The mean temperature of all zones together taken at 3-minute recovery decreased from day 1 to day 6. This difference was only statistically significant between day 1 and day 6 (Fig. 5).
This study shows that free abdominal flap breast reconstruction using IMV causes considerable changes in abdominal skin perfusion during the first postoperative week. These changes in skin perfusion are best explained using Huger’s vascular zones and the angiosome theory.11 , 12 It is important to realize that although the anatomic landmarks for the division of the abdomen in Huger’s zones have not changed, closure as in an abdominoplasty results in an inferior-medial advancement of skin and subcutaneous tissue into Huger’s zones I and II.
The qualitative results of this study showed a dynamic change in the pattern of hot spots after surgery. The patterns of hot spots on the IR images of the abdominal skin have been previously described.9 , 10 Heat radiation from the skin is registered with the IR camera with a higher IR emission at the hot spots. These hot spots are associated with locations where perforators, transporting warm blood to the skin, are connecting with the subdermal plexus. Studies on the use of DIRT in the planning of perforator flaps have shown that bright hot spots are associated with arterial Doppler sounds and clearly visible perforators on computed tomography angiography (CTA).10 , 13 Chubb et al.10 showed how DIRT also can be used to identify the robustness of interconnections between perforators.
The IR images at the end of surgery showed that hot spots had disappeared in zones I and II but also in subzone IVA caudal to the reconstructed breast. Closure after flap harvest proceeds as in an abdominoplasty and includes undermining in zones I and II, and most perforators in these zones are severed and, as a result, do not produce hot spots. The zones I and II become hypoperfused compared with the preoperative DIRT and the reference zone III. This explanation cannot be used for the disappearance of hot spots in the area beneath the reconstructed breast (zone IVA).
Skin perfusion in the submammary area is normally not affected by an abdominoplasty as shown by Mayr et al.14 using intraoperative indocyaninegreen videoangiography. However, in contrast to a formal abdominoplasty, in free abdominal flap breast reconstruction using IMV, the internal mammary artery (IMA) angiosome is involved. Ingvaldsen et al.15 studied the microcirculatory abdominal skin circulation after DIEP breast reconstruction using laser Doppler perfusion imaging, but they did not evaluate the effect of the IMV on abdominal skin perfusion. A plausible explanation for the changes in zone IVA may be found in the angiosome theory.12 The IMA has its own angiosome and divides at the sixth intercostal space into the superior epigastric artery (SEA) and musculophrenic artery (MPA).16 , 17 In free abdominal flap breast reconstruction, the IMA is transected at the third or fourth intercostal space. As a result, blood perfusion to the IMA angiosome distal to this level and also to the angiosomes of the SEA and MPA becomes drastically reduced. Perforators no longer transport blood to the skin and, as a result, hot spots disappear and the zone becomes hypoperfused. The hypoperfusion at the end of surgery was most pronounced in the infraumbilical region of Huger’s zone II and in subzone IVA.
Interestingly, hot spots reappeared in zones I and II and subzone IVA during the postoperative period. This may again be explained using the angiosome theory. In zones III and IV, the angiosomes of the intercostal, subcostal, and lumbar arteries lie adjacent to the angiosomes of zones I and II, which are the angiosomes of the paired internal mammary-epigastric systems and the angiosomes of the superficial inferior epigastric and iliac circumflex arteries. Because of undermining of the abdominoplasty flap, perforators of the angiosomes incorporated in zones I and II are no longer perfused by their source vessels but depend for their perfusion on the source vessels of adjacent angiosomes. This situation is comparable to that seen in the delay phenomenon of flaps. Dhar and Taylor18 reported on the anatomic changes that occur at the level of the reduced-caliber choke vessels between adjacent vascular territories of a pedicled flap. The results from their animal study on the delay phenomenon showed an initial vasoconstriction, which lasted for up to 3 hours. Between 3 and 24 hours, the choke vessels returned to a diameter comparable to the control and, thereafter, underwent progressive sequential dilation that was most dramatic between 48 and 72 hours. Other studies support these findings.19 , 20 With the opening of choke vessels, the adjacent angiosomes become reperfused. Our results show a reappearance of hot spots in the angiosomes incorporated in Huger’s vascular zones I and II and subzone IVA during the postoperative period. Further support for the reperfusion of zones I and II and subzone IVA from the adjacent angiosomes can be found in the change in direction of the rewarming pattern seen with DIRT. The intercostal, subcostal, and lumbar arteries follow the nerves and their dermatomes. These dermatomes have a nearly transverse course. In an abdominoplasty, closure of the skin defect results in skin advancement in an inferior-medial direction. The direction in the postoperative rewarming pattern seen with DIRT changed compared with the preoperative DIRT. Postoperatively, rewarming started laterally and proceeded inferiorly and medially.
This dynamic process of reperfusion with reappearances of hot spots in angiosomes was also seen in a DIRT study on the postoperative reperfusion of deep inferior epigastric artery (DIEA) and superficial inferior epigastric artery (SIEA) flaps.21
The number of hot spots in zone III and subzone IVB did not change. However, hot spots in these zones showed a more rapid rewarming at the end of surgery and the first postoperative day creating a state of hyperemia compared with the preoperative DIRT. This hyperemia subsided during the following days.
The quantitative analysis showed that the mean temperature difference between zones III and IV was significant for days 1, 3, and 6, whereas the difference between zones III and II was only significant for days 1 and 3 (Fig. 6). The mean temperature of all zones combined indicated a hyperemia on day 1, which disappeared during the following days. Although the hyperemia in zone III decreased, zone II showed an increase in mean skin temperature during the postoperative period (Fig. 4). We anticipate that the changes in hyperemia are a result of a redistribution of blood flow after an increase in the diameter of choke vessel lumen in the subcutaneous tissue and skin.
The change in skin perfusion in zone II, particularly the hypoperfusion during the first 3 postsurgical days, is an interesting finding. Wound break down usually occurs in zone II near the center of the suture line and was seen in 2 of our patients.1–3 Although tension at the suture line after wound closure can be responsible for hypoperfusion, it is also reasonable to assume that it is caused by delayed adequate reperfusion due to the long distances to the adjacent angiosomes. The IMA angiosome on the side the IMV are harvested does not contribute to the reperfusion of zone II. In addition, the transverse incision line prevents vascular territories in the suprapubic area to contribute to the reperfusion of zone II across the suture line. The area of hypoperfusion corresponds also with the area of hyposensitivity on the abdomen after DIEP breast reconstruction as described by Tindholdt et al. and Visconti et al. which is in agreement with the finding of Taylor and Palmer that blood vessels are accompanied by nerves.12 , 22 , 23
In unilateral DIEP breast reconstruction, one can select either an ipsilateral or a contralateral pedicle. Skin reperfusion of the abdominoplasty flap relies on the reperfusion of the involved zones from adjacent lateral zones and on the IMV vessels that are not used as recipient vessels as there is no blood supply coming from both deep inferior epigastric arteries. In such, we anticipate that an ipsilateral and a contralateral pedicle will have the same impact on abdominal skin perfusion. However, in bilateral DIEP breast reconstruction, one could speculate that the risk for abdominal wound problems increases as reperfusion of the abdominoplasty flap relies then mainly on adjacent lateral angiosomes as the IMV and DIEA on both sides have been used. Johnson et al.24 reported abdominal wall necrosis after harvest of both IMAs and deep inferior epigastric arteries.
The changes seen in skin perfusion may also reflect what has occurred with the blood supply to the rectus abdominis muscle. This muscle has a type III pattern of circulation according to the classification of Mathes and Nahai and has the DIEA and SEA as its dominant pedicles for blood supply, whereas the subcostal and six or seven intercostal arteries are minor pedicles.25 Harvesting the IMV and deep inferior epigastric vessels on the same side in DIEP and ms-TRAM flap breast reconstruction reduces the blood supply to this muscle and its overlying fascia layer drastically. We postulate that abdominal wall bulging or hernia formation after DIEP and ms-TRAM flap breast reconstruction is a result of impaired wound healing at the fascia layer because of the loss of its dominant blood supply when using an ipsilateral pedicle. In bilateral DIEP breast reconstructions, in which both DIEAs and IMAs are used, Vyas et al. reported a significant risk for hernia and bulge formation and also other abdominal complications.26
In DIEP breast reconstructions, donor-site morbidity may be reduced by using the thoracodorsal vessels as recipient vessels or using an IMA preserving approach by doing end-to-side anastomosis or anastomosing to a perforator of the IMV. Such would preserve the perfusion of zone IVA.
The limitation of this prospective and clinical perfusion study is the use of a method that provides only indirect information on skin perfusion. Based on the results of other studies, providing scientific support for the use of skin temperature to measure skin perfusion, reliable information was obtained on dynamic changes that occurred in abdominal skin perfusion after free abdominal flap breast reconstruction using IMV as recipient vessels.4–7 , 27–29
This study provides for the first time scientific information on the impact free abdominal flap breast reconstruction using IMV has on abdominal skin perfusion. DIRT showed in vivo the reperfusion of the abdominoplasty flap over time as a dynamic process, quite similar to that seen in flap delay.
The authors wish to thank Mr. Knut Steinnes at the Department of Medical Physiology, Faculty of Health Sciences, University of Tromsø, for his assistance in drawing the figures.
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