The posterior interosseous artery in the distal part of the forearm. Is the term recurrent branch of the anterior interosseous artery justified?

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1 The British Association of Plastic Surgeons (2004) 57, The posterior interosseous artery in the distal part of the forearm. Is the term recurrent branch of the anterior interosseous artery justified? q Martin G. Hubmer a, *, Thomas Fasching b, Franz Haas a, Horst Koch a, Franz Schwarzl a, Andreas Weiglein b, Erwin Scharnagl a a Division of Plastic Surgery, Department of Surgery, University Medical Center, Auenbruggerplatz 29, 8036 Graz, Austria b Anatomical Institute, Medical University, Graz, Austria Received 30 December 2003; accepted 10 June 2004 KEYWORDS Posterior interosseous artery; Distal anastomosis; Choke anastomosis; Recurrent branch of the anterior interosseous artery Summary In 1993 Angrigiani raised the question as to whether the distal part of the posterior interosseous artery (AIP) is a recurrent branch of the anterior interosseous artery (AIA) and forms a choke anastomosis with the AIP in the middle of the forearm. A dissection study was conducted on 66 upper extremities to evaluate the diameters of the dorsal branch of the anterior interosseous artery, the anastomotic branch, the diameter of the posterior interosseous artery at the point of origin of the septocutaneous perforators in the middle of the forearm and the diameter of the posterior interosseous artery at the point of emergence in the dorsal compartment. We further tried to identify different forms and types of the distal anastomosis and the connections to the dorsal carpal arch and the ulnar artery. A distal anastomosis between the AIA and AIP was found in 65 of the 66 upper extremities. Three different types of anastomosis could be identified. The smallest diameter was found at the middle of the forearm (mean diameter AIA 1.28 mm; anastomotic branch 0.6 mm; AIP at the middle of the forearm 0.39 mm; AIP prox mm). A branch through the fifth extensor compartment was present in all of our specimens (mean diameter 0.54 mm). A branch through the forth extensor compartment could be found in 16 specimens. Based on our findings and the embryological development, we conclude that the AIP is only present in the proximal half of the forearm. In the distal part, the dorsal branch of the anterior interosseous artery forms a vascular arcade, which gives off branches to the dorsal carpal arch, the ulnar head and the ulnar artery. This arcade anastomoses with the posterior interosseous artery in the middle of the forearm by means of a choke anastomosis. We also conclude that the term recurrent branch of the anterior interosseous artery for the distal part of posterior interosseous artery is correct. Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. q Presented at the 40th Annual meeting of the Austria Society of Plastic, Reconstructive and Aesthetic Surgery, Salzburg, October 18 19, 2002 and First Joint Meeting of the EACA and AACA, Graz, July 7 11, *Corresponding author. Tel.: þ ; fax: þ address: martin.hubmer@uni-graz.at S /$ - see front matter Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. doi: /j.bjps

2 The posterior interosseous artery in the distal part of the forearm 639 The interosseous arteries of the forearm, especially the posterior interosseous artery (PIA) provide the vascular basis for both proximally and distally based flaps. These flaps are useful as island 1 9 or free flaps. As a distally based flap, the blood supply depends on the posterior interosseous artery in the distal two-thirds of the forearm and its anastomosis with the dorsal branch of the anterior interosseous artery. In clinical use and anatomical dissections, absence or hypoplasia of the PIA in the distal part of the forearm 1,2,5,7,9,17,29 and the absence of the anastomosis between the posterior and anterior interosseous arteries 1,10,16,31 have been encountered. Anatomical dissections and clinical cases have shown that the diameter of the posterior interosseous artery may narrow in the middle part of the forearm, whereas the diameter of the anastomotic branch of the anterior interosseous artery is larger. 7,18 Angrigiani 7 hypothesised that the posterior interosseous artery is only present in the proximal part of the forearm and the distal part is formed by a recurrent branch of the anterior interosseous artery connected to the PIA by a choke anastomosis. The aim of our study was to determine 1. The diameter of the PIA in the proximal, middle and distal forearm, and whether there is a choke anastomosis between the posterior and anterior interosseous artery in the middle of the forearm which would make term recurrent branch of the anterior interosseous artery justified? 2. The form and diameter of the vascular arch between the anterior and posterior interosseous artery near the ulnar head. 3. The connection of this vascular arch to the dorsal carpal arch and the ulnar artery. septum between the extensor digiti minimi (EDM) and the extensor carpi ulnaris (ECU) in the middle third of the forearm were identified and preserved. Following the perforators between the EDM and ECU, the dorsal interosseous artery was identified and dissected from its point of emergence in the dorsal compartment of the forearm to the wrist. At this level, the connection to the dorsal branch of the anterior interosseous artery, the dorsal carpal arch and the ulnar artery were identified. The diameters of the vessels were measured with a slide caliper. The measuring points (Fig. 1) were 1. at the point of emergence of the dorsal branch of the anterior interosseous artery 2. the apex of the anastomotic arch between the AIA and AIP 3. at the origin of the septocutaneous perforator or, in the case of two or more perforators, the origin of the most proximal perforator 4. at the point of emergence of the posterior interosseous artery in the dorsal compartment Results The length of the forearm, measured between the lateral epicondyle of the humerus and the styloid process of the ulna was 248 mm ( mm). The posterior interosseous artery was present in 65 out of 66 specimens. In one case there was a small vessel in the proximal aspect of the intermuscular septum between the EDM and ECU, which faded out quickly. At wrist level, a very prominent dorsal branch of the anterior interosseous artery (external diameter 1.6 mm) ran straight through the fifth dorsal extensor compartment to anastomose with Materials and methods Our study was conducted on 33 cadavers of both sexes, aged from 42 to 94 years, dissected on both sides (total of 66). The subjects were embalmed with Thiel s technique. Intra-arterial injection used a liquid glue mixed with minimum dye after the method of Spanner modified by Thiel. 19,20 This injection technique allows vessels to be followed down to a diameter of 0.1 mm. The dissection was as follows: the skin was incised along a line between the lateral epicondyle, the ulnar head and the base of the fifth metacarpal bone. The skin was raised in a subcutaneous plane. Septocutaneous perforators that emerged from the Figure 1 Measure points. P1: At the point of emergence of the dorsal branch of the anterior interosseous artery. P2: The apex of the anastomotic arch between the AIA and AIP. P3: At the origin of the septocutaneous perforator or, in the case of two or more perforators, the origin of the most proximal perforator. P4: At the point of emergence of the posterior interosseous artery in the dorsal compartment.

3 640 M.G. Hubmer et al. the proximal dorsal carpal arch. No septocutaneous perforators were found (Fig. 2). In 65 specimens, the posterior interosseous artery was located in the intermuscular septum between the EDM and ECU. In 62 cases (95%), the artery entered the posterior compartment of the forearm underneath the supinator muscle. In three (4.8%) cases a small vessel appeared at this point and split into several branches. One of these branches formed the ascending branch of the posterior interosseous artery; the others followed the path of the descending branch or entered the extensor muscles. One branch faded out in the septum between the EDM and the ECU. The descending branch of the PIA in a narrow sense originated from the anterior interosseous artery distal to the supinator muscle and passed between the extensor pollicis longus muscle and the extensor digitorum communis muscle to reach the posterior compartment. The length of the descending branch of the PIA between the anastomosis with the dorsal branch of the anterior interosseous artery and the point of emergence in the posterior compartment in these cases was 65 mm (75 55 mm), in the other 62 cases, 135 mm ( mm). The results of the measurements of the diameter of the arteries showed that the posterior interosseous artery had its smallest diameter at the point of origin of the perforator or most proximal septocutaneous perforator. From distal to proximal, the diameter decreased from 1.28 mm ( mm) at the point of emergence of the dorsal branch of the anterior interosseous artery on the dorsal side of the interosseous membrane to the anastomotic arch (0.6 mm, range mm) and the perforator (0.39 mm, range mm). The diameter of the posterior interosseous artery at its point of emergence in the dorsal compartment was 1.35 mm ( mm) (Table 1). At wrist level, an anastomosis between the posterior interosseous artery with the dorsal branch of the anterior interosseous artery could be found in 65 specimens (98%). This branch pierced the interosseous membrane 47.6 mm (30 65 mm) proximal to the styloid process of the ulna to form an arch with the posterior interosseous artery, located 35 mm (30 38 mm) proximal to the styloid process. This arch was located underneath the extensor tendons and in close relation to the interosseous membrane and the periosteum of the ulna in 64 cases; in one case the dorsal branch of the anterior interosseous artery crossed the extensor indicis proprius muscle dorsally and the extensor digiti minimi muscle volarly to anastomose with the dorsal interosseous artery (Fig. 3). Three different types of arches could be identified (Fig. 4). All specimens showed a branch through the fifth extensor compartment. Except in the case described above, this branch emerged from the anastomotic arch between AIA and AIP to anastomose with the dorsal carpal arch. The length of this branch was 37 mm (30 65 mm), with an external diameter of 0.54 mm ( mm). Other branches, which rose from the anastomotic arch, from the dorsal branch of the anterior interosseous artery or the branch through the fifth dorsal compartment supplied the periosteum of the radius or terminated at the base of the fourth extensor compartment. In 16 cases a branch passed through this compartment to terminate in the dorsal carpal arch. There were also branches to the periosteum of Figure 2 The posterior interosseous artery is only present in the proximal part of the forearm. There is no vascular arcade at wrist level, a very prominent dorsal branch of the anterior interosseous artery runs straight through the fifth dorsal compartment. Figure 3 The dorsal branch of the anterior interosseous artery crosses the extensor digitorum communis (EDC) dorsally and passes then the extensor indicis proprius (EIP) volarly. It then runs in the septum between the extensor digiti minimi (EDM) and the extensor carpi ulnaris to anastomose with the posterior interosseous artery.

4 The posterior interosseous artery in the distal part of the forearm 641 Table 1 Diameter of the artery at the different measure points P1 P2 P3 P4 Diameter 1.28 mm ( mm) 0.6 mm ( mm) 0.39 mm ( mm) 1.35 mm ( mm) the ulnar head emerging from this arch. In only six specimens could an anastomosis with the dorsal carpal arch be identified. In one case there was a connection between these branches and the ulnar artery. The dissection of the septocutaneous perforators in the middle of the forearm revealed one perforator in 31 cases (47%), two perforators in 21 cases (32%) and three in 13 cases (20%). These perforators originated from the posterior interosseous artery between 65 and 120 mm from the styloid process of the ulna. Figure 4 Different types of the vascular arch at wrist level. The branches through the forth dorsal compartment and to the radius are only shown in type A.

5 642 M.G. Hubmer et al. Discussion Descriptions of the origin, course, and general arrangement of the posterior interosseous artery can be found in the classical literature These descriptions also include the anastomosis with the dorsal branch of the anterior interosseous artery and the connections with the dorsal carpal arch. The form of this arch, the relation to the ulnar head, and the connections to the dorsal carpal arch, are, of course, of greater importance now that it is possible to harvest fasciocutaneous flaps based on the posterior interosseous artery. Furthermore, the connections through the extensor compartments between the interosseous arteries and the dorsal carpal arch, as shown by Sheetz, 30 can provide the vascular basis for pedicled bone grafts. Nonetheless, reports on the exact form and type of anastomosis between the posterior and anterior interosseous artery are rare. Bayon and Pho 31 described the length, diameter and distance to the wrist joint of the anastomotic branch and found it constant in 35 dissected specimens. This branch was absent in one case and in another case too small for transfer purpose, as Tonkin 10 also encountered in a clinical case. In a case report, Dadalt 16 reported the absence of the distal anastomosis and presented patterns of arrangement of this anastomosis. In our own dissections we found an anastomosis in 65 out of 66 specimens. In one specimen, the posterior interosseous artery was absent in the distal part of the forearm. The dorsal branch of the anterior interosseous artery was of large caliber and terminated in the dorsal carpal arch by passing through the fifth extensor compartment. This variation was described by Adachi 32 in one case in a series of 535 specimens. In another one of our dissection specimens, a distal anastomosis was present, but crossed the extensor indicis proprius muscle dorsally and the extensor digiti minimi volarly to form an arch with the posterior interosseous artery. The dorsal branch of the anterior interosseous artery terminated in the dorsal carpal arch. Despite the uncommon course of this arch, a distally based fasciocutaneous flap could have been raised. We were able to identify three different types of anastomosis, located 35 mm (30 38 mm) proximal to the styloid process of the ulna. In all of our specimens these anastomoses were provided by only one branch, which is in contrast to other descriptions. 9,16 The anatomy of these anastomoses may be described as an arch, which is formed by the dorsal branch of the anterior interosseous artery. It emerges on the dorsal face of the interosseous membrane 44 mm (30 55 mm) proximal to the styloid process. The diameter decreases from 1.28 mm ( mm) at the point of emergence to 0.6 mm ( mm) at the apex of this arch. Although the branch through the fifth extensor compartment, which could be found in all of our specimens, seems to continue the course of the dorsal branch of the anterior interosseous artery in Type A (Fig. 4), we believe that this vessel is a branch originating from this vascular arch. In contrast to Sheetz, 30 we could only find a branch through the fourth extensor compartment in 16 cases. Other branches that emerged from this arch supplied the periosteum of the ulnar head. In only seven cases could we find a connection between this vascular arch and the ulnar artery and the dorsal carpal arch, in contrast to the clinical series of Büchler and Frey, 5 who found a communicating branch in 50% of their cases. The posterior interosseous artery was present in 65 out of 66 specimens. In the middle third of the forearm, we were able to identify 1 3 septocutaneous perforators in a range between 65 and 120 mm proximal to the styloid process of the ulna. This pattern is close to the findings of Costa and Soutar 4,9 and Angrigiani. 7 In our series, however, one single perforator was only present in 31 specimens (47%) and located 90 mm proximal to the styloid process, which is more distal to the average midpoint of 124 mm in our forearms than the 1 2 cm reported by Angrigiani. 7 At the point of origin of this perforator or, in the case of two or three perforators at the origin of the most proximal perforator of this group, we found the smallest diameter of the posterior interosseous artery in the forearm. This is in accordance with the findings of Angrigiani and Pahl and Schmid. 7,18 The form and diameter of the vascular arcade at wrist level and the narrowing of the posterior interosseous artery would support the hypothesis that the anastomosis between the dorsal branch of the anterior interosseous artery and the posterior interosseous artery is situated in the middle third of the forearm in the form of a choke anastomosis, an interarterial connection, which has been described by Boyd and Taylor between the deep inferior epigastric artery and the arteries of the intercostal system. 33,34 The posterior interosseous artery proper is only present in the proximal part of the forearm. The part of the dorsal interosseous arterial system, which has always been described as the anastomosis between the anterior and posterior interosseous artery would therefore be the recurrent branch of the anterior interosseous

6 The posterior interosseous artery in the distal part of the forearm 643 artery. This model of an interarterial choke connection in the forearm would explain the clinical observation by Büchler, 5 that tissue necrosis in a distally based posterior interosseous flap correlates with the delay in perfusion after release of the torniquet. A terminology decision should rely not only on classic dissection studies, but should also take embryological development into account. There are, however, no reports of the development of the posterior interosseous artery in the distal part of the forearm alone. According to the current theory, shown in almost any textbook, vascular development of the limb is a result of an angiogenic sprouting mechanism. It starts at stage 12 by the ingrowth of a capillary plexus in the limb bud. In the later stages, only one axial artery supplies the limb and terminates in a capillary plexus. In the forearm, this axial artery represents the anterior interosseous artery. A branch from the main trunk passes dorsally to form the posterior interosseous artery. This branch fades out in the middle of the forearm and does not contribute to the blood supply of the palmar arch. A second branch accompanies the median nerve. This median artery becomes the main artery of the forearm in the following stages, until the ulnar and finally the radial artery reaches the palm and the arterial pattern achieves its definitive morphology (Stage 21 23). This theory, however, has been called in question by the findings of Rodriguez-Niedenführ, 40 who suggested that the arterial pattern of the upper limb develops from an initial capillary plexus by a proximal to distal differentiation due to maintenance, enlargement, and differentiation of certain capillary vessels, and the regression of others. No matter which theory is correct, both can explain the types and forms of the vascular arch (and its absence), the choke anastomosis and the hypoplasia or aplasia of the posterior interosseous artery. Following the first theory, the arcade and the recurrent branch of the anterior interosseous artery are the result of a sprouting of this vessel from the dominant axial vessel in the first stages of vascular development. This vessel anastomoses with the posterior interosseous artery, which is also a branch of the anterior interosseous artery. According to the second theory, the final arterial pattern is the result of a process of enlargement and regression, leading to a smaller diameter of the vessel in the middle of the forearm. Based on our findings and the embryological development, we conclude that the posterior interosseous vascular system consists of a dual longitudinal system. The posterior interosseous artery itself is only present in the proximal half of the forearm. In the distal part, the dorsal branch of the anterior interosseous artery forms a vascular arcade, which gives off branches to the dorsal carpal arch, the ulnar head and the ulnar artery. In our series, the branch through the fifth extensor compartment was the most constant. The arcade anastomoses with the posterior interosseous artery by means of a choke anastomosis. This anastomosis is located at the origin of the most proximal perforator of the septocutaneous perforators at mid-forearm. We conclude that the term recurrent branch of the anterior interosseous artery for the part between the arcade and the posterior interosseous artery is correct. References 1. Penteado CV, Masquelet AC, Chevrel JP. The anatomic basis of the fasciocutaneous flap of the posterior interosseous artery. Surg Radiol Anat 1986;8: Masquelet AC, Penteado CV. Le Lambeau interosseux posterieur. Ann Chir Main 1987;6: Zancolli EA, Angrigiani C. Posterior interosseus island forearm flap. J Hand Surg 1988;13B: Costa H, Soutar DS. The distally based island posterior interosseous flap. Br J Plast Surg 1988;41: Büchler U, Frey HP. Retrograde posterior interosseous flap. J Hand Surg 1991;16A: Landi A, Luchetti R, Soragni O, De Santis G, Sacchetti GL. The distally based posterior interosseous island flap for the coverage of skin loss of the hand. Ann Plast Surg 1991;27: Angrigiani C, Grilli D, Dominikow D, Zancolli EA. Posterior interosseous reverse forearm flap: experience with 80 consecutive cases. Plast Reconstr Surg 1993;92: Mazzer N, Barbieri CH, Cortez M. The posterior interosseous forearm island flap for skin defects in the hand and elbow. A prospective study of 51 cases. J Hand Surg 1996;21B: Costa H, Garcia L, Vranchx J, Cunha C, Conde A, Soutar D. The posterior interosseous flap: a review of 81 clinical cases and 100 anatomical dissections assessment of indications in reconstruction of hand defects. Br J Plast Surg 2001;54: Tonkin MA, Stern H. The posterior interosseous artery free flap. J Hand Surg 1989;14B: Chen H, Tan Y, Chuang D, Wei F, Noordhoff MS. Microvascular free posterior interosseous flap and comparison with the pedicled posterior interosseous flap. Ann Plast Surg 1996;36: Shibata M, Iwabuchi Y, Kubota S, Matsuzaki H. Comparison of free and reversed pedicled posterior interosseous cutaneous flaps. Plast Reconstr Surg 1997;99: Park JJ, Kim JS, Chung JI. Posterior interosseous free flap: various types. Plast Reconstr Surg 1997;100: Chen H, Cheng M, Schneeberger AG, Cheng T, Wei F, Tang Y. Posterior interosseous flap and its variations for coverage of hand wounds. J Trauma 1998;45: Cavadas PC. Posterior interosseous free flap with extended pedicle for hand reconstruction. Plast Reconstr Surg 2001; 108: Dadalt LG, Ulson HJR, Penteado CV. Absence of the

7 644 M.G. Hubmer et al. anastomosis between the anterior and posterior interosseous arteries in a posterior interosseous flap: a case report. J Hand Surg 1994;19A: Giunta R, Lukas B. Impossible harvest of the posterior interosseous artery flap: a report of an individualized salvage procedure. Br J Plast Surg 1998;51: Pahl St, Schmidt HM. Klinische Anatomie der interossären Arterien des Unterarmes. Handchir Mikrochir Plast Chir 1994;26: Thiel W. Die Konservierung ganzer Leichen in natürlichen Farben. Ann Anat 1992;174: Thiel W. Eine Arterienmasse zur Nachinjektion bei der Konservierung ganzer Leichen. Ann Anat 1992;174: Pierer G, Steffen J, Hoflehner H. The vascular blood supply of the second metacarpal bone: anatomic basis for a new vascularized bone graft in hand surgery. Surg Radiol Anat 1992;14: Weiglein AH, Haas F, Pierer G. Anatomic basis of the lower trapezius musculocutaneous flap. Surg Radiol Anat 1996;18: Haas F, Rappl T, Koch H, Pittler P, Scharnagl E. Free osteocutaneous lateral arm flap: anatomy and clinical applications. Microsurgery 2003;23: Gray H. Anatomy, descriptive and surgical. Philadelphia: Henry C. Lae; pp Henle J. Grundriss der Anatomie des Menschen. Text. Braunschweig: Friedrich Vieweg und Sohn; pp Henle J. Grundriss der Anatomie des Menschen. Atlas. Braunschweig: Friedrich Vieweg und Sohn; pp Testut L. Traité d anatomie humaine. Tome deuxiéme. Paris: Charles Hérissey; pp Testut L. Tratado de anatomía humana, Octava edicion. Tomo segundo, Barcelona: Salvat Editores; pp Valdecasas-Huelin JMG, Barriero FJJ, Barcia EC. Etude radio anatomique des artères interosseuses. Acta Anat 1978;102: Sheetz KK, Bishop AT, Berger RA. The arterial blood supply of the distal radius and ulna and its potential use in vascularized pedicled bone grafts. J Hand Surg 1995;20A: Bayon P, Pho RWH. Anatomical basis of the dorsal forearm flap. J Hand Sug 1988;13B: Adachi B. Das Arteriensystem der Japaner. Band 1. Kyoto: Maruzen; pp Boyd JB, Taylor GI, Corlett RJ. The vascular territories of the superior epigastric and the deep inferior epigastric systems. Plast Reconstr Surg 1984;73: Taylor GI, Corlett RJ, Boyd JB. The versatile deep inferior epigastric (inferior rectus abdominis) flap. Br J Plast Surg 1984;37: Evans HM. Die Entwicklung des Blutes, des Gefäßsystems und der Milz. In: Keibel L, Mall FP, editors. Handbuch der Entwicklungsgeschichte des Menschen. Leipzig: S. Hirzel; p Lippert H, Papst R. Arterial variations in man. Classification and frequency. München: J.F. Bergmann; pp Schmidt HM, Lanz U. Chirurgische Anatomie der Hand. Stuttgart: Hippokrates; pp O Rahilly R, Müller F. Human embryology and teratology. New York: Wiley; pp Williams PL. Gray s anatomy, 38th ed. New York: Churchill Livingstone; pp Rodriguez-Niedenführ M, Burton GJ, Deu J, Sañudo JR. Development of the arterial pattern in the upper limb of staged human embryos: normal development and anatomic variations. J Anat 2001;199:

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