The Role of CT Angiography in Assessing Deep Inferior Epigastric Perforator Flap Patency in Patients With Pre-existing Abdominal Scars

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The Role of CT Angiography in Assessing DIEP Flap Patency in Patients With Preexisting Abdominal Scars Ledibabari M. Ngaage, MA (Cantab), MB BChir,a Raed Hamed, MB BCh,b,c Georgette Oni, MBChB, MRCS, MD, PhD, FRCS (Plast), FEBS,b Bruno Di Pace, MD,b,d Dina T. Ghorra, MB BCh,b,c Brendan C. Koo BMedSci, MB BCh, BAO, FRCR,e and Charles M. Malata, BSc (HB), MB ChB, MRCS, LRCP, FRCS (Glasg), FRCS (Plast)b,f,g,* a

The Clinical School of Medicine, University of Cambridge, Cambridge, UK Plastic & Reconstructive Surgery Department, Addenbrooke’s Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK c Plastic and Reconstructive Surgery Unit, Alexandria Medical School, Alexandria Main University Hospital, Alexandria, Egypt d Plastic Surgery Unit, Multidisciplinary Department of Medical-Surgical and Dental Specialities, Universita` degli Studi della Campania Luigi Vanvitelli, Naples, Italy e Department of Radiology, Addenbrooke’s Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK f Cambridge Breast Unit, Addenbrooke’s Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK g Anglia Ruskin University School of Medicine, Chelmsford & Cambridge, UK b

article info

abstract

Article history:

Background: Abdominal scars can affect the patency of deep inferior epigastric artery (DIEA)

Received 9 January 2018

perforators and are a concern when planning free flap breast reconstruction (FFBR).

Received in revised form

Computed tomography angiography (CTA) is routinely used for preoperative DIEA flap

11 September 2018

imaging. We investigated CTA utility in predicting the most clinically useful DIEA perfo-

Accepted 20 September 2018

rators in scarred abdomens.

Available online xxx

Methods: A single surgeon’s CTA FFBR patients were studied. All were imaged by one radiologist. CTA reports, abdominal scars, and flap intraoperative details were analyzed.

Keywords:

The operative findings were then correlated with the CTA “predictions.”

CT angiography or computed

Results: A hundred and six patients with preoperative CTAs underwent 132 FFBRs, 44% (58)

tomography angiography (CTA) Free flap breast reconstruction Abdominal scars or scarred abdomen

from scarred and 56% (74) from virgin abdomens. All flap transfers were successful. Concordance between perforators identified by CTA preoperatively and those selected by the surgeon intraoperatively was 95% (scarred 93%; non-scarred 96%, P ¼ 0.470). There was a significant difference in the proportion of single-perforator flaps between the two groups

Presented at: Society of University Surgeons 13th Annual Academic Surgical Congress, Jacksonville, FL. 29th Jane1st Feb 2018 53rd Congress of the European Society for Surgical Research, Madrid, 28th May - 2nd June 2018. * Corresponding author. Plastic and Reconstructive Surgery Department, Addenbrooke’s Hospital, Box 186 Cambridge University Hospitals NHS Foundation Trust, Hills Road, Cambridge, CB2 2QQ, UK. Tel.: þ44-1223-586672; fax: þ44-1223-257177. E-mail addresses: [email protected], [email protected] (C.M. Malata). 0022-4804/$ e see front matter Crown Copyright ª 2018 Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2018.09.059

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Operative time or surgery duration DIEP flaps

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(scarred 46%; non-scarred 28%, P ¼ 0.041). “Scarred” flaps were heavier (789 vs 676 g, P ¼ 0.0244) than those harvested from virgin abdomens. Conclusions: CTA accurately predicted perforator choice in flaps from scarred and virgin abdomens. “Scarred” flaps are more likely to be heavier and based on one perforator suggesting that scarring may have an effect on intraflap vascular anatomy. Further investigations are needed to delineate the mechanism by which this occurs. Crown Copyright ª 2018 Published by Elsevier Inc. All rights reserved.

Introduction The deep inferior epigastric perforator (DIEP) flap is considered the current gold standard in autologous breast reconstruction1,2 because of the availability of a large amount of well-vascularized tissue and the reliable vascular anatomy. However, operations through the anterior abdominal wall risk injuring the DIE vessels and thus can threaten or compromise the vascularity of subsequent abdominal free flaps. Preexisting abdominal scarring can complicate flap harvest by causing direct damage to perforator vessels or an alteration in their course.3 Although scarring has not been shown to have an adverse effect on flap survival,4-6 it has been associated with increased donor site morbidity.5 Scarring may also render some parts of the flap less well vascularized than non-scarred, or “virgin”, abdomens.3 There are very few studies on the anatomical changes in perforators following scarring, so little is known on the consequences for vessel integrity. Strategies have been reported to optimize flap success in this patient group with3,6 or without computed tomography angiography (CTA).7 Since its advent, CTA has made abdominal free flap breast reconstruction (FFBR) more predictable and consistently shortened the operative times8-10 by accurately identifying the course and branches of the DIE vessels.11-13 CTA is recommended when vascular anatomy is questionable.14 Conversely, incidental findings on CT angiography can preclude or influence decision-making in FFBR.15 Few studies address the effects of scars on DIE artery perforator patency. Therefore, the aim of the present study was to assess the utility of preoperative CTA in scarred abdomens and to explore the anatomical differences between non-scarred flaps and their scarred counterparts.

Materials and methods A retrospective study was performed on 109 patients who had undergone CTA of the anterior abdominal wall before immediate or delayed FFBR (132 flaps in total) at a tertiary referral university hospital over a 6-year period (November 2011 to August 2017). A single surgeon’s (C.M.M.) cohort of CTA FFBR patients was studied to eliminate interoperator variability. All scans were reported by one radiologist (B.C.K.). Patients were identified from a prospectively collected departmental free flap database. Unilateral, bilateral, and bipedicled DIEP flaps were included. Details on patient demographics, perforators used, abdominal scars, and intraoperative details were collected. The operative findings were then correlated with the “predictions” of the CTA scan reports. The data were tabulated in Microsoft Excel (Microsoft 2016, Redmond, Washington), and analysis was completed with the

IBM SPSS Software, version 24.0 (IBM Corp, 2017, IBM SPSS Statistics for Windows; IBM Corp, Armonk, NY). Data were initially analyzed with the Kolmogorov-Smirnov test and found not to follow a normal distribution. Therefore, differences in continuous data between the groups were evaluated with the nonparametric Mann-Whitney U test. The chi-squared test was used to calculate significance in differences between categorical data. Statistical significance was determined by a value of P  0.05.

Ethics This study was part of a quality improvement assessment and an ongoing departmental free flap audit within our hospital. Audits and quality improvement assessment are part of a larger framework for clinical governance, whereby National Health Service (NHS) organizations are accountable for continuously improving the quality of their services and safeguarding high standards. Clinical governance (inclusive of audits and quality improvement assessments) is compulsory within the NHS. No specific ethical committee approval is therefore needed. Under the Caldicott principles, non-identifiable patient data can be collected, stored, and used for purpose of audit without individual patient consent. In addition, all data were collected retrospectively from hospital medical records. Therefore, individual patient consent was not required for this study. Subjects in clinical photographs gave informed consent for use of images.

Results Patient and flap demographics In total, 109 patients underwent preoperative planning CTA during the study period. Of these, three patients did not undergo reconstructive surgery because of significant CTA incidental findings that rendered surgery unsafe, leaving a total of 106 patients for analysis. A total 132 flaps were performed during the 6-year period, 62 patients received unilateral flaps, whereas bilateral and bipedicled groups had 26 and 18 patients, respectively (Table 1). Of the 106 patients, 62 had virgin abdomens, and 44 were scarred. Of the 132 flaps, 56% (74) were from non-scarred, whereas 44% (58) originated from scarred abdomens (Fig. 1). Patients were comparable in terms of age and BMI (P > 0.05). Characteristics of the scarred and non-scarred groups are summarized in Table 1. All flaps survived, and both cohorts had similar re-exploration rates (5% in scarred abdomens versus 4% in non-scarred; P ¼ 0.76, chi-squared test). The abdominal scars encountered were Pfannenstiel (subdivided into Caesarean sections and other), midline laparotomy, appendicectomy, and laparoscopic (Table 2, Fig. 2).

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Table 1 e Patient demographics and flap characteristics in scarred and non-scarred abdomens. Patients

Non-scarred

Scarred

Total

62

44

106

Median age (range) years

49.2 [r: 34-77]

49.0 [r: 32-67]

49.0 [r: 32-77]

Median BMI

25.6 [r: 19-35]

27.6 [r: 23-35]

26.2 [r: 19-35]

Unilateral flaps

34

28

62

Bilateral flaps

12

14

26

Bipedicled flaps

16

2

18

Immediate flaps

58

38

96

Delayed flaps

16

20

36

Total number of flaps

74

58

132

3 (4%)

3 (5%)

6 (5%)

Re-exploration (%)

CTA concordance Intraoperative findings were highly concordant with CTA predictions (Fig. 3) with an overall concordance rate of 95% (125/132), which did not differ significantly between scarred (93%, 54/58) and non-scarred (96%, 71/74) abdomens (P ¼ 0.4695, chi-squared test). The utility of CTA imaging in extensive abdominal scarring is highlighted by the representative CTA images of a patient with a severely scarred abdomen from childhood abdominal surgery Figure 4A-C. CTA-enabled successful delayed DIEP flap reconstruction is shown in Fig. 4D-E.

Flap characteristics Moon and Taylor classification Deep inferior epigastric vessel anatomy was initially analyzed using Moon and Taylor classification of the DIE artery

branching pattern (Fig. 5); type I was the most common in all flaps (Table 3). The branching pattern used did not differ significantly between the scarred and non-scarred groups (P ¼ 0.8716).

Number of perforators One flap did not have data on the number of perforators used, so 131 flaps were included in this analysis. The median number of perforators used in all flaps was 2, but this differed significantly between non-scarred and scarred abdomens (P ¼ 0.0484, Mann-Whitney U test, Fig. 6). This distribution was further reinforced by the findings that a comparison of single perforatorebased versus multiple perforatorebased flaps showed a significant difference between the scarred and non-scarred abdomens (P ¼ 0.0414, chi-squared test, Fig. 7). Two perforators were most commonly used in virgin abdomens, whereas one perforator was most commonly used in scarred abdomens (Fig. 6).

Fig. 1 e Preoperative and postoperative appearances of a 57-year-old. (A) Deformed abdomen from an infected appendicectomy incision from childhood. (B) CTA-enabled delayed left breast reconstruction in the same patient with a DIEP flap harvested from the right abdomen. (Color version of figure is available online.)

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Table 2 e Abdominal scar types and their frequency. Scar type

Patients (n ¼ 44)

Caesarean section

24

Laparoscopy

12

Appendicectomy

11

Pfannenstieleother

9

Midline laparotomy

4

Flap weights The median flap weight in all flaps was 722 g (range: 1921226 g). Scarred flaps were significantly heavier than nonscarred flaps by 100 g (789 vs 676 g, P ¼ 0.0244, Mann-Whitney U test).

Perforator analysis versus BMI and scar types BMI was correlated with the number of perforators used. Patients with single-perforator flaps tended to have a higher median BMI than flaps based on multiple perforators (31 vs 26 kg/m2, P ¼ 0.067, Mann-Whitney U test). We next correlated the scar type with the number of perforators used. Those with multiple scars were excluded from this analysis to reduce heterogeneity in the data. The trend, though not significant, was that abdomens with Pfannenstiel (Caesarean section scars included) and laparoscopic scars yielded the lowest median number of perforators (1), followed by appendicectomy (2), whereas midline laparotomy scars had the highest median number of perforators (3) (P ¼ 0.2826, One-way ANOVA test).

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respectively (P ¼ 0.8058, chi-squared test). The donor site complications documented were hematoma, poor wound healing requiring surgical closure, wound infection (that required antibiotics or debridement), and skin necrosis (both conservatively and non-conservatively treated were included). Fat necrosis in the flaps was identified by histology reports of any biopsies done for symptomatic lumps in the reconstructed breasts and/or their subsequent radiological imaging (ultrasound scans, MRIs, and mammograms). There was no difference in the flap fat necrosis rates between those harvested from scarred abdomens versus those from virgin abdomens (11.3 % versus 3.3%, P ¼ 0.096, chi-squared test).

Operative duration and ischemia time Bipedicled flaps were excluded from this analysis because of the complexity of determining the true ischemia time for flaps based on multiple vascular pedicles, a situation that is further compounded by different times of revascularizations of the two “hemiflaps.” Unilateral operations were 3 hours faster than bilateral operations (413 vs 637 min, P < 0.00001, MannWhitney U test), and this held true for scarred (420 vs 640 min, P < 0.00001, Mann-Whitney U test) and non-scarred abdomens (410 vs 637 min, P < 0.00001, Mann-Whitney U test). Operative time for unilateral and bilateral flaps did not differ between the groups (P ¼ 0.4593, and P ¼ 0.0672, respectively, Mann Whitney U test) (Table 4). The median ischemic time was 86 min (range: 47-159 min) for all flaps. However, ischemia times did not differ significantly between the two groups (P ¼ 0.7351, Mann-Whitney U test) being 88 min (range: 54-127) for virgin abdomens and 85 min (range: 47-159) for scarred flaps.

Flap outcomes All flap transfers were successful. The flap re-exploration rate in non-scarred was 4% and that in scarred abdomens was 5% with no significance difference between them (P ¼ 0.7594, chisquared test). Overall donor site complication rates were 12.3% and 10.8% for scarred and non-scarred abdomens,

Discussion As techniques in autologous reconstruction evolve, the boundaries on what is achievable broaden. The literature clearly supports the role of preoperative CTA as a useful

Fig. 2 e Abdominal scar types and their frequency within the scarred group. (Color version of figure is available online.)

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Fig. 3 e Perforator concordance between CTA predictions and surgeon selection (concordance between perforators chosen predicted by CTA and surgeon selection). (Color version of figure is available online.)

adjunct in surgical planning before embarking on free flap breast reconstruction. The benefits include identification of the most suitable perforators, elaboration of perforator anatomy including delineation of the vessel pathway namely tortuosity and intramuscular course. In addition, CTA provides information on the communication between the superficial and deep systems.18 The aim of this perforator anatomy “road map” is to shorten the intraoperative time,8,9 by optimizing the preoperative planning.11,19 This study demonstrates that CTA can accurately predict perforator choice in flaps from scarred and virgin abdomens alike. The overall 95% concordance rate achieved is similar to that reported in the literature, which describes high sensitivity and specificity of CTA in the evaluation of perforator vessels.10,12,20,21 In terms of the branching pattern of the DIE vessels, Moon and Taylor type I was the most common branching pattern used in our cohort in contrast to the findings of others which report type II as the most commonly used in surgery, perhaps

due to their shorter intramuscular course.22,23 This did not differ between scarred and non-scarred abdomens suggesting that scarring does not alter anatomy greatly enough to affect the pattern of branching, which can be outside the rectus muscle. Interestingly, free flaps from scarred abdomens were more likely to be based on one perforator vessel than those from virgin abdomens. There could be several reasons for this. First, the degree of abdominal wall undermining that may have occurred at the time of the previous surgery which caused the scarring is unknown; this may reduce the absolute number of (available) perforators. Second, prior surgery may have caused a reaction similar to the “surgical delay” phenomenon, with surgical division of perforators leading to dilation of the remaining vessels. This would mean that absolute perforator size may be larger in scarred abdomens, such that one vessel is sufficient to perfuse a larger flap. Third, the previous scarring may have caused aberrant vascularization of the

Fig. 4 e (A) The coronal CTA image shows an absence of left-sided vessels with a Moon and Taylor type I right DIE vessel. These vessels were subsequently used during reconstruction showing that CTA prediction was concordant with surgical choice. (B) Corresponding preoperative AP photograph of the 44-year-old patient showing the severely deformed left lower abdomen from surgery as a child. (C) Her transverse CTA image showing absent periumbilical perforators, significant atrophy of the left rectus muscle, and in contrast, extensive adipofascial arborization of a large right paraumbilical perforator. (D and E) Preoperative and postoperative appearances after a hemi-DIEP flap delayed left breast reconstruction and a simultaneous contralateral balancing breast reduction. (Color version of figure is available online.)

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Fig. 5 e Moon and Taylor (1988) classification of DIEA branching.16 Reproduced with permission from Phillips et al. 2008.17 Type Iesingle trunk, type IIebifurcation into two trunks, and type IIIedivision into more than two trunks. The level of the umbilicus (x) is indicated on each illustration. EIA [ external iliac artery. (Color version of figure is available online.)

abdominal tissue secondary to distortion of anatomy,3 which may lead to the scenario found in this study whereby the scarred flaps are larger but based on fewer vessels due to possible changes in “angiosome” territories. Of note, although flaps from scarred abdomens were more likely to be based on one perforator, their weights were also significantly higher. This may support the proposed “surgical delay” theory as choke vessels within the abdominal tissue open, allowing larger flaps to be supported on a single perforating vessel.24 Future in vivo investigations might delineate the mechanism(s) by which this occurs. In our study, we found that single-perforator flaps tended to be associated with a higher BMI than patients with multiple perforator flaps, although this did not reach significance. Interestingly, the low number perforator flaps were predominant in abdomens with laparoscopic and Pfannenstiel scars. Pfannenstiel incision has the potential to divide the superior inferior epigastric vessels; indeed, Kim et al.25 found that patients with Pfannenstiel scars had more vascular communication between the superior inferior epigastric and DIEP vessels than those without scarring. This may support the

“surgical delay” theory. This does not, however, easily explain the findings in laparoscopic scars that are much smaller and whose locations are more variable. Previous abdominal surgery was not associated with an increased incidence of donor site complications or a higher rate of flap re-exploration in our study. The scarred flaps, although heavier and based on only one perforator, were not associated with a higher rate of complications such as fat necrosis or other recipient site problems. These results combined with earlier studies demonstrate that previous abdominal surgery or scarring is not a contraindication to FFBR.4-6

Table 3 e Number of vessels with Moon and Taylor types in scarred vs non-scarred abdomens. DIEA branching pattern

Non-scarred

Scarred

Total

Moon and Taylor I

48

35

86

Moon and Taylor II

36

28

63

Moon and Taylor III

3

1

4

DIEA ¼ deep inferior epigastric artery.

Fig. 6 e Distribution of the number of perforators used in the two study groups. (Color version of figure is available online.)

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supplied by the perforating vessels and see how these correlate to location of the prior scarring on the abdomen. Looking further afield still, this work could then be extrapolated to other procedures that may have been carried out previously on the abdomen prior such as liposuction or abdominoplasty.

Conclusion

Fig. 7 e Perforator numbers in scarred and non-scarred abdomens. * denotes P [ 0.0414.

CTA improves the efficiency and cost of FFBR principally via the reduced operative time. Some studies report costs utility savings as high as $3179 with use of CTA, a gain in quality-adjusted life-years of 0.25.26 Therefore, any reduction in total operating times afforded by CTA has clear positive resource implications, in terms of theatre utilization, staffing, and surgical waiting lists. What was interesting to note is that scarring did not significantly affect the operative time or the ischemic time. However, it has been shown that CTA reduces operative times.9,10 In centers that have targeted use of CTA, a CTA is more likely to be requested if a patient has had prior surgery to the abdomen. This study has several limitations. There is a relatively small sample size in the scarred group, particularly of patients with scars other than those in the lower abdomen (Caesarean section and Pfannenstiel scars). Caesarean section scarring is no longer considered a contraindication to abdominal free flap surgery.4,27 However, other scars higher in the abdomen are of continued interest. Particularly, the effects of unilateral abdominal scars on midline crossover of perfusion across the zones, which in turn will have an effect on parts of the flap, are viable and subsequent issues with postoperative fat necrosis. Intraoperative assessment of perforator anatomy and physiology is generally difficult to quantify. Further studies could involve the use of intraoperative monitoring systems such as SPY/indocyanine green, which can be used to look at real-time perfusion at the time of raising the flap. The benefit of this would be the ability to compare areas of perfusion

Table 4 e Median operative duration for bilateral and unilateral flaps. Flap type

Non-scarred (n ¼ 43)

Scarred (n ¼ 41)

Total (n ¼ 84)

Unilateral (n ¼ 59)*

410 [r: 270-615]

420 [r: 298-617]

413 [r:270-617]

Bilateral (n ¼ 25)y

637 [r: 540-705]

640 [r: 583-805]

637 [r: 540-805]

* y

p ¼ 0.4593. p ¼ 0.0672 using Mann Whitney U test.

Our study confirms the utility of CTA in facilitating FFBR from scarred abdomens and supports other studies that have shown that abdominal scarring is not a contraindication. In addition, flaps from scarred abdomens were more likely to be heavier and based on a single perforating vessel suggesting that scarring may precipitate a positive effect on intraflap vascular anatomy. Further investigations would need to be conducted to delineate the mechanism(s) by which this occurs.

Acknowledgment Authors’ contributions: L.M.N. contributed to data collection and analysis, study design, and manuscript writing. R.H. contributed to data collection, study design, and initial manuscript draft. Di Pace B contributed to data collection and initial manuscript draft. G.O. contributed to manuscript writing and editing. D.T.G. contributed to data collection, data analysis, and editing. B.C.K. was the author of all CTA reports and contributed to editing. C.M.M was the primary surgeon in all surgeries and contributed to prospective data collection, manuscript writing, study design, editing, and revisions. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The authors have no personal conflicts of interest with regard to this work.

Disclosure The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.

references

1. Blondeel PN. One hundred free DIEP flap breast reconstructions: a personal experience. Br J Plast Surg. 1999;52:104e111. 2. Nimalan N, Branford OA, Stocks G. Anaesthesia for free flap breast reconstruction. Br J Anaes Ed. 2016;16:162e166. 3. Rozen WM, Garcia-Tutor E, Alonso-Burgos A, et al. The effect of anterior abdominal wall scars on the vascular anatomy of the abdominal wall: a cadaveric and clinical study with clinical implications. Clin Anat. 2009;22:815e822. 4. Di Candia M, Al-Asfoor A, Mickute Z, Kumiponjera D, Hsieh F, Malata CM. Previous multiple abdominal surgery: a valid contraindication to abdominal free flap breast reconstruction? Eplasty. 2012;12:286e303.

n g a a g e e t a l  d i e p fl a p c t a s i n s c a r r e d a b d o m e n s

5. Parrett BM, Caterson SA, Tobias AM, Lee BT. DIEP flaps in women with abdominal scars: are complication rates affected? Plast Reconstr Surg. 2008;121:1527e1531. 6. Hsieh F, Kumiponjera D, Malata CM. An algorithmic approach to abdominal flap breast reconstruction in patients with preexisting scars: results from a single surgeon’s experience. J Plast Reconstr Aesthet Surg. 2009;62:1650e1660. 7. Hamdi M, Larsen M, Craggs B, Vanmierlo B, Zeltzer A. Harvesting free abdominal perforator flaps in the presence of previous upper abdominal scars. J Plast Reconstr Aesthet Surg. 2014;67:219e225. 8. Rozen WM, Whitaker IS, Ting JW, Ang GG, Acosta R. Deep inferior epigastric artery perforator flap harvest after abdominoplasty with the use of computed tomographic angiography. Plast Reconstr Surg. 2012;129:198ee200e. 9. Fitzgerald O’Connor E, Rozen WM, Chowdhry M, Band B, Ramakrishnan VV, Griffiths M. Preoperative computed tomography angiography for planning DIEP flap breast reconstruction reduces operative time and overall complications. Gland Surg. 2016;5:93e98. 10. Masia J, Clavero JA, Larran˜aga JR, et al. Multidetector-row computed tomography in the planning of abdominal perforator flaps. J Plast Reconstr Aesthet Surg. 2006;59:594e599. 11. Tong WM, Dixon R, Ekis H, Halvorson EG. The impact of preoperative CT angiography on breast reconstruction with abdominal perforator flaps. Ann Plast Surg. 2012;68:525e530. 12. Alonso-Burgos A, Garcia-Tutor E, Bastarrika G, et al. Preoperative planning of deep inferior epigastric artery perforator flap reconstruction with multislice-CT angiography: imaging findings and initial experience. J Plast Reconstr Aesthet Surg. 2006;59:585e593. 13. Suffee T, Pigneur F, Rahmouni A, Bosc R. Best choice of perforator vessel in autologous breast reconstruction: virtual reality navigation vs radiologist analysis (A prospective study). J Plast Surg Hand Surg. 2015;7:1e6. 14. Lee GK, Fox PM, Riboh J, et al. Computed tomography angiography in microsurgery: indications, clinical utility, and pitfalls. Eplasty. 2013;13:e42. 15. See MS, Pacifico MD, Harley OJ, Francis I, Smith RW, Jones ME. Incidence of ’Incidentalomas’ in over 100 consecutive CT angiograms for preoperative DIEP flap planning. J Plast Reconstr Aesthet Surg. 2010;63:106e110. 16. Moon HK, Taylor GI. The vascular anatomy of rectus abdominis musculocutaneous flaps based on the deep

17.

18.

19.

20.

21.

22.

23.

24.

25.

26.

27.

65

superior epigastric system. Plast Reconstr Surg. 1988;82:815e832. Phillips TJ, Stella DL, Rozen WM, et al. Abdominal wall CT angiography: a detailed account of a newly established preoperative imaging technique. Radiology. 2008;249:32e44. O’Malley RB, Robinson TJ, Kozlow JH, Liu PS. Computed tomography angiography for preoperative thoracoabdominal flap planning. Radiol Clin North Am. 2016;54:131e145. Malhotra A, Chhaya N, Nsiah-Sarbeng P, et al. CT-guided deep inferior epigastric perforator (DIEP) flap localization – better for the patient, the surgeon, and the hospital. Clin Radiol. 2013;68:131e138. Casares Santiago M, Garcı´a-Tutor E, Rodrı´guez Caravaca G, et al. Optimising the preoperative planning of deep inferior epigastric perforator flaps for breast reconstruction. Eur Radiol. 2014;24:2097e2108. Cina A, Barone-Adesi L, Rinaldi P, et al. Planning deep inferior epigastric perforator flaps for breast reconstruction: a comparison between multidetector computed tomography and magnetic resonance angiography. Eur Radiol. 2013;23:2333e2343. Molina A, Jones M, Hazari A, Francis I, Nduka C. Correlating the deep inferior epigastric artery branching pattern with type of abdominal free flap performed in a series of 145 breast reconstruction patients. Ann R Coll Surg Engl. 2012;94:493e495. Rozen WM, Palmer KP, Suami H, et al. The DIEA branching pattern and its relationship to perforators: the importance of preoperative computed tomographic angiography for DIEA perforator flaps. Plast Reconstr Surg. 2008;121:367e373. Taylor GI, Corlett RJ, Caddy CM, et al. An anatomic review of the delay phenomenon: II. Clinical applications. Plast Reconstr Surg. 1992;89:408e416. Kim SY, Lee KT, Mun GH. The influence of a Pfannenstiel scar on venous anatomy of the lower abdominal wall and implications for deep inferior epigastric artery perforator flap breast reconstruction. Plast Reconstr Surg. 2017;139:540e548. Ohkuma R, Mohan R, Baltodano PA, et al. Abdominally based free flap planning in breast reconstruction with computed tomographic angiography: systematic review and metaanalysis. Plast Reconstr Surg. 2014;133:483e494. Unukovych D, Caterson EJ, Carty MJ, Erdmann-Sager J, Halvorson E, Caterson SA. Bilateral free flap breast reconstruction outcomes: do abdominal scars affect bilateral flaps? Plast Reconstr Surg Glob Open. 2017;5:e1493.