Double-Pedicle DIEP and SIEA Flaps and Their Application in Breast Reconstruction

Nevertheless, large breast reconstruction still remains a challenge for the surgeons because the amount of fat that could be safely transferred with the DIEP and SIEA flaps in the conventional way could be insufficient to achieve a good symmetry with the contralateral breast. A contralateral reduction mammaplasty may solve some of these cases, but in other clinical situations a flap larger than standard is needed. This fact gains importance especially in patients with scant abdominal tissue or infraumbilical vertical scars, and in delayed reconstructions after previous modified radical mastectomy (MRM) where there is a severe lack of skin and subcutaneous tissue. Moreover, patients who previously had mastectomy plus expander breast reconstruction often show a depression of the cartilage rib cage which could need larger flap to be corrected.


Introduction
Autologous breast reconstruction with deep inferior epigastric artery perforator (DIEP) and superficial inferior epigastric artery (SIEA) flaps is nowadays considered the gold standard in post-mastectomy reconstruction. Excellent results could be achieved in term of softness and natural appealing breast, making these lower abdominal flaps very popular.
Nevertheless, large breast reconstruction still remains a challenge for the surgeons because the amount of fat that could be safely transferred with the DIEP and SIEA flaps in the conventional way could be insufficient to achieve a good symmetry with the contralateral breast. A contralateral reduction mammaplasty may solve some of these cases, but in other clinical situations a flap larger than standard is needed. This fact gains importance especially in patients with scant abdominal tissue or infraumbilical vertical scars, and in delayed reconstructions after previous modified radical mastectomy (MRM) where there is a severe lack of skin and subcutaneous tissue. Moreover, patients who previously had mastectomy plus expander breast reconstruction often show a depression of the cartilage rib cage which could need larger flap to be corrected.

Relevant applied microvascular anatomy of the DIEP and SIEA flaps
DIEP and SIEA flap relevant anatomy has been extensively explained in the relative chapters. In this paragraph we will focus on the microvascular anatomy of the abdominal flaps as its comprehension is key-point when choosing a double-pedicle instead of an unipedicle flap. A three-and four-dimensional computed tomographic angiography (CTA) study by Wong C. et al. on injected medial and lateral row DIE perforators demonstrates that the area of perfusion of a medial row DIE perforator is larger (around 300 cm 2 ) and more centralized when compared to the lateral row DIE perforator ones, that results smaller (around 200 cm 2 ) and more lateralized, encompassing almost only the ipsilateral hemiabdomen.

Arterial microvascular anatomy
When selecting a perforator for DIEP flap reconstruction, the largest perforator should be selected (i.e. the dominant perforator). The medial row perforators have been shown to often have dominance over the lateral row perforators. Furthermore, the "clinical" angiosome sustained by a medial row perforator is normally larger than the one sustained by a lateral row perforator.
The perfusion of the transverse lower abdominal flap was first described by Scheflan and Dinner on the unipedicle transverse rectus abdominis musculocutaneous (TRAM) flap. These authors divided the lower abdominal ellipse into four equal parts and named them with numbers according to their clinical impression of perfusion. However, the zoning system became known after Hartrampf's paper on the TRAM flap for breast reconstruction and took his name (Hartrampf zone of perfusion). As already described by Scheflan and Dinner, the flap is ideally divided in four zones, as follows. The abdomen midline divides the lower abdominal flap in two hemiabdominal flaps. These are ideally divided in two halves, thus resulting four zones, which are numbered from I to IV based on their perfusion and viability. Zone I is the most perfused zone being the one corresponding to the selected perforator. Zone IV is the most distant one and usually bad perfused and not viable. (figure 1) One year later Hartrampf's paper, Dinner's further investigation casted a shadow on the strictness of this zoning system as zone II and III should have to be switched. Twenty-three years later, Holm et al. confirmed Dinner's observation by decreeing that Hartrampf zone of perfusion II and III are reversed according to their fluorescent perfusion techniques. (figure 2).
It was only after the 3D and 4D CTA studies by Saint-Cyr et al., that the DIEP flap zones of perfusion were clarified. According to this study, zones of perfusion depend on the row position of the perforator harvested, as follows: - Flap based on a single medial row perforator shows a more centralized perfusion thus following the Hartrampf's classification of perfusion zones. However, both these theories are applied for a single dominant perforator. Depending on the perforator size and location, it is not uncommon that more than 1 perforator is harvested to improve DIEP flap perfusion. The perforasome concept is based on the fact that each perforator has its own vascular territory. It represents the "perforator" evolution of the Taylor's "anatomic angiosome".
Each perforasome is able to capture a variable number of adjacent perforasomes via direct and indirect linking vessels. This is what Taylor defines "clinical angiosome". Direct linking  vessels have large calibre and allow to capture adjacent perforasomes through an interperforasome flow mechanism. Indirect linking vessels are small calibre vessels , similar to the Taylor's choke vessels, allowing to capture adjacent perforasome through a recurrent flow mechanism. This normally takes place in the subdermal plexus.
In The vascular connection between the superficial vessels and both the medial and lateral row perforators of the same hemiabdomen are via indirect linking vessels in the subdermal plexus (recurrent flow).
In conclusion, when facing with the need of a large DIEP flap, a medial row perforator DIEP flap should be the choice. However, if the need is to transfer the whole lower abdominal skin and soft tissues (four zone DIEP flap) a double-pedicle (i.e perforator of the contralateral DIE or the SIEA/SIEV pedicle) is usually needed to increase the flap viable area.

Venous microvascular anatomy
The arterial anatomy of the lower abdominal skin and soft tissue has been widely described, and advances have been made with the modern concept of perforasome zones of perfusion.
On the other side, the venous microanatomy of the abdominal wall did not receive the same appraisal. In modern era of DIEP flap, the main vascular issues encountered are the venous drainage problems that can drive the flap from partial to complete necrosis. The venous drainage of the lower abdomen is provided by the superficial system belonging to SIEVs and the deep venous system belonging to DIEVs. Cadaver and in-vivo studies by Shaverien M et al. and Rozen WM et al. demonstrated the presence of small connecting veins (also called oscillating veins) between the superficial and the deep venous systems that usually diverts the subcutaneous venous flow from the superficial (SIEVs) to the deep veins (DIEVs) through the DIE perforator comitantes veins. In this case, the dominant perforator comitantes veins are often 1mm or bigger. On the other side, there could be also cases with prevalent venous drainage towards the superficial venous system, via SIEVs. A SIEV bigger than 1.5 mm at the inferior skin incision can be a pointer of this situation.
So far, the calibre of the selected perforator vein can be a limiting factor in DIEP flap drainage.
However, additional factors may be responsible for the lower abdomen soft tissue venous congestion: - The degree of communications between the superficial and deep system. The links between the superficial and the perforating system are not uniform and frequently via small calibre vessels, also called oscillating veins. These may limit the efficiency of the venous drainage. -Midline cross-over connections by the SIEVs. Each SIEV has been found to be a single trunk in the majority of the cases but sometimes can show a bifurcating or very rarely a trifurcating trunk below the umbilicus.
SIEV often supplies a medial branch that crosses the midline routinely at the arcuate line. Sometimes, there are additional cross-over just above and below the umbilicus. However, these midline cross-over connections can also be weak or even absent. These factors may also contribute to venous congestion.
In our centre, we usually study and evaluate the mid-line cross-over SIEV connections according to a grading scale where Grade I stands for absent connections at the midline, Grade II for weak connections, Grade III for good midline connection and Grade IV for good connections with at least one big size midline connection. (figure 6) In conclusion, when planning a four zone DIEP flap is paramount to predict and to evaluate that the flap has adequate arterial input and venous discharge. In four zone DIEP flap, a double-pedicle flap is what is normally needed to assure both good perfusion to all the four zones as well as efficient venous discharge. With reliable SIEA/SIEV, it is possible to raise a four zone lower abdominal flap on DIEP on one side and contralateral SIEA/SIEV or even based on bilateral SIEA/SIEV. In the latter, it is more appropriate to talk about a double I -II zone flap as each SIEA/SIEV flap sustains the corresponding hemiabdomen only.
There are few situations where an unipedicle DIEP flap with an additional venous anastomosis (one of the SIEVs) can be enough.
All this will be better explained in the next paragraphs.

Relevant applied vascular anatomy of the internal mammary vessels
The internal mammary vessels are widely used as recipient vessels in autologous tissue breast reconstruction. Their central location, reliability in terms of size and constancy,

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Breast Reconstruction -Current Techniques 184 freedom of flap insetting and the relatively resistance to atherosclerosis, preservation following radiation therapy and axillary surgery make them a natural choice as recipient vessel in breast reconstruction. Moreover, avoiding the use of thoracodorsal vessels as recipients, the latissumus dorsi (LD) flap is preserved as salvage option.
The internal mammary vessels are bilateral. On each side we can distinguish the internal mammary artery (IMA) and at least one internal mammary vein (IMV).

IMA
The internal mammary artery originates from the subclavian artery. Occasionally, it can have a common origin with the thyreocervical trunk, scapular artery, dorsal scapular artery, thyroid artery or costocervical trunk. It courses downward and medially joining the posterior surface of the first cartilaginous rib. It continues downward, ventral to the parietal pleura and on the posterior surfaces of the first six cartilaginous ribs being at the lateral sternal border. The distances between the IMA and the lateral sternal border is on average 15 mm, ranging from 6 to 24 mm. Starting from the third intercostal space, the IMA is found superficial to the trasversus thoracis muscle which separates the artery from the parietal pleura, making the dissection safer.
The IMA diameter varies at each intercostal space, being normally bigger proximally. Arnez et al. measures the IMA at the third, fourth and fifth intercostal spaces finding out an average diameter of 2.8, 2.6 and 2.6 mm, respectively. IMA tends to be larger on the right than the left side.
At the sixth intercostal space IMA normally splits in two trunks: the musculo-phrenic artery and the superior epigastric artery.
A combined radiologic and clinical study on 120 patients by Murray ACA et al. pointed out that in all patients both left and right IMA were always present and detectable both at ultrasound (US) and CTA. This study found out that in 99 % of the cases the IMA is a single trunk and in 1% of the case two trunks can be found. At the third intercostal space, where the IMV is normally split in two venous trunks, the IMA was found medial to the vein(s) in 22.5% of the cases, lateral to vein(s) in 6% of the cases and central positioned in 71.5% of the cases.
IMA shows anastomosis with the intercostal arteries of each space and gives off perforating branches at each intercostal space. However, a great variability has been described about IMA perforator calibre. The biggest IMA perforator is usually the one located at the second intercostal space followed by the ones at the third and first intercostal spaces with an average diameter of 1 mm, ranging from 0.5 to 2 mm. This makes the IMA perforator potential recipient vessels instead of the IMA itself, when the perforator has an acceptable calibre (more than 1 mm).
Besides all the positive aspects that makes the IMA the most favourite recipient vessel in breast reconstruction, there are rare cases where congenital anatomical variations, pathologic and iatrogenic phenomena can make the IMA not suitable as recipient vessel. This makes useful a preoperative radiologic assessment of IMA features by US or CTA. In our centre, we normally study the IMA preoperatively with color-doppler ultrasound (CDS).

IMV
Internal mammary veins originated from the confluence of the superior epigastric veins and the musculophrenic veins. This normally takes place at the sixth intercostal space. These veins are comitantes of the homonymous artery.
Generally, two IMVs accompany the IMA till the second/third intercostal spaces where the two venous trunks converge in an unique IMV. An anatomic study from Clark CP III et al showed that in 90 % of the cases, the IMV bifurcation takes place at the third rib on the left side and in 40% on the right side (in 60%of cases bifurcate downwards). This means that at the second intercostal spaces almost always a unique venous trunk is found on both right and left side. This place is the one we now prefer for the preparation of recipient vessels.
In literature, many authors choose the third intercostal space for recipient vessel preparation.
The IMV calibre varies at each intercostal space as the IMA calibre does. At the second intercostal space a vein about 3 mm is generally found. The same calibre is found only in 50 % of the cases at the third intercostal space, being generally not less than 2 mm till the fourth intercostal space. However, by progressing lower than the fourth intercostal space the vein calibre diminishes progressively till 1 mm or less, making the veins not consistent for a reliable anastomosis.
The physiologic IMV venous flow is toward the anonymous vein. The IMV is connected with intercostal and sternal veins at each intercostal space and gives off perforating vein at each intercostal space. From a rheologic point of view, this means that once the IMV is divided to be anastomosed to the flap pedicle, the proximal vein should be use because an anterograde flow is present but the distal vein may be not reliable because of valves that would limit the establishment of a retrograde flow.
The successful use of the distal limb of IMV as recipient vein in autologous breast reconstruction makes this logic assertion incorrect. Despite the presence of valve in the IMV, clinical experiences show that a retrograde flow takes place in the IMV distal limb, making it an important further recipient vein in breast reconstruction. This is especially useful when a second venous anastomosis is needed in autologous tissue reconstruction. Many theories has been advanced to explain the presence of a retrograde flow in the IMV despite the valves. Essentially, valves may be: -Not present at all. -Not present caudal to the venous anastomotic site. incompetent: the venous pressure proximal to the valve is higher than distally. This can force the valves making them incompetent. bypassed by collaterals: the rich connections between IMV and intercostals and sternal veins as well as the perforating branches of the IMV at each intercostal space can allow a bypass of the valvular system by these collaterals.
-Both incompetent and bypassed by collaterals.
The retrograde flow in the distal limb of the IMV can be explained as follows: - The IMV flow has been interrupted by the venous split and the corresponding decreased venous pressure gradient through the anonymous vein does not directly exist anymore for the IMV distal limb. -the corresponding deep superior epigastric vein has been ligated if a double-pedicle DIEP flap has been harvested, because the DIE has been harvested. This reduces the venous flow and pressure through the IMV distal limb. - The arterial input into the flap is responsible for the flap venous outflow and pressure. - The higher venous pressure gradient of the flap output on the remaining IMV distal limb venous afferents makes the direction of the venous flow reversed, thus a retrograde flow takes place.

Indications
Lower abdominal tissue nowadays represents the gold standard in breast autologous tissue reconstruction.
The four zones DIEAP flap identifies the case when the whole lower abdominal skin and soft tissue is harvested.
Regarding the recipient site in single breast reconstruction, the four zone DIEP flap has these general indications: -Need to reconstruct a large breast in patients with large contralateral breast that does not wish to reduce their breast size. Contraindications applied for standard DIEP and SIEA flaps are applied also to the four zone lower abdominal flap.

Flap markings
In the preoperative setting, abdominal mutidetector row computer tomography (MDCT) is very helpful to study the vascular architecture of the lower abdominal soft tissues in order to plan a reliable flap.
At our institution, all patients scheduled for lower abdominal flap breast reconstruction, undergo abdominal MDCT to investigate, localize and select "dominant" perforators. Care 187 is taken on: diameters of perforators and their branching into the subcutaneous layer, perforator's localization, intramuscular course, connection to the superficial epigastric veins (SIEV), DIEA branching pattern and superficial venous architecture. Fig. 7. Patient with a history of modified radical mastectomy, left axillary clearance and adjuvant radiation therapy. The patient developed a chest wall angiosarcoma. The skin resection needed is wider than the classic mastectomy pattern. When a four zone DIEP flap is needed for unilateral breast reconstruction, a double-pedicle DIEP flap is usually planned, as follows: when "true dominant" perforators are found on each hemiabdomen, the four zone flap will be raised based on these two perforators. The presence of a "dominant" lateral row perforator would be preferable in the double-pedicle four zone DIEP flap as better perfusion of the lateralmost part of the flap is expected. Moreover, dissection will be easier and faster than with the medial row perforators. -when one or multiple medium caliber perforators are found without the presence of a "true dominant" perforator, the best perforators are selected on each hemiabdomen. In this cases, more than one perforator for each hemiabdomen can be included in the flap, preferring to include perforators of the same row.
A four zone lower abdominal flap can be also raised on one DIE pedicle and one SIE pedicle. As a premise of the followings, it has to be remarked that we prefer to inset the flap after 180 degree rotation, in order to place the fattiest portion of the flap (i.e. the periumbelical one) to reconstruct the inferior quadrants. In the case of a flap raised on one DIE pedicle and one SIE pedicle, due to short pedicle of the superficial system (range 5 to 8 cm), it would be preferable to have the superficial pedicle on the ipsilateral side of the breast to reconstruct in order to avoid the need of further recipient vessel dissection than the internal mammary vessels (i.e. thoracodorsal vessels) and/or to use an artery and vein graft to allow anastomosis to the internal mammary vessels. Another option is to use the contralateral SIE pedicle anastomosed to the ipsilateral DIE pedicle (distal DIE stump or other row stump) with an intraflap anastomosis.
There are rare cases, when a four zone DIEP flap can be safely raised based on only one pedicle with additional SIEV supercharging in patients without mid-line abdominal scar. This is possible when a "true dominant" medial row perforator is present, a large caliber SIEV (more than 1.5 mm) is found along with good midline cross-over SIEV connections (grade III to IV).
The perforators identified by MDCT are then reported on the abdominal site, possibly with aid of CDS that further analyzes the caliber of perforators and flow velocity.
Markings begin on the abdominal area while the patient is in a supine position. The markings follows those of the standard abdominoplasty.

Double-pedicle DIEP flap harvest
The patient is placed in supine position with the arm of the side of affected breast elevated in order to expose the axilla (in immediate reconstruction) or the arms lying along the sides (in delayed reconstruction). The harvest of the flap begins by the dissection of the SIEV bilaterally. If a suitable SIEA is encountered on the ipsilateral side of the affected breast with a diameter of 1,5 mm at the level of the inferior skin incision, it can be dissected as well. The decision if the ipsilateral flap has to be raised on the SIE pedicle or on the DIEP pedicle depends on the characteristics of the dominant perforator/s. In case the dominant perforator/s caliber is bigger than 1,5mm at the preoperative MDCT, the choice shift toward the DIEP flap.
Harvesting the flap is done in standardized approach using perforators from both sides (or SIEA on one side). The DIE pedicle has to be dissected up to its entry into external iliac vessels to keep it as long as possible. The distal extent of DIE pedicle and the stump of the second row, when present, have to be dissected 1-2 centimeters futher to be ready for possible additional anastomoses.

Vascular construct
After dissection of both vascular systems on each side, consideration has to be given to the location and the dissection of the recipient vessels. Recipient vessels selection is highly influenced by the configuration that could provide the best orientation for flap positioning and inset.
Over the last thirty years the internal mammary vessels has become the gold-standard as recipients in autologous tissue breast reconstruction. Moreover, their diameter is favorable as it normally matches the one of the deep inferior epigastric artery and veins allowing an easier end-to-end anastomosis. However, other recipients site can be used. The most frequent alternative recipients to the internal mammary vessels are the thoracodorsal vessels. However, these vessels are laterally located and more prone to damage from previous axillary surgery and from radiation therapy. Furthermore, their use may preclude the possibility to rely on the LD flap as salvage option.
When raising the double-pedicle lower abdominal flap entails the need of simultaneous restoration of the blood supply of both pedicles. Various methods of reconstructing the blood supply of double-pedicle flaps have been reported.
The most common technique is to combine two different recipient vessels. Many anatomical solutions exist, the most popular one being internal mammary vessels, or its perforators when possible, and thoracodorsal vessels. In case they could not be both available, such as in some delayed reconstruction, other options are still possible: -Circumflex scapular vessels.
-Serratus branches -Thoracoacromial vessels. -Contralateral internal mammary vessels, with the drawback of an additional visible scar.
However, the split internal mammary vessels can be used to reconstruct both the arterial and venous flow of the double-pedicle flap. Since its first description almost ten years ago, we routinely use the inferior limb of the internal mammary artery and vein when an arterial and/or venous supercharging is needed.
Thus, there are two possibilities to reconstruct the vascular connection of the double-pedicle flap by using a single set of internal mammary vessels, as follows: -Double anastomoses to a single set of internal mammary vessels. DIE double anastomoses to both the superior and inferior limbs of the split internal mammary vessels, being with antegrade flow the superior limb anastomosis and with retrograde flow the inferior limb one (figure 9), as already described by Li S et al. and Xu H et al. This is also our preferred choice. Fig. 9. The two DIEP pedicle are anastomosed to a single set of internal mammary vessels. The black arrow points the contralateral DIEP pedicle anastomosed to the inferior limb of the internal mammary vessel. The blood flow is retrograde. The yellow arrow points the homolateral DIEP pedicle anastomosed to the superior limb of the internal mammary vessel. The blood flow is antegrade. - The "serial" intraflap anastomosis. Premising that the flap is 180 degree rotated, the contralateral DIE pedicle is anastomosed to the ipsilateral pedicle. The intraflap anastomosis may be performed on the abdomen while the flap is still perfused by the ipsilateral DIE pedicle, in order to reduce the ischaemia time. Moreover, this allows to check the patency of the intraflap anastomosis before completely dividing the DIE pedicle from the abdomen. This can be accomplished in an end-to-end fashion to the distal end of the ipsilateral DIE pedicle or to the other row stump of the DIE (if present).
One key point in harvesting double pedicle lower abdominal flaps is keeping the pedicles as long as possible to easily perform the additional anastomoses and to accommodate the pedicles according to these spatial configurations, thus avoiding subsequent stretching of the pedicles.

Flap inset
The flap is usually folded on one or both ends to create the most projecting point of the breast mound according with the contra lateral volume and shape of the breast.
Special attention has to be payed before the anastomoses to the spatial configuration of the pedicles in order to avoid kinking, twisting or their stretching. This is particularly true when the double DIE pedicle is anastomosed to both the superior and inferior limb of the internal mammary vessels.
DellaCroce FJ et al. extensively described another option for a full lower abdominal flap inset in single breast reconstruction with "stacked" DIEP flap. This is a layered combination in the recipient site of a two hemiabdominal free DIEP/SIEA flaps. Firstly, one hemiabdominal DIEP flap is deepithelialized and inset into the breast pocket, orienting its vascular pedicle for the anastomosis with the internal mammary vessels. Then, the second flap is inserted after performing the intraflap to the distal stump or other row stump of the first flap pedicle (DIEP or SIEA flaps).

Postoperative care and complications
Postoperative management of a four zone DIEP/SIEA flap are identical to that of a standard DIEP flap as well as the complications that could be experienced. Compared to a unipedicle DIEP flap, the likelihood of venous congestion are rarely experienced as we should think to double-pedicle flap as two I-II zones flaps. Consequentially, the rate of liponecrosis experienced in double-pedicle flaps is also faraway smaller than a unipedicle flap.

Acknowledgment
Thanks to Emiliano Visconti, M.D., Resident in-training, Department of Bioimages and Radiologic Sciences, University Hospital "A. Gemelli", Rome -Italy for its contribution in digital artworks.