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Hindawi Case Reports in Oncological Medicine Volume 2022, Article ID 4162832, 7 pages https://doi.org/10.1155/2022/4162832 Case Report A South African Breast Implant-Associated Anaplastic Large Cell Lymphoma: Clinical Presentation and Six-Year Follow-Up 1 1,2 1 1,3,4 Alexandra Grubnik, Yastira Ramdas , Barend Van der Bergh, Simon Nayler , 1,5 1,2,6 Carol-Ann Benn , and Bernardo L. Rapoport Netcare Breast Care Centre of Excellence, Milpark Hospital, 9 Guild Road Parktown, South Africa Department of Immunology, Faculty of Health Sciences, University of Pretoria, Corner Doctor Savage Road and Bophelo Road, Pretoria 0002, South Africa Drs Gritzman & Thatcher Inc. Laboratories, 4 Main Street, Bordeaux, Randburg, Johannesburg 2194, South Africa University of the Witwatersrand, Donald Gordon Medical Centre, 21 Eton Road, Parktown Johannesburg, 2193, South Africa Helen Joseph Hospital Breast Care Clinic, Department of Surgery, Faculty of Health Sciences, University of the Witwatersrand, 1 Perth Road, Auckland Park, Johannesburg, 2092 Gauteng, South Africa The Medical Oncology Centre of Rosebank, 129 Oxford Road, Johannesburg 2196, South Africa Correspondence should be addressed to Bernardo L. Rapoport; firstname.lastname@example.org Received 31 December 2021; Revised 8 May 2022; Accepted 13 May 2022; Published 31 May 2022 Academic Editor: Katsuhiro Tanaka Copyright © 2022 Alexandra Grubnik et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Breast augmentation is the most common surgical procedure for women globally, with 1,795,551 cases performed in 2019. Breast implant-associated anaplastic large cell lymphoma (BIA-ALCL) is highly uncommon, with 733 reported cases as of January 2020. In South Africa, there are less than 4000 breast augmentation surgeries annually. This case presents the ﬁrst case report documentation of a South African woman diagnosed with BIA-ALCL. The patient was a 61-year-old woman who consulted the Breast Care Centre of Excellence in Johannesburg in 2015. She had a prior history of bilateral augmentation mammoplasty with subsequent implant exchange. The patient presented with periprosthetic ﬂuid with a mass-like enhancement on the left breast. Aspiration of the mass-like ﬂuid was positive for CD45, CD30, and CD68 and negative for CD20 and ALK-1, indicative of BIA-ALCL. Surgical treatment included bilateral explantation, complete capsulectomies, and bilateral mastopexy. Macroscopic examination of the left breast capsulectomy demonstrated ﬁbrous connective tissue. The histological examination of the tumor showed extensive areas of broad coagulative necrosis with foamy histiocytes. Immunohistochemistry examination of this tumor showed CD3-, CD20-, and ALK-1-negative and CD30- and CD68-positive stains. PCR analysis for T-cell clonality showed monoclonal T-cell expansion. These ﬁndings conﬁrm the presence of BIA-ALCL. The patient recovered well after surgery and did not require adjuvant therapy. A patient with a conﬁrmed diagnosis of BIA-ALCL was successfully treated with explantation and complete capsulectomy. She was followed up regularly for six years, and the patient remains well and in remission. 1. Background subtype of T-cell non-Hodgkin’s lymphoma, is associated with textured surface breast implants [3, 4]. The cause of Breast augmentation remains the most common procedure BIA-ALCL remains unknown, although several theories, globally, with 1,795,551 performed in 2019 . An estimated including bioﬁlm, viral, shedding of particles, and genetic predisposition, have been proposed [5–9]. 10 million women have implants globally . In South Africa, 3297 breast augmentation cases with silicone BIA-ALCL is a novel malignant entity. It was ﬁrst implants were recorded in 2016 . Breast implant- described in 1997 and reported by the Food and Drug associated anaplastic large cell lymphoma (BIA-ALCL), a Administration (FDA) in 2011 [10–11]. In 2016, the World 2 Case Reports in Oncological Medicine TCRB; A-Vδ1-8, Vδ10, + multiple Jδ regions TCRG; and Health Organization (WHO) categorized it as a unique disease . NCCN diagnosis and treatment guidelines were B-Vδ9, Vδ11+multiple Jδ regions TCRG. published in 2016 and updated in 2019 . These abnormalities were detected on the gel electropho- resis according to the Euroclonality/Biomed-2 guidelines for As of January 2020, 733 cases of BIA-ALCL were reported to the FDA, including 36 deaths . The interpretation and reporting Ig/TCR clonality in suspected incidence and risk of BIA-ALCL have risen considerably lymphoproliferation . from early reports of 1 per million to current estimates of Histological examination of a gland removed below the between 1/2,832 and 1/30000, and in speciﬁc cohorts, an low age of the pectoralis minor muscle (level 1 axillary lymph node) showed a reactive lymph node without evi- incidence of as high as 1/355 was reported [10, 12, 13]. The disease incidence mainly depends on the “population” dence of lymphoma involvement. (implant type and characteristics) examined and increased Following surgery, the patient noted reduced swelling awareness of the disease . To our knowledge, this is the and pain. A six-week follow-up examination revealed no ﬁrst peer-reviewed case report of a patient with BIA-ALCL inﬂammation, reduced pain levels, and no evidence of recur- rence. No axillary or supraclavicular pathological lymphade- in South Africa and the African continent. nopathy was seen. Follow-up visits consisted of physical examination, full 2. Case Presentation blood counts, serum chemistry tests, ultrasound of the A 61-year-old woman initially had a bilateral breast aug- breast, chest roentgenograms, and ultrasound of the abdo- men and pelvis or computerized body tomography. The mentation with Nagor-textured silicone implants in 1994. She had bilateral implant exchange with Allergan, smooth patient was followed up at a six-month interval for ﬁve years. Currently, the patient is followed up yearly, and she remains implants in subpectoral pockets, and mastopexy in 2007. She presented to the Breast Care Centre of Excellence in in remission at year six. Johannesburg in 2015 with initial swelling of the left breast. Mammography, ultrasound, and MRI revealed a peripros- 3. Discussion thetic ﬂuid collection and mass-like enhancement on the left breast at the 4 o’clock region showing sustained peripheral BIA-ALCL was ﬁrst reported in 1997 . The risk of BIA- enhancement (Figure 1). Family history: the father died of ALCL increases yearly, with breast augmentation being the colon cancer. Fluid was aspirated, and cytologic smears on most common surgery performed annually for women. Still, a tissue block were analyzed by hematoxylin-eosin stain there are global discrepancies between surgeon preferences, and immunohistochemistry. The tumor cells were positive costs, and various implant technologies . for CD45, CD3, and CD30. Additionally, CD68 was positive The reported incidence of BIA-ALCL is increasing. This in a population of reactive background histiocytes. The may be due to increased disease awareness. BIA-ALCL is tumor was negative for ALK-1, and CD20 was indicative of exclusively associated with textured implants, with no con- BIA-ALCL. Preoperative positron emission topography ﬁrmed cases in patients with only smooth devices to date (PET) demonstrated level 1 lymph nodes on the left. The [11, 15, 18, 19]. Like our patient, patients with smooth patient was discussed at a multidisciplinary team (MDT) implants at the time of BIA-ALCL diagnosis were found to meeting at the Breast Care Centre of Excellence. The patient have a mixed implant history with the previous textured underwent “en bloc” capsulectomy, which includes remov- devices. In 2019, the FDA recommended a global voluntary ing the implant, capsule, and eventual mass surrounded by recall of Allergan Biocell textured implants, following ﬁnd- a margin of healthy tissue. Surgery and recovery were ings of increased BIA-ALCL risk with these devices . uneventful. Macroscopic examination of the right breast Shortly following this announcement, several regulatory capsulectomy tissue conﬁrmed a ﬁbrotic capsule showing boards, including France and Canada, have banned macro- typical pseudosynovial metaplasia. The left breast capsulect- textured implants, thus signiﬁcantly increasing public omy revealed similar ﬁbrous connective tissue with the awareness of BIA-ALCL. Another possible reason is under- tumor biopsy showing extensive areas of broad coagulative estimating the actual incidence in published studies with a necrosis with foamy histiocytes (Figure 2). short median follow of 2-4 years. BIA-ALCL usually occurs The tumor inﬁltrated the superﬁcial aspect of the capsule after a median of 6-13 years [11, 13]. only. The ink margins were clear. Immunohistochemistry Breast non-Hodgkin’s lymphoma (NHL) is primarily examination of this tumor showed CD3-, CD20-, and B-cell in origin (95%). T-cell lymphomas of the breast ALK-1-negative and CD3-, CD30-, and CD68-positive have 3 diﬀerent subtypes, including anaplastic lymphoma stains. PCR analysis for T-cell clonality showed monoclonal kinase- (ALK-) negative ALCL, ALK-positive ALCL, and T-cell expansion (Figures 3(a)–3(e)) . DNA was cutaneous ALCL . extracted from the submitted sample using QIAGEN® QIA Epidemiologically, non-Hodgkin’s lymphomas associ- amp DNA FFPE tissue kit. Clonality was performed by the ated with the breast account for less than 2% of extranodal IdentiClone™ TCRB+TCRG T-clonality Assay. The PCR NHL and less than 1% of NHL, with most presenting as product was electrophoresed with the Bio Rad® system. diﬀuse B-cell, marginal zone lymphoma and follicular The PCR showed monoclonal bands (Figure 4). The follow- lymphoma . BIA-ALCL is a rare subtype of T-cell ing abnormalities were detected: A-Vβ+Jβ1+Jβ2 regions lymphoma pathologically associated with CD30-positive, TCRB; B-VB+Jβ2 regions TCRB; C-Dβ+Jβ1+Jβ2 regions ALK-negative ALCL. The risk of women with implants Case Reports in Oncological Medicine 3 (a) (b) (c) Figure 1: (a–c) MRI images of periprosthetic ﬂuid and mass. (a) (b) Figure 2: Macroscopy examination: (a) right breast capsulectomy with a mass of 47 g and (b) left breast capsulectomy and implant 294 g. 4 Case Reports in Oncological Medicine (a) Microscopy examination: hematoxylin and eosin (b) Microscopy examination: hematoxylin and eosin staining ×200 magniﬁcation staining ×400 magniﬁcation (c) Microscopy examination: CD3-positive (d) Microscopy examination: CD30-positive cell ×20 magniﬁcation cell ×20 magniﬁcation (e) Microscopic examination: CD30-positive cell ×400 magniﬁcation Figure 3: (a–e) Microscopic examination. contracting BIA-ALCL is relatively low, and it was only response may be bacterial bioﬁlm. Hu et al. found Ralstonia pickettii in more than half of diseased capsules . Kadin recently classiﬁed as a unique disease . A recent European study by the Committee on Device Safety and et al. demonstrated that BIA-ALCL cells might be derived Development (CDSD) reported 420 cases in Europe, with from lymphocytes with Th1/Th17 polarization in capsular an overall prevalence of 1 : 13,745 cases in the 28 member tissues and surrounding seromas, suggesting a chronic bac- states of the European Union (EU-28). Countries where spe- terial antigen stimulation of the liposaccharide coat of ciﬁc measures have been implemented to tackle BIA-ALCL Gram-negative bacteria and a persistent T-cell proliferation account for 61% of the EU-28 population and actively might support BIA-ALCL initiation and disease progression reported 382 cases with an overall prevalence of 1 : 9121 . Another theory suggests that the immune response is . The disease is treated primarily surgically and is associ- caused by silicone particles shed from the surface of textured ated with a good prognosis with an overall survival rate of implants . In a separate report, Kadin et al. showed that 93-94% at three years and 89-91% at ﬁve years [24–26]. the BIA-ALCL microenvironment is characterized by high The pathogenesis of BIA-ALCL remains unknown; how- levels of interleukin-13 and IgE, suggesting that the immune ever, chronic inﬂammation and abnormal immune response response underlying BIA-ALCL has the proﬁle of chronic may be associated with this disease. The cause for such a allergic reaction . Di Napoli et al. reported novel insights Case Reports in Oncological Medicine 5 can aﬀect the CD30 immunochemistry . A recent report by Di Napoli et al. outlines biomarkers that might help to diﬀerentiate between BIA-ALCL from all types of benign late seromas. It has been reported that benign eﬀusions may also have an oligo-/monoclonal expansion of CD30+ cells, chal- lenging the diagnosis of BIA-ALCL . Di Napoli et al. applied a multiplexed immuno-based assay to BI-ALCL ser- omas. The researchers found that BI-ALCL is characterized by a Th2-type cytokine milieu associated with signiﬁcantly high levels of IL-10, IL-13, and eotaxin, which discriminate BIA-ALCL from all types of reactive seroma. Additionally, the authors found that a cutoﬀ value of IL10/IL-6 ratio of 0.104 is associated with a speciﬁcity of 100% and a sensitivity of 83% in distinguishing eﬀusions due to BIA-ALCL . Treatment guidelines for the management of BIA-ALCL are well established . There is a consensus reached between the surgical and oncology communities. In most cases, complete surgical excision of the lymphomatous tumor mass and the breast implant with en block capsulect- omy is recommended. Complete surgical excision prolongs Figure 4: Gel electrophoresis showing clonal band for T-cell overall survival and event-free survival . Additionally, receptor gamma. The tumor is shown in the S1 band. if BIA-ALCL with positive lymph nodes is present, adjuvant chemotherapy may be required, with brentuximab vedontin considered the preferred ﬁrst line . If residual disease is on the pathogenesis of BIA-ALCL . By performing gene expression proﬁling, the investigators compared the present, radiotherapy is advised [11, 33]. The prognosis is favorable; a study of 87 diagnosed BIA-ALCL patients transcriptional proﬁles of BIA-ALCL with those of normal T-cells and other peripheral T-cell lymphomas. Compared reported an overall survival of 94% and 91% at three and ﬁve to normal CD4+ T-cells, BIA-ALCL was associated with an years, respectively, with event-free survival recorded at 49% at ﬁve years . Similar results are noted in smaller study upregulation of genes involved in cell motility processes, including chemokine receptor 6 (CCR6), MET, hepatocyte groups, and a longer-term follow-up of 60 patients reported growth factor (HGF), and chemokine (C-X-C motif) ligand a median OS of 12 years, OS at three and ﬁve years measured 14 (CXCL14) . Several reports suggest activation of the at 97% and 92%, respectively . JAK-STAT3 pathway in 13-26% of BIA-ALCL cases . Of interest is the fact that this manuscript is the ﬁrst peer-reviewed documented case of BIA-ALCL reported in BIA-ALCL typically presents with late seroma in 60-90% of cases . It may also present with a solid mass in the South Africa, conﬁrmed after an extensive PubMed and capsule adjacent to the breast implant in 8-24% of cases literature review of cases prior to 2021. and, less commonly, with lymphadenopathy (4-12%) or local and systemic symptoms like skin rash and fevers 4. Conclusion (<5%) [11, 21, 26]. The majority of cases present at an average of 8-10 years after implantation . Patients with This case describes the successful surgical treatment and six- suspected BIA-ALCL typically present with unilateral breast year long-term follow-up of a BIA-ALCL South African swelling. An ultrasound should be performed, and if ﬂuid is patient. present, ﬁne needle aspiration of a minimum of 50 ml of ﬂuid should be undertaken . Fluid is sent for cytology, CD30 immunochemistry, and ﬂow cytometry [11, 29]. A Data Availability core needle biopsy is recommended if a solid mass is present . A positron emission tomography scan (PET CT scan) The data of this case report is available from the patient’s is performed for staging before surgery to avoid distortion medical records. for 2-3 months afterward . Once the diagnosis is made, the patient should be man- Ethical Approval aged by a multidisciplinary team comprising oncologists, pathologists, radiation oncologists, surgeons, and plastic Ethical approval was not required for this study by local and surgeons. Staging investigations include serum chemistry, national guidelines. serum lactate dehydrogenase, C-reactive protein, β2 micro- globulin, bone marrow examination (aspiration, biopsy, and ﬂow cytometry), and PET CT scan . However, there Consent are limitations to the current diagnosis methods mentioned owing to patients that underwent aspiration of the eﬀusion Written informed consent was obtained from the patient to or patients undergoing implant and capsule removal, which publish this case report and any accompanying images. 6 Case Reports in Oncological Medicine neoplasms Conflicts of Interest and acute leukemia,” Blood, vol. 127, no. 20, pp. 2391–2405, 2016. The authors declare that the research was conducted in the  M. W. 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