European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Review

Breast cancer and fat grafting: efcacy, safety and complicationsa

systematic review
M. De Deckera,1, L. De Schrijvera,1, F. Thiessena,b , T. Tondua,b , M. Van Goethema,c ,
W.A. Tjalmaa,d,*
a
Multidisciplinary Breast Clinic Antwerp University Hospital, University of Antwerp, Antwerpen, Belgium
b
Plastic Surgery Unit, Antwerp University Hospital, Antwerpen, Belgium
c
Department of Radiology, Antwerp University Hospital, Antwerpen, Belgium
d
Unit of Gynaecologic Oncology, Department of Obstetrics and Gynaecology, Antwerp University Hospital, University of Antwerp, Antwerpen, Belgium

A R T I C L E I N F O A B S T R A C T

Article history:
Received 13 February 2016 Autologous fat grafting (AFG) or lipolling is nowadays a popular technique for breast reconstruction
Received in revised form 7 October 2016 after breast cancer surgery. There is debate regarding the oncological safety and risks of this procedure in
Accepted 21 October 2016 breast cancer patients. A systematic review of the literature published between January rst 1995 and
October rst 2016 was conducted regarding the efcacy, safety and complications of this technique in
Keywords: breast cancer patients after their cancer treatment.
Fat grafting The databases PubMed, Science Direct and Thomson Reuters Web of Science were used to search for
Lipolling qualied articles. Inclusion criteria were women with a personal history of breast cancer and at least one
Breast cancer
lipolling procedure. Only studies containing a minimum of 20 patients were included in this systematic
Recurrence
review.
Safety
Imaging The search yielded a total of 23 suitable articles: 18 case series, 4 retrospective cohort studies and one
Review prospective cohort study. The systematic review encompassed a total of 2419 patients. Medical imaging
was used in the majority of the studies to assess the follow-up. Mammography was the most popular
technique (65.2%), followed by ultrasound (47.8%) and MRI (30.4%). The prevalence of complications was
the following: fat necrosis in 5.31%, benign lesions, like cysts or calcications in 8.78%, infections in 0.96%
and local cancer recurrence in 1.69%.
AFG or lipolling appears to be an oncological safe technique with a low morbidity in women with a
history of breast cancer. In order to have a better understanding and evidence of the oncological safety a
randomised controlled trial is urgently needed. We further recommend that all AFG be registered in the
cancer register.
2016 Elsevier Ireland Ltd. All rights reserved.

Contents

Introduction . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101

Methods . . . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Search and study collection .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Study selection . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Study quality . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Data selection . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Results . . . . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

* Corresponding author at: Multidisciplinary Breast Clinic, Gynaecological

Oncology Unit, Department of Obstetrics and Gynaecology, Antwerp University
Hospital, Wilrijkstraat 10, 2650 Edegem, Belgium.
E-mail addresses: wiebren.tjalma@telenet.be, Wiebren.Tjalma@uza.be
(W.A. Tjalma).
1
Equally contributed.

http://dx.doi.org/10.1016/j.ejogrb.2016.10.032
0301-2115/ 2016 Elsevier Ireland Ltd. All rights reserved.
 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108 101

Literature search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

Efcacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Patient traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Technique . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Patient satisfaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Follow-up . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Complications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
Conict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107

Introduction Study selection

Autologous fat grafting (AFG) or lipolling is nowadays a To narrow the amount of articles down, articles were excluded
commonly used technique to improve the aesthetic outcome after based on the title. The excluding was performed by two
breast conservative surgery (BCS) and after mastectomy with independent reviewers (D.D.M. and D.S.L). All articles of conict
reconstruction. The majority of patients that are diagnosed with were debated until mutual agreement was found. If the title did not
breast cancer nowadays undergo a tumorectomy, followed by correlate to the objective of this review, the article was discarded.
radiotherapy. Patients with an extended or multicentre breast Of the remaining articles the abstract was read while the following
cancer are treated with a mastectomy that can be followed by a criteria were kept in mind:
reconstruction. These interventions obviously cause a deformity to
the breast. Autologous fatty tissue harvested from donor sites such  The article is a study. This excludes reviews, book sections or
as the abdomen, buttocks and medial thighs can be used to correct lectures.
deformities. Lipolling is already commonly used in the eld of  The full text of the article is written in English or French.
reconstructive and aesthetic surgery, but still remains subject to  The primary outcome is fat grafting after BCS or mastectomy, or
discussion regarding its safety in an oncological setting. Angio- fat grafting prior to reconstructive therapy in breast cancer
genic factors that are present in adipose tissue might theoretically patients.
result in an increased risk of breast cancer recurrence [13].  A minimum of 20 female patients with a recent history of breast
Other complications like cysts, calcications or fat necrosis are cancer had to be incorporated in the study.
also observed in patients who undergo AFG [4]. Due to the
complications the American Society of Plastic and Reconstructive Articles corresponding to these criteria were accepted for
Surgeons (ASPRS) advised to terminate the use of the fat grafting further analysis. The same two independent reviewers assessed
technique in the eighties [5]. Nevertheless, the rst reports of the the full text of the remaining articles. Articles with a lack of validity,
clinical use of AFG were already presented in the same period by not declared bias or undened heterogeneous groups were
several authors [6,7]. After an improvement of the fat grafting discarded. If the article did not contain enough valid information
technique by Coleman, its usage regained popularity amongst plastic to implement in this review, it was not included in the analysis. The
surgeons [8]. The principles of this renovation are well described in articles left after the selection process were considered eligible and
the literature, highlighting the features of the technique in detail. The applicable in this review.
description covers three main topics: fat harvesting, fat processing
and fat injection. After the AFG procedure the patient satisfaction can Study quality
be scored with a questionnaire [9].
Present review was performed to assess the efcacy, safety and Using the Oxford Centre for Evidence-Based Medicine (OCEBM)
complications of AFG or lipolling in patients that underwent 2011 v2.1 the qualied articles were assessed for their level of
breast cancer surgery after the diagnosis of breast cancer. evidence by two independent reviewers. Any disparity between
them was discussed until both gave their consent.
Methods
Data selection
Search and study collection
The data extracted from the eligible articles included author,
The databases that were consulted for the systematic review publication date, number of patients, mean age, complication rate,
were PubMed, Science Direct and Thomson Reuters Web of medical imaging, type of surgery and radiotherapy. The collected
Science. The following search terms were used: [breast AND cancer data are registered in Table 1: A detailed overview of the articles
AND (fat grafting OR fat transplantation OR lipotransfer OR used, and Table 2: Radiotherapy treatment and type of surgery
lipolling OR lipostructuring OR lipomodelling)]. All articles that before AFG. The information regarding the AFG technique and the
had been published between January 1st, 1995 and October 1st, patient satisfaction was assembled in Table 3: A detailed overview
2016 were included. The search results were ltered in PubMed for of the technique used and patient satisfaction. Both reviewers
human species. Duplicates were removed and the amounts of discussed obscurities and contradictories until consensus was
references found through literature search were noted. reached.
102 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108

Table 1
A detailed overview of the articles used.

Author Year Evidence Patient Mean Complications Medical imaging

levela total age (y)
n = 2419 Fat Other benign Infection Local Others Rx Echo MRI
necrosis lesions recurrence

1 Bayti et al. [30] 2015 IV 68 53 6 1 1 2

2 Biazus et al. [31] 2015 IV 20 55.4 1 4 1 0 x
3 Bonomi et al. [23] 2013 IV 31 55 2 1 1 1 1 x
4 Brenelli et al. [36] 2014 IV 59 50 2 12 1 3 x xf
5 Costantini et al. [17] 2012 IV 22b 50.8 8 22d 0 1 x x x
6 Delay et al. [29] 2007 IV 42 50.7 2 1 x x x
7 Gale et al. [12] 2015 II b 211 52.2 2 x
8 Hoppe et al. [25] 2013 IV 28 52.4 4 1 1 0 1 x x
9 Ihrai et al. [18] 2012 IV 64 0 1 0 2 1 x
10 Longo et al. [34] 2014 IV 21 37.6 0 0 0 0 x x
11 Masia et al. [13] 2015 II b 100 49.2 3 x
12 Mestak et al. [16] 2016 IIb 32 53 0
13 Missana et al. [24] 2007 IV 69 51 5 0 0 0 x x x
14 Noor et al. [28] 2016 IV 90 53 16 13 0 xg xg
15 Perez-Cano et al. [19] 2012 IV 67 52 46 0 1 x
16 Petit et al. [35] 2011 IV 513 52.1 13 1 3 7 1 x
17 Petit et al. [15] 2011 II b 321 45 4
18 Pinell-White et al. [14] 2015 II b 46 49.6 1 3 x x x
19 Rietjens et al. [4] 2010 IV 155c 48 5 4 2 1 x
20 Riggio et al. [26] 2013 IV 60 49 2 x x
21 Rigotti et al. [51] 2010 IV 137 46.6 5
22 Sarfati et al. [21] 2013 IV 68 46 0 0
23 Silva-Vergara et al. [27] 2015 IV 195 52 24e 1 4 1 x x x

Technique used (x).

Information not mentioned ( ).
a
Oxford Centre for Evidence-Based Medicine 2011 Levels of Evidence. v2.1.
b
2 patients from this study had no history of breast cancer and were not included in this review.
c
3 patients from this study had no history of breast cancer and were not included in this review.
d
All dened as oil cysts diagnosed by ultrasound and MRI.
e
Total of fat necrosis and other complications.
f
On Rx indication.
g
On clinical indication.

Table 2
Radiotherapy treatment and type of cancer surgery before AFG.

Author Patient total Radiotherapy (RT) Mastectomy BCS

n = 2419 n = 1297 With RT No RT Total With RT No RT Total

(n = 390) (n = 353) (n = 1648) (n = 308) (n = 29) (n = 707)
1 Bayti et al. [30] 68 53 44 14 58 9 1 10
2 Biazus et al. [31] 20 20 0 0 0 20 0 20
3 Bonomi et al. [23] 31 31 0
4 Brenelli et al. [36] 59 56 0 0 0 56 3 59
5 Costantini et al. [17] 22a 15 8 6 14 7 1 8
6 Delay et al. [29] 42 36 0 0 0 36 6 42
7 Gale et al. [12] 211 108c 176 35
8 Hoppe et al. [25] 28 16 16 12 28 0 0 0
9 Ihrai et al. [18] 64
10 Longo et al. [34] 21 10 10 11 21 0 0 0
11 Masia et al. [13] 100 70 70 30 100 0 0 0
12 Mestak et al. [16] 32 32 0 0 0 32 0 32
13 Missana et al. [24] 69 30 30 30 60 0 9 9
14 Noor et al. [28] 90 90 58 0 58 32 0 32
15 Perez-Cano et al. [19] 67 61d 0 0 0 61 2 67
16 Petit et al. [35] 513 395 370 143
17 Petit et al. [15] 321 196 125
18 Pinell-White et al. [14] 46 21 21 25 46 0 0 0
19 Rietjens et al. [4] 155b 87 32 61 93 55 7 62
20 Riggio et al. [26] 60 11 11 49 60 0 0 0
21 Rigotti et al. [51] 137 22 22 115 137 0 0 0
22 Sarfati et al. [21] 68 68 68 0 68 0 0 0
23 Silva-Vergara et al. [27] 195 96 132 63

Information not mentioned ( ).

a
2 patients from this study had no history of breast cancer and were not included in this review.
b
3 patients from this study had no history of breast cancer and were not included in this review.
c
28 patients have an unknown radiotherapy status.
d
4 patients have an unknown radiotherapy status.
 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108 103

Table 3
A detailed overview of the technique used and patient satisfaction.

Author Fat grafting Mean injection volume Mean number Mean follow-up Patient satisfaction
technique per session (ml) of sessions (months)
1 Bayti et al. [30] Coleman 212.2 4.9 6.15 91.1% satised or very satised
2 Biazus et al. [31] Coleman 121 1 20.75 9.45/10
3 Bonomi et al. [23] Coleman 247 1.31 21 93,5% satised
4 Brenelli et al. [36] Coleman 52.3 34.4
5 Costantini et al. [17] Coleman 114.8 2.17 12
6 Delay et al. [29] Coleman 166 1.3 20.5 90% satised or very satised
7 Gale et al. [12] Coleman 1.28 32
8 Hoppe et al. [25] BEAULITM method 159 4.1 31.2 89% good to very good
9 Ihrai et al. [18] Coleman 3860a 1.57 46.44
10 Longo et al. [34] Coleman 164.3 4.14 25.9
11 Masia et al. [13] Coleman 98 29
12 Mestak et al. [16] Coleman 27
13 Missana et al. [24] Coleman 124.1 1.22 11.7
14 Noor et al. [28] 154 37.4
15 Perez-Cano et al. [19] ADRC-enriched 136 1.35 12 75% satised or very satised
16 Petit et al. [35] Coleman 107.3 1.25 19.2
17 Petit et al. [15] Coleman 26
18 Pinell-White et al. [14] Coleman 36.3 3.57 50.2
19 Rietjens et al. [4] Coleman 48 15c 18.3
20 Riggio et al. [26] Not Coleman 38.2855.12b 1.37 90
21 Rigotti et al. [51] Coleman 60
22 Sarfati et al. [21] Not Coleman 115 2.3 23 >80% good to very good
23 Silva-Vergara et al. [27] Not Coleman 160 1.6 31

Information not mentioned ( ).

a
38 ml in rst AFG and 60 ml in second and third AFG session.
b
47.13 ml, 38.28 ml and 55.12 ml in respectively rst, second and third AFG session.
c
Most of the patients required only one procedure, 16.8% required more than one.

Results Poland syndrome, gynaecomastia and asymmetry [4,17]. These

Literature search
The literature search, performed by previously dened search
terms, identied 804 records. PubMed, Science Direct and
Thomson Reuters Web of Science revealed 140, 477 and 187 articles
respectively. After adding 20 studies from references and removing
all duplicates, 647 articles remained for screening. The titles were
examined and discussed until 150 articles remained. Ninety
articles were excluded based on abstract, according to the in-
and exclusion criteria. After this selection process, 60 articles were
found eligible for full text reading. Twenty-three studies were
included in this systematic review and were used for the
quantitative synthesis. The process of data collection and selection
is shown in Fig. 1: PRISMA ow diagram showing the process of
data collection, selection and organisation. After reviewing, most
of the articles were discarded because of lack of information that
was required for the statistical analysis. Two interesting articles of
2016 were not included [10,11]. Both articles reviewed the number
of breasts so it was unclear how many patients were included. One
of these articles included patients that had previously undergone
mastectomies for breast cancer and/or prophylactic mammectomy
[11]. In the analysis of these patients no distinction was made
between the breast cancer group and the prophylaxis group. Nearly
all of the studies included in this review are case series, with the
exception of four retrospective cohort studies [1215] and one
prospective cohort study [16]. No published randomised control
studies were found.
Efcacy
Patient traits
The study population of this review comprises 2419 patients. All
patients had a personal history of breast cancer followed by BCS or
mastectomy. Five patients were treated for functional reasons like
patients did not meet the inclusion criteria and were not
incorporated in the patient total. This is mentioned in Table 1.
The study population had a mean age between 37.6 and 55.4 years
old. Table 2 shows that 1648 patients underwent a mastectomy.
There are 390 patients from this group which clearly received
radiotherapy and 353 patients which did not. BCS was used to treat
breast cancer in 707 patients. Of this group 308 patients received
radiotherapy and 61 patients did not. The remaining patients could
not be classied according to radiotherapy treatment due to
inadequate distinction between the BCS and the mastectomy
group. One study did not mention which type of surgery was used
[18]. Two studies reported a total of 32 patients with unknown
radiotherapy treatment status [12,19].
The most common types of cancer were invasive ductal breast
carcinomas and ductal carcinomas in situ. Early breast cancers and
ductal carcinoma in situ of the breast have an excellent prognosis
[20]. After surgical eradication of the cancer, every patient
underwent a secondary breast reconstruction with lipolling.
Technique
AFG as a sole intervention or after another reconstruction
technique such as a silicon implant, TRAM ap or latissimus dorsi
ap, was performed in all patient groups but one [21]. This study
explored a new application of fat grafting in which the AFG
procedure would be carried out prior to such a reconstruction.
Breast conservative surgery is almost always combined with
radiotherapy in order to reduce cancer recurrence. Irradiation
damages the surface, making it very thin and vulnerable. Lipolling
in these circumstances could potentially create a better coverage
for the implant.
The majority of the breast reconstructions were based on the
standardised technique of Coleman. This surgery is performed
under local or general anaesthesia or by a regional nerve block
depending on the patients wishes or the extensiveness of the
surgery. Fat is rst harvested at a donor site with a harvesting
104 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108

PRISMA 2009 Flow Diagram

Records identified through
database searching
(n = 804 )
Idencaon

Pubmed = 140 Additional records identified through

Sciencedirect = 477 other sources
Web of science = 187 (n = 20 )

Records after duplicates removed

(n = 647 )
Screening

Records screened Records excluded

(n = 150 ) (n = 90 )

Full-text articles assessed Full-text articles excluded

for eligibility (n = 37 )
Eligibility

(n = 60 ) - Not enough valid

information for the
systematic review
- Comparing between
AFG techniques
Studies included in - Groups too
qualitative synthesis heterogeneous
(n = 23 )
Included

Studies included in
quantitative synthesis
(n = 23 )

Fig. 1. PRISMA ow diagram showing the process of data collection, selection and organisation.

cannula connected to a Luer-Lock syringe [8]. The abdomen,
buttocks, thighs and the lumbar region are the most popular
locations. All donor sites seem to give the same outcome [8,22].
The choice of donor site is preoperatively discussed with the
patient. The harvested fat is centrifuged at 3000 revolutions per
minute (rpm) for three minutes. The aim of this process is to obtain
three layers. The upper, less dense layer mainly consists of oil while
the second layer contains the potentially viable parcels of fatty
tissue. The lowest, most-dense layer consists of blood and water,
and lidocaine if local anaesthesia was used. The middle layer is
isolated and prepared for injection. It is important to equally
distribute the fat in order to enlarge the contact surface between
donor and host tissue. The usage of a blunt cannula reduces the risk
of tissue damage and subsequently hematomas or ecchymoses [8].
The results of this review demonstrate that the mean amount of
injected volume fat per session had a very broad range between
36.3 and 247 ml. The volume depended on the surgeons
preferences and tissue quality. The mean number of sessions
per patient varied between 1 and 5, but the majority of patients
underwent one, two or occasionally three sessions until symmetry
and satisfaction was optimally reached. It is important to note that
on average 30% of fat is lost due to centrifugation. Another 30% is
lost within 4 months after the autologous fat transplantation in the
recipient site [23].
Not all studies succeeded to follow the technique proposed by
Coleman. In some studies, small modications were made to this
technique according to the surgeons preferences or based on his
experiences. Adaptations were made to the centrifugation speed
and time, the volume of the syringes or the use of anaesthetics. Fat
might, for example, be centrifuged for 4 min at 3500 rpm [24]. Two
authors used a completely different technique [19,25]. In a case
series of 28 patients the BEAULITM method was used [25]. The
prevalence of complications did not differ from any other study. In
this technique small vital fat cell clusters were harvested using
 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108
waterjet assisted liposuction (body-jet1). The fat was constantly
irrigated and simultaneously ltered and washed in a closed sterile
system (LipoCollectorTM). The fat underwent decanting for 5
10 min and was immediately injected. This means that centrifuga-
tion was not applied. The other study used the ADRC (Adipose-
Derived Regenerative Cells) enriched fat graft in a case series of
67 patients [19]. Three studies utilised a technique that was not
precisely dened [21,26,27]. One article did not mention the
lipolling technique that was applied [28].
Patient satisfaction
The efcacy of the fat grafting procedure is evaluated by
questioning the patient satisfaction. Unfortunately, there were
only seven studies that paid attention to this outcome. The
satisfaction assessments reported very pleasing results. Of all
patients, 7595% stated that they were pleased or very pleased
with the cosmetic outcome after the AFG procedure
[19,21,23,25,29,30]. In one study population the patients rated
the cosmetic result on a scale of 110, resulting in an average score
of 9.45/10 [31].
Safety
Follow-up
There is a broad range of mean follow-up time, varying from
6.15 months till 7.5 years. The follow-up of the patients was
performed either by clinical examination or by a combination of
clinical examination with medical imaging techniques. As pre-
sented in Table 1, fteen of the twenty-three studies utilised
mammography as a follow-up procedure (65.2%). Approximately
half of the studies made use of echography (47.8%) and to a more
limited extent, MRI (30.4%). However, the use of MRI is reported by
one study as the best follow-up procedure [17].
Complications
The fat grafting technique is an invasive procedure potentially
resulting, like any other surgical technique, in a variety of
complications. A broad range of complications was assembled
and divided into two categories: major and minor complications.
Minor complications included fat necrosis and other benign
lesions, which were more prevalent. Under benign lesions we
dened complications such as oil cysts, simple cysts, micro or
macro calcications, seromas, hematomas or a lump. Not all
studies reported these aspects because it did not correlate with the
purpose of their study. Major complications include an infection of
the recipient site, like cellulitis, or a local cancer recurrence. These
complications are less prevalent but have an important impact on
the graft survival and quality of life [32]. All studies included in this
systematic review did address the oncological safety after AFG. An
overview of the prevalence of complications and cancer recurrence
is shown in Table 4: Prevalence of complications and local cancer
recurrence.
Table 4
Prevalence of complications and local cancer recurrence.
CI 95%
Fat necrosis 5.31% 1.28%
Other benign lesions 8.78% 1.60%
Infection 0.96% 0.52%
Local cancer recurrence 1.69% 0.51%
105
It was important to differentiate between the four possible
types of cancer recurrence: local, regional or contralateral
recurrence or metastasis. Only a local recurrence could be related
to the fat grafting procedure and was taken into account to
determine the oncological safety of this procedure. On a total of
2419 patients included in this review, 41 patients were diagnosed
with a local cancer recurrence. The prevalence rate varied between
zero and seven cases per study group. An overall prevalence of
1.69% was noted down. The lesion was mostly diagnosed between
12 and 27 months of follow-up after fat grafting. The local cancer
recurrence occurred in 23 patients of the mastectomy group and in
15 patients of the BCS group. One study did not specify which type
of breast cancer surgery was used for the one patient with a local
recurrence [17]. One study did not report which breast cancer
surgery the patients received, however, the study reported two
local recurrences and stated that these two patients were treated
with a mastectomy [33]. A third study with no local cancer
recurrences did not state which breast cancer treatment its
patients had received [24]. Overall, the local cancer recurrence was
2.17% in the BCS group (690 patients) and 1.46% in the mastectomy
group (1574 patients). Eight studies observed no local cancer
recurrence at all [16,19,21,24,25,28,31,34]. These studies arranged a
mean follow-up ranging from 11.7 to 37.4 months.
Infection of the breast after fat transplantation is estimated to
occur in 0.96% of patients. After BCS, the induced inammation
might stimulate an infection of the breast tissue at the reinjection
site. Infection rate is recorded in fourteen of the twenty-three
included studies (1355 patients) [4,17,18,21,2325,27,2931,34
36]. In total, thirteen patients were recorded with an infection
(varying between zero and three cases per study group). Cellulitis
was treated with oral antibiotics or with a conservative approach
[23,27,29,36].
Fat necrosis, also known as steatonecrosis, is a pathological
process occurring when local fat starts to exhibit saponication,
which is a benign inammatory process [37]. In the past, a sharp
cannula was used to inject the fat into the breast. This could easily
damage the breast tissue, resulting in fat necrosis. The prevalence
of this complication has been reduced since the usage of a blunt
cannula [38]. This minor complication was analysed in approxi-
mately half of the patient population (1186 patients) included in
this review [4,14,17,18,2325,28,30,31,3436]. Fat necrosis was
observed in 63 patients (varying between zero and sixteen cases
per study group) resulting in an overall prevalence of 5.31%. Fat
necrosis has a rather good prognosis and will not lead to graft
removal.
Other benign complications like oil cysts, simple cysts, micro or
macro calcications, seromas, hematomas or lumps, are observed
in 8.78% of the patients. These results consist of thirteen studies
reporting the prevalence of benign lesions (1207 patients) [4,17
19,2325,28,30,31,3436]. In 106 patients benign lesions were
observed (varying between zero and forty-six patients per study
group). These lesions are not harmful but may interfere with the
oncological follow-up [39]. Differentiating between such a benign
lesion and a local recurrence might be troublesome for the
screening procedure. Sometimes a biopsy was indicated to provide
Patients analysed (n) Complication rate (n) Min. and max. rate (n)
1186 63 016
1207 106 046
1355 13 03
2419 41 07
106 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108
a conclusive answer. Two authors stated a very high prevalence of
benign lesions [17,19]. The rst study stated an occurrence of
22 benign lesions, all dened as oil cysts, in a population of
22 patients (100%) [17]. The second study observed 46 benign
lesions in a group of 67 patients after 12 months follow-up (69%)
[19]. One study did not differentiate fat necrosis from oil cysts in
23 cases [27]. They did however report one case of a hematoma.
Not all of the complications could be classied in previously
mentioned divisions. Six of the twenty-three articles presented
some other complications. Three studies observed one hematoma
of the donor site [19,23,25]. An infection of the donor site was seen
in one patient [18]. There was one case of a pneumothorax in a
group of 513 patients [35]. A single case of a prosthesis rupture was
seen in a group of 195 patients [27]. Complications of this kind
were not reported in the other seventeen articles.
Discussion
The use of fat grafting offers a broad range of possibilities. The
most common way is a correction after performing another
technique such as a breast implant or ap transplant (DIEP-, SIEA-,
SGAP- or TRAM-aps). A fat grafting intervention prior to such a
breast implant remains a possible, yet relatively unknown option
[21,40]. Fat grafting can also be used as the sole intervention for
immediate reconstruction of the breast after BCS [41]. Lipolling
allows reconstructive and aesthetic surgeons to use unwanted fat
to reshape and resize the treated breasts of patients. It is a practical
and efcient method. The efcacy can be evaluated by examining
several parameters. The patient satisfaction, which can be
examined with a questionnaire, is a good approach to assess the
efcacy. The volume gained in the breast or the aesthetic outcome
reported by the surgeon is an alternative approach in practice. The
quality of life after the AFG procedure could also be considered as a
way to address the efcacy of fat grafting.
The surgeon plays an important role in the quality of outcome
[42]. The experience, technique and material used determine
whether the results are satisfying [43]. There is no standard
guideline yet to be found in the literature regarding the AFG
technique [44]. Although, the most widely applied technique is the
Lipostructure procedure, which is described by Coleman [8]. A
couple of the studies in this review reported slight variations of
this procedure, not including the BEAULI method or the RESTORE-
2 trial [19,25]. These two innovative studies altered the fat grafting
technique or added an extra procedure to enhance its quality
[19,25]. This emphasises the developing state of this technique,
which creates more possibilities to be explored in the future. There
are four options possible to process the harvested fat: centrifuga-
tion, decanting, washing or no fat processing [45,46]. The Coleman
technique has been described with a centrifugation of 3000 rpm
for 3 min [38]. Some particular studies have utilised a different
rotational speed or time centrifuged. The application of decanting
is seen in two studies [21,26]. Washing of the harvested fat is not
mentioned in this systematic review, even though a comparative
study has indicated that this might be the best processing
technique for adipose tissue graft survival [33]. This study has
demonstrated that washing is the least aggressive method since it
preserves and maintains the integrity and number of adipocytes.
General anaesthesia is most often used when a great amount of
fatty tissue is scheduled to be collected. As with all the surgeries
under general anaesthesia, risks and complications are well
known. Local anaesthesia could potentially inuence the metabo-
lism and growth of the fatty tissue. Although, it has been
demonstrated that the glucose transport and lipolysis in adipo-
cytes are only temporarily inhibited by lidocaine for as long as the
cells are exposed to this anaesthetic. The cells regain their function
and growth if lidocaine is no longer present [47].
In this systematic review the prevalence of local cancer
recurrence after AFG is 1.69% in a population of 2419 patients. If
classied by breast cancer surgery, it shows a prevalence of 2.17% in
the BCS group and 1.46% in the mastectomy group. The question
remains whether this outcome can be compared to a population of
patients who did not receive fat grafting after breast cancer
surgery. The four retrospective cohort studies and the one
prospective cohort study that are included in this review compared
their results with a matching group of patients that did not receive
AFG [1216]. They showed a prevalence of local recurrence of
1.71%, 1.90%, 5.6%, and 7.8% and 4.4% in the non-fat grafted patient
groups. These numbers corroborate the statement that there is not
much difference between both groups and support the oncological
safety of AFG. One systematic review reported a 2.3% prevalence of
local cancer recurrence in studies that investigated this complica-
tion [48]. Another review showed a weighted mean recurrence rate
of 4.4% at 24.6 months [49]. Spear et al. stated in their review that
among the 6 studies that reported breast cancer recurrence,
follow-up times ranged from 12 to 91 months with a range of
recurrence from 0% to 12% [50]. Two recent studies were not
included in the analysis of this review [10,11]. The study of
Kronowitz et al. included 108 patients and 167 breasts [10]. A
mastectomy was performed in 97 breasts for breast cancer
treatment and in 70 breasts as breast cancer prophylaxis. During
a mean follow-up period of 20.2 months after the rst lipolling
session no local oncological recurrences were diagnosed. The study
of Kaoutzanis et al. included 719 breasts after breast cancer surgery
[11]. A local oncological recurrence occurred in nine breasts during
a mean follow-up period of 28.1 months.
Limitations
Nearly all of the articles in this review are case series, which
gives reason to belief there is more risk for bias. Cohort studies,
both prospective and retrospective, are less prevalent in this eld
of expertise. In general, there is more access to case series or expert
opinions. There are no published randomised controlled trials
found. This could potentially limit the quality of this systematic
review.
The follow-up procedure appeared to present a lot of diversity
in the articles assembled for this systematic review. Every study
centre had its own manner of performing the follow-up. There is no
guideline for a standardised period of follow-up [44]. In the results
of this review, we noticed that the minimal time for follow-up was
6.15 months and the maximal time was 90 months. This could lead
to an inaccurate display of cancer recurrences found in patients
after fat grafting. The chances of nding a cancer recurrence
increase when there is more time between the lipolling
procedure and the last day of follow-up [51]. One study had a
mean follow-up period of 4.2 years, which had a range between
1.6 years and 8.9 years follow-up [14].
There is still debate about the most appropriate medical
imaging technique during the follow-up. There are different
arguments to support the use of each independent technique,
whether it is mammography, echography or magnetic resonance
imaging [17]. Each technique has its own advantages and
disadvantages.
The prevalence of a local cancer recurrence (1.69%) is rather low
according to the results of this systematic review. It might be
possible that this is due to the safe execution of the procedure and
the choice in patients for this surgical intervention. It might be that
only patients with a good chance of a cancer-free survival were
eligible for the procedure. It is most important to obtain a precise
measurement of this major complication. Additional studies and a
longer follow-up period are required to guarantee the safety of AFG
 M. De Decker et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 207 (2016) 100108
in breast cancer patients [52,53]. Ideally AFG should be included in
the cancer registry.
The minor complications that occur after fat grafting cover a
large section of pathologies. Most of the benign lesions are not
harmful and are a normal nding after lipolling [54]. They are
easily treated or disappear after a small amount of time. It is likely
that the studies did not report all of these ndings. Two studies did
report a high prevalence of cysts which can conrm the statement
that many studies did not report all of the benign lesions [17,19].
The question may rise whether it is important to report these
minor complications. In this systematic review, the prevalence of
fat necrosis was individually assessed. In Table 4 it is shown that
5.31% of the cases had to deal with this side effect. According to its
denition it is not harmful and does not lead to malignancies. It is,
however, of importance to differentiate fat necrosis and other
benign lesions from a cancer recurrence [39].
Conclusion
The underlying purpose of this review is to contribute to the
discussion of AFG after BCS or mastectomy. It will give cause to a
more universal way of performing an intervention using lipolling
and introduce a standardised follow-up procedure. The efcacy of
the AFG technique was evaluated by the overall patient satisfac-
tion. The patient satisfaction was high to very high in 7595%. The
prevalence of fat necrosis and other benign lesions was respec-
tively 5.31% and 8.78%. These minor complications were easy to
handle with conservative treatment. The only inconvenience
caused by these minor complications is the possibility of
mimicking a malignancy during the follow-up screening protocol.
There was no high rate of major complications; infections were
limited to 1 in 100 patients (0.96%). In this review the prevalence of
a local cancer recurrence was 1.69%. The follow-up was performed
by clinical examination, mammography and to a lesser extent
ultrasound and MRI. To determine whether this technique brings
absolutely no oncological risk there is a need for a randomised
controlled trial. We further recommend that all AFG be registered
in the cancer register.
Conict of interest
The authors report no conict of interest.
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