ORIGINAL ARTICLE

Systemic Inflammatory Reaction After Silicone Breast Implant

Maira M. Silva • Miguel Modolin • Joel Faintuch • Camila M. Yamaguchi •

Cintia B. Zandona • Wilson Cintra Jr. • Haroldo Fujiwara •

Rui Curi • Rolf Gemperli • Marcos C. Ferreira

Received: 18 January 2011 / Accepted: 22 February 2011 / Published online: 18 March 2011

� Springer Science+Business Media, LLC and International Society of Aesthetic Plastic Surgery 2011

Abstract

Background Systemic inflammation after augmentation

mammaplasty with modern silicone implants is not cur-

rently recognized. In a prospective controlled study,

C-reactive protein and other variables were monitored,

aiming to test this hypothesis in a young cohort of patients.

Methods Females (18-30 years old, BMI = 18.5-30 kg/m2,

N = 52) were consecutively recruited for breast implant

(n = 24, Group I) and for abdominal liposuction (n = 28,

Group II/Controls). Patients were interviewed at baseline

and followed until 6 months after operation. Variables

included demographic and clinical information, surgical

outcome, inflammatory markers and autoantibodies.

Results Operations were well tolerated, without surgical

or infectious complications. Mean prosthesis size was

258 ± 21 ml (range = 220-280) and mean aspirate of

liposuction was 1972 ± 499 ml (range = 1200-3000).

Preoperative, 2-month, and 6-month C-reactive protein

concentrations for breast implant patients were 1.3 ± 1.2,

4.8 ± 3.0, and 4.3 ± 6.4 mg/l and for liposuction 3.5 ±

2.7, 3.5 ± 2.1, and 2.2 ± 2.2 mg/l, respectively. Change

at 2 months was significant (p = 0.001). Autoantibody

investigation failed to reveal remarkable aberrations,

except for anticardiolipin elevation, which was nearly

symmetrical in the two groups.

Conclusion C-reactive protein levels increased after

operation and correlated with proinflammatory and proco-

agulatory indices. A mild increase in anticardiolipin IgM

occurred but differences between populations were lacking.

Despite excellent cosmetic outcomes and lack of compli-

cations, acute phase reaction could signal ongoing immu-

nogenicity of silicone and long-term monitoring is

recommended.

Keywords Augmentation mammaplasty � Silicone breast

implant � Inflammatory reaction � Autoantibodies �C-reactive protein � Cosmetic breast surgery

Augmentation mammaplasty with silicone implants has

been conducted regularly since 1962, though not without

controversy. Between 1992 and 2006 a moratorium was

established in the USA for aesthetic devices due to suspi-

cion of immune reactions and rheumatologic complica-

tions, besides implant rupture, silicone leakage, and local

complications [1–4]. The majority of studies, including

extensive analysis by the Institute of Medicine, eventually

dispelled such fears [1, 3, 5]. Moreover, new-generation

products are made of cohesive silicone gel and carefully

engineered shells, thus implant rupture or gel bleed has

become uncommon, minor, and asymptomatic [2, 6, 7]. In

this sense, manufacturers all over the world offer devices of

multiple sizes, forms, and textures, and their use has never

been so widespread.

M. M. Silva � M. Modolin � C. B. Zandona � W. Cintra Jr. �R. Gemperli � M. C. Ferreira

Plastic Surgery Service, Sao Paulo University Medical School,

Sao Paulo, Brazil

J. Faintuch � C. M. Yamaguchi

Nutrition and Metabolism Unit, Sao Paulo University Medical

School, Sao Paulo, Brazil

H. Fujiwara � R. Curi

Institute of Biomedical Sciences, Sao Paulo University Medical

School, Sao Paulo, Brazil

J. Faintuch (&)

Hospital das Clinicas, II Surgical Division, Avenida Eneias

C. Aguiar 255- ICHC- 9th Floor, Room 9077, Sao Paulo,

SP 05403-900, Brazil

e-mail: jfaintuch@hcnet.usp.br

123

Aesth Plast Surg (2011) 35:789–794

DOI 10.1007/s00266-011-9688-x

Systemic inflammatory reactions in this context may be

divided into perioperative, early postoperative, and those in

the late follow-up period. During a few days immediately

after the operation inflammation is expected and can be

explained by surgical tissue damage itself, amplified or not

by hematoma, seroma, or bacterial contamination [8]. In

contrast, autoimmune diseases [1, 3, 5] were characteristi-

cally suspected in the past after an interval of years or even

decades. No study could be found about the clinical course

of inflammatory markers between these two extremes,

namely, during the early months after implantation.

In a prospective controlled protocol with young and

healthy women, C-reactive protein and other markers were

documented up to the sixth postoperative month. The

hypothesis was that even though modern products are

reputedly safe, reliable, and well-tolerated, systemic

inflammation might be elicited by these foreign bodies.

Patients and Methods

The project was approved by the Institutional Ethical

Committee and all participants gave written informed

consent. This was a prospective, controlled observational

clinical trial. Patients were seen on four occasions: (1)

preoperative assessment which included patient selection,

informed consent, clinical and biochemical assessment; (2)

perioperative period which included the surgical procedure,

complications, and conditions of discharge; (3) 2-month

follow-up which included evaluation of the operation and

biochemical tests; and (4) 6-month follow-up which

included evaluation of the same variables as the 60-day

follow-up, including autoantibodies.

Adult females who were candidates for breast augmen-

tation (index group) or for abdominal liposuction (controls)

were consecutively recruited. Criteria of inclusion were age

between 18 and 30 years old, BMI = 18.5-30 kg/m2, and

informed consent. Criteria of exclusion were previous

operation, burn, tumor, or radiotherapy in the anatomical

region, pregnancy or lactation, major disease (cancer, HIV/

AIDS, diabetes, hypertension, dyslipidemia, organ fail-

ures), rheumatologic or autoimmune conditions (lupus,

rheumatoid arthritis, dermatomyositis, scleroderma), use of

nonsteroidal anti-inflammatory drugs, corticosteroids, or

immune modulators, and refusal to participate in the study.

Eurosilicone Vertex textured implants were utilized

(Eurosilicone, Apt, France), with various shapes and sizes,

at the discretion of the responsible surgeon after discussion

with the patient. All of them exhibited layered shells

especially engineered to minimize rupture or leakage,

according to the manufacturer’s literature. The incision was

made in the inframammary fold and, conventionally, a

subglandular pocket was created. In four cases insufficient

glandular tissue was reported, so the submuscular (three

patients) or subfascial technique (one case) was employed.

Abdominal Liposuction

Targeted adiposity was in the lower abdomen, flanks, and

gluteal-trochanteric areas. Fluid was injected using the

tumescent technique, and fat was aspirated using a 3- or

4-mm cannula, according to the preference of the surgeon.

Compression garments were usually prescribed for

1 month.

General anesthesia was selected for both operations, and

patients were sent home after 24 h. An antibiotic (cepha-

lexin) was started 2 h before surgery and continued until

discharge.

Follow-up Routine

Demographic, nutritional, and clinical information was

collected, emphasizing criteria of inclusion and exclusion.

Diagnosis was based on current therapy, and the hospital

chart was scrutinized for confirmation. The surgical out-

come concerning aesthetic and general results (symmetry,

hematoma, fluid collection, hardness, pain, infection) and

rheumatologic complaints (fever, joint swelling, tender-

ness) were registered.

Biochemical Tests

The following inflammatory and coagulation/fibrinolysis

variables were considered at all times: white blood cell

count, C-reactive protein, complement fractions C3 and

C4, D-dimer, and fibrinogen. Rheumatoid factor, anticar-

diolipin antibodies (IgM, IgG), antinuclear and antimitoc-

hondrial antibodies, including anti-dsDNA and anti-Sm/

RNP, antiparietal cell, and anti-liver-kidney microsome

were measured after 6 months only.

Blood samples were collected the morning of the pro-

cedure, subsequent to overnight fast, and measured by a

modular analytical system (Roche/Hitachi Diagnostics, Sao

Paulo, Brazil). C-reactive protein was assayed by immu-

nonephelometry (Dade Behring, Sao Paulo, SP, Brazil),

and ELISA kits were selected for autoantibodies (Inova

Diagnostics, San Diego, CA, USA). The intra- and inter-

assay coefficients of variation did not exceed 6% for all

laboratory methods.

Statistical Analysis

Numerical results are presented as mean ± SD, and inter-

pretations along time were conducted by Student’s t test

and ANOVA, if necessary employing log conversion. The

percentage of autoantibody response was compared by v2

790 Aesth Plast Surg (2011) 35:789–794

123

analysis. Pearson or Spearman regression analysis was

selected for correlations of C-reactive protein, as appro-

priate. Significance was defined at 5% (p \ 0.05).

Results

A total of 52 patients were recruited (24 in Group I and 28

controls). Eight were eliminated (4 and 4, respectively)

because of criteria of inclusion and exclusion (4), incom-

plete follow-up (3), or pregnancy (1). The final numbers

were 20 in Group I and 24 controls.

All patients were successfully operated on, without

mortality. The mean volume of the breast prostheses was

258 ± 21 ml (range = 220-280) and the mean aspirated

volume in the course of liposuction was 1972 ± 499 ml

(range = 1200–3000). Perioperative troubles were limited

to one allergic reaction to the antibiotic cephalexin, which

was discontinued. No infectious or rheumatologic abnor-

mality was observed. When last examined, all mammary

implants were soft, painless, and cosmetically adequate.

Careful physical examination showed no evidence of rup-

ture, and only size was occasionally criticized as some

patients desired even larger breasts, but none of them

requested reoperation.

Table 1 lists the general characteristics of the two

populations. Groups were fairly well matched, though BMI

was somewhat higher in the liposuction candidates.

C-reactive protein was also numerically increased in this

population but without statistical significance. Though

liposuction involved more bleeding, the use of a vaso-

constrictor in the tumescent protocol was safe and effec-

tive. Operation time was comparable and blood transfusion

was not required.

General markers of coagulation and inflammation fluc-

tuated along time but changes were devoid of statistical

significance. Patients in the control group gained some

weight when last interviewed (p \ 0.019) (Table 2).

C-reactive protein strongly increased after 2 months in

patients who underwent breast enlargement (p = 0.001).

By 6 months values were still elevated, but significance

with respect to baseline was not reached because of wider

dispersion of the results, some returning to normal, others

further increasing (Fig. 1).

Anticardiolipin IgM was mildly elevated in 20.0% of

index patients and 8.0% of controls, and anticardiolipin

IgG in 15.0 and 16.0%, respectively, without significance.

One single case of borderline rheumatoid factor positivity

occurred in a control patient with normal C-reactive protein

(4.0%, 1/25). All other antibodies were negative.

Correlation of C-reactive protein with clinical and bio-

chemical findings in index patients highlighted an associ-

ation with operative time, prosthesis volume, and assorted

inflammatory and coagulatory indices. No significant

findings were present before operation. Interestingly, these

links remained robust even after 6 months, though eleva-

tion of C-reactive protein by that time was not statistically

confirmed (Table 3).

Table 1 Preliminary findingsVariable Mammary implant Liposuction Significance (p)

Age (years) 23.9 ± 3.9 25.9 ± 3.8 0.085

BMI (kg/m2) 21.2 ± 2.4 23.1 ± 1.6 0.021

Operative time (min) 62.8 ± 15.9 69.2 ± 18.9 0.229

Albumin (g/dl) 4.7 ± 0.4 4.7 ± 0.3 0.895

Hemoglobin (g/dl) 13.5 ± 0.9 12.8 ± 2.0 0.098

Glucose (mg/dl) 81.8 ± 7.7 81.0 ± 9.3 0.843

Creatinine (mg/dl) 0.7 ± 0.1 0.7 ± 0.1 0.735

C-reactive protein (mg/dl) 1.3 ± 1.2 3.5 ± 2.7 0.079

Table 2 Clinical course of inflammatory variables

Variable Preop 2 months 6 months

Mammary implant

WBC count (/mm3) 6.8 ± 1.2 7.5 ± 2.4 6.6 ± 1.4

C3 (mg/dl) 113 ± 28 119 ± 33 111 ± 17

C4 (mg/dl) 17.4 ± 4.8 18.1 ± 6.9 14.8 ± 2.0

D-dimer (mg/dl) 406 ± 210 532 ± 250 453 ± 187

Fibrinogen (mg/dl) 333 ± 85 330 ± 57 341 ± 58

BMI (kg/m2) 21.2 ± 2.4 21.7 ± 3.1 21.5 ± 3.2

Liposuction

WBC count (/mm3) 6.7 ± 1.2 6.9 ± 1.4 6.6 ± 1.0

C3 (mg/dl) 127 ± 27 121 ± 17 136 ± 37

C4 (mg/dl) 21.6 ± 5.9 21.3 ± 5.6 21.0 ± 9.3

D-dimer (mg/dl) 430 ± 222 441 ± 186 670 ± 371

Fibrinogen (mg/dl) 354 ± 86 399 ± 94 311 ± 61

BMI (kg/m2) 23.1 ± 1.6 23.3 ± 1.8 25.3 ± 1.9

Comparison along time and between groups failed to reveal statistical

differences, except for BMI in liposuction cases

WBC white blood cell count, CRP C-reactive protein, C3 complement

C3, C4 complement C4

Aesth Plast Surg (2011) 35:789–794 791

123

Discussion

Breast augmentation is one of the most common cosmetic

procedures in the United States and worldwide, with more

than 300,000 yearly interventions in the USA alone [9]. It

also involves the introduction of the largest amount of

foreign material inside the body of any surgical procedure

besides organ transplantation, up to 1000 cc or more.

Experimentally and clinically, a foreign body reaction

can be demonstrated, with mobilization of plasma proteins

and immuno-inflammatory cells encompassing neutrophils,

macrophages, and foreign body giant cells, followed by a

fibroblastic healing reaction [1, 3, 4]. Some defend that

since silicone is a hydrophobic elastomer, it is coated by

host proteins and blood clot after just a few hours. Naked

polymer surfaces would thus be largely shielded from

direct contact with antigen-responsive cells by a

comparably dense cellular and intercellular provisional

matrix. Tissue reaction occurs nonetheless, triggered by

mitogens, chemoattractants, cytokines, growth factors,

histamine, and other mediators, originating from the

crosstalk switchboard represented by the provisional matrix

[5, 10].

Capsule formation is part of the healing phase, and

indeed excessive or irregular collagen aggregation and

contraction is the most important long-term complication

of the intervention [6, 7]. The fibrous envelope that appears

in the ensuing weeks should not be construed as an

immunologic barrier. Even if no rupture occurs and sili-

cone bleeding into bodily tissues and fluids is prevented,

the foreign body reaction at the tissue-material interface

may continue for life [10].

Histology changes followed for up to 5 years have been

shown to include persistent accumulation and redeploy-

ment of inflammatory cells, suggesting a dynamic pattern

of scar synthesis, resorption, and remodeling. Silicone

particles are rarely embedded and may be associated with

severity of inflammation and capsular contracture, consis-

tent with a mild albeit chronic antigen-antibody reaction

[10–12].

Even metallic foreign bodies such as bone titanium

plates may elicit an inflammatory reaction [13], whereas no

comparable profile exists in wounds free from allogeneic

materials. In a study of conventional human scars of var-

ious sizes, types, and locations, including biopsy control, it

was demonstrated that redness faded by 7 months, and

12 months after operation no inflammatory cells were

detected by microscopic examination [14].

Tissue and cell response was out of the scope of this

clinical protocol, which addressed plasma markers only.

Indeed, routine capsule biopsy is not advised in the

implant-bearing population because of the risk of damag-

ing or puncturing the silicone shell. Only MRI examination

is suggested after the third year to search for silent ruptures

[7, 15].

Findings consistent with systemic inflammation were

present in the early postoperative months. C-reactive pro-

tein elevation was not a circumstantial or random finding,

as associations that were absent before operation robustly

suggested an integrated postoperative proinflammatory and

procoagulatory response. Not only relatively nonspecific

correlations were demonstrated, such as with coagulation/

fibrinolysis indices, but also with prosthesis volume itself

at the 6-month assessment when perioperative trauma

could no longer be invoked. Autoantibody synthesis was

not elicited, though a moderately increased risk for con-

nective tissue disease should not be entirely ruled out [15].

Use of liposuction controls might be criticized as non-

neutral because in experimental animals, release of cyto-

kines and other inflammatory mediators has been seen after

Fig. 1 Evolution of C-reactive protein. When baseline, 2 months,

and 6 months were compared, findings for breast implant patients

were 1.3 ± 1.2, 4.8 ± 3.0, and 4.3 ± 6.4 mg/l, respectively, whereas

corresponding values for liposuction patients were 3.5 ± 2.7,

3.5 ± 2.1, and 2.2 ± 2.2 mg/l. Elevation of CRP after 2 months in

implant patients was significant (p = 0.001)

Table 3 Postoperative correlations of C-reactive protein after breast

augmentation

Variable ‘‘r’’ correlation index Significance (p)

Two months

Operation time 0.445 0.049

White blood cell count 0.716 \0.001

Fibrinogen 0.606 0.005

C4 complement fraction 0.572 0.008

Six months

Prosthesis volume 0.543 0.014

White blood cell count 0.557 0.010

Fibrinogen 0.849 \0.001

D-dimer 0.804 \0.001

Only statistically significant findings are shown; no correlation with

C-reactive protein occurred before operation

792 Aesth Plast Surg (2011) 35:789–794

123

certain adipose tissue manipulations, particularly ultra-

sound lipoclasia [16]. Nevertheless, there is no reason to

believe that human liposuction is followed by a similar

phenomenon beyond the immediate perioperative period

[17]. Should any degree of activation exist, the current

statistical difference would become more, not less,

meaningful.

The biochemical profile was independent of cosmetic

and technical results, which were fully rewarding without

changes in breast contour and softness or physical evidence

of rupture during the observation period. Nevertheless, the

acute phase response could signal mild silicone immuno-

genicity and future capsular contracture. C-reactive protein

is a classic index of graft rejection subsequent to organ

transplantation [18] and might be associated with abnor-

malities following breast prostheses implantation.

In light of the conspicuous technical improvement

achieved with modern cohesive gel implants, along with

absolution of silicone from major autoimmune reactions

and rheumatologic diseases of which it was accused in the

past [3–7], inflammatory follow-up of operated patients has

been deemed unimportant and is mostly lacking in the

literature. Current circumstances suggest that high-sensi-

tivity C-reactive protein, cytokines, chemokines, and

adhesion molecules are worthy targets for future investi-

gations. Emphasis should be placed on biochemical/histo-

logical correlation whenever feasible, along with magnetic

resonance, Baker classification, and long-term clinical

complaints [5, 7, 10, 12].

Some clinical differences between patients and controls

should be acknowledged, despite strict adherence to criteria

of inclusion and exclusion. Such discrepancies should be

attributed to the intrinsic variability of surgical candidates,

even if young, healthy, and nonobese as in the current

circumstances. Also, the procedures were not identical,

though they involved similar duration, anesthesia use, and

hospitalization period. Only one study could be found that

compared silicone breast implant surgery with other sur-

gical maneuvers, and exclusively from the point of view of

wound healing. The authors opted to utilize controls

undergoing more disparate interventions performed

80 years earlier [19].

In synthesis, this is the first prospective controlled study

to our knowledge that demonstrated ongoing systemic

inflammation after modern augmentation mammaplasty.

Few clues exist about the outlook of this aberration, which,

as alluded to, requires further studies in larger populations.

It might simply vanish after months or years as a result of

immune tolerance. A highly unlikely hypothesis is pro-

gression toward a chronic and symptomatic condition,

mimicking connective tissue disorders. Another possibility

could be envisaged, namely, a silent clinical course anal-

ogous to such chronic endogenous troubles as diabetes,

obesity, and liver steatosis [20, 21], or perhaps to chronic

implant or transplant rejection.

Admittedly, surface physical and chemical properties

impact the immuno-inflammatory response, including cell

adhesion, biomolecule secretion, and fibroblast prolifera-

tion. In this sense, further studies focusing on implants with

different external architectures should be encouraged [10,

22]. Polyurethane-covered implants, which are popular in

several parts of the world and have not been investigated

with respect to systemic inflammation, should be one of the

priorities. In the current protocol a single brand of textured

products was used, rendering it important to focus on

additional surfaces, coatings, and finishes.

Disclosures None.

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