Surgical augmentation of skin blood flow and viability in a pig musculocutaneous flap model

A porcine rectus abdominis musculocutaneous (TRAM) flap model was designed and validated in nine pigs. This TRAM flap was based on the deep inferior epigastric (DIE) vessels with an 8 x 18 cm transverse skin paddle at the superior end of the rectus abdominis muscle. The model was subsequently used to test our hypothesis of surgical augmentation of flap viability by vascular territory expansion. Specifically, we observed that ligation of the superior epigastric (SE) vessels at 4, 7, 14, and 28 days (N = 6 to 8) prior to raising the TRAM flaps significantly increased (p less than 0.05) the length and area of the viable skin in the transverse skin paddles of the treatment flaps compared with the contralateral shammanipulated control flaps. This significant increase in skin viability was seen to be accompanied by a significant increase (p less than 0.05) in skin and muscle capillary blood flow in the treatment TRAM flaps compared with the controls (N = 9). The mechanism of vascular territory expansion is unclear. We postulate that hypoxia resulting from the ligation of the superior epigastric vessels prior to the flap surgery may play a role in the triggering of the deep inferior epigastric artery to take over some of the territory previously perfused by the superior epigastric artery. This would then increase the skin and muscle capillary blood flow in the transverse paddle when the TRAM flap was raised on the deep inferior epigastric vascular pedicle.     

Intraoperative physiologic blood flow studies in the TRAM flap.

An intraoperative study was done to establish the functional and quantitative properties of the blood supply to the TRAM flap through the assessment and manipulation of blood flow through the deep epigastric arterial system. Seventeen patients undergoing unilateral postmastectomy breast reconstruction with lower transverse rectus abdominis myocutaneous (TRAM) flaps were studied. The study is divided into two parts: (1) ultrasonic measurement of blood flow in the deep inferior epigastric artery (DIEA), and (2) direct measurement of blood pressure in the deep epigastric arterial system, after division of the deep inferior epigastric artery. With occlusion of the superior epigastric artery at the level of the upper edge of the skin flap, 71 percent of the patients had a decrease in the blood flow through the deep inferior epigastric artery, with an average decrease of 23 percent. This implies that the area of watershed perfusion in the lower TRAM flap is superior to the umbilicus, and therefore, survival of all lower TRAM flap tissues requires reversal in the normal direction of arterial flow to the flap. The blood pressure in the proximal stump of the deep inferior epigastric arterial system averaged 46 percent of the mean systemic blood pressure. Occlusion of the medial and lateral thirds of the isolated rectus muscle decreased the mean arterial blood pressure in the flap an average of 19 percent in 80 percent of the individuals studied. These data support the technique of harvesting the entire rectus muscle, avoiding muscle-splitting maneuvers that may compromise axial blood flow.     

The vascular territories of the superior epigastric and the deep inferior epigastric systems

The vascular territories of the superior and the deep inferior epigastric arteries were investigated by dye injection, dissection, and barium radiographic studies. By these means it was established that the deep inferior epigastric artery was more significant than the superior epigastric artery in supplying the skin of the anterior abdominal wall. Segmental branches of the deep epigastric system pass upward and outward into the neurovascular plane of the lateral abdominal wall, where they anastomose with the terminal branches of the lower six intercostal arteries and the ascending branch of the deep circumflex iliac artery. The anastomoses consist of multiple narrow "choke" vessels. Similar connections are seen between the superior and the deep inferior epigastric arteries within the rectus abdominis muscle well above the level of the umbilicus. Many perforating arteries emerge through the anterior rectus sheath, but the highest concentration of major perforators is in the paraumbilical area. These vessels are terminal branches of the deep inferior epigastric artery. They feed into a subcutaneous vascular network that radiates from the umbilicus like the spokes of a wheel. Once again, choke connections exist with adjacent territories: inferiorly with the superficial inferior epigastric artery, inferolaterally with the superficial circumflex iliac artery, and superiorly with the superficial superior epigastric artery. The dominant connections, however, are superolaterally with the lateral cutaneous branches of the intercostal arteries. For breast reconstruction, it would appear that prior ligation of the deep inferior epigastric artery would be of advantage when elevating the lower abdominal skin on a superiorly based rectus abdominis musculocutaneous flap. The vascularity of this flap would be further increased by positioning some part of the skin paddle over the dense pack of large paraumbilical perforators. Based on these anatomic studies, the relative merits of the superior and deep inferior epigastric arteries with respect to local and distant tissue transfer using various elements of the abdominal wall are discussed in detail.     

Breast reconstruction with superficial inferior epigastric artery flaps: a prospective comparison with TRAM and DIEP flaps

Breast reconstruction using the lower abdominal free superficial inferior epigastric artery (SIEA) flap has the potential to virtually eliminate abdominal donor-site morbidity because the rectus abdominis fascia and muscle are not incised or excised. However, despite its advantages, the free SIEA flap for breast reconstruction is rarely used. A prospective study was conducted of the reliability and outcomes of the use of SIEA flaps for breast reconstruction compared with transverse rectus abdominis musculocutaneous (TRAM) and deep inferior epigastric perforator (DIEP) flaps. Breast reconstruction with an SIEA flap was attempted in 47 consecutive free autologous tissue breast reconstructions between August of 2001 and November of 2002. The average patient age was 49 years, and the average body mass index was 27 kg/m. The SIEA flap was used in 14 (30 percent) of these breast reconstructions in 12 patients. An SIEA flap was not used in the remaining 33 cases because the SIEA was absent or was deemed too small. The mean superficial inferior epigastric vessel pedicle length was approximately 7 cm. The internal mammary vessels were used as recipients in all SIEA flap cases so that the flap could be positioned sufficiently medially on the chest wall. The average hospital stay was significantly shorter for patients who underwent unilateral breast reconstruction with SIEA flaps than it was for those who underwent reconstruction with TRAM or DIEP flaps. Of the 47 free flaps, one SIEA flap was lost because of arterial thrombosis. Medium-size and large breasts were reconstructed with hemi-lower abdominal SIEA flaps, with aesthetic results similar to those obtained with TRAM and DIEP flaps. The free SIEA flap is an attractive option for autologous tissue breast reconstruction. Harvest of this flap does not injure the anterior rectus fascia or underlying rectus abdominis muscle. This can potentially eliminate abdominal donor-site complications such as bulge and hernia formation, and decrease weakness, discomfort, and hospital stay compared with TRAM and DIEP flaps. The disadvantages of an SIEA flap are a smaller pedicle diameter and shorter pedicle length than TRAM and DIEP flaps and the absence or inadequacy of an arterial pedicle in most patients. Nevertheless, in selected patients, the SIEA flap offers advantages over the TRAM and DIEP flaps for breast reconstruction.     

Immediate breast reconstruction: why the free TRAM over the conventional TRAM flap?

Use of the transverse rectus abdominis myocutaneous (TRAM) flap for immediate breast reconstruction is controversial because of fear of flap loss and concern that a high complication rate could interfere with adjuvant therapy. One common complication of the TRAM, partial flap necrosis, can interfere with both institution of postoperative therapy and evaluation for recurrence. In an attempt to minimize this problem, we began using the free TRAM flap based on the inferior deep epigastric vessels. This study compares our experience with conventional superior-pedicled (cTRAM) flaps and free TRAM (fTRAM) flaps. A total of 68 breasts were reconstructed in 63 patients, of which 48 of 68 (71 percent) were conventional TRAM flaps and 20 of 68 (29 percent) were free TRAM flaps. Of the 48 conventional TRAM flaps, 26 (54 percent) were unipedicled and 22 (46 percent) were bipedicled. There were 39 of 48 (81 percent) conventional TRAM flaps and 17 of 20 (85 percent) free TRAM flaps with T1 or T2 lesions. Node-positive patients occurred in 14 of 48 (29 percent) conventional TRAM flaps and 2 of 20 (10 percent) free TRAM flaps. One-fourth of patients in both groups smoked cigarettes. Twenty-one of 48 patients (44 percent) with conventional TRAM flaps required postoperative chemotherapy, and 6 of 21 (29 percent) were delayed because of complications of the TRAM flap. Of the 7 of 20 (35 percent) free TRAM flap patients who required post-operative chemotherapy, only 1 of 7 (14 percent) was delayed because of TRAM flap complications.(ABSTRACT TRUNCATED AT 250 WORDS)     

Augmentation of transmidline skin perfusion and viability in transverse rectus abdominis myocutaneous (TRAM) flaps in the pig.

The aim of this experiment was to design a clinically relevant TRAM flap in the pig and to use this flap model to study the effectiveness of preoperative ligation of the dominant vascular pedicle in augmentation of muscle and skin capillary blood flow and skin viability in the TRAM flap. This TRAM flap model was based on the deep inferior epigastric vascular pedicle, with the center of the transverse skin paddle attached to the underlying rectus abdominis muscle at the superior end of the muscle and extending bilaterally from its attached muscle. The transverse skin paddle (8 x 30 cm) included a contralateral and ipsilateral random portion of skin. This flap model was based on the deep inferior epigastric rather than the superior epigastric vascular pedicle because the deep inferior epigastric vascular pedicle is the smaller of the two in the pig and augmentation of its blood supply by ligation of the dominant superior epigastric vascular pedicle resembles more closely the clinical situation. It was observed that ligation of the dominant superior epigastric vascular pedicle 14 days prior to raising the TRAM flap significantly (p less than 0.05; n = 5) increased the total muscle and skin capillary blood flow and skin viability in the transverse skin paddle compared with the sham-operated control (n = 5).(ABSTRACT TRUNCATED AT 250 WORDS)     

Venous congestion and blood flow in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps

A series of 240 deep inferior epigastric perforator (DIEP) flaps and 271 free transverse rectus abdominis myocutaneous (TRAM) flaps from two institutions was reviewed to determine the incidence of diffuse venous insufficiency that threatened flap survival and required a microvascular anastomosis to drain the superficial inferior epigastric vein. This problem occurred in five DIEP flaps and did not occur in any of the free TRAM flaps. In each of these cases, the presence of a superficial inferior epigastric vein that was larger than usual was noted. It is therefore suggested that if an unusually large superficial inferior epigastric vein is noted when a DIEP flap is elevated, the vein should be preserved for possible use in flap salvage. Anatomical studies with Microfil injections of the superficial venous system of the DIEP or TRAM flap were also performed in 15 cadaver and 3 abdominoplasty specimens to help determine why venous circulation (and flap survival) in zone IV of the flaps is so variable. Large lateral branches crossing the midline were found in only 18 percent of cases, whereas 45 percent had indirect connections through a deeper network of smaller veins and 36 percent had no demonstrable crossing branches at all. This absence of crossing branches in many patients may explain why survival of the zone IV portion of such flaps is so variable and unpredictable.     

Basic fibroblast growth factor expression following surgical delay of rat transverse rectus abdominis myocutaneous flaps

Partial transverse rectus abdominis myocutaneous (TRAM) flap loss in breast reconstruction can be a devastating complication for both patient and surgeon. Surgical delay of the TRAM flap has been shown to improve flap viability and has been advocated in "high-risk" patients seeking autogenous breast reconstruction. Despite extensive clinical evidence of the effectiveness of surgical delay of TRAM flaps, the mechanisms by which the delay phenomenon occurs remain poorly understood. To examine whether angiogenic growth factors such as basic fibroblast growth factor (bFGF) may play a role in the delay phenomenon, the authors studied the expression of bFGF in rat TRAM flaps subjected to surgical delay. Thirty-five female Sprague-Dawley rats were randomly assigned to one of four TRAM flap groups: no delay (n = 6), 7-day delay (n = 12), 14-day delay (n = 10), or 21-day delay (n = 7). Surgical delay consisted of incising skin around the perimeter of the planned 2.5 x 5.0-cm TRAM flap followed by ablation of both superior epigastric arteries and the left inferior epigastric artery, thus preserving the right inferior epigastric artery (the nondominant blood supply to the rectus abdominis muscle of the rat). TRAM flaps were then elevated after 7, 14, and 21 days of delay by raising zones II, III, and IV off the abdominal wall fascia. Once hemostasis was assured, the flaps were sutured back in place. All flaps were designed with the upper border of the flap 1 cm below the xiphoid tip. Three days after the TRAM procedure, postfluorescein planimetry was used to determine percent area viability of both superficial and deep portions of TRAM flaps. All rats were euthanized and full-thickness TRAM specimens were taken from zones I, II, III, and IV for enzyme-linked immunoabsorbent assay analysis of bFGF levels. Statistical testing was done by t test (percent viability) and two-way analysis of variance (bFGF levels). All delayed flaps had significantly higher bFGF levels when compared with all nondelayed control flaps (p < 0.05). The bFGF levels were not different in the rats that received TRAM flaps 7, 14, or 21 days after delay surgery. There was also no significant difference in bFGF levels among zones I through IV. Control rats had more peripheral zone necrosis compared with all delayed TRAM rats. All delayed flaps had a significantly higher area of flap viability superficially than nondelayed control flaps (p < 0.05). There was no difference in deep flap viability. Surgical delay of rat TRAM flaps is associated with improved flap viability and significantly elevated levels of bFGF over nondelayed TRAM flaps at postoperative day 3 after TRAM surgery. The increases in bFGF noted at this time point suggests that bFGF may play a role in the improved TRAM flap viability observed after delay surgery. Further investigation is needed to evaluate the role bFGF may play in the delay phenomenon.     

Ex vivo intraoperative angiography for rectus abdominis musculocutaneous free flaps

In this study, the vascular architecture of rectus abdominis free flaps nourished by deep inferior epigastric vessels was investigated using an ex vivo intraoperative angiogram. Oblique rectus abdominis free flaps were elevated and isolated from the donor site. In 11 patients, the vascular architecture of these flaps was analyzed before the flap was thinned. Radiographic study identified an average of 2.1 large deep inferior epigastric arterial perforators in each flap. In nine of the 11 flaps, the axial artery was visible. In four flaps, the axial artery originated from the perforator of the lateral branch of the deep inferior epigastric artery; in five others, it originated from the medial branch. In each flap, the angle of the axial perforator from its anterior rectus sheath in the vertical plane was measured; its mean was 50.6 degrees. All flaps survived, although three showed partial necrosis in the distal portions. In two of these three flaps, the axial artery was not visible in the angiograms, and the third revealed a one-sided distribution of axial flap arteries. Using ex vivo intraoperative angiography, the architecture of the individual flap, its axial perforator, and its connecting axial flap vessel could be investigated. This information can help the surgeon safely thin and separate the flap.     

Investigation of TRAM flap oxygenation and perfusion by near-infrared reflection spectroscopy and color-coded duplex sonography

Near-infrared reflection spectroscopy, used experimentally for investigation of tissue hemoglobin content and oxygenation in various flaps, was tested in the pedicled transverse rectus abdominis musculocutaneous (TRAM) flap, chosen as a simple clinical model because of its well-known vascular anatomy and clinical relevance. The study intended to answer the following questions: Does the near-infrared reflection spectroscopy system used in this study measure tissue hemoglobin content and oxygenation in the superficial skin layers only, as proposed by the manufacturer? Is near-infrared reflection spectroscopy able to detect differences of tissue hemoglobin content and oxygenation in distinct zones of the TRAM flap skin before, early, and late after surgery? Does tissue hemoglobin content and oxygenation correspond to blood flow in the supplying superior epigastric artery and to clinical signs of TRAM flap perfusion and viability? In 11 patients, tissue hemoglobin content and oxygenation in the lower abdomen/TRAM flap, mastectomy skin flap, and contralateral breast were measured by a new near-infrared reflection spectroscopy system preoperatively, early postoperatively, and late postoperatively. Simultaneously, systolic peak flow in the ipsilateral superior epigastric artery was obtained by color-coded duplex sonography. Routine clinical monitoring was performed throughout the early postoperative period. Tissue hemoglobin content and oxygenation in the lower abdomen, mastectomy skin flap, and contralateral breast were similar before surgery but varied considerably between different patients. There were no significant differences among preoperative, early postoperative, and late postoperative values of tissue hemoglobin content and oxygenation in the mastectomy skin flap and contralateral breast. However, near-infrared reflection spectroscopy measurements of the TRAM flap revealed significant differences between preoperative and early postoperative values of tissue hemoglobin content and oxygenation and among zones I, II, and III early after surgery. Tissue hemoglobin content in the TRAM flap skin increased and oxygenation decreased early after surgery. Near-infrared reflection spectroscopy values corresponded to clinical signs of venous congestion predominantly in zone III. Late postoperative return of hemoglobin content and oxygenation in the TRAM flap toward preoperative values can be attributed to improved venous return by reversed flow across regurgitant valves and development of collateral circulation. Finally, there was a significant increase of systolic peak flow in the ipsilateral superior epigastric artery early after surgery. This could be related to the opening of small-caliber choke arteries between the superior and deep inferior epigastric arteries following ligation of the dominant deep inferior epigastric artery and TRAM flap transfer to the chest. Systolic peak flow returned to preoperative values late after surgery. The near-infrared reflection spectroscopy system used in this study appeared to measure hemoglobin content and oxygenation in the superficial skin layers only. Near-infrared reflection spectroscopy was able to detect differences of tissue hemoglobin content and oxygenation in the TRAM flap between preoperative and postoperative measurements and between distinct zones of the TRAM flap early postoperatively. Postoperative changes in near-infrared reflection spectroscopy values corresponded to clinical observations and blood flow in the superior epigastric artery measured by color-coded duplex sonography. Further experience is needed before near-infrared reflection spectroscopy can be advocated for routine clinical flap monitoring.     

The relative importance of the deep and superficial vascular systems for delay of the transverse rectus abdominis musculocutaneous flap as demonstrated in a rat model

The use of some form of delay maneuver for "high-risk" patients before transfer of the superior pedicled lower transverse rectus abdominis musculocutaneous (TRAM) flap for breast reconstruction has augmented the rate of success in both the experimental and clinical arenas. A common method of vascular delay has been the bilateral division of both the superficial inferior epigastric and deep inferior epigastric vessels. Whether all of these must be divided to adequately effect the delay is unknown. For that matter, the relative importance of the superficial versus the deep vascular systems is unclear. To investigate this uncertainty, a delay was attempted in 61 Sprague-Dawley rats by division of either the superficial inferior epigastric or deep cranial epigastric vessels (the latter is the homologue to the human deep inferior epigastric) in unilateral or bilateral fashion. Division of the contralateral superficial inferior epigastric vessel resulted in significantly greater TRAM flap survival than either ipsilateral or bilateral superficial inferior epigastric vessel division (p = 0.0034 or p = 0.0093, respectively). Division of the ipsilateral or bilateral deep cranial epigastric vessel resulted in significantly greater flap survival than just contralateral deep cranial epigastric vessel division (p = 0.0034 or p = 0.006, respectively). No significant difference was observed between the group having contralateral superficial inferior epigastric or groups with ipsilateral deep cranial epigastric division, implying that either alone would be efficacious to achieve the desired delay effect. This would allow the other vascular system to be retained intact for later potential salvage maneuvers as needed.     

Contour abnormalities of the abdomen after breast reconstruction with abdominal flaps: the role of muscle preservation.

The purpose of the present study was to determine whether contour abnormalities of the abdomen after breast reconstruction with abdominal flaps are related to the harvest of the rectus abdominis muscle. Abdominal contour was analyzed in 155 women who had breast reconstruction with abdominal flaps; 108 women had free transverse rectus abdominis muscle (TRAM) flaps, 37 had pedicled TRAM flaps, and 10 had deep inferior epigastric perforator (DIEP) flaps. The reconstruction was unilateral in 110 women and bilateral in 45 women. Three methods of muscle-sparing were used; they are classified as preservation of the lateral muscle, preservation of the medial and lateral muscle, or preservation of the entire muscle. One of these three methods of muscle-sparing was used in 91 women (59 percent) and no muscle-sparing was used in 64 women (41 percent). Postoperative contour abnormalities occurred in 15 woman and included epigastric fullness in five, upper bulge in three, and lower bulge in 10. One woman experienced two abnormalities, one woman experienced three, and no woman developed a hernia. Of these abnormalities, 11 occurred after the free TRAM flap, seven after the pedicled TRAM flap, and none after the DIEP flap. Bilateral reconstruction resulted in 11 abnormalities in nine women, and unilateral reconstruction resulted in seven abnormalities in six women. chi2 analysis of the free and pedicled TRAM flaps demonstrates that muscle-sparing explains the observed differences in upper bulge and upper fullness (p = 0.02), with a trend toward significance for lower bulge (p = 0.06). chi2 analysis of the free TRAM and DIEP flaps does not explain the observed difference in abnormal abdominal contour. Analysis of muscle-sparing and non-muscle-sparing methods demonstrates that the observed difference between the techniques is only explained for a lower bulge after the bilateral free TRAM flap (p = 0.04).     

Breast Reconstruction with the free TRAM or DIEP flap: patient selection,choice of flap,and outcome

Recent reports of breast reconstruction with the deep inferior epigastric perforator (DIEP) flap indicate increased fat necrosis and venous congestion as compared with the free transverse rectus abdominis muscle (TRAM) flap. Although the benefits of the DIEP flap regarding the abdominal wall are well documented, its reconstructive advantage remains uncertain. The main objective of this study was to address selection criteria for the free TRAM and DIEP flaps on the basis of patient characteristics and vascular anatomy of the flap that might minimize flap morbidity. A total of 163 free TRAM or DIEP flap breast reconstructions were performed on 135 women between 1997 and 2000. Four levels of muscle sparing related to the rectus abdominis muscle were used. The free TRAM flap was performed on 118 women, of whom 93 were unilateral and 25 were bilateral, totaling 143 flaps. The DIEP flap procedure was performed on 17 women, of whom 14 were unilateral and three were bilateral, totaling 20 flaps. Morbidities related to the 143 free TRAM flaps included return to the operating room for 11 flaps (7.7 percent), total necrosis in five flaps (3.5 percent), mild fat necrosis in 14 flaps (9.8 percent), mild venous congestion in two flaps (1.4 percent), and lower abdominal bulge in eight women (6.8 percent). Partial flap necrosis did not occur. Morbidities related to the 20 DIEP flaps included return to the operating room for three flaps (15 percent), total necrosis in one flap (5 percent), and mild fat necrosis in two flaps (10 percent). Partial flap necrosis, venous congestion, and a lower abdominal bulge were not observed. Selection of the free TRAM or DIEP flap should be made on the basis of patient weight, quantity of abdominal fat, and breast volume requirement, and on the number, caliber, and location of the perforating vessels. Occurrence of venous congestion and total flap loss in the free TRAM and DIEP flaps appears to be independent of the patient age, weight, degree of muscle sparing, and tobacco use. The occurrence of fat necrosis is related to patient weight (p < 0.001) but not related to patient age or preservation of the rectus abdominis muscle. The ability to perform a sit-up is related to patient weight (p < 0.001) and patient age (p < 0.001) but not related to preservation of the muscle or intercostal nerves. The incidence of lower abdominal bulge is reduced after DIEP flap reconstruction (p < 0.001). The DIEP flap can be an excellent option for properly selected women.     

Comparison of TRAM and DIEP flap physiology in a rat model

Dynamic and physiologic studies objectively comparing the attributes of the transverse rectus abdominis musculocutaneous (TRAM) and deep inferior epigastric perforator (DIEP) flaps would be most practical in an animal model. This has now been accomplished using the ventral abdomen of the Sprague-Dawley rat. A conventional TRAM flap, a multiple perforator DIEP flap, and a solitary perforator DIEP flap were raised in three equal groups of five rats each. Flow studies using laser Doppler flowmetry demonstrated the highest flow in zone I in the TRAM flap group (87.6 +/- 15.4 percent), which was a statistically significant difference from the multiple perforator DIEP flap group (45.4 +/- 13.3 percent) and the solitary perforator DIEP flap group (43.4 +/- 26.4 percent) (p = 0.005). Flow in zone IV was proportionately lower for all groups, with no significant difference noted between TRAM and DIEP flaps (p = 0.736). Although ultimate flap survival was greatest for the TRAM flap group (96.1 +/- 6.7 percent) when compared with the multiple perforator DIEP flap (79.8 +/- 15.2 percent) or the solitary perforator DIEP flap groups (77.1 +/- 23.0 percent), this difference was not statistically significant (p = 0.183). In summary, relative flow to these rat ventral abdomen models was directly proportional to the number of retained musculocutaneous perforators, but a single perforator only could routinely allow near-total survival.     

Venous interruption is unnecessary to achieve an adequate delay in the rat TRAM flap model

Staged division of any or all inferior dominant pedicles to the human lower transverse rectus abdominis musculocutaneous (TRAM) flap has previously been attempted to invoke the delay phenomenon to enhance the rate of success with the superior-pedicled version, especially for patients at high risk for complications. Regardless of the specific vessels ligated, this has usually been accomplished by division of the source artery and its accompanying vein. Whether division of both vessels is essential remains unclear, however. This issue was investigated by using the authors' standard rat TRAM flap model in 43 female Sprague-Dawley rats, which were randomly assigned to four groups. In group A, both the predominant ipsilateral cranial epigastric artery and the cranial epigastric vein were divided 2 weeks before elevation of the TRAM flap. In group B, only the artery was divided; in group C, only the vein was divided. In an undelayed control group, the TRAM flap was elevated immediately, with no prior pedicle division. The percentages of flap survival in group A (89.3 +/- 7.0 percent) and group B (88.8 +/- 6.5 percent) (both with division of the predominant artery) were significantly greater than that in the control group (64.6 +/- 20.5 percent) (p < 0.001) or that in the group in which the vein alone was divided (73.9 +/- 11.3 percent) (p < 0.01). There was no significant difference between the group that underwent vein division only and the control group (p = 0.102). The clinical implication is that arterial division is critical for TRAM flap delay and that arbitrary venous interruption is unnecessary.     

The delay phenomenon: the story unfolds

Our previous studies have shown that when a flap is delayed, there is dilation of existing vessels within the flap not ingrowth of new vessels. The maximal anatomic effect on the arterial tree occurs at the level of the reduced-caliber "choke" anastomotic vessels that link adjacent vascular territories. To further investigate the sequence of anatomic changes that occurs during the delay phenomenon, a large series of 200 rabbits and 17 dogs underwent a flap delay procedure in either skin or muscle and the tissues were examined at postoperative periods between 1 hour and 1 year by using well-established fluorescein, angiographic, light microscopic, immunohistochemical, and electron microscopic techniques. These data in the rabbit skin consistently demonstrated an initial period of vasoconstriction that resolved within 3 hours postoperatively and was followed by an active and progressive dilation of choke vessels that was most dramatic between 48 and 72 hours. In vivo intravenous fluorescein dye testing revealed an interesting parallel in that there was a temporary barrier to the flow of fluorescein that occurred at the level of the choke vessels immediately after the flap was raised and that this temporary barrier-continued to impede the flow toward the flap tip in rabbits where flaps had been delayed for periods up to 72 hours. Thereafter, there was no obstruction to the flow of fluorescein along the flap. During this early delay period of 3 days, light microscopy revealed a decrease in vessel wall thickness associated with an increase in lumen diameter. Over the next 4 days, the luminal diameter continued to dilate to a lesser extent and the vessel wall thickened. Immunohistochemical analysis showed increased cell division, maximal between 24 and 72 hours, in all layers of the choke vessel wall. During this same postoperative interval, transmission electron microscopy revealed phenotypic changes in smooth muscle cells from contractile to synthetic cells. Hypertrophy of the smooth muscle cells was also observed. The vascular endothelium, which initially showed evidence of denudation, was restored to a healthy intact appearance within the first week after delay. When followed for longer periods, long-term studies of the delayed flap of up to 1 year demonstrated dramatically a permanent dilation of the choke vessel lumen and a thickening of the choke vessel wall. In canine studies, one rectus abdominis muscle was delayed by ligating the deep inferior epigastric artery. The time sequence of choke vessel dilation, studied by sequential angiograms in vivo, was comparable to that of the rabbit skin model. To ascertain the permanence and irreversibility of this dilation, the normal circulation of the delayed rectus abdominis muscle was restored by reanastomosing the deep inferior epigastric artery. Even after a recovery period of up to 3 months, the choke vessels remained dilated and tortuous instead of reverting to their original narrow diameters. From this work, it is suggested that the choke vessel dilation seen in the delay period is a permanent and irreversible event. It is an active process associated with both an increase (hyperplasia) and an enlargement (hypertrophy) of the cells in all layers of the choke artery wall and a resultant increase in caliber of these vessels. The time sequence for delay appears to be similar in different species and in different tissues, suggesting the possibility of a universal process for delay.     

Clinical results of TRAM flap delay by selective embolization of the deep inferior epigastric arteries

Preoperative selective embolization of the deep inferior epigastric arteries constitutes a new technique in TRAM flap delay. Whereas surgical ligation of these vessels has proved to be an effective delay procedure in experimental and clinical settings, it requires an additional operative step under general anesthesia. Despite the introduction of the free TRAM leading to improved flap perfusion, this microsurgical technique is not always available because of the requirements of specialized equipment and staff, longer operating hours, and subsequently higher expenses. The search for a minimally invasive, easy, and inexpensive technique to improve perfusion of the pedicled TRAM flap led us to selective embolization of the deep inferior epigastric arteries by an angiographic procedure. After 4 years of experience with this technique, we now present the first clinical results. Breast reconstruction by a delayed pedicled TRAM flap was performed in 40 patients with a mean age of 48.4 years (range, 31 to 66 years). The mean interval between embolization and surgery was 3.6 months. Postoperative data concerning flap survival and complications were available for all patients. Embolization of the deep inferior epigastric arteries was performed bilaterally in 35 patients (87.5 percent) and unilaterally in 5 patients (12.5 percent). Radiotherapy had been applied in 21 patients (52.5 percent) before surgery. Postoperative flap complications consisted of partial necrosis in three (7.5 percent), fat necrosis in one (2.5 percent), impaired wound healing in five (12.5 percent), and postoperative bleeding in two patients (5 percent). Abdominal wound healing complications occurred in six patients (15 percent), abdominal wall weakness in eight (20 percent), and hernia formation in four (10 percent). Surgical corrections were performed at the breast (TRAM flap) in 22 patients (55 percent) and at the abdomen (donor site) in 9 (22.5 percent). Preoperative selective embolization of the deep inferior epigastric arteries constitutes an alternative delay procedure for the pedicled TRAM flap. It is superior to the conventional procedure without delay, offers several advantages compared with surgical ligation of these vessels, and represents an alternative to the free TRAM flap in selected cases.     

Comparison of cost for DIEP and free TRAM flap breast reconstructions

A recent article by Kaplan and Allen suggested that deep inferior epigastric perforator (DIEP) flap breast reconstruction was less expensive than reconstruction performed with free transverse rectus abdominis musculocutaneous (TRAM) flaps. To test that hypothesis, a series of patients who had undergone unilateral breast-mound reconstruction by the first author using DIEP or free TRAM flaps between November 1, 1996, and March 30, 2000, were reviewed. Bilateral reconstructions and reconstructions performed by other surgeons in the department were excluded to eliminate all variables except the choice of flap. All hours in the operating room and days in the hospital until discharge were included. Early readmissions for the treatment of complications were included, as were the costs of the mastectomy in the case of immediate reconstructions, but late revisions and nipple reconstructions were not. The totals were then converted into resource costs in 1999 dollars, and the DIEP and free TRAM flap groups compared. There were 21 DIEP flaps and 24 free TRAM flaps in the series. In this series, there was no significant difference between the cost of DIEP and free TRAM flap breast reconstruction.     

Breast reconstruction with the DIEP flap or the muscle-sparing (MS-2) free TRAM flap: is there a difference?

The advantages of breast reconstruction using the deep inferior epigastric perforator (DIEP) flap and the muscle-sparing free transverse rectus abdominis musculocutaneous (TRAM) flap (MS-2) are well recognized. Both techniques optimize abdominal function by maintaining the vascularity, innervation, and continuity of the rectus abdominis muscle. The purpose of this study was to compare these two methods of breast reconstruction and determine whether there is a difference in outcome. The study considered 177 women who have had breast reconstruction using muscle-sparing flaps over a 4-year period. This includes 89 women who had an MS-2 free TRAM flap procedure, of which 65 were unilateral and 24 were bilateral, and 88 women who had a DIEP flap procedure, of which 66 were unilateral and 22 were bilateral. The total number of flaps was 223. Mean follow-up was 23 months (range, 3 to 49 months). For all MS-2 free TRAM flaps (n = 113), outcome included fat necrosis in eight (7.1 percent), venous congestion in three (2.7 percent), and total necrosis in two (1.8 percent). For the women who had an MS-2 free TRAM flap, an abdominal bulge occurred in three women (4.6 percent) after unilateral reconstruction and in five women (21 percent) after bilateral reconstruction. The ability to perform sit-ups was noted in 63 women (97 percent) after unilateral reconstruction and 20 women (83 percent) after bilateral reconstruction. For all DIEP flaps (n = 110), outcome included fat necrosis in seven (6.4 percent), venous congestion in five (4.5 percent), and total necrosis in three (2.7 percent) patients. For the women who had DIEP flap reconstruction, an abdominal bulge occurred in one woman (1.5 percent) after unilateral reconstruction and in one woman (4.5 percent) after bilateral reconstruction. The ability to perform sit-ups was noted in all women after unilateral reconstruction and in 21 women (95 percent) after bilateral reconstruction. These results demonstrate that there are no significant differences in fat necrosis, venous congestion, or flap necrosis after DIEP or MS-2 free TRAM flap reconstruction. The percentage of women who are able to perform sit-ups and the percentage of women who did not develop a postoperative abdominal bulge is increased after DIEP flap reconstruction; however, this difference is not statistically significant.     

Fat necrosis in free transverse rectus abdominis myocutaneous and deep inferior epigastric perforator flaps

A series of 310 breasts reconstructed by a single surgeon using free transverse rectus abdominis myocutaneous (TRAM) and deep inferior epigastric perforator (DIEP) flaps was reviewed to see if there were any differences in the incidence of fat necrosis and/or partial flap loss between the two techniques. During the study period, 279 breasts were reconstructed with free TRAM flaps and 31 breasts were reconstructed with DIEP flaps. In the breasts reconstructed with free TRAM flaps, the incidence of partial flap loss was 2.2 percent and the incidence of fat necrosis was 12.9 percent. The DIEP flaps were divided into two groups. For the first eight flaps, patients were selected using the same criteria normally used to choose patients for free TRAM flaps. In this unselected early group, the incidence of partial flap loss was 37.5 percent and the incidence of fat necrosis was 62.5 percent. Because of the high incidence of partial flap loss and fat necrosis in the first eight flaps, subsequent selection was modified to limit the use of DIEP flaps to patients who had at least one sufficiently large perforator in each flap (a palpable pulse and a vein at least 1 mm in diameter) and who did not require more than 70 percent of the flap to create a breast of adequate size. In this later (selected) group, fat necrosis (17.4 percent) and partial flap loss (8.7 percent) were reduced to a level only moderately higher than that found in the free TRAM flap group. From these data, it can be concluded that the incidence of partial flap loss and fat necrosis is higher in DIEP flaps than in free TRAM flaps, probably because the blood flow to the former flap is less robust. This difficulty can be circumvented to some extent, however, by careful patient selection. Factors that should be considered include tobacco use, size of the perforators (especially the vein), and (in unilateral reconstructions) the amount of flap tissue across the midline needed to create an adequately sized breast. If these factors are properly considered when planning the operation, fat necrosis and partial flap loss can be reduced to an acceptable level. For selected patients, the DIEP flap is an excellent technique that can obtain a successful, autologous tissue breast reconstruction with minimal donor-site morbidity. For patients who are not good candidates for reconstruction with this flap, the free TRAM flap remains a good alternative.