Michael A. Howard a, Babak Mehrara b, * REVIEW. Introduction

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1 International Journal of Surgery (2005) 3, 53e60 REVIEW Emerging trends in microsurgical breast reconstruction: Deep inferior epigastric artery perforator (DIEP) and the superior gluteal artery perforator (SGAP) flaps Michael A. Howard a, Babak Mehrara b, * a The Division of Plastic Surgery, Evanston Northwestern Hospital, 2650 Ridge Avenue, Evanston, IL 60201, USA b The Plastic Surgery Service, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, 11th Floor, New York, NY 10021, USA KEYWORDS Breast reconstruction; Microsurgery; Deep inferior epigastric artery perforator flap; DIEP; Superior gluteal artery perforator flap; SGAP Abstract Breast reconstruction is an important adjunct in the treatment of breast cancer. Many reconstructive options exist, however autologous tissue remains the gold standard. One drawback to autologous reconstruction methods is the potential for flap donor site morbidity. Recent advances in microsurgical techniques include the development of perforator flaps, including the Deep Inferior Epigastric Artery Perforator flap (DIEP) and the Superior Gluteal Artery Perforator (SGAP) flaps. Harvest of these flaps attempt to minimize the impact on the donor site and thereby reduce the incidence of donor site complications. This article will review of the indications, advantages and drawbacks to the use of perforator flaps in breast reconstruction surgery. ª 2005 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved. Introduction The incidence of breast cancer is rising. Nearly one in eight women in the USA will be diagnosed with * Corresponding author. Tel.: C ; fax: C address: mehrarab@mskcc.org (B. Mehrara). this disease at some point during their lifetime. According to the American Cancer Society, 211,300 new cases of invasive breast cancer were diagnosed in Although many women are treated with breast conservation, mastectomy remains an important treatment modality. Breast reconstruction has been shown to be an important adjunct in the treatment of women /$ - see front matter ª 2005 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.ijsu

2 54 M.A. Howard, B. Mehrara treated with mastectomy. 2 Numerous studies have demonstrated beneficial effects on quality of life and body image. 3,4 In addition, breast reconstruction serves as an important coping mechanism particularly in younger patients. 5,6 Traditionally, breast reconstruction has been performed using either autogenous tissues (excess fat from the abdomen or buttocks) or implants. The purpose of this manuscript is to review recent advancements in microsurgical autogenous tissue breast reconstruction. requiring mastectomy. Although tissue expander/ implant reconstruction is an excellent and expedient method for breast reconstruction, autogenous tissues remain the gold standard for a natural looking and natural feeling restoration of the female breast (Fig. 1). Autogenous tissue breast reconstruction can be divided into a number of categories based on the donor sites available and the methods used for tissue transfer. Background A number of reconstructive options ranging from simple procedures to complex microsurgical reconstructions are currently available for women Pedicled flaps Pedicled flaps refer to those that are transferred to the breast while the endogenous blood supply is kept intact. Examples of pedicled flaps include the Figure 1 (A and B) Pre-operative and (C and D) post-operative photographs of a woman treated with mastectomy and breast reconstruction using a deep inferior epigastric perforator flap.

3 Perforator flaps for breast reconstruction 55 pedicled transverse rectus abdominus myocutaneous flap (TRAM) and the latissimus dorsi myocutaneous flap. In general, pedicled flaps are transferred as a composite of muscle, fat, and skin and are then sculpted to re-create the missing breast. Most or all of the associated muscle is harvested in an effort to maintain the blood supply of the skin and overlying fat. Sacrifice of the rectus abdominus muscle may lead to significant abdominal wall morbidity including weakness, abdominal wall laxity, and abdominal wall hernia formation. 7e10 Often, synthetic mesh is required following flap harvest to repair the fascial defect. 11 The vascular supply of the pedicled TRAM flap is based on the superior epigastric vessels, which represents the secondary blood supply to the lower abdominal skin and subcutaneous tissues. Thus, these procedures may be associated with partial flap loss (7e31%). 12 Despite these shortcomings, pedicled flaps remain popular in many centers since they are relatively easy to perform and are, in general, associated with excellent outcomes. Perforator flaps Perforator flaps represent the logical extension of the microsurgical free flap. These flaps are designed to include the bare minimum of structures needed for reconstruction, while limiting the extraneous donor site tissues harvested with a flap. By reducing the amount of donor site tissue disturbance, one theoretically lowers the donor site morbidity. The development of these flaps arose from detailed anatomical description of the body s vascular supply to the skin and subcutaneous tissue. 18e22 Large, named vessels give off smaller branches that course superficially, or perforate through muscle and/or fascial planes to supply the overlying skin and subcutaneous tissue. These perforators are a neurovascular bundle consisting of an artery, vein, and nerve, and can be meticulously dissected through the muscle to their origin. This enables preservation of the myofibrils and their innervation, ultimately preserving the function of the underlying muscle. Two such perforator flaps have gained favor for autologous breast reconstruction. Microsurgical reconstruction The shortcomings of pedicled flaps have led to advancements in microsurgical breast reconstruction. In these procedures, small sections of the underlying muscle are dissected together with the dominant vascular pedicle and the blood supply of the tissue (flap) is temporarily disconnected and re-established in the breast pocket. Examples of free flaps include the free TRAM flap and gluteal flaps. The free TRAM flap theoretically decreases abdominal wall morbidity by preserving more innervated rectus muscle. In addition, the free TRAM and gluteal flaps are based on the dominant blood supply of the overlying skin, the deep inferior epigastric artery/vein (DIEA/V) and superior gluteal artery/vein (SGA/V), respectively, and are thus associated with decreased rates of partial flap loss or fat necrosis. Critics of the free TRAM flap procedure claim that overall abdominal complication rates remain high and comparable to pedicled TRAM flaps due to the alterations in muscle attachment and denervation. 13e16 They maintain that these alterations lead to weakness and atrophy of the remaining muscle with resultant abdominal wall function that is comparable to patients treated with pedicled TRAM flap harvest. 17 This concept remains contentious in the plastic surgery literature with a wide range of studies demonstrating various outcomes. Deep inferior epigastric artery perforator (DIEP) flap Rectus abdominus preservation Based on the TRAM flap concept, an abdominal skin and fat flap is dissected based on the perforating branches from the DIEA. 23e26 Unlike the pedicled or free TRAM flap harvest, however, the abdominal wall fascia and rectus muscle are not included with the flap. Preserving muscle vascularity and motor nerves in turn preserves the rectus muscle function. 27,28 Recent evidence suggests that preservation of the rectus muscle reduces donor site morbidity and results in lower rates of donor site complications such as site pain, abdominal wall laxity or hernia, back pain, and functional impairments. 29 These benefits are even more significant when bilateral reconstruction is performed. 30 DIEP anatomy/flap harvest Harvest of the DIEP flap is similar to thatof a standard free TRAM. The major differences lie in the meticulous dissection required to maintain the integrity of the rectus fibers and the continuity of the motor branches. Standard TRAM abdominal markings and incisions are utilized, giving consideration to pre-existing abdominal incisions. During initial flap

4 56 M.A. Howard, B. Mehrara Figure 2 (A) Identification of a single, dominate perforator entering abdominal flap (arrow); (B) DIEP flap has been harvested; single perforator entering central portion of the flap (arrow); (C) resulting donor site; note muscular viability and single incision of anterior rectus fascia that will be repaired with a simple running suture. For orientation, the patient s head is superior. elevation, perforators emerging from the anterior rectus sheath to the overlying flap are identified. A decision must be made as to which perforator(s) should be utilized, based on vessel size, quality, palpable pulse and location (Fig. 2AeC). Preferably, a single dominant perforator exists entering centrally on the flap. However, multiple perforators may be included if none appears dominant. The anterior rectus fascia is opened and the perforator is dissected along its course through the muscle to its origin from the deep inferior epigastric artery and vein. The vascular pedicle is further dissected until adequate length and caliber are achieved. Segmental sensory and motor nerves are encountered during dissection. The motor nerves are preserved to prevent de-innervation of the muscle. Sensory nerves that run with the perforator to the flap may be dissected for anastamosis in the chest for flap re-innervation. After flap harvest, a simple running or interrupted closure of the fascial incision is performed and the donor site is closed. The free flap is transferred to the mastectomy defect and microvascular anastamosis is performed to the internal mammary or thoracodorsal vessels. Neurotization is usually performed to medial branches of the 4th intercostals nerve. Further inset and shaping of the flap is then performed. DIEP patient selection Pre-operative considerations for the DIEP are similar to that of the free TRAM. They include the patient s breast size and volume, the amount and quality of abdominal tissue available, tobacco use, and coexisting medical conditions. 31 Obesity is a relative contraindication to the TRAM and DIEP flap due to increased rates of donor site complications, although some authors have argued that DIEP flaps may be safe in this setting as perforating vessels are often hypertrophied. 15,32 Pre-existing midline and Pfannenstiel incisions are of little consequence, however, midline incisions decrease the amount of tissue available for reconstruction as circulation to the contralateral flap is impeded by scar formation. Paramedian and ostomy incisions may have previously damaged the perforators and should be given particular consideration. A previous open cholecystectomy incision should not affect flap harvest; however, these incisions may diminish the blood supply of the anterior abdominal skin and result in wound healing complications. Intra-operatively, the decision to proceed with DIEP harvest is made based on the number, caliber, and location of the perforators, 31 and conversion to a standard free or pedicled TRAM necessary in

5 Perforator flaps for breast reconstruction 57 cases where adequate perforators are not identified. 16 Ideally, one dominant perforator is present which is usually able to supply the majority of the flap. Presence of several, smaller perforators may imply a less robust, though adequate, blood supply. In one series 20% of flaps were based on a single perforator, 50% on two perforators, and 30% on three or more. 16 In our experience, the majority of DIEP flaps are based on one or two large perforating vessels. Advantages of DIEP flap The DIEP flap is the preferred choice for many surgeons for delayed and immediate autologous breast reconstruction, particularly when performing bilateral breast reconstruction (Fig. 2A, B). 33 The DIEP is a reliable flap, with published success rates of 95e99.5% 15,16,31,32 and partial flap loss rate of 2.5%. 16 The fat necrosis rate (i.e., any amount of significant flap firmness post-operatively) ranges from 6 to 12.9%, 10,16,32,34 comparing favorably to that of the free or pedicled TRAM. 12,35,36 Use of the DIEP flap results in less impact on the abdominal donor site and therefore reduced donor site morbidity. 13,17,29 The reported abdominal hernia rate following DIEP harvest is 0.7% 16 and 2.1% in bilateral cases. 33 This compares favorably to the hernia rate of up to 15% following TRAM flap. 37 In the immediate setting, DIEP patients may experience less donor site pain 38 and ambulate sooner. 15 Also, the use of synthetic mesh is not required for fascial closure following DIEP harvest, while it may be needed following TRAM, harvest, particularly in bilateral flap harvest. 30 Drawbacks Use of the DIEP for reconstruction requires microsurgical proficiency and a hospital setting that provides competent care for microsurgical patients. In a surgeon s early experience with the DIEP flap, there may be an increased length of operative time due to perforator dissection. However, with experience, the operative times are rarely much longer than a free TRAM and the procedure has been shown to be a cost effective method of reconstruction. 39 Venous congestion may be problematic in the DIEP flap; therefore careful dissection of the superficial inferior epigastric vein for additional venous drainage may be necessary in some cases. 30,31,40,41 The DIEP flap has reduced, but not completely eliminated donor site complications. Gill et al. 16 reported that in a series of 758 DIEP flaps over 10 years, the overall donor site complication rate was 13.6%. While most of these complications consisted of delayed abdominal wound healing, the abdominal hernia rate was 0.7%. The incidence of complications is also significantly elevated among patients who actively smoke, suffer from hypertension, or who undergo post-operative XRT. 16,30,42 For this reason, many recommend avoiding flaps in active smokers and delaying flap reconstruction until after completion of XRT. 15,42 Gluteal artery perforator flaps General The gluteal donor sites provide another autologous option for those women who do not have adequate abdominal tissue, whose abdomen is not an option due to pre-existing scars, or those who prefer to avoid an abdominal donor site. The use of gluteal flaps, however, has been limited by the associated donor site scarring, difficult dissection, and short pedicle. 43e46 The superior gluteal artery perforator (SGAP) flap 47 and the inferior gluteal artery perforator (IGAP) flap 48 address these issues by avoiding gluteus muscle sacrifice and increasing pedicle length. Patient selection/indications Gluteal flaps are autologous reconstruction options for a select patient population who are not TRAM or DIEP flap candidates and who wish to avoid use of an implant or in whom an implant is not an option (i.e. poor chest skin quality following XRT). In addition, these flaps may be considered in patients who wish to avoid the abdominal donor site. Gluteal artery perforator flaps are also best suited to match a moderate-sized, non-ptotic, contralateral breast (Fig. 3). Gluteal flap anatomy/harvest Two different flaps may be harvested from the gluteal donor site. At the superior aspect of the buttock, a perforator emerges from the gluteus maximus one-third the distance between the posterior iliac spine and the greater trochanter. A flap up to 12! 32 cm in size may be designed over this perforator (Fig. 4). Harvest of the SGAP is performed from the ipsilateral buttock in the lateral decubitus position. The patient s torso may be corkscrewed to allow two-team approach.

6 58 M.A. Howard, B. Mehrara Figure 3 (A) Donor site from bilateral abdominal flap harvest, left TRAM (solid arrow) and right DIEP (empty arrow); (B) harvested flaps with vessels entering hemi-tram (solid arrow) and single perforator entering central portion of the DIEP flap (empty arrow). Note the lack of muscle harvested with DIEP flap. For orientation, the patient s head is superior. The flap elevated from lateral to medial until the perforator(s) is/are identified. The perforator is traced and dissected through the gluteus maximus to the level of anterior gluteal fascia, preserving the gluteal fibers. Dissection may be complete at this point if there is adequate vessel length and diameter or the fascia may be opened and dissection continued toward the superior gluteal artery. Use of the internal mammary vessels is preferred as the final pedicle length is often insufficient to reach the axilla. 27 If sensory re-innervation is planned, the nerves from T12-L2 entering the flap superiorly above muscle fascia layer should be identified at the outset of flap harvest. These fibers can be traced superiorly and included. 49,50 A second perforator flap may be designed on the lower buttock crease based on perforating vessels originating from the inferior gluteal artery (IGAP flap). Design of the flap places the inferior flap border and final closure in the gluteal crease. A flap 12e13 cm in vertical dimension can be harvested in a similar fashion to the SGAP flap. Care must be taken to prevent the resulting scar from extending to the anterior thigh and avoid damage to the sciatic and posterior cutaneous nerve that lie lateral to the inferior gluteal artery. Advantages The SGAP and IGAP flaps offer several advantages in autologous reconstruction. There is an Figure 4 (A) SGAP flap donor site markings; (B) harvested SGAP flap; (C) SGAP donor site; (D) healed donor site.

7 Perforator flaps for breast reconstruction 59 abundance of adipose tissue in gluteal region, even in thin patients, flap harvest results in a wellhidden scar, and the integrity of the gluteus maximus muscle is preserved. Due to the quality of the buttock tissue, the resulting flap has excellent projection of the reconstructed breast as compared to TRAM and DIEP without the need for folding the flap, which may affect flap circulation. This flap is an autologous option if the TRAM has been utilized previously. It also may be used in staged, bilateral breast reconstruction, whereas the TRAM offers a single-use opportunity. Advantages of the IGAP include the well-hidden donor site in the gluteal crease and a longer vascular pedicle than the SGAP that can reach the axilla. 51 Drawbacks The gluteal flaps are not widely taught in training programs, therefore, overall patient and physician comfort lags behind that of other alternatives. Like the DIEP flap, use of the gluteal flaps requires microsurgical experience and comfort with perforator dissection. In addition, patient positioning and operative logistics can be somewhat difficult, although in most instances simultaneous two-team work is possible. Bilateral reconstruction poses a particular challenge due to the long length of the surgical procedure and patient repositioning such that most surgeons choose to stage reconstruction. The gluteal donor site is thicker and more fibrous than the abdominal donor site tissue and less overall skin is available. These factors may limit the ability to achieve ptosis of the reconstructed breast and overall contouring to match the contralateral breast. This may also limit the flap s use in delayed reconstruction where the skin requirements are increased. SGAP flap harvest may result in a depressed scar particularly if more than 10 cm of skin is taken in the vertical dimension 51 or if significant undermining is performed to increase flap volume during harvest. This may result in difficulties with asymmetry an unsightly scarring. The IGAP donor site in the gluteal crease may affect sitting and ambulating in the short term, but this rarely persists. 48 Conclusions The DIEP flap is a reliable flap, results in fewer abdominal complications, and has minimal increase in surgical time as compared to traditional abdominal flaps used for breast reconstruction. Craigie et al. 30 point out that the initial arguments against use of the DIEP flap (i.e., long operative time and high failure rates) are no longer valid. The SGAP and the IGAP flaps are also excellent autologous tissue alternatives for breast reconstruction. The benefits of the flap reliability and inconspicuous donor site outweigh the slight increase in operative complexity due to the position change required intra-operatively. The DIEP, SGAP and IGAP flaps are reconstructive options available to appropriately selected patients undergoing autologous breast reconstruction. Familiarity with these options will enhance the care of the breast reconstruction patient. References 1. American Cancer Society, Inc.! Brandberg Y, Malm M, Blomqvist L. A prospective and randomized study, SVEA, comparing effects of three methods for delayed breast reconstruction on quality of life, patient-defined problem areas of life, and cosmetic result. Plastic and Reconstructive Surgery 2000;105(1): Edsander-Nord A, Brandberg Y, Wickman M. Quality of life, patients satisfaction, and aesthetic outcome after pedicled or free TRAM flap breast surgery. Plastic and Reconstructive Surgery 2001;107(5):1142e5. 4. Girotto JA, Schreiber J, Nahabedian MY. 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Plastic and Reconstructive Surgery 1989;84(6):875e Allen RJ, Tucker Jr C. Superior gluteal artery perforator free flap for breast reconstruction. Plastic and Reconstructive Surgery 1995;95(7):1207e Allen RJ. Perforator flaps in breast reconstruction: how to perform reliably. Philadelphia, PA: American Society of Plastic Surgeons; Blondeel PN. The sensate free superior gluteal artery perforator (S-GAP) flap: a valuable alternative in autologous breast reconstruction. British Journal of Plastic Surgery 1999;52(3):185e Blondeel PN, Demuynck M, Mete D, Monstrey SJ, Van Landuyt K, Matton G, et al. Sensory nerve repair in perforator flaps for autologous breast reconstruction: sensational or senseless? British Journal of Plastic Surgery 1999;52(1):37e Hidalgo DA. Superior gluteal free flap. In: Spear SL, Little JW, Lippman ME, et al., editors. Surgery of the breast: principles and art. Philadelphia: Lippincott-Raven Publishers; p. 627e35.