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Characteristics and Treatment of Advanced Breast Implant–Associated Anaplastic Large Cell Lymphoma

Collins, Meredith S. MD; Miranda, Roberto N. MD; Medeiros, L. Jeffrey MD; Silva de Meneses, Marcelo Pinheiro MD; Iyer, Swaminathan P. MD; Butler, Charles E. MD, FACS; Liu, Jun PhD; Clemens, Mark W. MD, FACS

Plastic and Reconstructive Surgery: March 2019 - Volume 143 - Issue 3S - p 41S-50S
doi: 10.1097/PRS.0000000000005568
Original Articles
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Background: Breast implant–associated anaplastic large cell lymphoma (BIA-ALCL) most commonly follows an indolent course; however, a subset of patients display more advanced disease marked by recurrent and disseminated growth refractory to treatment. This study evaluated outcomes of advanced disease, specifically bilateral disease, lymph node involvement, organ metastasis, and/or disease-related death.

Methods: Published cases of BIA-ALCL from 1997 to 2018 and unpublished cases at the authors’ institution were retrospectively reviewed, and patients with advanced disease were selected. Treatment and outcomes were compared against a control of BIA-ALCL subjects without advanced disease.

Results: Thirty-nine patients with advanced BIA-ALCL were identified who had bilateral disease (n = 7), lymph node and organ metastasis (stage IIB-IV, n = 24), and disease-related death (n = 8). Sixty-five patients were included in a comparison control group (stage 1A-1C). Treatment types for advanced disease patients were complete surgery, n = 16 (55.2%); limited surgery, n = 19 (65.5%); chemotherapy, n = 26 (89.7%); salvage chemotherapy, n = 11 (37.9%); radiation, n = 15 (51.7%); and autologous stem cell transplant, n = 6 (20.7%). The rates of complete remission for the bilateral and lymphadenopathy groups were 4 of 7 (57%, P < 0.001) and 16 of 24 (67%, P = 0.128), respectively. Compared with the control group, advanced disease patients had significantly longer time from diagnosis to definitive surgery (21 versus 8 months, P = 0.039) and a lower rate of complete surgery (59% versus 88%, P = 0.004).

Conclusions: Advanced disease BIA-ALCL may be a consequence of a delay or suboptimal treatment of BIA-ALCL. Optimal adjuvant chemotherapy and indications for radiation for BIA-ALCL patients with advanced features are not yet clearly defined. Advanced disease is the end of the spectrum of cancer stages, and these patients substantiate the World Health Organization classification of BIA-ALCL as a lymphoma rather than benign or lymphoproliferative.

Houston, Texas; and Aracaju, Brazil

From the Departments of Plastic Surgery, Hematopathology, and Lymphoma, University of Texas MD Anderson Cancer Center; and Hospital Santa Helena.

Received for publication September 28, 2018; accepted December 21, 2018.

Disclosure:Dr. Miranda has received honorarium as advisory scientific expert for Allergan. Dr. Clemens was an investigator for the ATHENA Trial (Mentor Corporation), is an investigator for the Motiva FDA Approval Trial (Establishment Labs), and was a former Allergan Consultant (2012–2015). All other authors report no conflicts of interest.

Mark W. Clemens, MD, FACS, Department of Plastic Surgery, University of Texas MD Anderson Cancer Center, 1400 Pressler Street, Unit 1488, Houston, TX 77096, mwclemens@mdanderson.org, Twitter: @clemensmd

Primary non-Hodgkin lymphomas of the breast are uncommon, accounting for 0.04%–0.5% of breast malignancies and 1%–2% of extranodal lymphomas.1–4 The most common lymphomas of the breast include diffuse large B-cell lymphoma and extranodal marginal lymphoma.5 T-cell lymphoma represents <10% of lymphomas of the breast.6 Breast implant–associated anaplastic large cell lymphoma (BIA-ALCL) is an uncommon primary T-cell lymphoma first described by Keech and Creech7 in 1997.8 Since that time, a number of publications have emerged describing this clinical entity.9–17

The World Health Organization provisionally classifies BIA-ALCL as a malignancy most commonly presenting as a primary effusion lymphoma with an indolent clinical course that can progress to infiltrative disease with mass aggregation in more advanced cases.18 Patients typically present with a late-onset periprosthetic malignant effusion or a mass adjacent to a textured implant.19 The National Comprehensive Cancer Network defined standardized diagnosis and treatment algorithms which call for explantation and total capsulectomy alone as curative for the majority of patients.20,21 A recent study by Miranda et al.22 reporting the long-term follow-up of 60 BIA-ALCL patients concluded that most patients achieve complete remission (72% and 93% for patients presenting with and without a mass, respectively). However, some patients have been reported with advanced disease that does not follow the typical indolent course.23,24

A subset of patients with BIA-ALCL display characteristics of a more advanced disease marked by persistent and recurrent growth refractory to treatment. There are patients that appear to have BIA-ALCL with advanced features, including those with bilateral disease, lymph node involvement, organ metastasis, and/or death related to BIA-ALCL. It is unclear why certain patients developed BIA-ALCL with advanced features, and to date, no studies have examined this specific group of patients. In this study, we further characterize BIA-ALCL with advanced disease by retrospectively investigating and comparing their clinical course with patients where disease remains confined to the implant capsule. We hypothesize that BIA-ALCL with advanced features is likely the result of inadequate or delayed treatment, rather than a separate and distinct clinical entity. A treatment strategy beyond surgical resection and explantation with adjunctive treatments for patients is discussed.

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METHODS

After obtaining approval from the University of Texas MD Anderson Institutional Review Board, we performed a retrospective literature review of all published cases from 1997 to 2018 and unpublished cases at our institution of BIA-ALCL. Each case was centralized to our institution and pathologically evaluated to ensure that the diagnostic criteria for BIA-ALCL were met. BIA-ALCL is defined as a T-cell lymphoma characterized by large lymphoid cells with pleomorphic nuclei that express CD30 and which are negative for anaplastic lymphoma kinase (ALK) protein or translocations involving the ALK gene at chromosome 2q23. Patients with BIA-ALCL with advanced disease were defined as patients with bilateral disease, lymph node or organ metastasis (tumor-node-metastasis stage IIB-IV), and/or disease-related death. Patient demographics, pathology, treatment, and outcomes were evaluated. Treatment and outcomes were then compared with control subjects with early-stage BIA-ALCL (stage IA-IC).

Patient demographics included age, laterality, implant type, and surgical indication (cosmetic versus reconstructive). Each patient’s pathology was evaluated for evidence of advanced features, including tumor infiltration into the breast ducts. Treatment types were also reviewed. Time from diagnosis to treatment was evaluated and compared with the control subjects. Definitive surgery was defined as implant removal, total capsulectomy, and complete ablation of any associated masses, whereas limited surgery included all other procedures, such as implant removal, retained mass, and/or partial capsulectomy. Patient outcomes included complete remission, death from BIA-ALCL, and death from unrelated disease.

Means and SDs were used to summarize age and time to definitive surgery. Frequencies and proportions were used to present treatment and outcomes. Fisher’s exact test was used to test associations between the categorical variables. A Wilcoxon rank sum test was applied to detect the difference in continuous variables. All the tests were 2-sided. A P value of <0.05 was considered significant. The analyses were performed in SAS 9.3 (SAS Institute Inc., Cary, N.C.).

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RESULTS

Thirty-nine patients with advanced BIA-ALCL were identified: bilateral disease (n = 7, Fig. 1), lymph node or organ metastases (n = 24, Figs. 2 and 3), and disease-related death (n = 8, Fig. 4). Sixty-five patients were included in the early-stage comparative group (stage IA-IC). Clinicopathologic characteristics of BIA-ALCL patients with advanced disease are listed in Table 1. The average age of the BIA-ALCL patients with and without advanced features was 52.6 (range = 29–77) and 53.4 (range = 36–75), respectively.

Table 1.

Table 1.

Fig. 1.

Fig. 1.

Fig. 2.

Fig. 2.

Fig. 3.

Fig. 3.

Fig. 4.

Fig. 4.

Treatment types for BIA-ALCL patients with and without advanced features are summarized in Table 2. Advance BIA-ALCL patients overall had more limited surgery, chemotherapy, salvage chemotherapy, and autologous stem cell transplant. A greater number of early-stage BIA-ALCL patients had definitive surgery compared with those patients with advanced features (88% versus 59%, P = 0.001). Mean time to definitive surgery was 21 months for advanced patients, compared with 8 months for early-stage patients, a difference which was statistically significant (P = 0.028).

Table 2.

Table 2.

Of the 39 patients with advanced BIA-ALCL, 24 patients had lymph node or organ metastasis (stage IIB-IV). Compared with early-stage (stage IA-IC) patients, fewer advanced patients with lymph node or organ involvement underwent definitive surgery (62% versus 88%, P = 0.013) and had a longer time to definitive surgery from onset of symptoms (22 versus 8 months, P = 0.001). Patients with lymph node or organ involvement more frequently received limited surgery, chemotherapy, salvage chemotherapy, and autologous stem cell transplant.

Of the 39 BIA-ALCL patients with advanced features, 7 patients had bilateral disease. Six patients with bilateral disease underwent complete capsulectomy with explantation surgery at diagnosis.

Eight of the 39 BIA-ALCL patients with advanced features were found to have BIA-ALCL disease-related death. One patient diagnosed with BIA-ALCL received definitive surgery and was subsequently free of disease for 120 months but developed a separate B-cell follicular lymphoma from which she ultimately died. No patients who died of BIA-ALCL underwent definitive surgery, a difference that was statistically significant when compared with early-stage patients (0% versus 87.7%, P < 0.001). Patients who died of BIA-ALCL had higher rates of limited surgery, chemotherapy, salvage chemotherapy, radiation, and autologous stem cell transplant; however, only the higher rate of salvage chemotherapy was found to be statistically significant (80% versus 10.2%, P = 0.002).

Outcomes for advanced disease BIA-ALCL patients are summarized in Table 3. Of the 39 patients with advanced features, 8 patients died of BIA-ALCL (20.5%), 2 patients died of an unrelated disease (5.1%), 1 patient was alive with disease (2.6%), and 28 patients had complete remission (71.8%). Patients with lymph node involvement had significantly higher rates of death from BIA-ALCL (20.8% versus 0%) and lower rates of complete remission (70.8% versus 100%) when compared with early-stage patients (P < 0.001). Patients with bilateral disease also had slightly higher rates of death from BIA-ALCL (12.5% versus 0%) and lower rates of complete remission (87.5% versus 100%) when compared with patients without early-stage disease; however, this was representative of a single case. Definitive surgery was significantly correlated with a higher rate of complete remission (78.9% versus 21.1%, P = 0.003). Salvage chemotherapy provided a lower complete remission rate which approached significance (35.3% versus 64.7%, P = 0.069; Table 4).

Table 3.

Table 3.

Table 4.

Table 4.

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Advanced Disease Case Examples

  1. Lymph node involvement: A 51-year-old woman with BRCA2 mutation underwent prophylactic bilateral skin-sparing mastectomies and immediate reconstruction with tissue expanders and textured silicone implants in 2001. In 2007, she underwent an implant exchange with textured silicone implants. In July 2014, she presented with painful swelling of her left breast. Left breast ultrasound revealed a pericapsular fluid collection, which demonstrated an anaplastic large T-cell lymphoma. She underwent bilateral partial capsulectomy with implant removal in August 2014. For surveillance, a follow-up positron emission tomography/computed tomography (PET-CT) scan was done in December 2014, which showed interval development of left internal mammary lymphadenopathy (LAD). She was treated with 3 cycles of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) chemotherapy, and follow-up PET-CT demonstrated resolution of the internal mammary LAD, but interval development of left supraclavicular LAD with malignant cells confirmed by fine-needle aspiration. She then underwent 3 cycles of brentuximab vedotin immune therapy with complete response demonstrated on follow-up PET-CT. She was then treated with an allograft stem cell transplantation and remains disease free for 3 years.
  2. Bilateral breast involvement: A 72-year-old woman developed left invasive breast cancer and was treated with bilateral mastectomies and bilateral latissimus flaps with textured silicone implants (Figs. 2 and 3). Postoperative course was uneventful until 2014 when she developed acute swelling of the left breast. Fine needle aspiration revealed BIA-ALCL on cytology, flow cytometry, and CD30 immunohistochemistry. Patient underwent left explantation and total capsulectomy with resection of a 5 cm mass invading through the capsule. Patient was disease free until 2016 when she developed right axillary LAD. A right explantation, capsulectomy, and selective lymphadenectomy were performed. Pathology demonstrated BIA-ALCL on the luminal surface of the right implant with reactive, but disease-free lymph nodes. Patient was considered to have 2 separate BIA-ALCL primary diseases (left stage IIA and right stage IC), received no further treatments, and remains disease free for 18 months.
  3. Death from disease: A 38-year-old woman received bilateral cosmetic breast augmentation with silicone textured implants in 1987. Postoperative course was uneventful until 1996 when she palpated a 4 × 3 cm mass in her left breast. She underwent a fine needle aspiration of the periprosthetic capsular mass and was diagnosed as CD30+ ALK ALCL. The patient was very adamant that she wanted to retain her implants for appearance reasons and declined ablative surgery against medical advice. She received CHOP chemotherapy followed by regional external beam radiation therapy, however, developed recurrence of disease within 4 months of adjunctive treatment. Disease progressed to central nervous system involvement with meningeal disease, and she expired after an additional 5 months.
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DISCUSSION

BIA-ALCL is an uncommon extranodal T-cell lymphoma associated with textured surface breast prostheses. BIA-ALCL is commonly regarded as having an indolent clinical course, and the majority of patients achieve complete remission with surgery alone. However, there exists a subset of BIA-ALCL patients who display characteristics of advanced disease marked by persistent and recurrent growth which can be refractory to treatment. For the purpose of this study, advanced disease includes those patients with bilateral disease, lymph node or organ involvement (stage IIB-IV), and/or death related to BIA-ALCL. In this study, we reviewed 39 patients with BIA-ALCL with advanced features, including 7 with bilateral disease, 24 with lymph node or organ involvement, and 8 who died from BIA-ALCL. We compared treatment and outcomes to 65 patients with early-stage (stage IA-IC) BIA-ALCL.

With regard to treatment, patients with BIA-ALCL with advanced features had higher rates of limited surgery, chemotherapy, salvage chemotherapy, external beam radiation therapy, and autologous stem cell transplantation when compared with a control group of early-stage BIA-ALCL. The rate of definitive surgery (explantation, total capsulectomy, tumor ablation) was significantly lower in patients with advanced BIA-ALCL (59.3% versus 87.7%, P = 0.002). Additionally, the time to definitive surgery was significantly longer in patients with advanced features (21 versus 8 months, P = 0.028). When evaluated by group, no patients who died of BIA-ALCL underwent definitive surgery, and patients with lymph node involvement and bilateral disease had lower rates of definitive surgery when compared with those without advanced features (62.5% versus 87.7%, and 50% versus 87.7%, respectively). Definitive surgery was also significantly correlated with higher rates of complete remission in patients with advanced BIA-ALCL (78.9% versus 21.1%, P = 0.003).

These data suggest that early definitive surgery plays a significant role in the treatment of BIA-ALCL. A smaller percentage of patients with advanced features were treated with definitive surgery, and the time from diagnosis to definitive surgery in this group was significantly longer. Furthermore, definitive surgery was significantly associated with a higher rate of complete remission in BIA-ALCL patients with advanced features. This suggests that patients who are treated with early definitive surgery are less prone to disease progression and more likely to have better outcomes. This also indicates that patients with advanced BIA-ALCL may have developed more advanced disease as a result of delay in treatment or inadequate therapy such as limited or incomplete surgery.

Outcomes were also significantly different between BIA-ALCL patients with and without advanced features. Patients with advanced features had higher rates of death from ALCL and death from an unrelated disease (22.2% versus 0% and 7.4% versus 0%, respectively) and lower rates of complete remission (70.4% versus 100%). Eight patients died from BIA-ALCL, and of these, 4 patients had lymph node involvement, and 1 patient had lymph node involvement and bilateral disease. When divided into groups, patients with lymph node involvement had higher rates of death related to BIA-ALCL (20.8% versus 0%) and death of an unrelated disease (8.3% versus 0%) and lower rates of complete remission (70.8% versus 100%). This suggests that BIA-ALCL patients with lymph node and organ metastasis are less likely to achieve complete remission and more likely to die from their disease than patients without advanced features; however, definitive conclusions are difficult to make with such a small cohort size with widely varied treatment strategies.

A definitive treatment algorithm for patients with advanced and/or refractory disease has yet to be determined. National Comprehensive Cancer Network guidelines provide the current standard of care which includes surgical management, including implant removal, total capsulectomy, and resection of any associated masses and involved lymph nodes with negative margins. Additional treatment for patients with advanced disease after surgery such as lymph node or organ involvement or unresectable tumor has included standard front-line treatment regimen with a combination anthracycline-based chemotherapy or alternatively with targeted immune therapy with brentuximab vedotin.

The main limitation of this study is small sample size. BIA-ALCL is an uncommon disease entity, and only 644 unique worldwide cases are currently known to our institution. Only 104 cases had detailed clinical history and treatment timeline information sufficient to include in this study, and of those, only 39 patients had advanced BIA-ALCL. As awareness of BIA-ALCL and its presentation in patients with breast prostheses increases, the number of patients identified with disease continues to grow. It is expected this will allow further investigation of these patients, their treatment, and outcomes. It is important to note that the advanced cases presented in this manuscript were centralized from the United States and Brazil. Currently, the relative proportion of advanced BIA-ALCL cases is disparate between countries with stage IIB-IV disease being reported as 18% in Italy, 13.8% in the United States, 9.5% in England, and 3.6% in Australia.8 These observed differences between countries may be secondary to differences in surgeon awareness, physician willingness to report cases, and the underlying medicolegal environment, though this remains speculative. Another potential limitation of this study is the incomplete history provided for some advanced disease patients. The majority of detailed clinical information was obtained about the subjects in this study; however, for certain cases, we were unable to obtain a complete history. For example, of the 39 patients with advanced features, it is unknown if 3 patients had limited surgery, 4 patients had salvage chemotherapy, and 2 patients had autologous stem cell transplantation. Thus, when evaluating patients who received each treatment, only the known number of patients was utilized for each category. Despite this small number of unknowns, we believe this is unlikely to significantly change the data and conclusions.

The data from this retrospective review of advanced disease BIA-ALCL patients suggest that this disease is likely not a distinct clinical entity separate from the more indolent or early-stage BIA-ALCL, but instead represents disease that has progressed. Fewer patients with BIA-ALCL with advanced features were treated with definitive surgery, and there was a significantly longer time from diagnosis to definitive surgery when compared with patients without advanced features. Patients who developed lymph node or organ involvement, bilateral disease, and/or death related to BIA-ALCL may have ultimately suffered from advanced disease as a result of a delay in treatment or incomplete therapy. Currently, we recommend initial treatment with en bloc implant removal, total capsulectomy, and excision of involved lymph nodes and associated masses, with negative margins for all patients with BIA-ALCL (Fig. 1). Definitive surgery has proven to increase the rate of complete remission in patients with BIA-ALCL. Of note, within this study, rapid disease was observed in 5 patients who had limited surgery and partially retained a mass. Disease progressed to a rapidly invasive chest wall mass or organ metastasis within months, suggesting that the BIA-ALCL, while usually indolent, may exhibit hyperprogression, an oncologic phenomenon reflecting a very rapid tumor progression when partially incised. Infiltration of breast ducts was uniquely noted in 2 aggressive cases that ultimately died of their disease. Predictors of hyperprogression are not possible to identify within these limited number of patients. Advanced disease patients support the World Health Organization classification of BIA-ALCL as a lymphoma. Whether early-stage effusion-limited disease will always progress to advanced disease or requires additional mutational degeneration has yet to be determined but is the subject of genetic sequencing analysis.

Advanced disease does not appear to be a unique clinical entity, but rather a progression of BIA-ALCL. BIA-ALCL patients with lymph node, organ involvement, and/or death related to BIA-ALCL likely developed advanced disease as a result of delayed or incomplete treatment. Bilateral disease may represent 2 separate primaries in a genetically susceptible patient rather than metastasis. Early recognition of symptoms and expedited treatment with definitive surgery appear to improve the rate of complete remission in patients with BIA-ALCL. Future randomized controlled trials will be needed to develop a definitive treatment algorithm for patients with advanced disease.

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ACKNOWLEDGMENT

Data analyses were supported in part by the Cancer Center Support Grant (NCI Grant P30 CA016672).

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