IS HOLM ZONE III SAFE FROM FAT NECROSIS IN MEDIAL ROW PERFORATOR-BASED DEEP INFERIOR EPIGASTRIC PERFORATOR FLAPS? KYEONG-TAE LEE, M.D.,1 JEONG-EON LEE, M.D., Ph.D.,2 SEOK-JIN NAM, M.D., Ph.D.,2 BOO-KYUNG HAN, M.D., Ph.D.,3 and GOO-HYUN MUN, M.D., Ph.D.1*
Background: This study investigated which zonal tissue would be more secure from the risk of fat necrosis between Holm zones II and III and examined the risk factors of fat necrosis in a clinical series of medial row perforator-based deep inferior epigastric artery perforator (DIEP) flaps. Patients and Methods: A retrospective chart review was performed for patients undergoing unilateral breast reconstructions with medial row perforator DIEP flaps. Data regarding patients, operation-related characteristics, and complications including fat necrosis were collected. Fat necrosis was mainly diagnosed by ultrasound examination, and its location was also assessed. Results: A total of 103 cases were analyzed. Fat necrosis was diagnosed in 13.6% of patients and developed more frequently in zone III (7.8%) than in zone II (4.9%). In risk factor analysis, the inset rate, the weight ratio of the inset flap to harvested flap, was significantly associated with the development of fat necrosis. The flaps with inset rates more than 79% showed 16 times higher risk of fat necrosis than those below 79% in multivariate analysis. The incidence of fat necrosis in zone III was significantly increased in the high inset rate group when compared with the low inset rate group, whereas the incidence in zone II did not change. Conclusions: In unilateral breast reconstruction using medial row perforator DIEP flaps, fat necrosis developed more frequently in zone III than in zone II, and this tendency was more prominent in high inset rate group. Not transferring excessive contralateral tissue including lateral zone III tissue might be helpful for C 2014 Wiley Periodicals, Inc. Microsurgery 35:272–278, 2015. reducing the risk of fat necrosis. V
Since
the deep inferior epigastric artery perforator (DIEP) flap was first introduced for breast reconstruction in 1994,1 it has been a main stream in autologous breast reconstruction.2 It contains not only the advantages of abdominal-based flaps, such as the ability of providing abundant tissue with a softness that is similar to the breast tissue, but also its original strength of low donor morbidity. However, a relatively high rate of fat necrosis remains one of the main disadvantages.3–5 Many efforts have been attempted to reduce the development of fat necrosis, and several risk factors have been reported.3,5–9 However, the problem of fat necrosis has remained unsolved. According to recent cadaver studies, the perforasomes of the DIEP flaps were different based on the perforator rows, namely, lateral row and medial row.10–12 The flaps based on lateral row perforators tended to have higher perfusion in ipsilateral tissue than in contralateral tissue, 1 Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea 2 Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea 3 Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea Financial Disclosure: None of the authors has a financial interest in any of the products, devices, or drugs mentioned in this manuscript. *Correspondence to: Goo-Hyun Mun, M.D., Ph.D., Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Ilwon-Dong 50, Gangnam-Gu, Seoul 135-710, South Korea. E-mail: [email protected] Received 13 April 2014; Revision accepted 4 August 2014; Accepted 29 August 2014 Published online 16 September 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22328
Ó 2014 Wiley Periodicals, Inc.
following the Holm’s perfusion zone classification (Fig. 1), whereas those based on medial row perforators showed relatively larger vascular territory to the contralateral tissue than to the ipsilateral tissue, which is similar to the classical Hartramph perfusion zone. In the clinical series, there is little controversy regarding the relatively higher affinity of lateral row perforators to the Holm zone II than zone III. However, debates remain regarding the perforasomes of the medial row perforators, and it is still uncertain whether the contralateral zone III tissue actually has better perfusion than zone II or not. In contrast with those cadaver studies, some clinical perfusion studies demonstrated similar vascularity between zones II and III or even higher perfusion indices in zone II than in zone III even in medial row perforator-based DIEP flaps.13,14 Despite these conflicting results between the cadaver study and the clinical perfusion study, clinical outcome studies regarding this topic have been sparse. In most of the previous clinical studies of DIEP flaps, both medial and lateral row perforator-based flaps were included15 or the zonal position of fat necrosis lesions were not identified,12 which make it difficult to compare those of zones II and III. Otherwise, only a very small number of patients were included.10 In this study, the authors reviewed their clinical experience and outcomes in cases of medial row perforator DIEP flaps for unilateral breast reconstruction to evaluate which zonal tissue would be more secure from the risk of fat necrosis between Holm zone II and zone III. We also investigated the risk factors for fat necrosis and their
Risk of Fat Necrosis in Holm Zone III
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After insetting and revascularizing the entire portion of harvested flaps, flap trimming was performed. Nearly the entire zone IV region was discarded in all cases, and a variable amount of zone II and zone III tissue was removed until bright colored bleeding was observed, with consideration of the amount of tissue needed. Diagnosis of Fat Necrosis
Figure 1. An illustration of Holm’s zonal classification. The red line indicates the pedicle of the DIEP flap.
impacts on the distribution pattern of fat necrosis development.
Fat necrosis was primarily diagnosed by ultrasound examination. The ultrasound examination was routinely performed by radiologists for cancer surveillance at least 6 months postoperatively. Cystic or solid lesions with diameters exceeding 5 mm were diagnosed as fat necrosis in ultrasound examination. In patients not receiving postoperative ultrasound examination, the diagnosis of fat necrosis depended on a physical examination performed by an attending reconstructive surgeon. The location of fat necrosis was also assessed by matching the ultrasound examination reports with operation records.
PATIENTS AND METHODS
A retrospective chart review was performed for consecutive patients who underwent unilateral breast reconstruction using DIEP flaps from June 2009 to December 2012. All reconstructive surgeries were performed by the senior author (G.-H.M.). The cases using lateral row perforators or both medial and lateral row perforators, those using bipedicled flap by intraflap crossover anastomosis, and those having infraumbilical vertical scars that could interrupt the perfusion of the contralateral tissues were excluded. Surgical Technique
Before the flap harvest, optimal perforators were mapped, and the volume of contralateral breasts was measured by checking preoperative computed tomography angiography (CTA) to estimate the weight of tissue needed for reconstruction and DIEP flaps to be harvested. When harvesting the flaps, the contralateral side from the reconstructed breasts of deep inferior epigastric artery was chosen as a main pedicle. The superficial inferior epigastric vein (SIEV) of the contralateral side from the main pedicle (ipsilateral side of the reconstructed breasts) was routinely harvested at an adequate length for microvascular anastomosis. The internal mammary vessels were used as recipient vessels. Venous augmentation with SIEV was selectively performed in those situations, which was determined by an attending surgeon, for cases needing a high inset rate or with dark red bleeding after main anastomosis from the zone III regions where needed to be included. Inset rate was defined as the ratio of the final weight of the flap transferred to the weight of the flap harvested initially. In brief, it was the weight ratio of the inset flap to harvested flap and presented as percentage (%).
Statistical Analyses
The incidence of fat necrosis was compared across the perfusion zones by v2 test. In the analysis of risk factors of fat necrosis, patient demographics and operationrelated data were analyzed with univariate analysis followed by multivariate analysis. For the risk factors showing statistical significance in the previous analysis, a subgroup analysis was also conducted to evaluate their potential impacts on the distribution of fat necrosis location. For univariate analysis, Fisher’s exact test was used in categorical variable examination, and Student’s t-test or Mann-Whitney test was used in continuous variable analysis. A P-value of 0.05; Table 1). Analysis of Risk Factors of Fat Necrosis Development
In univariate analysis, inset rate was significantly different between the cases with fat necrosis and those without fat necrosis (P 5 0.012; Table 2). Regarding the association between inset rate and fat necrosis, the incidence of fat necrosis significantly increased with higher inset rate of the flap. Receiver operating characteristic curve analysis was performed to identify the cutoff value of inset rate, and maximal statistical significance was achieved at an inset rate of 79.0% (P 5 0.020). The cases with inset rates below 79% showed a significantly lower rate of fat necrosis than those with rates more than 79.0% (8.3% vs. 36.8%, P 5 0.004; Table 3). An approximate image of flaps having inset rates of 79% was reconstructed by DICOM viewer software (Osirix version 5.7, Pixmeo, Switzerland) based on volumetry data (Fig. 2). According to that image, a flap with an inset rate of 79% corresponded to all of zone I, most of zone II, and about 80% of zone III. Multivariate logistic regression analysis was performed with all variables that could influence the development of fat necrosis including age, BMI, smoking, Pfannenstiel incision scars, venous augmentation, ischemic time, perforator number, postoperative radiation, and inset rate, either as a continuous variable or as a categorical variable divided by a threshold value of 79%. As a result, no variables demonstrated a significant impact on fat necrosis formation except inset rate. High inset rate was an independent risk factor for the development of fat necrosis both as a continuous variable (P 5 0.018) and as a categorical variable (P 5 0.001). The cases having inset rates more than 79% had an almost 16 times higher risk of fat necrosis, independently, than those having inset rates below 79% (odds ratio 5 16.083; 95% confidence interval 5 2.933–88.187; Table 4). Subgroup Analysis in Cases Having High Inset Rate Over Threshold Value
Subgroup analysis was performed in the patients with a high inset rate, which was a greater than the threshold value of 79%, to evaluate any possible protective factors or risk factors to fat necrosis formation. No variables showed a significant effect on fat necrosis formation. The presence of Pfannenstiel incision scars (P 5 0.227) or venous augmentation (P 5 0.378) did not have any significant protective effect on the development of fat necrosis. Although incorporation of multiple perforators showed a trend toward decreasing incidence of fat necrosis in low
Risk of Fat Necrosis in Holm Zone III Table 3. Analysis of Association Between Inset Rate and Fat Necrosis Fat necrosis (%) Inset rate As a continuous variable Trend association Below 60% (n 5 34) 60–80% (n 5 52) Above 80% (n 5 17) As a categorical variable Below 79% (n 5 84) Above 79% (n 5 19)
P-value 0.012 0.008
1 (2.9%) 8 (15.4%) 5 (29.4%) 0.004 7 (8.3%) 7 (36.8%)
Figure 2. The image of a flap with an inset rate of 79%, reconstructed by DICOM viewer software (Osirix) with reference to volumetry data. The inset rate 79% corresponded to the entire zone I, most of zone II, and about 80% of zone III tissue. The green area indicates the flaps of inset rate 79%, and the red area beyond the green zone indicates a potential “ danger zone” showing a high risk of fat necrosis development.
inset rate group, it failed to reduce the fat necrosis rate in high inset rate group (P 5 0.570; Table 5). Regarding the location of fat necrosis, the inset rate showed a significant influence on the distribution of fat necrosis. The rate of fat necrosis in zone II was similar between high inset rate and low inset rate groups, whereas that in zone III was significantly different between them. The high inset rate group had much higher incidence of fat necrosis in zone III when compared with low inset rate group (27.8% vs. 3.6%; Table 6). DISCUSSION
There has been a lot of discussion regarding the vascular reliability of contralateral tissue in DIEP flaps for
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breast reconstruction. Despite some cadaver studies demonstrating that the medial row perforators had relatively larger vascular territory to contralateral tissue than lateral row perforators,10,11 perfusion-related complications of zone III were encountered not infrequently in the clinical series of medial row perforator DIEP flaps.9,16 To the best of our knowledge, whether zone III was actually safer from the development of fat necrosis than zone II in medial row perforator DIEP flaps was not yet clinically proven in substantial series. In this study, fat necrosis developed more frequently in zone III rather than zone II, suggesting that zone III could have less reliable perfusion than zone II in medial row-based DIEP flaps, which is contradictory to the previous assumption. Moreover, the difference in fat necrosis rates between zones II and III was more prominent in the high inset rate group (5.6% vs. 27.8%) than in the low inset rate group (4.8% vs. 3.6%). Given that more lateral tissues were recruited when requiring transfers of flaps with high inset rate, the results could be interpreted as evidence that fat necrosis more frequently developed in the lateral zone III tissue. Thus, it can be assumed that not all of zone III tissue is well perfused and that the lateral part of zone III has less reliable perfusion in the medial row perforator DIEP flaps. There have been many anatomical and clinical experimental studies supporting our results of less reliable perfusion in zone III tissue. Some anatomical studies demonstrated that more vascular connections existed between ipsilateral zones than across the midline and that the sum of the external diameter of all communicating vessels between zones I and II was significantly larger than those between zones I and III,17,18 suggesting the possibility of more rapid and efficient blood supply from zone I to zone II than to contralateral zone III. Moreover, all clinical experimental studies published so far reported that ipsilateral zone II tissue had at least a similar and even higher blood supply than zone III tissue (Table 7).13–16,19 Although the reason why previous cadaver angiography studies showed different results is unclear, some hypothesis suggested by Rahmanian-Schwarz et al.13 could be helpful. The function of communicating vessels between the zones may be maintained properly under the control of several local and systemic mediators that exist only in living tissue. According to Figure 2, almost entire portion of zone I and II and about 80% of zone III may have a reliable perfusion in medial row perforator-based DIEP flaps. This pattern is very similar to the image of “the best vascularized parts of the lower abdominal wall” in the study by Eric et al.18, in which most of zone II and only part of zone III were included. Our territory was slightly larger than theirs, as the vascular territory in clinical situations can be larger than that in cadaver studies generally.10 In the current Microsurgery DOI 10.1002/micr
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Table 4. Multivariate Analysis of Risk Factors for Fat Necrosis Development Fat necrosis
Variable
P-value Odds ratio
Age BMI Smoking Pfannenstiel incision scar Venous augmentation Ischemic time Perforator numbers Adjuvant radiation Inset rate As a continuous variable As a categorical variable
95% confidence interval
0.120 0.571 0.999 0.998 0.857 0.358 0.605 0.271
0.923 1.075
0.834–1.021 0.837–1.381
0.860 1.014 0.825 3.516
0.167–4.429 0.985–1.043 0.398–1.709 0.375–32.977
0.018 0.001
1.081 16.083
1.013–1.153 2.933–88.187
BMI, body mass index.
Table 5. The Effect of Venous Supercharging and Harvesting More Perforators on Fat Necrosis Flap of inset rate below 79%
Flap of inset rate above 79%
PFat necrosis Fat necrosis rate (%) value rate (%) P-value Venous augmentation (1) (2) Inclusion of perforator Two or more perforators One perforator
10.0 8.1
0.603
50.0 30.8
0.378
3.1
0.173
40.0
0.570
11.5
33.3
Table 6. Location of Fat Necrosis Lesions No fat necrosis
Zone II
Zone III
Patients with 77 (91.7%) 4 (4.8%) 3 (3.6%) inset rate below 79% Patients with 12 (66.7%) 1 (5.6%) 5 (27.8%) inset rate above 79%
P-value 0.002
study, the risk of fat necrosis increased steeply in the flaps having inset rates higher than 79%. The extra tissues beyond this area can have less reliable perfusion and may be regarded as “danger zone.” The results of risk factor analysis for fat necrosis were also interesting. All possible risk factors mentioned in previous studies, including BMI, perforator numbers, ischemic time, adjuvant radiotherapy, and weight of inset flaps, did not have a significant impact on fat necrosis except inset rate. The high inset rate was significantly associated with the development of fat necrosis. Given that excessively large flap transfer can also lead to perfusion-related complications including partial flap loss in other kinds of perforator flaps,20–22 our results seem to be as expected. Too much tissue burden for blood supply by a limited number of perforators can result in a lessperfused tissue area and fat necrosis. Meanwhile, the absolute weight of the inset flap itself was not correlated with fat necrosis in this study, which was consistent with the findings of previous studies.23,24 It could be suggested that transfer of flap tissue beyond its perforasome, rather than the absolute tissue volume, gives rise to the development of fat necrosis formation. Although the inset rate of 79% was suggested to be a threshold value in this study, the value can be changed depending on various situations including cases with vertical scars or harvested flaps perfused by a different row of perforators. Infraumbilical vertical scars interrupt blood perfusion across the scars,17,25 and the reliable inset rate of flaps may be reduced. In the cases of lateral row perforator DIEP flaps, the contralateral tissue may have a less reliable blood supply, leading to a lower threshold value than those of medial row perforator DIEP flaps. In contrast, the combination of medial and lateral row perforators or the use of bipedicled DIEP flaps can produce a larger vascular territory,26 and a threshold value of inset rate can be elevated beyond our threshold of 79%. Interestingly, in subgroup analysis for the high inset rate group, no factor significantly influenced the development of fat necrosis. Actually, the authors expected that venous augmentation or harvesting more medial row
Table 7. The Previous Clinical Experimental Studies Regarding Perfusion in DIEP Flaps Perfusion index (Mean 6 SD) Reports 15
Holm et al. Schrey et al.16 Tindholdt et al.19 Rahmanian-Schwarz et al.13 Medial row perforator-based DIEP flap Lateral row perforator-based DIEP flap Losken et al.14
Microsurgery DOI 10.1002/micr
Patient number
Measuring instruments
Zone II
Zone III
15 9 10 16
Indocyanine green video angiography Positron emission tomography Laser Doppler perfusion imaging Micro-Lightguide spectrophotometer
52.1 6 22.6 2.69 6 1.13 39.9 6 9.2
33.4 6 20.3 2.43 6 1.34 35.1 6 10.3
53.6 6 20.3 59.7 6 22.3 21.81 6 8.0
46.4 6 18.7 59.4 6 17.7 20.73 6 11.1
18
Indocyanine green video angiography
Risk of Fat Necrosis in Holm Zone III
perforators might be helpful for reducing the fat necrosis rate in the high inset rate group; however, it was not. There have been several studies reporting the association between venous drainage and the development of fat necrosis.27–29 Gravvanis et al.27 also demonstrated the potential significance of good capacity of venous drainage of perforator complex and resolution of intraoperative congestion using additional SIEV anastomosis. However, the previous studies regarding the efficacy of venous augmentation have mainly focused on its role as a “lifeboat” to salvage the intraoperative congestion, which commonly occurred in superficially dominant flaps,27,30–32 and its potential role on reducing the fat necrosis in the flaps having high inset rate has not yet been clear. The current study suggests that venous augmentation alone does not have a significantly protective influence on fat necrosis formation in flaps with high inset rate. Prospective anatomical and clinical studies will be required to answer this question. In addition, little is known of the potential effect of the inclusion of larger numbers of medial row perforators on the perfusion of contralateral zone III in DIEP flaps. Baumann et al.3 showed that flaps having three to five perforators had significantly lower incidences of fat necrosis than those having one or two perforators, although medial and lateral row perforators were all combined in their study. In the current study, similar results were observed in the group with inset rates below 79%. However, harvesting more medial perforators did not reduce the fat necrosis rate in high inset rate group. It can be assumed that although inclusion of more medial row perforators can secure the vascular reliability within the perforasome, it would not augment the perfusion of vulnerable contralateral tissue, especially including lateral zone III tissue, and would not expand the safe perforasome. Furthermore, larger clinical studies would be ideal for more solid conclusions. A few options can be suggested when a large amount of contralateral tissue is required. Bipedicled flap harvest could be considered for safe transfer of high inset rate flaps. In our center, when the transfer of an excessively large proportion of flap, including total zone III and even part of zone IV tissue, is expected in volumetric analysis by preoperative CTA or when infraumbilical vertical scars are present, we perform a bipedicled flap harvest. Actually, seven cases of bipedicled flaps were harvested during the same study period, although they were not included based on the exclusion criteria. The fat necrosis rate (14.3%) of the bipedicled flap group was similar to that of the medial row perforator group, whereas the mean inset rate was much higher (79.8 vs. 66.0). The simultaneous use of implants with DIEP flaps can be suggested as a good option in optimizing large breast reconstruction.33 We can also reduce the inset rate of
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flaps by performing reduction mammaplasty of the contralateral side if the patients want smaller breasts. This study is limited by the relatively small number of cases and the retrospective study design. Moreover, our study populations had a lower average BMI when compared with the western people and did not include any patients with obesity, which can make it difficult to generalize the results. Large, prospective, and multicenter studies would be required to obtain more solid conclusions. One of the strengths of this study is the homogenous characteristics of the cases. Inclusion of only medial row perforator DIEP flaps and exclusion of cases having infraumbilical vertical scars can be helpful for reducing confounding effects and acquiring more focused conclusions. Furthermore, by using ultrasound examination, more accurate diagnosis and analysis with more reliable data were possible.34 CONCLUSIONS
In the medial row perforator-based DIEP flaps for unilateral breast reconstructions, fat necrosis developed more frequently in the contralateral zone III than in the ipsilateral zone II. The lateral portion of zone III tissue may not be safe from the development of fat necrosis. High inset rate more than 79% was significantly associated with the development of fat necrosis. Not transferring an excessively large proportion of contralateral tissue, especially lateral zone III tissue, can minimize the risk of fat necrosis in medial row perforator DIEP flap breast reconstruction.
REFERENCES 1. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg 1994;32:32–38. 2. Chang DW. Breast reconstruction with microvascular MS-TRAM and DIEP flaps. Arch Plast Surg 2012;39:3–10. 3. 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. 4. Khansa I, Momoh AO, Patel PP, Nguyen JT, Miller MJ, Lee BT. Fat necrosis in autologous abdomen-based breast reconstruction: A systematic review. Plast Reconstr Surg 2013;131:443–452. 5. Nahabedian MY, Tsangaris T, Momen B. Breast reconstruction with the DIEP flap or the muscle-sparing (MS-2) free TRAM flap: Is there a difference? Plast Reconstr Surg 2005;115:436–444; discussion 445–446. 6. Rogers NE, Allen RJ. Radiation effects on breast reconstruction with the deep inferior epigastric perforator flap. Plast Reconstr Surg 2002;109:1919–1924; discussion 1925–1926. 7. 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 90–92. 8. 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.
Microsurgery DOI 10.1002/micr
278
Lee et al.
9. Lee KT, Lee JE, Nam SJ, Mun GH. Ischaemic time and fat necrosis in breast reconstruction with a free deep inferior epigastric perforator flap. J Plast Reconstr Aesthet Surg 2013;66:174–181. 10. Bailey SH, Saint-Cyr M, Wong C, Mojallal A, Zhang K, Ouyang D, Arbique G, Trussler A, Rohrich RJ. The single dominant medial row perforator DIEP flap in breast reconstruction: Three-dimensional perforasome and clinical results. Plast Reconstr Surg 2010;126:739– 751. 11. Schaverien M, Saint-Cyr M, Arbique G, Brown SA. Arterial and venous anatomies of the deep inferior epigastric perforator and superficial inferior epigastric artery flaps. Plast Reconstr Surg 2008; 121:1909–1919. 12. Garvey PB, Salavati S, Feng L, Butler CE. Perfusion-related complications are similar for DIEP and muscle-sparing free TRAM flaps harvested on medial or lateral deep inferior epigastric artery branch perforators for breast reconstruction. Plast Reconstr Surg 2011;128: 581e–589e. 13. Rahmanian-Schwarz A, Rothenberger J, Hirt B, Luz O, Schaller HE. A combined anatomical and clinical study for quantitative analysis of the microcirculation in the classic perfusion zones of the deep inferior epigastric artery perforator flap. Plast Reconstr Surg 2011; 127:505–513. 14. Losken A, Zenn MR, Hammel JA, Walsh MW, Carlson GW. Assessment of zonal perfusion using intraoperative angiography during abdominal flap breast reconstruction. Plast Reconstr Surg 2012; 129:618e–624e. 15. Holm C, Mayr M, Hofter E, Ninkovic M. Perfusion zones of the DIEP flap revisited: A clinical study. Plast Reconstr Surg 2006;117: 37–43. 16. Schrey A, Kinnunen I, Kalliokoski K, Minn H, Grenman R, Vahlberg T, Niemi T, Suominen E, Aitasalo K. Perfusion in free breast reconstruction flap zones assessed with positron emission tomography. Microsurgery 2010;30:430–436. 17. Ohjimi H, Era K, Fujita T, Tanaka T, Yabuuchi R. Analyzing the vascular architecture of the free TRAM flap using intraoperative ex vivo angiography. Plast Reconstr Surg 2005;116:106–113. 18. Eric M, Ravnik D, Zic R, Dragnic N, Krivokuca D, Leksan I, Hribernik M. Deep inferior epigastric perforator flap: An anatomical study of the perforators and local vascular differences. Microsurgery 2012;32:43–49. 19. Tindholdt TT, Saidian S, Tonseth KA. Microcirculatory evaluation of deep inferior epigastric artery perforator flaps with laser Doppler perfusion imaging in breast reconstruction. J Plast Surg Hand Surg 2011;45:143–147. 20. Hwang JH, Lim SY, Pyon JK, Bang SI, Oh KS, Mun GH. Reliable harvesting of a large thoracodorsal artery perforator flap with emphasis on perforator number and spacing. Plast Reconstr Surg 2011;128:140e–150e.
Microsurgery DOI 10.1002/micr
21. Kim JT. Latissimus dorsi perforator flap. Clin Plast Surg 2003;30: 403–431. 22. Mosahebi A, Disa JJ, Pusic AL, Cordeiro PG, Mehrara BJ. The use of the extended anterolateral thigh flap for reconstruction of massive oncologic defects. Plast Reconstr Surg 2008;122:492–496. 23. Booi DI, Debats IB, Boeckx WD, van der Hulst RR. Risk factors and blood flow in the free transverse rectus abdominis (TRAM) flap: Smoking and high flap weight impair the free TRAM flap microcirculation. Ann Plast Surg 2007;59:364–371. 24. Gill PS, Hunt JP, Guerra AB, Dellacroce FJ, Sullivan SK, Boraski J, Metzinger SE, Dupin CL, Allen RJ. A 10-year retrospective review of 758 DIEP flaps for breast reconstruction. Plast Reconstr Surg 2004;113:1153–1160. 25. Han S, Sup Eom J, Ho Kim D. Effects of the abdominal midline incision on the survival of the transverse rectus abdominis musculocutaneous flap in rat model. Ann Plast Surg 2003;50:171–176. 26. Xu H, Dong J, Wang T. Bipedicle deep inferior epigastric perforator flap for unilateral breast reconstruction: Seven years’ experience. Plast Reconstr Surg 2009;124:1797–1807. 27. Gravvanis A, Tsoutsos D, Papanikolaou G, Diab A, Lambropoulou P, Karakitsos D. Refining perforator selection for deep inferior epigastric perforator flap: The impact of the dominant venous perforator. Microsurgery 2014;34:169–176. 28. Tran NV, Buchel EW, Convery PA. Microvascular complications of DIEP flaps. Plast Reconstr Surg 2007;119:1397–1405; discussion 1406–1408. 29. Blondeel PN, Arnstein M, Verstraete K, Depuydt K, Van Landuyt KH, Monstrey SJ, Kroll SS. Venous congestion and blood flow in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps. Plast Reconstr Surg 2000;106:1295–1299. 30. Boutros SG. Double venous system drainage in deep inferior epigastric perforator flap breast reconstruction: A single-surgeon experience. Plast Reconstr Surg 2013;131:671–676. 31. Xin Q, Luan J, Mu H, Mu L. Augmentation of venous drainage in deep inferior epigastric perforator flap breast reconstruction: Efficacy and advancement. J Reconstr Microsurg 2012;28:313–318. 32. Rothenberger J, Amr A, Schiefer J, Schaller HE, RahmanianSchwarz A. A quantitative analysis of the venous outflow of the deep inferior epigastric flap (DIEP) based on the perforator veins and the efficiency of superficial inferior epigastric vein (SIEV) supercharging. J Plast Reconstr Aesthet Surg 2013;66:67–72. 33. Figus A, Canu V, Iwuagwu FC, Ramakrishnan V. DIEP flap with implant: A further option in optimising breast reconstruction. J Plast Reconstr Aesthet Surg 2009;62:1118–1126. 34. Peeters WJ, Nanhekhan L, Van Ongeval C, Fabre 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.
Background: This study investigated which zonal tissue would be more secure from the risk of fat necrosis between Holm zones II and III and examined the risk factors of fat necrosis in a clinical series of medial row perforator-based deep inferior epigastric artery perforator (DIEP) flaps. Patients and Methods: A retrospective chart review was performed for patients undergoing unilateral breast reconstructions with medial row perforator DIEP flaps. Data regarding patients, operation-related characteristics, and complications including fat necrosis were collected. Fat necrosis was mainly diagnosed by ultrasound examination, and its location was also assessed. Results: A total of 103 cases were analyzed. Fat necrosis was diagnosed in 13.6% of patients and developed more frequently in zone III (7.8%) than in zone II (4.9%). In risk factor analysis, the inset rate, the weight ratio of the inset flap to harvested flap, was significantly associated with the development of fat necrosis. The flaps with inset rates more than 79% showed 16 times higher risk of fat necrosis than those below 79% in multivariate analysis. The incidence of fat necrosis in zone III was significantly increased in the high inset rate group when compared with the low inset rate group, whereas the incidence in zone II did not change. Conclusions: In unilateral breast reconstruction using medial row perforator DIEP flaps, fat necrosis developed more frequently in zone III than in zone II, and this tendency was more prominent in high inset rate group. Not transferring excessive contralateral tissue including lateral zone III tissue might be helpful for C 2014 Wiley Periodicals, Inc. Microsurgery 35:272–278, 2015. reducing the risk of fat necrosis. V
Since
the deep inferior epigastric artery perforator (DIEP) flap was first introduced for breast reconstruction in 1994,1 it has been a main stream in autologous breast reconstruction.2 It contains not only the advantages of abdominal-based flaps, such as the ability of providing abundant tissue with a softness that is similar to the breast tissue, but also its original strength of low donor morbidity. However, a relatively high rate of fat necrosis remains one of the main disadvantages.3–5 Many efforts have been attempted to reduce the development of fat necrosis, and several risk factors have been reported.3,5–9 However, the problem of fat necrosis has remained unsolved. According to recent cadaver studies, the perforasomes of the DIEP flaps were different based on the perforator rows, namely, lateral row and medial row.10–12 The flaps based on lateral row perforators tended to have higher perfusion in ipsilateral tissue than in contralateral tissue, 1 Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea 2 Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea 3 Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Gangnam-Gu, Seoul, South Korea Financial Disclosure: None of the authors has a financial interest in any of the products, devices, or drugs mentioned in this manuscript. *Correspondence to: Goo-Hyun Mun, M.D., Ph.D., Department of Plastic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Ilwon-Dong 50, Gangnam-Gu, Seoul 135-710, South Korea. E-mail: [email protected] Received 13 April 2014; Revision accepted 4 August 2014; Accepted 29 August 2014 Published online 16 September 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22328
Ó 2014 Wiley Periodicals, Inc.
following the Holm’s perfusion zone classification (Fig. 1), whereas those based on medial row perforators showed relatively larger vascular territory to the contralateral tissue than to the ipsilateral tissue, which is similar to the classical Hartramph perfusion zone. In the clinical series, there is little controversy regarding the relatively higher affinity of lateral row perforators to the Holm zone II than zone III. However, debates remain regarding the perforasomes of the medial row perforators, and it is still uncertain whether the contralateral zone III tissue actually has better perfusion than zone II or not. In contrast with those cadaver studies, some clinical perfusion studies demonstrated similar vascularity between zones II and III or even higher perfusion indices in zone II than in zone III even in medial row perforator-based DIEP flaps.13,14 Despite these conflicting results between the cadaver study and the clinical perfusion study, clinical outcome studies regarding this topic have been sparse. In most of the previous clinical studies of DIEP flaps, both medial and lateral row perforator-based flaps were included15 or the zonal position of fat necrosis lesions were not identified,12 which make it difficult to compare those of zones II and III. Otherwise, only a very small number of patients were included.10 In this study, the authors reviewed their clinical experience and outcomes in cases of medial row perforator DIEP flaps for unilateral breast reconstruction to evaluate which zonal tissue would be more secure from the risk of fat necrosis between Holm zone II and zone III. We also investigated the risk factors for fat necrosis and their
Risk of Fat Necrosis in Holm Zone III
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After insetting and revascularizing the entire portion of harvested flaps, flap trimming was performed. Nearly the entire zone IV region was discarded in all cases, and a variable amount of zone II and zone III tissue was removed until bright colored bleeding was observed, with consideration of the amount of tissue needed. Diagnosis of Fat Necrosis
Figure 1. An illustration of Holm’s zonal classification. The red line indicates the pedicle of the DIEP flap.
impacts on the distribution pattern of fat necrosis development.
Fat necrosis was primarily diagnosed by ultrasound examination. The ultrasound examination was routinely performed by radiologists for cancer surveillance at least 6 months postoperatively. Cystic or solid lesions with diameters exceeding 5 mm were diagnosed as fat necrosis in ultrasound examination. In patients not receiving postoperative ultrasound examination, the diagnosis of fat necrosis depended on a physical examination performed by an attending reconstructive surgeon. The location of fat necrosis was also assessed by matching the ultrasound examination reports with operation records.
PATIENTS AND METHODS
A retrospective chart review was performed for consecutive patients who underwent unilateral breast reconstruction using DIEP flaps from June 2009 to December 2012. All reconstructive surgeries were performed by the senior author (G.-H.M.). The cases using lateral row perforators or both medial and lateral row perforators, those using bipedicled flap by intraflap crossover anastomosis, and those having infraumbilical vertical scars that could interrupt the perfusion of the contralateral tissues were excluded. Surgical Technique
Before the flap harvest, optimal perforators were mapped, and the volume of contralateral breasts was measured by checking preoperative computed tomography angiography (CTA) to estimate the weight of tissue needed for reconstruction and DIEP flaps to be harvested. When harvesting the flaps, the contralateral side from the reconstructed breasts of deep inferior epigastric artery was chosen as a main pedicle. The superficial inferior epigastric vein (SIEV) of the contralateral side from the main pedicle (ipsilateral side of the reconstructed breasts) was routinely harvested at an adequate length for microvascular anastomosis. The internal mammary vessels were used as recipient vessels. Venous augmentation with SIEV was selectively performed in those situations, which was determined by an attending surgeon, for cases needing a high inset rate or with dark red bleeding after main anastomosis from the zone III regions where needed to be included. Inset rate was defined as the ratio of the final weight of the flap transferred to the weight of the flap harvested initially. In brief, it was the weight ratio of the inset flap to harvested flap and presented as percentage (%).
Statistical Analyses
The incidence of fat necrosis was compared across the perfusion zones by v2 test. In the analysis of risk factors of fat necrosis, patient demographics and operationrelated data were analyzed with univariate analysis followed by multivariate analysis. For the risk factors showing statistical significance in the previous analysis, a subgroup analysis was also conducted to evaluate their potential impacts on the distribution of fat necrosis location. For univariate analysis, Fisher’s exact test was used in categorical variable examination, and Student’s t-test or Mann-Whitney test was used in continuous variable analysis. A P-value of 0.05; Table 1). Analysis of Risk Factors of Fat Necrosis Development
In univariate analysis, inset rate was significantly different between the cases with fat necrosis and those without fat necrosis (P 5 0.012; Table 2). Regarding the association between inset rate and fat necrosis, the incidence of fat necrosis significantly increased with higher inset rate of the flap. Receiver operating characteristic curve analysis was performed to identify the cutoff value of inset rate, and maximal statistical significance was achieved at an inset rate of 79.0% (P 5 0.020). The cases with inset rates below 79% showed a significantly lower rate of fat necrosis than those with rates more than 79.0% (8.3% vs. 36.8%, P 5 0.004; Table 3). An approximate image of flaps having inset rates of 79% was reconstructed by DICOM viewer software (Osirix version 5.7, Pixmeo, Switzerland) based on volumetry data (Fig. 2). According to that image, a flap with an inset rate of 79% corresponded to all of zone I, most of zone II, and about 80% of zone III. Multivariate logistic regression analysis was performed with all variables that could influence the development of fat necrosis including age, BMI, smoking, Pfannenstiel incision scars, venous augmentation, ischemic time, perforator number, postoperative radiation, and inset rate, either as a continuous variable or as a categorical variable divided by a threshold value of 79%. As a result, no variables demonstrated a significant impact on fat necrosis formation except inset rate. High inset rate was an independent risk factor for the development of fat necrosis both as a continuous variable (P 5 0.018) and as a categorical variable (P 5 0.001). The cases having inset rates more than 79% had an almost 16 times higher risk of fat necrosis, independently, than those having inset rates below 79% (odds ratio 5 16.083; 95% confidence interval 5 2.933–88.187; Table 4). Subgroup Analysis in Cases Having High Inset Rate Over Threshold Value
Subgroup analysis was performed in the patients with a high inset rate, which was a greater than the threshold value of 79%, to evaluate any possible protective factors or risk factors to fat necrosis formation. No variables showed a significant effect on fat necrosis formation. The presence of Pfannenstiel incision scars (P 5 0.227) or venous augmentation (P 5 0.378) did not have any significant protective effect on the development of fat necrosis. Although incorporation of multiple perforators showed a trend toward decreasing incidence of fat necrosis in low
Risk of Fat Necrosis in Holm Zone III Table 3. Analysis of Association Between Inset Rate and Fat Necrosis Fat necrosis (%) Inset rate As a continuous variable Trend association Below 60% (n 5 34) 60–80% (n 5 52) Above 80% (n 5 17) As a categorical variable Below 79% (n 5 84) Above 79% (n 5 19)
P-value 0.012 0.008
1 (2.9%) 8 (15.4%) 5 (29.4%) 0.004 7 (8.3%) 7 (36.8%)
Figure 2. The image of a flap with an inset rate of 79%, reconstructed by DICOM viewer software (Osirix) with reference to volumetry data. The inset rate 79% corresponded to the entire zone I, most of zone II, and about 80% of zone III tissue. The green area indicates the flaps of inset rate 79%, and the red area beyond the green zone indicates a potential “ danger zone” showing a high risk of fat necrosis development.
inset rate group, it failed to reduce the fat necrosis rate in high inset rate group (P 5 0.570; Table 5). Regarding the location of fat necrosis, the inset rate showed a significant influence on the distribution of fat necrosis. The rate of fat necrosis in zone II was similar between high inset rate and low inset rate groups, whereas that in zone III was significantly different between them. The high inset rate group had much higher incidence of fat necrosis in zone III when compared with low inset rate group (27.8% vs. 3.6%; Table 6). DISCUSSION
There has been a lot of discussion regarding the vascular reliability of contralateral tissue in DIEP flaps for
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breast reconstruction. Despite some cadaver studies demonstrating that the medial row perforators had relatively larger vascular territory to contralateral tissue than lateral row perforators,10,11 perfusion-related complications of zone III were encountered not infrequently in the clinical series of medial row perforator DIEP flaps.9,16 To the best of our knowledge, whether zone III was actually safer from the development of fat necrosis than zone II in medial row perforator DIEP flaps was not yet clinically proven in substantial series. In this study, fat necrosis developed more frequently in zone III rather than zone II, suggesting that zone III could have less reliable perfusion than zone II in medial row-based DIEP flaps, which is contradictory to the previous assumption. Moreover, the difference in fat necrosis rates between zones II and III was more prominent in the high inset rate group (5.6% vs. 27.8%) than in the low inset rate group (4.8% vs. 3.6%). Given that more lateral tissues were recruited when requiring transfers of flaps with high inset rate, the results could be interpreted as evidence that fat necrosis more frequently developed in the lateral zone III tissue. Thus, it can be assumed that not all of zone III tissue is well perfused and that the lateral part of zone III has less reliable perfusion in the medial row perforator DIEP flaps. There have been many anatomical and clinical experimental studies supporting our results of less reliable perfusion in zone III tissue. Some anatomical studies demonstrated that more vascular connections existed between ipsilateral zones than across the midline and that the sum of the external diameter of all communicating vessels between zones I and II was significantly larger than those between zones I and III,17,18 suggesting the possibility of more rapid and efficient blood supply from zone I to zone II than to contralateral zone III. Moreover, all clinical experimental studies published so far reported that ipsilateral zone II tissue had at least a similar and even higher blood supply than zone III tissue (Table 7).13–16,19 Although the reason why previous cadaver angiography studies showed different results is unclear, some hypothesis suggested by Rahmanian-Schwarz et al.13 could be helpful. The function of communicating vessels between the zones may be maintained properly under the control of several local and systemic mediators that exist only in living tissue. According to Figure 2, almost entire portion of zone I and II and about 80% of zone III may have a reliable perfusion in medial row perforator-based DIEP flaps. This pattern is very similar to the image of “the best vascularized parts of the lower abdominal wall” in the study by Eric et al.18, in which most of zone II and only part of zone III were included. Our territory was slightly larger than theirs, as the vascular territory in clinical situations can be larger than that in cadaver studies generally.10 In the current Microsurgery DOI 10.1002/micr
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Table 4. Multivariate Analysis of Risk Factors for Fat Necrosis Development Fat necrosis
Variable
P-value Odds ratio
Age BMI Smoking Pfannenstiel incision scar Venous augmentation Ischemic time Perforator numbers Adjuvant radiation Inset rate As a continuous variable As a categorical variable
95% confidence interval
0.120 0.571 0.999 0.998 0.857 0.358 0.605 0.271
0.923 1.075
0.834–1.021 0.837–1.381
0.860 1.014 0.825 3.516
0.167–4.429 0.985–1.043 0.398–1.709 0.375–32.977
0.018 0.001
1.081 16.083
1.013–1.153 2.933–88.187
BMI, body mass index.
Table 5. The Effect of Venous Supercharging and Harvesting More Perforators on Fat Necrosis Flap of inset rate below 79%
Flap of inset rate above 79%
PFat necrosis Fat necrosis rate (%) value rate (%) P-value Venous augmentation (1) (2) Inclusion of perforator Two or more perforators One perforator
10.0 8.1
0.603
50.0 30.8
0.378
3.1
0.173
40.0
0.570
11.5
33.3
Table 6. Location of Fat Necrosis Lesions No fat necrosis
Zone II
Zone III
Patients with 77 (91.7%) 4 (4.8%) 3 (3.6%) inset rate below 79% Patients with 12 (66.7%) 1 (5.6%) 5 (27.8%) inset rate above 79%
P-value 0.002
study, the risk of fat necrosis increased steeply in the flaps having inset rates higher than 79%. The extra tissues beyond this area can have less reliable perfusion and may be regarded as “danger zone.” The results of risk factor analysis for fat necrosis were also interesting. All possible risk factors mentioned in previous studies, including BMI, perforator numbers, ischemic time, adjuvant radiotherapy, and weight of inset flaps, did not have a significant impact on fat necrosis except inset rate. The high inset rate was significantly associated with the development of fat necrosis. Given that excessively large flap transfer can also lead to perfusion-related complications including partial flap loss in other kinds of perforator flaps,20–22 our results seem to be as expected. Too much tissue burden for blood supply by a limited number of perforators can result in a lessperfused tissue area and fat necrosis. Meanwhile, the absolute weight of the inset flap itself was not correlated with fat necrosis in this study, which was consistent with the findings of previous studies.23,24 It could be suggested that transfer of flap tissue beyond its perforasome, rather than the absolute tissue volume, gives rise to the development of fat necrosis formation. Although the inset rate of 79% was suggested to be a threshold value in this study, the value can be changed depending on various situations including cases with vertical scars or harvested flaps perfused by a different row of perforators. Infraumbilical vertical scars interrupt blood perfusion across the scars,17,25 and the reliable inset rate of flaps may be reduced. In the cases of lateral row perforator DIEP flaps, the contralateral tissue may have a less reliable blood supply, leading to a lower threshold value than those of medial row perforator DIEP flaps. In contrast, the combination of medial and lateral row perforators or the use of bipedicled DIEP flaps can produce a larger vascular territory,26 and a threshold value of inset rate can be elevated beyond our threshold of 79%. Interestingly, in subgroup analysis for the high inset rate group, no factor significantly influenced the development of fat necrosis. Actually, the authors expected that venous augmentation or harvesting more medial row
Table 7. The Previous Clinical Experimental Studies Regarding Perfusion in DIEP Flaps Perfusion index (Mean 6 SD) Reports 15
Holm et al. Schrey et al.16 Tindholdt et al.19 Rahmanian-Schwarz et al.13 Medial row perforator-based DIEP flap Lateral row perforator-based DIEP flap Losken et al.14
Microsurgery DOI 10.1002/micr
Patient number
Measuring instruments
Zone II
Zone III
15 9 10 16
Indocyanine green video angiography Positron emission tomography Laser Doppler perfusion imaging Micro-Lightguide spectrophotometer
52.1 6 22.6 2.69 6 1.13 39.9 6 9.2
33.4 6 20.3 2.43 6 1.34 35.1 6 10.3
53.6 6 20.3 59.7 6 22.3 21.81 6 8.0
46.4 6 18.7 59.4 6 17.7 20.73 6 11.1
18
Indocyanine green video angiography
Risk of Fat Necrosis in Holm Zone III
perforators might be helpful for reducing the fat necrosis rate in the high inset rate group; however, it was not. There have been several studies reporting the association between venous drainage and the development of fat necrosis.27–29 Gravvanis et al.27 also demonstrated the potential significance of good capacity of venous drainage of perforator complex and resolution of intraoperative congestion using additional SIEV anastomosis. However, the previous studies regarding the efficacy of venous augmentation have mainly focused on its role as a “lifeboat” to salvage the intraoperative congestion, which commonly occurred in superficially dominant flaps,27,30–32 and its potential role on reducing the fat necrosis in the flaps having high inset rate has not yet been clear. The current study suggests that venous augmentation alone does not have a significantly protective influence on fat necrosis formation in flaps with high inset rate. Prospective anatomical and clinical studies will be required to answer this question. In addition, little is known of the potential effect of the inclusion of larger numbers of medial row perforators on the perfusion of contralateral zone III in DIEP flaps. Baumann et al.3 showed that flaps having three to five perforators had significantly lower incidences of fat necrosis than those having one or two perforators, although medial and lateral row perforators were all combined in their study. In the current study, similar results were observed in the group with inset rates below 79%. However, harvesting more medial perforators did not reduce the fat necrosis rate in high inset rate group. It can be assumed that although inclusion of more medial row perforators can secure the vascular reliability within the perforasome, it would not augment the perfusion of vulnerable contralateral tissue, especially including lateral zone III tissue, and would not expand the safe perforasome. Furthermore, larger clinical studies would be ideal for more solid conclusions. A few options can be suggested when a large amount of contralateral tissue is required. Bipedicled flap harvest could be considered for safe transfer of high inset rate flaps. In our center, when the transfer of an excessively large proportion of flap, including total zone III and even part of zone IV tissue, is expected in volumetric analysis by preoperative CTA or when infraumbilical vertical scars are present, we perform a bipedicled flap harvest. Actually, seven cases of bipedicled flaps were harvested during the same study period, although they were not included based on the exclusion criteria. The fat necrosis rate (14.3%) of the bipedicled flap group was similar to that of the medial row perforator group, whereas the mean inset rate was much higher (79.8 vs. 66.0). The simultaneous use of implants with DIEP flaps can be suggested as a good option in optimizing large breast reconstruction.33 We can also reduce the inset rate of
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flaps by performing reduction mammaplasty of the contralateral side if the patients want smaller breasts. This study is limited by the relatively small number of cases and the retrospective study design. Moreover, our study populations had a lower average BMI when compared with the western people and did not include any patients with obesity, which can make it difficult to generalize the results. Large, prospective, and multicenter studies would be required to obtain more solid conclusions. One of the strengths of this study is the homogenous characteristics of the cases. Inclusion of only medial row perforator DIEP flaps and exclusion of cases having infraumbilical vertical scars can be helpful for reducing confounding effects and acquiring more focused conclusions. Furthermore, by using ultrasound examination, more accurate diagnosis and analysis with more reliable data were possible.34 CONCLUSIONS
In the medial row perforator-based DIEP flaps for unilateral breast reconstructions, fat necrosis developed more frequently in the contralateral zone III than in the ipsilateral zone II. The lateral portion of zone III tissue may not be safe from the development of fat necrosis. High inset rate more than 79% was significantly associated with the development of fat necrosis. Not transferring an excessively large proportion of contralateral tissue, especially lateral zone III tissue, can minimize the risk of fat necrosis in medial row perforator DIEP flap breast reconstruction.
REFERENCES 1. Allen RJ, Treece P. Deep inferior epigastric perforator flap for breast reconstruction. Ann Plast Surg 1994;32:32–38. 2. Chang DW. Breast reconstruction with microvascular MS-TRAM and DIEP flaps. Arch Plast Surg 2012;39:3–10. 3. 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. 4. Khansa I, Momoh AO, Patel PP, Nguyen JT, Miller MJ, Lee BT. Fat necrosis in autologous abdomen-based breast reconstruction: A systematic review. Plast Reconstr Surg 2013;131:443–452. 5. Nahabedian MY, Tsangaris T, Momen B. Breast reconstruction with the DIEP flap or the muscle-sparing (MS-2) free TRAM flap: Is there a difference? Plast Reconstr Surg 2005;115:436–444; discussion 445–446. 6. Rogers NE, Allen RJ. Radiation effects on breast reconstruction with the deep inferior epigastric perforator flap. Plast Reconstr Surg 2002;109:1919–1924; discussion 1925–1926. 7. 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 90–92. 8. 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.
Microsurgery DOI 10.1002/micr
278
Lee et al.
9. Lee KT, Lee JE, Nam SJ, Mun GH. Ischaemic time and fat necrosis in breast reconstruction with a free deep inferior epigastric perforator flap. J Plast Reconstr Aesthet Surg 2013;66:174–181. 10. Bailey SH, Saint-Cyr M, Wong C, Mojallal A, Zhang K, Ouyang D, Arbique G, Trussler A, Rohrich RJ. The single dominant medial row perforator DIEP flap in breast reconstruction: Three-dimensional perforasome and clinical results. Plast Reconstr Surg 2010;126:739– 751. 11. Schaverien M, Saint-Cyr M, Arbique G, Brown SA. Arterial and venous anatomies of the deep inferior epigastric perforator and superficial inferior epigastric artery flaps. Plast Reconstr Surg 2008; 121:1909–1919. 12. Garvey PB, Salavati S, Feng L, Butler CE. Perfusion-related complications are similar for DIEP and muscle-sparing free TRAM flaps harvested on medial or lateral deep inferior epigastric artery branch perforators for breast reconstruction. Plast Reconstr Surg 2011;128: 581e–589e. 13. Rahmanian-Schwarz A, Rothenberger J, Hirt B, Luz O, Schaller HE. A combined anatomical and clinical study for quantitative analysis of the microcirculation in the classic perfusion zones of the deep inferior epigastric artery perforator flap. Plast Reconstr Surg 2011; 127:505–513. 14. Losken A, Zenn MR, Hammel JA, Walsh MW, Carlson GW. Assessment of zonal perfusion using intraoperative angiography during abdominal flap breast reconstruction. Plast Reconstr Surg 2012; 129:618e–624e. 15. Holm C, Mayr M, Hofter E, Ninkovic M. Perfusion zones of the DIEP flap revisited: A clinical study. Plast Reconstr Surg 2006;117: 37–43. 16. Schrey A, Kinnunen I, Kalliokoski K, Minn H, Grenman R, Vahlberg T, Niemi T, Suominen E, Aitasalo K. Perfusion in free breast reconstruction flap zones assessed with positron emission tomography. Microsurgery 2010;30:430–436. 17. Ohjimi H, Era K, Fujita T, Tanaka T, Yabuuchi R. Analyzing the vascular architecture of the free TRAM flap using intraoperative ex vivo angiography. Plast Reconstr Surg 2005;116:106–113. 18. Eric M, Ravnik D, Zic R, Dragnic N, Krivokuca D, Leksan I, Hribernik M. Deep inferior epigastric perforator flap: An anatomical study of the perforators and local vascular differences. Microsurgery 2012;32:43–49. 19. Tindholdt TT, Saidian S, Tonseth KA. Microcirculatory evaluation of deep inferior epigastric artery perforator flaps with laser Doppler perfusion imaging in breast reconstruction. J Plast Surg Hand Surg 2011;45:143–147. 20. Hwang JH, Lim SY, Pyon JK, Bang SI, Oh KS, Mun GH. Reliable harvesting of a large thoracodorsal artery perforator flap with emphasis on perforator number and spacing. Plast Reconstr Surg 2011;128:140e–150e.
Microsurgery DOI 10.1002/micr
21. Kim JT. Latissimus dorsi perforator flap. Clin Plast Surg 2003;30: 403–431. 22. Mosahebi A, Disa JJ, Pusic AL, Cordeiro PG, Mehrara BJ. The use of the extended anterolateral thigh flap for reconstruction of massive oncologic defects. Plast Reconstr Surg 2008;122:492–496. 23. Booi DI, Debats IB, Boeckx WD, van der Hulst RR. Risk factors and blood flow in the free transverse rectus abdominis (TRAM) flap: Smoking and high flap weight impair the free TRAM flap microcirculation. Ann Plast Surg 2007;59:364–371. 24. Gill PS, Hunt JP, Guerra AB, Dellacroce FJ, Sullivan SK, Boraski J, Metzinger SE, Dupin CL, Allen RJ. A 10-year retrospective review of 758 DIEP flaps for breast reconstruction. Plast Reconstr Surg 2004;113:1153–1160. 25. Han S, Sup Eom J, Ho Kim D. Effects of the abdominal midline incision on the survival of the transverse rectus abdominis musculocutaneous flap in rat model. Ann Plast Surg 2003;50:171–176. 26. Xu H, Dong J, Wang T. Bipedicle deep inferior epigastric perforator flap for unilateral breast reconstruction: Seven years’ experience. Plast Reconstr Surg 2009;124:1797–1807. 27. Gravvanis A, Tsoutsos D, Papanikolaou G, Diab A, Lambropoulou P, Karakitsos D. Refining perforator selection for deep inferior epigastric perforator flap: The impact of the dominant venous perforator. Microsurgery 2014;34:169–176. 28. Tran NV, Buchel EW, Convery PA. Microvascular complications of DIEP flaps. Plast Reconstr Surg 2007;119:1397–1405; discussion 1406–1408. 29. Blondeel PN, Arnstein M, Verstraete K, Depuydt K, Van Landuyt KH, Monstrey SJ, Kroll SS. Venous congestion and blood flow in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps. Plast Reconstr Surg 2000;106:1295–1299. 30. Boutros SG. Double venous system drainage in deep inferior epigastric perforator flap breast reconstruction: A single-surgeon experience. Plast Reconstr Surg 2013;131:671–676. 31. Xin Q, Luan J, Mu H, Mu L. Augmentation of venous drainage in deep inferior epigastric perforator flap breast reconstruction: Efficacy and advancement. J Reconstr Microsurg 2012;28:313–318. 32. Rothenberger J, Amr A, Schiefer J, Schaller HE, RahmanianSchwarz A. A quantitative analysis of the venous outflow of the deep inferior epigastric flap (DIEP) based on the perforator veins and the efficiency of superficial inferior epigastric vein (SIEV) supercharging. J Plast Reconstr Aesthet Surg 2013;66:67–72. 33. Figus A, Canu V, Iwuagwu FC, Ramakrishnan V. DIEP flap with implant: A further option in optimising breast reconstruction. J Plast Reconstr Aesthet Surg 2009;62:1118–1126. 34. Peeters WJ, Nanhekhan L, Van Ongeval C, Fabre 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.
