Aesth Plast Surg (2014) 38:139–145 DOI 10.1007/s00266-013-0232-z
REVIEW
BREAST
Is Late Seroma a Phenomenon Related to Textured Implants? A Report of Rare Complications and a Literature Review Bo Young Park • Dong-Han Lee • So Young Lim • Jai-Kyong Pyon • Goo-Hyun Mun • Kap-Sung Oh • Sa-Ik Bang
Received: 20 March 2013 / Accepted: 28 September 2013 / Published online: 21 November 2013 Ó Springer Science+Business Media New York and International Society of Aesthetic Plastic Surgery 2013
Abstract Background Late seroma is an infrequent complication that manifests as fluid collection in the periprosthetic space at least 1 year after breast enlargement surgery. Interest in late seroma has grown with the potential connection between breast implants and anaplastic large cell lymphoma (ALCL), which presents with clinical symptoms similar to those of late seroma. This report presents a case of late seroma experienced by a patient with a history of multiple implant ruptures and a review of the relevant literature. Methods Details are reported for a patient who presented with sudden swelling of an augmented breast that was initially suspected to be symptomatic of ALCL. A literature search of PubMed regarding this phenomenon also was conducted. Results The literature review identified 14 articles on late seroma involving 60 patients, including the reported case. Analyses included epidemiology, etiology, and management strategy. Although a detailed statistical analysis was not performed, 55 cases (92 %) of late seroma occurred that involved patients with textured implants. No evidencebased guideline for the management of late seroma has been established, although the patients were managed successfully in all cases using various strategies. Conclusions The reported case and data from the literature provide evidence of a relationship between textured implant use and late seroma. Based on their review, the authors offer ‘‘sequential treatment steps,’’ from conservative treatment to surgical management, which will be
B. Y. Park D.-H. Lee S. Y. Lim J.-K. Pyon G.-H. Mun K.-S. Oh S.-I. Bang (&) Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Irwon-dong 50, Gangnam-gu, Seoul, Korea e-mail: [email protected]
helpful for successful management of future late seroma cases. However, further study is needed to clarify the relationship, if any, between a particular type of textured implant and the development of late seroma. Level of Evidence V This journal requires that authors assign a level of evidence to each article. For a full description of these Evidence-Based Medicine ratings, please refer to the Table of Contents or the online Instructions to Authors www.springer.com/00266. Keywords Late seroma Breast augmentation Anaplastic large cell lymphoma
Introduction The use of breast implants has increased since their introduction in 1962 [1], and breast augmentation has become the most common cosmetic surgery in the United States [2]. Breast implants also have been used for breast reconstruction surgery after cancer-related mastectomy. It is estimated that *1 to 2 million women currently have silicone breast implants [3]. The increase in breast surgery has led to improved clinical outcomes. However, many imperfections related to breast implants still are reported. The exact rate of implant complications is not known, although it does not appear to be as low as many people presume, with problems occurring for approximately 20 % of women after implant surgery [3]. Complications after implant surgery include capsular contracture, rupture, leakage, infection, asymmetry, and migration of the implant [4]. Most of the complications occur in the early postoperative period, and later complications are infrequent. More recently, the rare development of late seroma-fluid collection in the periprosthetic space at least 1 year of the
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initial surgery has been described. Patients present with spontaneous progressive swelling, tenderness, and enlargement of augmented breasts. Pinchuk and Tymofii [5] reported the incidence of late seroma to be 0.88 % of all the breast augmentations performed at their center. Finally, late seroma can be associated with the presence of malignant cells related to anaplastic large cell lymphoma (ALCL). A review article reported that the majority of ALCL patients presented with late seroma phenomena, which was not differentiated from simple late seroma [6]. Widespread interest in late seroma currently is growing with evidence of a possible connection between breast implants and ALCL because the malignancy presents with the same clinical symptoms as late seroma. Descriptions of late seroma in the literature have been limited to a few case reports and original articles that suggest a common hypothesis about their etiology. Notably, the first report about late seroma appeared after the use of textured implants began [7]. Moreover, the majority of articles report that the seroma occurred in patients who had received textured implants. The etiology of late seroma, its relationship with textured implants, and the evaluation and management of the condition remain unclear. Articles regarding its etiology, its relationship with textured implants, its evaluation, and its management have not been sufficient. We present a case of late seroma involving a patient with a history of multiple implant ruptures. In this article, we seek to summarize all published reports comprehensively. In particular, we aim to analyze the epidemiology, etiology, and management strategy of late seroma.
Materials and Methods First, we present a case of sudden swelling of an augmented breast initially suspected to be symptomatic of ALCL. We conducted a literature search of PubMed using the search terms ‘‘breast implant,’’ ‘‘late seroma,’’ and ‘‘anaplastic large cell lymphoma.’’ Late seroma was defined as symptomatic swelling of the breast 1 year or more after breast implant surgery. We searched the literature from January 1990 through June 2012. No experimental article was found, so we included only the human-based topic and the English language articles. We searched 12 articles including cases, letters, and original articles about seroma.
Results Case Report A 62-year-old woman who had undergone breast augmentation surgery 4 years previously presented with
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sudden swelling of her left breast (Fig. 1a, b). She had a complicated breast augmentation history. Her first breast augmentation surgery was performed 30 years earlier in the early 1980 s. These implants ruptured in 2002. She underwent a second operation for implant replacement, but her second set of implants ruptured in 2004. A third breast augmentation/implant replacement surgery in 2004 was followed by another rupture in 2008. She visited our clinic in 2008 for implant replacement surgery. We suspected that the pressure induced by mammography could have contributed to the first and second ruptures involving silicone implants with a thin outer shell. Repetitive trauma or intense physical activity also could cause ruptures, although the patient denied any involvement in such activity. In recent studies, capsular contracture has been thought to wear on the implant shell, and subsequent implant ruptures have been reported. In a capsular contracture, the area of the connective tissue capsule covering an implant shrinks, leading to compression of the implant. As a result, rapid wear and tear occurs that eventually may cause a rupture based on various influencing factors (e.g., trauma, aggressive massage, physical training). Considering this aspect, the capsular contracture that forms after multiple surgeries with various planes could have been the cause of our patient’s complicated history [8]. In the patient’s fourth surgery, we performed a capsulectomy and replaced the implant with a Biocell style 110 textured implant (240 ml). The capsule was completely removed, and implants were inserted through the previous incision in the inframammary fold. The patient’s postoperative course was uneventful, and no complications were noted. The same patient visited our clinic reporting left breast enlargement in 2012. The swelling suddenly appeared in April 2012, with accompanying tenderness and pain. Clinical inspection showed no signs of infection such as redness or lymphadenopathy. Physical examination showed enlargement and tension of the left breast. The patient’s laboratory findings were within the normal range. Magnetic resonance imaging (MRI) showed bilateral intracapsular implant rupture together with significant retroperiprosthetic fluid collection that had low signal intensity on T1 images and high signal intensity on T2 images (Fig. 1c). Until the surgical treatment for capsulectomy and implant removal were performed, the enlargement of the patient’s breast progressed. The implants were approached through the original inframammary incision site, and removal with complete capsulectomy was achieved. During surgery, approximately 200 ml of tan-yellowcolored fluid was drained after the thin outer capsule of the left breast was opened. After drainage of the fluid, a thick inner capsule was observed around the implant (Fig. 2a).
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Fig. 1 a, b Preoperative photographs of a 62-year-old patient with breast augmentation who presented with sudden swelling of the left breast. c Magnetic resonance image (MRI) showing ruptured implants and a large amount of fluid collection in the left breast
Fig. 2 a Intraoperative photograph of the left breast capsule and seroma collection. b The removed implant was ruptured at multiple sites, showing an inner thick capsule and an outer thin capsule
No replacement implant was inserted, and the cavity was irrigated with a solution containing triple antibiotics. The inframammary incision was closed, and no complications were observed after surgery. During a 1-year follow-up period, the postoperative course was uneventful (Fig. 3). Literature Review
Fig. 3 Postoperative photograph 1 year after seroma drainage, implant removal, and capsulectomy
Both the thick inner and thin outer capsules were removed (Fig. 2b). The fluid was examined for cytology and culture but showed no significant findings. The removed implants were ruptured at multiple sites (Fig. 2b).
This analysis examined 14 articles regarding late seroma [2, 5, 9–18, 22, 23] (Table 1), which reported on 60 patients (including those in the current study). Spear et al. [18] reported on 28 cases of late seroma in 2012, which accounted for nearly half of the total cases involving this disease. The patients ranged in age from 18 to 63 years (mean, 42 years, 2 months). The interval between implant insertion and diagnosis of late seroma ranged from 365 to 8,030 days (mean, 1,413 days [3.87 years]). In five cases (8 %), augmentation mastopexy preceded surgery for implant insertion. Breast augmentation was performed in 42 cases (70 %), and implants were inserted for breast reconstruction in the remaining 13 cases (22 %) (Table 2). In three cases, implant-based reconstruction was performed on a previously irradiated breast. Textured implants were inserted in 55 cases (92 %) and smooth implants in only 2 cases (3 %) (Table 3; Fig. 4). Late seroma occurred in 49 cases (82 %) with textured implants manufactured by Allergan (Irvine, CA, USA), in 3
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Table 1 Articles about late seroma of the breast Year
Authors
Cases
Titles
Journal name
Article type
1992
Wuest [9]
1
Breast implant seroma in pregnancy
Br J Plast Surg 45:328
Case
2005
Roman and Perkins [22]
1
Progressive spontaneous unilateral enlargement of the breast twentytwo years after prosthetic breast augmentation
Br J Plast Surg 58:88–91
Case
2007
Oliveira et al. [10]
1
Late seroma after breast augmentation with silicone prosthesis: A case report
Breast J 13:421–423
Case
2009
Chourmouzi et al. [2]
1
New spontaneous breast seroma 5 years after augmentation: A case report
Case J 2:7126
Case
2009
Fodor and Moscona [11]
1
Late posttraumatic intracapsular seroma after breast augmentation
J Plast Reconstr Aesthetic Surg 62:e609–e610
Correspondence and communication
2011
Pinchuk and Tymofii [5]
6
Seroma as a late complication after breast augmentation
Aesthetic Plast Surg 35:303–314
Original
2011
Farina et al. [13]
1
J Plast Reconstr Aesthetic Surg 64:e216–e217
Correspondence and communication
2011
Bengtson et al. [12]
0
Jogging as a possible cause of late seroma after aesthetic breast augmentation with textured silicone prosthesis: A conservative approach Managing late periprosthetic fluid collections(seroma) in patients with breast implants: A consensus panel recommendation and review of the literature
Plast Reconstr Surg 128:1–7
Original
2011
Tansle and Powell [15]
1
Late swelling after bilateral breast augmentation
J Plast Reconstr Aesthetic Surg 64:261–263
Case
2011
Hall-Findlay [19]
3
Breast implant complication review: Double capsules and late seroma
Plast Reconstr Surg 127:56–66
Original
2011
Cheng et al. [23]
1
Late haematoma and seroma in patients with silicone mammary prosthesis: Our reports and literature review
J Plast Reconstr Aesthet Surg 64:185–186
Correspondence and communication
2012
Roth et al. [17]
1
Late seroma during pregnancy, a rare complication in prosthetic breast augmentation: Case report
J Plast Reconstr Aesthetic Surg 65:973–976
Case
2012
Mazzocchi et al. [16]
13
A clinical study of late seroma in breast implantation surgery
Aesthetic Plast Surg 36:97–104
Original
2012
Spear et al. [18]
28
Late seromas after breast implants: Theory and practice
Plast Reconstr Surg 130:423–435
Original
Table 2 Patient characteristics Age (18–63 years; mean, 42 years 2 months) Interval (365–8,030 days; mean, 1,413 days) Type of operation Augmentation mastopexy: 5 (8 %) Breast augmentation: 42 (70 %) Breast reconstruction: 13 (22 %)
cases (5 %) with implants from Mentor (Santa Barbara, CA, USA), and in 2 cases (3 %) with implants from Polytech (Dieburg, Germany) (Table 3). Of the 49 Allergan textured implant cases, 43 had known style numbers
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(14 denoting round textured implants and 29 denoting anatomically shaped implants) (Table 3). A history of minor trauma was reported before the occurrence of seroma in 12 cases (20 %). Breast enlargement was the only symptom reported in 50 cases (83 %). Upper respiratory infection-like symptoms and general weakness were reported in five cases (3.5 %), and possible signs of infection including redness, swelling, or fever were reported in five cases (3.5 %). In 14 of 60 cases, the volume of seroma was analyzed. The aspirated volume ranged widely from 5 to 700 ml (average, 262 ml). The implants had been placed in the subglandular pocket in 20 cases (33 %), the subpectoral plane in 37 cases (62 %), the subfascial plane in two cases
Aesth Plast Surg (2014) 38:139–145 Table 3 Implant characteristics associated with late seroma (60 cases)
143 Table 4 Surgical procedures in late seroma patients Surgical procedure
Cases n (%)
Textured implant: 55 (92 %)
Capsulectomy, seroma drainage, implant change
29(60)
Smooth implant: 2 (3 %)
Capsulectomy, seroma drainage, implant removal
6(12)
Unknown: 3 (5 %)
Capsulectomy, seroma drainage, implant reinsertion
1(2)
Seroma drainage, implant change
3(6)
Silicone: 57 (95 %)
Seroma drainage, implant removal
6(12)
Saline: 1 (2 %)
Seroma drainage, implant reinsertion
2(4)
Unknown: 2 (3 %)
Open seroma drainage (capsulocentesis)
2(4)
Total
49
Surface type of implant
Fill type of implant
Manufacturer of implants Allergan textured implant: 49 (82 %) Style 110: 3 Style 115: 8 Style 120: 3 Style 153: 5 Style 410: 24 Unknown style number textured: 6 Allergan smooth saline implant: 2 (3 %) Mentor textured implant: 3 (5 %) Polythec textured implant: 2 (3 %) Unknown origin textured implant: 4 (7 %)
In the surgery group, three surgical procedures were performed including capsulectomy, seroma drainage, and implant management (change/removal/reinsertion). Of the 49 surgically treated late seroma cases, 37 (76 %) involved capsulectomy and 12 (24 %) did not. Seroma drainage was performed in all cases. Previously inserted implants were managed in various ways, including change, removal, and reinsertion. In 37 (76 %) of 49 cases, implants were replaced (with textured implants in 24 cases and smooth implants in 13 cases). In seven cases (14 %), implants were removed with no replacement. The patient’s original implants were reused in five cases (10 %) (Table 4).
Discussion
Fig. 4 Textured implants were inserted in 55 cases (92 %) and smooth implants in only 2 cases (3 %)
(3 %), and the dual plane in one case (2 %). All tested fluid showed negative results for malignant cells, and culturing showed only two cases (3 %) of growth, Staphylococcus epidermidis in both cases. No comments concerning the ‘‘double-capsule phenomenon’’ were noted except in the article by Findlay and co-authors [18]. However, during surgery in the reported case, double-capsule formation of an inner thick capsule with an outer thin capsule was observed. Late seroma has been treated in various ways. No evidence-based consensus exists on how to treat late seroma using breast implant surgery. Surgery was involved in 49 cases (82 %) of the 60 late seromas, and 11 cases (18 %) were treated nonsurgically with medication (antiviral agents or antibiotics) or ultrasound-guided aspiration.
Reports of individual cases and small case series of breast implantation have triggered concerns about late seroma. Altogether, 60 cases of breast implant-associated late seroma have been reported, including the case reported in this article. However, the known incidence may be underestimated, and no consensus has been reached on recommended treatment. According to the data from the adjunct (n = 83,968) and core (n = 940) clinical trials sponsored by Allergan, 62 cases involving a minimal amount of periprosthetic late fluid collection occurred 1 year or more after implantation despite the identification of only 60 cases in the literature review [12]. A small amount of fluid is frequently observed in the periprosthetic cavity during revisional surgery. This fluid plays a role in reducing frictional force and in protecting the sliding surface. It was observed in 15 % of cases, and a small amount of fluid can be considered normal in maintenance of the balance between exudation and resorption [20]. However, a pathologic exudation to the periprosthetic space results in formation of seroma. The diagnosis of late seroma can be confirmed by negative results from bacteriologic and cytologic examination at least 1 year after implant surgery. The etiology of this
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phenomenon comprises nonmechanical factors (subclinical infection due to biofilm or chemical reaction) and mechanical factors (macro and micro repetitive trauma). A nonmechanical factor is thought to be implicated in seroma due to local inflammatory reactions. According to the subclinical infection theory, inflammatory mediators such as histamine, serotonin, and prostaglandins may be released and can produce vasodilation that increases interstitial fluid drainage. An influx of inflammatory cells creates a change in the osmotic gradient that generates further serous fluid accumulation [5]. Chemical reactions to the silicone gel ingredients in implants, which can cause a local allergic reaction, have been reported. Also, implant ruptures have been observed frequently in late seroma patients [21]. Pinchuk and Tymofii [5] managed six cases of late seroma patients and posited that any change in the body, including hormonal change and hypothermia, that weakens the immune system may result in a severe inflammatory reaction, with excessive exudates of serous fluid similar to that of synovitis. However, mechanical causes of late seroma are more commonly reported than nonmechanical causes. In this scenario, the capsule on the macropore textured implants adheres like Velcro and can be easily separated [19]. After the initial adherence of the capsule to an implant, it becomes separated. Minor repeated trauma results in an excessively rough surface and can create a seroma due to shearing forces. Evidence for this scenario has been provided by histologic examinations after removal of the macropore textured implants and capsulectomy. Recently, this mechanical theory of the association between late seroma and textured implants has received greater attention. In 49 cases (82 %), late seroma was found in patients with Biocell textured implants, suggesting that late seroma formation is strongly associated with the mechanical features of certain breast implants. The authors suggest that mechanical factors play an important role in the formation of late seroma due to evidence provided in the current literature review. Most cases of late seroma have involved a particular type of textured implant. Also, the capsule around Biocell textured implants, confirmed during other revision surgeries, has been separated easily with minor physical force. The late seroma phenomenon can sometimes be accompanied by implant rupture, as in the reported case, which is further evidence of frictional force. However, understanding of the biology, etiology, treatment, and prognosis of implantrelated late seroma will require substantial research effort, including in vitro experiments, collection of clinical information, and well-designed epidemiologic studies, to show the association with macropore textured implants. With regard to treatment strategy, it is most important that treatment guidelines be standardized based on a
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thorough understanding of late seroma phenomena. Currently, no consensus or evidence-based guideline exists for the treatment of late seroma. In 2011, the Breast Implant Working Group devised a comprehensive diagnostic and therapeutic algorithm for breast surgeons through the review of 12 late seroma cases [12]. In the first step of the algorithm, infection should be ruled out, and aspiration of fluid, culture, and cell counts are recommended when possible. Empirical broad-spectrum antibiotics are an option if clinical suspicion of infection is high. The second step involves imaging studies including ultrasound, which is recommended, or MRI, which is optional. The ultrasound should examine the periprosthetic fluid drainage and assist with procedures to obtain fluid for culture or cytology for differential diagnosis. The MRI can be used to aid in differential diagnosis of periprosthetic fluid collection versus generalized breast swelling or in the detection of combined implant rupture. When palpable or radiologic evidence of a mass is encountered, standard oncologic evaluation should be performed. Surgical exploration is recommended if the diagnosis is ambiguous or if the seroma is refractory with no evidence of neoplasia. Of 60 late seroma cases, 11 (18 %) were managed nonsurgically without recurrence, highlighting the fact that surgeons should consider conservative management first, including medication or ultrasound-guided aspiration. Surgical procedures are recommended to resolve recurrent periprosthetic fluid collection with negative cultures that do not respond to antibiotics. For surgical exploration, the Breast Implant Working Group recommended, by consensus, total capsulectomy with or without replacement of a new implant if technically possible without damage to surrounding tissues. The capsule should be examined for any abnormality, and additional histologic examination is recommended. In clinical cases, capsulectomy was performed in 37 of the 49 surgical cases of late seroma, with a sequential procedure involving capsulectomy, seroma drainage, and implant change most frequently applied. After a thorough literature review, we can propose the following more simplified guidelines for late seroma management. In the first stage, infection should be excluded for all patients with sudden-onset breast swelling. If signs of infection are observed, surgeons should treat the patient with antibiotics or antiviral agents. If this management is not effective, ultrasound-guided aspiration should be performed for diagnosis and treatment. The obtained fluid should be examined for culture, cytology, and/or cell count to rule out malignancy. Also, MRI is recommended in this step for confirmation of the diagnosis and for investigation of combined abnormality such as implant rupture.
Aesth Plast Surg (2014) 38:139–145
If symptoms recur or do not improve after the radiologic step (ultrasound-guided aspiration), surgery should be considered. In this step, seroma drainage and capsulectomy (when possible without damage to the breast tissue) may be essential, and implant removal or change should be performed. Also, cytology and culture should be repeated to confirm the diagnosis. One surprising feature of the reviewed cases was the almost complete success with implant exchange, whether the implants were replaced with a new Biocell textured implant or a smooth implant. However, at this writing, the follow-up period has not been sufficiently long for a clinical determination regarding their appropriateness. It seems reasonable to pursue conservative treatment first because surgical treatment is not required in all cases. In every case, the patient should be treated after the aforementioned sequential steps, and culture and cytology are required to rule out infection and malignancy. We concur with the opinions of the Breast Implant Working Group that nontreatment, random biopsy, closing of the surgical incision, and repetition of ultrasound-guided aspiration of reaccumulated fluid are not recommended [12]. Furthermore, a study investigating the association between a particular type of textured implant and the development of late seroma should be undertaken to evaluate etiologic factors.
Conclusion Late seroma is an infrequently reported complication of breast implant surgery. The etiology is not clearly understood, but most cases have occurred with use of the Biocell textured implant. Suspicion regarding this association is increasing, but further evaluations are needed. Guidelines regarding the management of late seroma have not been confirmed, and it has been treated with various methods. However, sequential simplified treatment steps would be helpful for successful management of late seroma. Nevertheless, during any type of treatment strategy, cytology and culture are essential for the differential diagnosis of ALCL.
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5. 6.
7. 8.
9. 10.
11.
12.
13.
14. 15. 16.
17.
18.
19. 20.
References 1. Kulmala I, McLaughlin JK, Pakkanen M, Lassila K, Holmich LR, Lipworth L, Boice JD Jr, Raitanen J, Luoto R (2004) Local complications after cosmetic breast implant surgery in Finland. Ann Plast Surg 53:413–419 2. Chourmouzi D, Vryzas T, Drevelegas A (2009) New spontaneous breast seroma 5 years after augmentation: a case report. Cases J 2:7126 3. Kjoller K, Holmich LR, Jacobsen PH, Friis S, Fryzek J, McLaughlin JK, Lipworth L, Henriksen TF, Jorgensen S,
21.
22.
23.
Bittmann S, Olsen JH (2002) Epidemiological investigation of local complications after cosmetic breast implant surgery in Denmark. Ann Plast Surg 48:229–237 Nahabedian MY, Patel K (2009) Management of common and uncommon problems after primary breast augmentation. Clin Plast Surg 36(vii):127–138 Pinchuk V, Tymofii O (2011) Seroma as a late complication after breast augmentation. Aesthetic Plast Surg 35:303–314 Kim B, Roth C, Young VL, Chung KC, van Busum K, Schnyer C, Mattke S (2011) Anaplastic large cell lymphoma and breast implants: results from a structured expert consultation process. Plast Reconstr Surg 128:629–639 Cormack G (1991) Breast hypoplasia. Br J Plast Surg 44:628 Pinchuk V, Tymofii O, Tkach O, Zamkoboy V (2013) Implant ruptures after augmentation mammoplasty. Aesthetic Plast Surg 37:60–67 Wuest WL (1992) Breast implant seroma in pregnancy. Br J Plast Surg 45:328 Oliveira VM, Roveda Junior D, Lucas FB, Lucarelli AP, Martins MM, Rinaldi JF, Aoki T (2007) Late seroma after breast augmentation with silicone prostheses: A case report. Breast J 13:421–423 Fodor L, Moscona R (2009) Late posttraumatic intracapsular seroma after breast augmentation. J Plast Reconstr Aesthet Surg 62:e609–e610 Bengtson B, Brody GS, Brown MH, Glicksman C, Hammond D, Kaplan H, Maxwell GP, Oefelein MG, Reisman NR, Spear SL, Jewell ML (2011) Managing late periprosthetic fluid collections (seroma) in patients with breast implants: a consensus panel recommendation and review of the literature. Plast Reconstr Surg 128:1–7 Farina JA Jr, Ramalli EL, Da Silva MF, Silva R (2011) Jogging as a possible cause of late seroma after aesthetic breast augmentation with textured silicone prosthesis: A conservative approach. J Plast Reconstr Aesthet Surg 64:e216–e217 Robinson HN (2011) Breast implant complication review: Double capsules and late seromas. Plast Reconstr Surg 128:818–819 Tansley PD, Powell BW (2011) Late swelling after bilateral breast augmentation. J Plast Reconstr Aesthet Surg 64:261–263 Mazzocchi M, Dessy LA, Corrias F, Scuderi N (2012) A clinical study of late seroma in breast implantation surgery. Aesthetic Plast Surg 36:97–104 Roth FS, Gould DJ, Chike-Obi CJ, Bullocks JM (2012) Late seroma during pregnancy, a rare complication in prosthetic breast augmentation: case report. J Plast Reconstr Aesthet Surg 65:973–976 Spear SL, Rottman SJ, Glicksman C, Brown M, Al-Attar A (2012) Late seromas after breast implants: theory and practice. Plast Reconstr Surg 130:423–435 Hall-Findlay EJ (2011) Breast implant complication review: double capsules and late seromas. Plast Reconstr Surg 127:56–66 Ahn CY, Ko CY, Wagar EA, Wong RS, Shaw WW (1995) Clinical significance of intracapsular fluid in patients’ breast implants. Ann Plast Surg 35:455–457 Flassbeck D, Pfleiderer B, Klemens P, Heumann KG, Eltze E, Hirner AV (2003) Determination of siloxanes, silicon, and platinum in tissues of women with silicone gel-filled implants. Anal Bioanal Chem 375:356–362 Roman S, Perkins D (2005) Progressive spontaneous unilateral enlargement of the breast twenty-two years after prosthetic breast augmentation. Br J Plast Surg 58:88–91 Cheng NX, Chen B, Li Q, Wu DH, Zhu L, Zhang XM, Chen YL (2011) Late haematoma and seroma in patients with silicone mammary prosthesis: our reports and literature review. J Plast Recontr Aesthet Surg 64:e185–e186
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REVIEW
BREAST
Is Late Seroma a Phenomenon Related to Textured Implants? A Report of Rare Complications and a Literature Review Bo Young Park • Dong-Han Lee • So Young Lim • Jai-Kyong Pyon • Goo-Hyun Mun • Kap-Sung Oh • Sa-Ik Bang
Received: 20 March 2013 / Accepted: 28 September 2013 / Published online: 21 November 2013 Ó Springer Science+Business Media New York and International Society of Aesthetic Plastic Surgery 2013
Abstract Background Late seroma is an infrequent complication that manifests as fluid collection in the periprosthetic space at least 1 year after breast enlargement surgery. Interest in late seroma has grown with the potential connection between breast implants and anaplastic large cell lymphoma (ALCL), which presents with clinical symptoms similar to those of late seroma. This report presents a case of late seroma experienced by a patient with a history of multiple implant ruptures and a review of the relevant literature. Methods Details are reported for a patient who presented with sudden swelling of an augmented breast that was initially suspected to be symptomatic of ALCL. A literature search of PubMed regarding this phenomenon also was conducted. Results The literature review identified 14 articles on late seroma involving 60 patients, including the reported case. Analyses included epidemiology, etiology, and management strategy. Although a detailed statistical analysis was not performed, 55 cases (92 %) of late seroma occurred that involved patients with textured implants. No evidencebased guideline for the management of late seroma has been established, although the patients were managed successfully in all cases using various strategies. Conclusions The reported case and data from the literature provide evidence of a relationship between textured implant use and late seroma. Based on their review, the authors offer ‘‘sequential treatment steps,’’ from conservative treatment to surgical management, which will be
B. Y. Park D.-H. Lee S. Y. Lim J.-K. Pyon G.-H. Mun K.-S. Oh S.-I. Bang (&) Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Irwon-dong 50, Gangnam-gu, Seoul, Korea e-mail: [email protected]
helpful for successful management of future late seroma cases. However, further study is needed to clarify the relationship, if any, between a particular type of textured implant and the development of late seroma. Level of Evidence V This journal requires that authors assign a level of evidence to each article. For a full description of these Evidence-Based Medicine ratings, please refer to the Table of Contents or the online Instructions to Authors www.springer.com/00266. Keywords Late seroma Breast augmentation Anaplastic large cell lymphoma
Introduction The use of breast implants has increased since their introduction in 1962 [1], and breast augmentation has become the most common cosmetic surgery in the United States [2]. Breast implants also have been used for breast reconstruction surgery after cancer-related mastectomy. It is estimated that *1 to 2 million women currently have silicone breast implants [3]. The increase in breast surgery has led to improved clinical outcomes. However, many imperfections related to breast implants still are reported. The exact rate of implant complications is not known, although it does not appear to be as low as many people presume, with problems occurring for approximately 20 % of women after implant surgery [3]. Complications after implant surgery include capsular contracture, rupture, leakage, infection, asymmetry, and migration of the implant [4]. Most of the complications occur in the early postoperative period, and later complications are infrequent. More recently, the rare development of late seroma-fluid collection in the periprosthetic space at least 1 year of the
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initial surgery has been described. Patients present with spontaneous progressive swelling, tenderness, and enlargement of augmented breasts. Pinchuk and Tymofii [5] reported the incidence of late seroma to be 0.88 % of all the breast augmentations performed at their center. Finally, late seroma can be associated with the presence of malignant cells related to anaplastic large cell lymphoma (ALCL). A review article reported that the majority of ALCL patients presented with late seroma phenomena, which was not differentiated from simple late seroma [6]. Widespread interest in late seroma currently is growing with evidence of a possible connection between breast implants and ALCL because the malignancy presents with the same clinical symptoms as late seroma. Descriptions of late seroma in the literature have been limited to a few case reports and original articles that suggest a common hypothesis about their etiology. Notably, the first report about late seroma appeared after the use of textured implants began [7]. Moreover, the majority of articles report that the seroma occurred in patients who had received textured implants. The etiology of late seroma, its relationship with textured implants, and the evaluation and management of the condition remain unclear. Articles regarding its etiology, its relationship with textured implants, its evaluation, and its management have not been sufficient. We present a case of late seroma involving a patient with a history of multiple implant ruptures. In this article, we seek to summarize all published reports comprehensively. In particular, we aim to analyze the epidemiology, etiology, and management strategy of late seroma.
Materials and Methods First, we present a case of sudden swelling of an augmented breast initially suspected to be symptomatic of ALCL. We conducted a literature search of PubMed using the search terms ‘‘breast implant,’’ ‘‘late seroma,’’ and ‘‘anaplastic large cell lymphoma.’’ Late seroma was defined as symptomatic swelling of the breast 1 year or more after breast implant surgery. We searched the literature from January 1990 through June 2012. No experimental article was found, so we included only the human-based topic and the English language articles. We searched 12 articles including cases, letters, and original articles about seroma.
Results Case Report A 62-year-old woman who had undergone breast augmentation surgery 4 years previously presented with
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sudden swelling of her left breast (Fig. 1a, b). She had a complicated breast augmentation history. Her first breast augmentation surgery was performed 30 years earlier in the early 1980 s. These implants ruptured in 2002. She underwent a second operation for implant replacement, but her second set of implants ruptured in 2004. A third breast augmentation/implant replacement surgery in 2004 was followed by another rupture in 2008. She visited our clinic in 2008 for implant replacement surgery. We suspected that the pressure induced by mammography could have contributed to the first and second ruptures involving silicone implants with a thin outer shell. Repetitive trauma or intense physical activity also could cause ruptures, although the patient denied any involvement in such activity. In recent studies, capsular contracture has been thought to wear on the implant shell, and subsequent implant ruptures have been reported. In a capsular contracture, the area of the connective tissue capsule covering an implant shrinks, leading to compression of the implant. As a result, rapid wear and tear occurs that eventually may cause a rupture based on various influencing factors (e.g., trauma, aggressive massage, physical training). Considering this aspect, the capsular contracture that forms after multiple surgeries with various planes could have been the cause of our patient’s complicated history [8]. In the patient’s fourth surgery, we performed a capsulectomy and replaced the implant with a Biocell style 110 textured implant (240 ml). The capsule was completely removed, and implants were inserted through the previous incision in the inframammary fold. The patient’s postoperative course was uneventful, and no complications were noted. The same patient visited our clinic reporting left breast enlargement in 2012. The swelling suddenly appeared in April 2012, with accompanying tenderness and pain. Clinical inspection showed no signs of infection such as redness or lymphadenopathy. Physical examination showed enlargement and tension of the left breast. The patient’s laboratory findings were within the normal range. Magnetic resonance imaging (MRI) showed bilateral intracapsular implant rupture together with significant retroperiprosthetic fluid collection that had low signal intensity on T1 images and high signal intensity on T2 images (Fig. 1c). Until the surgical treatment for capsulectomy and implant removal were performed, the enlargement of the patient’s breast progressed. The implants were approached through the original inframammary incision site, and removal with complete capsulectomy was achieved. During surgery, approximately 200 ml of tan-yellowcolored fluid was drained after the thin outer capsule of the left breast was opened. After drainage of the fluid, a thick inner capsule was observed around the implant (Fig. 2a).
Aesth Plast Surg (2014) 38:139–145
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Fig. 1 a, b Preoperative photographs of a 62-year-old patient with breast augmentation who presented with sudden swelling of the left breast. c Magnetic resonance image (MRI) showing ruptured implants and a large amount of fluid collection in the left breast
Fig. 2 a Intraoperative photograph of the left breast capsule and seroma collection. b The removed implant was ruptured at multiple sites, showing an inner thick capsule and an outer thin capsule
No replacement implant was inserted, and the cavity was irrigated with a solution containing triple antibiotics. The inframammary incision was closed, and no complications were observed after surgery. During a 1-year follow-up period, the postoperative course was uneventful (Fig. 3). Literature Review
Fig. 3 Postoperative photograph 1 year after seroma drainage, implant removal, and capsulectomy
Both the thick inner and thin outer capsules were removed (Fig. 2b). The fluid was examined for cytology and culture but showed no significant findings. The removed implants were ruptured at multiple sites (Fig. 2b).
This analysis examined 14 articles regarding late seroma [2, 5, 9–18, 22, 23] (Table 1), which reported on 60 patients (including those in the current study). Spear et al. [18] reported on 28 cases of late seroma in 2012, which accounted for nearly half of the total cases involving this disease. The patients ranged in age from 18 to 63 years (mean, 42 years, 2 months). The interval between implant insertion and diagnosis of late seroma ranged from 365 to 8,030 days (mean, 1,413 days [3.87 years]). In five cases (8 %), augmentation mastopexy preceded surgery for implant insertion. Breast augmentation was performed in 42 cases (70 %), and implants were inserted for breast reconstruction in the remaining 13 cases (22 %) (Table 2). In three cases, implant-based reconstruction was performed on a previously irradiated breast. Textured implants were inserted in 55 cases (92 %) and smooth implants in only 2 cases (3 %) (Table 3; Fig. 4). Late seroma occurred in 49 cases (82 %) with textured implants manufactured by Allergan (Irvine, CA, USA), in 3
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Table 1 Articles about late seroma of the breast Year
Authors
Cases
Titles
Journal name
Article type
1992
Wuest [9]
1
Breast implant seroma in pregnancy
Br J Plast Surg 45:328
Case
2005
Roman and Perkins [22]
1
Progressive spontaneous unilateral enlargement of the breast twentytwo years after prosthetic breast augmentation
Br J Plast Surg 58:88–91
Case
2007
Oliveira et al. [10]
1
Late seroma after breast augmentation with silicone prosthesis: A case report
Breast J 13:421–423
Case
2009
Chourmouzi et al. [2]
1
New spontaneous breast seroma 5 years after augmentation: A case report
Case J 2:7126
Case
2009
Fodor and Moscona [11]
1
Late posttraumatic intracapsular seroma after breast augmentation
J Plast Reconstr Aesthetic Surg 62:e609–e610
Correspondence and communication
2011
Pinchuk and Tymofii [5]
6
Seroma as a late complication after breast augmentation
Aesthetic Plast Surg 35:303–314
Original
2011
Farina et al. [13]
1
J Plast Reconstr Aesthetic Surg 64:e216–e217
Correspondence and communication
2011
Bengtson et al. [12]
0
Jogging as a possible cause of late seroma after aesthetic breast augmentation with textured silicone prosthesis: A conservative approach Managing late periprosthetic fluid collections(seroma) in patients with breast implants: A consensus panel recommendation and review of the literature
Plast Reconstr Surg 128:1–7
Original
2011
Tansle and Powell [15]
1
Late swelling after bilateral breast augmentation
J Plast Reconstr Aesthetic Surg 64:261–263
Case
2011
Hall-Findlay [19]
3
Breast implant complication review: Double capsules and late seroma
Plast Reconstr Surg 127:56–66
Original
2011
Cheng et al. [23]
1
Late haematoma and seroma in patients with silicone mammary prosthesis: Our reports and literature review
J Plast Reconstr Aesthet Surg 64:185–186
Correspondence and communication
2012
Roth et al. [17]
1
Late seroma during pregnancy, a rare complication in prosthetic breast augmentation: Case report
J Plast Reconstr Aesthetic Surg 65:973–976
Case
2012
Mazzocchi et al. [16]
13
A clinical study of late seroma in breast implantation surgery
Aesthetic Plast Surg 36:97–104
Original
2012
Spear et al. [18]
28
Late seromas after breast implants: Theory and practice
Plast Reconstr Surg 130:423–435
Original
Table 2 Patient characteristics Age (18–63 years; mean, 42 years 2 months) Interval (365–8,030 days; mean, 1,413 days) Type of operation Augmentation mastopexy: 5 (8 %) Breast augmentation: 42 (70 %) Breast reconstruction: 13 (22 %)
cases (5 %) with implants from Mentor (Santa Barbara, CA, USA), and in 2 cases (3 %) with implants from Polytech (Dieburg, Germany) (Table 3). Of the 49 Allergan textured implant cases, 43 had known style numbers
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(14 denoting round textured implants and 29 denoting anatomically shaped implants) (Table 3). A history of minor trauma was reported before the occurrence of seroma in 12 cases (20 %). Breast enlargement was the only symptom reported in 50 cases (83 %). Upper respiratory infection-like symptoms and general weakness were reported in five cases (3.5 %), and possible signs of infection including redness, swelling, or fever were reported in five cases (3.5 %). In 14 of 60 cases, the volume of seroma was analyzed. The aspirated volume ranged widely from 5 to 700 ml (average, 262 ml). The implants had been placed in the subglandular pocket in 20 cases (33 %), the subpectoral plane in 37 cases (62 %), the subfascial plane in two cases
Aesth Plast Surg (2014) 38:139–145 Table 3 Implant characteristics associated with late seroma (60 cases)
143 Table 4 Surgical procedures in late seroma patients Surgical procedure
Cases n (%)
Textured implant: 55 (92 %)
Capsulectomy, seroma drainage, implant change
29(60)
Smooth implant: 2 (3 %)
Capsulectomy, seroma drainage, implant removal
6(12)
Unknown: 3 (5 %)
Capsulectomy, seroma drainage, implant reinsertion
1(2)
Seroma drainage, implant change
3(6)
Silicone: 57 (95 %)
Seroma drainage, implant removal
6(12)
Saline: 1 (2 %)
Seroma drainage, implant reinsertion
2(4)
Unknown: 2 (3 %)
Open seroma drainage (capsulocentesis)
2(4)
Total
49
Surface type of implant
Fill type of implant
Manufacturer of implants Allergan textured implant: 49 (82 %) Style 110: 3 Style 115: 8 Style 120: 3 Style 153: 5 Style 410: 24 Unknown style number textured: 6 Allergan smooth saline implant: 2 (3 %) Mentor textured implant: 3 (5 %) Polythec textured implant: 2 (3 %) Unknown origin textured implant: 4 (7 %)
In the surgery group, three surgical procedures were performed including capsulectomy, seroma drainage, and implant management (change/removal/reinsertion). Of the 49 surgically treated late seroma cases, 37 (76 %) involved capsulectomy and 12 (24 %) did not. Seroma drainage was performed in all cases. Previously inserted implants were managed in various ways, including change, removal, and reinsertion. In 37 (76 %) of 49 cases, implants were replaced (with textured implants in 24 cases and smooth implants in 13 cases). In seven cases (14 %), implants were removed with no replacement. The patient’s original implants were reused in five cases (10 %) (Table 4).
Discussion
Fig. 4 Textured implants were inserted in 55 cases (92 %) and smooth implants in only 2 cases (3 %)
(3 %), and the dual plane in one case (2 %). All tested fluid showed negative results for malignant cells, and culturing showed only two cases (3 %) of growth, Staphylococcus epidermidis in both cases. No comments concerning the ‘‘double-capsule phenomenon’’ were noted except in the article by Findlay and co-authors [18]. However, during surgery in the reported case, double-capsule formation of an inner thick capsule with an outer thin capsule was observed. Late seroma has been treated in various ways. No evidence-based consensus exists on how to treat late seroma using breast implant surgery. Surgery was involved in 49 cases (82 %) of the 60 late seromas, and 11 cases (18 %) were treated nonsurgically with medication (antiviral agents or antibiotics) or ultrasound-guided aspiration.
Reports of individual cases and small case series of breast implantation have triggered concerns about late seroma. Altogether, 60 cases of breast implant-associated late seroma have been reported, including the case reported in this article. However, the known incidence may be underestimated, and no consensus has been reached on recommended treatment. According to the data from the adjunct (n = 83,968) and core (n = 940) clinical trials sponsored by Allergan, 62 cases involving a minimal amount of periprosthetic late fluid collection occurred 1 year or more after implantation despite the identification of only 60 cases in the literature review [12]. A small amount of fluid is frequently observed in the periprosthetic cavity during revisional surgery. This fluid plays a role in reducing frictional force and in protecting the sliding surface. It was observed in 15 % of cases, and a small amount of fluid can be considered normal in maintenance of the balance between exudation and resorption [20]. However, a pathologic exudation to the periprosthetic space results in formation of seroma. The diagnosis of late seroma can be confirmed by negative results from bacteriologic and cytologic examination at least 1 year after implant surgery. The etiology of this
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phenomenon comprises nonmechanical factors (subclinical infection due to biofilm or chemical reaction) and mechanical factors (macro and micro repetitive trauma). A nonmechanical factor is thought to be implicated in seroma due to local inflammatory reactions. According to the subclinical infection theory, inflammatory mediators such as histamine, serotonin, and prostaglandins may be released and can produce vasodilation that increases interstitial fluid drainage. An influx of inflammatory cells creates a change in the osmotic gradient that generates further serous fluid accumulation [5]. Chemical reactions to the silicone gel ingredients in implants, which can cause a local allergic reaction, have been reported. Also, implant ruptures have been observed frequently in late seroma patients [21]. Pinchuk and Tymofii [5] managed six cases of late seroma patients and posited that any change in the body, including hormonal change and hypothermia, that weakens the immune system may result in a severe inflammatory reaction, with excessive exudates of serous fluid similar to that of synovitis. However, mechanical causes of late seroma are more commonly reported than nonmechanical causes. In this scenario, the capsule on the macropore textured implants adheres like Velcro and can be easily separated [19]. After the initial adherence of the capsule to an implant, it becomes separated. Minor repeated trauma results in an excessively rough surface and can create a seroma due to shearing forces. Evidence for this scenario has been provided by histologic examinations after removal of the macropore textured implants and capsulectomy. Recently, this mechanical theory of the association between late seroma and textured implants has received greater attention. In 49 cases (82 %), late seroma was found in patients with Biocell textured implants, suggesting that late seroma formation is strongly associated with the mechanical features of certain breast implants. The authors suggest that mechanical factors play an important role in the formation of late seroma due to evidence provided in the current literature review. Most cases of late seroma have involved a particular type of textured implant. Also, the capsule around Biocell textured implants, confirmed during other revision surgeries, has been separated easily with minor physical force. The late seroma phenomenon can sometimes be accompanied by implant rupture, as in the reported case, which is further evidence of frictional force. However, understanding of the biology, etiology, treatment, and prognosis of implantrelated late seroma will require substantial research effort, including in vitro experiments, collection of clinical information, and well-designed epidemiologic studies, to show the association with macropore textured implants. With regard to treatment strategy, it is most important that treatment guidelines be standardized based on a
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thorough understanding of late seroma phenomena. Currently, no consensus or evidence-based guideline exists for the treatment of late seroma. In 2011, the Breast Implant Working Group devised a comprehensive diagnostic and therapeutic algorithm for breast surgeons through the review of 12 late seroma cases [12]. In the first step of the algorithm, infection should be ruled out, and aspiration of fluid, culture, and cell counts are recommended when possible. Empirical broad-spectrum antibiotics are an option if clinical suspicion of infection is high. The second step involves imaging studies including ultrasound, which is recommended, or MRI, which is optional. The ultrasound should examine the periprosthetic fluid drainage and assist with procedures to obtain fluid for culture or cytology for differential diagnosis. The MRI can be used to aid in differential diagnosis of periprosthetic fluid collection versus generalized breast swelling or in the detection of combined implant rupture. When palpable or radiologic evidence of a mass is encountered, standard oncologic evaluation should be performed. Surgical exploration is recommended if the diagnosis is ambiguous or if the seroma is refractory with no evidence of neoplasia. Of 60 late seroma cases, 11 (18 %) were managed nonsurgically without recurrence, highlighting the fact that surgeons should consider conservative management first, including medication or ultrasound-guided aspiration. Surgical procedures are recommended to resolve recurrent periprosthetic fluid collection with negative cultures that do not respond to antibiotics. For surgical exploration, the Breast Implant Working Group recommended, by consensus, total capsulectomy with or without replacement of a new implant if technically possible without damage to surrounding tissues. The capsule should be examined for any abnormality, and additional histologic examination is recommended. In clinical cases, capsulectomy was performed in 37 of the 49 surgical cases of late seroma, with a sequential procedure involving capsulectomy, seroma drainage, and implant change most frequently applied. After a thorough literature review, we can propose the following more simplified guidelines for late seroma management. In the first stage, infection should be excluded for all patients with sudden-onset breast swelling. If signs of infection are observed, surgeons should treat the patient with antibiotics or antiviral agents. If this management is not effective, ultrasound-guided aspiration should be performed for diagnosis and treatment. The obtained fluid should be examined for culture, cytology, and/or cell count to rule out malignancy. Also, MRI is recommended in this step for confirmation of the diagnosis and for investigation of combined abnormality such as implant rupture.
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If symptoms recur or do not improve after the radiologic step (ultrasound-guided aspiration), surgery should be considered. In this step, seroma drainage and capsulectomy (when possible without damage to the breast tissue) may be essential, and implant removal or change should be performed. Also, cytology and culture should be repeated to confirm the diagnosis. One surprising feature of the reviewed cases was the almost complete success with implant exchange, whether the implants were replaced with a new Biocell textured implant or a smooth implant. However, at this writing, the follow-up period has not been sufficiently long for a clinical determination regarding their appropriateness. It seems reasonable to pursue conservative treatment first because surgical treatment is not required in all cases. In every case, the patient should be treated after the aforementioned sequential steps, and culture and cytology are required to rule out infection and malignancy. We concur with the opinions of the Breast Implant Working Group that nontreatment, random biopsy, closing of the surgical incision, and repetition of ultrasound-guided aspiration of reaccumulated fluid are not recommended [12]. Furthermore, a study investigating the association between a particular type of textured implant and the development of late seroma should be undertaken to evaluate etiologic factors.
Conclusion Late seroma is an infrequently reported complication of breast implant surgery. The etiology is not clearly understood, but most cases have occurred with use of the Biocell textured implant. Suspicion regarding this association is increasing, but further evaluations are needed. Guidelines regarding the management of late seroma have not been confirmed, and it has been treated with various methods. However, sequential simplified treatment steps would be helpful for successful management of late seroma. Nevertheless, during any type of treatment strategy, cytology and culture are essential for the differential diagnosis of ALCL.
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4.
5. 6.
7. 8.
9. 10.
11.
12.
13.
14. 15. 16.
17.
18.
19. 20.
References 1. Kulmala I, McLaughlin JK, Pakkanen M, Lassila K, Holmich LR, Lipworth L, Boice JD Jr, Raitanen J, Luoto R (2004) Local complications after cosmetic breast implant surgery in Finland. Ann Plast Surg 53:413–419 2. Chourmouzi D, Vryzas T, Drevelegas A (2009) New spontaneous breast seroma 5 years after augmentation: a case report. Cases J 2:7126 3. Kjoller K, Holmich LR, Jacobsen PH, Friis S, Fryzek J, McLaughlin JK, Lipworth L, Henriksen TF, Jorgensen S,
21.
22.
23.
Bittmann S, Olsen JH (2002) Epidemiological investigation of local complications after cosmetic breast implant surgery in Denmark. Ann Plast Surg 48:229–237 Nahabedian MY, Patel K (2009) Management of common and uncommon problems after primary breast augmentation. Clin Plast Surg 36(vii):127–138 Pinchuk V, Tymofii O (2011) Seroma as a late complication after breast augmentation. Aesthetic Plast Surg 35:303–314 Kim B, Roth C, Young VL, Chung KC, van Busum K, Schnyer C, Mattke S (2011) Anaplastic large cell lymphoma and breast implants: results from a structured expert consultation process. Plast Reconstr Surg 128:629–639 Cormack G (1991) Breast hypoplasia. Br J Plast Surg 44:628 Pinchuk V, Tymofii O, Tkach O, Zamkoboy V (2013) Implant ruptures after augmentation mammoplasty. Aesthetic Plast Surg 37:60–67 Wuest WL (1992) Breast implant seroma in pregnancy. Br J Plast Surg 45:328 Oliveira VM, Roveda Junior D, Lucas FB, Lucarelli AP, Martins MM, Rinaldi JF, Aoki T (2007) Late seroma after breast augmentation with silicone prostheses: A case report. Breast J 13:421–423 Fodor L, Moscona R (2009) Late posttraumatic intracapsular seroma after breast augmentation. J Plast Reconstr Aesthet Surg 62:e609–e610 Bengtson B, Brody GS, Brown MH, Glicksman C, Hammond D, Kaplan H, Maxwell GP, Oefelein MG, Reisman NR, Spear SL, Jewell ML (2011) Managing late periprosthetic fluid collections (seroma) in patients with breast implants: a consensus panel recommendation and review of the literature. Plast Reconstr Surg 128:1–7 Farina JA Jr, Ramalli EL, Da Silva MF, Silva R (2011) Jogging as a possible cause of late seroma after aesthetic breast augmentation with textured silicone prosthesis: A conservative approach. J Plast Reconstr Aesthet Surg 64:e216–e217 Robinson HN (2011) Breast implant complication review: Double capsules and late seromas. Plast Reconstr Surg 128:818–819 Tansley PD, Powell BW (2011) Late swelling after bilateral breast augmentation. J Plast Reconstr Aesthet Surg 64:261–263 Mazzocchi M, Dessy LA, Corrias F, Scuderi N (2012) A clinical study of late seroma in breast implantation surgery. Aesthetic Plast Surg 36:97–104 Roth FS, Gould DJ, Chike-Obi CJ, Bullocks JM (2012) Late seroma during pregnancy, a rare complication in prosthetic breast augmentation: case report. J Plast Reconstr Aesthet Surg 65:973–976 Spear SL, Rottman SJ, Glicksman C, Brown M, Al-Attar A (2012) Late seromas after breast implants: theory and practice. Plast Reconstr Surg 130:423–435 Hall-Findlay EJ (2011) Breast implant complication review: double capsules and late seromas. Plast Reconstr Surg 127:56–66 Ahn CY, Ko CY, Wagar EA, Wong RS, Shaw WW (1995) Clinical significance of intracapsular fluid in patients’ breast implants. Ann Plast Surg 35:455–457 Flassbeck D, Pfleiderer B, Klemens P, Heumann KG, Eltze E, Hirner AV (2003) Determination of siloxanes, silicon, and platinum in tissues of women with silicone gel-filled implants. Anal Bioanal Chem 375:356–362 Roman S, Perkins D (2005) Progressive spontaneous unilateral enlargement of the breast twenty-two years after prosthetic breast augmentation. Br J Plast Surg 58:88–91 Cheng NX, Chen B, Li Q, Wu DH, Zhu L, Zhang XM, Chen YL (2011) Late haematoma and seroma in patients with silicone mammary prosthesis: our reports and literature review. J Plast Recontr Aesthet Surg 64:e185–e186
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