BREAST 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 Kwok Hao Lie, M.A., M.B., B.Chir. Anthony S. Barker, M.B., B.S., M.Surg. Mark W. Ashton, F.R.A.C.S. Parkville, Victoria, Australia
Background: In a comprehensive review of 17,096 deep inferior epigastric perforator (DIEP) flaps in 693 articles published between the first description of the DIEP flap in 1989 and August of 2011, the authors found that the methods used to categorize partial necrosis and fat necrosis were inconsistent. As a result, these surgical outcomes cannot be meaningfully compared among series and centers. In contrast, complete flap failure is an unambiguous and universally reported outcome that represents only a portion of the entire spectrum of flap necrosis. Methods: The authors created a database of every article with data on DIEP flaps by searching PubMed and Embase for the terms “DIEP,” “DIEAP,” “epigastric AND perforator,” “perforator,” and “flap AND reconstruction” and manually reviewing the 14,480 citations the search generated. The authors then reviewed 693 articles with data on DIEP flaps for incidence and other clinical details of flap loss, partial necrosis, and fat necrosis. Results: The authors found a broad range of definitions of partial and fat necrosis based on different parameters (e.g., percentage of flap lost, area of flap lost, necessity of reoperation) that were not directly comparable. Of 152 documented DIEP flap losses, 67 had reported causes: 40 percent (27 of 67) involved venous problems, 28 percent (19 of 67) arterial, and 21 percent (14 of 67) mechanical (pedicle kinking, hematoma). Conclusions: At present, there is no consensus on the reporting of partial necrosis and flap necrosis. The authors propose a new flap necrosis classification system that prevents ambiguity and allows direct objective comparison of surgical outcomes among centers. (Plast. Reconstr. Surg. 132: 1401, 2013.)
T
he quest for better autologous breast reconstruction with reduced donor-site morbidity and improved surgical outcomes has driven a shift from transverse rectus abdominis myocutaneous (TRAM) flaps to deep inferior epigastric artery perforator (DIEP) flaps.1–13 In this context, flap survival or failure is invariably mentioned as a marker of reconstructive success.14 The literature describes a broad spectrum of complications ranging from nil to fat necrosis to partial flap failure and, finally, total flap failure. Whereas total flap failure is unambiguous and universally reported, From the Taylor Laboratory, Department of Anatomy and Neuroscience, University of Melbourne, Royal Melbourne Hospital. Received for publication April 4, 2013; accepted June 13, 2013. Copyright © 2013 by the American Society of Plastic Surgeons DOI: 10.1097/01.prs.0000434402.06564.bd
our analysis of 17,096 DIEP flaps revealed that the interpretations and reporting of both fat and partial flap necrosis were variable and inconsistent. There is no universally accepted definition or classification of partial necrosis and fat necrosis in DIEP flaps; different authors have defined their inclusion criteria independently. The wide variety of inclusion criteria can be based on clinical presentation (absolute size15,16 versus proportion of flap necrosed17–20) or surgical management (usually incidence of reoperative management1,21–23). This leads to highly variable complication rates that cannot be meaningfully compared among different centers or even case series. In addition, the current classification systems fail to recognize Disclosure: The authors have no financial interest to declare in relation to the content of this article.
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Plastic and Reconstructive Surgery • December 2013 that varying degrees of flap loss require different surgical strategies that will directly affect the subsequent reconstructive result. In contrast with the poorly standardized reporting of fat necrosis and partial flap necrosis, total flap failure is well defined and invariably included when reporting surgical outcomes. DIEP total failure rate ranges from 0 percent24–26 to 10 percent27 in the literature, with most larger series including more than 30 DIEP flaps reporting rates of less than 3 percent.28–30 The largest number of total flap failures in any given series is 11 (2 percent) of 564 DIEP flaps.31 This article is composed of two parts. We first present a metareview on the incidence of the entire spectrum of complications from fat necrosis to partial flap failure and total flap loss. We then propose a new classification system that unequivocally defines and standardizes the complete spectrum of flap necrosis complications.
METHODS We aimed to compile the most comprehensive database of all English-language articles published on the DIEP flap. We conducted multiple Boolean searches of the PubMed and EMBASE databases using the terms “DIEP,” “DIEAP,” and “epigastric AND perforator” in the title, author, and/or abstract, as well as “perforator” and “flap AND reconstruction” in any abstract. We considered only articles in the English language published between January of 1989 (first description of the DIEP flap) and August of 2011 (cutoff month for data collection). The results from each individual search were compiled into a citation database yielding 14,480 citations. We then independently reviewed the individual 14,480 citations. We excluded any citations of articles that did not pertain to plastic surgery (e.g., those that involved molecular biology, physics, engineering, and so on) and articles that specifically focused on one flap type that was not the DIEP flap, yielding 1518 citations. Of these remaining 1518 citations, two authors (K.H.L. and A.S.B.) independently reviewed each article in full. Only the articles with data on one or more DIEP flaps were selected, which resulted in 693 publications in our working database of DIEP flap literature. Each of the 693 published articles in this final DIEP flap literature database was analyzed for total and partial flap failure, as well as definitions and incidence for partial and fat necrosis. For each case of total flap failure, the direct cause, if stated,
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was recorded. Any further surgical management (e.g., another flap) was also noted. Because of the variability of definitions of partial necrosis and fat necrosis, direct comparisons could not be made meaningfully (Fig. 1).
RESULTS There were 98 articles that reported DIEP flaps that experienced partial necrosis and 84 articles that reported DIEP flaps with fat necrosis. Of the articles with DIEP flaps suffering partial necrosis and fat necrosis, only 66 percent (65 of 98) and 52 percent (44 of 84) stated their working definitions of the respective terms. The reported rate of partial flap necrosis ranged from 0 percent23,32–34 to 11.1 percent.19 In the latter case, the article split partial flap necrosis into two categories: less than 20 percent of flap volume and greater than 20 percent of flap volume. No explanation was offered for this particular categorization. The reported rate of fat necrosis ranged from 0.5 percent35 to 42.9 percent.36 Of the two articles, only the former defined fat necrosis as requiring a secondary operation; there was no stated definition for fat necrosis in the latter article. It is interesting that the highest incidence of fat necrosis was reported in the series with the highest combined incidence of obesity, smoking, and radiotherapy (Table 1). In this particular scenario, where the working definitions of partial flap and fat necrosis varied, the standard meta-analysis toolkit could not be meaningfully applied to pool the available data for increased statistical power. Partial necrosis definitions ranged from absolute area,15,16 proportion of flap lost,37 to surgical management.38–40 Some articles also described it as any skin loss caused by ischemia.41 Most authors considered skin loss between 10 and 20 percent17,18,20,42–45 as their cutoff for inclusion, although some authors labeled flaps with less than 5 percent skin loss as “partial necrosis,”46,47 and others categorized skin loss greater than 20 percent as “partial necrosis.”19,35,39,48 Fat necrosis had a range of definitions, including (1) absolute size (lumps >0.5 cm,49 >1 cm,6,25,39,50 >2 cm,15,40,51 >3 cm16 confirmed not to be malignant recurrence) detected clinically or by ultrasound49,52,53 and/or mammography46,54, (2) proportion of volume of flap18,43, and (3) incidence of secondary operations to address fat necrosis..21,22,55–57 Other authors chose to describe necrosis as “minor,”58 “minimal,”59 or “limited.”60 Another variable in fat necrosis reporting was the time frame—many authors reported detection
Volume 132, Number 6 • DIEP Flap Necrosis Classification System
Fig. 1. Exclusion diagram for creating the DIEP literature database.
rates at 239 to 36,15 months after the initial reconstruction, but others reported rates at 1 month41 or even 1 year.61 In the selected 693 articles with data on 17,096 DIEP flaps, there were 152 cases of complete DIEP flap failures (1.12 percent average incidence). Of these, 67 had reported causes while no cause was stated for the other 85 failures. In addition, 40.3 percent (27 of 67) of reported causes were venous in nature, 28.4 percent (19 of 67) of reported causes were related to arterial problems, and 20.9 percent (14 of 67) were mechanical (e.g., hematoma compression, pedicle kinking, and avulsion or injury). (Tables 2 and 3 and Fig. 2). Table 1. Reported Rates of Partial and Fat Necrosis No. of Articles Partial necrosis rate 0% 0.1–4.9% 5.0–9.9% 10+% Fat necrosis incidence 0% 0.1–4.9% 5.0–9.9% 10–14.9% 15–19.9% 20+%
31 (31.6%) 36 (36.7%) 20 (20.4%) 11 (11.2%) 7 (8.3%) 17 (20.2%) 22 (26.2%) 16 (19.0%) 18 (21.4%) 4 (4.8%)
FLAP NECROSIS CLASSIFICATION SYSTEM Our review shows the two main challenges to interpretation of the existing literature are to standardize the reporting of both partial necrosis and fat necrosis by establishing universal grading criteria, and to link clinical presentation to surgical management. In an ideal scenario, this new Table 2. Causes of DIEP Flap Failures: Methods of Secondary Reconstruction after Failed DIEP Flaps Cause of DIEP Flap Failure Pedicle problems Arterial Arterial thrombosis Arterial inflow problem Arterial anastomotic rupture Venous Venous thrombosis Venous congestion Mechanical Hematoma Pedicle kinking Pedicle stretch/avulsion/compression Injury to pedicle during flap raising Poor cosmesis from subtotal necrosis Death or limb amputation Hypercoagulability Reason not stated Total
No. 13 5 1 11 16 5 3 2 4 3 3 1 85 152
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Plastic and Reconstructive Surgery • December 2013 Table 3. Methods Used to Address Failed DIEP Reconstruction of 17 Cases with Data on Follow-Up Care after a Failed DIEP Flap* Method
No.
Another perforator flap
8
Latissimus dorsi flap ± implant
7
Skin expander + implant Not stated
2 135
References Masia et al.,28 Hamdi et al.,34 Levine et al.,55 Flores et al.62 Andree et al.,35 Tønseth et al.,63 Tønseth et al.,64 Dragu et al.65 Georgeu et al.66
*No breasts were left unreconstructed. Each patient was provided with some form of alternative reconstruction.
clinical classification system would allow objective grading of complications and their appropriate clinical management and also enable direct comparison among centers and databases. Hence, we present the classification system shown in Table 4. Five levels of DIEP flap necrosis are suggested that reflect the amount of flap involved and the likely cosmetic sequelae. Grade I represents less than 5 percent of flap involved; grade II, 5 to 15 percent; grade III, 15 to 50 percent; grade IV, greater than 50 percent; and grade V, complete flap loss. Fat necrosis is frequently diagnosed in a clinical setting and without the aid of further imaging techniques such as ultrasonography. It was therefore important to include a corresponding clinical finding despite its inherent variability and subjectivity. The use of less than 5 percent for grade I, 5 to 15 percent for grade II, and 15 to 50 percent for grade III correlates with recommendations for management obtained from the literature review. At these points, surgeons change their preferred method of managing the complications from a conservative method (e.g., patient
Fig. 2. Causes of DIEP flap failures.
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reassurance) to a more proactive approach (e.g., excision of fat necrosis). Grade I necrosis is defined as minimal, having negligible impact on the overall reconstruction; appropriate management in the majority of cases would be conservative and involve patient reassurance. Grade II necrosis is minor but can have subtle effects on the aesthetic of the final result; skin necrosis can leave unsightly scars if untreated, and fat necrosis can cause lumpiness and discomfort (i.e., big enough to require excision but amenable to primary closure or closure by secondary intention, such as granulation). Grade III necrosis is defined as “requires secondary procedures after excision/débridement to achieve satisfactory cosmesis.” Such secondary procedures can include skin grafting and fat injection. Subtotal grade IV necrosis involves such a large portion of the flap that necrosectomy will generally leave a poor and unacceptable result and/or compromise the viability of the reconstruction. This will require either a completely new flap or at least a second flap to address such problems. When presented with grade IV necrosis, some surgeons choose to use secondary flaps to cover local defects,38,39 whereas others prefer to restart the reconstructive process afresh with a new free flap.65,67 General consensus on appropriate management is lacking, but individual decisions should ultimately be decided case by case. Grade V necrosis (i.e., an unviable flap) is commonly referred to as complete flap failure, although grade IV necrosis addressed by flap removal and a new flap has occasionally been labeled as complete flap failure in the literature.65,67 DIEP flaps have both a skin component and a fat component that have different patterns of microvascular supply and can therefore undergo necrosis independently. To facilitate such a distinction when reporting flap necrosis, we also suggest
Volume 132, Number 6 • DIEP Flap Necrosis Classification System Table 4. DIEP Necrosis Classification Prospective Grading Grade I II III IV V
Description
Retrospective Grading
Proportion of Flap Necrosed*
Clinical Findings
50 percent of flap involvement), secondary procedures will involve either an additional local flap or even removal of the original reconstruction and replacement with a completely new flap.65,67 As noted by Caterson and colleagues, “The scope of fat necrosis is difficult to assess because
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Plastic and Reconstructive Surgery • December 2013 there is not a standard gradation system that allows practitioners to compare their results to the literature.”68 There are three broad levels of detection of fat necrosis: patient reported, clinician palpated, and detection through imaging techniques (e.g., ultrasound or mammography). In a series comprising 202 consecutive DIEP flaps, Peeters and colleagues noted a 35 percent (71 of 202) incidence of greater than 5-mm ultrasounddetected fat necrosis, which corresponded to 14 percent (28 of 202) clinical detection and 15 of 71 cases requiring surgical excision.49 There are also three broad levels of intervention required to address fat necrosis: patient reassurance, simple excision, and excision with subsequent procedures to address secondary defects such as loss of volume or contour deformities (e.g., by fat injection or grafting). To further complicate interpretation of the literature, fat necrosis detection has been reported from 141 to 36,15 months to 1 year61 after initial reconstruction. The radiological and ultrasonographic appearance of fat necrosis evolves over time—necrosis and apoptosis of the fat cells requires time to organize into discrete palpable lumps.69,70 In balancing the challenges of arranging regular patient follow-up as opposed to allowing fat necrosis sufficient time to develop, we recommend reporting fat necrosis rates at 3 months after the initial flap reconstruction. Our results demonstrate that grade Vsf total flap failures are frequently attributed to problems with the flap pedicle and the microanastomosis. More than 88 percent of published flap losses are due to problems with the flap pedicle,with 40 percent attributed to venous problems and 28 percent to arterial problems. Other patient factors, such as patient mobility (e.g., stretching,71 strenuous physical activity,62 excessive intraabdominal pressure72), can lead to avulsion and other mechanical complications of the microanastomosis up to a fortnight following reconstruction,62,73 some of which have been successfully salvaged. After a failed DIEP flap, it is interesting that in the 17 published cases of follow-up management, no microsurgeon chose to abandon the reconstructive process and leave the breast unreconstructed—each patient ultimately received either latissimus dorsi flaps, implants under expanded chest wall skin, or a second perforator flap (i.e., second DIEP flap, anterolateral thigh flap, or superior gluteal artery perforator flap). In contrast with grade V complete flap failures, grade I to grade IV flap failures are caused by inadequate microcirculation in limited portions
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of the flap. This is closely related to the microvascular architecture of the flap, and its incidence is caused by suboptimal flap design, including lack of consideration of interzonal and superficial-todeep microvascular communications. Although our proposed prospective classification system serves as a guide to surgical management, it is based on subjective assessment. For any classification of complications that depends on subjective assessment, the inherent risk is of underreporting or downgrading results to improve reported outcomes. This problem is addressed by the inclusion of the retrospective grading that is objective and is based on actual postreconstruction management of complications rather than on direct subjective assessment of outcomes, as is widely used in general surgical and urological fields with the Clavien-Dindo classification.74–76 This will facilitate greater precision in direct comparisons of surgical outcomes.
CONCLUSIONS At present, there is no formal classification of partial necrosis and fat necrosis in DIEP flaps. Reporting is not standardized, and data cannot be meaningfully compared among centers. We propose a significant refinement to the reporting of DIEP flap necrosis on the basis of clinical presentation and amount/component of flap involved (e.g., skin, fat), acceptability of aesthetic outcome, and interventions undertaken to address the problem. This system will allow greater precision in reporting flap necrosis and allow objective comparison of outcomes to be made across a variety of settings. Kwok Hao Lie, M.A., M.B.B.Chir. E533 Medical Building University of Melbourne Grattan Street Parkville, Victoria 3051, Australia [email protected]
ACKNOWLEDGMENTS
The authors thank the team at the Taylor Laboratory, and specifically Russell Corlett, F.R.A.C.S., and Simone Matousek, F.R.A.C.S., for their suggestions and helpful critique of this work. REFERENCES 1. Bajaj AK, Chevray PM, Chang DW. Comparison of donorsite complications and functional outcomes in free musclesparing TRAM flap and free DIEP flap breast reconstruction. Plast Reconstr Surg. 2006;117:737–746; discussion 747. 2. Blondeel N, Vanderstraeten GG, Monstrey SJ, et al. The donor site morbidity of free DIEP flaps and free TRAM flaps for breast reconstruction. Br J Plast Surg. 1997;50:322–330.
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22. Damen TH, Mureau MA, Timman R, Rakhorst HA, Hofer SO. The pleasing end result after DIEP flap breast reconstruction: A review of additional operations. J Plast Reconstr Aesthet Surg. 2009;62:71–76. 23. Drazan L, Vesely J, Hyza P, et al. Bilateral breast reconstruction with DIEP flaps: 4 years’ experience. J Plast Reconstr Aesthet Surg. 2008;61:1309–1315. 24. DellaCroce FJ, Sullivan SK, Trahan C. Stacked deep inferior epigastric perforator flap breast reconstruction: A review of 110 flaps in 55 cases over 3 years. Plast Reconstr Surg. 2011;127:1093–1099. 25. Henry SL, Chang CC, Misra A, Huang JJ, Cheng MH. Inclusion of tissue beyond a midline scar in the deep inferior epigastric perforator flap. Ann Plast Surg. 2011;67:251–254. 26. Visser NJ, Damen TH, Timman R, Hofer SO, Mureau MA. Surgical results, aesthetic outcome, and patient satisfaction after microsurgical autologous breast reconstruction following failed implant reconstruction. Plast Reconstr Surg. 2010;126:26–36. 27. Leonhardt H, Mai R, Pradel W, et al. Free DIEP-flap reconstruction of tumour related defects in head and neck. J Physiol Pharmacol. 2008;59(Suppl 5):59–67. 28. Masià J, Sommario M, Cervelli D, Vega C, León X, Pons G. Extended deep inferior epigastric artery perforator flap for head and neck reconstruction: A clinical experience with 100 patients. Head Neck 2011;33:1328–1334. 29. Nahabedian MY, Momen B. Lower abdominal bulge after deep inferior epigastric perforator flap (DIEP) breast reconstruction. Ann Plast Surg. 2005;54:124–129. 30. Parrett BM, Caterson SA, Tobias AM, Lee BT. DIEP flaps in women with abdominal scars: Are complication rates affected? Plast Reconstr Surg. 2008;121:1527–1531. 31. Enajat M, Rozen WM, Whitaker IS, Smit JM, Acosta R. A single center comparison of one versus two venous anastomoses in 564 consecutive DIEP flaps: Investigating the effect on venous congestion and flap survival. Microsurgery 2010;30:185–191. 32. Beausang ES, McKay D, Brown DH, et al. Deep inferior epigastric artery perforator flaps in head and neck reconstruction. Ann Plast Surg. 2003;51:561–563. 33. Agarwal JP, Gottlieb LJ. Double pedicle deep inferior epigastric perforator/muscle-sparing TRAM flaps for unilateral breast reconstruction. Ann Plast Surg. 2007;58:359–363. 34. Hamdi M, Blondeel P, Van Landuyt K, Tondu T, Monstrey S. Bilateral autogenous breast reconstruction using perforator free flaps: A single center’s experience. Plast Reconstr Surg. 2004;114:83–89; discussion 90. 35. Andree C, Munder BI, Behrendt P, et al. Improved safety of autologous breast reconstruction surgery by stabilisation of microsurgical vessel anastomoses using fibrin sealant in 349 free DIEP or fascia-muscle-sparing (fms)-TRAM flaps: A twocentre study. Breast 2008;17:492–498. 36. Scheer AS, Novak CB, Neligan PC, Lipa JE. Complications associated with breast reconstruction using a perforator flap compared with a free TRAM flap. Ann Plast Surg. 2006;56:355–358. 37. Blondeel PN. One hundred free DIEP flap breast reconstructions: A personal experience. Br J Plast Surg. 1999;52:104–111. 38. de Weerd L, Woerdeman LA, Hage JJ. The lateral thoracodorsal flap as a salvage procedure for partial transverse rectus abdominis myocutaneous or deep inferior epigastric perforator flap loss in breast reconstruction. Ann Plast Surg. 2005;54:590–594. 39. Jandali S, Nelson JA, Sonnad SS, et al. Breast reconstruction with free tissue transfer from the abdomen in the morbidly obese. Plast Reconstr Surg. 2011;127:2206–2213.
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Plastic and Reconstructive Surgery • December 2013 40. Momoh, AO, Colakoglu S, Westvik TS, et al. Analysis of complications and patient satisfaction in pedicled transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flap breast reconstruction. Ann Plast Surg. 2012;69:19–23. 41. Guerra AB, Metzinger SE, Bidros RS, et al. Bilateral breast reconstruction with the deep inferior epigastric perforator (DIEP) flap: An experience with 280 flaps. Ann Plast Surg. 2004;52:246–252. 42. Ali R, Bernier C, Lin YT, et al. Surgical strategies to salvage the venous compromised deep inferior epigastric perforator flap. Ann Plast Surg. 2010;65:398–406. 43. Bailey SH, Saint-Cyr M, Wong C, et al. The single dominant medial row perforator DIEP flap in breast reconstruction: Three-dimensional perforasome and clinical results. Plast Reconstr Surg. 2010;126:739–751. 44. Chevray PM. Breast reconstruction with superficial inferior epigastric artery flaps: A prospective comparison with TRAM and DIEP flaps. Plast Reconstr Surg. 2004;114:1077–1083; discussion 1084. 45. Munhoz AM, Arruda E, Montag E, et al. Immediate skin-sparing mastectomy reconstruction with deep inferior epigastric perforator (DIEP) flap: Technical aspects and outcome. Breast J. 2007;13:470–478. 46. Cheng MH, Robles JA, Ulusal BG, Wei FC. Reliability of zone IV in the deep inferior epigastric perforator flap: A single center’s experience with 74 cases. Breast 2006;15:158–166. 47. de Weerd L, Weum S, Mercer JB. The value of dynamic infrared thermography (DIRT) in perforatorselection and planning of free DIEP flaps. Ann Plast Surg. 2009;63:274–279. 48. Langer S, Munder B, Seidenstuecker K, et al. Development of a surgical algorithm and optimized management of complications—Based on a review of 706 abdominal free flaps for breast reconstruction. Med Sci Monit. 2010;16:CR518–CR522. 49. Peeters WJ, Nanhekhan L, Van Ongeval C, Fabré G, Vandevoort M. Fat necrosis in deep inferior epigastric perforator flaps: An ultrasound-based review of 202 cases. Plast Reconstr Surg. 2009;124:1754–1758. 50. Baumann DP, Lin HY, Chevray PM. Perforator number predicts fat necrosis in a prospective analysis of breast reconstruction with free TRAM, DIEP, and SIEA flaps. Plast Reconstr Surg. 2010;125:1335–1341. 51. Keller A. The deep inferior epigastric perforator free flap for breast reconstruction. Ann Plast Surg. 2001;46:474–479; discussion 479. 52. Bozikov K, Arnez T, Hertl K, Arnez ZM. Fat necrosis in free DIEAP flaps: Incidence, risk, and predictor factors. Ann Plast Surg. 2009;63:138–142. 53. Figus A, Mosahebi A, Ramakrishnan V. Microcirculation in DIEP flaps: A study of the haemodynamics using laser Doppler flowmetry and lightguide reflectance spectrophotometry. J Plast Reconstr Aesthet Surg. 2006;59:604–612; discussion 613. 54. Follmar KE, Prucz RB, Manahan MA, Magarakis M, Rad AN, Rosson GD. Internal mammary intercostal perforators instead of the true internal mammary vessels as the recipient vessels for breast reconstruction. Plast Reconstr Surg. 2011;127:34–40. 55. Levine SM, Lester ME, Fontenot B, Allen RJ Sr. Perforator flap breast reconstruction after unsatisfactory implant reconstruction. Ann Plast Surg. 2011;66:513–517. 56. Garvey PB, Buchel EW, Pockaj BA, Gray RJ, Samson TD. The deep inferior epigastric perforator flap for breast reconstruction in overweight and obese patients. Plast Reconstr Surg. 2005;115:447–457. 57. Gautam AK, Allen RJ Jr, LoTempio MM, et al. Congenital breast deformity reconstruction using perforator flaps. Ann Plast Surg. 2007;58:353–358.
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58. Hsieh F, Kumiponjera D, Malata CM. An algorithmic approach to abdominal flap breast reconstruction in patients with pre-existing scars: Results from a single surgeon’s experience. J Plast Reconstr Aesthet Surg. 2009;62:1650–1660. 59. Jandali S, Nelson JA, Wu LC, Serletti JM. Free transverse rectus abdominis myocutaneous flap for breast reconstruction in patients with prior abdominal contouring procedures. J Reconstr Microsurg. 2010;26:607–614. 60. Matteucci P, Stanley PR, Bates J, Riaz M. Complete absence of lower rectus abdominus muscle and deep inferior epigastric artery complicating free DIEP flap breast reconstruction. J Plast Reconstr Aesthet Surg. 2009;62:e112–e113. 61. Hofer SO, Damen TH, Mureau MA, Rakhorst HA, Roche NA. A critical review of perioperative complications in 175 free deep inferior epigastric perforator flap breast reconstructions. Ann Plast Surg. 2007;59:137–142. 62. Flores JI, Rad AN, Shridharani SM, Stapleton SM, Rosson GD. Saphenous vein grafts for perforator flap salvage in autologous breast reconstruction. Microsurgery 2009;29:236–239. 63. Tønseth KA, Hokland BM, Tindholdt TT, Abyholm FE, Stavem K. Patient-reported outcomes after breast reconstruction with deep inferior epigastric perforator flaps. Scand J Plast Reconstr Surg Hand Surg. 2007;41:173–177. 64. Tønseth KA, Hokland BM, Tindholdt TT, Abyholm FE, Stavem K. Quality of life, patient satisfaction and cosmetic outcome after breast reconstruction using DIEP flap or expandable breast implant. J Plast Reconstr Aesthet Surg. 2008;61:1188–1194. 65. Dragu A, Linke R, Kuwert T, et al. Interesting image: Tc-99m sestamibi SPECT/CT as a new tool for monitoring perfusion and viability of buried perforator based free flaps in breast reconstruction after breast cancer. Clin Nucl Med. 2010;35:36–37. 66. Georgeu GA, Caulfield R, Niranjan N. Salvage of total loss of DIEP and skin envelope in breast reconstruction with tissue expansion. J Plast Reconstr Aesthet Surg. 2009;62:1299–1302. 67. Hamdi M, Andrades P, Thiessen F, et al. Is a second free flap still an option in a failed free flap breast reconstruction? Plast Reconstr Surg. 2010;126:375–384. 68. Caterson SA, Nyame T, Phung T, Lee B, Tobias AM. Pyoderma gangrenosum following bilateral deep inferior epigastric perforator flap breast reconstruction. J Reconstr Microsurg. 2010;26:475–479. 69. Bilgen IG, Ustun EE, Memis A. Fat necrosis of the breast: Clinical, mammographic and sonographic features. Eur J Radiol. 2001;39:92–99. 70. Soo MS, Kornguth PJ, Hertzberg BS. Fat necrosis in the breast: Sonographic features. Radiology 1998;206:261–269. 71. Gahankari D, Malyon A, Weiler-Mithoff EM. Avulsion of vascular anastomosis in free-flap breast reconstruction. Br J Plast Surg. 2001;54:167–168. 72. Lykoudis EG, Ziogas DE, Papanikolaou GE. Vascular pedicle avulsion in free flap breast reconstruction: A case of DIEP flap salvage following early avulsion of venous anastomosis and literature review. Microsurgery 2010;30:233–237. 73. Rao SS, Parikh PM, Goldstein JA, Nahabedian MY. Unilateral failures in bilateral microvascular breast reconstruction. Plast Reconstr Surg. 2010;126:17–25. 74. Clavien PA, Barkun J, de Oliveira ML, et al. The ClavienDindo classification of surgical complications: Five-year experience. Ann Surg. 2009;250:187–196. 75. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–213. 76. Morgan M, Smith N, Thomas K, Murphy DG. Is Clavien the new standard for reporting urological complications? BJU Int. 2009;104:434–436.
Background: In a comprehensive review of 17,096 deep inferior epigastric perforator (DIEP) flaps in 693 articles published between the first description of the DIEP flap in 1989 and August of 2011, the authors found that the methods used to categorize partial necrosis and fat necrosis were inconsistent. As a result, these surgical outcomes cannot be meaningfully compared among series and centers. In contrast, complete flap failure is an unambiguous and universally reported outcome that represents only a portion of the entire spectrum of flap necrosis. Methods: The authors created a database of every article with data on DIEP flaps by searching PubMed and Embase for the terms “DIEP,” “DIEAP,” “epigastric AND perforator,” “perforator,” and “flap AND reconstruction” and manually reviewing the 14,480 citations the search generated. The authors then reviewed 693 articles with data on DIEP flaps for incidence and other clinical details of flap loss, partial necrosis, and fat necrosis. Results: The authors found a broad range of definitions of partial and fat necrosis based on different parameters (e.g., percentage of flap lost, area of flap lost, necessity of reoperation) that were not directly comparable. Of 152 documented DIEP flap losses, 67 had reported causes: 40 percent (27 of 67) involved venous problems, 28 percent (19 of 67) arterial, and 21 percent (14 of 67) mechanical (pedicle kinking, hematoma). Conclusions: At present, there is no consensus on the reporting of partial necrosis and flap necrosis. The authors propose a new flap necrosis classification system that prevents ambiguity and allows direct objective comparison of surgical outcomes among centers. (Plast. Reconstr. Surg. 132: 1401, 2013.)
T
he quest for better autologous breast reconstruction with reduced donor-site morbidity and improved surgical outcomes has driven a shift from transverse rectus abdominis myocutaneous (TRAM) flaps to deep inferior epigastric artery perforator (DIEP) flaps.1–13 In this context, flap survival or failure is invariably mentioned as a marker of reconstructive success.14 The literature describes a broad spectrum of complications ranging from nil to fat necrosis to partial flap failure and, finally, total flap failure. Whereas total flap failure is unambiguous and universally reported, From the Taylor Laboratory, Department of Anatomy and Neuroscience, University of Melbourne, Royal Melbourne Hospital. Received for publication April 4, 2013; accepted June 13, 2013. Copyright © 2013 by the American Society of Plastic Surgeons DOI: 10.1097/01.prs.0000434402.06564.bd
our analysis of 17,096 DIEP flaps revealed that the interpretations and reporting of both fat and partial flap necrosis were variable and inconsistent. There is no universally accepted definition or classification of partial necrosis and fat necrosis in DIEP flaps; different authors have defined their inclusion criteria independently. The wide variety of inclusion criteria can be based on clinical presentation (absolute size15,16 versus proportion of flap necrosed17–20) or surgical management (usually incidence of reoperative management1,21–23). This leads to highly variable complication rates that cannot be meaningfully compared among different centers or even case series. In addition, the current classification systems fail to recognize Disclosure: The authors have no financial interest to declare in relation to the content of this article.
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Plastic and Reconstructive Surgery • December 2013 that varying degrees of flap loss require different surgical strategies that will directly affect the subsequent reconstructive result. In contrast with the poorly standardized reporting of fat necrosis and partial flap necrosis, total flap failure is well defined and invariably included when reporting surgical outcomes. DIEP total failure rate ranges from 0 percent24–26 to 10 percent27 in the literature, with most larger series including more than 30 DIEP flaps reporting rates of less than 3 percent.28–30 The largest number of total flap failures in any given series is 11 (2 percent) of 564 DIEP flaps.31 This article is composed of two parts. We first present a metareview on the incidence of the entire spectrum of complications from fat necrosis to partial flap failure and total flap loss. We then propose a new classification system that unequivocally defines and standardizes the complete spectrum of flap necrosis complications.
METHODS We aimed to compile the most comprehensive database of all English-language articles published on the DIEP flap. We conducted multiple Boolean searches of the PubMed and EMBASE databases using the terms “DIEP,” “DIEAP,” and “epigastric AND perforator” in the title, author, and/or abstract, as well as “perforator” and “flap AND reconstruction” in any abstract. We considered only articles in the English language published between January of 1989 (first description of the DIEP flap) and August of 2011 (cutoff month for data collection). The results from each individual search were compiled into a citation database yielding 14,480 citations. We then independently reviewed the individual 14,480 citations. We excluded any citations of articles that did not pertain to plastic surgery (e.g., those that involved molecular biology, physics, engineering, and so on) and articles that specifically focused on one flap type that was not the DIEP flap, yielding 1518 citations. Of these remaining 1518 citations, two authors (K.H.L. and A.S.B.) independently reviewed each article in full. Only the articles with data on one or more DIEP flaps were selected, which resulted in 693 publications in our working database of DIEP flap literature. Each of the 693 published articles in this final DIEP flap literature database was analyzed for total and partial flap failure, as well as definitions and incidence for partial and fat necrosis. For each case of total flap failure, the direct cause, if stated,
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was recorded. Any further surgical management (e.g., another flap) was also noted. Because of the variability of definitions of partial necrosis and fat necrosis, direct comparisons could not be made meaningfully (Fig. 1).
RESULTS There were 98 articles that reported DIEP flaps that experienced partial necrosis and 84 articles that reported DIEP flaps with fat necrosis. Of the articles with DIEP flaps suffering partial necrosis and fat necrosis, only 66 percent (65 of 98) and 52 percent (44 of 84) stated their working definitions of the respective terms. The reported rate of partial flap necrosis ranged from 0 percent23,32–34 to 11.1 percent.19 In the latter case, the article split partial flap necrosis into two categories: less than 20 percent of flap volume and greater than 20 percent of flap volume. No explanation was offered for this particular categorization. The reported rate of fat necrosis ranged from 0.5 percent35 to 42.9 percent.36 Of the two articles, only the former defined fat necrosis as requiring a secondary operation; there was no stated definition for fat necrosis in the latter article. It is interesting that the highest incidence of fat necrosis was reported in the series with the highest combined incidence of obesity, smoking, and radiotherapy (Table 1). In this particular scenario, where the working definitions of partial flap and fat necrosis varied, the standard meta-analysis toolkit could not be meaningfully applied to pool the available data for increased statistical power. Partial necrosis definitions ranged from absolute area,15,16 proportion of flap lost,37 to surgical management.38–40 Some articles also described it as any skin loss caused by ischemia.41 Most authors considered skin loss between 10 and 20 percent17,18,20,42–45 as their cutoff for inclusion, although some authors labeled flaps with less than 5 percent skin loss as “partial necrosis,”46,47 and others categorized skin loss greater than 20 percent as “partial necrosis.”19,35,39,48 Fat necrosis had a range of definitions, including (1) absolute size (lumps >0.5 cm,49 >1 cm,6,25,39,50 >2 cm,15,40,51 >3 cm16 confirmed not to be malignant recurrence) detected clinically or by ultrasound49,52,53 and/or mammography46,54, (2) proportion of volume of flap18,43, and (3) incidence of secondary operations to address fat necrosis..21,22,55–57 Other authors chose to describe necrosis as “minor,”58 “minimal,”59 or “limited.”60 Another variable in fat necrosis reporting was the time frame—many authors reported detection
Volume 132, Number 6 • DIEP Flap Necrosis Classification System
Fig. 1. Exclusion diagram for creating the DIEP literature database.
rates at 239 to 36,15 months after the initial reconstruction, but others reported rates at 1 month41 or even 1 year.61 In the selected 693 articles with data on 17,096 DIEP flaps, there were 152 cases of complete DIEP flap failures (1.12 percent average incidence). Of these, 67 had reported causes while no cause was stated for the other 85 failures. In addition, 40.3 percent (27 of 67) of reported causes were venous in nature, 28.4 percent (19 of 67) of reported causes were related to arterial problems, and 20.9 percent (14 of 67) were mechanical (e.g., hematoma compression, pedicle kinking, and avulsion or injury). (Tables 2 and 3 and Fig. 2). Table 1. Reported Rates of Partial and Fat Necrosis No. of Articles Partial necrosis rate 0% 0.1–4.9% 5.0–9.9% 10+% Fat necrosis incidence 0% 0.1–4.9% 5.0–9.9% 10–14.9% 15–19.9% 20+%
31 (31.6%) 36 (36.7%) 20 (20.4%) 11 (11.2%) 7 (8.3%) 17 (20.2%) 22 (26.2%) 16 (19.0%) 18 (21.4%) 4 (4.8%)
FLAP NECROSIS CLASSIFICATION SYSTEM Our review shows the two main challenges to interpretation of the existing literature are to standardize the reporting of both partial necrosis and fat necrosis by establishing universal grading criteria, and to link clinical presentation to surgical management. In an ideal scenario, this new Table 2. Causes of DIEP Flap Failures: Methods of Secondary Reconstruction after Failed DIEP Flaps Cause of DIEP Flap Failure Pedicle problems Arterial Arterial thrombosis Arterial inflow problem Arterial anastomotic rupture Venous Venous thrombosis Venous congestion Mechanical Hematoma Pedicle kinking Pedicle stretch/avulsion/compression Injury to pedicle during flap raising Poor cosmesis from subtotal necrosis Death or limb amputation Hypercoagulability Reason not stated Total
No. 13 5 1 11 16 5 3 2 4 3 3 1 85 152
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Plastic and Reconstructive Surgery • December 2013 Table 3. Methods Used to Address Failed DIEP Reconstruction of 17 Cases with Data on Follow-Up Care after a Failed DIEP Flap* Method
No.
Another perforator flap
8
Latissimus dorsi flap ± implant
7
Skin expander + implant Not stated
2 135
References Masia et al.,28 Hamdi et al.,34 Levine et al.,55 Flores et al.62 Andree et al.,35 Tønseth et al.,63 Tønseth et al.,64 Dragu et al.65 Georgeu et al.66
*No breasts were left unreconstructed. Each patient was provided with some form of alternative reconstruction.
clinical classification system would allow objective grading of complications and their appropriate clinical management and also enable direct comparison among centers and databases. Hence, we present the classification system shown in Table 4. Five levels of DIEP flap necrosis are suggested that reflect the amount of flap involved and the likely cosmetic sequelae. Grade I represents less than 5 percent of flap involved; grade II, 5 to 15 percent; grade III, 15 to 50 percent; grade IV, greater than 50 percent; and grade V, complete flap loss. Fat necrosis is frequently diagnosed in a clinical setting and without the aid of further imaging techniques such as ultrasonography. It was therefore important to include a corresponding clinical finding despite its inherent variability and subjectivity. The use of less than 5 percent for grade I, 5 to 15 percent for grade II, and 15 to 50 percent for grade III correlates with recommendations for management obtained from the literature review. At these points, surgeons change their preferred method of managing the complications from a conservative method (e.g., patient
Fig. 2. Causes of DIEP flap failures.
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reassurance) to a more proactive approach (e.g., excision of fat necrosis). Grade I necrosis is defined as minimal, having negligible impact on the overall reconstruction; appropriate management in the majority of cases would be conservative and involve patient reassurance. Grade II necrosis is minor but can have subtle effects on the aesthetic of the final result; skin necrosis can leave unsightly scars if untreated, and fat necrosis can cause lumpiness and discomfort (i.e., big enough to require excision but amenable to primary closure or closure by secondary intention, such as granulation). Grade III necrosis is defined as “requires secondary procedures after excision/débridement to achieve satisfactory cosmesis.” Such secondary procedures can include skin grafting and fat injection. Subtotal grade IV necrosis involves such a large portion of the flap that necrosectomy will generally leave a poor and unacceptable result and/or compromise the viability of the reconstruction. This will require either a completely new flap or at least a second flap to address such problems. When presented with grade IV necrosis, some surgeons choose to use secondary flaps to cover local defects,38,39 whereas others prefer to restart the reconstructive process afresh with a new free flap.65,67 General consensus on appropriate management is lacking, but individual decisions should ultimately be decided case by case. Grade V necrosis (i.e., an unviable flap) is commonly referred to as complete flap failure, although grade IV necrosis addressed by flap removal and a new flap has occasionally been labeled as complete flap failure in the literature.65,67 DIEP flaps have both a skin component and a fat component that have different patterns of microvascular supply and can therefore undergo necrosis independently. To facilitate such a distinction when reporting flap necrosis, we also suggest
Volume 132, Number 6 • DIEP Flap Necrosis Classification System Table 4. DIEP Necrosis Classification Prospective Grading Grade I II III IV V
Description
Retrospective Grading
Proportion of Flap Necrosed*
Clinical Findings
50 percent of flap involvement), secondary procedures will involve either an additional local flap or even removal of the original reconstruction and replacement with a completely new flap.65,67 As noted by Caterson and colleagues, “The scope of fat necrosis is difficult to assess because
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Plastic and Reconstructive Surgery • December 2013 there is not a standard gradation system that allows practitioners to compare their results to the literature.”68 There are three broad levels of detection of fat necrosis: patient reported, clinician palpated, and detection through imaging techniques (e.g., ultrasound or mammography). In a series comprising 202 consecutive DIEP flaps, Peeters and colleagues noted a 35 percent (71 of 202) incidence of greater than 5-mm ultrasounddetected fat necrosis, which corresponded to 14 percent (28 of 202) clinical detection and 15 of 71 cases requiring surgical excision.49 There are also three broad levels of intervention required to address fat necrosis: patient reassurance, simple excision, and excision with subsequent procedures to address secondary defects such as loss of volume or contour deformities (e.g., by fat injection or grafting). To further complicate interpretation of the literature, fat necrosis detection has been reported from 141 to 36,15 months to 1 year61 after initial reconstruction. The radiological and ultrasonographic appearance of fat necrosis evolves over time—necrosis and apoptosis of the fat cells requires time to organize into discrete palpable lumps.69,70 In balancing the challenges of arranging regular patient follow-up as opposed to allowing fat necrosis sufficient time to develop, we recommend reporting fat necrosis rates at 3 months after the initial flap reconstruction. Our results demonstrate that grade Vsf total flap failures are frequently attributed to problems with the flap pedicle and the microanastomosis. More than 88 percent of published flap losses are due to problems with the flap pedicle,with 40 percent attributed to venous problems and 28 percent to arterial problems. Other patient factors, such as patient mobility (e.g., stretching,71 strenuous physical activity,62 excessive intraabdominal pressure72), can lead to avulsion and other mechanical complications of the microanastomosis up to a fortnight following reconstruction,62,73 some of which have been successfully salvaged. After a failed DIEP flap, it is interesting that in the 17 published cases of follow-up management, no microsurgeon chose to abandon the reconstructive process and leave the breast unreconstructed—each patient ultimately received either latissimus dorsi flaps, implants under expanded chest wall skin, or a second perforator flap (i.e., second DIEP flap, anterolateral thigh flap, or superior gluteal artery perforator flap). In contrast with grade V complete flap failures, grade I to grade IV flap failures are caused by inadequate microcirculation in limited portions
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of the flap. This is closely related to the microvascular architecture of the flap, and its incidence is caused by suboptimal flap design, including lack of consideration of interzonal and superficial-todeep microvascular communications. Although our proposed prospective classification system serves as a guide to surgical management, it is based on subjective assessment. For any classification of complications that depends on subjective assessment, the inherent risk is of underreporting or downgrading results to improve reported outcomes. This problem is addressed by the inclusion of the retrospective grading that is objective and is based on actual postreconstruction management of complications rather than on direct subjective assessment of outcomes, as is widely used in general surgical and urological fields with the Clavien-Dindo classification.74–76 This will facilitate greater precision in direct comparisons of surgical outcomes.
CONCLUSIONS At present, there is no formal classification of partial necrosis and fat necrosis in DIEP flaps. Reporting is not standardized, and data cannot be meaningfully compared among centers. We propose a significant refinement to the reporting of DIEP flap necrosis on the basis of clinical presentation and amount/component of flap involved (e.g., skin, fat), acceptability of aesthetic outcome, and interventions undertaken to address the problem. This system will allow greater precision in reporting flap necrosis and allow objective comparison of outcomes to be made across a variety of settings. Kwok Hao Lie, M.A., M.B.B.Chir. E533 Medical Building University of Melbourne Grattan Street Parkville, Victoria 3051, Australia [email protected]
ACKNOWLEDGMENTS
The authors thank the team at the Taylor Laboratory, and specifically Russell Corlett, F.R.A.C.S., and Simone Matousek, F.R.A.C.S., for their suggestions and helpful critique of this work. REFERENCES 1. Bajaj AK, Chevray PM, Chang DW. Comparison of donorsite complications and functional outcomes in free musclesparing TRAM flap and free DIEP flap breast reconstruction. Plast Reconstr Surg. 2006;117:737–746; discussion 747. 2. Blondeel N, Vanderstraeten GG, Monstrey SJ, et al. The donor site morbidity of free DIEP flaps and free TRAM flaps for breast reconstruction. Br J Plast Surg. 1997;50:322–330.
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