Semin Plast Surg 2019; 33(04): 270-278
DOI: 10.1055/s-0039-1696998
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Finding Consensus After Two Decades of Breast Implant-Associated Anaplastic Large Cell Lymphoma

Mark W. Clemens
1   Department of Plastic Surgery, MD Anderson Cancer Center, Houston, Texas
,
Ryan C. DeCoster
2   Lucille P. Markey Cancer Center, University of Kentucky, Lexington, Kentucky
3   Division of Plastic and Reconstructive Surgery, Department of Surgery, University of Kentucky, Lexington, Kentucky
,
Berry Fairchild
4   Department of Surgery, University of Texas Health Science Center, Houston, Texas
,
Alexander A. Bessonov
5   City Cancer Center, St. Petersburg, Russia
,
Fabio Santanelli di Pompeo
6   Department of Plastic Surgery, Sant'Andrea Hospital, “Sapienza” University of Rome, Italy
› Author Affiliations
Funding Sources Dr. DeCoster is supported by a National Cancer Institute Surgeon-Scientist training grant (T32CA160003).
Further Information

Publication History

Publication Date:
17 October 2019 (online)

Abstract

Breast implant-associated anaplastic large cell lymphoma (BIA-ALCL) is an emerging and indolent, but potentially fatal cancer of the immune system that can develop around textured-surface breast implants. The World Health Organization first recognized BIA-ALCL as a unique clinical entity in 2016. To date, over 600 confirmed cases have been reported worldwide. BIA-ALCL most commonly presents with disease confined to the capsule, as a seroma or a mass adjacent to the implant. While BIA-ALCL has a fairly indolent clinical course, with an excellent prognosis in early stage disease, disseminated cancer and death have also been reported. In this review, the authors focus on the early diagnosis and treatment, including reconstructing the breast following BIA-ALCL, and also discuss recently updated National Comprehensive Cancer Network guidelines. They also review the current epidemiology and risk factors associated with BIA-ALCL. Finally, they discuss important medicolegal considerations and the bioethics surrounding the continued use of textured-surface breast implants.

 
  • References

  • 1 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
  • 2 Keech Jr JA, Creech BJ. Anaplastic T-cell lymphoma in proximity to a saline-filled breast implant. Plast Reconstr Surg 1997; 100 (02) 554-555
  • 3 McCarthy CM, Loyo-Berríos 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
  • 4 Eaves 3rd F, Nahai F. Anaplastic large cell lymphoma and breast implants: FDA report. Aesthetic Surg J 2011; 31 (04) 467-468
  • 5 Swerdlow SH, Campo E, Pileri SA. , et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 2016; 127 (20) 2375-2390
  • 6 Blombery P, Thompson ER, Prince HM. Molecular drivers of breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2019; 143 (3S A review of breast implant-associated anaplastic large cell lymphoma): 59S-64S
  • 7 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
  • 8 Carty MJ, Pribaz JJ, Antin JH. , et al. A patient death attributable to implant-related primary anaplastic large cell lymphoma of the breast. Plast Reconstr Surg 2011; 128 (03) 112e-118e
  • 9 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
  • 10 Srinivasa DR, Mirnada RR, Kaura A. , et al. Global adverse event reports of breast implant-associated ALCL: an international review of 40 government authority databases. Plast Reconstr Surg 2017; 139 (05) 1029-1039
  • 11 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
  • 12 Australian Therapeutic Goods Administration. Breast implants and anaplastic large cell lymphoma-Update: TGA's review of textured breast implants and preliminary outcomes. Available at https://www.tga.gov.au/alert/breast-implants-and-anaplastic-large-cell-lymphoma . Published 2019. Accessed July 13, 2019
  • 13 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
  • 14 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
  • 15 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
  • 16 Magnusson M, Beath K, Cooter R. , et al. The epidemiology of breast implant-associated anaplastic large cell lymphoma in Australia and New Zealand confirms the highest risk for Grade 4 surface breast implants. Plast Reconstr Surg 2019; 143 (05) 1285-1292
  • 17 Stein H, Mason DY, Gerdes J. , et al. The expression of the Hodgkin's disease associated antigen Ki-1 in reactive and neoplastic lymphoid tissue: evidence that Reed-Sternberg cells and histiocytic malignancies are derived from activated lymphoid cells. Blood 1985; 66 (04) 848-858
  • 18 Morris SW, Kirstein MN, Valentine MB. , et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 1994; 263 (5151): 1281-1284
  • 19 Oishi N, Brody GS, Ketterling RP. , et al. Genetic subtyping of breast implant-associated anaplastic large cell lymphoma. Blood 2018; 132 (05) 544-547
  • 20 Willemze R, Jaffe ES, Burg G. , et al. WHO-EORTC classification for cutaneous lymphomas. Blood 2005; 105 (10) 3768-3785
  • 21 Bekkenk MW, Geelen FA, van Voorst Vader PC. , et al. Primary and secondary cutaneous CD30(+) lymphoproliferative disorders: a report from the Dutch Cutaneous Lymphoma Group on the long-term follow-up data of 219 patients and guidelines for diagnosis and treatment. Blood 2000; 95 (12) 3653-3661
  • 22 Clemens MW, Nava MB, Rocco N, Miranda RN. Understanding rare adverse sequelae of breast implants: anaplastic large-cell lymphoma, late seromas, and double capsules. Gland Surg 2017; 6 (02) 169-184
  • 23 Rastogi P, Riordan E, Moon D, Deva AK. Theories of etiopathogenesis of breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2019; 143 (3S A review of breast implant-associated anaplastic large cell lymphoma): 23S-29S
  • 24 Di Napoli A, De Cecco L, Piccaluga PP. , et al. Transcriptional analysis distinguishes breast implant-associated anaplastic large cell lymphoma from other peripheral T-cell lymphomas. Mod Pathol 2019; 32 (02) 216-230
  • 25 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
  • 26 DeCoster RC, Vasconez HC, Butterfield TA. CRISPR/Cas9-mediated genomic editing: implications for engineering an animal model of breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2019 . Doi: 10.1097/PRS.0000000000006051 [epub ahead of print]
  • 27 De Boer M, van der Sluis WB, de Boer JP. , et al. Breast Implant-Associated Anaplastic Large-Cell Lymphoma in a Transgender Woman. Aesthet Surg J 2017; 37 (08) 83-87 . doi:10.1093/asj/sjx098
  • 28 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 . doi:10.1053/j.jfas.2010.08.009
  • 29 Yoon HJ, Choe JY, Jeon YK. Mucosal CD30-Positive T-Cell Lymphoproliferative Disorder Arising in the Oral Cavity Following Dental Implants. Internat J Surg Path 2015; 23 (08) 656-661 . doi:10.1177/1066896915599059
  • 30 Tuck M, Lim J, Lucar J, Benator D. Anaplastic large cell lymphoma masquerading as osteomyelitis of the shoulder: an uncommon presentation. BMJ Case Rep 2016 2016. doi: 10.1136/bcr-2016-217317
  • 31 Mendes Jr J, Mendes Maykeh VA, Frascino LF. Gluteal Implant-Associated Anaplastic Large Cell Lymphoma. Plast Reconstr Surg 2019; 144 (03) 610-613 . doi: 10.1097/PRS.0000000000005910
  • 32 Manikkam Umakanthan J, McBride CL, Greiner T. , et al. Bariatric Implant Associated Anaplastic Large-Cell Lymphoma. J Onc Practice 2017; 13 (12) 838-839 . doi:10.1200/jop.2017.026153
  • 33 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 Sézary Syndrome. J Clin Onc 2013; 31 (06) e87-e89 . doi:10.1200/jco.2012.42.9241
  • 34 Food and Drug Administration. Medical device reports of breast implant-associated anaplastic large cell lymphoma. Available at: https://www.fda.gov/medical-devices/breast-implants/medical-device-reports-breast-implant-associated-anaplastic-large-cell-lymphoma . Published 2018. Accessed July 14, 2019
  • 35 Brody GS, Deapen D, Taylor CR. Anaplastic large cell lymphoma occurring in women with breast implants: analysis of 173 cases. Plast Reconstr Surg 2015; 135 (03) 695-705 . Doi: 10.1097/PRS.0000000000001033
  • 36 Wroblewski LE, Peek Jr RM, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010; 23 (04) 713-739
  • 37 Zhu H, Shen Z, Luo H, Zhang W, Zhu X. Chlamydia trachomatis infection-associated risk of cervical cancer: A meta-analysis. Medicine (Baltimore) 2016 95(13):e3077
  • 38 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
  • 39 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
  • 40 Sorotos M, Longo B, Amorosi V, Santanelli di Pompeo F. Macrotextured breast implants with defined steps to minimize bacterial contamination around the device: experience in 42,000 implants. Plast Reconstr Surg 2018; 142 (03) 412e-413e
  • 41 Walker JN, Hanson B, Pinkner CL. , et al. Insights into the microbiome of breast implants and periprosthetic tissue in breast implant-associated anaplastic large cell lymphoma. Sci Rep 2019; 9 (01) 10393
  • 42 Deva AK. Reply: 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 (06) 1059e-1060e
  • 43 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
  • 44 Seif F, Khoshmirsafa M, Aazami H, Mohsenzadegan M, Sedighi G. The role of JAK-STAT signaling pathway and its regulators in the fate of T helper cells. Cell Commun Signal 2017; 15 (01) 23
  • 45 Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420 (6917): 860-867
  • 46 Bizjak M, Selmi C, Praprotnik S. , et al. Silicone implants and lymphoma: The role of inflammation. J Autoimmun 2015; 65: 64-73
  • 47 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
  • 48 Oishi N, Miranda RN, Feldman AL. Genetics of Breast Implant-Associated Anaplastic Large Cell Lymphoma (BIA-ALCL). Aesthet Surg J 2019; 39 (77, Supplement_1): S14-S20
  • 49 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
  • 50 Thomas SJ, Snowden JA, Zeidler MP, Danson SJ. The role of JAK/STAT signalling in the pathogenesis, prognosis and treatment of solid tumours. Br J Cancer 2015; 113 (03) 365-371
  • 51 Letourneau A, Maerevoet M, Milowich D. , et al. Dual JAK1 and STAT3 mutations in a breast implant-associated anaplastic large cell lymphoma. Virchows Arch 2018; 473 (04) 505-511
  • 52 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
  • 53 Blombery P, Thompson E, Ryland GL. , et al. Frequent activating STAT3 mutations and novel recurrent genomic abnormalities detected in breast implant-associated anaplastic large cell lymphoma. Oncotarget 2018; 9 (90) 36126-36136
  • 54 Lechner MG, Megiel C, Church CH. , et al. Survival signals and targets for therapy in breast implant-associated ALK--anaplastic large cell lymphoma. Clin Cancer Res 2012; 18 (17) 4549-4559
  • 55 Hodge DR, Hurt EM, Farrar WL. The role of IL-6 and STAT3 in inflammation and cancer. Eur J Cancer 2005; 41 (16) 2502-2512
  • 56 Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009; 9 (11) 798-809
  • 57 Pastorello RG, D'Almeida Costa F, Osório CABT. , et al. Breast implant-associated anaplastic large cell lymphoma in a Li-FRAUMENI patient: a case report. Diagn Pathol 2018; 13 (01) 10
  • 58 Bautista-Quach MA, Nademanee A, Weisenburger DD, Chen W, Kim YS. Implant-associated primary anaplastic large-cell lymphoma with simultaneous involvement of bilateral breast capsules. Clin Breast Cancer 2013; 13 (06) 492-495
  • 59 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
  • 60 Clemens MW, Jacobsen ED, Horwitz SM. 2019 NCCN consensus guidelines on the diagnosis and treatment of breast implant-associated anaplastic large cell lymphoma (BIA-ALCL). Aesthet Surg J 2019; 39 (Supplement_1): S3-S13
  • 61 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
  • 62 Cheson BD, Fisher RI, Barrington SF. , et al; Alliance, Australasian Leukaemia and Lymphoma Group; Eastern Cooperative Oncology Group; European Mantle Cell Lymphoma Consortium; Italian Lymphoma Foundation; European Organisation for Research; Treatment of Cancer/Dutch Hemato-Oncology Group; Grupo Español de Médula Ósea; German High-Grade Lymphoma Study Group; German Hodgkin's Study Group; Japanese Lymphorra Study Group; Lymphoma Study Association; NCIC Clinical Trials Group; Nordic Lymphoma Study Group; Southwest Oncology Group; United Kingdom National Cancer Research Institute. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 2014; 32 (27) 3059-3068
  • 63 Mehta-Shah N, Clemens MW, Horwitz SM. How I treat breast implant-associated anaplastic large cell lymphoma. Blood 2018; 132 (18) 1889-1898
  • 64 Richardson K, Alrifai T, Grant-Szymanski K. , et al. Breast implant-associated anaplastic large-cell lymphoma and the role of brentuximab vedotin (SGN-35) therapy: A case report and review of the literature. Mol Clin Oncol 2017; 6 (04) 539-542
  • 65 Lamaris GA, Butler CE, Deva AK. , et al. Breast reconstruction following breast implant-associated anaplastic large cell lymphoma. Plast Reconstr Surg 2019; 143 (3S A review of breast implant-associated anaplastic large cell lymphoma): 51S-58S
  • 66 O'Neill AC, Zhong T, Hofer SOP. Implications of breast implant-associated anaplastic large cell lymphoma (BIA-ALCL) for breast cancer reconstruction: an update for surgical oncologists. Ann Surg Oncol 2017; 24 (11) 3174-3179
  • 67 Health R, Food US. Anaplastic large cell lymphoma (ALCL) in women with breast implants: preliminary FDA findings and analyses. U S FDA website. 2011
  • 68 Reisman NR. Discussion: breast implant informed consent should include the risk of anaplastic large cell lymphoma. Plast Reconstr Surg 2016; 137 (04) 1123
  • 69 Roberts JM, Carr LW, Jones A, Schilling A, Mackay DR, Potochny JD. A prospective approach to inform and treat 1,340 patients at risk for BIA-ALCL. Plast Reconstr Surg 2019; 144 (01) 46-54
  • 70 Haddock NT, Teotia SS. Discussion: a prospective approach to inform and treat 1,340 patients at risk for BIA-ALCL. Plast Reconstr Surg 2019; 144 (01) 57-59
  • 71 Chung KC, Malay S, Shauver MJ, Kim HM. Economic analysis of screening strategies for rupture of silicone gel breast implants. Plast Reconstr Surg 2012; 130 (01) 225-237
  • 72 US Food and Drug Administration. FDA Requests Allergan Voluntary Recall. Available at: https://www.fda.gov/medical-devices/safety-communications/fda-requests-allergan-voluntarily-recall-natrelle-biocell-textured-breast-implants-and-tissue . Accessed August 15, 2019
  • 73 Aladily TN, Medeiros LJ, Amin MB. , et al. Anaplastic large cell lymphoma associated with breast implants: a report of 13 cases. Am J Surg Pathol 2012; 36 (07) 1000-1008
  • 74 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
  • 75 Miranda RN, Medeiros LJ, Ferrufino-Schmidt MC. , et al. Pioneers of breast implant-associated anaplastic large cell lymphoma: history from case report to global recognition. Plast Reconstr Surg 2019; 143 (3S A review of breast implant-associated anaplastic large cell lymphoma): 7S-14S