Aesthet Surg J 2017;38(01):38-48 https://doi.org/10.1093/asj/sjx157
  32. Hu H, Jacombs A, Vickery K, Merten SL, Pennington DG, Deva AK. Chronic biofilm infection in breast implants is associated with an increased T-cell lymphocytic infiltrate: implications for breast implant-associated lymphoma. Plast Reconstr Surg 2015;135(02):319-329 https://doi.org/10.1097/PRS.0000000000000886
  33. Atlan M, Nuti G, Wang H, Decker S, Perry T. Breast implant surface texture impacts host tissue response. J Mech Behav Biomed Mater 2018;88:377-385 https://doi.org/10.1016/j.jmbbm.2018.08.035
  34. Mempin M, Hu H, Chowdhury D, Deva A, Vickery K. The A, B and C's of silicone breast implants: anaplastic large cell lymphoma, biofilm and capsular contracture. Materials (Basel) 2018;11(12):2393 https://doi.org/10.3390/ma11122393
  35. Hu H, Johani K, Almatroudi A, et al. Bacterial biofilm infection detected in breast implant-associated anaplastic large-cell lymphoma. Plast Reconstr Surg 2016;137(06):1659-1669 https://doi.org/10.1097/PRS.0000000000002010
  36. McGuire P, Reisman NR, Murphy DK. Risk factor analysis for capsular contracture, malposition, and late seroma in subjects receiving Natrelle 410 form-stable silicone breast implants. Plast Reconstr Surg 2017;139(01):1-9 https://doi.org/10.1097/PRS.0000000000002837
  37. Cordeiro PG, Ghione P, Ni A, et al. Risk of breast implant associated anaplastic large cell lymphoma (BIA-ALCL) in a cohort of 3546 women prospectively followed long term after reconstruction with textured breast implants. J Plast Reconstr Aesthet Surg 2020;73(05):841-846 https://doi.org/10.1016/j.bjps.2019.11.064
  38. Decision du 02/04/2019 portant interdiction de mise sur le marche, de distribution, de publicite et d'utilisation d'implants mammaires a enveloppe macro-texturee et d'implants mammaires polyurethane, ainsi que retrait de ces produits. c2021. Available at: https://ansm.sante.fr/Decisions/Injonctions-decisions-de-police-sanitaire-sanctions-financieres-interdictionsde-publicite-Decisions-de-police-sanitaire/Decisiondu-02-04-2019-portant-interdiction-de-mise-sur-le-marche-de-distribution-de-publicite-et-d-utilisation-d-implants-mammaires-aenveloppe-macro-texturee-et-d-implants-mammaires-polyurethane-ainsi-que-retrait-de-ces-produits
  39. Health Canada advises Allergan of its intent to suspend its licences for Biocell breast implants as a precautionary measure. C2021. Available at: https://healthycanadians.gc.ca/recall-alertrappel-avis/hc-sc/2019/69520a-eng.php
  40. Statement from FDA Principal Deputy Commissioner Amy Abernethy, M.D., Ph.D., and Jeff Shuren, M.D., J.D., director of the FDA's Center for Devices and Radiological Health on FDA's new efforts to protect women's health and help to ensure the safety of breast implants. C2021. Available at: https://www.fda.gov/news-events/pressannouncements/statement-fda-principal-deputy-commissioner-amyabernethy-md-phd-and-jeff-shuren-md-jd-director-fdas
  41. Deva AK, Turner SD, Kadin ME, et al. Etiology of breast implant-associated anaplastic large cell lymphoma (BIA-ALCL): current directions in research. Cancers (Basel) 2020;12(12):3861 https://doi.org/10.3390/cancers12123861
  42. Story SK, Schowalter MK, Geskin LJ. Breast implant-associated ALCL: a unique entity in the spectrum of CD30+ lymphoproliferative disorders. Oncologist 2013;18(03):301-307 https://doi.org/10.1634/theoncologist.2012-0238
  43. Zucca E, Bertoni F, Vannata B, Cavalli F. Emerging role of infectious etiologies in the pathogenesis of marginal zone B-cell lymphomas. Clin Cancer Res 2014;20(20):5207-5216 https://doi.org/10.1158/1078-0432.CCR-14-0496
  44. Hart AM, Lechowicz MJ, Peters KK, Holden J, Carlson GW. Breast implant-associated anaplastic large cell lymphoma: report of 2 cases and review of the literature. Aesthet Surg J 2014;34(06):884-894 https://doi.org/10.1177/1090820x14539503
  45. Kadin ME, Morgan J, Xu H, et al. IL-13 is produced by tumor cells in breast implant-associated anaplastic large cell lymphoma: implications for pathogenesis. Hum Pathol 2018;78:54-62 https://doi.org/10.1016/j.humpath.2018.04.007
  46. Blombery P, Thompson ER, Jones K, et al. Whole exome sequencing reveals activating JAK1 and STAT3 mutations in breast implant-associated anaplastic large cell lymphoma anaplastic large cell lymphoma. Haematologica 2016;101(09):e387-e390 https://doi.org/10.3324/haematol.2016.146118
  47. Laurent C, Nicolae A, Laurent C, et al. Gene alterations in epigenetic modifiers and JAK-STAT signaling are frequent in breast implant-associated ALCL. Blood 2020;135(05):360-370
  48. Di Napoli A, Jain P, Duranti E, et al. Targeted next generation sequencing of breast implant-associated anaplastic large cell lymphoma reveals mutations in JAK/STAT signalling pathway genes, TP53 and DNMT3A. Br J Haematol 2018;180(05):741-744 https://doi.org/10.1111/bjh.14431
  49. Yoon HJ, Choe JY, Jeon YK. Mucosal CD30-positive T-cell lymphoproliferative disorder arising in the oral cavity following dental implants: report of the first case. Int J Surg Pathol 2015;23(08):656-661 https://doi.org/10.1177/1066896915599059
  50. Manikkam Umakanthan J, McBride CL, Greiner T, et al. Bariatric implant-associated anaplastic large-cell lymphoma. J Oncol Pract 2017;13(12):838-839 https://doi.org/10.1200/JOP.2017.026153
  51. Shauly O, Gould DJ, Siddiqi I, Patel KM, Carey J. The first reported case of gluteal implant-associated anaplastic large cell lymphoma (ALCL). Aesthet Surg J 2019;39(07):NP253-NP258 https://doi.org/10.1093/asj/sjz044
  52. Engberg AK, Bunick CG, Subtil A, Ko CJ, Girardi M. Development of a plaque infiltrated with large CD30+ T cells over a silicone-containing device in a patient with history of Sezary syndrome. J Clin Oncol 2013;31(06):e87-e89 https://doi.org/10.1200/JCO.2012.42.9241
  53. Kellogg BC, Hiro ME, Payne WG. Implant-associated anaplastic large cell lymphoma: beyond breast prostheses. Ann Plast Surg 2014;73(04):461-464 https://doi.org/10.1097/SAP.0b013e31827faff2
  54. Hallab NJ, Samelko L, Hammond D. The inflammatory effects of breast implant particulate shedding: comparison with orthopedic implants. Aesthet Surg J 2019;39(Suppl 1):S36-S48 https://doi.org/10.1093/asj/sjy335
  55. Palraj B, Paturi A, Stone RG, et al. Soft tissue anaplastic large T-cell lymphoma associated with a metallic orthopedic implant: case report and review of the current literature. J Foot Ankle Surg 2010;49(06):561-564 https://doi.org/10.1053/j.jfas.2010.08.009
  56. Thienpaitoon P, Disphanurat W, Warnnissorn N. Breast implant-associated anaplastic large cell lymphoma in an Asian patient: the firstcase report from Thailand. Arch Plast Surg 2020;47(05):478-482 https://doi.org/10.5999/aps.2020.00108
  57. Clemens MW, Medeiros LJ, Butler CE, et al. Complete surgical excision is essential for the management of patients with breast implant-associated anaplastic large-cell lymphoma. J Clin Oncol 2016;34(02):160-168
  58. Leberfinger AN, Behar BJ, Williams NC, et al. Breast implant-associated anaplastic large cell lymphoma: a systematic review. JAMA Surg 2017;152(12):1161-1168 https://doi.org/10.1001/jamasurg.2017.4026
  59. Dashevsky BZ, Gallagher KM, Grabenstetter A, et al. Breast implant-associated anaplastic large cell lymphoma: clinical and imaging findings at a large US cancer center. Breast J 2019;25(01):69-74 https://doi.org/10.1111/tbj.13161
  60. Mehta-Shah N, Clemens MW, Horwitz SM. How I treat breast implant-associated anaplastic large cell lymphoma. Blood 2018;132(18):1889-1898 https://doi.org/10.1182/blood-2018-03-785972
  61. NCCN. National Comprehensive Cancer Network. C2021. Available at: https://www.nccn.org/professionals/physician_gls/pdf/tcell.pdf
  62. Adrada BE, Miranda RN, Rauch GM, et al. Breast implant-associated anaplastic large cell lymphoma: sensitivity, specificity, and findings of imaging studies in 44 patients. Breast Cancer Res Treat 2014;147(01):1-14 https://doi.org/10.1007/s10549-014-3034-3
  63. Clemens MW, Brody GS, Mahabir RC, Miranda RN. How to diagnose and treat breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2018;141(04):586e-599e https://doi.org/10.1097/PRS.0000000000004262
  64. Montes-Mojarro IA, Steinhilber J, Bonzheim I, Quintanilla-Martinez L, Fend F. The pathological spectrum of systemic anaplastic large cell lymphoma (ALCL). Cancers (Basel) 2018;10(04):107 https://doi.org/10.3390/cancers10040107
  65. Clemens MW, Miranda RN. Coming of age: breast implant-associated anaplastic large cell lymphoma after 18 years of investigation. Clin Plast Surg 2015;42(04):605-613 https://doi.org/10.1016/j.cps.2015.06.006
  66. Clemens MW, Horwitz SM. NCCN consensus guidelines for the diagnosis and management of breast implant-associated anaplastic large cell lymphoma. Aesthet Surg J 2017;37(03):285-289 https://doi.org/10.1093/asj/sjw259
  67. Miranda RN, Aladily TN, Prince HM, et al. Breast implant-associated anaplastic large-cell lymphoma: long-term follow-up of 60 patients. J Clin Oncol 2014;32(02):114-120 https://doi.org/10.1200/JCO.2013.52.7911
  68. Armitage JO. Staging non-Hodgkin lymphoma. CA Cancer J Clin 2005;55(06):368-376 https://doi.org/10.3322/canjclin.55.6.368
  69. Swerdlow SH, Campo E, Harris N, et al. World Health Organization Classification of Tumours of Haematopoietic and Lymphoid Tissues. 4th ed. Lyon, France: IARC Press; 2017
  70. Chiarle R, Simmons WJ, Cai H, et al. Stat3 is required for ALK-mediated lymphomagenesis and provides a possible therapeutic target. Nat Med 2005;11(06):623-629 https://doi.org/10.1038/nm1249
  71. Crescenzo R, Abate F, Lasorsa E, et al; European T-Cell Lymphoma Study Group, T-Cell Project: Prospective Collection of Data in Patients with Peripheral T-Cell Lymphoma and the AIRC 5xMille Consortium "Genetics-Driven Targeted Management of Lymphoid Malignancies" Convergent mutations and kinase fusions lead to oncogenic STAT3 activation in anaplastic large cell lymphoma. Cancer Cell 2015;27(04):516-532 https://doi.org/10.1016/j.ccell.2015.03.006
  72. Feldman AL, Dogan A, Smith DI, et al. Discovery of recurrent t(6;7) (p25.3;q32.3) translocations in ALK-negative anaplastic large cell lymphomas by massively parallel genomic sequencing. Blood 2011;117(03):915-919 https://doi.org/10.1182/blood-2010-08-303305
  73. Parrilla Castellar ER, Jaffe ES, Said JW, et al. ALK-negative anaplastic large cell lymphoma is a genetically heterogeneous disease with widely disparate clinical outcomes. Blood 2014;124(09):1473-1480 https://doi.org/10.1182/blood-2014-04-571091
  74. Vasmatzis G, Johnson SH, Knudson RA, et al. Genome-wide analysis reveals recurrent structural abnormalities of TP63 and other p53-related genes in peripheral T-cell lymphomas. Blood 2012;120(11):2280-2289 https://doi.org/10.1182/blood-2012-03-419937
  75. Vase MO, Friis S, Bautz A, Bendix K, Sorensen HT, d'Amore F. Breast implants and anaplastic large-cell lymphoma: a danish population-based cohort study. Cancer Epidemiol Biomarkers Prev 2013;22(11):2126-2129 https://doi.org/10.1158/1055-9965.EPI-13-0633
  76. Warschkow R, Cerny T, Schmied BM, Guller U, Thuerlimann B, Joerger M. A population-based analysis of secondary malignancies in breast cancer patients receiving breast reconstruction. Br J Cancer 2016;115(01):80-84 https://doi.org/10.1038/bjc.2016.108
  77. Campanale A, Di Napoli A, Ventimiglia M, et al. Chest wall infiltration is a critical prognostic factor in breast implant-associated anaplastic large-cell lymphoma affected patients. Eur J Cancer 2021;148:277-286 https://doi.org/10.1016/j.ejca.2021.01.041
  78. Oishi N, Brody GS, Ketterling RP, et al. Genetic subtyping of breast implant-associated anaplastic large cell lymphoma. Blood 2018;132(05):544-547 https://doi.org/10.1182/blood-2017-12-821868
  79. Laurent C, Haioun C, Brousset P, Gaulard P. New insights into breast implant-associated anaplastic large cell lymphoma. Curr Opin Oncol 2018;30(05):292-300 https://doi.org/10.1097/CCO.0000000000000476
  80. Lechner MG, Lade S, Liebertz DJ, et al. Breast implant-associated, ALK-negative, T-cell, anaplastic, large-cell lymphoma: establishment and characterization of a model cell line (TLBR-1) for this newly emerging clinical entity. Cancer 2011;117(07):1478-1489 https://doi.org/10.1002/cncr.25654
  81. Kadin ME, Deva A, Xu H, et al. Biomarkers provide clues to early events in the pathogenesis of breast implant-associated anaplastic large cell lymphoma. Aesthet Surg J 2016;36(07):773-781 https://doi.org/10.1093/asj/sjw023
  82. Quesada AE, Zhang Y, Ptashkin R, et al. Next generation sequencing of breast implant-associated anaplastic large cell lymphomas reveals a novel STAT3-JAK2 fusion among other activating genetic alterations within the JAK-STAT pathway. Breast J 2021;27(04):314-321 https://doi.org/10.1111/tbj.14205
  83. Turner SD, Inghirami G, Miranda RN, Kadin ME. Cell of origin and immunologic eventsin the pathogenesis of breast implant-associated anaplastic large-cell lymphoma. Am J Pathol 2020;190(01):2-10 https://doi.org/10.1016/j.ajpath.2019.09.005