Systematic review

Applicability and safety of autologous fat for reconstruction of the breast

F. Claro Jr1,2 , J. C. A. Figueiredo2 , A. G. Zampar2 and A. M. Pinto-Neto1
1 Department of Gynaecology and Obstetrics, School of Medical Sciences, State University of Campinas, Campinas, and 2 Santa Cruz Plastic Surgery Institute, S o Paulo, Brazil a Correspondence to: Dr F. Claro Jr, Departamento de Ginecologia e Obstetrcia da Faculdade de Ci ncias M dicas da UNICAMP, R. Alexander Fleming, e e 101, 13083-881 Campinas, SP, Brazil (e-mail: fclarojr@gmail.com)

Background: Autologous fat grafting to the breast for cosmetic and reconstructive purposes is still

controversial with respect to its safety and efcacy. The objective of this study was to conduct a systematic review of the clinical applicability and safety of the technique. Methods: An online search of the Cochrane Library, MEDLINE, Embase and SciELO was conducted from July 1986 to June 2011. Studies included in the review were original articles of autologous liposuctioned fat grafting to the female breast, with description of clinical complications and/or radiographic changes and/or local breast cancer recurrence. Results: This review included 60 articles with 4601 patients. Thirty studies used fat grafting for augmentation and 41 for reconstructive procedures. The incidence of clinical complications, identied in 21 studies, was 39 per cent (117 of 3015); the majority were induration and/or palpable nodularity. Radiographic abnormalities occurred in 332 (130 per cent) of 2560 women (17 studies); more than half were consistent with cysts. Local recurrence of breast cancer (14 of 616, 23 per cent) was evaluated in three studies, of which only one was prospective. Conclusion: There is broad clinical applicability of autologous fat grafting for breast reconstruction. Complications were few and there was no evidence of interference with follow-up after treatment for breast cancer. Oncological safety remains unclear.
Paper accepted 2 February 2012 Published online 4 April 2012 in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.8722

Introduction

The transfer of autologous fat for surgical reconstruction dates back to 1893, when Neuber described implanting a small piece of upper arm fat tissue to correct a scar depression in the face1,2 . Since then, fat tissue has been employed for the correction of multiple body deformities3,4 and was reported to be the source of the rst breast reconstruction. In 1895, Czerny used a large lipoma from the dorsal ank for breast reconstruction after excision of a benign lesion5,6 . With the advent of liposuction in the 1970s, aspirated fat could be reinjected without any preparation by plastic surgeons7,8 . Fat grafting has become widely used in gynaecological, urological, neurological, orthopaedic, ear, nose and throat, trauma and thoracic surgery. It is efcient in correcting deformities in virtually all body areas and is widely used in cosmetic procedures3,4,9,10 . Unlike other
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body areas, aesthetic and reconstructive results in the breast remained unsatisfactory, together with the appearance of many complications11,12 . Furthermore, it was suggested that adipocytes might stimulate the formation of breast cancer or induce radiographic changes if used after breast cancer surgery. This could compromise the detection of recurrence or new malignant lesions. In 1987, the American Society of Plastic Surgeons prohibited the use of autologous fat grafting to the female breast13 . Subsequently, Coleman14,15 formulated new concepts, standardizing the technique of structural fat grafting. This then became the therapeutic method used in various surgical specialties for cosmetic and reconstructive purposes. In breast reconstruction, unlike elsewhere in the body, adipocytes are implanted in a poorly vascularized and loose space. Therefore, the fat needs greater contact with the host
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tissue to ensure adequate nutrition and immobilization for adipocyte survival in the rst few days, as the adipocytes become incorporated. These anatomical characteristics in the breast explain the poor results and the high rate of complications. The concept of structural fat grafting is that the fat must be inserted in small amounts using multiple tunnels, in many layers and directions, so that the largest possible number of adipocytes are in contact with host tissue and thus receive adequate nutrition for their survival (Fig. 1)14 . Thin cannulas (123 mm) and syringes of low volume (120 ml) allow greater accuracy, avoiding bolus injections (Fig. 2). Several authors used this method10,16 19 before it was formally described by Coleman. Any necrotic tissue that is not completely absorbed causes an inammatory reaction, resulting in brosis and/or cystic formation, with or without calcication, and also local infection20 23 . A number of studies using structural fat grafting to the breast have been published, with good results16,17,24 . This led to renewed interest in the procedure; however, fat grafting still raises doubts with respect to indication and safety in clinical practice. In 2009, the American Society of Plastic Surgeons did not prohibit the procedure (owing to lack of evidence), although they did not recommend it25 . The aim of this study was to identify the indications and safety of the procedure, by means of a systematic review of clinical complications, radiographic changes and incidence of breast cancer (primary or recurrent) in women treated with fat grafting to the breast.

Fig. 2

Thin cannulas (123 mm) and low-volume syringes (120 ml) allow greater accuracy of the amount grafted per tunnel, avoiding bolus injection. After preparation of the liposuctioned material (in the three syringes in the vertical position), the lower and uppermost levels are discharged. The middle layer contains the viable adipocytes

Methods

Search strategy
A systematic review of autologous fat grafting to the female breast was conducted according to the guidelines in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement26 . The search for articles published in the past 25 years (from July 1986 to June 2011) was carried out independently by two reviewers after accessing the electronic databases of the Cochrane Library, US National Library of Medicine (MEDLINE), Embase and Scientic Electronic Library Online (SciELO). Appropriate keywords in the English language were combined by Boolean logical operators, as follows: fat autografting OR fat grafting OR fat autograft OR fat graft OR fat transplantation OR fat injection OR autologous fat OR lipostructuring OR lipotransfer OR lipomodelling OR lipomodeling AND breast, adapted to the appropriate syntax of each database. Studies that were considered potentially relevant based on titles were cross-referenced in a search for additional articles of potential interest, with no restriction on language, type of study or publication media.

Fig. 1

Structural fat grafting. The fat is grafted in small amounts via multiple tunnels in many layers, avoiding the gland tissue, as illustrated on the left breast with directions shown on the right breast. Thus the largest possible number of adipocytes are in contact with the host tissue and receive adequate nutrition for survival

Inclusion criteria
Original articles concerning autologous fat grafting to the human female breast, with fat recently removed
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by liposuction, were eligible for inclusion in this review. Only articles that mentioned results such as clinical complications and/or radiographic changes and/or incidence of breast cancer in patients treated with the previously described technique were included.

Assessment of study quality

The methodological quality of the studies was assessed by two independent reviewers; level of evidence and grade of recommendation were scored according to the criteria of the Oxford Centre for Evidence-based Medicine28 , and Grading of Recommendation Assessment, Development and Evaluation (GRADE)29 . Observational studies and clinical trials lacking a detailed description of the randomization procedure were considered to have a high potential for bias30 32 .

Exclusion criteria
Duplicate articles were excluded. Studies using recently aspirated mature adipocytes in a proportion lower than 50 per cent, characterizing stem cell implants, and those that did not contain a description of the indication for the procedure were not considered eligible for this review. Articles without original data, such as reviews or technical descriptions, were also ineligible.

Statistical analysis
Outcomes of interest were tabulated, and shown in descriptive and individual form, considering the methodological quality of each study. The prevalence of clinical complications and radiological changes was identied. Meta-analysis was not done because of the heterogeneous methodology among studies30 32 .
Results

Study selection
Abstracts of studies initially selected were evaluated by all four reviewers independently to determine eligibility. In this case the full text of articles was retrieved for evaluation, data extraction and inclusion in the systematic review. When a selected study was not available in the electronic media or local libraries, the authors were contacted to request a copy27 .

Extraction of data
Data extracted from articles included: authors, date of publication, number of subjects, indication for the procedure, type of study, technique used for adipocyte implantation, follow-up time, efcacy of treatment, clinical complications, radiographic changes, and incidence of primary and recurrent breast cancer. They were extracted independently and tabulated by two reviewers; discrepancies were discussed and reviewed by all four reviewers until agreement was reached. In clinical trial articles and observational cohort studies, casecontrol and case series with more than 20 patients, the outcomes of interest previously dened were: indication, efcacy, clinical complications, radiological changes and breast cancer. Although efcacy was described in a subjective and widely heterogeneous way among the studies, it was presented according to the original authors assessment. Case reports and case series with up to 20 patients were used only as an additional source for the summation analysis of types of complication and radiographic changes, but were excluded from the assessment of their rates because of the likelihood of bias.
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A database search for the prespecied keywords identied 302 articles (171 in Embase, 131 in MEDLINE and none in the Cochrane Library or SciELO). After exclusion of duplicate articles and manual cross-referencing, two new articles were included33,34 , giving a total of 95. Of these, 23 articles were excluded after reading the abstracts and 72 were eligible for full-text reading. Among these, one was excluded for using fat block transplantation instead of liposuction35 , two for using more than 50 per cent immature adipocytes, which characterizes stem cell transplantation36,37 , two for failing to record the outcomes of interest38,39 and seven that were apparently repeat case studies40 46 . Sixty articles (4601 women) remained and were used in this systematic review6,11,12,16 19,24,27,33,34,47 95 . Only 27 articles were assessed for incidence of clinical complications and/or radiological ndings and/or breast cancer (Fig. 3). Of these, 21 studies that included 3015 women were used to extract the incidence of clinical complications, 17 studies with 2560 women to calculate the incidence of radiographic changes, and three studies with 616 women to evaluate oncological risk. There were 58 observational studies: 37 case reports and case series, seven retrospective cohort studies, 12 prospective cohort studies, one diagnostic validation cohort study and one casecontrol study. Two studies were clinical trials without a description of the randomization. The methodology and quality of each study are shown in Table 1.
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Records identified by database searching n = 302 Embase = 171 MEDLINE = 131 SciELO = 0 The Cochrane Library = 0 Studies of potential interest identified by crossreferencing n = 2 Records after duplicates removed n = 167

Records screened for more detailed evaluation after reading title n = 95 Records excluded after reading abstract as failed inclusion/exclusion criteria n = 23 Full-text articles assessed for eligibility n = 72

Articles excluded after reading full text n = 12 Fat block transplantation n = 1 Duplicate database n = 7 No numerical data on outcomes n = 2 Used more than 50% immature adipocytes n = 2

Studies included in the systematic review n = 60 Article assessed for incidence of clinical complications, radiological findings and breast cancer n = 27
Fig. 3

Selection of articles for review

Clinical applicability
Thirty of the studies, with at least 930 patients, used fat grafting to the breast for aesthetic augmentation; 41 studies with more than 3646 patients described the procedure for breast reconstruction. The majority of these articles were considered to be of low or very low quality according to the GRADE criteria. In general, the procedure was reported as being satisfactory (Table 1). Clinical indications for autologous fat grafting according to the GRADE criteria for methodological quality are illustrated in Fig. 4. In the aesthetic eld, the main indication for the procedure was primary breast augmentation (30 studies including about 1000 women), followed by secondary augmentation after removal of an alloplastic implant, or to improve the contour of the breasts after placement of the implant. All studies investigating these indications were observational. Most consisted of case reports and case series, of low or very low quality. In the reconstructive eld, the procedure was used mainly for partial breast reconstruction and/or correction of breast deformities. This was the second most frequent indication
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(15 studies, more than 365 women), followed by total breast reconstruction. In more recent studies (starting in 2009), autologous fat grafting was reported as therapy for postradiotherapy radiodermatitis67,84 and as treatment for capsular contracture in breasts with alloplastic implants80 (Fig. 4).

Safety Clinical complications Initially, all 60 studies were evaluated for clinical complications, which were identied in 155 of 4601 patients. Nodularity and/or induration was identied in 93 patients (600 per cent), followed by deep infection in 19 (123 per cent). There was no recorded death. Three cases of sepsis were identied in case reports of complications when structured fat grafting was not used (Fig. 5). In one of these, the patient received fat grafting to the breasts and buttocks. She developed abscesses in one breast and in one gluteal region, requiring open drainage for both regions33 . Considering the 21 studies with better methodological quality, which described xed follow-up, a standard
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Table 1

Characteristics of included studies

No. of patients (breasts)

Reference Bircoll18 Bircoll and Novack19 Horl et al.11 Maillard12 Uchiyama et al.47 Cheung et al.48 Valdatta et al.49 Gulsun et al.50 Kwak et al.51 Spear et al.24 Pierrefeu-Lagrange et al.52 Pulagam et al.53 Coleman and Saboeiro6 Missana et al.54 Yoshimura et al.55 Cotrufo et al.56 Gosset et al.57 Pinsolle et al.58 Mojallal et al.27 Zheng et al.59 Zocchi and Zuliani60 Carvajal and Patino61 Wang et al.62 Kaufman et al.63 ElFadl et al.64 Delaporte et al.65 Hyakusoku et al.66 Panettiere et al.67 Kanchwala et al.68 Del Vecchio69 Mu et al.70 Lazaretti et al.71 Delay et al.17 Illouz and Sterodimas16 Salgarello et al.72 Pereira and Sterodimas73 Babovic74 Rigotti et al.75 Serra-Renom et al.76 Erol et al.77 Talbot et al.33 Wang et al.78 Villani et al.79 Ueberreiter et al.80 Veber et al.81 Del Vecchio and Bucky82 Pettus et al.34 Rietjens et al.83 Panettiere et al.84 Serra-Renom et al.85 Serra-Renom et al.86 Lee et al.87 Sarfati et al.88 Losken et al.89 Yang and Lee90 Young and Zellner91 Murphy et al.92

Year 1987 1987 1989 1994 2000 2000 2001 2003 2004 2005 2006 2006 2007 2007 2008 2008 2008 2008 2008 2008 2008 2008 2008 2009 2009 2009 2009 2009 2009 2009 2009 2009 2009 2009 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2011 2011 2011 2011 2011 2011 2011 2011 2011 2011 2011 2011 2011

Study design Case report Case report Case report Case report Case report Case report Case report Case report Case report Retrospective cohort Case series Case report Retrospective cohort Retrospective cohort Retrospective cohort Case series Case series Case series Case report Case series Retrospective cohort Case series Case series Prospective cohort Prospective cohort Prospective cohort Case series Clinical trial Retrospective cohort Case report Case series Case report Case series Case series Case report Case report Case report Clinical trial Case series Case report Case report Prospective cohort Case series Prospective cohort Diagnostic validation cohort Prospective cohort Case report Prospective cohort Case report Prospective cohort Prospective cohort Case report Prospective cohort Case series Case report Case series Prospective cohort

GRADE* Very low Very low Very low Very low Very low Very low Very low Very low Very low Low Low Very low Low Low Low Low Low Low Very low Low Low Low Low Low Low Low Low Moderate Low Very low Very low Very low Low Low Very low Very low Very low Moderate Low Very low Very low Low Low Low Moderate Low Very low Low Very low Low Low Very low Low Low Very low Low Low

Cosmetic augmentation 1 (2) 1 (2) 1 (2) 3 (6) 1 (2) 1 (2) 1 (2) 1 (2) 1 (2) 10 (20) 40 (80) 47 181 (326) 20 (40) 33 (66) 1 12 (24) 1 (2) 17 (34) 1 (2) 30 385 (770) 1 (2) 1 (2) 41 (82) 52 (104) 44 NS 1 (2) 1 (2)

Reconstruction 1 (1) 43 30 (34) 1 (1) 7 (11) 74 42 21 7 1 19 9 (9) 21 15 (15) 22 (22) 110 850 435 (478) 2 (2) 1 (2) 1 (1) 911 65 (65) 1 (1) 5 (5) 33 32 NS 1 (2) 157 (192) 1 (2) 28 (56) 8 (9) 28 107 1 (1) 100 (130) 100

Efcacy Satisfactory Satisfactory RCC RCC RAR RAR RCC RAR RAR Satisfactory Satisfactory RAR Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory RAR RAR Satisfactory Satisfactory Satisfactory RCC Satisfactory Satisfactory Satisfactory RCC RCC Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory RCC RCC RAR Satisfactory Satisfactory Satisfactory Satisfactory RAR Satisfactory Satisfactory Satisfactory Satisfactory RCC Satisfactory Satisfactory Satisfactory Satisfactory Satisfactory

(Continued overleaf)

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Table 1

(Continued)
No. of patients (breasts)

Reference Beck et al.94 Irani et al.95 Petit et al.93 Overall

Year 2012 2012 2012

Study design Prospective cohort Retrospective cohort Casecontrol

GRADE* Low Low Moderate

Cosmetic augmentation 930 + NS

Reconstruction 10 25 (25) 321 3646 + NS

Efcacy Satisfactory Satisfactory NR

*Methodological quality according to Grading of Recommendation Assessment, Development and Evaluation (GRADE) classication29 . RCC, report of clinical complication; RAR, report of radiological alteration; NS, number of patients not specied; NR, not reported.
Aesthetic augmentation Partial breast reconstruction or correction of deformities Total breast reconstruction associated with myocutaneous flaps Total breast reconstruction associated with breast implant Poland's syndrome or congenital deformity Total breast reconstruction associated with myocutaneous flaps and breast implant Total breast reconstruction with fat grafting alone Total breast reconstruction before implantation of breast prosthesis or myocutaneous flaps Augmentation after removal of breast implant Tuberous breast Cosmetic improvement after breast implant Treatment of radiological sequelae Treatment of capsular contracture 0 (27) (21) (15) 5 10 15 20 No. of studies 25 30 (365 + NS) (524 + NS) (325 + NS) (59 + NS) (74 + NS) (26 + NS) (133) (273 + NS) (46 + NS) Methodology quality according to GRADE Very low quality Low quality Moderate quality High quality (928 + NS)

Fig. 4

Indications for autologous fat grafting to the breast in relation to methodological quality of studies assessed according to the Grading of Recommendation Assessment, Development and Evaluation criteria. Numbers of patients are shown in parentheses. NS, number of patients not specied
Palpable induration/nodule Deep infection Dysaesthesia Haematoma Superficial infection Pain Sepsis Abnormal breast secretion Pneumothorax 0 (19) (19) (06) (06) 10 20 30 40 50 60 No. of complications 70 80 90 (123) (90) (77) (58) Structured fat grafting Non-structured fat grafting (600)

Fig. 5

Distribution of 155 complications described in 60 studies according to fat grafting technique. Values in parentheses are percentages
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Table 2

Incidence of clinical complications after fat grafting in studies with better methodological quality
Year 2005 2007 2008 2008 2008 2008 2008 2009 2009 2009 2009 2010 2010 2011 2011 2011 2011 2011 2011 2011 2012 No. of patients 37 69 40 42 66 181 33 22 110 880 820 65 85 25 158 28 22 107 100 100 25 3015 Technique Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Non-structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Mean follow-up (months) 15 12 6 7 37 12 3 5 21 12 12 12 6 6 183 12 17 8 8 NR 6 1235 Clinical complications 3 of 37 0 of 69 0 of 40 1 of 42 1 of 66 19 of 181 14 of 33 2 of 22 0 of 110 35 of 880 17 of 820 0 of 65 2 of 85 0 of 25 7 of 158 0 of 28 0 of 22 12 of 107 2 of 100 0 of 100 2 of 25 117 of 3015 (39)

Reference Spear et al.24 Missana et al.54 Yoshimura et al.55 Cotrufo et al.56 Zheng et al.59 Zocchi and Zuliani60 Wang et al.62 ElFadl et al.64 Kanchwala et al.68 Delay et al.17 Illouz and Sterodimas16 Serra-Renom et al.76 Ueberreiter et al.80 Del Vecchio and Bucky82 Rietjens et al.83 Serra-Renom et al.85 Sarfati et al.88 Losken et al.89 Young and Zellner91 Murphy et al.92 Irani et al.95 Overall

Values in parentheses are percentages.

Cyst Microcalcification Benign-type calcifications Increased density Mass with or without calcification Cyst (anechoic area) Cyst and solid mass Solid mass (hypoechoic or isoechoic area) Cyst and liponecrotic cyst Sclerotic nodule

746 134 54 47 20 Mammography Ultrasound imaging Magnetic resonance imaging 894 60 45 652 348 15 30 45 60 75 90 % of abnormalities

Fig. 6

Prevalence of radiological changes identied in 60 studies among 299 abnormal ndings described on mammography, 331 on ultrasound imaging and 46 on magnetic resonance imaging

technique and more than 20 patients, the incidence of clinical complications was 39 per cent (117 of 3015) (Table 2). Among these, the most serious complication reported was pneumothorax (Fig. 5).

Radiographic changes A total of 299 abnormal radiological ndings were identied on mammography during follow-up; 746 per cent were consistent with cysts and 134 per cent with microcalcication. On ultrasound imaging, 894 per cent of the 331 radiographic changes were consistent with cyst and/or liponecrotic cysts. Magnetic resonance imaging
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also showed images consistent with cystic change in 652 per cent of the 46 ndings identied, and nodulation in 348 per cent (Fig. 6). The overall rate of abnormal radiological ndings during follow-up was 130 per cent (332 of 2560 patients), taken from the studies with better methodology (Table 3).

Breast cancer risk Three studies that evaluated 616 patients (mean follow-up 452 months) were used to identify the oncological risk in women with breast cancer treated with fat grafting. Fourteen recurrent cancers were described (23 per cent)75,83,93 .
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Table 3

Incidence of radiographic changes

Year 2006 2007 2008 2008 2008 2008 2008 2009 2009 2009 2010 2010 2011 2011 2011 2011 2011 No. of patients 30 69 40 21 66 181 33 22 880 820 41 85 31 25 79 107 30 2560 Technique Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Non-structured fat graft Structured fat graft Structured fat graft Structured fat graft Non-structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Structured fat graft Mean followup (months) 12 12 6 12 37 12 3 5 12 12 16 6 12 6 183 8 NR 123 Radiological changes 12 of 30 5 of 69 2 of 40 18 of 21 11 of 66 7 of 181 14 of 33 2 of 22 176 of 880 17 of 820 34 of 41 0 of 85 20 of 31 0 of 25 4 of 79 1 of 107 9 of 30 332 of 2560 (130)

Reference Pierrefeu-Lagrange et al.52 Missana et al.54 Yoshimura et al.55 Gosset et al.57 Zheng et al.59 Zocchi and Zuliani60 Wang et al.62 ElFadl et al.64 Delay et al.17 Illouz and Sterodimas16 Wang et al.78 Ueberreiter et al.80 Veber et al.81 Del Vecchio and Bucky82 Rietjens et al.83 Losken et al.89 Murphy et al.92 Overall

Values in parentheses are percentages.

In all these women the initial treatment was mastectomy for breast cancer. No report described a new primary breast cancer.
Discussion

This systematic review was performed with information from different studies using a wide range of methods. The majority had a low grade of recommendation, with a high likelihood of bias30 32 . Despite these difculties and some limitations, after organization and assessment of the results it was possible to demonstrate the relative safety of autologous fat grafting to the female breast with fat removed by recent liposuction for the aesthetic and reconstructive treatment of diverse breast disorders. Although some studies recorded the site of fat harvest and its method of preparation, previous studies have not reported any effect on the outcomes96 100 so these technical aspects were not studied here. Fat is usually harvested from the abdomen, hip and inner thigh. Most authors centrifuge the liposuctioned material at 3000 r.p.m. for 3 min, as this gives a higher adipocyte concentration, allowing greater predictability of outcome. The technique is carried out mainly for aesthetic breast augmentation (30 of 60 articles used in this review). Most articles were observational and there were not enough data to provide an accurate assessment of efcacy. This will be assessed in ongoing prospective studies. In the eld of breast reconstruction, the articles were also observational and descriptive; however, it was possible to conclude that fat grafting may be used for total and
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partial reconstruction, and usually requires more than one application session. It may also be used in combination with myocutaneous aps, such as the transverse rectus abdominis myocutaneous ap, latissimus dorsi muscle ap or even free microsurgical aps, to improve breast shape and volume. In addition, fat grafting may be used with alloplastic implants, to prepare the recipient site in women with thin subcutaneous tissue or previously irradiated skin67 . Other improvements in irradiated skin include ulcer healing and regeneration of brotic areas of the breast36,67,84 . Finally autologous fat grafting has been used successfully to correct congenital deformities such as Polands syndrome6,16,27,58,81,82,83,90 and tuberous breast6,81,85 . In this review, the authors found 155 reported complications among 4601 women treated with breast fat grafting in the 60 studies identied. Most of the reported complications (600 per cent) were breast mass and/or induration, disorders of low morbidity and commonly reported after breast surgery. Fat grafting uses the patients own tissue, so an immune response is not elicited. Three cases of severe sepsis were identied33,49,87 ; however, the authors did not describe the technique used, and some problems may have occurred because bolus liposuction was employed rather than structural fat grafting. In this review, the rate (39 per cent within 12 months in higher-quality publications) and severity of clinical complications after autologous fat grafting were lower than those described after breast cosmetic and reconstruction procedures performed with breast implants and/or myocutaneous aps101 113 . Some specialists still believe that the
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palpable nodularity responsible for most clinical complications could interfere with future breast cancer screening, in addition to causing anxiety among patients. Similarly, in the 17 articles (2560 patients) used to assess the risk of abnormal radiographic changes, the rate was 130 per cent after a mean of 12 months, similar to that following other breast surgical procedures52,57 . Veber et al.81 compared mammograms obtained before and after autologous fat grafting to the breast, and observed an improvement in radiological pattern 1 year after the procedure. They concluded that fat grafting did not cause additional difculties in differentiating a suspected radiological change. Concerning the potential risk of breast cancer, experimental studies in the scientic environment have reported that recently grafted adipocytes and preadipocytes (representing around 10 per cent of fat cells in the lipoaspirate) have carcinogenic potential108 112 . The risk is based on a higher local concentration of oestrogen resulting from aromatases derived from adipocytes, and some adipocytokines released from these cells that can stimulate angiogenesis and induce cancer113,114 . The theory was refuted in a recent systematic review of experimental studies on the subject by Lohsiriwat and co-workers113 . Of all the studies included in this review, only three were designed to assess oncological risk. A prospective cohort study by Rietjens and colleagues83 with followup of 18 months analysed 155 patients treated for breast cancer (191 breasts; 114 total mastectomies, 77 partial mastectomies) and found only one recurrence, which was diagnosed shortly after the fat grafting procedure, and considered not relevant. Similarly, Rigotti and co-workers75 compared tumour recurrence in a nonrandomized study of patients treated for breast cancer with modied radical mastectomy and autologous fat grafting for breast reconstruction. Although ve of the 137 patients developed recurrence, the authors concluded that there was no higher oncological risk in patients treated with lipolling than in the control group. Finally, Petit et al.93 conducted a casecontrol study, in which 321 women treated by fat grafting were matched and compared with 642 women who received similar oncological treatment during a mean of 26 months. There were eight local recurrences in the lipolling group compared with 19 in controls, suggesting that fat grafting was not contributory. In this review the rate of breast cancer recurrence in women who had fat grafting to the breast was similar to published rates for patients undergoing mastectomy who did not receive fat grafting115 119 . At present there is no evidence that fat grafting increases the risk of breast
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cancer25,75,83,93 , but conrmation of oncological safety awaits the results of controlled trials.
Acknowledgements

This research was funded by Coordena ao de c Aperfei oamento de Pessoal de Nvel Superior (CAPES), c the Brazilian federal institution for post graduation programmes. Disclosure: The authors declare no conict of interest.
References
1 Shiffman MA, Kaminski MV. Fat transfer to the face. In Simplied Facial Rejuvenation, Shiffman MA, Mirrafati SJ, Samuel ML (eds). Springer: Berlin, 2008; 202211. 2 Ersek RA, Chang P, Salisbury MA. Lipo layering of autologous fat: an improved technique with promising results. Plast Reconstr Surg 1998; 101: 820826. 3 Illouz YG. The fat cell graft: a new technique to ll depressions. Plast Reconstr Surg 1986; 78: 122123. 4 Ellenbogen R. Fat transplantation. Plast Reconstr Surg 1987; 79: 306. 5 Hinderer UT, del Rio J. Erich Lexers mammoplasty. Aesth Plast Surg 1992; 16: 101107. 6 Coleman SR, Saboeiro AP. Fat grafting to the breast revisited: safety and efcacy. Plast Reconstr Surg 2007; 119: 775785. 7 Illouz YG. Une novelle technique pour les lipodystrophies localisees. Rev Chir Esth Franc 1980; 6: 19. 8 Illouz YG. Body contouring by lipolysis: a 5-year experience with over 3000 cases. Plast Reconstr Surg 1983; 72: 591597. 9 Illouz YG. Present results of fat injection. Aesthetic Plast Surg 1988; 12: 175181. 10 Fornier PF. Microlipoextraction et microlipoinjection. Rev Chir Esthet Lang Franc 1985; 10: 3640. 11 Horl HW, Feller AM, Steinau HU, Biener E. [Autologous injection of fatty tissue following liposuction not a method for breast augmentation.] Handchir Mikrochir Plast Chir 1989; 21: 5961. 12 Maillard GF. Liponecrotic cysts after augmentation mammaplasty with fat injections. Aesthetic Plast Surg 1994; 18: 405406. 13 Report on autologous fat transplantation. ASPRS Ad-Hoc Committee on New Procedures. Plast Surg Nurs 1987; 7: 140141. 14 Coleman SR. Long-term survival of fat transplants: controlled demonstrations. Aesth Plast Surg 1995; 19: 421425. 15 Coleman SR. Structural Fat Grafting. Quality Medical Publishing: St Louis, 2004. 16 Illouz YG, Sterodimas A. Autologous fat transplantation to the breast: a personal technique with 25 years of experience. Aesth Plast Surg 2009; 33: 706715.

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17 Delay E, Garson S, Tousson G, Sinna R. Fat injection to the breast: technique, results, and indications based on 880 procedures over 10 years. Aesthet Surg J 2009; 29: 360376. 18 Bircoll M. Cosmetic breast augmentation utilizing autologous fat and liposuction techniques. Plast Reconstr Surg 1987; 79: 267271. 19 Bircoll M, Novack BH. Autologous fat transplantation employing liposuction techniques. Ann Plast Surg 1987; 18: 327329. 20 Carpaneda C, Ribeiro M. Study of the histological alterations and viability of the adipose graft in humans. Aesthetic Plast Surg 1993; 17: 4347. 21 Niechajev I, Sev uk O. Long-term results of fat c transplantation: clinical and histologic studies. Plast Reconstr Surg 1994; 94: 496506. 22 Segura S, Requena L. Anatomy and histology of normal subcutaneous fat, necrosis of adipocytes, and classication of the panniculitides. Dermatol Clin 2008; 26: 419424. 23 Nguyen A, Pasyk KA, Bouvier TN, Hasset CA, Argenta LC. Comparative study of survival of autologous adipose tissue taken and transplanted by different techniques. Plast Reconstr Surg 1990; 85: 379386. 24 Spear SL, Wilson HB, Lockwood MD. Fat injection to correct contour deformities in the reconstructed breast. Plast Reconstr Surg 2005; 116: 13001305. 25 Gutowski KA; ASPS Fat Graft Task Force. Current applications and safety of autologous fat grafts: a report of the ASPS fat graft task force. Plast Reconstr Surg 2009; 124: 272280. 26 Moher D, Liberati A, Tetzlaff J, Altman DG; The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Open Med 2009; 3: 123130. 27 Mojallal A, Shipkov C, Braye F. Breast reconstruction in Poland anomaly with endoscopically-assisted latissimus dorsi muscle ap and autologous fat tissue transfer: a case report and review of the literature. Folia Med (Plovdiv) 2008; 50: 6369. 28 Oxford Centre for Evidence-based Medicine Levels of Evidence (March 2009). http://www2.cch.org.tw/ebm/le/CEBMLevels-of-Evidence.pdf [accessed 1 April 2011]. 29 Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, Flottorp S et al.; GRADE Working Group. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 14901494. 30 Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions. The Cochrane Book Series. John Wiley & Sons: Chichester, 2008. 31 Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 1996; 17: 112. 32 Moher D, Pham B, Jones A, Cook DJ, Jadad AR, Moher M et al. Does quality of reports of randomised trials affect estimates of intervention efcacy reported in meta-analyses? Lancet 1998; 352: 609613.

33 Talbot SG, Parrett BM, Yaremchuk MJ. Sepsis after autologous fat grafting. Plast Reconstr Surg 2010; 126: 162e164e. 34 Pettus BJ, Brandt KE, Middleton WD, Reichert VC. Sonographic ndings in a palpable abnormality after mastectomy and autologous fat grafting. J Ultrasound Med 2011; 30: 576578. 35 Bar-Meir ED, Yueh JH, Tobias AM, Lee BT. Autologous fat grafting: a technique for stabilization of the microvascular pedicle in DIEP ap reconstruction. Microsurgery 2008; 28: 495498. 36 Rigotti G, Marchi A, Gali` M, Baroni G, Benati D, e Krampera M et al. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg 2007; 119: 14091422. 37 Calabrese C, Orzalesi L, Casella D, Cataliotti L. Breast reconstruction after nipple/areola-sparing mastectomy using cell-enhanced fat grafting. Ecancermedicalscience 2009; 3: 116. 38 Khouri R, Del Vecchio D. Breast reconstruction and augmentation using pre-expansion and autologous fat transplantation. Clin Plast Surg 2009; 36: 269280. 39 Gosset J, Flageul G, Toussoun G, Gu rin N, Tourasse C, e Delay E. [Lipomodelling for correction of breast conservative treatment sequelae. Medicolegal aspects. Expert opinion on ve problematic clinical cases.] Ann Chir Plast Esthet 2008; 53: 190198. 40 Delay E, Gosset J, Toussoun G, Delaporte T, Delbaere M. [Efcacy of lipomodelling for the management of sequelae of breast cancer conservative treatment.] Ann Chir Plast Esthet 2008; 53: 153168. 41 Delay E, Sinna R, Delaporte T, Flageul G, Tourasse C, Tousson G. Patient information before aesthetic lipomodeling (lipoaugmentation): a French plastic surgeons perspective. Aesthet Surg J 2009; 29: 386395. 42 Delay E, Sinna R, Chekaroua K, Delaporte T, Garson S, Toussoun G. Lipomodeling of Polands syndrome: a new treatment of the thoracic deformity. Aesth Plast Surg 2010; 34: 218225. 43 Sinna R, Delay E, Garson S, Delaporte T, Toussoun G. Breast fat grafting (lipomodelling) after extended latissimus dorsi ap breast reconstruction: a preliminary report of 200 consecutive cases. J Plast Reconstr Aesthet Surg 2010; 63: 17691777. 44 Herold C, Ueberreiter K, Cromme F, Busche MN, Vogt PM. [The use of mamma MRI volumetry to evaluate the rate of fat survival after autologous lipotransfer.] Handchir Mikrochir Plast Chir 2010; 42: 129134. 45 Brenelli F, Rietjens M, De Lorenzi F, Rossetto F. Autologous fat graft after breast cancer: Is it safe? A single surgeon experience with 194 procedures. Eur J Plast Surg 2010; 8(Suppl): 141142. 46 Herold C, Ueberreiter K, Cromme F, Grimme M, Vogt PM. [Is there a need for intrapectoral injection in autologous fat transplantation to the breast? An MRI

2012 British Journal of Surgery Society Ltd Published by John Wiley & Sons Ltd

www.bjs.co.uk

British Journal of Surgery 2012; 99: 768780

778

F. Claro Jr, J. C. A. Figueiredo, A. G. Zampar and A. M. Pinto-Neto

47

48

49

50

51

52

53

54

55

56

57

58

59

60 61

volumetric study.] Handchir Mikrochir Plast Chir 2011; 43: 119124. Uchiyama N, Kumazaki T, Miyagawa K, Matsue H, Moriyama N. Radiographic ndings of the breast after augmentation by fat injection. Jpn J Clin Radiol 2000; 45: 687691. Cheung M, Houssami N, Lim E. The unusual mammographic appearance of breasts augmented by autologous fat injection. Breast 2000; 9: 220222. Valdatta L, Thione A, Buoro M, Tuinder S. A case of life-threatening sepsis after breast augmentation by fat injection. Aesthetic Plast Surg 2001; 25: 347349. Gulsun M, Basaran C, Basugun N, Demirkazk FB, Ariyurek M. Giant liponecrotic cyst secondary to augmentation with autologous fat injection. Eur J Radiol 2003; 45: 6466. Kwak JY, Lee SH, Park HL, Kim JY, Kim SE, Kim EK. Sonographic ndings in complications of cosmetic breast augmentation with autologous fat obtained by liposuction. J Clin Ultrasound 2004; 32: 299301. Pierrefeu-Lagrange AC, Delay E, Guerin N, Chekaroua K, Delaporte T. [Radiological evaluation of breasts reconstructed with lipomodeling.] Ann Chir Plast Esthet 2006; 51: 1828. Pulagam SR, Poulton T, Mamounas EP. Long-term clinical and radiologic results with autologous fat transplantation for breast augmentation: case reports and review of the literature. Breast J 2006; 12: 6365. Missana MC, Laurent I, Barreau L, Balleyguier C. Autologous fat transfer in reconstructive breast surgery: indications, technique and results. Eur J Surg Oncol 2007; 33: 685690. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, Harii K. Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 2008; 32: 4855. Cotrufo S, Mandal A, Mithoff EM. Fat grafting to the breast revisited: safety and efcacy. Plast Reconstr Surg 2008; 121: 701. Gosset J, Guerin N, Toussoun G, Delaporte T, Delay E. [Radiological evaluation after lipomodelling for correction of breast conservative treatment sequelae.] Ann Chir Plast Esthet 2008; 53: 178189. Pinsolle V, Chichery A, Grolleau JL, Chavoin JP. Autologous fat injection in Polands syndrome. J Plast Reconstr Aesthet Surg 2008; 61: 784791. Zheng DN, Li QF, Lei H. Autologous fat grafting to the breast for cosmetic enhancement: experience in 66 patients with long-term follow up. J Plast Reconstr Aesthet Surg 2008; 61: 792798. Zocchi ML, Zuliani F. Bicompartmental breast lipostructuring. Aesthetic Plast Surg 2008; 32: 313328. Carvajal J, Patino JH. Mammographic ndings after breast augmentation with autologous fat injection. Aesthet Surg J 2008; 28: 153162.

62 Wang H, Jiang Y, Meng H, Yu Y, Qi K. Sonographic assessment on breast augmentation after autologous fat graft. Plast Reconstr Surg 2008; 122: 36e38e. 63 Kaufman GJ, Sarfarti I, Metzinger C, Daho F, Nos C, Inguenault C et al. Impact of fat grafting the chest wall prior to implant reconstruction in high risk patients. Cancer Res 2009; 69(Suppl): abstract 4143. 64 ElFadl D, Mahapatra T, McManus P, Drew P. Lipomodelling of the breast. Cancer Res 2009; 69(Suppl): abstract 4149. 65 Delaporte T, Delay E, Toussoun G, Delbaere M, Sinna R. [Breast volume reconstruction by lipomodeling technique: about 15 consecutive cases.] Ann Chir Plast Esthet 2009; 54: 303316. 66 Hyakusoku H, Ogawa R, Ono S, Ishii N, Hirakawa K. Complications after autologous fat injection to the breast. Plast Reconstr Surg 2009; 123: 360370. 67 Panettiere P, Marchetti L, Accorsi D. The serial free fat transfer in irradiated prosthetic breast reconstructions. Aesth Plast Surg 2009; 33: 695700. 68 Kanchwala SK, Glatt BS, Conant EF, Bucky LP. Autologous fat grafting to the reconstructed breast: the management of acquired contour deformities. Plast Reconstr Surg 2009; 124: 409418. 69 Del Vecchio D. Breast reconstruction for breast asymmetry using recipient site pre-expansion and autologous fat grafting: a case report. Ann Plast Surg 2009; 62: 523527. 70 Mu DL, Luan J, Mu L, Xin MQ. Breast augmentation by autologous fat injection grafting: management and clinical analysis of complications. Ann Plast Surg 2009; 63: 124127. 71 Lazaretti MG, Giovanardi G, Gibertoni F, Cagossi K, Artioli F. A late complication of fat autografting in breast augmentation. Plast Reconstr Surg 2009; 123: 71e72e. 72 Salgarello M, Visconti G, Farallo E. Autologous fat graft in radiated tissue prior to alloplastic reconstruction of the breast: report of two cases. Aesthetic Plast Surg 2010; 34: 510. 73 Pereira LH, Sterodimas A. Autologous fat transplantation and delayed silicone implant insertion in a case of Mycobacterium avium breast infection. Aesthetic Plast Surg 2010; 34: 14. 74 Babovic S. Complete breast reconstruction with autologous fat graft a case report. J Plast Reconstr Aesthet Surg 2010; 63: e561e563. 75 Rigotti G, Marchi A, Stringhini P, Baroni G, Gali` M, e Molino AM et al. Determining the oncological risk of autologous lipoaspirate grafting for post-mastectomy breast reconstruction. Aesthetic Plast Surg 2010; 34: 475480. 76 Serra-Renom JM, Munoz-Olmo JL, Serra-Mestre JM. Fat grafting in postmastectomy breast reconstruction with expanders and prostheses in patients who have received radiotherapy: formation of new subcutaneous tissue. Plast Reconstr Surg 2010; 125: 1218. 77 Erol OO, Agaoglu G, Uysal AO. Liponecrotic pseudocysts following fat injection into the breast. Plast Reconstr Surg 2010; 125: 168e170e.

2012 British Journal of Surgery Society Ltd Published by John Wiley & Sons Ltd

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British Journal of Surgery 2012; 99: 768780

Autologous fat for reconstruction of the breast

779

78 Wang H, Jiang Y, Meng H, Zhu Q, Dai Q, Qi K. Sonographic identication of complications of cosmetic augmentation with autologous fat obtained by liposuction. Ann Plast Surg 2010; 64: 385389. 79 Villani F, Caviggioli F, Klinger F, Maione L, Klinger M. Fat graft before breast reconstruction by latissimus dorsi. Plast Reconstr Surg 2010; 126: 190e192e. 80 Ueberreiter K, von Finckenstein JG, Cromme F, Herold C, TM Tanzella U, Vogt PM. [BEAULI a new and easy method for large-volume fat grafts.] Handchir Mikrochir Plast Chir 2010; 42: 379385. 81 Veber M, Tourasse C, Toussoun G, Moutran M, Mojallal A, Delay E. Radiographic ndings after breast augmentation by autologous fat transfer. Plast Reconstr Surg 2011; 127: 12891299. 82 Del Vecchio DA, Bucky LP. Breast augmentation using preexpansion and autologous fat transplantation: a clinical radiographic study. Plast Reconstr Surg 2011; 127: 24412450. 83 Rietjens M, De Lorenzi F, Rossetto F, Brenelli F, Manconi A, Martella S et al. Safety of fat grafting in secondary breast reconstruction after cancer. J Plast Reconstr Aesthet Surg 2011; 64: 477483. ` 84 Panettiere P, Accorsi D, Marchetti L, Sgro F, Sbarbati A. Large-breast reconstruction using fat graft only after prosthetic reconstruction failure. Aesthetic Plast Surg 2011; 35: 703708. 85 Serra-Renom JM, Munoz-Olmo J, Serra-Mestre JM. Breast reconstruction with fat grafting alone. Ann Plast Surg 2011; 66: 598601. 86 Serra-Renom JM, Munoz-Olmo J, Serra-Mestre JM. Treatment of grade 3 tuberous breasts with Pucketts technique (modied) and fat grafting to correct the constricting ring. Aesthetic Plast Surg 2011; 35: 773781. 87 Lee KS, Seo SJ, Park MC, Park DH, Kim CS, Yoo YM et al. Sepsis with multiple abscesses after massive autologous fat grafting for augmentation mammoplasty: a case report. Aesthetic Plast Surg 2011; 35: 641645. 88 Sarfati I, Ihrai T, Kaufman G, Nos C, Clough KB. Adipose-tissue grafting to the post-mastectomy irradiated chest wall: preparing the ground for implant reconstruction. J Plast Reconstr Aesthet Surg 2011; 64: 11611166. 89 Losken A, Pinell XA, Sikoro K, Yezhelyev MV, Anderson E, Carlson GW. Autologous fat grafting in secondary breast reconstruction. Ann Plast Surg 2011; 66: 518522. 90 Yang H, Lee H. Successful use of squeezed-fat grafts to correct a breast affected by Poland syndrome. Aesthetic Plast Surg 2011; 35: 418425. 91 Young AO, Zellner E. The hybrid breast reconstruction use of autologous fat transfer to augment the autologous tissue to implant ratio in oncoplastic breast reconstruction. Ann Oncol 2011; 22(Suppl 2): ii48ii50. 92 Murphy C, ElFadl D, McManus P. Experience of autologous fat transfer in a single breast unit rst 100 cases. Eur J Surg Oncol 2011; 37: 5(S14).

93 Petit JY, Botteri E, Lohsiriwat V, Rietjens M, De Lorenzi F, Garusi C et al. Locoregional recurrence risk after lipolling in breast cancer patients. Ann Oncol 2012; 23: 582588. 94 Beck M, Amar O, Bodin F, Lutz JC, Lehmann S, Bruant-Rodier C. Evaluation of breast lipolling after sequelae of conservative treatment for cancer. A prospective study of ten cases. Aesthetic Plast Surg 2012; 35: 221228. 95 Irani Y, Casanova D, Amar E. [Autologous fat grafting in radiated tissue prior to breast prosthetic reconstruction: Is the technique reliable?] Ann Chir Plast Esthet 2012; 57: 5966. 96 Rohrich RJ, Sorokin ES, Brown SA. In search of improved fat transfer viability: a quantitative analysis of the role of centrifugation and harvest site. Plast Reconstr Surg 2004; 113: 391395. 97 Ullmann Y, Shoshani O, Fodor A, Ramon Y, Carmi N, Eldor L et al. Searching for the favorable donor site for fat injection: in vivo study using the nude mice model. Dermatol Surg 2005; 31: 13041307. 98 Boschert MT, Beckert BW, Puckett CL, Concannon MJ. Analysis of lipocyte viability after liposuction. Plast Reconstr Surg 2002; 109: 761765. 99 Pu LL, Coleman SR, Cui X, Ferguson RE Jr, Vasconez HC. Autologous fat grafts harvested and rened by the Coleman technique: a comparative study. Plast Reconstr Surg 2008; 122: 932937. 100 Mojallal A, Foyatier JL. [The effect of different factors on the survival of transplanted adipocytes.] Ann Chir Plast Esthet 2004; 49: 426436. 101 Tebbetts JB. Out points criteria for breast implant removal without replacement and criteria to minimize reoperations following breast augmentation. Plast Reconstr Surg 2004; 114: 12581262. 102 Osborn JM, Stevenson TR. Pneumothorax as a complication of breast augmentation. Plast Reconstr Surg 2005; 116: 11221126. 103 Hall-Findlay EJ. Breast implant complication review: double capsules and late seromas. Plast Reconstr Surg 2011; 127: 5666. 104 Poblete JV, Rodgers JA, Wolfort FG. Toxic shock syndrome as a complication of breast prostheses. Plast Reconstr Surg 1995; 96: 17021708. 105 Alderman AK, Wilkins EG, Kim HM, Lowery JC. Complications in postmastectomy breast reconstruction: two-year results of the Michigan breast reconstruction outcome study. Plast Reconstr Surg 2002; 109: 22652274. 106 Hvilsom GB, Holmich LR, Henriksen TF, Lipworth L, McLaughlin JK, Friis S. Local complications after cosmetic breast augmentation: results from the Danish Registry for Plastic Surgery of the Breast. Plast Reconstr Surg 2009; 124: 919925. 107 Colakoglu S, Khansa I, Curtis MS, Yueh JH, Ogunleye A, Haewyon C et al. Impact of complications on patient satisfaction in breast reconstruction. Plast Reconstr Surg 2011; 127: 14281436.

2012 British Journal of Surgery Society Ltd Published by John Wiley & Sons Ltd

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British Journal of Surgery 2012; 99: 768780

780

F. Claro Jr, J. C. A. Figueiredo, A. G. Zampar and A. M. Pinto-Neto

108 Manabe Y, Toda S, Miyazaki K, Sugihara H. Mature adipocytes, but not preadipocytes, promote the growth of breast carcinoma cells in collagen gel matrix culture through cancerstromal cell interactions. J Pathol 2003; 201: 221228. 109 Yu JM, Jun ES, Bae YC, Jung JS. Mesenchymal stem cells derived from human adipose tissues favor tumor cell growth in vivo. Stem Cells Dev 2008; 17: 463473. 110 Iyengar P, Combs TP, Shah SJ, Gouon-Evans V, Pollard JW, Albanese C et al. Adipocyte-secreted factors synergistically promote mammary tumorigenesis through induction of anti-apoptotic transcriptional programs and proto-oncogene stabilization. Oncogene 2003; 22: 64086423. 111 Vona-Davis L, Rose DP. Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 2007; 14: 189206. 112 Hou WK, Xu YX, Yu T, Zhang L, Zhang WW, Fu CL et al. Adipocytokines and breast cancer risk. Chin Med J 2007; 120: 15921596. 113 Lohsiriwat V, Curigliano G, Rietjens M, Goldhirsch A, Petit JY. Autologous fat transplantation in patients with breast cancer: silencing or fueling cancer recurrence? Breast 2011; 20: 351357. 114 Figueiredo JCA, Naufal RR, Claro F Jr, Arias V, Bueno-Pereira PR, Inaco-Cirino LM. Prefabricated ap

115

116

117

118

119

composed by skin and terminal gastromental vessels. Experimental study in rabbits. J Plast Reconstr Aesthet Surg 2010; 63: e525e528. Slavin SA, Love SM, Goldwyn RM. Recurrent breast cancer following immediate reconstruction with myocutaneous aps. Plast Reconstr Surg 1994; 93: 11911204. Kroll SS, Schusterman MA, Tadjalli HE, Singletary SE, Ames FC. Risk of recurrence after treatment of early breast cancer with skin-sparing mastectomy. Ann Surg Oncol 1997; 4: 193197. Veronesi U, Cascinelli N, Mariani L, Greco M, Saccozzi R, Luini A et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 2002; 347: 12271232. Fisher B, Anderson S, Bryant J, Margolese RG, Deutsch M, Fisher ER et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 2002; 347: 12331241. Petit JY, Gentilini O, Rotmensz N, Rey P, Rietjens M, Garusi C et al. Oncological results of immediate breast reconstruction: long term follow-up of a large series at a single institution. Breast Cancer Res Treat 2008; 112: 545549.

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