Eur J Plast Surg (1996) 19:289-292 European ~ ' ~ 1 ~1 Q

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Viability of the vertical rectus abdominis musculocutaneous flap in the rat following prior internal mammary artery ligation

G.G. Hallock

Division of Plastic Surgery, The Lehigh Valley Hospital, Allentown, Pennsylvania, USA

Abstract. A large abdominal skin flap nourished superi- orly by a single rectus abdominis muscle has well known advantages for providing vascularized tissue coverage of thoracic defects. Unfortunately, if both internal mamma- ry arteries have previously been violated, as is increas- ingly common today following coronary artery revascu- larization, initial consideration of this flap would seem to be contraindicated. Nevertheless, anecdotal examples of clinical survival of the rectus abdominis muscle flap in this situation exist. This laboratory study was initiated to ascertain whether a musculocutaneous flap could also be expected to survive. Using a Sprague-Dawley rat model, identical bilateral vertical rectus abdominis mus- culocutaneous (VRAM) flaps were designed. The inter- nal thoracic [sic. mammary] vessels supplying one mus- cle had been divided two weeks previously just above the costal margin, as frequently encountered in the clini- cal situation. Mean survival of control flaps (intact inter- nal thoracic) was 85.5_+5.9% versus 67.9_+35.3% for the delayed flap that relied on collateral circulation for any viability. Although no statistical difference per se existed between these groups (p=0.32), the great variability in surviving portions of those flaps dependent only on available collaterals suggests extreme caution before as- suming that any abdominal skin flap based on a rectus abdominis muscle without an intact internal mammary source vessel would be reliable.

Key words: Rectus abdominis musculocutaneous flap - Internal mammary

Recalcitrant thoracic and especially lower third median sternotomy wound often are best treated using the rectus abdominis muscle as a vascularized flap [1]. More ex- tensive defects may be more reliably obliterated if the

Presented in part at the Tenth Annual Meeting, Northeastern Soci- ety of Plastic and Reconstructive Surgeons, Pittsburgh, September 11, 1993.

Correspondence to: G. Hallock, 1230 South Cedar Crest Boule- vard, Suite 306, Allentown, Pennsylvania 18103, USA

overlying skin is included as via a vertical rectus abdo- minis musculocutaneous (VRAM) flap which sometimes obviates the need for multiple flaps in critically ill pa- tients [2, 3].

Unfortunately, one or both internal mammary arteries are ever more commonly utilized for coronary artery re- vascularization, or a subcostal incision from prior chole- cystectomy may be present which still is not unusual in older age groups. Under these circumstances, selection of the rectus abdominis muscle would seem to be contra- indicated [4, 5], and strong consideration of other sec- ond tier alternatives such as the omentum has been advo- cated despite the inherent morbidity of the requisite lap- arotomy [1].

To circumvent such potential risks due to this dil- emna, a few courageous attempts have previously suc- ceeded in demonstrating that the rectus abdominis mus- cle as a superior-based local rotation flap can still sur- vive through collateral circulation, especially via the eighth posterior intercostal artery, even though both in- ternal mammary arteries had previously been divided [5-7]. Total rectus abdominis muscle viability after sur- gical disruption of the internal mammary vessels was then proven feasible in a dog model [4]. To date, surviv- al of a composite rectus abdominis musculocutaneous flap under similar conditions has not been verified ex- perimentally in any model; although a single clinical ex- ample of an upper transverse rectus abdominis musculo- cutaneous flap without an intact superior epigastric ar- tery has been reported by serendipity to have successful- ly closed a chest wall defect [6]. Without laboratory evi- dence of the safety of such a maneuver, however, unre- quited enthusiasm for use of a rectus abdominis muscu- locutaneous flap must be tempered. This has now been attempted using a rat VRAM flap model.

Method

Previously we demonstrated in the rat the consistent presence of musculocutaneous perforators from the cranial [sic: superior] epi- gastric vessels that course through the rectus abdominis muscle to

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Fig. 1, Lead oxide carotid injection study of the anterior torso of the rat. The internal thoracic artery (black arrows) runs parallel to the edge of the sternum. Just above the costal margin this termi- nates as the cranial epigastric artery (white arrows), continuing lateral to the xiphoid to enter the rectus abdominis muscle. Note numerous intercostal, diaphragmatic, and cross-over branches that intercommunicate to form a dense system of collateral circulation for the thoracic region

Fig. 2. Skin boundaries of the proposed bilateral vertical rectus abdominis musculocutaneous (VRAM) flaps just below the out-

line of the xiphoid and costal margin. The left side for each rat served as its own control (C), Note the healed incision over the right fifth intercostal space through which the internal thoracic vessels had been divided 2 weeks previously in this rat from group 1

Fig. 3. Elevation of each musculocutaneous flap ceased at the xi- phoid level (X), and laterally preserved inflow from all collateral vessels beneath the costal margin

penetrate the anterior rectus sheath and supply the overlying in- tegument [8]. Just as in the human, an ipsilateral vertical skin pad- dle encompassing these perforators can be expected to remain to- tally viable. Also as in the human, the cranial epigastric vessels represent the terminus of the internal thoracic [sic: mammary] vessels, which enter the muscle just lateral to the xiphoid after ex- iting from underneath the costal margin [6, 8, 9]. The internal tho- racic artery arises from the subclavian to run caudoventrally to ap- proach the sternum near the second intercostal space [10, 11]. Thereafter, these paired vessels run in parallel tracks staying very close to the lateral margin of the sternum just above the parietal pleura of the thoracic cavity. This preliminary knowledge was confirmed by our anatomical dissections and carotid lead oxide injection studies rats using the method of Taylor [12] in 10 adult male Sprague-Dawley rats (Fig. 1).

Based on this anatomical information, 2 additional groups of 5 adult male sprague-Dawley rats each ranging in weight from 300-400 grams were anaesthetized in our standard fashion using an enflurane induction and intramuscular injection of ketamine and acetylpromazine according to the protocols of our institution- al animal care committee. An incision was made in the first group at the level of the right fifth intercostal space and in the second group one interspace above the costal margin to identify the inter- nal thoracic bundle just lateral to the sternum, which was then di- vided with electrocautery carefully preserving the underlying pari- etal pleura to avoid a tension pneumothorax. The skin incision was closed and the rat returned to an individual cage for recovery with food and water provided ad libitum.

Simulating the usual time lag prior to clinical consultation and intervention in the human, 2 weeks later a second operation was performed on each rat. Again under anaesthesia, just distal to the xiphoid a 4 cm wide by 6 cm long rectangle was drawn, centered about the midline (Fig. 2). The perimeter and midline were then incised down to the abdominal musculature, to create two smaller but identical vertically oriented rectangles. All rectus abdominis perforators to each rectangle were preserved. The linea alba and lateral rectus sheaths were incised entering the peritoneal cavity, and the insertion of each rectus abdominis muscle transected at the pubis so that these 2 musculocutaneous flaps remained at- tached only superiorly by the muscle and its cranial epigastric vascular pedicle (Fig. 3). Any superior dissection of the rectus ab- dominis muscle ceased at the level of the xiphoid medially, and laterally just below the costal margin to intentionally preserve all intercostal vessels and collaterals.

The abdominal wall was reclosed beneath both flaps. A sili- cone sheet was placed underneath them to prevent neovasculariza- tion that could inappropriately augment skin survival. Both flaps were then inset in their original position, and again each rat was returned to its independent cage for further maintainence.

48 h after this second procedure, the rats were reanaesthetized and the flaps inspected. All viable surface area for each flap was outlined on clear X-ray film as had been done after the original in- setting. Any difference in film weight served as a measure of the percentage of flap survival. The left VRAM flap for each animal served as its own control.

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minor necrosis occurred in each of these flaps except for total necrosis in one (Fig. 5). This great variability prob- ably was a result of anatomical variations in collaterals as well as possible differences in surgical dissection in spite of the protocol outlined.

Fig. 4. Total survival of both control (C) or collateral-nourished VRAM flaps as noted 48 h after flap elevation when right internal mammary vessel had been previously divided at the fifth intercos- tal space (group 1 rat)

Fig. 5. In this case, virtual total survival of control (C) VRAM flap was present, but collateral-nourished flap was obviously to- tally necrotic. Arrow points to incision used for prior ligation of right internal mammary vessels one interspace above the costal margin (group 2 rat)

Results

Lead oxide studies of the arteries of the anterior torso of the rat were remarkably similar to that found by Taylor in the human [13]. The internal thoracic artery skirted the edge of the sternum (Fig. 1). Following its inferior course, branches were given off at each anterior inter- costal space. Close to the insertion of the diaphragm, its terminus as the musculophrenic and cranial epigastric arteries occurred with numerous interconnections as not- ed. The cranial epigastric artery just lateral to the xi- phoid entered the respective rectus abdominis muscle from which eventually the musculocutaneous perforators to the abdominal skin arose. On the chest wall, from a lateral origin the posterior intercostal vessels communi- cated with their anterior counterparts. Multiple sternal and diaphragmatic branches were also noted to cross the midline and interconnect all major vessels.

In the group of rats with the internal thoracic vessels divided at the right fifth intercostal space, all such "de- layed" VRAM flaps as well as the control flaps totally survived (Fig. 4). This is completely understandable due to the excellant available collaterals via the numerous in- tercostal spaces before reaching the xiphoid. However, the second group better simulated the typical dissection of the internal mammary artery by the cardiothoracic surgeon often approaching the costal margin. This ma- neuver should reduce the number of collateral vessels. Mean survival percentage by area was 85.5+5.9% for control flaps with no skin necrosis noted in any rat (skin contraction accounted for the difference from expected 100%). This compared to "delayed" flaps with mean survival of 67.9+35.3%. Unlike the control flaps, some

Discussion

Although traditionally the skin circulation in "loose- skinned" animals has been considered to be dominated by axial cutaneous vessels, a supplemental and often in- dependent source via musculocutaneous perforators also occurs as characterized by the rat rectus abdominis mus- culocutaneous flap [14-16]. The rat provides a simple model for investigation of the nuances especially for the rectus abdominis flap due to its low acquisition price, minimal maintainence requirements, and is readily avail- able in most microsurgical training laboratories [17]. Nevertheless, any conclusions must be tempered by ac- knowledging some deficiencies including the fact that unlike the dog or human, the superior source of inflow via the cranial epigastric is the dominant pedicle to the rat rectus abdominis muscle [8, 18]. The caudal epigas- tric vessel, if it exists, is usually vestigial [18].

In the human, the survival of a superior-based rectus abdominis muscle flap in spite of prior division of the internal mammary artery is postulated to be due to a "diffuse intrathoracic collateral network involving the internal mammary system, with multiple branches and intercommunications on the same side, as well as across the midline... [6]." Ligation of the internal mammary vessels on one side initiates the delay phenomenon, whereby according to Taylor choke anastomoses be- tween vascular territories become larger, or even true anastomoses to enhance this phenomenon [13]. Since by comparative anatomy the deep plane of circulation is re- markably similar in the rat as in the human [18], this same reasoning can explain survival of major portions of our "delayed" VRAM flaps in the rat in spite of prior di- vision of the corresponding internal thoracic vessels. However, as in the human, the extent of collateralization and ability to perfuse skin perforators can be variable. Therefore, as shown with at least the rat VRAM flap, no guarantee can be made for absolute or total survival of the composite portion of a rectus abdominis muscle flap following prior ipsilateral internal mammary artery liga- tion. Extrapolation to the clinical situation is inferred.

Acknowledgements. David C. Rice, B.S., Director, and Lisa M. Hill, from the Dorothy Rider Pool Microsurgery and Laser Labo- ratory, Allentown, Pennsylvania, assisted with the animal studies. Thomas E. Wasser, MEd, Biostatistician, The Lehigh Valley Hos- pital, Allentown, Pennsylvania, provided the pertinant statistical analysis.

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G.G. Hallock