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Optimizing Perforator Selection: A Multivariable Analysis of Predictors for Fat Necrosis and Abdominal Morbidity in DIEP Flap Breast Reconstruction

Hembd, Austin, M.D.; Teotia, Sumeet S., M.D.; Zhu, Hong, Ph.D.; Haddock, Nicholas T., M.D.

Plastic and Reconstructive Surgery: September 2018 - Volume 142 - Issue 3 - p 583–592
doi: 10.1097/PRS.0000000000004631
Breast: Original Articles

Background: This study aims to elucidate the important predicting factors for fat necrosis and abdominal morbidity in the patient undergoing deep inferior epigastric artery perforator flap reconstruction.

Methods: The authors conducted a retrospective review of 866 free-flap breast reconstructions performed at one institution from 2010 to 2016. Twenty-eight potential predictors were included in multivariable analyses to control for possible confounding interactions.

Results: Four hundred nine total deep inferior epigastric artery perforator flaps were included in the statistical analysis. Of these, 14.4 percent had flap fat necrosis, 21.3 percent had an abdominal wound or complication, and 6 percent had an abdominal bulge or hernia. Analysis showed an increase in the odds of fat necrosis with increasing flap weight (OR, 1.002 per 1-g increase; p = 0.0002). A decrease in the odds of fat necrosis was seen with lateral row (OR, 0.29; p = 0.001) and both medial and lateral row perforator flaps (OR, 0.21; p = 0.001), if indocyanine green angiography was used (OR, 0.46; p = 0.04), and with increasing total flow rate of the flap (OR, 0.62 per 1-mm/second increase; p = 0.05). Increased odds of abdominal bulge or hernia were seen with lateral row or both medial and lateral row perforators (OR, 3.21; p = 0.05) versus medial row perforator-based flaps, and with patients who had an abdominal wound postoperatively (OR, 2.59; p = 0.05).

Conclusions: The authors’ results suggest that using larger caliber perforators and perforators from the lateral row alone, or in addition to medial row perforators, can decrease fat necrosis more than simply harvesting more perforators alone. However, lateral and both medial and lateral row perforator flaps come at the cost of increasing abdominal bulge rates.

CLINICAL QUESTION/LEVEL OF EVIDENCE: Risk, III.

Dallas, Texas

From the Department of Plastic Surgery and the Department of Clinical Science, Division of Biostatistics, Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center.

Received for publication January 17, 2018; accepted March 8, 2018.

Disclosure: The authors have no commercial or financial associations related to the submitted article, and no commercial or financial conflicts of interest. No funding was received for the performance of this research of production of the article.

Nicholas T. Haddock, M.D., University of Texas Southwestern Medical Center, 1801 Inwood Road, Dallas, Texas 75390, nicholas.haddock@utsouthwestern.edu

Perforator selection in deep inferior epigastric artery perforator (DIEP) flap breast reconstruction is paramount to providing adequate perfusion to the free tissue and reducing the incidence of postoperative fat necrosis. There has been a growing body of literature aiming to clarify what variables affect fat necrosis: perforator number, flap weight, body mass index, smoking, perforator row, and perforator caliber, among others, have all been proposed in various studies, albeit with conflicting conclusions.1–10

In addition, studies have debated whether perforator selection, among other patient and operative factors, can potentially have an effect on abdominal donor-site morbidity and bulge rates.11–21 The problem is that there has been a paucity of large-sample, up-to-date analyses that include all of these purported predicting variables in a single multivariable model, thus controlling for their possible confounding interaction. This study aims to elucidate the salient predicting factors not only to allow more accurate patient counseling and risk stratification based on patient characteristics, but moreover to give the reconstructive surgeon a clearer understanding of what operative decisions regarding perforator selection actually impact fat necrosis and abdominal morbidity.

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PATIENTS AND METHODS

Retrospective Review

A retrospective review was performed on 866 free flaps for breast reconstruction at the University of Texas Southwestern Medical Center from 2010 to 2016. One or both of the two senior authors (N.T.H. and S.S.T.) performed every operation as attending surgeon, and their surgical and perioperative strategies are standardized between each other.

Strict inclusion criteria were applied before statistical analysis: all patients had preoperative computed tomographic angiography, all flaps were single DIEP hemiflaps for either bilateral or unilateral breast reconstruction, and all flaps included only a single pedicled artery and vein anastomosed to one cranial internal mammary artery and vein. The patient had a minimum of two postoperative follow-up physical examinations by the senior surgeons, with a minimum follow-up time of 3 months. Exclusion criteria included all superficial inferior epigastric artery and muscle-sparing transverse rectus abdominis musculocutaneous (TRAM) flaps, any DIEP flap used on the same side as another free flap, DIEP flaps that were “turbocharged” or “supercharged” with any technique, or “extended” flaps across the midline.

The patient demographic information and operative factors that were compiled for univariable analysis are listed in Table 1. Examples of DIEP flaps with variable numbers of perforators are shown in Figure 1. Biological mesh was used for flaps where the rectus fascia was of poor quality or the resultant fascia defect from the perforator dissection was significant.

Table 1

Table 1

Fig. 1

Fig. 1

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Total Flow Rate

Both surgeons use visual estimates of the external diameter of perforating vessels as they enter the flap with a specific, five-category measurement system: less than 1 mm and not seen on computed tomographic angiography, 1 mm, 1.5 mm, 2.0 mm, and 2.5 mm and above. Concordance between the two senior authors was confirmed for all co-surgery reconstructions. These calibers were then used to calculate flow from the Poiseuille law in millimeters per second. For all calculations, the pressure differential was between a theoretical 120 and 80 mmHg to simulate systolic and diastolic blood pressures, viscosity was 40 mP for blood, and the length was 1 mm.

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Postoperative Follow-Up and Assessment of Fat Necrosis and Abdominal Morbidity

Standard postoperative protocol for the senior surgeons is a 2-week, a 6-week, and then an additional 12-week follow-up followed by annual visits. Fat necrosis and abdominal morbidity data were recorded from postoperative clinic notes and imaging with the senior authors, the oncologic breast surgeons, or both.

Fat necrosis was defined as a greater than 1-cm palpable, distinct mass on physical examination or imaging that was present beyond 6 weeks postoperatively. Careful review ensured that the first evidence of fat necrosis was noted before secondary fat grafting or revision surgery.

Abdominal wounds and donor-site complications were defined as any wound with delayed healing that required local wound care or negative-pressure wound therapy, abdominal cellulitis, incisional fat necrosis or asymmetry, and any hematoma or seroma. Abdominal bulges were defined by physical examination and computed tomographic imaging. All documentation or imaging for abdominal bulges or wounds was carefully reviewed for laterality in patients undergoing bilateral breast reconstruction.

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Nerve-Sparing and Nerve-Repair Techniques

If all identifiable nerves were successfully spared during perforator harvest, it was deemed a nerve-sparing procedure. If identifiable nerves had to be sacrificed to adequately mobilize the pedicle, but then all were primarily repaired, this was deemed a nerve-repairing procedure. Figure 2 depicts a nerve-sparing dissection.

Fig. 2

Fig. 2

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Statistical Analysis

A univariable logistical regression analysis was first conducted with all 28 of the above-listed patient demographic and surgical factors to calculate an odds ratio with 95 percent confidence intervals on three primary outcomes: (1) DIEP flap fat necrosis, (2) abdominal wounds or complications, and (3) abdominal bulge or hernia. All variables with a value of p < 0.15 for the calculated odds ratio in univariable analysis were then entered in a backward selection algorithm to yield the parsimonious multivariable logistic regression model. An odds ratio with a value of p ≤ 0.05 in the multivariable analysis was considered statistically significant.

Summary statistics for patient characteristics were reported using medians and ranges for continuous variables, and using counts and percentages for categorical variables. Patient characteristics were compared to analyze potentially confounding presurgical patient demographics among the significant predicting variables. For continuous patient characteristics, analysis of variance or Kruskal-Wallis nonparametric analysis of variance was used as appropriate for comparisons of three or more groups, and two-sample t test or the nonparametric Wilcoxon rank sum test was used for two-group comparisons. For categorical patient characteristics, the chi-square test or Fisher’s exact test was used as appropriate. All analyses were conducted using SAS version 9.4 (SAS Institute, Inc., Cary, N.C.).

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RESULTS

Cohort Characteristics

Four hundred nine total DIEP flaps were included in our statistical analysis after strict inclusion and exclusion criteria were applied. The average age and body mass index of the patients was 50.5 and 30.7 kg/m2, respectively; 68.5 percent were Causation, 16.9 percent were black, 9 percent were Hispanic, and 5.6 percent were Asian. The average follow-up for these patients was 18.5 months, with a median of 15.75 months; 91.9 percent of flaps were bilateral and 8.1 percent were unilateral reconstructions for 32 percent immediate, 50.9 percent delayed-immediate, and 17.1 percent delayed breast reconstructions. Of these, 14.4 percent had flap fat necrosis, 21.3 percent had an abdominal wound or complication, and 6 percent had an abdominal bulge or hernia.

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Multivariable Analysis

Fat Necrosis

Analysis showed a significant increase in the odds of fat necrosis with increasing flap weight (OR, 1.002 per 1-g increase; or OR, 1.2 per 100-g increase; p = 0.0002), and earlier year of surgery (OR, 2.51 for 2010 to 2013 versus 2014 to 2016; p = 0.01).

A significant decrease in the odds of fat necrosis was seen with lateral row (OR, 0.29; p = 0.001) and both medial and lateral row perforator flaps (OR, 0.21; p = 0.001) versus medial row–based flaps, in patients who underwent neoadjuvant chemotherapy (OR, 0.36; p = 0.01), and if indocyanine green was used to assess perfusion (OR, 0.46; p = 0.04). Overall, indocyanine green was used intraoperatively in 130 flaps (31.8 percent) and directly guided excision of areas with poor perfusion in 38.5 percent of those cases.

The average total flow rate for all flaps was 0.78 mm/second (median, 0.52 mm/second). Increasing total flow rate of the flap also decreased the odds of fat necrosis (OR, 0.62 per 1-mm/second increase; p = 0.05).

The number of perforators did not significantly affect fat necrosis rates after being controlled for by these other significant variables in the multivariable analysis. In addition, excising corners/zones of the flap prophylactically without indocyanine green angiography did not significantly affect fat necrosis rates. The results of the multivariable analysis for fat necrosis are summarized in Table 2.

Table 2

Table 2

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Abdominal Wounds and Complications

There were significant increased odds of having an abdominal wound or donor-site complications with smoking (OR, 1.86; p = 0.02), hypertension (OR, 1.72; p = 0.04), and increasing flap weight (OR, 1.001 per 1-g increase; p = 0.001). Body mass index was not a significant factor for abdominal wounds when controlled by flap weight in the multivariable analysis. Overall, only 25.3 percent of abdominal wounds or complications required operative treatment, including dog-ear or scar revisions. The results of the multivariable analysis for abdominal wounds and complications are summarized in Table 3.

Table 3

Table 3

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Abdominal Bulge or Hernia

Increased odds of abdominal bulge or hernia were seen with a return to the operating room on the initial hospital stay (OR, 5.05; p = 0.01), with flaps based on the lateral or both medial and lateral row perforators (OR, 3.21; p = 0.05) versus medial row perforators, and with patients who had an abdominal or umbilical wound postoperatively (OR, 2.59; p = 0.05). In total, there were 127 nerve-sparing (31 percent) and 22 nerve-repairing (5.4 percent) flap dissections. However, using mesh for rectus fascia repair in 7.8 percent of flaps and using nerve-sparing or nerve-repairing techniques did not significantly affect the odds of abdominal bulges. There were no complications from mesh use. The results of the multivariable analysis for abdominal bulges or hernias are summarized in Table 4.

Table 4

Table 4

Table 5 summarizes the comparisons of patient demographics between perforator row types. Similar tables were made for each significant variable after multivariable analysis (data not shown). The only differences between presurgical demographics that had a significant effect on one of the primary outcomes measures was fewer smokers (21 percent; p = 0.0008) in the lateral row cohort versus medial (36.2 percent) and both medial and lateral row (45.4 percent) cohorts, less hypertension (32.1 percent versus 42.2 percent; p = 0.041) and more neoadjuvant chemotherapy (35.9 percent versus 21.7 percent; p = 0.003) in the 2014 to 2016 versus 2010 to 2013 cohorts, and less smoking in the group that received neoadjuvant chemotherapy (27.8 percent versus 37.8 percent; p = 0.049).

Table 5

Table 5

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DISCUSSION

Previous publications have described variables that affect free flap fat necrosis after abdominally based autologous breast reconstruction. Baumann et al. showed in their series of 228 abdominal free flaps that fat necrosis was higher in flaps with only one or two perforators, in patients who smoked, and the inclusion of zone 3 in flaps.1 Although this study used a multivariable analysis and estimates of perforator caliber, it included muscle-sparing TRAM and superficial inferior epigastric artery flaps which, as pointed out by Rozen et al.,2 have anatomical and physiologic differences. Grover et al. added to the specificity of this concept by showing in a review of 395 DIEP flaps that with a single-perforator flap there was a higher rate of fat necrosis than with a multiperforator flap.3 However, this was not a multivariable analysis and perforator location was not a measured variable. A similar result was seen with 100 flaps in addition to a correlation between higher body mass index and increased fat necrosis by using a multivariable model.4

In contrast, Mulvey et al. looked at 179 muscle-sparing TRAM and DIEP flaps and found higher odds of fat necrosis with increasing flap weight, but not with perforator number or perforator row.5 Their multivariable analysis suggested that including multiple perforators may be protective for fat necrosis, but this was not statistically significant because of the small sample size.

Lindsey, in a critique of conclusions to simply include more perforators to decrease fat necrosis, cited the importance of also considering perforator caliber and perforator location.6 , 7 Kamali et al. confirmed the importance of perforator location, with a 24.5 percent versus 8.2 percent fat necrosis occurrence from DIEP flaps based on the medial row versus the lateral row.8 This study showed a general decrease in fat necrosis within the same row with increasing perforator number, but no statistical test was conducted to assess the significance of different numbers of perforators on fat necrosis rates.

On univariable analysis of our flap data, multiple-perforator flaps had decreased odds of fat necrosis compared with single-perforator flaps (OR, 0.54; p = 0.03). This significance was lost in the multivariable model (p = 0.55). This model instead showed that flaps based on lateral and both medial and lateral row perforators (OR, 0.29 and 0.21, respectively) decreased the odds of fat necrosis independently (Table 2). In addition, increasing total flow to the flap (OR, 0.63 per 1-mm/second increase) (Table 2) was associated with a lower rate of fat necrosis. Overall, our fat necrosis rate of 14.4 percent was consistent with the rate from other recent studies.1 , 8 According to the Poiseuille law, increasing the caliber of a perforator has an exponentially larger effect on flow rates than adding additional small perforators. The results follow this concept and subsequently suggest that perforator location and perforator caliber may be more important intraoperative factors to decrease fat necrosis than simply recruiting more perforators alone.

Because of the presumptions made to calculate the total flow rate, the absolute values are less meaningful than the overall trend. In addition, we acknowledge the potential inaccuracies of estimating flow based on external diameters of blood vessels,2 but calculating perforator size solely based on preoperative computed tomographic angiography has its own limitations. For the senior authors, after being guided by computed tomographic angiography, intraoperative visual estimates of external diameter coupled with the pulse and Doppler signal best simulates what is used in the operative room to assess the quality of a perforator.

Using laser-assisted indocyanine green fluorescence angiography for assessing perfusion to abdominal free flaps has been described, with several studies correlating areas of hypoperfusion on indocyanine green angiography with postoperative flap or fat necrosis.22–27 Indocyanine green angiography was used as an adjunct to our computed tomographic angiography–guided perforator selection algorithm in 31.8 percent of flaps. Primarily, it was used after the flap had been anastomosed on the chest to subjectively assess for areas of hypoperfusion if there was clinical concern. Less commonly, it was used to subjectively assess perforator quality on the abdomen if there was a discrepancy with clinical findings versus preoperative computed tomographic angiography. This use of indocyanine green angiography decreased the odds of fat necrosis (OR, 0.46) (Table 2).

There have been studies purporting the safety of performing breast reconstruction after neoadjuvant chemotherapy with similar complication rates to patients without neoadjuvant chemotherapy,15 , 27–32 albeit with some conflicting data.33 When comparing the demographic data between flaps performed in 2010 to 2013 versus 2014 to 2016, there was less neoadjuvant chemotherapy in the earlier cohort (21.7 percent versus 35.9 percent). Interestingly, neoadjuvant chemotherapy was associated with reduced odds of fat necrosis (OR, 0.36) in the multivariable analysis even after being controlled for by year of surgery (Table 2). However, in the flap cohort that underwent neoadjuvant chemotherapy, we found there was less smoking (27 percent versus 37 percent), less immediate breast reconstructions (18.2 percent versus 38.2 percent), less adjuvant chemotherapy (16.7 percent versus 27.9 percent), and a younger age (46.9 years versus 52.1 years). These variables have previously been shown to affect fat necrosis and could have had a cumulative unmeasured effect in our study.1 , 9 , 31 Thus, we believe that the decreased odds of fat necrosis in the later period were attributable to improved surgeon experience rather than more patients with neoadjuvant chemotherapy having undergone reconstruction.

In addition, the size of the flap is important to consider, as flap weight increases not only the odds of fat necrosis (OR, 1.2 per 100-g increase) (Table 2) but also abdominal wound or complication rates (OR, 1.1 per 100-g increase) (Table 3). The relationship between flap weight and fat necrosis is depicted in Figure 3, with an increase in the probability of fat necrosis from 11.25 percent to 25 percent from a 500-g flap to a 1500-g flap, respectively. The other factors associated with increased odds of abdominal wounds and complications were active smoking (OR, 1.869) (Table 3) and hypertension (OR, 1.72) (Table 3), which is consistent with other studies.5 , 15 , 16 , 20

Fig. 3

Fig. 3

The presence of an abdominal wound itself was independently associated with increased risk of abdominal bulge or hernia (OR, 2.59) (Table 4). This scenario is particularly true with umbilical necrosis, which can cause a loss of domain, and one should critically evaluate umbilical stalk height to try and prevent the sequelae of these donor-site wounds.20 , 34 Returning to the operating room on the initial hospital stay significantly increased the odds of abdominal bulge (OR, 5.05) (Table 4). Because 95.7 percent of these take-backs were for recipient-site hematomas or flap congestion, we believe this association with abdominal bulge is attributable to the urgent nature of these cases and flexed positioning not being well maintained.

Rozen et al. suggested that the important motor nerves supplying the rectus enter with the lateral row perforators, thus placing them at risk when harvesting a laterally based flap.11–13 , 19 This is particularly salient in the setting of our results that, along with previous data,8 suggest that the addition of a lateral row perforator decreases fat necrosis. However, Garvey et al. published data on 615 abdominal free flaps and found no difference in donor-site bulge or hernia (overall rate, 4.6 percent) between medial and lateral harvest.14 Our overall abdominal and hernia rate of 6.1 percent is comparable. However, their criteria excluded all flaps based on both rows. With the idea that in either a lateral or both medial and lateral row perforator harvest there is potential insult to the lateral motor nerves,11 we compared lateral and both medial and lateral row–based flaps together versus medial row flaps and found an increased risk of bulge rates (OR, 3.21) with the former (Table 4). Conversely, neither nerve-sparing, nerve-repairing, nor mesh repair was found to significantly reduce abdominal bulge rates (Table 4). However, given the low incidence of this complication and the low number of nerve-sparing, nerve-repairing, and mesh fascia repairs, the analysis lacks adequate power to extrapolate this negative finding and confidently conclude that neither mesh nor nerve preservation has a role in abdominal bulging. Therefore, additional, larger studies will be needed in the future to clarify their efficacy.

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CONCLUSIONS

This study aims to elucidate the predicting factors for fat necrosis and abdominal morbidity in the patient undergoing DIEP flap reconstruction to aid in preoperative risk stratification and to help prioritize specific perforator selection parameters to optimize outcomes. Our results suggest that using larger caliber perforators and perforators from the lateral row alone, or in addition to medial row perforators, can decrease fat necrosis rather than by simply harvesting more perforators alone. However, lateral and both medial and lateral row perforator flaps come at the cost of increasing abdominal bulge rates. In addition, we found that the use of intraoperative indocyanine green angiography decreased the odds of fat necrosis, whereas increasing flap weight increased these odds. Larger flaps, smoking, and hypertension led to a higher rate of abdominal wounds. Returning to the operating room during the initial hospital stay and abdominal wounds themselves were associated with higher abdominal bulge rates.

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ACKNOWLEDGMENTS

The authors thank Hong Zhu, Ph.D., and Jingsheng Yan, Ph.D., of the Division of Biostatistics, Department of Clinical Sciences, Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, for expedient and accurate work.

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