BREAST Indocyanine Green Laser Angiography Improves Deep Inferior Epigastric Perforator Flap Outcomes following Abdominal Suction Lipectomy William J. Casey III, M.D. Katharine A. Connolly, M.D. Alisha Nanda, B.S. Alanna M. Rebecca, M.D. Galen Perdikis, M.D. Anthony A. Smith, M.D. Phoenix, Ariz.; and Jacksonville, Fla.
Background: The reliability of deep inferior epigastric artery perforator (DIEP) flap reconstruction following abdominal liposuction is controversial. The authors’ early cases were technically successful; however, they experienced high partial flap loss and fat necrosis rates. The authors sought to compare DIEP flap outcomes in the setting of prior liposuction after the use of intraoperative indocyanine green angiography compared to when flaps were assessed on clinical grounds alone. Methods: A retrospective review of a consecutive series of DIEP flaps following liposuction at a single institution was performed, comparing those evaluated on clinical grounds alone and those in which indocyanine green angiography was used intraoperatively. Outcomes measured included anastomotic complications, total flap loss, partial flap loss, fat necrosis, and postoperative abdominal wounds. Results: Thirteen DIEP flaps following prior liposuction were performed on 11 patients from July of 2003 through January of 2014. All patients had preoperative imaging with duplex ultrasound or computed tomographic angiography to analyze perforator suitability before surgical exploration. Seven flaps were evaluated intraoperatively on clinical grounds alone. Six flaps were assessed and modified based on indocyanine green angiography. All flaps were successful; however, partial flap loss and fat necrosis rates dropped from 71.4 percent to 0 percent when indocyanine green angiography was used intraoperatively (p = 0.02). Conclusions: Indocyanine green angiography is an excellent vascular imaging modality for intraoperative use to assess flap perfusion, and improves outcomes in DIEP flaps when harvested after prior abdominal suction lipectomy. (Plast. Reconstr. Surg. 135: 491e, 2015.)
N
umerous studies over the past century have increased our knowledge of the vascular anatomy of the skin and subcutaneous tissue.1–8 This information has been applied clinically with new flap designs and refinements in surgical techniques resulting in reliable, sophisticated options in reconstructive surgery. The concept of a perforator flap was introduced by Kroll and Rosenfield in 1988.9 They demonstrated that the underlying muscle is a passive carrier for the local perforators and is not essential for flap survival. From the Division of Plastic and Reconstructive Surgery, Mayo Clinic in Arizona; the University of Arizona College of Medicine–Phoenix Campus; and the Division of Plastic and Reconstructive Surgery, Mayo Clinic in Florida. Received for publication May 9, 2014; accepted August 8, 2014. This paper is to be presented at the American Society for Reconstructive Microsurgery Annual Meeting in the Bahamas on January 25, 2015. Copyright © 2015 by the American Society of Plastic Surgeons DOI: 10.1097/PRS.0000000000000964
Perforator flaps have been developed as a means of maximizing the reconstructive surgical results and minimizing donor-site morbidity. The lower abdomen has become a preferred donor site for autologous breast reconstruction. Koshima and Soeda demonstrated that the lower abdominal skin and subcutaneous fat could be harvested for free tissue transfer without the inclusion of the rectus abdominis muscle.10 Allen and Treece subsequently described the deep inferior epigastric perforator (DIEP) flap for breast reconstruction.11 Large series have documented the safety, efficacy, and reliability of the DIEP flap12 and have shown improvements in donor-site morbidity compared with free transverse rectus abdominis myocutaneous (TRAM) and pedicled TRAM flaps.13,14 Disclosure: The authors have no financial disclosures related to the preparation, presentation, or submission of this article.
www.PRSJournal.com
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Plastic and Reconstructive Surgery • March 2015 The reliability of DIEP flap harvest following abdominal suction lipectomy is controversial. Several small case series have demonstrated that successful abdominally based free flap reconstruction is possible in the setting of prior abdominal suction lipectomy.15–20 Our initial experience with DIEP breast reconstruction following abdominal liposuction consisted of seven flaps in six patients. Although all flaps survived, significant partial flap loss or fat necrosis occurred in five of seven flaps (71.4 percent). Indocyanine green laser angiography (SPY Intraoperative Imaging Systems; Novadaq Technologies, Inc., Mississauga, Ontario, Canada) has been used clinically to assess mastectomy skin flap and autologous flap perfusion.21–30 Because of its ability to aid in flap design and elevation, and determining areas of adequate perfusion, we have since used laser angiography in DIEP flap cases when prior abdominal suction lipectomy has been performed. The purpose of this study is to determine whether DIEP flap outcomes are improved when indocyanine green laser angiography is used compared to cases in which it is not used.
of 2003 through January of 2014. DIEP flaps that were harvested and transferred in the setting of prior abdominal suction lipectomy were identified. Radiographic modalities used for perforator mapping as a means of preoperative planning are described. Initially, adequate flap perfusion was assessed intraoperatively on clinical grounds alone (color, Doppler signals, and punctate bleeding from flap edges). Because we experienced relatively high rates of partial flap loss and fat necrosis in DIEP flaps that had previously undergone suction lipectomy, indocyanine green laser angiography was used intraoperatively in all subsequent cases (Figs. 1 through 8). This was performed at the
PATIENTS AND METHODS Following approval from our institutional review board, a retrospective review of all muscle-sparing free TRAM flaps, DIEP flaps, and superficial inferior epigastric artery flaps was performed at the Mayo Clinic in Arizona from July Fig. 2. Preoperative computed tomographic angiogram demonstrating an excellent left periumbilical DIEP perforator.
Fig. 1. Preoperative photograph of a 45-year-old woman with Paget disease of the left breast. Surgical history included abdominal liposuction and bilateral reduction mammaplasty. Her original reconstruction with bilateral tissue expanders was complicated by right breast implant infection requiring removal. She presented for a left breast implant exchange and right DIEP flap reconstruction.
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Fig. 3. Note the extensive central and anterolateral subcutaneous fibrosis from the prior abdominal suction lipectomy.
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction
Fig. 4. Successful harvest of a two-perforator DIEP flap following prior abdominal liposuction. Some fibrosis was encountered in the deep subcutaneous tissue adjacent to the deep fascia; however, the perforators remained patent.
Fig. 6. Intraoperative indocyanine green laser angiogram of zones 2 and 3 of the DIEP flap. A large portion of zone 3 was found to have insufficient perfusion despite appearing adequate on clinical evaluation alone.
Fig. 5. Clinical evaluation of a two-perforator DIEP flap following completion of the dissection. Note the punctate bright red blood at the dermal incision at the junction of zones 3 and 4.
Fig. 7. SPY-Q analysis demonstrating areas of DIEP flap hypoperfusion in the upper lateral and lower lateral aspects of zone 3 of the flap.
start of the procedure to center the flap over the perforators chosen based on preoperative radiographic imaging. It was then repeated once flap elevation had been completed before transfer with excision of areas of hypoperfusion. Once the anastomoses were completed, laser angiography was again used to assess anastomotic patency and adequacy of flap perfusion. Clinical outcomes were compared in DIEP flaps following abdominal suction lipectomy between cases in which laser angiography was used and cases in which flap perfusion was assessed on clinical grounds alone. Outcomes measured included total flap loss rates, partial flap loss rates, fat necrosis rates, anastomotic complications, and abdominal wound complications. Fat necrosis was defined as a stable,
palpable, or radiographically identified area of firmness, creating a mass 1 cm or larger within the confines of the transferred flap tissue. Partial flap loss was defined as subtotal, nonviable soft tissue within the confines of the transferred flap tissue resulting in tissue loss requiring removal using local dressing changes or surgical débridement. Because of the low expected values, statistical analysis was performed using Fisher’s exact test.
RESULTS Five hundred twenty-seven muscle-sparing free TRAM flaps, DIEP flaps, and superficial inferior epigastric artery flaps were performed at the Mayo Clinic in Arizona from July of 2003 through
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No No No No
No
No No No No No No 0 0 0 0 0 0 1 2 2 1 2 1 7 7 3 9 7 9 45 48 51 57 2 3 4 5
Unilateral Unilateral Unilateral Unilateral
Bilateral 36
CTA, computed tomographic angiography; US, duplex ultrasound. *There were no instances of total flap loss. There no anastomotic complications.
CTA CTA CTA CTA CTA CTA None None None None None Preoperatively
Unilateral Unilateral Unilateral Unilateral 42 53 52 55
3 4 5 6 With SPY 1
67 66 Without SPY 1 2
Delayed Delayed Delayed Delayed Immediate Delayed
No Yes No No No No No No No Yes No No Yes Yes 0 50 30 0 30 40 20 1 2 1 2 3 2 2 47 70 70 14 27 29 24 CTA US US CTA CTA CTA CTA None Preoperatively None None None None None Immediate Delayed Delayed Delayed Immediate Delayed Delayed
Follow-Up (mo) Preoperative Imaging Irradiation History DIEP Flap Timing Laterality Age (yr) Patient
Table 1. Case Summary*
January of 2014. Anastomotic complications occurred in 32 cases (6.1 percent). There were 14 total flap losses (2.7 percent). Fat necrosis was identified clinically or radiographically in 59 flaps (11.2 percent). Thirteen DIEP flaps were performed for autologous breast reconstruction following prior abdominal suction lipectomy in 11 patients (summarized in Table 1). Average follow-up was 22 months. All patients underwent preoperative imaging with computed tomographic angiography for perforator assessment and mapping, except one patient who underwent Duplex ultrasonography for preoperative localization. Seven flaps were transferred in six patients who were evaluated intraoperatively for signs of adequate flap perfusion on clinical grounds alone. All cases in which preoperative perforator mapping was performed using computed tomographic angiography showed some evidence of subcutaneous fibrosis caused by previous liposuction (Figs. 2 and 3). All flaps demonstrated sufficient appearing perforators on preoperative radiographic evaluation for possible free tissue transfer. Although all seven flaps were transferred successfully with no anastomotic complications or total flap losses, five of seven flaps (71.4 percent) suffered considerable partial flap loss and fat necrosis. Four of these seven DIEP flaps required subsequent augmentation with either another autologous flap or prosthetic implant to provide sufficient breast volume and contour. The flap volume reduction because of partial flap loss ranged from 0 to 50 percent (mean, 24.3 percent).
No. of Perforators
Fig. 8. Postoperative photograph following successful right DIEP flap reconstruction following prior abdominal liposuction and a left breast implant exchange. No donor-site or flap-related complications developed.
Unilateral Bilateral
Partial Flap Loss (%)
Fat Necrosis
Abdominal Wound Complications
Plastic and Reconstructive Surgery • March 2015
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction Six flaps were performed in five patients that were evaluated intraoperatively with indocyanine green laser angiography. All patients underwent preoperative computed tomographic angiography for planning purposes. Every case demonstrated evidence of subcutaneous fibrosis because of prior liposuction (Figs. 2 and 3); however, all cases appeared to have satisfactory perforators for flap harvest. Intraoperative indocyanine green laser angiography was used at the beginning of the operative procedure to assess the perfusion pattern and extent of perfusion of the desired perforators, allowing flap design to be optimized around the areas of sufficient perfusion. It also guided excision of areas of hypoperfusion following flap harvest. All six flaps were transferred successfully with no anastomotic complications, no total flap losses, and no partial flap loss or fat necrosis. Each of these patients has had successful DIEP flap reconstruction with sufficient breast volume and excellent contours that have not required any operative revision. The amount of tissue resected because of areas of hypoperfusion based on indocyanine green laser angiography findings that appeared clinically viable is difficult to determine because of the retrospective nature of this study. Based on review of the saved intraoperative indocyanine green images and comparison with the operative notes, this is estimated to be 0 to 20 percent (mean 10 percent) of the overall flap volume. The abdominal incisions healed uneventfully in all cases in both subgroups. In evaluating DIEP flaps harvested after abdominal liposuction, there was no difference in the rate of anastomotic complications or total flap loss in those assessed on clinical grounds alone compared to those visualized with indocyanine green laser angiography. There was, however, a statistically significant decrease in the rate of partial flap loss and fat necrosis in those flaps in which laser angiography was used to monitor flap perfusion (p = 0.02). From a cost standpoint, indocyanine green laser angiography is an expensive test. It was used in these cases because they were presumed to be at higher risk for complications based on prior experience. As an adjunct procedure at the time of surgery, the patient’s professional charge in these cases was $264. Supply costs were $527. With a conservative estimate of 10 minutes for its use (at $42 per minute), the total costs for its use in this retrospective analysis is $4991 for each of these six patients. In contrast, the operative costs for subsequent procedures in the clinical examination
group (six patients) were greater. Three patients required operative débridement and closure because of partial flap loss, with charges ranging from $1518 to $5200 (mean, $3006). Four flaps in three patients required at least one further reconstructive procedure (flap or implant) to achieve adequate breast contours and volume (range, one to three procedures; mean, two procedures), with these costs accounting for patient charges of $108,153 (range, $11,905 to $36,480; mean, $18,025.50), without including another patient in whom revision using another flap was recommended.
DISCUSSION The lower abdomen has become a preferred donor site for autologous breast reconstruction. The DIEP flap was developed as a means of transferring large volumes of well-vascularized autologous tissue and minimizing donor-site morbidity. Large studies have documented its safety and efficacy.12 Despite its widespread acceptance in reconstructive surgery and its low total flap loss rates, a review of 17,096 DIEP flaps demonstrated that partial flap loss rates still occur in 0 to 11.1 percent of cases and fat necrosis rates range from 0.5 to 42.9 percent.31 Improvements in flap design and refinements in surgical technique have been made possible by anatomical studies that have increased our knowledge of the blood supply to muscle, subcutaneous fat, and the overlying skin.1–8 Following Kroll and Rosenfield’s description of a perforator flap in 1988, our understanding of tissue perfusion at the microcirculatory level has grown immensely.9 Pioneering work by Taylor et al.5,32 and Saint-Cyr et al.7,8 has aided in ideal DIEP flap design and has helped define the limits of DIEP flap volume that may be reliably transferred based on decreasing numbers of perforators. DIEP flap harvest has been shown to be safe and effective in the presence of many prior abdominal scars.33 Its harvest following previous abdominal suction lipectomy, in contrast, is somewhat controversial. Several small series have demonstrated that it is feasible.15–20 Our early attempts at breast reconstruction using DIEP flaps after suction lipectomy were successful from the perspective of anastomotic patency and no total flap losses. However, we experienced a high partial flap loss rate and a high incidence of fat necrosis, with the majority of these cases requiring further augmentation at a later date with either another autologous flap or prosthetic implant.
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Plastic and Reconstructive Surgery • March 2015 Computed tomographic angiography has been used for DIEP flap planning to evaluate perforator location, define the course of the perforator through the rectus muscle and overlying fascia, expedite the surgical procedure, and optimize flap outcomes.34–38 Computed tomographic angiography does not provide physiologic information regarding blood flow through the visualized perforators. Its resolution at the microcirculatory level is also limited. This provides some insight as to why the partial flap loss and fat necrosis rates in our early DIEP flaps following liposuction were relatively high despite what appeared to be the presence of excellent perforators on preoperative radiographic imaging. Perforator flap perfusion relies on “direct and indirect linking vessels” to supply blood flow to the periphery of the flap.7,8 Abdominal suction lipectomy may have damaged some of these important vessels or limited their appropriate function because of the resultant scarring. Blondeel et al. have demonstrated varied effects of ultrasound-assisted and conventional liposuction on the perforators and microcirculation in the lower abdominal wall.39 In our series, preoperative computed tomographic angiography demonstrated considerable visible scarring in the subcutaneous tissue in all cases (Figs. 2 and 3). Indocyanine green laser angiography is a vascular imaging modality that provides real-time assessment of tissue perfusion. Indocyanine green has many desirable characteristics for intraoperative use. It binds strongly to plasma proteins, causing it to remain in the intravascular space; has a short plasma half-life (3 to 5 minutes); and has an excellent safety profile, making it an ideal agent with which to assess tissue perfusion, particularly when repeated assessments are necessary. It allows early identification of insufficiently perfused tissue that has the potential for postoperative necrosis. Its clinical utility for detecting ischemic tissue and minimizing postoperative complications has been documented in several clinical studies.21–30 Our early experience with DIEP flaps following abdominal suction lipectomy was complicated by relatively high rates of partial flap loss and fat necrosis. This occurred despite preoperative radiologic imaging of suitable perforators and intraoperative clinical examination of the flaps. As such, indocyanine green laser angiography has been used in all subsequent DIEP flap cases in the face of prior liposuction to complement preoperative computed tomographic angiography and intraoperative clinical examination. This has aided in flap design and elevation, and evaluation of areas of sufficient perfusion for inclusion
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in the flap. The use of this intraoperative imaging modality has resulted in the elimination of partial flap losses and fat necrosis in all subsequent cases since the inception of its use. This was found to be statistically significant. Indocyanine green laser angiography allows optimal DIEP flap design around the areas of sufficient perfusion and removal of nonviable tissue, some of which may have appeared viable from a purely clinical standpoint (Figs. 5 through 7). Each of these patients has had successful DIEP flap reconstruction with sufficient breast volume and excellent contours that have not required any operative revision. The use of indocyanine green laser angiography in these cases may have an economic advantage by limiting costs, strictly because subsequent procedures may be avoided in these challenging cases.
CONCLUSIONS Successful DIEP flap harvest and transfer are possible following prior abdominal suction lipectomy. Preoperative imaging with computed tomographic angiography is useful for documentation of sufficient perforators. Abdominal suction lipectomy results in subcutaneous fibrosis and may compromise the peripheral perfusion of harvested DIEP flaps. Clinical inspection of these flaps alone is insufficient to document areas of hypoperfusion that are at risk for postoperative necrosis. Indocyanine green laser angiography is an excellent vascular imaging modality for intraoperative use to assess flap perfusion, and improves outcomes in DIEP flaps when harvested after prior abdominal suction lipectomy. William J. Casey III, M.D. Division of Plastic and Reconstructive Surgery Mayo Clinic in Arizona 5777 East Mayo Boulevard Phoenix, Ariz. 85054 [email protected]
references 1. Manchot C. Die Hautarterien des Menschlichen Korpers. Leipzig: F. C. W. Vogel; 1889. 2. Salmon M. Arteres de la Peau. Paris: Masson et Cie; 1936. 3. McGregor IA, Morgan G. Axial and random pattern flaps. Br J Plast Surg. 1973;26:202–213. 4. Cormack GC, Lamberty BGH. The Arterial Anatomy of Skin Flaps. 2nd ed. Edinburgh: Churchill Livingstone; 1994. 5. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: Experimental study and clinical applications. Br J Plast Surg. 1987;40:113–141. 6. Boyd JB, Taylor GI, Corlett R. The vascular territories of the superior epigastric and the deep inferior epigastric systems. Plast Reconstr Surg. 1984;73:1–16.
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction 7. Saint-Cyr M, Schaverien M, Arbique G, Hatef D, Brown SA, Rohrich RJ. Three- and four-dimensional computed tomographic angiography and venography for the investigation of the vascular anatomy and perfusion of perforator flaps. Plast Reconstr Surg. 2008;121:772–780. 8. Saint-Cyr M, Wong C, Schaverien M, Mojallal A., Rohrich RJ. The perforasome theory: Vascular anatomy and clinical implications. Plast Reconstr Surg. 2009;124:1529–1544. 9. Kroll SS, Rosenfield L. Perforator-based flaps for low posterior midline defects. Plast Reconstr Surg. 1988;81:561–566. 10. Koshima I, Soeda S. Inferior epigastric artery skin flaps without rectus abdominis muscle. Br J Plast Surg. 1989;42:645–648. 11. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg. 1994;32:32–38. 12. Gill PS, Hunt JP, Guerra AB, et al. A 10-year retrospective review of 758 DIEP flaps for breast reconstruction. Plast Reconstr Surg. 2004;113:1153–1160. 13. Nahabedian MY, Momen B, Galdino G, Manson PN. Breast reconstruction with the free TRAM or DIEP flap: Patient selection, choice of flap, and outcome. Plast Reconstr Surg. 2002;110:466–475; discussion 476. 14. Garvey PB, Buchel EW, Pockaj BA, et al. DIEP and pedicled TRAM flaps: A comparison of outcomes. Plast Reconstr Surg. 2006;117:1711–1719. 15. Karanas Y, Santoro T, DaLio A, Shaw WW. Free TRAM flap reconstruction after abdominal liposuction. Plast Reconstr Surg. 2003;112:1851–1854. 16. Godfrey PM, Godfrey NV. Transverse rectus abdominis musculocutaneous flaps after liposuction of the abdomen. Ann Plast Surg. 1994;33:209–210. 17. May JW Jr, Silverman RP, Kaufman JA. Flap perfusion mapping: TRAM flap after abdominal suction-assisted lipectomy. Plast Reconstr Surg. 1999;104:2278–2281. 18. Hess CL, Gartside RL, Ganz JC. TRAM reconstruction after abdominal liposuction. Ann Plast Surg. 2004;53:166–169. 19. De Frene B, Van Landuyt K, Hamdi M, et al. Free DIEAP and SGAP flap breast reconstruction after abdominal/gluteal liposuction. J Plast Reconstr Aesthet Surg. 2006;59:1031–1036. 20. Kim J, Chang D, Temple C, Beahm EK, Robb GL. Free transverse rectus abdominis musculocutaneous flap reconstruction in patients with prior abdominal suction-assisted lipectomy. Plast Reconstr Surg. 2004;113:28e–31e. 21. Munabi NC, Olorunnipa OB, Goltsman D, Rohde CH, Ascherman JA. The ability of intra-operative perfusion mapping with laser-assisted indocyanine green angiography to predict mastectomy flap necrosis in breast reconstruction: A prospective trial. J Plast Reconstr Aesthet Surg. 2014.67:449–455. 22. Duggal CS, Madni T, Losken A. An outcome analysis of intraoperative angiography for postmastectomy breast reconstruction. Aesthet Surg J. 2014;34:61–65. 23. Moyer HR, Losken A. Predicting mastectomy skin flap necrosis with indocyanine green angiography: The gray area defined. Plast Reconstr Surg. 2012;129:1043–1048. 24. Phillips BT, Lanier ST, Conkling N, et al. Intraoperative perfusion techniques can accurately predict mastectomy skin flap necrosis in breast reconstruction: Results of a prospective trial. Plast Reconstr Surg. 2012;129:778e–788e.
25. Komorowska-Timek E, Gurtner GC. Intraoperative perfusion mapping with laser-assisted indocyanine green imaging can predict and prevent complications in immediate breast reconstruction. Plast Reconstr Surg. 2010;125:1065–1073. 26. Newman MI, Samson MC, Tamburrino JF, Swartz KA, Brunworth L. An investigation of the application of laserassisted indocyanine green fluorescent dye angiography in pedicle transverse rectus abdominis myocutaneous breast reconstruction. Can J Plast Surg. 2011;19:e1–e5. 27. Pestana IA, Coan B, Erdmann D, Marcus J, Levin LS, Zenn MR. Early experience with fluorescent angiography in free-tissue transfer reconstruction. Plast Reconstr Surg. 2009;123:1239–1244. 28. Chatterjee A, Krishnan NM, Van Vliet MM, Powell SG, Rosen JM, Ridgway EB. A comparison of free autologous breast reconstruction with and without the use of laser-assisted indocyanine green angiography: A cost-effectiveness analysis. Plast Reconstr Surg. 2013;131:693e–701e. 29. Francisco BS, Kerr-Valentic MA, Agarwal JP. Laser-assisted indocyanine green angiography and DIEP breast reconstruction. Plast Reconstr Surg. 2010;125:116e–118e. 30. Gurtner GC, Jones GE, Neligan PC, et al. Intraoperative laser angiography using the SPY system: Review of the literature and recommendations for use. Ann Surg Innov Res. 2013;7:1. 31. Lie KH, Barker AS, Ashton MW. A classification system for partial and complete DIEP flap necrosis based on a review of 17,096 DIEP flaps in 693 articles including analysis of 152 total flap failures. Plast Reconstr Surg. 2013;132:1401–1408. 32. Taylor GI, Chubb DP, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: Part I. Anatomical location. Plast Reconstr Surg. 2013;132:1447–1456. 33. Hamdi M, Larsen M, Craggs B, Vanmierlo B,Zeltzer A. Harvesting free abdominal perforator flaps in the presence of previous upper abdominal scars. J Plast Reconstr Aesthet Surg. 2014;67:219–225. 34. Rozen WM, Phillips TJ, Ashton MW, Stella DL,Gibson RN, Taylor GI. Preoperative imaging for DIEA perforator flaps: A comparative study of computed tomographic angiography and Doppler ultrasound. Plast Reconstr Surg. 2008;121(Suppl):1–8. 35. Casey WJ III, Chew RT, Rebecca AM, Smith JA,Collins JM, Pockaj BA. Advantages of preoperative computed tomography in deep inferior epigastric artery perforator flap breast reconstruction. Plast Reconstr Surg. 2009;123:1148–1155. 36. Smit JM, Dimopoulou A, Liss AG, et al. Preoperative CT angiography reduces surgery time in perforator flap reconstruction. J Plast Reconstr Aesthet Surg. 2009;62:1112–1117. 37. Scott JR, Liu D, Said H, Neligan PC, Mathes DW. Computed tomographic angiography in planning abdomen-based microsurgical breast reconstruction: A comparison with color duplex ultrasound. Plast Reconstr Surg. 2010;125:446–453. 38. Masia J, Clavero JA, Larranaga JR, Alomar X, Pons G, Serret P. Multidetector-row computed tomography in the planning of abdominal perforator flaps. J Plast Reconstr Aesthet Surg. 2006;59:594–599. 39. Blondeel PN, Derks D, Roche N, Van Landuyt KH,Monstrey SJ. The effect of ultrasound-assisted liposuction and conventional liposuction on the perforator vessels in the lower abdominal wall. Br J Plast Surg. 2003;56:266–271.
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Background: The reliability of deep inferior epigastric artery perforator (DIEP) flap reconstruction following abdominal liposuction is controversial. The authors’ early cases were technically successful; however, they experienced high partial flap loss and fat necrosis rates. The authors sought to compare DIEP flap outcomes in the setting of prior liposuction after the use of intraoperative indocyanine green angiography compared to when flaps were assessed on clinical grounds alone. Methods: A retrospective review of a consecutive series of DIEP flaps following liposuction at a single institution was performed, comparing those evaluated on clinical grounds alone and those in which indocyanine green angiography was used intraoperatively. Outcomes measured included anastomotic complications, total flap loss, partial flap loss, fat necrosis, and postoperative abdominal wounds. Results: Thirteen DIEP flaps following prior liposuction were performed on 11 patients from July of 2003 through January of 2014. All patients had preoperative imaging with duplex ultrasound or computed tomographic angiography to analyze perforator suitability before surgical exploration. Seven flaps were evaluated intraoperatively on clinical grounds alone. Six flaps were assessed and modified based on indocyanine green angiography. All flaps were successful; however, partial flap loss and fat necrosis rates dropped from 71.4 percent to 0 percent when indocyanine green angiography was used intraoperatively (p = 0.02). Conclusions: Indocyanine green angiography is an excellent vascular imaging modality for intraoperative use to assess flap perfusion, and improves outcomes in DIEP flaps when harvested after prior abdominal suction lipectomy. (Plast. Reconstr. Surg. 135: 491e, 2015.)
N
umerous studies over the past century have increased our knowledge of the vascular anatomy of the skin and subcutaneous tissue.1–8 This information has been applied clinically with new flap designs and refinements in surgical techniques resulting in reliable, sophisticated options in reconstructive surgery. The concept of a perforator flap was introduced by Kroll and Rosenfield in 1988.9 They demonstrated that the underlying muscle is a passive carrier for the local perforators and is not essential for flap survival. From the Division of Plastic and Reconstructive Surgery, Mayo Clinic in Arizona; the University of Arizona College of Medicine–Phoenix Campus; and the Division of Plastic and Reconstructive Surgery, Mayo Clinic in Florida. Received for publication May 9, 2014; accepted August 8, 2014. This paper is to be presented at the American Society for Reconstructive Microsurgery Annual Meeting in the Bahamas on January 25, 2015. Copyright © 2015 by the American Society of Plastic Surgeons DOI: 10.1097/PRS.0000000000000964
Perforator flaps have been developed as a means of maximizing the reconstructive surgical results and minimizing donor-site morbidity. The lower abdomen has become a preferred donor site for autologous breast reconstruction. Koshima and Soeda demonstrated that the lower abdominal skin and subcutaneous fat could be harvested for free tissue transfer without the inclusion of the rectus abdominis muscle.10 Allen and Treece subsequently described the deep inferior epigastric perforator (DIEP) flap for breast reconstruction.11 Large series have documented the safety, efficacy, and reliability of the DIEP flap12 and have shown improvements in donor-site morbidity compared with free transverse rectus abdominis myocutaneous (TRAM) and pedicled TRAM flaps.13,14 Disclosure: The authors have no financial disclosures related to the preparation, presentation, or submission of this article.
www.PRSJournal.com
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Plastic and Reconstructive Surgery • March 2015 The reliability of DIEP flap harvest following abdominal suction lipectomy is controversial. Several small case series have demonstrated that successful abdominally based free flap reconstruction is possible in the setting of prior abdominal suction lipectomy.15–20 Our initial experience with DIEP breast reconstruction following abdominal liposuction consisted of seven flaps in six patients. Although all flaps survived, significant partial flap loss or fat necrosis occurred in five of seven flaps (71.4 percent). Indocyanine green laser angiography (SPY Intraoperative Imaging Systems; Novadaq Technologies, Inc., Mississauga, Ontario, Canada) has been used clinically to assess mastectomy skin flap and autologous flap perfusion.21–30 Because of its ability to aid in flap design and elevation, and determining areas of adequate perfusion, we have since used laser angiography in DIEP flap cases when prior abdominal suction lipectomy has been performed. The purpose of this study is to determine whether DIEP flap outcomes are improved when indocyanine green laser angiography is used compared to cases in which it is not used.
of 2003 through January of 2014. DIEP flaps that were harvested and transferred in the setting of prior abdominal suction lipectomy were identified. Radiographic modalities used for perforator mapping as a means of preoperative planning are described. Initially, adequate flap perfusion was assessed intraoperatively on clinical grounds alone (color, Doppler signals, and punctate bleeding from flap edges). Because we experienced relatively high rates of partial flap loss and fat necrosis in DIEP flaps that had previously undergone suction lipectomy, indocyanine green laser angiography was used intraoperatively in all subsequent cases (Figs. 1 through 8). This was performed at the
PATIENTS AND METHODS Following approval from our institutional review board, a retrospective review of all muscle-sparing free TRAM flaps, DIEP flaps, and superficial inferior epigastric artery flaps was performed at the Mayo Clinic in Arizona from July Fig. 2. Preoperative computed tomographic angiogram demonstrating an excellent left periumbilical DIEP perforator.
Fig. 1. Preoperative photograph of a 45-year-old woman with Paget disease of the left breast. Surgical history included abdominal liposuction and bilateral reduction mammaplasty. Her original reconstruction with bilateral tissue expanders was complicated by right breast implant infection requiring removal. She presented for a left breast implant exchange and right DIEP flap reconstruction.
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Fig. 3. Note the extensive central and anterolateral subcutaneous fibrosis from the prior abdominal suction lipectomy.
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction
Fig. 4. Successful harvest of a two-perforator DIEP flap following prior abdominal liposuction. Some fibrosis was encountered in the deep subcutaneous tissue adjacent to the deep fascia; however, the perforators remained patent.
Fig. 6. Intraoperative indocyanine green laser angiogram of zones 2 and 3 of the DIEP flap. A large portion of zone 3 was found to have insufficient perfusion despite appearing adequate on clinical evaluation alone.
Fig. 5. Clinical evaluation of a two-perforator DIEP flap following completion of the dissection. Note the punctate bright red blood at the dermal incision at the junction of zones 3 and 4.
Fig. 7. SPY-Q analysis demonstrating areas of DIEP flap hypoperfusion in the upper lateral and lower lateral aspects of zone 3 of the flap.
start of the procedure to center the flap over the perforators chosen based on preoperative radiographic imaging. It was then repeated once flap elevation had been completed before transfer with excision of areas of hypoperfusion. Once the anastomoses were completed, laser angiography was again used to assess anastomotic patency and adequacy of flap perfusion. Clinical outcomes were compared in DIEP flaps following abdominal suction lipectomy between cases in which laser angiography was used and cases in which flap perfusion was assessed on clinical grounds alone. Outcomes measured included total flap loss rates, partial flap loss rates, fat necrosis rates, anastomotic complications, and abdominal wound complications. Fat necrosis was defined as a stable,
palpable, or radiographically identified area of firmness, creating a mass 1 cm or larger within the confines of the transferred flap tissue. Partial flap loss was defined as subtotal, nonviable soft tissue within the confines of the transferred flap tissue resulting in tissue loss requiring removal using local dressing changes or surgical débridement. Because of the low expected values, statistical analysis was performed using Fisher’s exact test.
RESULTS Five hundred twenty-seven muscle-sparing free TRAM flaps, DIEP flaps, and superficial inferior epigastric artery flaps were performed at the Mayo Clinic in Arizona from July of 2003 through
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No No No No
No
No No No No No No 0 0 0 0 0 0 1 2 2 1 2 1 7 7 3 9 7 9 45 48 51 57 2 3 4 5
Unilateral Unilateral Unilateral Unilateral
Bilateral 36
CTA, computed tomographic angiography; US, duplex ultrasound. *There were no instances of total flap loss. There no anastomotic complications.
CTA CTA CTA CTA CTA CTA None None None None None Preoperatively
Unilateral Unilateral Unilateral Unilateral 42 53 52 55
3 4 5 6 With SPY 1
67 66 Without SPY 1 2
Delayed Delayed Delayed Delayed Immediate Delayed
No Yes No No No No No No No Yes No No Yes Yes 0 50 30 0 30 40 20 1 2 1 2 3 2 2 47 70 70 14 27 29 24 CTA US US CTA CTA CTA CTA None Preoperatively None None None None None Immediate Delayed Delayed Delayed Immediate Delayed Delayed
Follow-Up (mo) Preoperative Imaging Irradiation History DIEP Flap Timing Laterality Age (yr) Patient
Table 1. Case Summary*
January of 2014. Anastomotic complications occurred in 32 cases (6.1 percent). There were 14 total flap losses (2.7 percent). Fat necrosis was identified clinically or radiographically in 59 flaps (11.2 percent). Thirteen DIEP flaps were performed for autologous breast reconstruction following prior abdominal suction lipectomy in 11 patients (summarized in Table 1). Average follow-up was 22 months. All patients underwent preoperative imaging with computed tomographic angiography for perforator assessment and mapping, except one patient who underwent Duplex ultrasonography for preoperative localization. Seven flaps were transferred in six patients who were evaluated intraoperatively for signs of adequate flap perfusion on clinical grounds alone. All cases in which preoperative perforator mapping was performed using computed tomographic angiography showed some evidence of subcutaneous fibrosis caused by previous liposuction (Figs. 2 and 3). All flaps demonstrated sufficient appearing perforators on preoperative radiographic evaluation for possible free tissue transfer. Although all seven flaps were transferred successfully with no anastomotic complications or total flap losses, five of seven flaps (71.4 percent) suffered considerable partial flap loss and fat necrosis. Four of these seven DIEP flaps required subsequent augmentation with either another autologous flap or prosthetic implant to provide sufficient breast volume and contour. The flap volume reduction because of partial flap loss ranged from 0 to 50 percent (mean, 24.3 percent).
No. of Perforators
Fig. 8. Postoperative photograph following successful right DIEP flap reconstruction following prior abdominal liposuction and a left breast implant exchange. No donor-site or flap-related complications developed.
Unilateral Bilateral
Partial Flap Loss (%)
Fat Necrosis
Abdominal Wound Complications
Plastic and Reconstructive Surgery • March 2015
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction Six flaps were performed in five patients that were evaluated intraoperatively with indocyanine green laser angiography. All patients underwent preoperative computed tomographic angiography for planning purposes. Every case demonstrated evidence of subcutaneous fibrosis because of prior liposuction (Figs. 2 and 3); however, all cases appeared to have satisfactory perforators for flap harvest. Intraoperative indocyanine green laser angiography was used at the beginning of the operative procedure to assess the perfusion pattern and extent of perfusion of the desired perforators, allowing flap design to be optimized around the areas of sufficient perfusion. It also guided excision of areas of hypoperfusion following flap harvest. All six flaps were transferred successfully with no anastomotic complications, no total flap losses, and no partial flap loss or fat necrosis. Each of these patients has had successful DIEP flap reconstruction with sufficient breast volume and excellent contours that have not required any operative revision. The amount of tissue resected because of areas of hypoperfusion based on indocyanine green laser angiography findings that appeared clinically viable is difficult to determine because of the retrospective nature of this study. Based on review of the saved intraoperative indocyanine green images and comparison with the operative notes, this is estimated to be 0 to 20 percent (mean 10 percent) of the overall flap volume. The abdominal incisions healed uneventfully in all cases in both subgroups. In evaluating DIEP flaps harvested after abdominal liposuction, there was no difference in the rate of anastomotic complications or total flap loss in those assessed on clinical grounds alone compared to those visualized with indocyanine green laser angiography. There was, however, a statistically significant decrease in the rate of partial flap loss and fat necrosis in those flaps in which laser angiography was used to monitor flap perfusion (p = 0.02). From a cost standpoint, indocyanine green laser angiography is an expensive test. It was used in these cases because they were presumed to be at higher risk for complications based on prior experience. As an adjunct procedure at the time of surgery, the patient’s professional charge in these cases was $264. Supply costs were $527. With a conservative estimate of 10 minutes for its use (at $42 per minute), the total costs for its use in this retrospective analysis is $4991 for each of these six patients. In contrast, the operative costs for subsequent procedures in the clinical examination
group (six patients) were greater. Three patients required operative débridement and closure because of partial flap loss, with charges ranging from $1518 to $5200 (mean, $3006). Four flaps in three patients required at least one further reconstructive procedure (flap or implant) to achieve adequate breast contours and volume (range, one to three procedures; mean, two procedures), with these costs accounting for patient charges of $108,153 (range, $11,905 to $36,480; mean, $18,025.50), without including another patient in whom revision using another flap was recommended.
DISCUSSION The lower abdomen has become a preferred donor site for autologous breast reconstruction. The DIEP flap was developed as a means of transferring large volumes of well-vascularized autologous tissue and minimizing donor-site morbidity. Large studies have documented its safety and efficacy.12 Despite its widespread acceptance in reconstructive surgery and its low total flap loss rates, a review of 17,096 DIEP flaps demonstrated that partial flap loss rates still occur in 0 to 11.1 percent of cases and fat necrosis rates range from 0.5 to 42.9 percent.31 Improvements in flap design and refinements in surgical technique have been made possible by anatomical studies that have increased our knowledge of the blood supply to muscle, subcutaneous fat, and the overlying skin.1–8 Following Kroll and Rosenfield’s description of a perforator flap in 1988, our understanding of tissue perfusion at the microcirculatory level has grown immensely.9 Pioneering work by Taylor et al.5,32 and Saint-Cyr et al.7,8 has aided in ideal DIEP flap design and has helped define the limits of DIEP flap volume that may be reliably transferred based on decreasing numbers of perforators. DIEP flap harvest has been shown to be safe and effective in the presence of many prior abdominal scars.33 Its harvest following previous abdominal suction lipectomy, in contrast, is somewhat controversial. Several small series have demonstrated that it is feasible.15–20 Our early attempts at breast reconstruction using DIEP flaps after suction lipectomy were successful from the perspective of anastomotic patency and no total flap losses. However, we experienced a high partial flap loss rate and a high incidence of fat necrosis, with the majority of these cases requiring further augmentation at a later date with either another autologous flap or prosthetic implant.
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Plastic and Reconstructive Surgery • March 2015 Computed tomographic angiography has been used for DIEP flap planning to evaluate perforator location, define the course of the perforator through the rectus muscle and overlying fascia, expedite the surgical procedure, and optimize flap outcomes.34–38 Computed tomographic angiography does not provide physiologic information regarding blood flow through the visualized perforators. Its resolution at the microcirculatory level is also limited. This provides some insight as to why the partial flap loss and fat necrosis rates in our early DIEP flaps following liposuction were relatively high despite what appeared to be the presence of excellent perforators on preoperative radiographic imaging. Perforator flap perfusion relies on “direct and indirect linking vessels” to supply blood flow to the periphery of the flap.7,8 Abdominal suction lipectomy may have damaged some of these important vessels or limited their appropriate function because of the resultant scarring. Blondeel et al. have demonstrated varied effects of ultrasound-assisted and conventional liposuction on the perforators and microcirculation in the lower abdominal wall.39 In our series, preoperative computed tomographic angiography demonstrated considerable visible scarring in the subcutaneous tissue in all cases (Figs. 2 and 3). Indocyanine green laser angiography is a vascular imaging modality that provides real-time assessment of tissue perfusion. Indocyanine green has many desirable characteristics for intraoperative use. It binds strongly to plasma proteins, causing it to remain in the intravascular space; has a short plasma half-life (3 to 5 minutes); and has an excellent safety profile, making it an ideal agent with which to assess tissue perfusion, particularly when repeated assessments are necessary. It allows early identification of insufficiently perfused tissue that has the potential for postoperative necrosis. Its clinical utility for detecting ischemic tissue and minimizing postoperative complications has been documented in several clinical studies.21–30 Our early experience with DIEP flaps following abdominal suction lipectomy was complicated by relatively high rates of partial flap loss and fat necrosis. This occurred despite preoperative radiologic imaging of suitable perforators and intraoperative clinical examination of the flaps. As such, indocyanine green laser angiography has been used in all subsequent DIEP flap cases in the face of prior liposuction to complement preoperative computed tomographic angiography and intraoperative clinical examination. This has aided in flap design and elevation, and evaluation of areas of sufficient perfusion for inclusion
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in the flap. The use of this intraoperative imaging modality has resulted in the elimination of partial flap losses and fat necrosis in all subsequent cases since the inception of its use. This was found to be statistically significant. Indocyanine green laser angiography allows optimal DIEP flap design around the areas of sufficient perfusion and removal of nonviable tissue, some of which may have appeared viable from a purely clinical standpoint (Figs. 5 through 7). Each of these patients has had successful DIEP flap reconstruction with sufficient breast volume and excellent contours that have not required any operative revision. The use of indocyanine green laser angiography in these cases may have an economic advantage by limiting costs, strictly because subsequent procedures may be avoided in these challenging cases.
CONCLUSIONS Successful DIEP flap harvest and transfer are possible following prior abdominal suction lipectomy. Preoperative imaging with computed tomographic angiography is useful for documentation of sufficient perforators. Abdominal suction lipectomy results in subcutaneous fibrosis and may compromise the peripheral perfusion of harvested DIEP flaps. Clinical inspection of these flaps alone is insufficient to document areas of hypoperfusion that are at risk for postoperative necrosis. Indocyanine green laser angiography is an excellent vascular imaging modality for intraoperative use to assess flap perfusion, and improves outcomes in DIEP flaps when harvested after prior abdominal suction lipectomy. William J. Casey III, M.D. Division of Plastic and Reconstructive Surgery Mayo Clinic in Arizona 5777 East Mayo Boulevard Phoenix, Ariz. 85054 [email protected]
references 1. Manchot C. Die Hautarterien des Menschlichen Korpers. Leipzig: F. C. W. Vogel; 1889. 2. Salmon M. Arteres de la Peau. Paris: Masson et Cie; 1936. 3. McGregor IA, Morgan G. Axial and random pattern flaps. Br J Plast Surg. 1973;26:202–213. 4. Cormack GC, Lamberty BGH. The Arterial Anatomy of Skin Flaps. 2nd ed. Edinburgh: Churchill Livingstone; 1994. 5. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: Experimental study and clinical applications. Br J Plast Surg. 1987;40:113–141. 6. Boyd JB, Taylor GI, Corlett R. The vascular territories of the superior epigastric and the deep inferior epigastric systems. Plast Reconstr Surg. 1984;73:1–16.
Volume 135, Number 3 • DIEP Flap Outcomes after Liposuction 7. Saint-Cyr M, Schaverien M, Arbique G, Hatef D, Brown SA, Rohrich RJ. Three- and four-dimensional computed tomographic angiography and venography for the investigation of the vascular anatomy and perfusion of perforator flaps. Plast Reconstr Surg. 2008;121:772–780. 8. Saint-Cyr M, Wong C, Schaverien M, Mojallal A., Rohrich RJ. The perforasome theory: Vascular anatomy and clinical implications. Plast Reconstr Surg. 2009;124:1529–1544. 9. Kroll SS, Rosenfield L. Perforator-based flaps for low posterior midline defects. Plast Reconstr Surg. 1988;81:561–566. 10. Koshima I, Soeda S. Inferior epigastric artery skin flaps without rectus abdominis muscle. Br J Plast Surg. 1989;42:645–648. 11. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg. 1994;32:32–38. 12. Gill PS, Hunt JP, Guerra AB, et al. A 10-year retrospective review of 758 DIEP flaps for breast reconstruction. Plast Reconstr Surg. 2004;113:1153–1160. 13. Nahabedian MY, Momen B, Galdino G, Manson PN. Breast reconstruction with the free TRAM or DIEP flap: Patient selection, choice of flap, and outcome. Plast Reconstr Surg. 2002;110:466–475; discussion 476. 14. Garvey PB, Buchel EW, Pockaj BA, et al. DIEP and pedicled TRAM flaps: A comparison of outcomes. Plast Reconstr Surg. 2006;117:1711–1719. 15. Karanas Y, Santoro T, DaLio A, Shaw WW. Free TRAM flap reconstruction after abdominal liposuction. Plast Reconstr Surg. 2003;112:1851–1854. 16. Godfrey PM, Godfrey NV. Transverse rectus abdominis musculocutaneous flaps after liposuction of the abdomen. Ann Plast Surg. 1994;33:209–210. 17. May JW Jr, Silverman RP, Kaufman JA. Flap perfusion mapping: TRAM flap after abdominal suction-assisted lipectomy. Plast Reconstr Surg. 1999;104:2278–2281. 18. Hess CL, Gartside RL, Ganz JC. TRAM reconstruction after abdominal liposuction. Ann Plast Surg. 2004;53:166–169. 19. De Frene B, Van Landuyt K, Hamdi M, et al. Free DIEAP and SGAP flap breast reconstruction after abdominal/gluteal liposuction. J Plast Reconstr Aesthet Surg. 2006;59:1031–1036. 20. Kim J, Chang D, Temple C, Beahm EK, Robb GL. Free transverse rectus abdominis musculocutaneous flap reconstruction in patients with prior abdominal suction-assisted lipectomy. Plast Reconstr Surg. 2004;113:28e–31e. 21. Munabi NC, Olorunnipa OB, Goltsman D, Rohde CH, Ascherman JA. The ability of intra-operative perfusion mapping with laser-assisted indocyanine green angiography to predict mastectomy flap necrosis in breast reconstruction: A prospective trial. J Plast Reconstr Aesthet Surg. 2014.67:449–455. 22. Duggal CS, Madni T, Losken A. An outcome analysis of intraoperative angiography for postmastectomy breast reconstruction. Aesthet Surg J. 2014;34:61–65. 23. Moyer HR, Losken A. Predicting mastectomy skin flap necrosis with indocyanine green angiography: The gray area defined. Plast Reconstr Surg. 2012;129:1043–1048. 24. Phillips BT, Lanier ST, Conkling N, et al. Intraoperative perfusion techniques can accurately predict mastectomy skin flap necrosis in breast reconstruction: Results of a prospective trial. Plast Reconstr Surg. 2012;129:778e–788e.
25. Komorowska-Timek E, Gurtner GC. Intraoperative perfusion mapping with laser-assisted indocyanine green imaging can predict and prevent complications in immediate breast reconstruction. Plast Reconstr Surg. 2010;125:1065–1073. 26. Newman MI, Samson MC, Tamburrino JF, Swartz KA, Brunworth L. An investigation of the application of laserassisted indocyanine green fluorescent dye angiography in pedicle transverse rectus abdominis myocutaneous breast reconstruction. Can J Plast Surg. 2011;19:e1–e5. 27. Pestana IA, Coan B, Erdmann D, Marcus J, Levin LS, Zenn MR. Early experience with fluorescent angiography in free-tissue transfer reconstruction. Plast Reconstr Surg. 2009;123:1239–1244. 28. Chatterjee A, Krishnan NM, Van Vliet MM, Powell SG, Rosen JM, Ridgway EB. A comparison of free autologous breast reconstruction with and without the use of laser-assisted indocyanine green angiography: A cost-effectiveness analysis. Plast Reconstr Surg. 2013;131:693e–701e. 29. Francisco BS, Kerr-Valentic MA, Agarwal JP. Laser-assisted indocyanine green angiography and DIEP breast reconstruction. Plast Reconstr Surg. 2010;125:116e–118e. 30. Gurtner GC, Jones GE, Neligan PC, et al. Intraoperative laser angiography using the SPY system: Review of the literature and recommendations for use. Ann Surg Innov Res. 2013;7:1. 31. Lie KH, Barker AS, Ashton MW. A classification system for partial and complete DIEP flap necrosis based on a review of 17,096 DIEP flaps in 693 articles including analysis of 152 total flap failures. Plast Reconstr Surg. 2013;132:1401–1408. 32. Taylor GI, Chubb DP, Ashton MW. True and ‘choke’ anastomoses between perforator angiosomes: Part I. Anatomical location. Plast Reconstr Surg. 2013;132:1447–1456. 33. Hamdi M, Larsen M, Craggs B, Vanmierlo B,Zeltzer A. Harvesting free abdominal perforator flaps in the presence of previous upper abdominal scars. J Plast Reconstr Aesthet Surg. 2014;67:219–225. 34. Rozen WM, Phillips TJ, Ashton MW, Stella DL,Gibson RN, Taylor GI. Preoperative imaging for DIEA perforator flaps: A comparative study of computed tomographic angiography and Doppler ultrasound. Plast Reconstr Surg. 2008;121(Suppl):1–8. 35. Casey WJ III, Chew RT, Rebecca AM, Smith JA,Collins JM, Pockaj BA. Advantages of preoperative computed tomography in deep inferior epigastric artery perforator flap breast reconstruction. Plast Reconstr Surg. 2009;123:1148–1155. 36. Smit JM, Dimopoulou A, Liss AG, et al. Preoperative CT angiography reduces surgery time in perforator flap reconstruction. J Plast Reconstr Aesthet Surg. 2009;62:1112–1117. 37. Scott JR, Liu D, Said H, Neligan PC, Mathes DW. Computed tomographic angiography in planning abdomen-based microsurgical breast reconstruction: A comparison with color duplex ultrasound. Plast Reconstr Surg. 2010;125:446–453. 38. Masia J, Clavero JA, Larranaga JR, Alomar X, Pons G, Serret P. Multidetector-row computed tomography in the planning of abdominal perforator flaps. J Plast Reconstr Aesthet Surg. 2006;59:594–599. 39. Blondeel PN, Derks D, Roche N, Van Landuyt KH,Monstrey SJ. The effect of ultrasound-assisted liposuction and conventional liposuction on the perforator vessels in the lower abdominal wall. Br J Plast Surg. 2003;56:266–271.
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