Eur Radiol DOI 10.1007/s00330-014-3243-5

VASCULAR-INTERVENTIONAL

Optimising the preoperative planning of deep inferior epigastric perforator flaps for breast reconstruction Miguel Casares Santiago & Emilio García-Tutor & Gil Rodríguez Caravaca & Julián del Cerro González & Léa Marie Klein & Alberto Alonso-Burgos

Received: 13 March 2014 / Revised: 20 April 2014 / Accepted: 14 May 2014 # European Society of Radiology 2014

Abstract Objectives Preoperative planning of deep inferior epigastric perforator (DIEP) flaps has become increasingly important in radiology services as multidetector CT angiography (CTA) has been proven to be the technique of choice. We aim to optimise the process, checking the value of the “Navarra criteria,” assessing radiological and surgical concordance. Methods Preoperative CTA was obtained in 105 DIEP flaps involving 101 women (mean age 49.1 years). A main perforator pedicle and an alternative were chosen, applying a modification of the “Navarra criteria,” assessing the correlation between the main perforator chosen by the radiologist and the one that was ultimately used to perform the flap using the Kappa index. Results In 100 of the 105 DIEP flaps (95.2 %), the perforator pedicles chosen were ultimately used to raise the flap. Four of M. Casares Santiago (*) Department of Radiology, Hospital Universitario de Torrejon, C/ Mateo Inurria s/n. C.P.28550, Torrejon de Ardoz, Madrid, Spain e-mail: [email protected] E. García-Tutor : J. del Cerro González : L. M. Klein Hospital Universitario Guadalajara, Guadalajara, Spain E. García-Tutor e-mail: [email protected] J. del Cerro González e-mail: [email protected] L. M. Klein e-mail: [email protected] G. Rodríguez Caravaca Hospital Universitario Fundación Alcorcón, Madrid, Spain e-mail: [email protected] A. Alonso-Burgos Hospital Universitario Fundación Jiménez Díaz, Madrid, Spain e-mail: [email protected]

the perforator pedicles that were not used were dismissed due to avoidable errors in the radiological approach. Concordance was very high, with a Kappa index of 0.93 (95 % CI: 0.87– 0.99). CT room time was less than 12 minutes, and reading time was 10 minutes. Conclusions The application of the “Navarra criteria” in preoperative planning of DIEP flaps improves radiological and surgical concordance as well as the reading process. Key Points • DIEP flap is one of the best techniques for breast reconstruction. • Preoperative planning is essential in DIEP flaps. • CTA is the best option for the preoperative planning of DIEP flaps. • “Navarra criteria” allow radiologists to choose the best perforator to form flaps. • Modified “Navarra criteria” improves radiological and surgical concordance.

Keywords Breast reconstruction . DIEP flap . Preoperative planning . CTA . Preoperative imaging

Abbreviations CDS Colour Doppler sonography CTA Multidetector computed tomography angiography DIEA Deep inferior epigastric artery DIEP Deep inferior epigastric perforator MIP Maximum intensity projection MPR Multiplanar reconstruction MRA Magnetic resonance angiography SIEA Superficial inferior epigastric artery TRAM Transverse rectus abdominis myocutaneous VR Volume rendering

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Introduction The preoperative planning of breast reconstruction with deep inferior epigastric perforator (DIEP) flap is becoming increasingly common in radiology departments as multidetector computed tomography angiography (CTA) has become the technique of choice [1–8]. Breast reconstruction is an essential component of the overall treatment plan of breast cancer patients, and the techniques employed in reconstruction are becoming more and more sophisticated, seeking to optimize the appearance and sensation of a native breast. One such technique is autologous breast reconstruction using perforator flaps, which is able to create a new breast that looks and feels like the original breast. Perforator flaps allow the transfer of the patient’s own skin and fat using microsurgery, the soft tissue of the lower abdomen being a good source for this purpose. Autologous breast reconstruction with abdominal tissue using a DIEP flap is an evolution of the classical transverse rectus abdominis myocutaneous (TRAM) flap, which can perfuse the same tissue without sacrificing the rectus muscle or fascia, thereby minimizing donor-site morbidity, pain, and recovery time [9]. We report the most important benefits, as follows. The DIEP flap is the largest perforator flap that can be raised in the entire body, and allows a primary closing. It also offers one of the longest vascular pedicles, as the dissection is taken all the way from the origin of the deep epigastric system, and is therefore the most widely used in breast reconstruction surgery. Furthermore, it allows the performance of both immediate and delayed reconstructions, since the volume of tissue that is obtained can be used to cover the bloodiest and most retractile scars, including those that present with postradiation ulcerations. The DIEP flap is also associated with fewer complications, such as weakness of the abdominal wall and/or affectation of the muscular function. It has even been shown to decrease the duration of hospital stays, and it is lower in cost compared to alternative surgical reconstructions [10–13]. The abdominal scar is similar to that of an aesthetic eventroplasty, easily hidden by clothing (even with a bikini), and produces a remodelling of the abdominal fat, which tends to be appreciated by the patient. However, raising a perforator flap requires meticulous dissections of the perforator vessels, sparing the muscular structure and being mindful of the presence of broad interindividual variability in the deep inferior epigastric artery (DIEA) branching pattern and the location of its perforators. These perforators originate from the DIEA, which is usually located between the posterior layer of the rectus sheath and the posterior border of the rectus muscle; they penetrate the posterior surface of the rectus abdominus and have a variable intramuscular segment. After this segment, the vessels penetrate the anterior surface of the rectus sheath and the anterior

layer of the fascial sheath simultaneously, or they can have a varying subfascial segment between the anterior border of the rectus muscle and the anterior layer of the rectus sheath. Finally, there is a subcutaneous segment with a variable branching pattern within the subcutaneous fat [14]. Importantly, it is each patient’s anatomy that dictates the perforator(s) on which the flap will be based [10, 11], which is why a preoperative mapping of the anatomy of these perforators is essential. In order to obtain a map of the perforator arteries of the abdominal wall and to develop an adequate preoperative surgical plan, there are three fundamental tools currently available in daily clinical practice: colour Doppler ultrasound (CDS), multidetector CT angiography, and magnetic resonance angiography (MRA). CDS has been progressively abandoned in favour of CTA, as it is an operator-dependent, long, and difficult exploration, with documented falsepositive pitfalls [6, 7]. MRA is becoming replacing CTA as an alternative, avoiding the exposure to ionizing radiation and iodinated contrast medium, with similar results for the study of large perforators [15, 16]. However, MRA is more expensive and less available than CTA [15–17], and so it may replace CTA in selected subgroups of patients such as young women or women allergic to iodinated contrast, [15]. CTA is considered the current gold standard, as it can provide all of the information necessary for the vascular mapping of the anterior abdominal wall, with reported sensitivity and specificity reaching 96 %–100 % and 95 %–100 %, respectively, in cadaveric and clinical studies. It has also been proven to reduce perforator dissection times and postoperative complications [1–8]. All of these imaging modalities for the surgical planning of the DIEP flaps were analysed and discussed during the course of an international and multi-disciplinary meeting that took place in Navarra (Spain) [18], the aim of which was to reach international consensus with respect to the precise information that the imaging studies must be able to provide to the surgeon prior to the intervention. Agreement was reached concerning the criteria that must be met by the “ideal” vascular pedicle (Table 1). These criteria were chosen to simplify and accelerate the operation and minimize existing complications in the DIEP flap surgery, focusing on getting a good blood supply and good venous drainage for the flap. Although not designed initially with this particular objective in mind, these criteria have a direct application in the CT images, allowing the selection of this ideal vascular pedicle (within all the abdominal perforator pedicles). The aim of this study is to find a way to optimise the information provided by the CTA, using the “Navarra meeting” criteria, in order to issue a report of maximum usefulness for the plastic surgeon without requiring a great investment of time on the part of the radiologist. Our goal is to evaluate the

Eur Radiol Table 1 “Navarra meeting” ideal vascular pedicle description. From: Rozen WM, Garcia-Tutor E, Alonso-Burgos A, et al. Planning and optimizing DIEP flaps with virtual surgery: the Navarra experience. J Plast Reconstr Aesthet Surg 2010; 63:289–297(25) The “Navarra meeting” ideal vascular pedicle criteria 1) Large-calibre DIEA and vascular pedicle 2) Large-calibre perforator (both artery and veins) 3) Central location within the flap 4) Short intramuscular course 5) Perforating veins communicate with the superficial venous network 6) Broad subcutaneous branching, particularly into the flap 7) Longer subfascial course 8) Avoids tendinous intersections

usefulness of the Navarra meeting criteria for preoperative planning using CTA in patients undergoing postmastectomy DIEP flap reconstruction by assessing radiological and clinical concordance.

Materials and methods Patient sample Through sampling by consecutive inclusion, all patients scheduled to undergo autologous reconstructive breast surgery in our institution during the period from March 2009 to November 2013 were included in this study. The indication for breast reconstruction surgery using a DIEP flap was the only selection criterion. Patients with a history of sensitivity to iodinated contrast medium were pre-medicated, and this condition was not considered an exclusion criterion. CTA protocol After obtaining informed consent in all the cases, a CTA was performed using a 64-row Toshiba Aquilion CT (Toshiba Medical, Tokyo, Japan). The parameters of the exploration are summarized in Table 2. The exploration should be carried out with the patient in supine position, which is the same as that carried out afterward on the operating table. It is important to remove the underwear to avoid markings over the abdominal fat and skin, which may modify the trajectory of the perforator vessels. Patient’s arms must be alongside the body, with flexed elbows to avoid artefacts, or behind the head. In any case, they must be in the same position as they would be on the operating table. The performance of CTA requires the intravenous administration of iodinated contrast medium, using 100 ml of ioversol (Optiray 320 mg/ml) at a flow rate of 4 ml/s. A fixed dose of contrast material is easier to manage routinely, but a

Table 2 CTA imaging protocol CTA imaging protocol • Aquilion 64 MDCT, Toshiba • Scan range: 5 cm upward from umbilicus to the small trochanter. • Injection of 100 ml of ioversol contrast medium (Optiray 320 mg) at a flow rate of 4 ml/s. • Bolus track in abdominal aorta, 2 cm above bifurcation; 180 HU threshold, then scan delay of 15-20 seconds *. • No oral contrast medium • Image Thickness: 0.5 Recon Interval: 0.4 *Even though the studies are aimed to characterize the arterial system, the scan is delayed 15–20 seconds from the bolus trigger to allow an analysis of the superficial venous network, important for the flap outcome

dose of 1.3 ml/kg of body weight can be used in either very thin or overweight patients. We do not routinely use highconcentration iodinated contrast material, as it is not available in our hospital; however, it has been reported as useful for the identification of tiny perforator branches in intramuscular segments [14]. No oral contrast is administered. The CTA programming is performed with bolus tracking, placing the sample in the aortic lumen, 2 cm away from the bifurcation and with a shot margin of 180 UH. The shot is initiated with a delay of 10–15 seconds. The delay of the shot is necessary in order to obtain a late arterial or early venous phase, in which we can study not only the perforator arteries but also the superficial venous system. These late phases are crucial to match the previously described Navarra criteria. The range of the exploration should involve an area from 5 cm above the umbilicus to the femoral trochanters in order to be able to evaluate the deep epigastric arteries from their origin. There is no need to perform the exploration very far above the umbilicus, since the flap will be obtained from the cutaneous and adipose tissue of the lower abdomen. This allows us to reduce the radiation dose received by the patient. Mapping process The obtained axial images were processed on an Advantage Windows Volume Share 2 workstation (GE Healthcare, Waukesha, WI, USA), obtaining multiplanar reconstructions (MPR), maximum-intensity projections (MIP), and volume reconstructions (VR). The processing software for the images is not exclusive of the brand and is available in the market. The preoperative study was performed by two trained radiologists with more than three years of experience in preoperative planning of reconstructive surgery using CTA, delivering a single consensus report. Only two ideal perforator pedicles were chosen, matching the Navarra criteria. We marked one main perforator with which the concordance study would be performed and one rescue alternative. This rescue perforator was always chosen in the contralateral

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hemiabdomen, and the concordance was considered as having failed when the flap was raised within this pedicle. The Navarra criteria are directly applicable to the image, with the exception of the third parameter, which refers to the importance of having the perforator artery in a central position in relation to the flap. This appears to be a problem for the design of the flap in the operating room, which does not depend on the image, and therefore this criterion was substituted by an alternative one: the marking of the perforator arteries located more than 3 cm above the umbilicus should be avoided, as the subcutaneous adipose tissue loses thickness as one moves in a cranial direction away from the umbilicus, making retrieval of a flap with sufficient volume more difficult. The Navarra criteria applied to the CTA image would then remain as shown in Table 3. We also added the abdominal scars to the eighth criterion, as it is important to avoid fibrous tissue that is difficult to dissect, not only in tendinous intersections, but also in abdominal scars. The choice of the perforator artery is easily made over a thick axial MIP reconstruction, which allows simultaneous evaluation of the calibre of the vascular pedicle, the intramuscular trajectory, the subcutaneous branches, and the superficial venous system. Once the ideal perforator pedicle has been chosen, the exact point where it emerges through the superficial fascia of the rectus muscle is located in the 1 mm axial images. This point is taken to a frontal volumetric reconstruction of the abdominal wall (Fig. 1), where it is marked with respect to the umbilicus and measured in orthogonal axes. It can be useful for the surgeon to superimpose a grid to facilitate a direct transfer of the volume image – with the marked perforator artery – to the abdominal wall on the operating table (Fig. 2). For statistical purposes, the “ideal” perforators chosen were divided into four areas: on each side of the abdominal midline, and starting with the right margin, lateral and medial area was named as depended on the medial or lateral area to the deep inferior epigastric artery branch. In cases where the interindividual anatomical variability may not define two zones Table 3 The “Navarra” criteria, modified to fit the CTA image. The “Navarra meeting” criteria applied to the CTA image 1) Large-calibre DIEA and vascular pedicle 2) Large-calibre perforator (both artery and veins) 3) Located no more than 3 cm above the umbilicus as the maximum limit in the cranial direction 4) Short intramuscular course 5) Perforating veins communicate with the superficial venous network 6) Broad subcutaneous branching, particularly into the flap 7) Longer subfascial course 8) Avoids tendinous intersections and abdominal wall scars

of irrigation, reference was made to the centre of the muscle mass of the rectus abdominis, defining a medial and lateral to each side of the midline. Thus, we define (Fig. 3): a) “A” Perforator: dominant perforator in the territory of the lateral branch of the right DIEA or located in the lateral half of the right rectus muscle. b) “B” Perforator: dominant perforator in the territory of the medial branch of the right DIEA or located in the medial half of the right rectus muscle. c) “C” Perforator: dominant perforator in the territory of the medial branch of the left DIEA or located in the medial half of the left rectus muscle. d) “D” Perforator: dominant perforator in the territory of the lateral branch of the left DIEA or located in the lateral half of the left rectus muscle.

In some cases, patients initially admitted to the operating room for a DIEP flap ultimately received a SIEA flap. Although the SIEA flap transfers the same area of skin and subcutaneous fat from the lower abdomen as the DIEP flap, it uses another flow, namely the superficial inferior epigastric artery (SIEA). Therefore, it is not necessary to open the muscle fascia and dissect the intramuscular path of the artery, resulting in shorter and easier surgery. While the SIEA features great anatomical variability and is rarely useful for a flap, in some patients the surgeon can find a favourable SIEA at the beginning of the dissection of the abdominal wall, and may decide to convert a DIEP flap surgery to a SIEA flap. These were excluded from our statistical analysis, as they are outside the scope of our study. The radiologist performs preoperative planning by assessing DIEA perforators, although he is able to assess the existence of a good-calibre SIEA, However, the surgeon will not evaluate the DIEA perforators, and thus our correlation analysis is not possible. Once the ideal perforator pedicles have been selected, their trajectory and relations can be evaluated in depth using the MIP and VR reconstructions, which are particularly illustrative for the surgeon, allowing him or her to perform a preoperative “virtual” surgery. On the operating table, the surgeon uses the VR images as a reference in order to mark directly on the skin the origin of the perforating artery prior to initiating the dissection (Fig. 4). After surgery, the senior surgeon documents the perforator that was ultimately used to perform the flap. He also documents the intraoperative variations of the CTA preoperative planning, such as alterations in the intramuscular course, communications with the superficial venous system, or abdominal scars or fibrous tissue adjacent to the chosen perforators. Hemiabdominal perforators are evaluated for unilateral

Eur Radiol Fig. 1 a and b Axial MIP image, showing a good-calibre right perforator artery, with various subcutaneous branches, which surrounds the muscle medially, facilitating the dissection. The communications with the venous system are visible in the lateral margin. c VR image of the anterior abdominal wall, using the umbilicus as a reference, orthogonal measurements are performed to facilitate the location of the origin of the perforator artery on the operating table

DIEPs; bilateral cases are considered as two separated hemiabdomens. In summary, the radiologist’s contribution to the procedure should include: 1. A short report highlighting the chosen perforator pedicles and, if available, local or regional anatomical facts of interest. 2. Axial MIP images of the chosen perforator pedicles and their location in a frontal coronal plane of a VR reconstruction of the anterior abdominal wall (Fig. 1). Fig. 2 a and b VR image of the anterior abdominal wall with the orthogonal measurements of the origin of the perforating artery. b Over the image of the abdominal wall we superimpose a grid in order to facilitate the references once in the operating room. c Once in the operating room, the surgeon marks the origin of the perforator artery using the VR images as a reference. Only one right perforator artery has been marked

3. Axial or sagittal oblique MIP or VR images of the chosen perforator pedicle, showing its path from the DIEA to the subcutaneous tissue, depending upon the surgeon’s choice in each case (Figs. 5 and 6).

Statistical analysis The concordance between the perforator pedicle chosen by the radiologist and the pedicle chosen by the surgeon and ultimately used to raise the flap was calculated with Cohen’s

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Fig. 3 Coronal MIP image (left) and axial (right) of the abdomen, showing the areas on which we define the dominant perforator

Kappa index, with its confidence intervals set at 95 %. The index of concordance was calculated in a global and stratified manner according to the type of intervention (immediate or delayed) and the complete years of work. Statistical calculations were performed using SPSS 16 (SPSS, Chicago, IL), considering a p value < 0.05 as significant.

Results A total of 101 women were studied (101 consecutive CTA prior to breast reconstruction using the DIEP flap at our institution). In six of these patients, the surgery ultimately Fig. 4 a Preoperative image of delayed breast reconstruction with DIEP flap. b: Image of averted flap, the blue arrow marks the beginning of the perforator. c Image of the reconstruction result. The nipple and areola can be reconstructed in a second surgery if the patient requests it

resulted in a SIEA flap, and these patients were excluded from the study. In 10 of these patients, a bilateral DIEP flap was performed, so the radiologist marked one ideal and rescue perforator for each hemiabdomen. In summary, the statistical analysis was performed with 105 perforators marked by the radiologist and 105 DIEP flaps performed by the surgeon. The mean age was 49.1 years, range 29–73 years (SD= 9.0). A total of 66 patients (62.9 %) underwent immediate and 39 (37.1 %) underwent delayed breast reconstruction. The mean age of the women in both groups correlates with a median of 48 years. The distribution frequency of the type of surgery, stratified by age of work, showed an increased frequency of immediate surgeries over time, from 64 % in 2009 to 100 % in 2013. The trend assessment, performed by Chi squared for linear trend, showed a statistically significant upward trend. In 100 of the 105 DIEP flaps performed (95.2 % of cases), the perforators chosen in the CTA preoperative planning were the same as those ultimately used to raise the flap. In six of these patients, additional small perforators close to the marked one were identified during surgery. These perforators were able to be dissected in order to improve the vascularization of the flap, but they had either not been previously identified or were not significantly relevant in the CTA images. Most perforators chosen by both the radiologist and the surgeon were in zones B and C, which correspond to the areas closest to the midline (Fig. 7). In the remaining 5 of the 105 patients, the perforator arteries chosen in the CTA planning were not used in the final creation of the flap:

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Fig. 5 VR Reconstruction of the anterior abdominal wall, showing segmental anatomy of a DIEA perforator

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In one patient, the chosen perforator pedicle was located in a fibrotic area within the subcutaneous cellular tissue. This finding (not identified in the CTA images) hinders the vessels dissection, and therefore the rescue perforator artery of the contralateral hemiabdomen was used. In two patients, the marked perforator pedicles were located too cranially from the umbilicus, so that the skin and the underlying subcutaneous adipose tissue at this level were insufficient to design a flap in accordance with the expectations of breast symmetry. Consequently, more caudally located alternatives needed to be located in the operating room. In one patient, the perforator pedicle that had been marked presented scarce venous component. As previously described, this finding is important for the long-term survival of the flap, as it may result in post-implantation venous congestion. The rescue perforator pedicle was chosen in the operating room. In one patient, the perforator pedicle that had been marked as the first option was damaged during the dissection of the flap, and the rescue alternative was used.

The global concordance was very high, with a Kappa index of 0.9 (95 % CI: 0.87–0.99). Concordance stratified by type of surgery was very high for the delayed surgery, with a Kappa index of 0.9 (95 % CI: 0.88–1.00) and also very high for the immediate surgery, with a Kappa index of 0.9 (95 % CI: 0.82– 1.00). Concordance stratified by the presence of previous abdominal scars was very high in both cases, with a Kappa index of 0.9 (95 % CI: 0.83–0.99) in cases without abdominal scars and 0.9 (95 % CI: 0.88–1.00) in cases with abdominal scars. Concordance stratified by complete years of work was very high in the four years, with a Kappa index of 0.9 in 2009, 2010, and 2012, and a perfect correlation index of 1 (95 % CI: 1.00–1.00) in 2011. The exploration time of the CTA did not exceed 12 minutes in any case, including the process from the vein cannulation to the exit of the patient from the CT room. The location of the perforator arteries according to the Navarra criteria was possible in all cases, as planned. The ideal perforator was located on 1 mm axial images, supported by the MIP reconstructions, using the modified Navarra

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Fig. 6 MIP Reconstruction of the anterior abdominal wall, showing segmental anatomy of a DIEA perforator, detailing the superficial venous system

criteria. The exact point where the perforator emerges through the superficial fascia of the rectus muscle was located. This point was taken to a frontal volumetric reconstruction of the abdominal wall, where it was marked, adding this image and an identical image with a superimposed grid to the report. The Fig. 7 Areas of distribution of the perforator chosen by the radiologist and surgeon.

process was then repeated for the rescue perforator. Finally, MPR and VR reconstructions were made of only these two perforators, according to the surgeon’s request. The entire process in the workstation, including the transmission of the report and the described images, was completed in an average

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of 10 minutes. In cases, the surgeon may have required clarification regarding the images; as this length of time was highly variable, we did not include it in the study results.

Discussion There is a growing presence of preoperative planning of DIEP flap in radiology services, as DIEP flaps are becoming the technique of choice in postmastectomy reconstructive surgery, and CTA has been shown to improve surgical outcomes, reducing operative time as well as postoperative complications [1–8]. Since the 2006 publication by Alonso-Burgos et al. and Masia et al. of the initial experiences with preoperative planning of DIEP flaps with CTA, in different groups [1, 2], most articles in the literature have established a complete map of all of the perforator arteries of the DIEA or a marking of many of them based on their own non-standardized criteria, which have included large vessel diameter and, more recently, branching pattern and superficial venous system communications. It is always useful for the radiologist to have a list of criteria to support his/her diagnostics. With this in mind, we have applied the Navarra criteria, created to describe the ideal vascular pedicle for a flap, in the CTA image. Our experience has shown that the second criterion, choosing the largest perforator, is the most critical. As is amply described in the literature, a higher-calibre vascular pedicle not only ensures better flow in the flap, but facilitates the dissection and subsequent anastomosis as well [1, 18, 19]. The first criterion, choosing the highest-calibre DIEA, has been less relevant in terms of its application in imaging. In our experience, both DIEAs usually have a virtually indistinguishable size in the CTA image, or if there are significant differences, the larger-calibre perforator is usually dependent upon the larger-calibre DIEA. We have appreciated that the DIEA type I – the non-branching type – often comes with higher calibre distally and also gives rise to periumbilical perforators of a larger calibre. As we have not specifically studied this finding, and it is not described in the literature, it may represent a future research opportunity. The third criterion, as previously described, defines the importance of not marking perforators over 3 cm above the umbilicus. Since larger-gauge perforators usually cross the superficial fascia of the rectus muscle in the vicinity of the umbilicus, it is important to keep this criterion in mind, and not be tempted to mark the perforators that are above the maximum 3 cm cranial limit, even if they are the largest calibre or the most favourable. The fourth criterion concerns the intramuscular course. A short intramuscular course has several benefits. Because its separation from the adjacent muscle is easier, it facilitates dissection of the perforator, thus reducing the likelihood of

muscular branches requiring ligation. In the case of more than one perforator being included in the flap, a short transverse distance is associated with shorter dissection time and less need for sacrifice of muscle [18]. We have often found that good-calibre perforators next to the umbilicus drill the superficial rectus abdominis fascia by surrounding the muscular mass medially, without ever becoming intramuscular, which is the best possible option. The fifth criterion is of particular importance, as it demonstrates that extensive communication with the superficial venous system reduces the likelihood of post-implantation venous congestion of the flap, a serious complication that in some cases is fatal for the survival of the flap. The Blondeel team [20] demonstrated that, wherever communication between the deep and superficial venous systems was evident on preoperative angiography, issues with venous drainage were less likely to occur. This also allows drawing a second drainage line in case of failure of the central vein of the flap. With the sixth criterion, which relates to the importance of having broad subcutaneous branching, particularly into the flap, our experience has shown us that the larger the size of the perforator, the greater and more patent its subcutaneous ramifications, and thus this criterion can be applied in cases where there are two very similar perforators. The reason for this is simple: the larger and broader the subcutaneous branching, the richer the subcutaneous flow in all areas of the flap, which reduces the onset of fat necrosis. The seventh criterion is associated with the fourth, as it has been observed that a long subfascial segment is usually associated with a short intramuscular segment [18]. Usually, the perforators emerging from the DIEA show an oblique course in the cranial direction, so that part of their location is subfascial and another part is intramuscular. Generally, the longer the subfascial course of the perforator, the shorter its intramuscular course, and vice versa. In most cases, the choice of best perforator (which is our main objective) was conditioned by the election of the calibre and its intramuscular course. Therefore, this criterion may be included in the fourth criterion, as it does not actually enter into the final decision. Last but not least, we must mention the eighth criterion. Tendinous intersections should be avoided because the fibrous tissue is difficult to dissect and can cause injury of the vessel during surgery. Scars, often unnoticed in the CTA image, are associated with difficult dissections, and sometimes result in amputations of small-calibre vessel vascularization areas next to the chosen perforator. This can be limiting, since in some cases favourable perforators have been discarded because they were in a tendinous intersection or near abdominal scars. The current trend in the experienced surgical groups is to perform an immediate surgery in order to reduce the number of interventions, general anaesthetics, and days of hospitalization, as well as to reduce costs and patient discomfort [21, 22]. In our study, 62.9 % of the operations were performed

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immediately, which is superior to most of the working groups in the literature, and reflects the effort of this team to improve the quality of treatment. In fact, this favourable frequency distribution has increased over time, and we have gone from 64.7 % immediate surgery in 2009 to 100 % in 2013, and thus the valuation of the Chi squared test showed a statistically significant upward trend. Most perforators selected by the radiologist, as well as those that ultimately were chosen to perform the flap, were in B and C (central) regions of the abdomen. This is consistent with anatomical studies cited in literature, which show that larger-calibre perforators are more often periumbilical. It is also consistent with the publications of most current groups, which refer to these perforators as guaranteeing greater viability of the flap [1, 7, 23–25]. In 100 of 105 DIEP flaps performed (95.2 % of cases), the perforators chosen in the preoperative planning were used to raise the flap, representing a very high concordance ratio, with a Kappa index of 0.9 (95 % CI: 0.87–0.99). We also performed concordance analysis stratified by type of surgery (immediate and delayed), which showed no significant difference. The stratified concordance by complete years of work was very high during the four years, with a perfect correlation index in 2011, which we were not able to maintain in 2012. Such high correlation between the perforator chosen by the radiologist in preoperative planning on CTA images and the perforator ultimately used in surgery reflects not only the anatomical precision and high diagnostic capability of the CTA image for the detection of abdominal vascular pedicle, but also that the application of the Navarra criteria allows us to choose the best vascular pedicle to form the flap. The high anatomical reliability of CTA is no surprise, given the extensive experience in the vascular assessment of these images on other clinical applications, and correlates with almost all of the articles published and referenced multiple times in this work [1, 3–8]. Assuming that the CTA image corresponds to the anatomical reality of the abdominal wall of the patient, the application of the Navarra criteria is able, in essence, to employ the surgeon’s priorities in selecting the best vascular pedicle to form the flap, but to do so virtually and preoperatively. Most of the articles in the literature correlating CTA with surgical findings raise a vascular mapping of the abdominal wall as a reference to the surgeon, or choose a couple of dominant pedicles based on the calibre of the perforator and ease for dissection of the intramuscular route, and directly relate to the findings at surgery, without trying to determine the best pedicle to form the flap. With this design, the correlation was above 99 % for Rozen et al. [3, 4, 6, 8], and up to 100 % for Alonso-Burgos [1] and Clavero and Masia [2, 26, 27], the three pioneers, and the most productive groups in the literature.

Since the early use of CTA for preoperative planning of DIEP flap reconstructions in 2006, there have been no publications that attempt to standardize a protocol for the selection and marking of DIEA perforators. Now that CTA has been proven to be the best imaging method available for this purpose, it seems of great interest to create a protocol that is not only effective and easily reproducible, but also efficient. To our knowledge, there is only one article in the literature with a design similar to the present study. This was a retrospective study by Keys et al. in 2013 [28] of 37 patients with a total of 57 DIEP flap reconstructions. A CTA was obtained, marking the three larger-size perforators, and correlating them with those used in the flap. With this approach, they marked 76, of which 62 (82 %) were ultimately used in surgery. Of the 14 unused perforators, 10 were abandoned due to the surgeon’s reported inadequacy of the preoperative CTA; the other four did not have a recorded reason. If a perforator was added or removed intraoperatively because of intramuscular course or because the planned perforators were deemed insufficient, the CTA was labelled as inadequate. The authors also conclude that 23/52 flaps (44 %) involved intraoperative changes due to features not appreciated on preoperative CTA. In our experience, only two perforators (1.9 %) were rejected due to errors in the CTA image: a perforator that was in an area of fibrosis, which was not identified on the image, and a pedicle that had a small venous component, also not significantly identified in the preoperative image. The areas of fibrosis are often very difficult to identify, especially in 1 mm axial images. To avoid the marking of a perforator over an area of fibrosis or a scar, it is important to assess the patient’s clinical history and correlate fine axial images with the 3D surface reconstruction to identify scars without error. In order to determine whether the presence of abdominal scars could change our concordance rate, we performed a concordance study stratified by the presence of previous abdominal scars. Agreement was very high in both cases, with a Kappa index of 0.9 (95 % CI: 0.83 to 0.99) in cases without previous scar and a slightly lower Kappa index, 0.8 (95 % IC: 0.88 to 1.00), in patients with a scar. There was no statistically significant difference. It is possible that a larger sample could produce significant differences. Our error in assessing the venous component of the vascular pedicle was related to the CTA imaging planning. In our group, the images are obtained with bolus tracking after 12 to 15 seconds of delay. Therefore, we want to achieve early venous phase, which allows us to evaluate not only the perforator artery but also those veins that collect blood specifically from these arteries. The superficial venous system, as previously described, is vitally important for the survival of the flap. Rozen et al. and Masia and Clavero performed pure arterial phase [2, 8], while Alonso -Burgos and Rosson performed better venous assessment similar to our group schemes [1, 5]. The current trend is to obtain pure venous phase, which

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allows a good evaluation of the venous component of the vascular pedicle, but penalizes the arterial assessment. It also produces low arterial enhancement and high tissue enhancement, so that the contrast between the perforator and the adjacent muscle is reduced and evaluation of the intramuscular segment of the perforator is more difficult. The other two rejected perforators were due to errors in the marking, as the marked perforator was too cranial in origin to the umbilicus, and as previously mentioned, the skin and the underlying fat at that level were not enough to design a quality flap. This was a planning error that led to a modification of the Navarra criteria, as described above. Keys et al. describe many cases (73 % of the total) of additional perforators identified during surgery that could be used in the formation of the flap but that were not marked on CTA. As mentioned previously, this also occurred in our study, but only in six patients. In some cases, these perforators can be assessed retrospectively in the CTA, but generally are low-calibre and were dismissed in the marking. The results of this study, compared to our own work, reinforce the need for a protocol to enhance the accuracy of radiologists in selecting the ideal perforator. We think that this is achieved with the modified Navarra criteria, which we have applied in our work. On the other hand, our study showed that marking two perforators was sufficient, as our first choice of perforator achieved a very high correlation index, as evidence of our efficiency. It would be desirable to expand the sample to assess a greater number of cases, and with the experience gained during the process, we might achieve perfect or near perfect agreement. We acknowledge a limitation in our study design: a diagnostic review bias can occur, given that the surgeon is knowledgeable of the preoperative planning of the radiologist, so it would appear that he could dismiss all of the perforators not marked in the CTA image. However, as the surgeon begins the dissection of the flap in the lateral margins of the lower abdomen, he needs to value all of the perforators in his way as he proceeds medially in the dissection of the flap. In each case, he must decide whether to keep the perforator to use as a vascular pedicle or band it [29]. While one might assume that prior knowledge of the images and the CTA report makes it easier to dismiss unmarked pedicles, we maintain that the surgeon must review them all, and therefore judgment and experience will prevail regardless of the CTA images. The initial idea of the study was to develop a better approach to preoperative planning of DIEP flaps. The whole design is based on the application of the Navarra criteria, supported by the international meeting consensus. The application of our modification of these criteria facilitates the radiologist’s work on the perforators of the abdominal wall with a fast and reproducible method in the sense that there is no need to map and perform reconstructions of all of the perforator pedicles in the abdominal wall, but rather that it

suffices to mark and reconstruct just one or two “ideal” pedicles in each case. For the surgeon, the benefits are even greater, because they can identify their choice of the best perforator to create the DIEP flap, and they receive a report with sharp and detailed images on the morphology and course of these vessels, as well as possible findings of anatomical variations that may change their approach. Our study’s real interest lies in the exportation of our protocol to all departments of radiology in order to improve their daily workflow in the preoperative planning of DIEP flaps, with benefits for both the radiologist and the surgeon. Acknowledgements The scientific guarantor of this publication is Dr. Emilio Garcia-Tutor ([email protected]). The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. One of the authors, Gil Rodríguez Caravaca, has significant statistical expertise. Institutional Review Board approval was obtained, as it is an observational study, which does not change the usual diagnosis and treatment sequences. All of the information and images of patients used for the study was anonymous. Written informed consent was obtained from all subjects (patients) in this study. Some study subjects have been previously reported as a poster in ECR 2013 with DOI: 10.1594/ecr2013/C-1030. Methodology: prospective, observational, performed at one institution.

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20. Blondeel PN, Arnstein M, Verstraete K, Depuydt K, Van Landuyt KH, Monstrey SJ, Kroll SS (2000) Venous congestion and blood flow in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps. Plast Reconstr Surg 106:1295– 1299 21. Elder EE, Brandberg Y, Björklund T, Rylander R, Lagergren J, Jurell G et al (2005) Quality of life and patient satisfaction in breast cancer patients after immediate breast reconstruction: A prospective study. Breast 14:201–208 22. Khoo A, Kroll SS, Reece GP, Miller MJ, Evans GR, Robb GL (1998) A comparison of resource costs of immediate and delayed breast reconstruction. Plast Reconstr Surg 101:964–968, Discussion 969– 970 23. Blondeel PN, Morris SF, Hallock GG, Neligan PC (2006) Perforator flaps, anatomy, technique & clinical applications. St Louis Quality Medical Publishing 24. Giunta RE, Geisweid A, Feller AM (2000) The value of preoperative Doppler sonography for planning free perforator flaps. Plast Reconstr Surg 105:2381–2386 25. Rozen WM, Ashton MW, Pan WR, Taylor GI (2007) Raising perforator flaps for breast reconstruction: the intramuscular anatomy of the deep inferior epigastric artery. Plast Reconstr Surg 120:1443–1449 26. Clavero JA, Masia J, Larrañaga J, Monillm JM, Pons G, Siurana S, Alomar X (2008) MDCT in the preoperative planning of abdominal perforator surgery for postmastectomy breast reconstruction. Am J Roentgenol 191:670–676 27. Masia J, Larranaga J, Clavero JA, Vives L, Pons G, Pons JM (2008) The value of the multidetector row computed tomography for the preoperative planning of deep inferior epigastric artery perforator flap: our experience in 162 cases. Ann Plast Surg 60:29–36 28. Keys KA, Louie O, Said HK, Neligan PC, Mathes DW (2013) Clinical utility of CT angiography in DIEP breast reconstruction. J Plast Reconstr Aesthet Surg 66:e61–e65 29. Granzow JW, Levine JL, Chiu ES, Allen RJ (2006) Breast reconstruction using perforator flaps. Review. J Surg Oncol 94:441–454