Breast Fat Grafting with Platelet-Rich Plasma: AComparative Clinical Study

BREAST

Breast Fat Grafting with Platelet-Rich Plasma: AComparative Clinical Study and Current Stateof the Art

Marzia Salgarello, M.D.Giuseppe Visconti, M.D.Antonio Rusciani, M.D.,

Ph.D.

Rome, Italy

Background: The role of platelet-rich plasma in enhancing fat graft take isattracting the scientific community. There is, however, a lack of clinical studieson the matter. The aim of this article is to report the authors’ experience inbreast fat grafting with and without platelet-rich plasma and to investigate thestate of the art on adipose tissue platelet-rich plasma enrichment.Methods: The authors retrospectively reviewed 42 women who underwentbreast fat grafting between September of 2007 and September of 2009. Seven-teen of these patients (40 percent) were grafted with fat (according to Coleman)enriched with platelet-rich plasma at 10 percent (group A), and 25 patients (60percent) received only fat grafts according to Coleman (group B). All patientsunderwent preoperative breast ultrasound and mammography and were regu-larly followed up with breast ultrasound 3 months later and then at 6-monthintervals. The reconstructive and aesthetic outcomes were evaluated using thefollowing parameters: (1) clinical outcomes according to the surgeons and thepatient, (2) the rate of liponecrosis at breast ultrasound, and (3) the need offurther fat grafting to achieve the planned result.Results: The clinical outcomes, the rate of liponecrosis at breast ultrasound,and the need for further fat grafting reveal that fat grafting plus platelet-richplasma at 10 percent is not superior to Coleman fat grafting alone.Conclusions: In the authors’ retrospective analysis, no effect of platelet-richplasma was seen in enhancing fat graft take when compared with the Colemanfat graft. Further research and prospective clinical studies are needed to un-derstand the role of platelet-rich plasma, if any, in fat grafting. (Plast. Reconstr.Surg. 127: 2176, 2011.)

Autologous fat grafting has gained wide pop-ularity because it exhibits many qualities asa natural filler and has demonstrated ther-

apeutic potential.1–3 Nowadays, the quality of thetransplanted fat, the rate of adipose-derived stemcells contained in the ready-for-transplant fat, andthe nutrition of the graft from the recipient siteare widely considered the key factors influencingthe survival of the grafted fat. Recently, the influ-ence of local anesthetic solution on cellular via-bility has been investigated in vitro as well.4 Fatgraft viability, however, remains a controversial

subject. Due to the graft’s unpredictability, mul-tiple operations are usually needed to reach thetarget volume. Furthermore, failure of fat grafts totake may lead to the development of liponecroticlesions. To obviate these drawbacks, some strate-gies have been advanced to improve graft viability.Tissue-engineering approaches and the use ofchemical cell-stimulating factors, such as insulin,vitamins, and growth factors,5–10 are some exam-ples. Among these, most recently, the role of fatenriched with autologous platelet-rich plasma isattracting many surgeons.

From the Department of Plastic and Reconstructive Surgery,Catholic University of Sacro Cuore, University Hospital Ag-ostino Gemelli; and Department of Oculoplastics, San Carlodi Nancy Hospital.Received for publication August 2, 2010; accepted November29, 2010.Copyright ©2011 by the American Society of Plastic Surgeons

DOI: 10.1097/PRS.0b013e3182139fe7

Disclosure: RegenLab (Le Mont-sur-Lausanne,Switzerland) supplied the RegenKit Extracell Adi-pocyte for this clinical study. The authors have nofinancial interests to declare in relation to the con-tent of this article.

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Platelet-rich plasma is a concentration of au-tologous human platelets (three to five timeshigher than baseline platelet count) in a smallvolume of plasma, containing the seven maingrowth factors proved to be actively degranulatedby platelets to start the wound-healing process.The three isomers of platelet-derived growth fac-tor (PDGF��, PDGF��, and PDGF��), two iso-mers of transforming growth factor-� (TGF�1 andTGF�2), vascular endothelial growth factor, andepithelial growth factor are the main growth fac-tors released. They are able to stimulate cell pro-liferation and cell differentiation for tissue regen-eration and neoangiogenesis.11,12 In addition tothese growth factors, platelet-rich plasma also con-tains fibronectin, vitronectin, fibrinogen, osteo-calcin, and osteonectin, known to act as cell ad-hesion molecules and as a matrix for cellularprocesses.13 The active secretion of these growthfactors is initiated by the clotting process of blood.The natural process can be started by addingthrombin or calcium chloride. The active secre-tion of these growth factors by platelets beginswithin 10 minutes after clotting, with more than 95percent of the presynthesized growth factors se-creted within 1 hour. After this initial burst, theplatelets synthesize and secrete additional pro-teins for the balance of their lives (5 to 10 days).13

Successful clinical applications have been re-ported using platelet-rich plasma, such as indifficult wounds, maxillofacial bone defects,and cosmetic surgery.13–16 To our knowledge, alimited number of articles have been publishedon adipose tissue enriched with platelet-richplasma.17,18 The purpose of this study is to report

our early experience with breast fat grafts en-riched with platelet-rich plasma and to investi-gate the current state of art on adipose tissueplatelet-rich plasma enrichment.

PATIENTS AND METHODSForty-two women who underwent autologous

fat grafting to the breast with different indicationsbetween September of 2007 and September of2009 were retrospectively reviewed (Table 1).Among these patients, 17 (40 percent) weregrafted with fat enriched with 10 percent plate-let-rich plasma, representing the experimentalgroup (group A) in this series. Twenty-five pa-tients (60 percent) received only fat grafts ac-cording to Coleman, representing the controlgroup (group B) in this series.

Each patient underwent a preoperative breastultrasound and mammography to exclude any sus-pect lesion. Breast fat grafting was performed fordifferent indications (Table 1). The mean age atthe time of surgery was 47 years (range, 27 to 68years). A total of 14 patients underwent adjuvantradiation therapy. For these cases, fat grafting hadbeen performed at least 6 months after radiation.

Fat Grafting to the BreastThe adipose tissue was harvested from the ab-

domen, flanks, trochanter regions, inner thigh,and medial aspect of the knees, based on patientphysical constitution. Through small incisions, thedefined area was infiltrated with the anestheticsolution (NaCl 0.9% with Xylocaine 2% and epi-nephrine 1:500,000) according to the superwet

Table 1. Indications for Breast Fat Graft, Number of Patients Treated, and Number of Patients withLiponecrosis Correlated to Group A and Group B

Liponecrosis

No. of PatientsOil Cyst

(No. of Cases)Complex Cystic Images

(No. of Cases)

Indications Group A Group B Group A Group B Group A Group B

Contour deformities after postmastectomy implantreconstruction, not radiated 7 13 2 1 — —

Contour deformities after postmastectomy implantreconstruction, radiated 3 2 — — 1 2

Contour deformities after postmastectomy autologousreconstruction, not radiated 2 3 — 1 — —

Contour deformities after breast-conserving surgery,radiated 4 5 2 1 2 2

Contour deformities after augmentationmammaplasty — 1 — — — —

Poland syndrome 1 1 — 1 1 —Total 17 25 4 4 4 4Group A, fat graft with platelet-rich plasma; group B, fat graft without platelet-rich plasma.

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technique. The adipose tissue was aspirated usinga two-holed blunt harvesting cannula (3 mm in theinner diameter) attached to a 10-ml Luer-Lok sy-ringe (Becton-Dickinson, Franklin Lakes, N.J.);gentle negative pressure was created by withdraw-ing the plunger gradually.

The capped 10-ml Luer-Lok syringes wereplaced in a centrifuge (MPW-53; MPW MedicalInstruments, Warsaw, Poland) and spun at 3000rpm for 3 minutes. After the superior layer (oil)and the inferior layer (mostly blood and infil-tration liquids) were discarded, the middle layerconsisting of purified lipoaspirate was trans-ferred through a Luer-Lok connector to 1-ml or3-ml syringes.

Group A: Experimental GroupThe platelet-rich plasma was obtained using

the RegenKit Extracell Adipocyte (RegenLab, LeMont-sur-Lausanne, Switzerland), according tothe manufacturer’s instructions. From 16 to 40 mlof blood was withdrawn from the each patientusing Regen BHT 8-ml vacuum tubes. The vac-uum tubes were placed in a centrifuge and spunat 3500 rpm for 5 minutes to obtain about 4 mlof platelet-rich plasma for each tube. Calciumchloride (10%) was added to platelet-richplasma. Thus, the 3-ml syringes were filled with2.7 ml of processed lipoaspirate and 0.3 ml ofplatelet-rich plasma (platelet-rich plasma at10%, platelet-rich plasma:fat ratio, 1:9). The sy-ringes were then gently inverted one to twotimes to allow a better mixture of the two com-ponents and were ready for transplant.

Group B: Control GroupThe 1-ml syringes were filled with 0.9 ml of

processed lipoaspirate and 0.09 ml of normal sa-line and were ready for transplant. A 17-G, one-holed, blunt Coleman cannula was connected tothe 1-ml and 3-ml syringes. The content was thentransplanted in the recipient site as the bluntcannula was withdrawn, according to the Cole-man technique. The fat was transplanted mul-tidirectionally from deep to superficial tissues,transplanting around 0.2 ml each time the can-nula was withdrawn.

Clinical and Radiological Evaluation and Post-operative Follow-Up

To compare both groups, the reconstructiveand aesthetic outcomes were evaluated based onthree parameters, as follows: (1) clinical outcomesaccording to the surgeons and the patient, (2) therate of fat necrosis at breast ultrasound, and (3)

the need for further fat grafting to achieve theplanned result.

The clinical outcomes were evaluated sepa-rately by a blinded group of plastic surgeons as wellas by the attending surgeon using a grading scaleat least 3 months after the last fat grafting. Thisassessment was based on clinical examinations andby reviewing clinical pictures of the breasts. Theevaluation scale consisted of five ascendinggrades, from 1 to 5, as follows: grade 1, no resultobtained; grade 2, poor improvement; grade 3,fair visible result; grade 4, good result that almostsatisfies the volume and result expected; andgrade 5, excellent result, attributed when the de-sired outcomes are achieved. Patient satisfactionwas evaluated using the patient self-assessmentquestionnaire according to Anderson et al.19 Fi-nally, the mean between patient evaluation andsurgeon evaluation was determined.

Breast ultrasound and mammography wereperformed on all patients preoperatively. Postop-eratively, each patient underwent breast ultra-sound 3 months after the operation and then at6-month intervals. This was done to evaluate therate of fat necrosis (Table 1).

Statistical AnalysisThe clinical outcome scores were analyzed us-

ing the Mann-Whitney test to determine whetherthere were any significant differences between thetwo groups. The percentage of patients who ex-perienced postoperative fat necrosis was analyzedusing Fisher’s exact test to determine whetherthere was any significant difference. The percent-age of patients for each group who underwentfurther sessions of fat grafting was analyzed usingthe Mann-Whitney test to determine whetherthere was any significant difference; p values lessthan 0.05 were considered significant.

RESULTSGroup A

An average of 120 cc of fat was transplanted ateach session (range, 25 to 231 cc). The averageclinical follow-up for this group was 9 months(range, 3 to 16 months). The average radiologicalfollow-up time from the last fat graft was 6 months(range, 3 to 12 months). Seven patients had ahistory of breast radiation.

Of a total of 17 patients, eight (47 percent)were evaluated as grade 2, five as grade 3 (29percent), four as grade 4 (24 percent), and noneas grade 5 (Figs. 1 and 2). At breast postoperativeultrasound, seven patients (41 percent) showed

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signs of fat necrosis. Among these, five patientshad been previously radiated. Two patients (12percent) underwent three sessions of fat grafting,10 patients (59 percent) had two sessions, and theremaining five (29 percent) had one session each.

Group BAn average of 115 cc of fat was transplanted at

each session (range, 21 to 169 cc). The averageclinical follow-up for this group was 9 months(range, 3 to 24 months). The radiological fol-low-up time from the last fat graft was 9 months(range, 3 to 24 months). Seven patients had ahistory of breast radiation. Of a total of 25 patients,five (20 percent) were evaluated as grade 2, 13 asgrade 3 (52 percent), five as grade 4 (20 percent),and two as grade 5 (8 percent) (Figs. 3 and 4).

At breast postoperative ultrasound, seven pa-tients (28 percent) showed signs of fat necrosis.

Among these, four patients (57 percent) had ahistory of radiation. Four patients (16 percent)had three fat grafting sessions, 14 (56 percent)had two, and seven (28 percent) had only onesession.

Comparison between Group A and Group BThe clinical outcome scores for the experi-

mental and control groups demonstrated no sig-nificant differences between the groups (Fig. 5).The percentage of patients who experienced fatnecrosis in the two groups showed no significantdifference (Fig. 6).

The percentage of patients who required an-other session of fat grafting for each group dem-onstrated no significant differences between thegroups (Fig. 7). So far, clinical outcomes, fat ne-crosis experienced at breast ultrasound, and needfor further fat grafting have revealed that platelet-rich plasma is not superior to fat grafting alone.

Fig. 1. The patient had undergone left breast implant reconstruction after radical modified mastectomy and right breastaugmentation. (Above) The patient shows a contour defect in the left upper pole. She underwent two sessions of fat graftingwith platelet-rich plasma at 10%. At each session, she received 70 cc of fat. (Below) Three months after the last fat graft, thepatient was satisfied. The result was classified as grade 4.


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DISCUSSIONPlatelet-rich plasma is supposed to favor fat

graft viability, both promoting cell proliferationand favoring neoangiogenesis of the transplantedfat in the recipient site. In our hands, we experi-enced no enhancement of fat graft take using fatenriched with platelet-rich plasma at 10% (plate-let-rich plasma:fat ratio, 1:9) when compared withfat grafting alone. Moreover, platelet-rich plasmadid not lead to a reduction in the number of fatgrafting sessions needed to achieve the plannedresult when compared with fat grafting alone.

We investigated the rate of fat necrosis at reg-ular postoperative breast ultrasound as an objec-tive parameter to evaluate the effect on fat grafttake using the two compared methods. The ra-diologic pattern of fat necrosis after breast fatgrafting has been described extensively by Frenchauthors.20,21 These authors have concluded that fat

necrosis can occur when there is a failure of fatgraft take in the recipient site. In our series, weparadoxically observed a higher rate of liponecro-sis in patients treated with platelet-rich plasma,even if this was not statistically significant.

The unpredictability of fat graft survival hasled surgeons worldwide to investigate alternativetechniques in fat grafting to improve its take. Manyapproaches have been proposed in recent years.Currently, the Coleman technique remains themost reliable.21–24

Nevertheless, increasing attention is beingplaced on platelet-rich plasma in fat grafting dis-proportionate to the experimental and clinicalreports available. This is probably because thereis a fascinating but still unclear theory behindthe potential advantages of platelet-rich plasmain fat grafting. Furthermore, the clinical appli-cation described is easy to perform, does not

Fig. 2. The patient presented with a contour defect after right superolateral quadrantectomy plus radiation therapy. (Above)She underwent two sessions of fat grafting with platelet-rich plasma at 10%. In the first session, she received 150 cc of fat in theright upper poles. After 4 months, she underwent a second fat graft with 197 cc of fat in the upper pole. (Below) Ten monthsafter the last fat graft, the patient was not satisfied with the result. She was classified as grade 2.


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influence the duration of surgery, is not aggres-sive for the patient, and does not require speciallaboratory machines.

With this article, we retrospectively analyze ourexperience in platelet-rich plasma fat enrichment.The limitations of our study are represented by thefact that it is a retrospective and not randomizedstudy. To our knowledge, no prospective random-ized studies on humans are available in the liter-ature on fat grafting with platelet-rich plasma.Therefore, many open questions remain unan-swered and need to be clarified by prospective,randomized studies on the matter to understandwhether platelet-rich plasma has a role in enhanc-ing fat graft take when compared with fat graftingaccording to Coleman alone in the clinical setting.

What Is the Theory behind the Technique?Positive effects of platelet-rich plasma in fa-

voring angiogenesis processes and proliferation of

adipose-derived stem cells have been demon-strated experimentally. In relation to angiogene-sis, Eppley et al.14 reported that platelet-richplasma growth factors stimulate endothelial cellsnear their application site, favoring proliferationand formation of new capillaries. Moreover, in anin vitro study, Hu et al.25 concluded that platelet-rich plasma is a potential contributor in possiblystarting the process of angiogenesis, recruiting theendothelial cells that line blood vessels and be-ginning the initiation of bone regeneration. Thisis because they observed mRNA expression of vas-cular endothelial growth factor and platelet-de-rived growth factor in rat bone marrow stromalcell differentiation inducted by using platelet-richplasma. Thus, this may begin and strengthen theprocess of angiogenesis, favoring early contact ofthe graft with new microvessels. Rughetti et al.26

and Giusti et al.27 studied the in vitro effect ofplatelet-rich plasma on human umbilical vein en-

Fig. 3. The patient presented with a contour defect after medial-inferior quadrantectomy plus radiation therapy. (Above) Sheunderwent three sessions of fat grafting without platelet-rich plasma. The scar tissue was released using a NoKor needle(Becton-Dickinson, Franklin Lakes, N.J.). She received 78 cc of fat at the first session and 88 cc and 87 cc at the second and thirdsessions, respectively. (Below) Fourteen months later the patient was very satisfied with the result. She was classified as grade 5.


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dothelial cells isolated from umbilical cord veins.They observed that when used at specific concen-trations, platelet gel-released supernatant is ableto induce proliferation and to stimulate motility

and invasiveness of endothelial human cells.Higher concentrations induce a reversion of thestimulatory processes. Adipose tissue angiogenesis,however, is a complex process that involves many

Fig. 4. The patient presented with a contour defect after lateral pole quadrantectomy plus radiation therapy. (Above) Sheunderwent one session of fat grafting without platelet-rich plasma. The scar tissue was released using a NoKor needle. Shereceived 169 cc of fat. (Below) Six months later the patient was not satisfied with the result. She was classified as grade 2.

Fig. 5. Clinical outcomes score for each patient in group A and group B. PRP, platelet-rich plasma.


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steps, such as basement membrane breakdown,vasculogenesis, angiogenic remodeling, vessel sta-bilization, and vascular permeability.

Is Platelet-Rich Plasma Really Sufficient toSupport the Entire Adipose Tissue AngiogenesisProcess?

In relation to cell proliferation, Kakudo et al.28

showed that activated platelet-rich plasma con-tains large amounts of PDGF-AB and TGF-�1 andthat they promoted the proliferation of humanadipose-derived stem cells and human dermal fi-broblast in vitro. Cell proliferation was maximallypromoted when 5% activated platelet-rich plasmawas added to the culture medium. Paradoxically,the addition of 20% activated platelet-rich plasmadid not promote it. Similarly, Hsu et al.29 observedthat the proliferation of oral cells is significantlydecreased when treated with high concentrationsof platelet-rich plasma. Abundant secretion ofthrombospondin-1 from concentrated platelet-rich plasma may explain the antiproliferative ef-

fect. So far, there is evidence in vitro that productsfrom platelet-rich plasma positively interact withadipose-derived stem cells and may promote an-giogenesis at certain concentrations.

Is Platelet-Rich Plasma Really Effective for En-hancing Fat Graft Take in the Clinical Setting?

In the in vivo settings, the advantages of en-riching purified fat with platelet-rich plasma arequestionable. In 2008, Por et al.30 published an invivo experimental study evaluating the effect ofplatelet-rich plasma on increasing fat graft survivalin the nude mouse. They evaluated weight, vol-ume, cellular integrity of the fat cells, vascularityof the specimens, degree of fibrosis, necrosis, andinflammation. The treated group received fat, pu-rified according to Coleman, enriched with plate-let-rich plasma with a ratio of fat to platelet-richplasma of 4:1 (platelet-rich plasma at 20%). Com-paring the treated group with controls, these au-thors demonstrated no significant differences be-tween the two groups for any of the parameters

Fig. 6. Percentage of patients with postoperative liponecrosis at ultrasound follow-up in group Aand group B. US, ultrasound; PRP, platelet-rich plasma.

Fig. 7. Number of fat grafting sessions needed for each patient in group A and group B. PRP, plate-let-rich plasma.


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considered. However, Nakamura et al.31 recentlyevaluated the effects of platelet-rich plasma on fatgrafting in rats by using autologous fat and blood.They grafted entire pieces of fat harvested fromthe inguinal region of the rats instead of lipoas-pirate. They found that a platelet-rich plasma:fatratio of 1:4 (platelet-rich plasma at 20%) supportsfat graft volume and viability by promoting capil-lary formation in the graft for at least 120 dayscompared with fat grafting alone in rats. Theyfound no differences in the early 10 days betweenboth groups.

Besides our series, the only clinical reportson humans available in the literature on the useof platelet-rich plasma with purified fat comefrom Cervelli et al.17,18 The authors presentedtwo series of patients treated for facial soft-tissuedefects with loss of volume and elasticity and signsof aging. They maintained that the use of platelet-rich plasma during fat grafting with a platelet-richplasma:fat ratio of 1:2 improves adipose tissuemaintenance and survival when compared with fatgrafting alone.17,18

Which Is the Most Appropriate Fat:Platelet-RichPlasma Ratio to Be Used in the Clinical Setting?

The results from both in vivo and in vitro stud-ies are in line with our experience. In fact, theexperience from our series and from Por et al.’sstudy on nude mice reveals that no advantages arefound using platelet-rich plasma at 10% and 20%(platelet-rich plasma:fat ratios of 1:9 and 1:4)added to purified fat according to Coleman ifcompared with fat grafting alone.30 Nakamura etal.’s findings cannot be compared, as they did notgraft lipoaspirate.31

Despite this, Cervelli et al. maintain that amajor concentration of platelet-rich plasma addedto purified fat (platelet-rich plasma at 33%, plate-let-rich plasma:fat ratio of 1:2) is superior to fatgrafting alone.17,18 Because facial fat grafting hasbeen extensively demonstrated in the literatureto be successful and long lasting,32–34 it would havebeen more interesting if these authors had sup-plied their series with radiologic information (rateof cytosteatonecrosis, preoperative/postoperativethree-dimensional volume study) to demonstratean objective effectiveness of the platelet-richplasma in fat graft take.

In our opinion, if the 1:2 ratio is demonstratedto be the right one, this would limit the use ofplatelet-rich plasma for a large quantity of fat toselected patients. For example, transplanting 200cc of fat, we would need around 100 ml of platelet-

rich plasma. With current platelet-rich plasma ex-tracting kits, this means a blood withdrawal ofaround 200 cc at each operation.

Which Is the Most Appropriate Technique toTransfer Purified Fat and Platelet-Rich Plasma?

In our experience, we mixed the platelet-richplasma with purified lipoaspirate in the same 3 ml-syringe. What we observed is that it is difficult toobtain a homogeneous mixture because of thedifferent physical properties of the two compo-nents. Thus, when we grafted the mixed compo-nents, we were not sure of spreading both con-stituents in equal parts at each passage, probablyresulting in some microtunnels with higher andothers with lower concentrations of platelet-richplasma. It would be interesting to investigate theuse of a double syringe to be technically sure ofspreading a constant quantity of platelet-richplasma and fat at each passage.

CONCLUSIONSOur experience demonstrates that breast fat

grafting enriched with platelet-rich plasma at 10%does not enhance fat graft take compared with fatgrafting (according to Coleman) alone. The lackof clinical evidence on the efficacy of platelet-richplasma in enhancing fat graft take when com-pared with the well-known Coleman fat graftingsuggests that further research and prospectiveclinical studies are needed to understand the roleof platelet-rich plasma, if any, in fat grafting.

Marzia Salgarello, M.D.Via Massimi 101

00136, Rome, [email protected]

ACKNOWLEDGMENTThe authors thank Anna Monda, Department of

Economics and Statistics, University of Salerno, Italy, forstatistical support in this article.

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Breast Fat Grafting with Platelet-Rich Plasma: AComparative Clinical Study