Superficial lateral sural artery free flap for intraoral reconstruction: Anatomic study and clinical implications

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ORIGINAL ARTICLE Superficial lateral sural artery free flap for intraoral reconstruction: Anatomic study and clinical implications Klaus-Dietrich Wolff, MD, DDS, PhD, 1 Florian Bauer, MD, DDS, 1 Sebastian Kunz, MD, 2 David Andrew Mitchell, MB, FDS, FRCS, 3 Marco Rainer Kesting, MD, DDS, PhD 1 * 1 Department for Oral and Maxillofacial Surgery, Klinikum Rechts der Isar, Technische Universit at, Munich, Germany, 2 Institute for Forensic Medicine, Ludwig-Maximilian- University, Munich, Germany, 3 Oral and Facial Specialties Department, Pinderfields General Hospital, Wakefield, United Kingdom. Accepted 27 June 2011 Published online 22 October 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.21885 ABSTRACT: Background. A posterolateral calf free flap is anatomically assessed and its usefulness for intraoral reconstruction is described. Methods. Records of 42 cadaver dissections including anatomic parameters of the superficial lateral sural artery serving as pedicle were analyzed. Data of 20 patients with primary oral cancer who underwent reconstructions with posterolateral calf free flaps are presented. Results. The superficial lateral sural artery was present in 36 of 42 of all cadavers (85.8%). In all, 25 specimens of 36 were suitable as flaps (69.4%). It originated from the lateral sural and the popliteal artery (31% vs 69%). It was accompanied by 1 vein (40.5%) or 2 veins (59.5%). The artery pierced the crural fascia on average 3 cm lateral to the midline and 0 to 12 cm below the fibular head. Eight patients had inadequate superficial lateral sural vessels and were reconstructed by peroneal perforator flaps. One flap was lost. Conclusions. Cutaneous flaps from the posterolateral calf can be a useful alternative for reconstruction of moderate sized defects with minimal donor site morbidity. VC 2011 Wiley Periodicals, Inc. Head Neck 34: 1218 1224, 2012 KEY WORDS: head and neck oncology, posterolateral calf, donor site morbidity, free flap, intraoral defect cover Thin and pliable skin flaps for oral reconstruction are frequently raised from the forearm but can also be obtained from other regions, for example the anterolateral thigh. Despite their advantages such as familiar anatomy with long and high caliber vessels, donor site morbidity can occur at the forearm, or the flaps may need thinning when taken from the thigh, upper arm, or trunk. Therefore, donor sites for thin skin flaps that can be closed directly and are less exposed than the forearm are sought particularly for intraoral reconstructions. Although the texture, thickness, and accessibility of the skin of the lower leg are similar to those of the forearm, until now this donor area has failed to achieve widespread use for intraoral defect cover. One reason for this is the fact that the harvesting of free skin flaps such as the dorsalis pedis-, peroneal-, tibialis anterior, and -posterior flaps are associated with the sacrifice of a main lower leg artery, and that the anatomy of the cutaneous perforators is highly variable in the lower leg. 1 4 With increasing knowledge of the vascular anatomy and improved instruments, the techniques devised to harvest perforator flaps allow the transfer of these flaps on their terminal branches to the skin, leaving the source vessels intact. These flaps provide thin and pliable skin similar to the *Corresponding author: M. R. Kesting, Department for Oral and Maxillofacial Surgery, Klinikum Rechts der Isar, Technische Universit at, Munich, Germany. E-mail: kesting@mkg.med.tum.de forearm with low donor site morbidity. One of the earliest flaps described from the lower leg is the sural flap, which is supplied by either medial, lateral, or median superficial arteries, originating from the popliteal artery or deep sural vessels. 5 7 To gain the popularity of this thin, medium sized free skin flap, an investigation was made to assess the anatomy and the reliability of the superficial lateral sural vessels to serve as a free flap pedicle. We also developed a safe and straightforward strategy for skin flap elevation at the posterolateral calf, which can be applied even if no suitable superficial sural vessels are found. Finally, we evaluated the usefulness of this donor site for transferring free flaps to the oral cavity in a series of 20 consecutive patients. Anatomic study To evaluate the anatomy of the superficial lateral sural artery, 42 legs in 21 cadavers were investigated. After marking the flexion crease of the knee joint, the midline of the calf, the posterior intermuscular septum, and the fibular head, a skin incision was made starting from the midpoint of the popliteal fossa toward the posterior intermuscular septum. The dissection was carried out at the level above the fascia, and the superficial lateral sural artery was exposed. The vessel was followed to its origin in the popliteal fossa, and the point where it pierced the crural fascia was documented. The pedicle length was defined as the distance from this point to the source 1218 HEAD & NECK DOI 10.1002/HED SEPTEMBER 2012

SUPERFICIAL LATERAL SURAL FLAP FOR INTRAORAL RECONSTRUCTION TABLE 1. Patients and reconstructions. Patient/age, y/sex Defect Flap size, cm Pedicle/length, cm SLSA pedicle Complications 1 / 51 / M FOM 7 4 SLSA / 10 VAN None 2 / 60 / M FOM 6 4 SLSA / 7.5 VVAN None 3/53/M P 8 5 SLSA / 6 VA None 4 / 44 / M FOM/T 7 5 PP / 6 A too small None 5/67/M T 7 4 SLSA / 7 VAN None 6/48/F C 9 5 SLSA / 7 VVAN None 7 / 50 / F FOM 5 3.5 PP / 5.5 V too small None 8/53/F T 6 4 PP / 7 No A None 9 / 61 / M FOM 5 4.5 SLSA / 8 VVAN V revised 10 / 61 / M T 6 4 PP / 6.5 A too small None 11 / 45 / F FOM 4 3 SLSA / 7 VVAN Failed 12 / 69 / M FOM/T 7 5 SLSA / 6.5 VA None 13 / 64 / F P 6 5 PP / 8.5 Spasm of A None 14 / 60 / M T 7 4.5 SLSA / 7 VAN Infection 15 / 55 / M T 4 4 SLSA / 6 VVAN None 16 / 46 / M FOM 6 4 PP / 6 A too small None 17 / 68 / M FOM/T 7.5 4.5 SLSA / 7.5 VVAN None 18 / 42 / M BM 4.5 4 PP / 8.5 No A None 19 / 69 / M FOM 4 3 SLSA / 6 VAN None 20 / 50 / M BM 5.5 4 PP / 10 V too small None Abbreviations: SLSA, superficial lateral sural artery; FOM, floor of mouth; A, artery; V, vein; N, nerve; T, tongue; P, palate; PP peroneal perforator; BM, buccal mucosa, C, cheek skin; M, male; F, female. vessel. Structures around the artery such as the comitant veins, the small saphenous vein, and the lateral sural nerve were assessed. The outer diameter of the artery was measured at its origin, and a distinction was made between sizable arteries with a diameter of 1 mm or more and smaller vessels. Finally, the proximal posterior intermuscular septum was explored for the presence of a peroneal perforator. No further dissection took place. PATIENTS AND METHODS From July 2009 to November 2010, harvesting of flaps at the posterolateral aspect of the upper calf was performed in 20 patients (Table 1). All patients but 1 had T1 or T2 classification squamous cell carcinoma of the oral cavity, located at the floor of the mouth, tongue, buccal mucosa, or palate. In 1 patient, the flap was placed into a defect at the cheek following skin cancer resection. There were 15 men and 5 women with a mean age of 55.8 years (range, 42 69 years). Ipsilateral supraomohyoid neck dissection was carried out in all patients with preservation of the superior thyroid, lingual, and facial arteries. For venous anastomoses, the retromandibular vein or its side branches were dissected and preserved. In patients needing resections wider than 5 cm or patients who had mandibular resection, other flaps were used for reconstruction. Only patients with primary tumors in whom no neck dissection had been performed previously were included. All patients underwent either a CT angiography scan or an MRI of the lower leg to visualize the morphology and the course of the main vessels. Additionally, the origin of the superficial lateral sural artery was located. As a preoperative measure, the posterior intermuscular septum was auscultated along its upper half with an audible Doppler, and a proximal peroneal perforator was marked as a back-up vessel in case no suitable superficial lateral sural vessels were found intraoperatively. Flap harvest The leg was bent at the knee joint and brought into a prone position to get optimal access to the lateral and posterior aspect of the calf. No tourniquet was used to allow for assessment of the vessels strength and pulse. The posterior intermuscular septum as well as the midpoint of the popliteal fossa were palpated and marked. Beginning at the popliteal fossa, the skin was incised in the distolateral direction, ending at the posterior intermuscular septum. The crural fascia was left intact. With suprafascial blunt dissection, the superficial lateral sural artery and its concomitant structures were exposed. The vessel was then followed into the popliteal fossa after opening the fascia. To decide whether the vessels were suitable to serve as a vascular pedicle, their diameter and the pulse of the artery were assessed. The vessels were considered to be reliable if the artery had a diameter of at least 1 mm, showing a clearly visible, strong pulse. Furthermore, a vein with a diameter similar to that of the artery had to be present. If this was the case, the raising of a lateral sural flap was continued, and the skin island was circumscribed along the axis of the vascular pedicle including the crural fascia, but without any muscular tissue. The pedicle was clipped close to the source vessels; in 2 cases, a short segment of the deep lateral sural artery and vein was included to enlarge the vessel caliber. If the lateral sural nerve was in close proximity to the vessels it was left untouched to prevent mechanical trauma to the delicate vessels, thereby including it into the pedicle. To allow for primary closure, all flaps were elevated at the proximal half of the lower leg, and the flap width never exceeded 5 cm. If either the superficial lateral sural artery or vein were not felt to be reliable, the skin incision was continued along the intermuscular septum, and a proximal peroneal perforator was identified using the preoperative Doppler mapping as a guide. The perforator was exposed by HEAD & NECK DOI 10.1002/HED SEPTEMBER 2012 1219

WOLFF ET AL. reflecting the fascia, and the peroneal muscles were retracted anteriorly, so that the lateral margin of the fibula could be palpated. The posterior intermuscular septum was incised around the perforator without any direct manipulation of this vessel. The pedicle was followed by retrograde intramuscular dissection until the peroneal vessels were reached, leaving a small cuff of the soleus muscle at both sides. Pedicle length and diameter were increased by continuing dissection to the peroneal artery and vein when necessary. An elliptical skin island was created, having a vertical axis along the posterior septum and with the perforator in its center. For microvascular transfer, the pedicle was clipped directly at its origin from the peroneal vessels, which were left intact. After drain insertion, wound closure was achieved by wide undermining in the suprafascial plane. RESULTS In the anatomic dissections, the superficial lateral sural artery was present in 36 of the 42 legs (85.5%), but 11 had calibers <1 mm and were considered potentially unreliable for microvascular transfer. In 25 legs, 2 veins were found (59.5%), the larger having a caliber comparable to that of the artery. In 11 cases (40.5%), only 1 vein with a slightly larger caliber up to 1.5 mm was present (Figure 1). The vessels ascended through the fatty tissue of the popliteal fossa in a distolateral direction, passed superficial to the lateral belly of the gastrocnemius muscle, and reached the crural fascia at the level of the fibular head or up to 12 cm distal to it. In all but 3 cadavers, the artery was accompanied by the lateral sural nerve. The short saphenous vein could be found medial to the vascular pedicle, having a distance to the superficial lateral sural artery of 3.5 to 5 cm. The superficial lateral sural artery originated from the lateral sural artery in 31% of legs, and directly from the popliteal artery in 69%. The artery perforated the crural fascia 0 to 12 cm below the fibular head, mostly between 2 and 6 cm distally, and 3 cm medial to the midline in average (Figure 2). The distance between this point and the origin of the artery from the source vessel ranged from 6 to 14 cm, leading to a pedicle length of 8 cm on average. A single FIGURE 1. Superficial lateral sural vessels with flap including crural fascia. A single large comitant vein is present. [Color figure can be viewed in the online issue, which is available at FIGURE 2. Results of the anatomic dissections. Note: The points indicate the perforation of the crural fascia by the superficial lateral sural artery. perforator was present, running along the posterior intermuscular septum a distance of 3 to 10 cm below the fibular head in 31 of the 42 lower legs. In 11 specimens, 2 perforators were found. The perforator was regularly accompanied by 2 veins and always originated from the peroneal artery (Figure 3). A fine anastomotic network could be seen between this perforator and the superficial lateral sural artery in 30 specimens (Figure 4). Of the 20 patients undergoing operation, a suitable superficial lateral sural artery and vein was found in 12 patients, whereas in 8 patients, no suitable vascular pedicle was present. Despite careful and meticulous dissection, no superficial lateral sural artery could be seen in 2 patients, and in 5 patients, either the artery 3 or the vein 2 was too small for a safe anastomosis. In another patient, spasm of the artery developed after exposure, and we felt this could be unreliable. As a back-up procedure, in these patients the incision was continued along the intermuscular septum and a soleus perforator flap was raised instead, using a proximal peroneal perforator as the pedicle (Table 1). If suitable superficial lateral sural vessels were found, flap rising could be performed quickly and easily. The skin island was circumscribed along the axis of the vascular pedicle including the crural fascia, and a thin flap was developed subfascially above the gastrocnemius muscle (Figures 5 and 6). To prevent damage or mechanical trauma to the vessels, no separation of the lateral sural nerve from the vessels was performed, and the nerve was included into the pedicle (Figures 7 and 8). In 2 cases, a short segment of the deep lateral sural artery and vein was included, thereby enlarging the vessel caliber. Flap size ranged from 4 cm 3cmto9cm 5 cm, being 4 cm 6 cm on average, and all donor site defects could be closed primarily. The pedicle length ranged from 6 to 10 cm in the superficial lateral sural flaps (average, 7.1 cm) and from 5.5 to 10 cm in the soleus perforator flaps (average, 7.2 cm). In 1 patient, both pedicles were reaching the skin paddle, and the superficial lateral sural 1220 HEAD & NECK DOI 10.1002/HED SEPTEMBER 2012

SUPERFICIAL LATERAL SURAL FLAP FOR INTRAORAL RECONSTRUCTION FIGURE 5. Three-month postoperative result showing reconstruction of the anterolateral floor of the mouth (case 1). [Color figure can be viewed in the online issue, which is available at FIGURE 3. Anatomic dissection of the superficial lateral sural and peroneal pedicle, both providing blood supply to the skin of the posterolateral calf. [Color figure can be viewed in the online issue, which is available at vessels were selected due to their ease of dissection. Anastomoses were performed either end to end to branches of the superior thyroid, lingual, or facial artery or, directly to these vessels, using end to side technique. Despite the limited pedicle length, tension to the vessels could be avoided in all cases. The flaps were thin and pliable and fit well into the surgical defects of the oral cavity, leading to satisfying functional results. All patients were immediately able to speak intelligibly. Drinking and eating a soft diet caused no problems. One flap showed signs of arterial occlusion and could not be salvaged FIGURE 4. Anastomotic network between superficial lateral sural artery and peroneal perforator. [Color figure can be viewed in the online issue, which is available at FIGURE 6. Donor site appearance after 3 months (case 1). [Color figure can be viewed in the online issue, which is available at HEAD & NECK DOI 10.1002/HED SEPTEMBER 2012 1221

WOLFF ET AL. FIGURE 7. Thin flap after harvest (case 6). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary. com.] despite early revision. In another patient, the venous anastomosis was revised successfully; and 1 flap developed marginal wound dehiscence, but finally healed without further surgical measures. After superficial lateral sural flap harvest, 4 of the 12 patients recognized reduced sensibility around the lateral ankle, but no patients complained about any functional restrictions. The appearance of the donor scar was very well tolerated, and the donor site morbidity was considered very low by all patients. There was no contour deficit. During the follow-up of 18 months, none of the patients needed secondary flap thinning. DISCUSSION As described by Manchot, 8 the skin of the posterior calf is nourished by superficial sural arteries, which can be found at the medial, lateral, and median region and are derived from the deep medial or lateral sural arteries or directly from the popliteal artery. Taylor and Daniel 5 were the first to suggest the possibility of flap harvest at the posterior calf, using the superficial medial sural artery as the pedicle. To demonstrate their reliability, the superficial sural arteries have already been a subject of anatomic investigations. One of the first studies was performed in 22 cadavers by Haertsch, 9 who described a dominant median artery, called the saphenous artery, and other cutaneous branches from the popliteal artery. These results were confirmed by Cormack and Lamberty 6 who also stated, that among the 3 superficial sural arteries, the median vessel is dominant and therefore should be used for raising of cutaneous flaps. Fachinelli et al 10 reported their results in 60 cadaveric dissections. They showed that the superficial lateral sural artery ran along the sural nerve in 75% of their specimens, originating from the popliteal artery in 65%, 20% from the medial, and in 8% from the lateral sural artery. In this study, the diameter of the superficial lateral sural artery was found to be 0.5 mm on average, whereas the superficial median artery had a diameter of 1 mm. In a recent study by Shimizu et al 11 superficial median and lateral sural arteries with diameters of 0.8 to 2.7 mm (median) and 0.4 to 2.5 mm (lateral) were found in 12 formalin- fixed legs, but in 3 specimens, no suitable superficial system was present at all. Walton et al 7,12 dissected 11 cadaver legs and described the superficial sural artery as a direct cutaneous branch developing from the popliteal artery in 50% and from the deep lateral sural artery in 45% of the specimens. This artery pierced the fascia 4 cm below the level of the tibial condyle. Shortly thereafter, they reported on successful microvascular transfer of this flap in 4 patients. Li and colleagues 13 performed a latex injection study in 20 legs and found that the superficial lateral sural artery branched off directly from the femoral artery in 17 cases and from the lateral inferior genicular artery in 3 cases. The artery had a diameter of 0.4 to 0.6 mm and was always accompanied by the lateral cutaneous sural nerve. It pierced the deep fascia at 4 to 6 cm below the lateral condyle of the tibia. In their study, they found 2 comitant veins with a diameter of 0.8 to 1.5 mm. As we also found, Li et al 13 described anastomoses of the superficial lateral sural artery with branches of the peroneal artery to form a suprafascial vascular network. From the results of their anatomic study, the authors preferred to use the superficial lateral sural artery, which they also found to be most consistent in their 17 successful clinical cases. Independent from these superficial sural vessels, myocutaneous perforators from the deep medial or lateral sural vessels provide an additional blood supply to the skin of the posterior lower leg. Consequently, perforator flaps predominantly from the medial sural artery have been described. 14 20 These authors found an average of 2 sizable medial sural perforators located between 9 to 18 cm distal to the flexor crease of the knee joint. Compared with the superficial arteries, the deep sural vessels have larger diameters, and pedicle lengths of up to 16 cm can be obtained. Due to its more constant anatomy and the favorable vascular pedicle, the medial sural artery perforator flap has proven to be useful for many indications including head and neck reconstruction. 20 Intramuscular dissection is necessary to develop the pedicle and any FIGURE 8. Appearance of the flap after 4 weeks (case 6). [Color figure can be viewed in the online issue, which is available at 1222 HEAD & NECK DOI 10.1002/HED SEPTEMBER 2012

SUPERFICIAL LATERAL SURAL FLAP FOR INTRAORAL RECONSTRUCTION FIGURE 9. Vascular supply of a posterolateral calf skin flap by superficial lateral sural and peroneal perforator vessels. [Color figure can be viewed in the online issue, which is available at muscular tissue has to be removed to obtain a thin flap. Another disadvantage is that a contour deformity can result at the donor site, and a skin graft may be necessary, especially in wider, more distally located flaps. 20 In a clinical study by Kashiwa et al, 21 the lateral gastrocnemius perforating vessels show a higher degree of variations and, as a consequence, they had to change the flapharvesting technique in 6 of their 10 patients. They proposed that for safe flap elevation from the lateral aspect of the posterior calf, 1 of the superficial sural arteries has to be preserved, until reliable perforators from the deep system above the lateral head of the gastrocnemius muscle are identified. In their study, 4 of 10 patients received microvascular flaps using 1 of the superficial sural vessels as the pedicle. As the literature shows, free skin flaps from the posterior lower leg are raised predominantly from the medial side and from the deep sural system. In this study, we describe for the first time a series of intraoral reconstructions using thin cutaneous flaps from the lateral aspect of the posterior calf with the superficial lateral sural vessels as the pedicle. The purpose of this investigation was to find an easy and reliable flap-raising procedure to obtain thin skin flaps for medium sized defects, without the need for intramuscular pedicle dissection or muscle resection and causing only a minimal donor site morbidity. As a prerequisite, the surgeon must be able to master anastomoses with calibers of about 1 mm. In both the anatomic and the clinical part of our study, the variability of the superficial lateral sural artery was confirmed. In the cadaver dissections, the superficial lateral sural arterywasmissingin6ofthe42 specimens, and in 11 cadavers, the artery was <1 mm. Therefore, a microvascular transfer would have been difficult or even impossible in 17 of the 42 specimens (40.5%). In the clinical study, elevation of a superficial lateral sural flap was possible in only 12 of the 20 patients, because either the artery was missing, 2 the vessels were too small, 5 or developed spasm. 1 Whereas pedicled cutaneous flaps from the posterior calf have been described as reliable for local defect cover, 13,22 25 there are only very few reports with small numbers of patients in relation to microvascular transfers on the superficial vascular system. 7,21 This might be explained by the assumption that performing microvascular anastomoses on very small vessels with an inconstant and variable anatomy might have been initially associated with high failure rates, so that this method was abandoned. As we have shown in our study, despite these drawbacks the skin of the posterolateral calf can be transferred as a free flap with high success rates, if the proximal peroneal perforator is used as a back-up pedicle (Figure 9). It has already been shown in a number of anatomic investigations that this perforator can be found regularly in the upper half of the lower leg, 4,26,27 making flap harvesting safe and primary closure possible. In 8 of our clinical cases, the peroneal vessels were preserved completely, and the flap was transferred solely on the perforating vessels as described in a previous study. 28 When comparing the superficial lateral sural and the peroneal perforator pedicle, due to its superficial course, the dissection of the former can be performed quickly and easily as soon as it has been exposed in the popliteal fossa. In contrast to this, dissecting the peroneal perforators is more demanding because they have to be followed into the deep flexor space to the peroneal vessels, which are located behind the fibula. In addition, a small cuff of the flexor hallucis longus muscle often has to be included. Therefore, the superficial lateral sural vessels were selected as the first choice, as soon as their presence and reliability were confirmed by direct visualization. Because of their close proximity, changing the concept of flap raising from the sural to the peroneal perforator vessels creates little additional scars or other morbidity. CONCLUSION The superficial lateral sural vessels show anatomic variations, which make the use of this pedicle for microvascular transplantation unreliable or impossible in 40% of all cases. Nevertheless, cutaneous free flaps from the proximal posterolateral calf can be transferred safely, if a close proximal peroneal perforator is selected as a backup. A staged skin incision allows accomplishing flap harvest using the most appropriate pedicle. If sizable superficial lateral sural vessels are present, the good accessibility of this pedicle allows quick and easy flap elevation. The thin and pliable skin of the posterolateral lower leg is very well suited for intraoral defect cover. Considering its anatomic variations, this donor site can be a useful expansion to harvest flaps for covering of moderate sized, flat defects. REFERENCES 1. Carriquiry C, Costa MA, Vasconez LO. An anatomic study of the septocutaneous vessels of the leg. Plast Reconstr Surg 1985;76:354 363. 2. Wee JT. Reconstruction of the lower leg and foot with the reverse-pedicled anterior tibial flap: preliminary report of a new fasciocutaneous flap. Br J Plast Surg 1986;39:327 337. 3. Zhang S, Li J, Song K. Clinical applications of the free posterior tibial flap. Chin Surg 1983;21:743 745. 4. Yoshimura M, Shimada T, Hosokawa M. 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