
==== Front
Plast Reconstr Surg Glob Open
Plast Reconstr Surg Glob Open
GOX
Plastic and Reconstructive Surgery Global Open
2169-7574
Lippincott Williams & Wilkins Hagerstown, MD

GOX-D-23-01064
00035
10.1097/GOX.0000000000006152
3
Breast
Original Article
Fat Necrosis in Single Perforator Deep Inferior Epigastric Artery and Superficial Epigastric Artery Perforator Free Flaps: A Prospective Randomized Study
Miller Rebecca L.R. MD *
Nguyen Christopher M. MD *
Peters Blair R. MD *
Sigurdson Leif MD, MSc, MBA *
Hayakawa Thomas E.J. MD *
Spiwak Rae PhD †
Dalke Kimberly MSc *
Buchel Edward W. MD *
From the * Section of Plastic Surgery, Department of Surgery, University of Manitoba, Winnipeg, Manitoba, Canada
† Department of Surgery, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba, Canada.
Edward W. Buchel, MD, Max Rady College of Medicine, AE101-820 Sherbrook Street, Winnipeg, Manitoba R3A 1R9, Canada, E-mail: ebuchel@hsc.mb.ca
9 2024
12 9 2024
12 9 e615222 11 2023
17 7 2024
Copyright © 2024 The Authors. Published by Wolters Kluwer Health, Inc. on behalf of The American Society of Plastic Surgeons.
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Background:

The deep inferior epigastric perforator (DIEP) flap is the standard of care in autologous breast reconstruction. The superficial inferior epigastric artery perforator flap (SIEA) is an alternative reconstructive option, with the compromise of less donor-site morbidity but variable perfusion to subscarpal fat zones. Fat necrosis is a known complication from marginal perfusion variability. Volumetric analysis of fat necrosis has not been performed between the two reconstructive options, nor has the amount of flap necrosis following radiation. Our objective was to compare rates and volume of fat necrosis between single-perforator DIEP and SIEA flap techniques.

Methods:

A single-center, blinded, prospective cohort study of patients randomized between SIEA and DIEP breast reconstruction was conducted over 2 years (June 2011–July 2013). Inclusion criteria were women undergoing immediate reconstruction following mastectomy. Randomization protocols were strictly followed. Fat necrosis volumetric analysis was determined by an ultrasound-trained attending surgeon at 12 months postoperatively. Patient demographics and adjuvant/neoadjuvant cancer treatment were analyzed. Statistical analyses included Mann-Whitney U tests, chi square, and/or Fisher exact tests. P values of 0.05 or less were considered significant.

Results:

Fat necrosis was detected in 11 of 46 flaps (23.9%), with a median area of 17.9 cm2. There was no significant difference in prevalence of fat necrosis between the two flap types (P = 0.19). Postoperative radiation did not increase the prevalence (P = 0.30) or extent (P = 0.92) of fat necrosis.

Conclusion:

Single-perforator DIEP and SIEA flaps have comparable rates of fat necrosis. Postoperative radiation did not result in increased prevalence or extent of fat necrosis.

OPEN-ACCESSTRUE
COUNTRYCANADA
==== Body
pmcTakeaways

Question: If abdominal wall angiosomes are respected when harvesting single-perforator deep inferior epigastric perforator (DIEP) and superficial inferior epigastric artery perforator flap (SIEA) flaps for breast reconstruction, will the prevalence and volume of fat necrosis differ between the flaps?

Findings: Our study showed that if abdominal wall angiosomes are respected when harvesting DIEP and SIEA flaps, there is no difference in fat necrosis rates between SIEA and DIEP flaps, with or without postoperative radiation.

Meaning: The SIEA is a valid alternative to the DIEP flap for breast reconstruction, with no increase in fat necrosis of the reconstructed breast and potentially less donor-site morbidity.

INTRODUCTION

The deep inferior epigastric perforator (DIEP) flap is the current standard of care in autologous breast reconstruction.1 First described by Koshima in 1989,2 the perfusion capability, dissection technique, and ability to minimize donor-site morbidity by the DIEP flap fostered an era of utilizing microvascular perforator flaps for breast reconstruction. These axial perforator-based flaps are limited by their respective angiosomes and perforasomes described by Taylor3,4 and Saint-Cyr,5 respectively. Although the DIEP flap is an improvement to the transverse rectus abdominis muscle (TRAM) or muscle-sparing TRAM flap in that the DIEP flap avoids loss of the rectus abdominis muscle, during DIEP pedicle dissection there is still damage to the anterior rectus fascia with potential for intercostal nerve injury.6 Harvest of a longer vascular pedicle results in a longer fascial incision and greater chance of intercostal nerve damage, which can lead to increased pain, lower abdominal wall bulging, and hernia development.6

The superficial inferior epigastric artery (SIEA) flap uses the medially located superficial epigastric artery for perfusion,6 which has been shown to behave like a lateral row perforator and not perfuse across the midline, limiting its use to the harvest of a hemiabdomen.7 The SIEA flap is considered by some authors to be a less morbid option, as the abdominal wall fascia is left intact in all cases, essentially eliminating the possibility of an iatrogenic abdominal wall hernia.6 Pain is typically decreased, as the muscle, fascia, and nerves to the anterior abdominal wall are left intact.6 The use of this flap has been limited in breast reconstruction, with cited reasons including that typical perfusion only supports an ipsilateral hemiabdomen, the vessels have been cut preoperatively in many cases due to previous Pfannenstiel incisions, and the diameter of the artery is believed to be of insufficient size.1,6 Additionally, the SIEA flap commonly has a short pedicle with a small-diameter artery.8

Due to its different angiosome and smaller diameter artery than the DIEP flap, a common criticism of the SIEA flap is the higher rate of fat necrosis.9 Analysis of DIEP, SIEA, and muscle-sparing TRAM flaps has shown that the incidence of fat necrosis is decreased as the number of perforators to the flap increases9; a DIEP flap commonly has one to two musculocutaneous perforators, whereas an SIEA flap has only one fasciocutaneous perforator. Fat necrosis can compromise the overall result of the breast reconstruction, leading to a firm, unnatural appearing and painful breast with unfortunate patient concerns of cancer recurrence.9 Despite these potential complications, the SIEA flap provides an abdominal-based flap for autologous breast reconstruction with the lowest potential donor-site morbidity. We hypothesized that if the angiosomes of the abdominal wall were respected when harvesting single-perforator DIEP and SIEA flaps, there would be a difference of less than 10% in the rates of fat necrosis between DIEP and SIEA flaps.

METHODOLOGY

Patient Recruitment

A single-center, blinded, randomized, prospective cohort study in patients randomized between SIEA and DIEP flap-based breast reconstruction was conducted at our tertiary care hospital (Health Sciences Center, Winnipeg, MB, Canada) over the course of a 2-year period (June 2011–July 2013). Primary inclusion criteria were (1) women older than 18 years of age, (2) breast reconstruction after unilateral or bilateral mastectomy, and (3) breast reconstruction performed using DIEP or SIEA flaps. Patients were excluded if breast reconstruction was planned using (1) a latissimus dorsi flap, (2) a gluteal artery perforator flap, (3) a lumbar artery perforator flap, or (4) an implant/tissue expander. Patient data collected included body mass index (BMI), smoking status, comorbidities, and breast cancer treatment (adjuvant/neoadjuvant, chemotherapy, and/or radiation therapy).

Randomization Protocol

A random number generator was used to assign an even (DIEP) or odd (SIEA) number to each patient. These assignments were written and placed in a sealed envelope which was opened by the surgeon on the morning of surgery for every patient. As not every patient anatomically would have an intact SIEA (due to transection from previous abdominal surgery), if they were randomized to the SIEA group and no SIEA was found, then the patient would undergo DIEP reconstruction and be analyzed as intention-to-treat. Additionally, the absolute vessel size of the SIEA at the level of the femoral artery and size mismatch ratio between the SIEA and internal mammary artery (IMA) was assessed. If the SIEA was found to be less than 1mm in diameter or the vessel mismatch was greater than 2:1, the patient underwent DIEP reconstruction and was analyzed as intention-to-treat. All DIEP flaps were harvested with a single-perforator pedicle. All DIEP and SIEA flaps were performed as immediate reconstructions at the time of mastectomy. Computed tomography angiography of the abdomen was not performed preoperatively for any patients.

Fat Necrosis Volumetric Analysis

Ultrasound assessments were performed postoperatively by an attending plastic surgeon (L.S.) trained in bedside ultrasound who was blinded to the treatment arm. All ultrasound assessments were performed at 12 months postoperatively. Visualized ultrasonic fat necrosis was characterized as cystic or solid masses in the breast parenchyma. With ultrasound, cystic lesions seem complex with mural nodules or internal echogenic bands, whereas solid masses have circumscribed or ill-defined margins and are often associated with distortion of the breast parenchyma. Any evidence of fat necrosis was recorded, as well as the measured area (cm2).

Statistical Analyses

Study cohorts were examined using Mann-Whitney U tests and chi square tests to determine differences in the areas of ethnicity, BMI, smoking status, chemotherapy, and radiation. Mann-Whitney U tests were used to examine differences between groups for continuous study outcomes (extent of fat necrosis in radiated compared with nonradiated flaps) and chi square and/or Fisher exact tests to analyze the differences in categorical outcomes depending on sample size (participant ethnicities/BMI/smoking status/chemotherapy treatment/radiation treatment, fat necrosis prevalence, prevalence of fat necrosis in relation to postoperative radiation). Point serial correlation was used to analyze for correlation between BMI and fat necrosis prevalence. P values of 0.05 or less were considered significant.

RESULTS

Table 1 outlines characteristics of the included participants. There were 33 participants (15 participants in the SIEA group, 18 participants in the DIEP group). The average age at the time of surgery in SIEA patients was 51.4 years (range 33–70 years), whereas the average age at the time of surgery in DIEP patients was 50.9 years (range 38–63 years). There were no significant differences between study cohorts in ethnicity, BMI, smoking status (including comparison of current to prior smoking), chemotherapy treatment (including current or prior), and radiation treatment (including current or prior).

Table 1. Patient Demographic Factors

	No. Participants in SIEA Cohort (n = 15)	No. Participants in DIEP Cohort (n = 18)	P	
Age (y)		51.4 (33–70)	50.9 (38–63)	0.968	
Ethnicity	White	14	13	0.428	
Indigenous peoples	1	3	
Other	0	2	
BMI	<18.5 (underweight)	0	0	0.789	
18.5–24.9 (healthy)	2	4	
25.0–29.9 (overweight)	7	7	
>30.0 (obese)	6	7	
Nonsmoker	9	11	0.948	
Smoker	Current	2	0	0.192	
Prior	4	7	
Chemotherapy	None	5	9	0.335	
Preoperative	1	0	1.000	
Postoperative	9	9	
Radiation	None	7	13	0.135	
Preoperative	1	1	1.000	
Postoperative	7	4	

Overall, 46 flaps were included in the study. There were 21 flaps performed in the SIEA group (14 SIEA and seven DIEP analyzed as intention-to-treat). In the DIEP group, 25 flaps were performed (24 DIEP and one SIEA analyzed as intention-to-treat). Within the SIEA cohort, the mean BMI in patients who received an SIEA flap was 30.6 compared with a BMI of 26.7 in patients who received a DIEP analyzed as intention-to-treat; this was not statistically significant (P = 0.25). Comorbidities present in both cohorts included hypertension, diabetes, and dyslipidemia (Fig. 1).

Fig. 1. Patient comorbidities.

Fat necrosis was detected using ultrasound in 11 of 46 flaps (23.9%) with an average area of 17.9 cm2 (Table 2). There was no statistically significant correlation between the presence of fat necrosis and the patient’s BMI (rpb = 0.17, P = 0.34). There was no statistically significant difference in the prevalence of fat necrosis between SIEA and DIEP flaps (P = 0.19). The average area of fat necrosis in the SIEA group was 0.33 cm2 and in the DIEP group was 9.71 cm2, and this was not statistically significant (Z = 1.01, P = 0.31). Of the 11 flaps with fat necrosis identified on ultrasound, only eight flaps had clinically palpable fat necrosis, and only three flaps (0.07%) underwent surgical excision of areas of fat necrosis (two SIEA, one DIEP).

Table 2. Prevalence of Fat Necrosis in SIEA and DIEP Groups (Fischer Exact Test)

	SIEA (% Column)	DIEP (% Column)	Totals	P	
Fat necrosis	Yes	3 (14.29%)	8 (32.00%)	11 (23.91%)	0.188	
No	18 (85.71%)	17 (68.00%)	35 (76.09%)	
Totals		21 (100.00%)	25 (100.00%)	46 (100.00%)		

Postoperative radiation to the flap was not found to significantly increase the overall prevalence of fat necrosis (χ2 = 1.09, P = 0.30; Table 3). Additionally, if fat necrosis was present, the extent of fat necrosis was not found to be significantly greater in the radiated compared with nonradiated flaps (Z = 0.09, P = 0.92).

Table 3. Prevalence of Fat Necrosis Compared with Postoperative Radiation (Chi Square Test)

	Postoperative Radiation	Totals	P	
Yes (% Column)	No (% Column)	
Fat necrosis	Yes	5 (33.33%)	6 (19.35%)	11 (23.91%)	0.297	
No	10 (66.67%)	25 (80.65%)	35 (76.09%)	
Totals		15 (100.00%)	31 (100.00%)	46 (100.00%)		

DISCUSSION

Despite being the current standard of care in autologous breast reconstruction, the DIEP flap requires an incision of the anterior rectus fascia and potential sacrifice of rectus abdominis motor nerves, leading to donor-site morbidity. The main advantage of the SIEA flap over the DIEP is its suprafascial dissection, which eliminates potential donor-site morbidity such as abdominal wall weakness, hernia, and bulges.6,10,11 However, the primary limitation of the SIEA is the reliability of the vascular pedicle, which has been reported to have increased rates of flap failure.1,8,11,12 The aesthetic results of breast reconstruction using DIEP and SIEA flaps has been noted to be indistinguishable.13 Comparing the potential complications of abdominal wall morbidity versus flap loss, abdominal hernia and bulge from a DIEP could be considered worse as it can lead to long-term functional impairment and debilitation to the patient, but flap failure and subsequent loss of an SIEA is an aesthetic issue which can be addressed with implant-based breast reconstruction as an alternative.14 The literature has shown that SIEA flaps are anatomically adequate for use in approximately 30% of patients.10 In our study population, 66.7% of patients assigned to the SIEA cohort (14 of 21 patients) had SIEA vessels adequate to support the free flap reconstruction.

Fat necrosis is a complication that is common in autologous breast reconstruction, affecting between 0.5% and 42.9% of patients.15 Fat necrosis is detected clinically as a palpable lump, and may also present with pain, skin changes, and lymphadenopathy, which can result in distress to patients, as these symptoms often mimic cancer recurrence.15 Park et al describe a fat necrosis rate of 10.8% in 145 SIEA and superficial circumflex iliac artery flaps used in breast reconstruction.12 Our study yielded similar results of 14.29% fat necrosis rate in the SIEA population. It is understood that the DIEP and SIEA flaps are not equal in perfusion capabilities due to their different angiosomes. DIEP flaps are typically centrally based, with the best perfusion in the periumbilical region.16 The angiosome of the SIEA is obliquely and laterally based and typically does not cross the midline, resulting in reliable use of an SIEA flap limited to a hemiabdomen.7 The general rates of fat necrosis between the DIEP and SIEA flaps have been described, but limited studies have directly compared single-perforator DIEP flaps to SIEA flaps. In DIEP, SIEA, and muscle-sparing TRAM flaps, fat necrosis has been demonstrated to decrease as the number of perforators to the flap increase, with the lowest incidence of fat necrosis being in flaps with three to five perforators.9 An SIEA flap has one fasciocutaneous perforator, while a DIEP flap typically has one to two musculocutaneous perforators. Baumann et al describe muscle-sparing TRAM and DIEP flaps with one to two perforators as having the highest rate of fat necrosis with a 7.7-fold increase, while the SIEA had an intermediate 4.7-fold rate of fat necrosis; 14% SIEA flaps underwent fat necrosis.9 Our results demonstrate that there is no significant difference in either the prevalence or extent of fat necrosis between single-perforator DIEP and SIEA flaps if the angiosomes of each flap are respected.

The effects of adjuvant radiation therapy on subcutaneous tissues have been well described. Our results demonstrate that postoperative radiation of either SIEA or DIEP flaps did not affect the absolute number of flaps that developed fat necrosis. Additionally, the two-dimensional extent of fat necrosis in postoperatively irradiated flaps was not statistically different compared with nonirradiated flaps. This is in keeping with the results of Baumann et al, who demonstrated that radiation does not significantly affect the incidence of fat necrosis in both univariate and multivariate analyses9; similar results were yielded by Spiegel and Khan.10

Ultrasound is a well-established, time-efficient, effective modality for imaging of the breast for fat necrosis.17,18 Fat necrosis on ultrasound can look like a solid mass (with well-circumscribed margins, or indistinct or spiculated margins) or a cystic mass (including simple cysts, complex cysts with a mural nodule, complex cysts with echogenic bands, or round anechoic lipid cysts).5,17,19–21 A defined sonographic indicator of fat necrosis is a mass with echogenic internal bands, which shift in orientation with changes in patient position.22 A recent systematic review of fat necrosis in autologous breast reconstruction recommended ultrasound as the only imaging modality for workup of clinically identified fat necrosis.15 Surgical education in breast ultrasound has stressed the importance of this modality as a hand-on technology, minimizing the need to defer to sonographers and technicians.23 Outpatient-based surgeon-performed ultrasounds not only allows surgeons to develop and maintain their skills, but also lessens the patient load on radiology departments.24 Ultrasounds of the breast performed by experienced surgeons has been shown to be accurate in the diagnosis of symptomatic breast disease (sensitivity 98.3%, specificity 91.7%) and demonstrated complete concordance with radiologist assessment in 96.1% of cases.25

Although vessel caliber was not measured in our study, multiple studies have described algorithms to guide the decision-making process for free flap breast reconstruction and state that an SIEA should only be used if the vessel diameter is greater than 1.5 mm10,14,26 and/or with a visible and palpable pulse10,11; these algorithms also include the use of preoperative computed tomography angiography for anastomosis planning.27 However, other studies state that venous drainage in SIEA flaps is the limiting factor rather than arterial inflow, and recommend the superficial inferior epigastric vein have a diameter of at least 1.5 mm and the SIEA have a palpable pulse regardless of size.11 Recently, Zhang et al28 described a positive correlation in perfusion level between the SIEA and DIEP systems with BMI, concluding that the SIEA acts as a compensatory vessel in patients with a higher BMI and can be a reasonable choice for breast reconstruction in those patients. They also concluded that SIEA diameter of more than 2.0 mm only occurred in patients with a BMI of 25 kg/m2 or more. We observed in our study that twice the number of patients with a BMI of less than 25 kg/m2 underwent DIEP reconstruction as opposed to SIEA reconstruction. The correlation shown by Zhang et al could explain the differences between groups within a BMI of less than 25 kg/m2 category, as patients may not have a usable caliber of SIEA pedicle for anastomosis. However, our study demonstrated no statistically significant difference in BMI between the SIEA and DIEP cohorts, and no statistically significant correlation between BMI and the presence of fat necrosis.

Additional research into perfusion patterns of the lower abdomen has been completed using advanced imaging modalities. Laser-induced indocyanine green (ICG) fluorescence was first used to evaluate intraoperative perfusion of free microvascular tissue transfer in 2002.29 Perfusion of the lower abdomen by the deep inferior epigastric vessels is conventionally described using Hartrampf zones30 and, as discussed above, is considered to be centrally based in the periumbilical region (zone I and II). Holm et al assessed the perfusion pattern of the DIEP flap using ICG and instead found that zone III perfusion happened consistently faster and with higher intensity than zone II, concluding that blood supply to the lower abdomen should be thought of as two halves separated by the midline with the ipsilateral half having a very reliable, axial pattern of perfusion.31 The contralateral half of the abdomen was shown to have random-pattern, individually variable blood supply with a mean reduction in skin perfusion of 95% to zone IV.31 The abdominal perfusion pattern of the SIEA was also analyzed using ICG, and in patients fulfilling the conventional criteria for microvascular transfer using the SIEA (as described above), the extent of complete abdominal flap perfusion ranged from 0% to 100%.32 The vascular territory of the SIEA did not cross the midline in 64% of patients.32 Therefore, based on volume alone, breast reconstruction requiring greater than a hemiabdomen is better suited to reconstruction with a DIEP flap, while reconstruction requiring a hemiabdomen or less can be reconstructed with either a DIEP or SIEA flap. It should be noted that intraoperative SPY imaging of SIEA flap perfusion in situ, before flap division from the abdomen, may not correspond accurately to flap perfusion once transferred to the breast. It is agreed that the typically smaller arterial diameter of the SIEA may cause decreased perfusion to the flap and can also result in a size mismatch between the donor IMA and recipient SIEA, which consequently may cause turbulent blood flow and localized thrombosis, ultimately resulting in fat necrosis.8,26,28 Additionally, the SIEA is prone to vasospasm,8 the degree of which is worsened following vessel manipulation and microanastamosis. We previously have published our algorithm for deciding between SIEA and DIEP flap reconstruction.6 If the breast reconstruction requires greater than a hemiabdomen, a DIEP flap will be performed. The number of perforators harvested with a DIEP flap is the number that optimizes flap perfusion while minimizing denervation to the abdominal wall. Typically, we will only divide a single motor branch to the rectus muscle, which is then repaired at the completion of flap harvest. If additional perforators are desired but would require sacrifice of additional motor nerve branches, we will perform an abdominal perforator exchange flap.33 SPY imaging is used in the final steps of perforator selection, to confirm adequate perfusion of the flap via the chosen perforator(s) as well as the extent of perfusion to the flap edges. If an SIEA flap reconstruction is being considered, the absolute vessel size of the SIEA at the level of the femoral artery and size mismatch between the SIEA and IMA are assessed (as described above in our Methodology). Additionally, the length of the SIEA pedicle must be twice the thickness of the SIEA flap to provide enough length for anastomosis to the IMA and flap inset. SPY is also used to ensure perfusion of the flap based on the SIEA vessels after clamping the DIEP perforator(s).

A strength of our study is that multiple patient variables were assessed (age, ethnicity, BMI, smoking status, chemotherapy, radiation) to rule out confounding factors. Another strength is the consistency in assessment of fat necrosis at 1 year postoperatively. For all patients, the fat necrosis assessments were performed by a single ultrasound-trained plastic surgeon.

There are several limitations to our study. The first includes the small sample size and single-center cohort. In addition, although a moderate rate of fat necrosis was identified on ultrasound (11 of 46 flaps), there is no criteria to define clinically significant fat necrosis: only eight flaps had clinically detectable fat necrosis and of those, only three flaps underwent surgical excision of those areas. Finally, there was no confirmatory study (such as pathology) to verify the ultrasonic diagnosis of fat necrosis, and no radiologist or higher sensitivity imaging study (such as magnetic resonance imaging) used to corroborate ultrasonic findings.

CONCLUSIONS

Single-perforator DIEP and SIEA flaps have similar rates of fat necrosis provided they are harvested adhering to their specific angiosomes. This study shows no difference in fat necrosis between DIEP and SIEA groups, and no difference in the prevalence or extent of fat necrosis in postoperatively radiated compared with nonradiated flaps. This finding supports our belief that that if the angiosomes of the abdominal wall are respected when harvesting single-perforator DIEP and SIEA flaps, there is no difference in the rates of fat necrosis. Larger prospective, multicentered randomized controlled trials are warranted.

DISCLOSURE

The authors have no financial interest to declare in relation to the content of this article.

Published online 12 September 2024.

Disclosure statements are at the end of this article, following the correspondence information.
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