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Anatomical study of the cutaneous perforator arteries and vascularisation of the biceps femoris muscle
British Journal of Plastic Surgery (2005) 58, 1079–1085
Anatomical study of the cutaneous perforator arteries and vascularisation of the biceps femoris muscle J.F. Salvador-Sanz*, A. Novo Torres, F. Terol Calpena, J.R. Sanz-Gimenez-Rico, S. Carnero Lopez, E. Lorda Barraquer Department of Histology and Human Anatomy, University Miguel Hernandez School of Medicine, Crta. Nacional Alicante-Valencia, Km-332, s/n San Juan, 03550 Alicante, Spain Received 4 December 2003; accepted 17 May 2005
KEYWORDS Biceps femoris; Perforator artery; Short head; Long head; Axial vessel
Summary We present an anatomical study that describes the distribution of the cutaneous perforators (CP) of both heads of the biceps femoris muscle. Material and methods: In this study, we dissected 18 legs from nine cadavers. The study was centered on the biceps femoris muscle and musculocutaneous perforator arteries from both muscular heads. Only perforator arteries with comitant vein diameters of over 0.5 mm were selected. The vascular origin and length were also studied. In all cases, measurements were taken from the bicondyle line. Results: The measurements taken from the muscle bellies of the biceps gave the following results; for the long head 33.91 cm as medium length (SDZ2.70) and for the short head 23.85 cm as medium length (SDZ2.96). The total number of perforator arteries obtained from the two muscle bellies was 139, with the greatest percentage located in the lower half of the thigh. The majority follow an intramuscular route (80.48%) and less frequently they are septals (19.52%). The lengths of perforator arteries from its origin in the axial vessel of the muscle to the subcutaneous fat were, for the short head 5.01G1.33 (3.0–10.0), whereas the same measurement, in the long head was 4.54G1.36 (2.5–9.0). The principal vascular origin of the perforator arteries was the popliteal artery in both muscle bellies, whilst the second arterial vessel in importance was the first and second profunda perforator artery. Conclusion: From the results obtained in our work, we can deduce that it is always possible to locate perforator arteries in both muscle bellies; most frequently they have intramuscular distribution and are located in the proximity of the vascular septum. Their most common origins are the popliteal artery and first and second profunda perforator artery. Finally, it is possible to design pedicle and free flaps, with less morbidity and more versatility than musculocutaneous flaps. q 2005 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Address: Department of Plastic and Reconstructive Surgery, University Hospital Alicante, C/Maestro Alonso 109, 03010 Alicante, Spain. Tel.: C34 965938294. E-mail address: [email protected] (J.F. Salvador-Sanz).
S0007-1226/$ - see front matter q 2005 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2005.05.015
1080 Since 1987, with the introduction of the concept of angiosomes by Taylor and Palmer,1,2 and the subsequent development of perforator flaps by Koshima,3,4 the design and extraction of diverse flaps in the lower limb according to the cutaneous distribution of the perforator vessels5–8 are possible. The biceps femoris muscle has been classically used as a rotation muscular flap (long head) for the treatment of ischial sores and as a cutaneous advanced muscle flap with a cutaneous paddle for adjacent soft tissue defects.9–15 Since, this muscle has two heads with different inervation and irrigation, it is possible to use them independently one from the other. Sanahan et al.16–18 carries out a study of the intramuscular vascularisation of the long head of the biceps demonstrating that there exists communication between the principal and secondary
J.F. Salvador-Sanz et al. pedicles, taking advantage of this discovery in the design of flaps.19 In 2001, Hayashi and Maruyama published the vascular anatomy of the short head of the biceps femoris in relation to the lateral intermuscular septum of the thigh.20 Recently, they published the neurovascularised free short head of the biceps femoris muscle transfer for one-stage reanimation of facial paralysis.21 Our article presents an anatomical study that describes the distribution of the cutaneous perforators arteries (CP) of both heads of the biceps femoris, their origin, length and clinical applications as perforator flaps (Figs. 3 and 4).
Materials and methods We dissected 18 legs from nine cadavers fixed with
Figure 1 (A) The presence of musculocutaneous perforator vessels was constant. Pink needles indicate perforator vessels from long head of biceps femoris muscle. LH-BH, long head of biceps femoris muscle; SHBF, short head of biceps femoris muscle. (B) Magnification of two perforator vessels from short head biceps femoris muscle.
Figure 2 (A) Formolized cadaver. Perforator vessels from lateral edge of short head of biceps femoris muscle. PA, perforator artery; CV, venae comitantes; SH-BF, short head of biceps femoris muscle. (B) Formolized cadaver. Septal perforator vessels from septum between two heads of biceps femoris muscle.
Biceps femoris perforator arteries formaldehyde and with coloured latex injection in the femoral vessels. Six cadavers were male and three female. The posterior region of the thigh was dissected with a longitudinal incision in the medial line and another two incisions on the extremes of the same, one following the inferior gluteal line and the other on the bicondyle line. As reference, we used the bicondyle line for all measurements. The medial and lateral fasciocutaneous flaps were harvested exposing both muscular heads of the biceps, the long head and the short head. While harvesting the fasciocutaneous flaps, the CP were identified with their comitant veins with a diameter of over 0.5 mm. References were obtained from lateral and medial edges of both muscular heads. Measurements of the long and short heads of the biceps muscle of each leg were obtained, as well as the length of the leg measured from the bicondyle line to the ischial tuberosity. Since the tendinous insertions of the long head were the same as for the thigh. As a result, we consider that the length of the thigh to be the length of the long head of the biceps. The CP were dissected to their origins in the axial vessels (Figs. 1 and 2). The length of CP from the axial vessels to the subdermal fat was measured. Also the axial vessels were referenced as the origin of the CP, both of the short head and of the long head. In order to study the biceps femoris vascularisation, the axial vessels of this muscle were dissected in all cases, identifying their origins, their length and their entry in the muscle as nutrient artery. The entry of the diverse vessels in the muscle, marked the reference with respect to the bicondyle line.
Figure 3 Cross section diagram. 1. Bone 2. Axial artery 3. Muscle artery 4. Musculacutaneous artery 5. Septocutaneous artery 6. Subcutaneous layer 7. Skin padle.
1081
Results The measurements taken from the muscle bellies of the biceps gave the following results for the long head, 33.91 cm as medium length (SDZ2.70) and for the short head, 23.85 cm as medium length (SDZ2.96).
Figure 4 Vascular anatomy. 1. Femoris artery 2. Media circumflex femoris artery 3. Lateral circumflex femoris artery 4. ramus descendens 5. First, second and third profunda perforator arteries 6. Long head of biceps femoris muscle 7. Short head of biceps femoris muscle.
1082
Figure 5 length.
J.F. Salvador-Sanz et al.
References of perforator arteries respecting the bicondyle line; 0Zbicondyle line, 1Zmaximum thigh
Figure 6
References of perforator arteries respecting the lateral and medial edges of both biceps femoris heads.
Distribution of the perforators (CP) To locate the CP we took the measurement between their emergence at the muscle edges and the bicondyle line. Since, the length of the muscular belly depends on the length of the leg, we decided to turn the absolute values of reference with regard to the bicondyle line into relative values, dividing the distance obtained in every CP with regard to the bicondyle line by the total length of the thigh. Thanks to this conversion we can locate the CP as is recorded in Fig. 5, where 0 on the X axis
Table 1
Perforator arteries (CP) length (in cm) from axial vessel to skin flap N
Long head perforator arteries (CP) Short head perforator arteries (CP) a b
represents the bicondyle line and the 1.0 represents the ischial tuberosity. The total number of CP obtained for both muscle bellies were 139 (in all 18 legs). Their distribution, depending on whether they were lateral or medial, is shown for both muscle bellies in Fig. 6. For the short head of the biceps the highest number of CP were centered on the points of 0.2 (14 perforators) and 0.3 (17 perforators). On the long head of the biceps, the highest number were centered on the points 0.2 (12 perforators) and 0.4 (15 perforators). The highest percentage of CP is located in the
% Laterala
70
9.0
69
70.5
% Medialb
Minimal length
Maximal length
Medial length
SD
91
3.0
10
5.01
1.33
29.5
2.5
4.54
1.36
Lateral, emergence from the lateral edge of the bı´ceps femoris. Medial, emergence from the medial edge of the biceps femoris.
9.0
Biceps femoris perforator arteries Table 2
1083
Vascular origin of perforator arteries (CP)
MCFA 1P 2P 3P Popliteal artery Vasa nervorum
Short head perforator arteries, CP (%)
Long head perforator arteries, CP (%)
3.7 3.9 33.3 11.1 42.6 0
10.7 21.4 21.4 1.8 32.1 12.5
MCFA, medial circumflex femoris artery; 1P, first profunda perforator artery of the profunda femoris artery; 2P, second profunda perforator artery of the profunda femoris artery; 3P, third profunda perforator artery of the profunda femoris artery.
lower half of the thigh. The majority follow an intramuscular route (80.48%) and less frequently they are septals (19.52%). The lengths of CP from its origin in the axial vessel of the muscle to the subcutaneous fat were, for the short head 5.01G1.33 (3.0–10.0), whereas the same measurement, in the long head was 4.54G1.36 (2.5–9.0). The vascular origin of the CP found according to the axial vessels is expressed in Table 1, where the principal axial vessel was the popliteal artery in both muscle bellies (42.6 and 32.1%, respectively, in the short head and long head), whilst the second arterial vessel in importance is the 2PPA for the short head and the 1PPA and 2PPA for the long head.
in the Table 2. The average number of axial arteries in each muscle belly was: 2.12 (SDZ1.14) for the short head and 3.25 (SDZ0.93) for the long head (Table 3). Using the same scheme of conversion in relative values used in the location of the CP, the following information was obtained for the principal muscular axial arteries.
Muscular axial arteries
Long head The MCFA was the axis in 18 legs. The reference with regard to the bicondyle line was 0.73 (range 0. 59–0.90). The 1PPA was the axis in 17 legs. The reference with regard to the bicondyle line was 0.58 (range 0. 46–0.74).
Five principal axial arteries were found in the biceps femoris muscle: Medial circumflex femoris artery (MCFA), first profunda perforator artery (1PPA), second profunda perforator artery (2PPA), third profunda perforator artery (3PPA), popliteal artery and vasa nervorum arteries of the sciatic nerve. The distribution in percentages is expressed
Short head The 2PPA was the axis in nine legs. The reference with regard to the bicondyle line was 0.44 (range 0.21–0.57). The popliteal artery was the axis in seven legs. The reference with regard to the bicondyle line was 0.30 (range 0.22–0.45).
Discussion Table 3 Summary of muscle axial vessels respect their arterial origin
MCFA 1P 2P 3P Popliteal artery Vasa nervorum
Axial vessels short head (%)
Axial vessels long head (%)
9.4 6.3 28.1 18.7 37.5 0
38.5 42.3 13.5 0 38.0 1.9
MCFA, medial circumflex femoris artery; 1P, first profunda perforator artery of the profunda femoris artery; 2P, second profunda perforator artery of the profunda femoris artery; 3P, third profunda perforator artery of the profunda femoris artery.
Cutaneous perforators (CP) There are no published studies on the existence and distribution of CP in the biceps femoris muscle, therefore it’s not possible to do comparative studies with results obtained by other authors. From the results obtained, we can say that in all cases there are CP in both muscle bellies. There are many CP with the possibility of clinical application in the design of vascular flaps and can be located in the edges of both muscle bellies. The fact that in our study is a high number of CP that appear on the medial edge of the long head as well as the lateral edge of the short head. This is
1084 explained on the basis of the proximity of the vascular septum; the deep femoral vascular axis between the biceps and semimembranous muscles for the medial perforators of the long head and the vascular axis between the thin tensor fasciae latae and biceps femoris muscles for the lateral perforators of the short head of the biceps. This information corroborates the results published by Hayashi and Maruyama.20 The highest percentage of CP have their origin in the popliteal artery and the 2PPA for the short head and in the popliteal artery and in the 1PPA for the long head (Table 2). The length and calibre of the CP in both muscle bellies are adequate to be adapted for posterior use in vascular free or pedicled flap design. There also exists the possibility of location through Doppler of CP at the moment of the flap design. The posterior region of the thigh and in particular the cutaneous territory served by CP of the biceps femoris muscle maintain characteristics of thickness, malleability and texture similar to the anterolateral region of the thigh, which make it useful as donor site tissues with minimal sequels (small flaps may be closed directly or, when necessary, skin grafts may be used on muscle bellies with good blood supply). The dissection of the CP, both intramuscular and extramuscular do not offer many differences in respect to the dissection of the rest of the CP used in other similar flaps. With regard to the comitant veins, most of the CP are accompanied by two veins. In a few cases, a single vein was observed but cases without comitant veins were exceptional.
Vascular axes For Mathes and Nahai the biceps femoris muscle follows a vascular patron type I, that later was classified as type II.17 We found the same dominant vascular axes as other scientific workers.13–15,18,20 For the short head of the biceps, 28.1% comes from the 2PPA (58% for Hayashi)20 and 18.7% from the 3PPA (33% for Hayashi);20 for the long head, 38.5% comes from the MCFA, 42.3% from the 1PPA and 13.5% from the 2PPA. We can say that whichever axes have the muscular belly, greater reliability of dissection of CP cradles in one of them without jeopardising the vascularisation of the complete muscular belly thanks to the intramuscular existence of anastomosis; nevertheless, they add major difficulty to the dissection.
J.F. Salvador-Sanz et al. On the basis of this study, we can design flaps, both of the short head and long head, centred on the points 0.2–0.4, where there are more possibilities in finding existing CP. This design in the distal third of the thigh makes it possible to obtain longer vascular lengths for the selected CP. It is always possible to locate CP in both muscle bellies, with lengths adapted for the design of flaps and it is also possible to extend with the dissection of the axial vessels. These CP are located most frequently in the proximities of the vasculoaponeurotic septum and in its great majority they have an intramuscular distribution. The vascular axes that originate CP with most frequency are the popliteal artery and the 2PPA for the short head of the biceps and the poplı´teal artery and the 1PPA and 2PPA for the long head of the biceps. The dominance of the vascular axes are not possible to establish with absolute exactness in cadaver studies with post-mortem latex injections. Using the proximal axes (MCFA, 1PPA, 2PPA and 3PPA), it is possible to use flaps for ischial or trocanter defects and even in the inguinal zone. Using distal axis (superior lateral genicular artery) it is possible to design flaps for the knee, popliteal fossa and the proximal part of the leg, excepting the medial regions as described by Hayashi.20 The short head of the biceps as a free flap based on the 2PPA and 3PPA can be used for coverage of defects needing cutaneoadipose flaps of moderate thickness, with good arterial and venous vessels for microvascular suture and pedicle lengths of over 8 cm. The long head of the biceps, based on the MCFA, 1PPA and 2PPA, would act the same way. Hayashi also considers the possibility of designing compound musculocutaneous flaps with the short and long heads of the biceps and even the design of chimeric flaps using both muscular heads. With good function of the adjacent muscles that stabilises and flex the knee, the functional and aesthetic result for donor muscle is acceptable.14,20 Though, this alternative is valid when existing the need of major quantity of tissue or in cases of muscular reconstruction (quadriceps), the possibility of harvesting perforator flaps without muscle has widened a new field of indications and also contributed in reducing the morbidity of the donor site. As Quaba described in his work, due to the direction entry of the dominant axis in the long head of the biceps, with entry of the second pedicle to approximately 14 cm from the ischial tuberosity, the muscle has no rotation at 1808 for the coverage
Biceps femoris perforator arteries of ischial sores without the risk of suffering muscular necrosis.14 This risk can be resolved with the use of perforator flaps based on the principal axes since it allows wider rotations without provoking vascular compromise (Table 3). Summarising, we conclude that 1. It is always possible to locate CP in both muscle bellies; most frequently they have intramuscular distribution and their most common origins are the popliteal artery and the 1PPA and 2PPA. 2. It is possible to obtain large thin flaps. 3. It’s possible to design chimeric flaps in association with muscles and septum from adjacent anatomic regions. 4. An important decrease in donor-site morbidity as a consequence of the preservation of muscle innervation, vascularisation and functionality of the donor muscle. 5. Higher versatility than the musculocutaneous flaps.
1085
6. 7.
8.
9.
10.
11.
12.
13.
Acknowledgements We would like to thank Human Anatomy Department of Miguel Hernandez University, for assistance in preparing cadaver and Jose ´ Sanchez-Paya, MD, PhD, for assistance with the statistical analysis.
14.
15.
16. 17.
References 1. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: Experimental study and clinical applications. Br J Plast Surg 1987;40:113. 2. Taylor GI, Pan WR. Angiosomes of the leg: Anatomic Study and Clinical Implications. Plast Reconstr Surg 1998;102: 599–616. 3. Koshima I, Soeda S. Inferior epigastric artery skin flaps without rectus abdominis muscle. Br J Plast Surg 1989;42: 645. 4. Koshima I, Soeda S. Free posterior tibial perforator based flaps. Ann Plast Surg 1991;26:284. 5. Kimata Y, Uchiyama K, Ebihara S, Nakatsuka T, Harii K.
18.
19.
20.
21.
Anatomic variations and technical problems of the anterolateral thigh flap: A report of 74 cases. Plast Reconstr Surg 1998;102(5):1517–23. Kimura N. A microdissected thin tensor fasciae latae perforator flap. Plast Reconstr Surg 2002;109(1):69–77. Valdatta L, Tuinder S, Buoro M. Lateral circumflex femoral arterial system and perforator of the anterolateral thigh flap: An Anatomic Study. Ann Plast Surg 2002;49(2):145–50. Angrigiani C, Grilli D, Thorne CH. The adductor flap: A new method for transferring posterior and medial thigh skin. Plast Reconstr Surg 2001;107(7):1725–31. Conway H, Griffinth BH. Plastic surgery for closure of decubitus ulcers in patients with paraplegia. Am J Surg 1956;91:946. McCraw JB, Dibell DG, Carraway JH. Clinical definition of independent myocutaneous vascular territories. Plast Reconstr Surg 1977;60:341. James JH, Moir IH. The biceps femoris musculocutaneous flap in the repair of pressure sores around the hip. Plast Reconstr Surg 1980;66(5):736. Shanahan DA, George B, Williams NS, Sinnataneby CS, Riches DJ. The long head of the biceps femoris: Anatomic basis for its possible use in the construction of an electrically stimulated neonal sphinter. Plast Reconstr Surg 1993;92(2): 55–8. Rab M, et al. Basic anatomical investigation of semitendinosus and the long head of bı´ceps femoris muscle for their posible use in electrically stimulated neosphinter formation. Surg Radiol Anat 1997;19:13–15. Quaba AA, Chapman R, Hackett ME. Extended application of the bı´ceps femoris musculocutaneos flap. Plast Reconstr Surg 1988;81(1):94–105. Tobin GR, Sanders BP, Man D, Weiner LJ. The biceps femoris myocutaneous advancementent flap: A useful modification for ischial pressure ulcer reconstruction. Ann Plast Surg 1981;6:396. Romanes GJ. Cunningham’s textbook of anatomy. Oxford: Oxford University Press; 1981 p. 404–7. Maquelet AC, Gilbert A. An atlas of flaps in limb reconstruction.: Martin Dunitz; 1995 p. 107–10. Farouk O, Krettek C, Miclau T. The topography of the perforating vessels of the deep femoral artery. Clin Orthop 1999;368:255–9. Shanahan D, Jordan RK, Coulthard A, Cooper PN, Varma J. The intramuscular arterial anatomy of the long head of biceps femoris muscle. J Anat 1997;190(3):467–72. Hayashi A, Maruyama Y. Lateral intermuscular septum of the thigh and short head of the biceps femoris muscle: An anatomic investigation with new clinical applications. Plast Reconstr Surg 2001;108(6):1636–54. Hayashi A, Maruyama Y. Neurovascularized free short head of the biceps femoris muscle transfer for one-stage reanimation of facial paralysis. Plast Reconstr Surg 2005; 115(2):394–405.
Anatomical study of the cutaneous perforator arteries and vascularisation of the biceps femoris muscle J.F. Salvador-Sanz*, A. Novo Torres, F. Terol Calpena, J.R. Sanz-Gimenez-Rico, S. Carnero Lopez, E. Lorda Barraquer Department of Histology and Human Anatomy, University Miguel Hernandez School of Medicine, Crta. Nacional Alicante-Valencia, Km-332, s/n San Juan, 03550 Alicante, Spain Received 4 December 2003; accepted 17 May 2005
KEYWORDS Biceps femoris; Perforator artery; Short head; Long head; Axial vessel
Summary We present an anatomical study that describes the distribution of the cutaneous perforators (CP) of both heads of the biceps femoris muscle. Material and methods: In this study, we dissected 18 legs from nine cadavers. The study was centered on the biceps femoris muscle and musculocutaneous perforator arteries from both muscular heads. Only perforator arteries with comitant vein diameters of over 0.5 mm were selected. The vascular origin and length were also studied. In all cases, measurements were taken from the bicondyle line. Results: The measurements taken from the muscle bellies of the biceps gave the following results; for the long head 33.91 cm as medium length (SDZ2.70) and for the short head 23.85 cm as medium length (SDZ2.96). The total number of perforator arteries obtained from the two muscle bellies was 139, with the greatest percentage located in the lower half of the thigh. The majority follow an intramuscular route (80.48%) and less frequently they are septals (19.52%). The lengths of perforator arteries from its origin in the axial vessel of the muscle to the subcutaneous fat were, for the short head 5.01G1.33 (3.0–10.0), whereas the same measurement, in the long head was 4.54G1.36 (2.5–9.0). The principal vascular origin of the perforator arteries was the popliteal artery in both muscle bellies, whilst the second arterial vessel in importance was the first and second profunda perforator artery. Conclusion: From the results obtained in our work, we can deduce that it is always possible to locate perforator arteries in both muscle bellies; most frequently they have intramuscular distribution and are located in the proximity of the vascular septum. Their most common origins are the popliteal artery and first and second profunda perforator artery. Finally, it is possible to design pedicle and free flaps, with less morbidity and more versatility than musculocutaneous flaps. q 2005 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Address: Department of Plastic and Reconstructive Surgery, University Hospital Alicante, C/Maestro Alonso 109, 03010 Alicante, Spain. Tel.: C34 965938294. E-mail address: [email protected] (J.F. Salvador-Sanz).
S0007-1226/$ - see front matter q 2005 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2005.05.015
1080 Since 1987, with the introduction of the concept of angiosomes by Taylor and Palmer,1,2 and the subsequent development of perforator flaps by Koshima,3,4 the design and extraction of diverse flaps in the lower limb according to the cutaneous distribution of the perforator vessels5–8 are possible. The biceps femoris muscle has been classically used as a rotation muscular flap (long head) for the treatment of ischial sores and as a cutaneous advanced muscle flap with a cutaneous paddle for adjacent soft tissue defects.9–15 Since, this muscle has two heads with different inervation and irrigation, it is possible to use them independently one from the other. Sanahan et al.16–18 carries out a study of the intramuscular vascularisation of the long head of the biceps demonstrating that there exists communication between the principal and secondary
J.F. Salvador-Sanz et al. pedicles, taking advantage of this discovery in the design of flaps.19 In 2001, Hayashi and Maruyama published the vascular anatomy of the short head of the biceps femoris in relation to the lateral intermuscular septum of the thigh.20 Recently, they published the neurovascularised free short head of the biceps femoris muscle transfer for one-stage reanimation of facial paralysis.21 Our article presents an anatomical study that describes the distribution of the cutaneous perforators arteries (CP) of both heads of the biceps femoris, their origin, length and clinical applications as perforator flaps (Figs. 3 and 4).
Materials and methods We dissected 18 legs from nine cadavers fixed with
Figure 1 (A) The presence of musculocutaneous perforator vessels was constant. Pink needles indicate perforator vessels from long head of biceps femoris muscle. LH-BH, long head of biceps femoris muscle; SHBF, short head of biceps femoris muscle. (B) Magnification of two perforator vessels from short head biceps femoris muscle.
Figure 2 (A) Formolized cadaver. Perforator vessels from lateral edge of short head of biceps femoris muscle. PA, perforator artery; CV, venae comitantes; SH-BF, short head of biceps femoris muscle. (B) Formolized cadaver. Septal perforator vessels from septum between two heads of biceps femoris muscle.
Biceps femoris perforator arteries formaldehyde and with coloured latex injection in the femoral vessels. Six cadavers were male and three female. The posterior region of the thigh was dissected with a longitudinal incision in the medial line and another two incisions on the extremes of the same, one following the inferior gluteal line and the other on the bicondyle line. As reference, we used the bicondyle line for all measurements. The medial and lateral fasciocutaneous flaps were harvested exposing both muscular heads of the biceps, the long head and the short head. While harvesting the fasciocutaneous flaps, the CP were identified with their comitant veins with a diameter of over 0.5 mm. References were obtained from lateral and medial edges of both muscular heads. Measurements of the long and short heads of the biceps muscle of each leg were obtained, as well as the length of the leg measured from the bicondyle line to the ischial tuberosity. Since the tendinous insertions of the long head were the same as for the thigh. As a result, we consider that the length of the thigh to be the length of the long head of the biceps. The CP were dissected to their origins in the axial vessels (Figs. 1 and 2). The length of CP from the axial vessels to the subdermal fat was measured. Also the axial vessels were referenced as the origin of the CP, both of the short head and of the long head. In order to study the biceps femoris vascularisation, the axial vessels of this muscle were dissected in all cases, identifying their origins, their length and their entry in the muscle as nutrient artery. The entry of the diverse vessels in the muscle, marked the reference with respect to the bicondyle line.
Figure 3 Cross section diagram. 1. Bone 2. Axial artery 3. Muscle artery 4. Musculacutaneous artery 5. Septocutaneous artery 6. Subcutaneous layer 7. Skin padle.
1081
Results The measurements taken from the muscle bellies of the biceps gave the following results for the long head, 33.91 cm as medium length (SDZ2.70) and for the short head, 23.85 cm as medium length (SDZ2.96).
Figure 4 Vascular anatomy. 1. Femoris artery 2. Media circumflex femoris artery 3. Lateral circumflex femoris artery 4. ramus descendens 5. First, second and third profunda perforator arteries 6. Long head of biceps femoris muscle 7. Short head of biceps femoris muscle.
1082
Figure 5 length.
J.F. Salvador-Sanz et al.
References of perforator arteries respecting the bicondyle line; 0Zbicondyle line, 1Zmaximum thigh
Figure 6
References of perforator arteries respecting the lateral and medial edges of both biceps femoris heads.
Distribution of the perforators (CP) To locate the CP we took the measurement between their emergence at the muscle edges and the bicondyle line. Since, the length of the muscular belly depends on the length of the leg, we decided to turn the absolute values of reference with regard to the bicondyle line into relative values, dividing the distance obtained in every CP with regard to the bicondyle line by the total length of the thigh. Thanks to this conversion we can locate the CP as is recorded in Fig. 5, where 0 on the X axis
Table 1
Perforator arteries (CP) length (in cm) from axial vessel to skin flap N
Long head perforator arteries (CP) Short head perforator arteries (CP) a b
represents the bicondyle line and the 1.0 represents the ischial tuberosity. The total number of CP obtained for both muscle bellies were 139 (in all 18 legs). Their distribution, depending on whether they were lateral or medial, is shown for both muscle bellies in Fig. 6. For the short head of the biceps the highest number of CP were centered on the points of 0.2 (14 perforators) and 0.3 (17 perforators). On the long head of the biceps, the highest number were centered on the points 0.2 (12 perforators) and 0.4 (15 perforators). The highest percentage of CP is located in the
% Laterala
70
9.0
69
70.5
% Medialb
Minimal length
Maximal length
Medial length
SD
91
3.0
10
5.01
1.33
29.5
2.5
4.54
1.36
Lateral, emergence from the lateral edge of the bı´ceps femoris. Medial, emergence from the medial edge of the biceps femoris.
9.0
Biceps femoris perforator arteries Table 2
1083
Vascular origin of perforator arteries (CP)
MCFA 1P 2P 3P Popliteal artery Vasa nervorum
Short head perforator arteries, CP (%)
Long head perforator arteries, CP (%)
3.7 3.9 33.3 11.1 42.6 0
10.7 21.4 21.4 1.8 32.1 12.5
MCFA, medial circumflex femoris artery; 1P, first profunda perforator artery of the profunda femoris artery; 2P, second profunda perforator artery of the profunda femoris artery; 3P, third profunda perforator artery of the profunda femoris artery.
lower half of the thigh. The majority follow an intramuscular route (80.48%) and less frequently they are septals (19.52%). The lengths of CP from its origin in the axial vessel of the muscle to the subcutaneous fat were, for the short head 5.01G1.33 (3.0–10.0), whereas the same measurement, in the long head was 4.54G1.36 (2.5–9.0). The vascular origin of the CP found according to the axial vessels is expressed in Table 1, where the principal axial vessel was the popliteal artery in both muscle bellies (42.6 and 32.1%, respectively, in the short head and long head), whilst the second arterial vessel in importance is the 2PPA for the short head and the 1PPA and 2PPA for the long head.
in the Table 2. The average number of axial arteries in each muscle belly was: 2.12 (SDZ1.14) for the short head and 3.25 (SDZ0.93) for the long head (Table 3). Using the same scheme of conversion in relative values used in the location of the CP, the following information was obtained for the principal muscular axial arteries.
Muscular axial arteries
Long head The MCFA was the axis in 18 legs. The reference with regard to the bicondyle line was 0.73 (range 0. 59–0.90). The 1PPA was the axis in 17 legs. The reference with regard to the bicondyle line was 0.58 (range 0. 46–0.74).
Five principal axial arteries were found in the biceps femoris muscle: Medial circumflex femoris artery (MCFA), first profunda perforator artery (1PPA), second profunda perforator artery (2PPA), third profunda perforator artery (3PPA), popliteal artery and vasa nervorum arteries of the sciatic nerve. The distribution in percentages is expressed
Short head The 2PPA was the axis in nine legs. The reference with regard to the bicondyle line was 0.44 (range 0.21–0.57). The popliteal artery was the axis in seven legs. The reference with regard to the bicondyle line was 0.30 (range 0.22–0.45).
Discussion Table 3 Summary of muscle axial vessels respect their arterial origin
MCFA 1P 2P 3P Popliteal artery Vasa nervorum
Axial vessels short head (%)
Axial vessels long head (%)
9.4 6.3 28.1 18.7 37.5 0
38.5 42.3 13.5 0 38.0 1.9
MCFA, medial circumflex femoris artery; 1P, first profunda perforator artery of the profunda femoris artery; 2P, second profunda perforator artery of the profunda femoris artery; 3P, third profunda perforator artery of the profunda femoris artery.
Cutaneous perforators (CP) There are no published studies on the existence and distribution of CP in the biceps femoris muscle, therefore it’s not possible to do comparative studies with results obtained by other authors. From the results obtained, we can say that in all cases there are CP in both muscle bellies. There are many CP with the possibility of clinical application in the design of vascular flaps and can be located in the edges of both muscle bellies. The fact that in our study is a high number of CP that appear on the medial edge of the long head as well as the lateral edge of the short head. This is
1084 explained on the basis of the proximity of the vascular septum; the deep femoral vascular axis between the biceps and semimembranous muscles for the medial perforators of the long head and the vascular axis between the thin tensor fasciae latae and biceps femoris muscles for the lateral perforators of the short head of the biceps. This information corroborates the results published by Hayashi and Maruyama.20 The highest percentage of CP have their origin in the popliteal artery and the 2PPA for the short head and in the popliteal artery and in the 1PPA for the long head (Table 2). The length and calibre of the CP in both muscle bellies are adequate to be adapted for posterior use in vascular free or pedicled flap design. There also exists the possibility of location through Doppler of CP at the moment of the flap design. The posterior region of the thigh and in particular the cutaneous territory served by CP of the biceps femoris muscle maintain characteristics of thickness, malleability and texture similar to the anterolateral region of the thigh, which make it useful as donor site tissues with minimal sequels (small flaps may be closed directly or, when necessary, skin grafts may be used on muscle bellies with good blood supply). The dissection of the CP, both intramuscular and extramuscular do not offer many differences in respect to the dissection of the rest of the CP used in other similar flaps. With regard to the comitant veins, most of the CP are accompanied by two veins. In a few cases, a single vein was observed but cases without comitant veins were exceptional.
Vascular axes For Mathes and Nahai the biceps femoris muscle follows a vascular patron type I, that later was classified as type II.17 We found the same dominant vascular axes as other scientific workers.13–15,18,20 For the short head of the biceps, 28.1% comes from the 2PPA (58% for Hayashi)20 and 18.7% from the 3PPA (33% for Hayashi);20 for the long head, 38.5% comes from the MCFA, 42.3% from the 1PPA and 13.5% from the 2PPA. We can say that whichever axes have the muscular belly, greater reliability of dissection of CP cradles in one of them without jeopardising the vascularisation of the complete muscular belly thanks to the intramuscular existence of anastomosis; nevertheless, they add major difficulty to the dissection.
J.F. Salvador-Sanz et al. On the basis of this study, we can design flaps, both of the short head and long head, centred on the points 0.2–0.4, where there are more possibilities in finding existing CP. This design in the distal third of the thigh makes it possible to obtain longer vascular lengths for the selected CP. It is always possible to locate CP in both muscle bellies, with lengths adapted for the design of flaps and it is also possible to extend with the dissection of the axial vessels. These CP are located most frequently in the proximities of the vasculoaponeurotic septum and in its great majority they have an intramuscular distribution. The vascular axes that originate CP with most frequency are the popliteal artery and the 2PPA for the short head of the biceps and the poplı´teal artery and the 1PPA and 2PPA for the long head of the biceps. The dominance of the vascular axes are not possible to establish with absolute exactness in cadaver studies with post-mortem latex injections. Using the proximal axes (MCFA, 1PPA, 2PPA and 3PPA), it is possible to use flaps for ischial or trocanter defects and even in the inguinal zone. Using distal axis (superior lateral genicular artery) it is possible to design flaps for the knee, popliteal fossa and the proximal part of the leg, excepting the medial regions as described by Hayashi.20 The short head of the biceps as a free flap based on the 2PPA and 3PPA can be used for coverage of defects needing cutaneoadipose flaps of moderate thickness, with good arterial and venous vessels for microvascular suture and pedicle lengths of over 8 cm. The long head of the biceps, based on the MCFA, 1PPA and 2PPA, would act the same way. Hayashi also considers the possibility of designing compound musculocutaneous flaps with the short and long heads of the biceps and even the design of chimeric flaps using both muscular heads. With good function of the adjacent muscles that stabilises and flex the knee, the functional and aesthetic result for donor muscle is acceptable.14,20 Though, this alternative is valid when existing the need of major quantity of tissue or in cases of muscular reconstruction (quadriceps), the possibility of harvesting perforator flaps without muscle has widened a new field of indications and also contributed in reducing the morbidity of the donor site. As Quaba described in his work, due to the direction entry of the dominant axis in the long head of the biceps, with entry of the second pedicle to approximately 14 cm from the ischial tuberosity, the muscle has no rotation at 1808 for the coverage
Biceps femoris perforator arteries of ischial sores without the risk of suffering muscular necrosis.14 This risk can be resolved with the use of perforator flaps based on the principal axes since it allows wider rotations without provoking vascular compromise (Table 3). Summarising, we conclude that 1. It is always possible to locate CP in both muscle bellies; most frequently they have intramuscular distribution and their most common origins are the popliteal artery and the 1PPA and 2PPA. 2. It is possible to obtain large thin flaps. 3. It’s possible to design chimeric flaps in association with muscles and septum from adjacent anatomic regions. 4. An important decrease in donor-site morbidity as a consequence of the preservation of muscle innervation, vascularisation and functionality of the donor muscle. 5. Higher versatility than the musculocutaneous flaps.
1085
6. 7.
8.
9.
10.
11.
12.
13.
Acknowledgements We would like to thank Human Anatomy Department of Miguel Hernandez University, for assistance in preparing cadaver and Jose ´ Sanchez-Paya, MD, PhD, for assistance with the statistical analysis.
14.
15.
16. 17.
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Anatomic variations and technical problems of the anterolateral thigh flap: A report of 74 cases. Plast Reconstr Surg 1998;102(5):1517–23. Kimura N. A microdissected thin tensor fasciae latae perforator flap. Plast Reconstr Surg 2002;109(1):69–77. Valdatta L, Tuinder S, Buoro M. Lateral circumflex femoral arterial system and perforator of the anterolateral thigh flap: An Anatomic Study. Ann Plast Surg 2002;49(2):145–50. Angrigiani C, Grilli D, Thorne CH. The adductor flap: A new method for transferring posterior and medial thigh skin. Plast Reconstr Surg 2001;107(7):1725–31. Conway H, Griffinth BH. Plastic surgery for closure of decubitus ulcers in patients with paraplegia. Am J Surg 1956;91:946. McCraw JB, Dibell DG, Carraway JH. Clinical definition of independent myocutaneous vascular territories. Plast Reconstr Surg 1977;60:341. James JH, Moir IH. The biceps femoris musculocutaneous flap in the repair of pressure sores around the hip. Plast Reconstr Surg 1980;66(5):736. Shanahan DA, George B, Williams NS, Sinnataneby CS, Riches DJ. The long head of the biceps femoris: Anatomic basis for its possible use in the construction of an electrically stimulated neonal sphinter. Plast Reconstr Surg 1993;92(2): 55–8. Rab M, et al. Basic anatomical investigation of semitendinosus and the long head of bı´ceps femoris muscle for their posible use in electrically stimulated neosphinter formation. Surg Radiol Anat 1997;19:13–15. Quaba AA, Chapman R, Hackett ME. Extended application of the bı´ceps femoris musculocutaneos flap. Plast Reconstr Surg 1988;81(1):94–105. Tobin GR, Sanders BP, Man D, Weiner LJ. The biceps femoris myocutaneous advancementent flap: A useful modification for ischial pressure ulcer reconstruction. Ann Plast Surg 1981;6:396. Romanes GJ. Cunningham’s textbook of anatomy. Oxford: Oxford University Press; 1981 p. 404–7. Maquelet AC, Gilbert A. An atlas of flaps in limb reconstruction.: Martin Dunitz; 1995 p. 107–10. Farouk O, Krettek C, Miclau T. The topography of the perforating vessels of the deep femoral artery. Clin Orthop 1999;368:255–9. Shanahan D, Jordan RK, Coulthard A, Cooper PN, Varma J. The intramuscular arterial anatomy of the long head of biceps femoris muscle. J Anat 1997;190(3):467–72. Hayashi A, Maruyama Y. Lateral intermuscular septum of the thigh and short head of the biceps femoris muscle: An anatomic investigation with new clinical applications. Plast Reconstr Surg 2001;108(6):1636–54. Hayashi A, Maruyama Y. Neurovascularized free short head of the biceps femoris muscle transfer for one-stage reanimation of facial paralysis. Plast Reconstr Surg 2005; 115(2):394–405.