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Surgery: Current Research
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Using Breast MRI to Evaluate Complications of Autologous Fat Grafting

Li-Kuo Shen1, Shoei-Loong Lin2, Cheuk-Sing Choy3, Wing P Chan4, Mimmo Gasbarri5 and Ting-Kai Leung4,6*

1Department of Radiology, Shuang Ho Hospital, Taipei Medical University, New Taipei City 235, Taiwan

2Department of Surgery, Taipei Hospital, Ministry of health and Welfare, Taiwan., R.O.C and Department of Surgery, School of Medicine, College of Medicine, Taipei Medical University, Taiwan

3Department of Emergency and Intensive Care, Taipei Hospital, Department of Health, Taiwan

4Department of Radiology, School of Medicine, College of Medicine, Taipei Medical University and Department of Radiology, Wan Fang Hospital, Taipei Medical University, Taiwan

5Dept. of Natural Health Studies / London College of Training & Management, London, UK

6Diagnostic Radiology Department, Taipei Hospital, Ministry of Health and Welfare, Taiwan

*Corresponding Author:
Ting-Kai Leung
Department of Emergency and Intensive Care
Taipei Hospital, Department of Health, Taiwan
Tel: 886982802149
E-mail: [email protected]

Received date: February 22, 2014; Accepted date: June 26, 2014; Published date: June 28, 2014

Citation: Shen LK, Lin SL, Choy CS, Chan WP, Gasbarri M, et al. (2014) Using Breast MRI to Evaluate Complications of Autologous Fat Grafting. Surgery Curr Res 4:197. doi:10.4172/2161-1076.1000197

Copyright: © 2014 Shen LK, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract

Introduction: During the past few years in Taiwan, there has been a rapid growth of autologous fat grafting procedures performed for cosmetic reasons. We retrospectively demonstrate Complications of Autologous Fat Grafting in the breast, based on clinical presentations and breast MRI imaging. We also discuss the possible method of early detection of complications. Material and method: Twenty-one ethnic Chinese (Taiwanese) women were transferred for delicate breast MRI study in the past year. These patients had suffered different signs and symptoms following the procedure. Clinical and image information were collected from the hospital database. Results: Breast MRI successfully detected all viable fat tissues and complicated lesions of the breasts. The image findings corresponded to the clinical presentation and were used in therapeutic decision making. Fat necrosis with granuloma formations caused by graft rejection was the main complications. The most severe complication was an abscess formation and impending sepsis. Management procedures included operation or drainage; received oral antibiotics; and received clinical observation. Discussion and Conclusion: MRI is capable of detecting the surviving fat graft tissues, and to distinguish degree of malignancy from benign lesions. In complicated cases, the highest incidences showed granuloma formations and fat necrosis. However, laboratory data such as CRP, IgE and complement (C3 &C4) levels only reflected some of the infectious cases and could not be used as monitoring parameters. Breast MRI is an ideal tool for early detection of autologous fat complications without causing indistinguishable conclusions from malignancy. Breast MRI should be performed as early as possible for this complication, so that help for early treatment can be planned.

Keywords

Breast MRI; Autologous fat graft; Survive; Abscess formation; Fat necrosis; Rejection; Complication

Introduction

Autologous fat grafting is a technique that involves using the patient’s own adipose tissue to be applied on a subcutaneous area of the body to increase total fat volume [1-3]. Breast augmentation using autologous fat grafting is not associated with implant related problems such as implant leakage, breast deflation, visible or palpable implants, or the development of breast capsular contracture. Regarding successful cases of autologous fat grafting, under the condition of suspected tumor growth, a usual biopsy procedure can be performed without risk of a stabbing rupture of the implanted materials. However, autologous fat grafting in the breast is not a simple procedure and should be performed by highly trained and skilled surgeons. The recipient of autologous fat grafting is at risk of intraoperative pneumothorax, calcification, multiple cyst formation [4], focal breast indurations, pain, infection, and abscesses [5], abnormal breast discharge, and reactive lymphadenopathy. In contrast to the aforementioned successful cases, these patients require life-long follow up for breast cancer screening because of the difficulty of cancer detection. These patients should also undergo long-term imaging analyses [6,7]. Autologous fat grafts are also believed to have the disadvantage of the unpredictability graft tissue survival because of fat necrosis and re-absorption [8]. The incidence of calcifications (mostly due to fat necrosis) after all types of breast operations varies, but has been reported in as many as 50 percent of patients within 2 years [9].

It was also reported that breast asymmetrical densities were present in approximately half of patients throughout the follow-up period of post-mammoplasty. In additions, fat necrosis occurred in approximately one tenth of the patients [9]. Many plastic surgeons have rejected fat grafting in the breast because of the speculation that transplanted fat might undergo necrosis or die off gradually, forming lumps or calcifications. Fat grafting raises the concern of interfering with breast cancer detection. In fact, injecting small volumes of fat produces microcalcifications, which can be indistinguishable from carcinomas in mammograms; whereas injecting larger volumes might result in the liponecrotic pseudocyst formation that can interfere with physical breast examination and cause a growing and painful mass [10,11]. Regarding breast image screening and diagnosis for such patients, mammography is favored by radiologists to differentiate cancer microcalcifications from benign calcifications of the breast. However, most cosmetic mammoplasty patients are among the young age group that should receive non-ionized radiation screening of breast tissues. Therefore, the first line screening for this age group is usually sonography, but the sensitivity and specificity of sonography to differentiate calcification and microcalcifications is not reliable [12]. Breast MRI should be considered a first line screening tool or at least used when clinical suspicion or radiographic abnormality is indeterminate.

Breast MRI has also been reported to be more capable than mammography of early detection of fat necrosis and clinically nondetectable masses and nodules, although MRI is not used to detect calcifications or microcalcifications [13].

During the past 2 years in Taiwan, there has been a rapid growth of autologous fat grafting procedures performed for cosmetic reasons. In this study, we demonstrate cases of autologous fat grafting in the breast, including complications, based on clinical presentations and breast MRI imaging. We also discuss the possible method of early detection of the Complications of Autologous Fat Grafting of the breast.

Materials and Methods

Cases collections

From March 2011 to February 2012, twenty-one ethnic Chinese (Taiwanese) women were transferred to the Breast Health Center (Taipei Medical University Hospital) for delicate breast MRI study. These patients exhibited different symptoms and signs after the procedure. Clinical and image information were collected between March 2011and February 2012 from the hospital database. The patients were between 25 and 62 years old, and none had undergone treatment in the period between mammoplasty and breast MRI study. Furthermore, information collected and recorded included clinical expression, laboratory data such as Immunoglobulin E (IgE), Antinuclear Antibodies (ANA), complement (C3&C4), C-Reactive Protein (CRP), antinuclear antibodies (ANA), monocyte and bacteria culture, as well as the possible pathological diagnosis and method of treatment.

Image processing using delicate breast MRI

Pre-enhanced and post-enhanced subtracted images were obtained, and an enhanced curve analysis was performed. All imaging studies were performed on a 1.5 T dedicated spiral breast MRI system (Aurora Systems, USA) [14-17]. The breasts were fitted and positioned using a breast transmission–receiving (TR) coil. The off-resonance spiral image mode was used. A gradient echo with 10 ms of TR and T2-weighted spin echo with 2.5 ms of TR were acquired. The echo time was 5 ms for RODEO and 120 ms for the T2 sequences. The volumetric matrix size was 360x360x128 mm. The slice thickness was 1.1 mm. The field of view of each station was 20–36 cm. Sequences were performed before and after the infusion of 0.2 mmol/kg adolinium-diethylenetriamine pentaacetic acid (Magnevist; Bayer-Schering Pharma AG, Berlin, Germany), administered as a bolus dose with a power injector, followed by a 20-mL saline flush. Subtraction images were also performed [14-17].

Results

According to our data on these 21 patients (Table 1), the complications may have developed 12 days to 24 months later after autologous fat grafting, including infection, granuloma, and fibrotic change [18-20]. The mean of duration that represent for MRI image diagnosis was 8.1 months. All of the patients suffered from breast tenderness, palpable lumps, pain or fever. The most severe complication was immediate post-operative abscess formation and impending sepsis. All of the cases were diagnosed with fat necrosis and granuloma formations caused by fail of graft tissue survival or graft rejection. Serum test for two of the patients were exhibited CRP elevation, and serum test for IgE was also found elevated in another 3 patients. Among these 21 cases, 19% required operation or incisional drainage; 23.8% received oral antibiotics for conservative treatment; and 57.1% of the cases were suggested for observation after image diagnosis. Based on the MRI images (Figures 1-21), all of the fat grafted tissue from the 21 cases could be identified, even Case 4, who received the procedure for over 2 years. According to the pictures of breast MRI, no case revealed a lesion indistinguishable from malignancy that required additional biopsy.

Case No. Age Period of autologous fat graft Symptoms and signs Image findings on MRI Visibility  of grafted fat Laboratory data Clinical or pathological diagnosis Treatment
Case 1
(Figure 1)
35 12days Pain and fever (1)Right breast enhanced cavities
(2)Ipsilateral lymphadenopathy (>2cm)
Yes (1) Anemia (1) Abscess Operation and drainage
(2) Significant CRP elevation (2) Impending sepsis
(3) Bacterial culture:Candidaalbicans isolated  
Case 2
(Figure 2)
30 4months Right breast tenderness with lump (1)Multiple granulomas and abscess formation at deep superior
andsubareolar region of right breast. The largest one is over 3.2cm.
Yes (1) IgE elevation Mastitis and granulomatous formation Operation and drainage
(2) Monocyte increase
(2)Mild inflammation of pectoral
major muscle.
(3) CRP normal
(4) Bacterial Culture: No growth
Case 3(Figure 3) 27 3months Tenderness at bilateral sides (1) Diffuse granuloma formations , pockets of thick wall pockets with varioussizes, within glandular tissues of bilateral breasts.Suggest process of fat necrosis and non-infectious inflammatory process Yes Nil Mastitis and granulomatous formation Observation
(2)Nonspecific enlarged LNs at bilateral breast axillary regions.
Case 4
(Figure 4)
51 24months (1) Tenderness at bilateral sides (1)Multiple small ill defined encapsulate fat masses, most of the
masses exhibit wall enhancement.
Yes Nil Mastitis and granulomatous formation Oral Antibiotics
(2) Middle chest pain
(2)Focal inflammatory lesion at anterior of sternum, with 1.8cm.
(3)Non specific reactive axillary LNs.
Case 5
(Figure 5)
25 8months Palpable lumps at superior of right breast and medial of left breast 1) Diffuse granuloma formations , pockets of thick wall pockets with various Yes Nil Mastitis and granulomatous formation Observation
sizes, within glandular tissues of bilateral breasts.
Suggest process of fat necrosis and non-infectious inflammatory process
(2)Nonspecific enlarged LNs at bilateral breast axillary region.
Case 6
(Figure 6)
44 1months Palpable lumps at superior of right breast (1)Multiple granulomas like masses at right breast. Suggest ongoing process of inflammation with fat necrosis, Yes Nil Mastitis and granulomatous formation Oral Antibiotics
(2) Possibility ofmild infection is also considered.
Case 7
(Figure 7)
26 12months Palpable lumps (1)Multiple granulomas like masses at bilateral breasts. Yes (1) IgE elevation Mastitis and granulomatous formation Observation
(2)Obvious abnormal LNs(>1.5cm, dense) at bilateral breasts axillary regions. (2) Antinuclear Antibodies (ANA): 1:40 (elevation)
(3) Significant (complement,C4) :elevation
(4) Normal CRP
Case 8
(Figure 8)
62 12months Palpable lumps at right breast (1) Right breast mass; and other smaller nodular lesions in bilateral breasts Yes Nil Mastitis and granulomatous formation Operation
(2) Probably chronic inflammation due to fat grafting induced granuloma formations
Case 9
(Figure 9)
36 6months Inferior lump at right; Bilateral medial pain for 2 weeks (1)granulomas and Yes Nil Mastitis and granulomatous formation Oral Antibiotics
fat necrosis.
(2)Suspect status of inflammatory infectious or noninfectious
mastitis at right breast.
Case 10
(Figure 10)
35 6months Bilateral chest pain after movements, for 1 months (1)Fat grafted cavities at bilateral sides of subglandular regions. (2)Fluid content at left side fat grafted cavities. (3)Some pockets with fluid at inferior of left breast. (4)Post GD enhanced glandular tissues at left anterior and bilateral of breast. Yes (1) white cell count: normal Mastitis ; acute stage fat necrosis with  granuloma formations Operation and aspiration
(2) CRP: normal
(3) IgE: normal
(4) Complements(C3&C4): normal
Case 11
(Figure 11)
35 9months Bilateral breast pain after 2 months of fat grafts (1)Fat grafted pockets in bilateral sides(one at Rt side and several
at left side) of subglandular regions.
Yes (1) White cell count: normal, but neutrophil predominate(>75%) Fat necrosis Oral antibiotics
(2) CRP: elevation Infectious mastitis
(2)Minimal fluid content within left side fat grafted pocket. (3) IgE: normal  
(4) Complements(C3&C4): normal  
3)Enhanced area at left side subareolar region
Case 12
(Figure 12)
37 7 months Palpable lumps without pain (1)Post fat grafted and fat necrosis, with cavities within
inferior of right  breast.
Yes (1)White cell count: normal, but neutrophil predominate(>75%) Fat necrosis Observation
(2)CRP: normal Non-infectious mastitis
(2) Enhanced area at left side (3)IgE: normal
(4)Complements(C3&C4): normal
Case 13
(Figure 13)
54 18 months Palpable lumps without pain Post fat grafted and fat necrosis, with cavities(like honeycomb) at subglandular of right  breast. Yes Nil Fat necrosis Observation
Case 14
(Figure 14)
31 10 months Palpable lumps without pain, at right breast Enhanced area at right side and reactive lymphadenoapthy Yes (1)White cell count: normal Non-infectious mastitis Observation
(2)CRP: normal
(3)IgE: slightly elevation
(4)Complements(C3&C4): normal
Case 15
(Figure 15)
39 13 months Palpable lumps without pain, at right breast Enhanced area at right side and reactive lymphadenoapthy Yes (1)White cell count: normal Non-infectious mastitis Observation
(2)CRP: normal
(3)IgE: normal
(4)Complements(C3&C4): normal
Case 16
(Figure 16)
56 5 months Palpable lumps without pain, at bilateral breasts Fat necrosis, with cavities within
bilateral breasts. Enhanced lesion at deep of left breast
Yes (1)White cell count: normal Non-infectious mastitis Observation
(2)CRP: normal
(3)IgE: remarkable elevation
(4)Complements(C3&C4): normal
Case 17
(Figure 17)
53 4 months Palpable lumps without pain, at bilateral breasts There are multiple fat grafted cavities at bil sides of subglandular
Regions, with rim
enhancements and fluid like signal intensity.
Yes (1)White cell count: normal Non-infectious mastitis Observation
(2)CRP: normal
(3)IgE: remarkableelevation
(4)Complements(C3&C4): normal
Case 18
(Figure 18)
24 11 months Palpable lump at peri-areolar of Lt breast Focal enhanced non-mass lesion with irregular border, at subcutaneous skin at anterior lateral inferior of Lt breast.
No extensive fat necrosis.
Yes (1)White cell count: normal Non-infectious mastitis Observation
(2)CRP: normal
(3)IgE: normal
(4)Complements(C3 ): slightlyelevation
Case 19
(Figure 19)
30 7 months Palpable lumps without pain, at bilateral breasts Multiple fat grafted cavities at superior lateral of bilateral breasts. Yes Nil Fat necrosis with  granuloma formations Observation
Case 20
(Figure 20)
31 3 months Palpable lumps with pain for 2 months, at bilateral breasts Areas of enhancement with impending
abscess formations at superior
lateral of right breast
Yes (1) Anaerobic Culture Mastitis, minimal abscess Oral Antibiotics
(2) Aerobic Culture
Case 21
(Figure 21)
45 6 months Pain for 2 months and no lump Reactive lymphadenitis at bilateral axillary regions Yes Nil Non-infectious mastitis Observation

Table 1: Clinical presentation, image finding and treatment of the patients.

surgery-current-research-inflammation

Figure 1a: An abscess formation at the lateral of the right breast, associate with generalized cellulitis and glandular inflammation, including the pectoral major muscle. Subtract image further rule out the possibility of malignancy. b: Multiple reactive >2.0 cm axillary lymph nodes.

surgery-current-research-granulomas

Figure 2: Multiple granulomas and abscess formation at deep superior and subareolar region of the right breast. The largest is over 3.2 cm, with a mild inflammation of the pectoral major muscle.

surgery-current-research-glandular

Figure 3: Thick wall pockets of various sizes within glandular tissues of the left breast. On color mapping, there are showed in different color areas represents minimal fluid, fat, protein components.

surgery-current-research-inflammatory

Figure 4: Focal inflammatory lesion at anterior of sternum.

surgery-current-research-encapsulated

Figure 5: Multiple, large and small, ill-defined encapsulated fat masses, most of which exhibit wall enhancement.

surgery-current-research-subglandular

Figure 6: Multiple granuloma-like masses at the subglandular of the right breast. The largest mass (3.0 cm) exhibits wall enhancement with semifluid and semi-fat content.

surgery-current-research-granuloma

Figure 7: Small solid granuloma-like masses at right breast.

surgery-current-research-heterogenous

Figure 8: Ill-defined heterogenous enhanced masses at the superior lateral of the right breast ,with wall enhancement.

surgery-current-research-bilateral

Figure 9: Multiple granulomas and fat masses at deep inferior of bilateral breasts.

surgery-current-research-subglandular

Figure 10: Fat grafted cavities at bilateral sides of subglandular regions. Some pockets with fluid at inferior of left breast. There are also enhanced glandular tissues at left anterior and bilateral lateral of breasts, represent mastitis.

surgery-current-research-subglandular

Figure 11: Multiple thick wall enhanced pockets with minimal fluid at inferior of left breast. There are also enhanced glandular tissues at left anterior and bilateral lateral of breasts, represent mastitis.

surgery-current-research-necrosis

Figure 12: Post fat grafted and fat necrosis, with cavities within inferior of right breast (left figure); and enhanced area at left breast (right figure).

surgery-current-research-honeycomb

Figure 13: Honeycomb appearance at subglandular of right breast.

surgery-current-research-lymphadenopathy

Figure 14: Post GD enhanced mastitis area (black thick arrow) at right breast with and reactive lymphadenopathy (thin white arrow).

surgery-current-research-autologous

Figure 15: Subglandular autologous fat graft, with enhanced area at medial of left breast (red color).

surgery-current-research-grafted

Figure 16: Post grafted fat necrosis at right breast (thick arrow); and enhanced area at left breast (thin arrow).

surgery-current-research-intensity

Figure 17: Fat necrosis, with cavities within left breast, with fluid like signal intensity.

surgery-current-research-enhancement

Figure 18: Focal patch form of non-mass lesion at left breast(circle) with obvious enhancement.

surgery-current-research-bilateral

Figure 19: Post grafted fat necrosis at superior lateral of bilateral breasts (circles).

surgery-current-research-bilateral

Figure 20: Area of mastitis with impending abscess formations at superior lateral of right breast.

surgery-current-research-nonspecific

Figure 21: Nonspecific enhanced LNs in bil axillary regions.

Discussion

There are two issues to discuss. Firstly, is that complications of the fat graft can be detected and survived; secondly is breast MRI is capable to distinguish malignancy from benign lesions. In early 2007, Kaufman MR et al reported no evidence of the post autologous fat grafting fat survivability and the predictability of volume restoration. In conducting a quantitative study using large-scale clinical assessment and three-dimensional volumetric imaging to provide useful outcome data, they found that fat survival of autologous fat graft in that period is questionable [21]. By contrast, a rapid growth of new procedures used to collect larger amounts of transplantable fatty tissue by using liposuction (e.g., water-assisted liposuction); and the procedure of autologous lipo-transplantation after tissue separations. By conducting a series of procedures that focus on the superfluous water, fat purification, and centrifugation, the viable fat tissue could then be harvested [22,23]. Smith et al. using breast MRI to compare the image morphological change of fat grafted breasts before and after using this type of improved technique in operations [22]. They found that 41.1% of the studied patients exhibited a significant volume increase of grafted fat within the treated areas. The average size of increase was approximately 100-150 ml. Approximately 2.4% patients developed palpable subcutaneous nodules which finally proved to be granulomas [22]. For these cases that developed complications, the pathologic results for the excised granulomas, included fat necrosis, calcification, hyalinization, and fibroplasia [24]. Our observations support the results of these previous studies, in that the complication rate of granuloma formation (a complex of chronic inflammation with fat necrosis), is ahead of infection and mastitis. Therefore, granuloma formations due chronic inflammation of fat tissues, acted as the leading complication type in autologous graft breasts.

Granulomatous formation is caused by the failed attempts of the human immune system to eliminate foreign substances. Granulomas are seen in various diseases that relate to both infectious and noninfectious [25-27]. Granulomatous formation is a type of inflammation, with an important feature that it may contain necrosis. The identification of necrosis in granulomas is important because granulomas with necrosis tend to have infectious causes. However, in most of our cases with granulomatous formations that were associated with fat necrosis, infection did not occur. Fat necrosis has been reported in many different surgical procedures, such as reduction mammoplasty, mastectomy and post reconstructive procedures and others [28-35]. It was also shown that some over-obese animals are predisposed to fat necrosis without trauma and surgical inductions [36,37].

The mechanism of post-operative fat necrosis is still poorly understood but a variety of factors are thought to be some of the causes, such as direct trauma, infection, avascularity, hypoperfusion and lipolytic enzymatic digestion [36-39]. To compare the image features of granulomas under mammography, sonography and breast MRI, it was found the typical mammographic pictures of granulomas as asymmetrical focal densities with no distinct margins, ill-defined masses with spiculated contours, and bilateral multiple ill-defined nodules were seen [40]. Under sonography, granulomas may appear as nonspecific discrete or heterogenous hypoechoic masses [38-40]. Thus, the mammography and sonography may not provide a conclusive result for determination of the necessity of surgical treatment, or to rule out malignancy [38]. It was believed that a major part of autologous fat injection for breast augmentation would not survive due to the associated physiological response of fat to succumb to necrosis and then lead to scarring and calcification. Under mammography, the clusters of microcalcifications in the breast may be observed but cannot be distinguished from malignant calcifications. A common biopsy or a biopsy using mammographically guided needle localization is needed [39,40].

On our dynamic breast MRI, the survival of fat grafted tissues can be qualitatively observed and quantitatively measured. Also, the most frequent finding of complication was focal or diffusely asymmetrical signal intensity changes with fluid or semi-fluid content, without significant mass effect. Nodular lesions, mass-like enhancement, ringlike enhancement, and nodular enhancement were observed. Although, most of the dynamic curves of post-gadolinium enhancement did not have characteristic findings, but based on the morphology and subtracted image, malignancy could be ruled out. From our result, we found four cases that had received operation, drainage or aspiration, but only five cases had higher levels of one or more than one of the following items: CRP, IgE or complement (C4) /ANA. We found the laboratory data are not able to predict all the corresponding post fat grafting infection and rejection with granuloma formations. It supports our contention that breast MRI should acting as first line screening method for early diagnosis and for treatment.

Conclusion

This is a study of using breast MRI to evaluate the conditions of post autologous fat grafting complications. Chronic inflammation with granuloma formations and fat necrosis has the highest incidence rate; we also found acute infection with abscess is the most urgent condition. Overall, 19% of the cases suffering complications had need of an additional operative treatment. Serum test for laboratory data should not be independently used as monitoring parameter for early detection of fat necrosis, granulomatous mastitis or abscess. However, breast MRI is a reliable imaging tool for precise diagnosis on the fat survival, fat necrosis, and other complications.

Acknowledgement

This study is funded by Taipei Medical University & Shuang Ho Hospital (Project Number: 101TMU-SHH-22).The authors are grateful to Dr. Pai-Jung Huang and Ms. Jinnia Tsai (AUROA, ASIA) for their dedicated assistance.

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