BREAST

Fat Necrosis in Autologous Abdomen-Based Breast Reconstruction: A Systematic Review

Ibrahim Khansa, M.D. Adeyiza O. Momoh, M.D. Priti P. Patel, M.D. John T. Nguyen, M.D. Michael J. Miller, M.D. Bernard T. Lee, M.D., M.B.A.
Columbus, Ohio; Ann Arbor, Mich.; and Boston, Mass.

Background: Fat necrosis is a common and potentially exasperating complication of autologous breast reconstruction. The authors performed a systematic review of the English literature on autologous breast reconstruction to determine significant patient and surgical factors that are predictors of postoperative fat necrosis. Methods: A PubMed search using the terms fat necrosis and breast reconstruction was conducted. Articles were screened using predetermined inclusion and exclusion criteria. Data collected included patient characteristics, reconstructive techniques used, and the specific postoperative morbidity of interest. Patient cohorts were pooled, and the incidence of fat necrosis was calculated in the presence and absence of each risk factor. Chi-square analysis was applied, and p 0.05 was considered statistically significant. Results: Of 172 articles found, 70 met the inclusion criteria. The mean rate of fat necrosis was 11.3 percent. Deep inferior epigastric artery perforator flaps had the highest rate of fat necrosis (14.4 percent), followed by pedicled transverse rectus abdominis musculocutaneous (12.3 percent), superficial inferior epigastric artery (8.1 percent), and free transverse rectus abdominis musculocutaneous flaps (6.9 percent). Significant predictors of fat necrosis included obesity (p 0.035), prereconstruction irradiation (p 0.022), postreconstruction irradiation (p 0.001), active smoking (p 0.001), and abdominal scars (p 0.05). Protective factors included supercharging (p 0.001) and bilateral reconstruction (p 0.01). Conclusions: Although there is little agreement in the literature regarding risk factors for fat necrosis, the authors were able to demonstrate several significant predictors by systematically analyzing 70 articles. Improved knowledge of the risk factors for fat necrosis can help surgeons provide improved preoperative counseling and take measures to minimize the risk of this complication. (Plast. Reconstr. Surg. 131: 443, 2013.)

at necrosis is a common complication in autologous breast reconstruction. It presents as a nodule or mass that can be palpated after reconstruction.1 It is caused by ischemia of the subcutaneous adipose tissue, leading to adipose cell necrosis, scarring, and sometimes calcification. Although fat necrosis is not inherently dangerous, it can mimic breast cancer recurrence
From the Department of Plastic Surgery, The Ohio State University Wexner Medical Center; the Department of Surgery, Division of Plastic and Reconstructive Surgery, University of Michigan Medical Center; and the Department of Surgery, Division of Plastic and Reconstructive Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School. Received for publication July 18, 2012; accepted September 12, 2012. Copyright 2013 by the American Society of Plastic Surgeons DOI: 10.1097/PRS.0b013e31827c6dc2

both clinically and radiographically. Clinically, it may feel benign when it consists of a smooth round nodule, but it can be an irregular, fixed mass with skin retraction.1 On mammography, it can appear as an irregular density, spiculated mass, or microcalcifications.2 When it mimics cancer recurrence, fat necrosis can lead to patient anxiety and additional biopsies.3 Fat necrosis can also negatively affect cosmetic outcome by causing distortion of the reconstructed breast. There is no uniform definition of fat necrosis in the literature. The most commonly used defi-

Disclosure: The authors have no financial interests in this research project or in any of the techniques or equipment used in this study. The authors have no conflicts of interest to disclose.

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nition is that of a palpable subcutaneous firmness not due to cancer.4 Other authors define fat necrosis based on size, with some using firmness measuring 1 cm in diameter3 and others placing the size threshold at 2 cm.5 A less commonly used definition of fat necrosis is radiologic, and defines it as an ultrasound-detectable lesion greater than 5 mm.6 Reported rates of fat necrosis vary widely, from 3.04 to 37.9 percent.7 Although some risk factors for fat necrosis are consistent in the literature, others such as obesity, irradiation, and abdominal scars are the subject of debate. Two studies have systematically examined fat necrosis in autologous breast reconstruction. Man et al. conducted a meta-analysis of 36 studies,8 and Sailon et al. conducted a systematic review of eight studies.9 Both reviews included only free transverse rectus abdominis musculocutaneous (TRAM) and deep inferior epigastric artery perforator (DIEP) flaps, and did not specifically examine risk factors for fat necrosis. The only risk factor analyzed was flap type, with both studies concluding that the rate of fat necrosis was higher in DIEP flaps than in free TRAM flaps. In this systematic review, our objectives were (1) to calculate the overall rate of fat necrosis in abdomen-based autologous breast reconstruction, including pedicled TRAM, free TRAM, DIEP, and superficial inferior epigastric artery (SIEA) flaps; and (2) to identify potential predictors of fat necrosis, including flap type, obesity, irradiation, smoking, abdominal scars, recipient vessel selection, surgical delay, supercharging, and laterality of reconstruction. were excluded, yielding 70 articles suitable for analysis (Fig. 1). Data Extraction For each article, we extracted the data listed in Table 1. Not all data were available in every article. The fat necrosis risk factors analyzed were flap type, obesity, irradiation (prereconstruction or postreconstruction), smoking (former or current), abdominal scars, recipient vessel, surgical delay, supercharging, and laterality. The flap types included were pedicled TRAM, free TRAM, DIEP, and SIEA flaps. We excluded less commonly used flaps (e.g., superior gluteal artery perforator flaps) because of a scarcity of data. Latissimus dorsi flaps were excluded, as few articles measured fat necrosis rates. Data Analysis and Statistics When two or more articles from the same institution had overlapping data collection dates, they were assumed to be from the same cohort. When computing the overall rate of fat necrosis, the article with the largest number of patients was included, and redundant articles were excluded. However, some of the redundant articles analyzed distinct predictors of fat necrosis, and those were included in the analysis of individual fat necrosis predictors. All articles that contained extractable data related to potential risk factors were used. The data were pooled, and the number of flaps with fat necrosis was computed in the presence and absence of that risk factor. A chi-square test was applied, with values of p 0.05 signifying statistical significance.

MATERIALS AND METHODS

Literature Search A PubMed database search was conducted in March of 2011 using the terms fat necrosis and breast reconstruction as key words to identify studies in the English language published between 1982 and 2011. The articles were examined, and references were screened for further relevant articles. The search yielded a total of 172 citations. Inclusion criteria were English-language publication, human subjects, autologous breast reconstruction, extractable outcomes on fat necrosis, and full-text availability. Exclusion criteria were systematic reviews and meta-analyses, case reports and case series with fewer than 15 patients, nonconsecutive cases, reconstructions that included expanders or implants, and reconstructions that included fat grafting. One hundred two studies

RESULTS
Overall Rate of Fat Necrosis Forty-one articles3,5,6,10 47 described distinct patient cohorts and were included in computation of the overall rate of fat necrosis. Those represented a total of 10,764 flaps in 8970 patients; 1212 flaps had fat necrosis, for an overall rate of 11.3 percent. Flap Type Thirty-three articles3,6,7,20 49 representing 7233 flaps in 6394 patients analyzed the rate of fat necrosis by flap type (Table 2). The overall rate of fat necrosis was 11.1 percent. DIEP flaps had a significantly higher rate of fat necrosis (14.4 percent) than free TRAM (6.9 percent, p 0.001), pedicled TRAM (12.3 percent, p 0.04), and SIEA flaps (8.1 percent, p 0.02).

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Fig. 1. Study attrition diagram.

Free TRAM flaps had the lowest rate of fat necrosis (6.9 percent), which was significant in comparison with pedicled TRAM (p 0.001) and DIEP flaps (p 0.001). Obesity Five articles45 47,50,51 representing 1741 flaps in 1592 patients analyzed the rate of fat necrosis depending on body mass index (Table 3). The rate of fat necrosis in obese patients (body mass index 30) was 12.6 percent, significantly higher than normal weight (body mass index 25, 7.8 percent; p 0.009) and nonobese patients (body mass index 30, 8.7 percent; p 0.035). Fat necrosis was also nonsignificantly higher in obese patients than in overweight patients (body mass index 25 and 30, 12.6 percent versus 8.7 percent; nonsignificant). Fat necrosis was more common in obese patients than in normal weight patients receiving a pedicled TRAM flap (15.4 percent versus 9 percent, p 0.02) but not in free TRAM (7.8 percent versus 6.1 percent) or DIEP flaps (9.9 percent versus 11.4 percent).

Radiation Therapy Twelve articles3,6,18,19,23,24,45,5256 representing 5059 flaps in 4587 patients analyzed the effect of radiation therapy on fat necrosis (Table 4). The rate of fat necrosis among patients with no history of irradiation was 8.7 percent, significantly lower than in patients who had prereconstruction (11 percent, p 0.022) and postreconstruction irradiation (22.3 percent, p 0.001). In pedicled TRAM flaps, those with prereconstruction irradiation had a higher rate of fat necrosis than patients with no history of irradiation (13.4 percent versus 9.3 percent, p 0.028). Smoking Seven articles3,6,22,44,45,51,57 representing 2347 flaps in 2187 patients analyzed the rate of fat necrosis in relation to smoking (Table 5). The rate of fat necrosis among current smokers was 15.6 percent, which was significantly higher compared with patients who had never smoked (7.1 percent, p 0.001), former smokers (8.7 percent, p 0.03), and non current smokers (9.7 percent, p

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Table 1. Data Extracted from the Articles
Study characteristics Institution Dates of data collection Patients and flaps No. of patients No. of flaps Flap type pTRAM fTRAM DIEP SIEA Patient characteristics BMI Normal weight (25) Overweight (25 and 30) Nonobese (30)* Obese (30) Irradiation No irradiation Prereconstruction irradiation Postreconstruction irradiation Smoking Never smoked Former smoker Noncurrent smoker Current smoker Abdominal scars No scar(s) Scar(s) Other surgical details Recipient vessel used Internal mammary Thoracodorsal Surgical delay of pTRAM flap pTRAM without delay pTRAM with delay Supercharge of TRAM flap TRAM without supercharge TRAM with supercharge Laterality Unilateral reconstruction Bilateral reconstruction Fat necrosis Definition Overall rate Predictors
pTRAM, pedicled TRAM; fTRAM, free TRAM; BMI, body mass index. *Obtained by combining the patients in the normal weight and overweight categories. Obtained by combining the patients in the never smoker and former smoker categories.

tients with abdominal scars was significantly higher than in those without abdominal scars (14.9 percent versus 10.4 percent, p 0.05). This difference was also present in pedicled TRAM flaps (16.8 percent versus 8.5 percent, p 0.005) but not any other flap type. One of the three articles58 specified what type of abdominal scar each patient had and found that patients with Pfannenstiel, laparoscopic, midline, and right lower quadrant scars did not have an increased rate of fat necrosis, whereas patients with paramedian (50 percent versus 15 percent, p 0.17) and subcostal scars (20 percent versus 15 percent, p 0.75) had a nonsignificant increase in fat necrosis. Recipient Vessels Five articles3,56,59 61 representing 2064 flaps in 1621 patients analyzed the effect of recipient vessel choice on fat necrosis (Table 6). The rate of fat necrosis was no different when internal mammary vessels were used compared with thoracodorsal vessels (6.2 percent versus 7.6 percent, p 0.22). Among free TRAM flaps, the rate of fat necrosis was significantly lower when internal mammary vessels were used compared with thoracodorsal vessels (24.2 percent versus 14 percent, p 0.026). Delay of Pedicled TRAM Flaps Two articles62,63 representing 250 flaps in 181 patients analyzed the effect of surgical delay on fat necrosis in pedicled TRAM flap reconstruction (Table 7). The rate of fat necrosis tended to be lower when surgical delay was performed, but the difference was not statistically significant (5.7 percent versus 11.8 percent, p 0.097). Supercharge of Pedicled TRAM Flaps Three articles3133 representing 104 flaps in 104 patients analyzed the effect of microsurgical supercharging of pedicled TRAM flaps on fat necrosis (Table 7). Supercharged flaps were found to have a significantly lower rate of fat necrosis than nonsupercharged pedicled TRAM flaps (12.3 percent versus 41 percent, p 0.001). Unilateral versus Bilateral Reconstruction Nine articles6,20,21,43,51,64 67 representing 1838 flaps in 1209 patients analyzed the effect of laterality on fat necrosis (Table 6). Bilateral reconstructions had a significantly lower rate of fat necrosis than unilateral reconstructions (10.7 percent versus 14.8 percent, p 0.01). The same

0.001). The difference between current smokers and non current smokers was significant in pedicled TRAM flaps (18.7 percent versus 9.5 percent, p 0.004), but not in free TRAM (11.1 percent versus 7.7 percent, p 0.22) or DIEP flaps (14.5 percent versus 12.8 percent, p 0.68). Fat necrosis in former smokers was no higher than in never smokers (8.7 percent versus 7.1 percent, p 0.47). Abdominal Scars Three articles22,45,58 representing 874 flaps in 824 patients analyzed the effect of abdominal scars on fat necrosis (Table 6). Fat necrosis among pa-

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Table 2. Fat Necrosis Rates in the Systematic Review of the Literature and Crude Pooled Analysis
Flap Type pTRAM fTRAM DIEP SIEA Total No. of Flaps 2208 2423 2429 173 7233 Fat Necrosis (%) 272 (12.3) 168 (6.9) 350 (14.4) 14 (8.1) 804 (11.1) Range (%) 6.8376033 2.14028.632 3.34242.920 5.73813.511 2.1406033 p 0.001 (vs. pTRAM) 0.04 (vs. pTRAM); 0.001 (vs. fTRAM) NS (vs. pTRAM); NS (vs. fTRAM); 0.02 (vs. DIEP)

pTRAM, pedicled TRAM; fTRAM, free TRAM.

Table 3. Obesity as a Predictor of Fat Necrosis

No. of Flaps Normal weight (BMI 25) pTRAM fTRAM DIEP Overweight (BMI 25, 30) pTRAM fTRAM DIEP Nonobese (BMI 30) pTRAM fTRAM DIEP Obese (BMI 30) pTRAM fTRAM DIEP 965 488 442 35 242 212 30 1431* 488 654 289 310 175 64 71 Fat Necrosis (%) 75 (7.8) 44 (9) 27 (6.1) 4 (11.4) 21 (8.7) 19 (9) 2 (6.7) 125 (8.7)* 44 (9) 46 (7) 35 (12.1) 39 (12.6) 27 (15.4) 5 (7.8) 7 (9.9) p 0.009 (vs. normal weight); NS (vs. overweight); 0.035 (vs. nonobese) 0.02 (vs. normal weight); 0.02 (vs. nonobese) NS (vs. normal weight, overweight and nonobese) NS (vs. normal weight, overweight and nonobese)

BMI, body mass index; pTRAM, pedicled TRAM; fTRAM, free TRAM; NS, nonsignificant. *The numbers for nonobese patients may be larger than the sum of the numbers for normal weight and overweight patients, because some articles report results as obese versus nonobese rather than obese versus overweight versus normal weight. No extractable data on obesity were available for SIEA flaps.

Table 4. Radiation Therapy as a Predictor of Fat Necrosis

No. of Flaps Prereconstruction XRT pTRAM fTRAM DIEP Postreconstruction XRT pTRAM fTRAM DIEP No XRT pTRAM fTRAM DIEP 1051* 343 170 77 188* 19 32 55 3820* 1169 233 Fat Necrosis (%) 116 (11)* 46 (13.4) 22 (12.9) 12 (15.6) 42 (22.3)* 3 (15.8) 14 (43.8) 14 (25.5) 334 (8.7)* 109 (9.3) 39 (16.7) p 0.022 (vs. prereconstruction XRT); 0.001 (vs. postreconstruction XRT) 0.028 (vs. prereconstruction XRT); NS (vs. postreconstruction XRT) NS (vs. prereconstruction and postreconstruction XRT)

XRT, radiation therapy; pTRAM, pedicled TRAM; fTRAM, free TRAM; NS, nonsignificant. *The numbers for each category may be larger than the sum of the subcategories by flap type, because some articles that were included do not break their results down by flap type. No extractable data on irradiation were available for free TRAM and SIEA flaps.

was true among free TRAM flaps (1 percent versus 11.1 percent, p 0.003). There was also a not statistically significant tendency toward lower rates of fat necrosis in bilateral DIEP (12.6 percent versus 16.7 percent, p 0.076) and pedicled TRAM flaps (10.3 percent versus 12.6 percent, p 0.48) compared with unilateral reconstructions.

DISCUSSION
The studies analyzed cite a fat necrosis rate in autologous breast reconstruction ranging from 3.04 to 37.9 percent.7 The overall rate of fat necrosis was 11.3 percent across all types of breast reconstruction in aggregate. In articles that differentiated by type of reconstruction, the overall

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Table 5. Smoking as a Predictor of Fat Necrosis
No. of Flaps Never smoked pTRAM fTRAM DIEP Former smoker pTRAM fTRAM DIEP Noncurrent smoker* pTRAM fTRAM DIEP Current smoker pTRAM fTRAM DIEP 680 162 518 173 21 152 2026* 665 757 399 321 107 108 83 Fat Necrosis (%) 48 (7.1) 13 (8) 35 (6.8) 15 (8.7) 2 (9.5) 13 (8.6) 197 (9.7)* 63 (9.5) 58 (7.7) 51 (12.8) 50 (15.6) 20 (18.7) 12 (11.1) 12 (14.5) p 0.001 (vs. never smoked); 0.03 (vs. former smoker); 0.001 (vs. noncurrent smoker) 0.009 (vs. never smoked); NS (vs. former smoker); 0.004 (vs. noncurrent smoker) NS (vs. never smoked, former smoker and noncurrent smoker) NS (vs. noncurrent smoker)

pTRAM, pedicled TRAM; fTRAM, free TRAM. *The numbers for non current smokers may be larger than the sum of the numbers for never smoked and former smokers, because some articles report results as current smoker vs. non current smoker rather than current smoker vs. former smoker vs. never smoker. Extractable data on smoking were not available for SIEA flaps.

Table 6. Recipient Vessel, Laterality, and Abdominal Scars as Predictors of Fat Necrosis in Microsurgical Breast Reconstruction*
No. of Flaps Recipient vessel Internal mammary fTRAM Thoracodorsal fTRAM Laterality Unilateral reconstruction pTRAM fTRAM DIEP Bilateral reconstruction pTRAM fTRAM DIEP Abdominal scars No abdominal scars pTRAM fTRAM DIEP Abdominal scars pTRAM fTRAM DIEP 776 143 1288 153 580 127 99 354 1258 526 96 636 566 413 39 114 308 143 61 104 Fat Necrosis (%) 48 (6.2) 20 (14) 98 (7.6) 37 (24.2) 86 (14.8) 16 (12.6) 11 (11.1) 59 (16.7) 135 (10.7) 54 (10.3) 1 (1) 80 (12.6) 59 (10.4) 35 (8.5) 7 (17.9) 17 (14.9) 46 (14.9) 24 (16.8) 7 (11.5) 15 (14.4) p NS 0.026 0.01 NS 0.003 NS 0.05 0.005 NS NS

Table 7. Surgical Delay and Supercharging as Predictors of Fat Necrosis in Pedicled TRAM Flap Reconstruction
No. of Flaps Surgical delay Delay No delay Supercharging pTRAM Supercharged pTRAM 106 144 39 65 Fat Necrosis (%) 6 (5.7) 17 (11.8) 16 (41) 8 (12.3) p

NS 0.001

NS, not significant; pTRAM, pedicled TRAM.

pTRAM, pedicled TRAM; fTRAM, free TRAM; NS, nonsignificant. *No extractable data on recipient vessel selection were available for DIEP and SIEA flaps. No extractable data on laterality or abdominal scars were available for SIEA flaps.

rate of fat necrosis was 11.1 percent. The most important predictor of fat necrosis was flap type, with free TRAM flaps having the lowest rate of fat necrosis (6.9 percent), followed by SIEA (8.1 percent), pedicled TRAM (12.3 percent), and DIEP flaps (14.4 percent).

The lower rate of fat necrosis in free TRAM compared with DIEP flaps has been demonstrated in the past. In their meta-analysis, Man et al. found that DIEP flaps were twice as likely as free TRAM flaps to have fat necrosis.8 Sailon et al.9 and Scheer et al.20 had similar findings. The free TRAM flap uses the dominant pedicle to the lower abdominal tissue, the deep inferior epigastric vessels, taking advantage of all perforators that course through the rectus muscle to the overlying adipose tissue and skin.68 In contrast, the DIEP flap selects only the largest perforators, potentially leading to areas with suboptimal perfusion. A recent advance in DIEP flap reconstruction has been preoperative perforator mapping using computed tomographic angiography or magnetic resonance angiography, which allows identification of a dominant perforator preoperatively and likely shortens operative times.69 More studies are needed to show whether this translates into lower rates of fat ne-

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crosis. Another potential explanation for differences between free TRAM and DIEP flaps may be that articles analyzing DIEP flaps were published by surgeons early in the learning curve.35 Obesity is considered a risk factor for fat necrosis in autologous breast reconstruction, with some studies demonstrating a significant relationship,3,20,22,24,41,45,67,70,71 and others not.6,11,15,46,47,50 In our systematic analysis, obese patients had a significantly higher rate of fat necrosis than nonobese patients. This relationship was true across all reconstruction types combined and for pedicled TRAM flaps alone. This is likely related to the larger size flap required in obese patients. In the past, zone IV has been included to increase the size of the reconstruction; however, current practices avoid use of zone IV, as perfusion is less reliable. Using ex vivo angiograms, Ohjimi et al. demonstrated much lower perfusion in zone IV.72 Vega et al. lowered rates of fat necrosis by routinely excising zone IV in all patients.4 Kroll lowered fat necrosis rates in DIEP flaps from 62.5 percent to 17.4 percent by limiting the use of the DIEP flap to 70 percent of the flap, supporting the discarding of zone IV.73 The literature on prereconstruction irradiation and fat necrosis is inconclusive. In our analysis, patients with a history of prereconstruction irradiation were at increased risk of fat necrosis compared with no irradiation. One study demonstrated increased rates of fat necrosis after prereconstruction radiation therapy with pedicled TRAM flaps.70 Many studies, however, have not demonstrated an increased rate of fat necrosis.3,6,23,65 Fosnot et al. found that prereconstruction irradiation made the dissection and microvascular anastomosis more difficult.18 In our analysis, patients with postreconstruction irradiation had more than twice the rate of fat necrosis compared with no irradiation. Irradiation is known to affect the microcirculation, and irradiating a flap can compromise the blood supply to the adipose tissue, leading to fat necrosis. Multiple studies have found a correlation between postreconstruction irradiation and fat necrosis.29,52,53,74 Some studies investigating the relationship between smoking and fat necrosis have demonstrated a relationship,3,4,29,44,75 whereas others have not.6,11,45,57 In a review of 1195 breast reconstructions, Mehrara et al. found that smokers were at no increased risk of fat necrosis.15 In our analysis, active smokers had a significantly higher rate of fat necrosis compared with past smokers and never smokers. Former smokers were at no increased risk of fat necrosis compared with never smokers, demonstrating that patients who quit smoking can safely undergo autologous breast reconstruction. Smoking is known to adversely affect both microvasculature and macrovasculature by several mechanisms, including nicotine-mediated vasospasm. The literature is ambivalent on abdominal scars as a risk factor for fat necrosis. Some studies have demonstrated a relationship between scars and fat necrosis,15,45 whereas others have not.22,58 In our analysis, patients with abdominal scars had significantly higher rates of fat necrosis. Parrett et al. found that women with a Pfannenstiel scar were at no increased risk of fat necrosis, provided that the scar was included at the border and not undermined.58 Midline scars were not a risk factor for fat necrosis, provided that the contralateral part of the flap was discarded in unilateral reconstructions. The highest rates of fat necrosis were found in paramedian and subcostal scars, as these have the highest potential to interrupt perforators to the abdominal wall. Interestingly, Mahajan et al. found that patients with a Pfannenstiel scar had larger perforators and concluded that the scar effectively led to surgical delay by ligation of the superficial inferior epigastric vessels.76 Xu et al. have advocated the use of bipedicle flaps for unilateral breast reconstruction in patients with abdominal scars.14 On review of the literature, free flaps anastomosed to the internal mammary and thoracodorsal vessels had the same rate of fat necrosis. Temple et al.56 and Saint-Cyr et al.60 reached a similar conclusion. The choice of recipient vessel is often made on a case-by-case basis. The thoracodorsal vessels are exposed and readily available in cases where axillary dissection is performed. However, with the rise of sentinel lymph node biopsy, the need for axillary dissection has decreased, and use of the internal mammary vessels has become more common.59 Surgical delay has been used to improve vascularity of axial flaps. In pedicled TRAM flaps, ligation of the superficial and deep inferior epigastric vessels is performed 2 to 3 weeks before the planned reconstruction. On review of studies analyzing pedicled TRAM flaps in high-risk patients, we found a nonsignificant decrease in fat necrosis in patients who had undergone surgical delay. Codner et al. found a nonsignificant trend toward lower rates of fat necrosis when surgical delay was performed (3.3 percent versus 12 percent, p 0.14).62 Supercharging is another method of improving blood flow in pedicled TRAM flaps. It consists of anastomosing the deep inferior epigastric vessels to recipient vessels in the chest in addition to

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the primary vascular supply of the superior epigastric pedicle. We found that supercharged pedicled TRAM flaps have a significantly lower rate of fat necrosis. Most studies examining the effect of supercharging found that it does improve outcomes, namely, fat necrosis. Lee et al. demonstrated a significant increase in the venous oxygen concentration in the flap, and lower rates of fat necrosis.33 Because most fat necrosis tends to occur in zone IV of the flap, supercharging a unipedicled TRAM flap through the contralateral inferior epigastric vessels may provide improved blood flow into zone IV, as shown by Yamamoto et al.32 Hamdi et al. achieved a low rate of fat necrosis by performing bipedicled perforator free flaps with two microvascular anastomoses for unilateral reconstruction.77 This is an innovative form of supercharging specific to perforator flaps, and further studies are warranted to measure its effectiveness. We found that bilateral reconstructions had significantly lower rates of fat necrosis than unilateral reconstructions. Kroll demonstrated a similar result in DIEP flaps.73 Paige et al. found a nonsignificant tendency toward lower rates of fat necrosis in bilateral pedicled TRAM flaps.67 The effect of laterality relates to the size and reliability of the zones that are harvested. As bilateral flaps, by definition, cannot use any tissue across the midline, these flaps are smaller and the blood supply is more reliable. Although our systematic review has several strengths, including a large number of patients and flaps, and analysis of multiple risk factors for fat necrosis across four different types of autologous breast reconstruction, it does have some limitations. The majority of studies in our review are retrospective and observational, with confounders and biases beyond our control. Ideally, a metaanalysis would be performed from randomized control studies, but these were not found in our review and would be difficult to perform. Our systematic review can be considered a form of pooled analysis or meta-analysis from published data. Finally, fat necrosis does not have a consistent definition across studies, as discussed in the Introduction. This affects our ability to truly compare studies. As a result of the heterogeneity of the definition of fat necrosis, and different levels of experience among surgeons, the results shown in this article may not reflect each surgeons individual experience, but are designed to identify risk factors for fat necrosis in general.

CONCLUSIONS
There is significant variability in the literature regarding risk factors for fat necrosis in autologous breast reconstruction. By providing a comprehensive review of risk factors for fat necrosis, this study can help plastic surgeons adequately counsel patients preoperatively and take measures to minimize the incidence of this complication.
Bernard T. Lee, M.D., M.B.A. Department of Surgery Division of Plastic and Reconstructive Surgery Beth Israel Deaconess Medical Center Harvard Medical School 110 Francis Street, Suite 5A Boston, Mass. 02215 blee3@bidmc.harvard.edu

REFERENCES
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13. Chang EI, Vaca L, DaLio AL, Festekjian JH, Crisera K. Assessment of advanced age as a risk factor in microvascular breast reconstruction. Ann Plast Surg. 2011;67:255259. 14. Xu H, Dong J, Wang T. Bipedicle deep inferior epigastric perforator flap for unilateral breast reconstruction: Seven years experience. Plast Reconstr Surg. 2009;124:17971807. 15. Mehrara BJ, Santoro TD, Arcilla E, Watson JP, Shaw WW, Da Lio AL. Complications after microvascular breast reconstruction: Experience with 1195 flaps. Plast Reconstr Surg. 2006; 118:11001109; discussion 11101111. 16. Follmar KE, Prucz RB, Manahan MA, Magarakis M, Rad AN, Rosson GD. Internal mammary intercostal perforators instead of the true internal mammary vessels as the recipient vessels for breast reconstruction. Plast Reconstr Surg. 2011; 127:3440. 17. Clough KB, ODonoghue JM, Fitoussi AD, Vlastos G, Falcou MC. Prospective evaluation of late cosmetic results following breast reconstruction: II. TRAM flap reconstruction. 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Microvascularly augmented transverse rectus abdominis myocutaneous flap for breast reconstruction: Reappraisal of its value through clinical outcome assessment and intraoperative blood gas analysis. Microsurgery 2008;28:656662. 34. Takeishi M, Fujimoto M, Ishida K, Makino Y. Muscle sparing-2 transverse rectus abdominis musculocutaneous flap for breast reconstruction: A comparison with deep inferior epigastric perforator flap. Microsurgery 2008;28:650655. 35. Busic V, Das-Gupta R, Mesic H, Begic A. The deep inferior epigastric perforator flap for breast reconstruction, the learning curve explored. J Plast Reconstr Aesthet Surg. 2006; 59:580584. 36. Keller A. The deep inferior epigastric perforator free flap for breast reconstruction. Ann Plast Surg. 2001;46:474479; discussion 479480. 37. Andrades P, Fix RJ, Danilla S, et al. Ischemic complications in pedicled, free and muscle-sparing transverse rectus abdominis myocutaneous flaps for breast reconstruction. 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