Received: 24 June 2019 | Accepted: 25 June 2019

DOI: 10.1002/jso.25626

REVIEW ARTICLE

Breast implant–associated anaplastic large cell lymphoma,

a systematic review and in‐depth evaluation of the
current understanding

Peggy J. Ebner BA1 | Alice Liu BA1 | Daniel J. Gould MD, PhD2 |
Ketan M. Patel MD2

1
Keck School of Medicine of University of
Southern California, Los Angeles, California Abstract
2
Department of Plastic and Reconstructive Breast implant–associated anaplastic large cell lymphoma (BIA‐ALCL) is a T‐cell
Surgery, University of Southern California,
neoplasm that arises in the capsule around breast implants. While an association
Los Angeles, California
with implants has been proposed, no causal link has been identified and the
Correspondence
pathophysiology and natural history of BIA‐ALCL remain unknown. A literature
Ketan M Patel, Keck Hospital of University of
Southern California, 1510 San Pablo St, Suite review of 391 articles was performed to assess the current understanding of
415, Los Angeles, CA 90033.
BIA‐ALCL and to provide a balanced and unbiased view of the current
Email: ketan.patel@med.usc.edu
controversy surrounding the disease.

KEYWORDS
BIA‐ALCL, breast implants, lymphoma

1 | INTRODUCTION 2 | METHODS

Interest in anaplastic large cell lymphoma (ALCL) and breast
implants has increased dramatically since the announcement of a
possible association in 2011 by the Food and Drug Administra-
tion (FDA). 1 Since that time, the number of articles and case
reports describing lymphomas and other neoplasms in the
context of implants has grown each year. Several possible
mechanisms have been proposed and further efforts have been
made to quantify the true incidence of the disease in patients
with breast implants. Multiple databases designed to capture
information from patients with breast implant–associated ALCL
(BIA‐ALCL), some private and some government sponsored, have
been created across the world. Contention exists as to the
pathogenesis, etiology, prevalence, incidence, and demographic
factors of the disease, although the prognosis is generally
regarded to be excellent.2 The growing interest in BIA‐ALCL is
reflective of its implications for both reconstructive and cosmetic
breast surgery, as a possible correlation could influence recon-
structive modalities, choice of implant, and even the future of
other implanted devices.
A systematic review was conducted according to PRISMA guidelines.3 A
literature search was performed in Pubmed/Medline, Web of Science,
and Embase using the following keywords: breast implant–associated
large cell lymphoma, lymphoma and breast implants, and the MeSH
terms: lymphoma and mammaplasty. A total of 1 073 results were
obtained and 659 documents matched the search criteria after
deduplication with Mendeley. These were further sorted by title and
abstract to include reviews, case reports, and original research. Non‐
English language papers, letters, and commentary were excluded. The
references of these works were checked for other relevant publications.
Total number of 391 articles, including 85 case reports, were ultimately
evaluated.
3 | RESULTS
Total number of 85 case reports were assessed for patient age, race,
survival, implant life, indication for implants, implant volume, implant
type, implant brand, clinical presentation, biomarkers, laterality, and

J Surg Oncol. 2019;1-5. wileyonlinelibrary.com/journal/jso © 2019 Wiley Periodicals, Inc. | 1

2 |
survival. The average age of patients documented was 53.6 years. The
majority of cases presented with unilateral breast swelling (including
enlargement and tenderness),4-9 lymphadenopathy,10,11 skin manifesta-
tions,12,13 and B symptoms (fever, chills, weight loss, night sweats, etc).10
Imaging done showed a pericapsular fluid collection in the majority of
patients, with masses and superficial lesions presenting much more
rarely.5,14-16 One patient was clinically asymptomatic with the exception
of relapsing pericapsular effusion, which was drained multiple times
before being found on cytology to be BIA‐ALCL.17 Several patients had
implants placed for cancer reconstruction and relapse of the original
breast neoplasm was suspected until biomarkers were analyzed.12 The
average implant life before presentation was 9.9 years, with the shortest
implant duration being 2 months in a patient who had undergone
exchange of old implants.18 After diagnosis, four patients who did not
undergo immediate removal of the implants developed recurrent BIA‐
ALCL; of these, three achieved remission upon explantation19-21 but the
fourth expired.22 Data surrounding the indication for implants, volume,
type, brand, and laterality were inconsistently recorded.
3.1 | Characterization and diagnosis
BIA‐ALCL was provisionally classified as a novel lymphoma by
the World Health Organization in 2016.23 These criteria classify
BIA‐ALCL as an anaplastic lymphoma kinase ALK(‐) T‐cell lymphoma
distinct from systemic ALK(−)ALCL (sALCL).24 BIA‐ALCL is, by definition,
CD30+ and ALK1−; however, neither of these features (nor both in
25
combination) is pathognomonic of the disease. BIA‐ALCL arises around
an implant and is a disease of the breast implant capsule (the scar tissue
formed by the body around the implant) and not of the breast tissue
itself.26 Useful imaging includes ultrasound and magnetic resonance
imaging, with positron emission tomography/computed tomography
for staging if disease is confirmed.25 It is important to note that
mammography has no utility in the detection of peri‐capsular lymphoma,
as mammography generally depends on the presence of microcalcifica-
tions that are absent in BIA‐ALCL.26 Treatment and diagnostic guidelines
updated by the National Comprehensive Cancer Network (NCCN) in
March 2019 state that while the diagnosis is based upon the presence of
positive CD30 staining on immunohistochemical analysis of the fluid
surrounding the capsule, CD30+ cells can often occur in the context of
normal inflammation and this finding must be correlated to the patient’s
presentation before a final diagnosis is made with a combination of
immunohistochemical analysis and clinical judgment.25
The diagnosis requires the following findings: CD30+ immunohisto-
chemistry, large anaplastic cells on cytology, and clonal expansion on flow
cytometry.26 Cytology has been demonstrated to be effective as a
minimally invasive diagnostic method and is endorsed in the NCCN
27
guidelines as the first step of a pathology workup. Fine needle
aspiration should then be combined with flow cytometry.
The average time from the insertion of an implant to the
development of BIA‐ALCL varies by patient group due to small sample
sizes, but the American Society for Aesthetic Plastic Surgery and
American Society of Plastic Surgeon report an average of 8 years with a
26
range of 2 to 28 years.
EBNER ET AL.
3.2 | Genetic studies and biomarkers
Many of the genetic findings in patients with BIA‐ALCL are similar or
identical to the characteristics found in systemic ALCL. Activation of
the signal responsive transcription factor 3 (STAT3) is considered the
central abnormality in sALCL. Whole genome sequencing of patients
with BIA‐ALCL has revealed similar STAT3 overactivation.28 Activat-
ing mutations have also been demonstrated in JAK1 and JAK3.19,29
Prognosis in sALCL has been shown to be related to several known
translocations, such as DUSP22, with excellent prognosis, and TP63
rearrangements, with poor prognosis.30 While BIA‐ALCL morpholo-
gically and phenotypically resembles sALCL, the clinical progression
and behavior of the two diseases are distinct.31 Patient with BIA‐
ALCL have also been found to have differences in HLA A*26, which
may reveal a genetic susceptibility to developing lymphoma.32
BIA‐ALCL also has several features in common with primary
cutaneous ALCL (pcALCL), such as the expression of the transcription
factors suppressor of cytokine signaling 3 (SOCS3), JunB, and
SATB1.33 Activation of STAT3 and SOCS3 have been associated
with the transition from the benign precursor lymphomatoid
papulosis to malignant pcALCL, and Kadin et al34 have suggested a
similar progression may occur in BIA‐ALCL.
3.3 | Treatment and prognosis
The natural history of BIA‐ALCL is unknown.2 Complete surgical
excision of the implant and capsule is the accepted course of action,
with additional chemotherapy if the disease found to have spread
outside the capsule.25,35 While the prognosis of most cases is
excellent with surgical resection, fatal cases have been documented
and it remains unclear whether earlier detection or inherent
differences in the characteristics of the lymphoma account for these
discrepancies in survival.22,25
3.4 | Pathogenesis
There is no consensus on the pathogenesis of BIA‐ALCL, although
many theories have been proposed. Chronic but mild stimulation of
the immune system due to the implant or bacteria around the implant
are the most commonly proposed etiologies. CD30+ lymphomas have
been known to occur after various stimuli including arthropod bites,
metallic orthopedic implants, trauma, and various drugs.36,37 Allergic
reaction to the implant has also been proposed as a possible etiology
due to the presence of interleukin‐13, a cytokine associated with
allergic inflammation.34,38
Breast implants and breast implant capsules have been asso-
ciated with several types of non ALCL cancers, including squamous
cell carcinoma,39 large B cell lymphoma,40,41 primary T‐cell lympho-
ma,18,42,43 Sezary syndrome,44,45 and hairy cell leukemia.16 To add to
this heterogeneity, ALK+ cases of lymphoma around a breast implant
have also been documented46 despite the fact that BIA‐ALCL is
nearly always ALK−, a feature now required for its diagnosis.
EBNER ET AL.
3.5 | Textured vs smooth implants
All confirmed cases of BIA‐ALCL have occurred in patients with
textured implants.25 There have been reported cases in patients with
smooth implants however, and the raw data from the FDA Medical
Device Reports (updated September 2018) list 39 cases (n = 660)
reported in patients with smooth implants.47 Whether these cases
were reported prematurely and represent late seroma or another
process is unclear.
It has recently been proposed that the material of breast implants
may also be an important factor. Magnusson et al report an odds
ratio of 23.4 for Silimed polyurethane implants and 16.5 for Siltex
implants when compared with Biocell implants as the reference
group using data from Australia and New Zealand.48
3.6 | Biofilm theory and microbiology
It has been suggested that BIA‐ALCL arises due to subclinical
infection and chronic inflammation around the breast implant. The
presence of bacteria on the capsule may provide antigen stimulation
to T cells that becomes aberrant in some patients.33 Some authors
have suggested that the increased surface area of textured implants
harbor more bacteria and thus increase the chances of developing
BIA‐ALCL,49 while others have pointed out that biofilms form on a
variety of implantables (most notably orthopedic devices) and generally
50 51
cause sarcomas or histiocytomas when malignancy arises. Hu et al
have identified Ralstonia species as the common pathogen amongst
patients with ALCL using polymerase chain reaction and a Ralstonia
specific probe. This microbiology, they argued, is unique and represents
a difference from the Staphylococcus predominant infections that cause
capsular contracture. It is important to note that while the presence of
Ralstonia DNA does imply an episode of contamination by this pathogen
(a ubiquitous contaminant in drinking water52), it may or may not be
consistent with an ongoing infection of the breast capsule.
3.7 | Data collection and reporting
Since the FDA advisory in 2011, efforts have been made worldwide
to record cases of BIA‐ALCL and establish true incidence and
prevalence rates for the disease. The largest repository of reported
cases comes from the Patient Registry and Outcomes for breast
Implants anaplastic large cell Lymphoma etiology and Epidemiology
(PROFILE) database sponsored by the Plastic Surgery Foundation. In
the initial report released in 2019, PROFILE recorded 186 distinct
cases of ALCL between 2012‐2018.53 Cases are also reported to the
FDA’s Manufacturer and User Facility Device Experience (MAUDE), a
database designed to monitor the safety and efficacy of implanted
medical devices. As of 2015, 459 entries resulting in 130 confirmed
cases of BIA‐ALCL were recorded in MAUDE (110 in the United
States and 20 from other countries).54
Records of BIA‐ALCL are often duplicated within registries,54 and
no standardization exists for which registry to report to. Many
countries have independent breast implant registries (such as the
| 3
Dutch Breast Implant Registry55) and other countries are capturing
information on BIA‐ALCL within other health registries (such as
the French Lymphoma Study Association56). Despite the existence of
the International Breast Implant Registry, created in 2002, and the
formation of the International Collaboration of Breast Implant
Registries, there is no unifying registry for data concerning breast
implants or their adverse effects.57
4 | D I S C U SS I O N
The true incidence of BIA‐ALCL remains unknown. This is predominantly
due to the difficulty in diagnosing a disease that depends partly on
nonspecific biomarkers (CD30, ALK) and partly on nonspecific clinical
presentation (breast swelling, tenderness, lymphadenopathy, etc). This is
also due to the fragmentation of the known data on BIA‐ALCL and the
recent attention paid to the disease. Since the first documented cases in
1997, the number of papers published on the subject has steadily
increased.58 The rate of diagnosis of BIA‐ALCL is also increasing but
cannot be used to draw any meaningful conclusions, as increased
awareness and the creation of several new patient registries act as
confounders.
The reason for the attention BIA‐ALCL has received is clear: such
a disease could have far‐reaching implications for the estimated
10 million people worldwide with breast implants.1 The possibility of
a causative link between implants and lymphoma could change not
only the choice of implants but also the method of reconstruction,
and could deter patients from pursuing cosmetic surgery.
The treatment for BIA‐ALCL is complete surgical resection of the
implant and capsule, which has left many patients and surgeons with
the question of how to reconstruct a breast after lymphoma. One
case series showed that 27% of patients opted for reconstruction
after BIA‐ALCL, with immediate, autologous, and delayed reconstruc-
tion options exercised depending on the presentation.59
The most important aspect of analysis of BIA‐ALCL is informing
the patients who will ultimately undergo breast augmentation or
reconstruction of what their eventual risk may be. By all analyses to
date, the risk of BIA‐ALCL is less than 1 in 1 million, and Sieber et al60
have explained this risk as contributing to future mortality less than
drinking a half liter of wine or walking 17 miles. The cost to patients,
both in terms of anxiety over the possibility of disease and the
avoidance of interventions that can improve quality of life, must be
considered as part of the ongoing investigation of BIA‐ALCL.
5 | L IM I T AT IO N S
This study has several limitations. The first is its retrospective nature
and reliance on already published literature. The second is the
inconsistency among case reports, which often exclude data that
the authors would prefer to include. Conflicting reports exist in the
literature and the authors have made the utmost effort to include the
most relevant and up to date data on BIA‐ALCL.
4 |
6 | CONC LU SION
Further investigation of the disease process, pathophysiology,
and true prevalence is necessary to draw meaningful conclusions
about BIA‐ALCL. While the implications of a causal link could be
far‐reaching, care must be taken to provide realistic and
evidence‐based information to patients and clinicians while
investigations continue.
CO NFLICT OF I NTERE STS
The authors declare no conflicts of interest.
D A T A A C C ES SI B I L I T Y
The data that support the findings of this study are openly available
and accessible in the public domain.
OR CID
Peggy J. Ebner http://orcid.org/0000-0003-2539-6016
Alice Liu http://orcid.org/0000-0001-5672-3222
Daniel J. Gould http://orcid.org/0000-0002-3576-3775
Ketan M. Patel http://orcid.org/0000-0002-6883-4816
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How to cite this article: Ebner PJ, Liu A, Gould DJ, Patel KM.
Breast implant–associated anaplastic large cell lymphoma, a
systematic review and in‐depth evaluation of the current
understanding. J Surg Oncol. 2019;1‐5.
https://doi.org/10.1002/jso.25626