Physical Address
304 North Cardinal St.
Dorchester Center, MA 02124
This chapter provides an overview of the angiosome concept and reviews the vascular anatomy of the body. The historical perspective summarizes the major progress in understanding the vascular basis and clinical applications of flaps in reconstructive surgery.
The anatomical basis of angiosomes, choke anastomotic vessels, arterial territories, and venous drainage of the human body are summarized. The neurovascular territories of skin and muscle are described. Comparisons with other species highlights the consistent features of vascular anatomy of the human body and illustrates the need to be aware of the vascular anatomy of animal flap models.
The vascular anatomy of skin, muscle, and bone of each region of the body is discussed with an emphasis on flap design, avoiding surgical complications and providing an overview of angiosomes of the body.
The general concepts of the vascular supply to tissues of the body are reviewed. The importance of these concepts to flap design is highlighted with clinical examples. These concepts also provide the basis for interpreting physiologic and pathologic events in skin flaps.
The overall architecture of the vasculature of the human body is consistent but there is significant variability in individual perforator anatomy. Therefore, a versatile operative plan is needed for successful flap design.
Methods of preoperative assessment of vascular anatomy and types of flaps, including skin, fasciocutaneous, musculocutaneous and perforator flaps, are reviewed.
The anatomic basis of the delay phenomenon and procedure is explored.
Access video lecture content for this chapter online at Elsevier eBooks+
The angiosome theory has become well accepted in the field of plastic and reconstructive surgery and allows the conceptualization of the vascular supply to all tissues of the human body. An angiosome is a composite block of tissue supplied by a main source vessel. The adjacent angiosomes are linked either by reduced-caliber choke anastomotic vessels or vessels without reduction in caliber – the true anastomoses of adjacent arterioles. The latter are seen in many muscles or in the skin, especially where vessels accompany cutaneous nerves. Flaps designed along an axis of vessels linked by true anastomoses have a longer survival length similar to a flap that has been delayed. The anastomotic arteries are matched by veins devoid of valves that allow bidirectional flow. The entire human body consists of innumerable arcades of interconnecting vessels which supply all tissues ( ).
In 1977, Converse stated that “there is no simple and all-encompassing system which is suitable for classifying skin flaps”. It is now generally agreed that the anatomical vascular basis of the flap provides the most accurate approach for classification. Specific, anatomically based nomenclature simplifies communication between surgeons and allows for the advancement of the field of plastic and reconstructive surgery. The main named source vessels throughout the body provide a useful road map for the description of flaps.
The vascular architecture of the body is arranged anatomically as a continuous series of vascular loops, like the tiers of a Roman aqueduct, that increase in number while their size and caliber decrease as they approach the capillary bed ( Fig. 23.1 ). The reverse situation occurs on the venous side. This anatomic arrangement of the vascular “skeleton” is shown beautifully in the corrosion cast studies of newborn babies performed by Tompsett that reside in the Hunterian Museum at the Royal College of Surgeons in London ( Fig. 23.2 ). Note how the main arterial loops hug the bony framework and the secondary arcades follow the intermuscular and intramuscular connective tissue framework. The “keystones” of these arcades are represented usually by reduced-caliber (choke anastomotic) arteries and arterioles, matched on the venous side by avalvular (oscillating) veins that permit bidirectional flow. Choke arteries and avalvular veins have an essential role in controlling this pressure gradient across the capillary bed (see Fig. 23.1 ).
The angiosome (from the Greek angeion , meaning vessel, and somite , meaning segment or sector of the body derived from soma , body) is defined as a composite block of tissue supplied by a main source artery. The source arteries (segmental or distributing arteries) that supply these blocks of tissue are responsible for the supply of the skin and the underlying deep structures. When pieced together like a jigsaw puzzle, they constitute the three-dimensional vascular territories of the body. In this section we present the basis of the anatomical studies which are the foundation of the angiosome concept.
The angiographic studies produced by Salmon using lead oxide, gelatin, and water were exceptional; however, modifications of the technique have further improved results. In particular, reducing the concentration of lead oxide has improved computed tomographic (CT) angiographic anatomic studies. A review of vascular injection techniques reveals the wide array of techniques available for investigation.
Initially, cadaver injection studies to study the vascular anatomy of the human integument and other structures utilized intra-arterial injections of radiopaque substances such as barium sulfate or lead oxide or visible substances such as latex and ink. Depending on the specific study, the area of tissue of interest was then dissected and radiographed. As the radiographic film quality improved, the quality of the image of the small blood vessels improved. However, studies using simple radiographs have largely been replaced by CT techniques. These investigations were conducted in fresh cadavers. In the majority of studies, the anatomical question was problem-oriented in a desire to provide a surgical solution to the individual patient's needs. We have performed a large number of fresh cadaver studies, investigating various regions, tissues, and combinations of tissues. This has included an investigation of the entire integument and underlying deep structures in a series of total body studies of the arteries, which led to the angiosome concept, discussed in detail in a later section. This was followed by studies of the veins and the neurovascular territories of the body and detailed studies of the angiosomes of the forearm, the leg, and the head and neck, as well as a comparative study of a series of mammals. As well, we have performed detailed analyses of numerous muscle flaps, including sartorius, rectus femoris, gracilis, pectoralis major, and skin flaps, including the reversed sural artery flap, thoracodorsal artery perforator flap, profunda femoris artery perforator flap, and the superior and inferior gluteal artery perforator flaps.
The investigations initially involved an analysis of various regions of the body to define possible donor sites for free skin flap transfer. The studies subsequently focused on other tissues and included the anatomic basis for the transfer of bone, nerve, and certain muscles. Encouraged by the success of some of the resulting clinical procedures, the authors expanded the research to investigate composite units of tissue, supplied by a single vascular system. Units of skin and tendon, muscle with nerve, and skin, muscle, and bone were analyzed. It was from this work that the angiosome concept germinated. Various regions, including the anterior abdominal wall, the anterior thorax, the lower limb, and the upper limb, were studied. The results added strength to the angiosome concept of the blood supply and revealed the interconnections that exist at all levels between adjacent vascular territories, a relationship that is evident throughout the body.
In cadaver vascular research, various techniques can be used to identify and study the area of interest. In the past, the integument (skin and subcutaneous tissue) was removed, and the sites of emergence of the dominant cutaneous perforators (0.5 mm diameter or more) were identified on the surface of the deep fascia with lead beads. Currently, individual perforators are easily identified on CT angiography (CTA). Approximately 400 cutaneous perforators on average were identified per body. The three-dimensional branching pattern of main source vessels can be identified. Previous workers, including Salmon, had made topographic boundary incisions to remove areas of skin, particularly in the lines of the groins, axillae, neck, and limb joints ( Fig. 23.5 ). These junctional regions are of great clinical importance, and for this reason the incisions were designed to retain their continuity wherever possible. In our current techniques, using CTA, the incisions utilized for dissection are not as crucial since the pathway and branches of individual vessels are clearly documented prior to dissection.
In the original studies of the vascular supply of tissues of the body, the integument was radiographed, and a montage of the entire cutaneous circulation was constructed in “plan view” ( Fig. 23.6 , Fig. 23.7 ). Although Manchot and Salmon described the origin and course of the cutaneous arteries, and Salmon made a separate study of the individual muscles, neither worker illustrated the course of the arteries between the deep tissues and the skin. Therefore, the skin and subcutaneous tissues were cut into parallel strips and placed on their side, and radiographs were taken to provide “elevation views” of the vessels in different regions of the body ( Fig. 23.8 ). Current CTA techniques allow a far more detailed three-dimensional appraisal of the vascular anatomy of tissues ( Fig. 23.9 ).
All cutaneous perforators of diameter greater than 0.5 mm were traced to their underlying source arteries. The results were averaged from each cadaveric study and plotted on a diagram of the body ( Fig. 23.10 ). Subsequently, investigations were expanded to map out the venous territories (venosomes) of the body along with the neurovascular territories of the skin and muscle. These results have led to an overall picture of the vascular territories of the entire body. The remainder of this section gives a brief overview of the arterial, venous, and nervous territories of the body.
Plastic surgery evolved as a specialty in Europe and North America to restore the mutilated victims of the two World Wars. With artistic flair and geometric precision, tissues were advanced and rotated. These random flaps were transposed locally and dispatched to distant sites on limb carriers, only to be rebuffed on occasion by necrosis. Gillies often lamented that “plastic surgery is a constant battle between blood supply and beauty”. Gradually, rigid length-to-breadth flap ratios were calculated for different regions of the body because most of the flaps were designed without a precise knowledge or appreciation of the vascular supply of flaps. The flaps designed were “random” since it was not appreciated that the vascular supply was crucial to flap survival and there was little understanding of the anatomy of the underlying vasculature.
Unfortunately, this anatomic information was available but overlooked. In 1889, Manchot performed the first examination of the vascular supply of the human integument. His treatise, Die Hautarterien des menschlichen Körpers [The Cutaneous Arteries of the Human Body] , was initially published in German and later translated to English. Manchot identified the cutaneous perforators, assigned them to their underlying source vessels, and charted the cutaneous vascular territories of the body ( Fig. 23.3 ). He did not have the advantage of radiography since Röentgen was not to make his discovery until several years later. Nevertheless, the accuracy of Manchot's work has mostly stood the test of time.
In 1893, Spalteholz published an important paper on the origin, course, and distribution of the cutaneous perforators in adult and neonatal cadavers. He performed arterial injections of gelatin and various pigments. The soft tissues were fixed in alcohol and subtracted in xylol, and the resulting vascular network was embedded in Canada Balsam. Spalteholz's main study concentrated on the detailed circulation of the skin. He made an important distinction between direct cutaneous vessels, which supply the skin, and indirect cutaneous vessels, which are terminal branches of vessels supplying the deeper organs, especially the muscles. A detailed account of this work was published by Timmons in a review of the landmarks in the anatomic study of the skin's blood supply.
The next major study was performed by Salmon, a French anatomist and surgeon in the 1930s. Manchot had defined approximately 40 cutaneous territories that excluded the head, neck, hands, and feet. Salmon knew of Manchot's studies and set out to reappraise his work. Aided by radiography, he was able to delineate the smaller vessels of the cutaneous circulation and charted more than 80 territories encompassing the entire body ( Fig. 23.4 ). Salmon noted the interconnections that exist between perforators, and his observation of the density and size of the vessels in different regions of the body led him to define what he called the hypervascular and hypovascular zones. His work has become available in English. Ironically, in the preface to Michel Salmon's book on the cutaneous vascular anatomy published originally in 1936, Raymond Grégoire stated: “This new work by Michel Salmon is a painstaking study that no surgeon from now on can ignore and few anatomists would have had the courage to undertake.” Indeed, if we had heeded this advice, plastic surgery would have evolved much earlier!
In 1975, Schafer published an important study on the arterial and venous anatomy of the lower extremity. Scribtol and an ink–serum mixture were injected into the lower limbs of adults and into the entire circulation of fetal and neonatal cadavers. Schafer concluded that most cutaneous arteries emerge in rows from the intermuscular septa or occasionally from the intramuscular septa. In addition, he highlighted the two systems of perforating veins: the venae communicantes, large veins that pierce the deep fascia and connect the superficial venous plexus to the deep venous system; and the venae comitantes, small, usually paired veins that accompany the cutaneous arterial perforators.
Early last century, advances on the clinical front gave significance to the work of these great anatomists. In 1906, Tansini reported a latissimus dorsi flap supplied by the thoracodorsal artery. In 1919, Davis published Plastic Surgery and introduced many of the chapters with illustrations from Manchot's book. In 1921, Blair described a forehead flap based on the superficial temporal vessels, and in 1929, Esser published Artery Flaps . In 1937, Webster again cited the work of Manchot when he described a long, bipedicled thoracoepigastric flap based on named arteries that extended from the groin to the axilla. Shaw and Payne used the clinical information available in wartime to provide one-stage direct flaps for hand reconstruction. In 1965, Bakamjian drew attention to the long paramedian perforators of the internal thoracic system.
The 1970s witnessed the beginning of the “anatomic revolution”. McGregor and Morgan differentiated between large flaps based on a known axial blood supply and those based on random vessels. Daniel and Williams reappraised the work of Manchot and others and classified the cutaneous arteries into direct cutaneous and musculocutaneous vessels.
Studies on the free flap by Taylor and Daniel were published in 1973, and a few years later the musculocutaneous flap was revived by McCraw and Mathes and Nahai. Both procedures demanded a precise knowledge of the vascular supply of the tissue transfers. In the search for new donor sites for tissue transfer, surgeons returned to the dissection room. In the 1980s the pedicled musculocutaneous flap and the free microvascular transfer gained popularity and their use became common. However, on occasion there was a tendency for the techniques to neglect the aesthetic side of plastic surgery. The results could sometimes be what McDowell described as “globs and blobs”.
To escape from the hamburger of muscle and skin, surgeons soon rediscovered that blood vessels follow fascial planes and, starting in the 1980s, there was a much greater awareness of the fasciocutaneous flap. With this development, there has been an explosion of new terms and new classifications of the cutaneous circulation. The thesaurus of flaps now includes a bewildering array of terms including axial, random, direct cutaneous, musculocutaneous, fasciocutaneous, supercutaneous, septocutaneous, chimeric, retrograde, antegrade, and perforator. Indeed, there has been an attempt to classify flaps into no less than 10 types and subtypes on the basis of the origin of the cutaneous perforators. In many ways, these flap classification terms are simply different expressions of the basic cutaneous architecture that Manchot published in 1889 and Salmon reported in 1936. In an effort to standardize the literature and add clarity to descriptions of flaps, we have previously suggested using the name of the main source vessel to define the flap. Cormack and Lamberty published a book, The Arterial Anatomy of Skin Flaps , that contains a concise appraisal of the history, anatomy, and clinical aspects of skin flap surgery. The relationship of vessel size to vascular territory and axiality of vessels in the fasciocutaneous system has also been described by Cormack and Lamberty.
The vertical rectus abdominis musculocutaneous flap was described by Michael Drever in 1977. The transverse rectus abdominis muscle (TRAM) flap reported initially by Hartrampf et al . demonstrated that the skin paddle survives based on the musculocutaneous perforators of the superior epigastric vessels. The pedicled and, later, the free TRAM flap became very popular for postmastectomy breast reconstruction. As the anatomy of the musculocutaneous perforators became better understood, surgeons harvested less of the rectus abdominis muscle in order to preserve function of the muscle. Investigators pushed the boundaries once again with the rediscovery of the perforator flap, whereby a large abdominal skin flap can be raised with preservation of the underlying rectus muscle and hence reduce the potential problems of an abdominal incisional hernia and abdominal wall weakness. This gradual change in flap design gave rise to the deep inferior epigastric artery perforator (DIEAP) flap based on perforators of the deep inferior epigastric vessels. This evolution of autogenous reconstruction of the breast – from pedicled TRAM flap, to free TRAM flap, to muscle-sparing free TRAM flaps, to DIEAP flaps – reflects a greater awareness of the precise anatomy of the underlying musculocutaneous perforators and an attempt to reduce donor site morbidity and improve results. As knowledge of individual perforators to the skin improved, the spectrum of flap options increased dramatically. There has been a virtual explosion in published surgical work regarding perforator flaps.
The recent enthusiasm for perforator flaps has heightened awareness of the vascular supply to tissues of the body. Instead of 10–20 named arterial flaps in the body we now have a vast array of flap options based on any one of the over 400 arterial perforators of the body. This heightened awareness has led to greater understanding of the seemingly infinite possibilities for customized flap options.
The arterial network of the body forms a continuous interlocking arcade of vessels throughout each tissue and throughout the body, linked by reduced caliber choke anastomotic vessels or true anastomoses. The course of the cutaneous perforators depends on the proximity of the source artery to the undersurface of the deep fascia. As Michel Salmon noted in 1936, arteries supply branches to each tissue that they pass, including the intermuscular septae, fascia, nerves, and tendons. Arteries generally fall into two groups, direct and indirect ( Fig. 23.11 ). In our anatomical dissections, it is clear that there is great variability in the exact course and size of individual perforators; however, the main source vessels are relatively consistent. The direct cutaneous vessels pass between the deep tissues before piercing the outer layer of the deep fascia. They are usually the primary cutaneous vessels and their main destination is the skin. They tend to supply the skin with larger-diameter vessels, which have a large vascular territory (e.g., circumflex scapular artery). The direct branches include direct cutaneous vessels (sometimes called axial vessels) and septocutaneous vessels. The indirect vessels can be considered the secondary cutaneous supply. They emerge from the deep fascia as terminal branches of arteries which supply the muscles and other deep tissues. The majority of indirect branches are musculocutaneous perforators which emerge to supply the skin. In fact, there is usually significant variability in the distribution of direct and indirect vessels and their vascular territory from individual to individual. There is a vast interconnected network of direct and indirect arteries which supply the skin. The vascular territories of individual perforators vary and tend to be reciprocal with adjacent arterial vascular territories according to the so-called law of equilibrium, described by Salmon and supported by our work.
The direct cutaneous vessels arise from: (1) source arteries just beneath the deep fascia (e.g., the superficial inferior epigastric artery); (2) direct continuation of the source artery (e.g., the cutaneous branches of the external carotid artery); (3) deeply situated source artery or one of its branches to a muscle; they follow the intermuscular septa to the surface (e.g., septocutaneous branches of the lateral circumflex femoral artery). Indirect cutaneous vessels generally emerge from the main source artery as it courses on the undersurface of a muscle and penetrate through the muscle; e.g., musculocutaneous perforators of the deep inferior epigastric arteries (DIEA). In the human body, there are approximately 400 perforators, about 40% of vessels are direct and 60% indirect perforators.
The direct cutaneous perforators pierce the deep fascia near where it is anchored to bone or the intermuscular and intramuscular septa (see Fig. 23.10 ). These lines and zones of fixation also correspond to the fixed skin areas of the body. From these points, the vessels flow toward the convexities of the body surface, branching within the integument. In general, the wider the distance between the cavities and the higher the summit, the longer the vessel (see Fig. 23.8 ). The size and density of the direct perforators also vary in different regions. For example, in the head, neck, torso, arm, and thigh, the vessels are larger, longer, and less numerous. In the forearm, leg, and dorsum of the hands and feet, the vessels tend to be smaller, shorter, and more numerous. In the palms of the hands and the soles of the feet, where the skin is fixed, there is a high density of smaller perforators. Hence, the primary supply of each cutaneous territory varies between source arteries. Each of these territories also has indirect perforators.
The course of the cutaneous perforators between the deep fascia and the skin also varies in different regions. Regardless of their site, however, they follow the connective tissue framework of the superficial fascia, interconnecting at all levels. They ramify on the undersurface of the subcutaneous fat adjacent to the deep fascia and then branch and course toward the subdermal plexus, working their way between the fat lobules. The smaller vessels tend to course vertically toward the skin, whereas the larger vessels branch in all directions in a stellate pattern or course in a particular axis, branching as they pass parallel to the skin surface.
In the scalp and limbs, where the skin is relatively fixed to the deep fascia, the larger vessels hug that surface. They course on the deep fascia for a considerable distance in the loose areolar layer that separates them from the subcutaneous fat (see Fig. 23.8 ). This is especially true when a perforator accompanies a cutaneous nerve.
In the loose skin areas of the body, the direct cutaneous vessels course for a variable distance parallel to the deep fascia. They are more intimately related to the undersurface of the subcutaneous fat, however, being plastered to it by a thin fascial sheet that separates them on their deep surface from a plexus of smaller vessels. This plexus lies in loose areolar tissue on the surface of the deep fascia. It is formed by branches that arise from the direct perforators as they pierce the deep fascia and the connections these branches make with smaller indirect perforators. The large direct perforators then pierce the subcutaneous layer. They ascend within the superficial fascia (subcutaneous fat) to reach the rich subdermal plexus, where they travel for considerable distances (see Fig. 23.8 ).
Within the deep tissue, whether muscle, tendon, nerve, or bone, a pattern similar to that in the integument exists, with a three-dimensional network of vessels interlinking between vascular territories, the perimeters of which are linked by choke arteries. Within the muscles, these choke vessels often exhibit a characteristic corkscrew appearance on angiography.
The cutaneous veins also form a three-dimensional plexus of interconnecting channels throughout the body ( Fig. 23.12 ). There are valved segments in which valves direct flow in a particular direction, and there are avalvular segments where no valves are present. The avalvular or oscillating veins allow bidirectional flow between adjacent venous territories. They connect veins whose valves may be oriented in opposite directions, thus providing for the equilibration of flow and pressure. Indeed, there are many veins whose valves direct flow initially in a distal direction, away from the heart, before joining veins whose flow is proximal. An example of this is the superficial inferior epigastric vein that drains the lower abdominal wall integument toward the groin. In some regions, valved channels direct flow radially away from a plexus of avalvular veins, for example, in the venous drainage of the nipple–areola complex. In other areas, valved channels direct flow toward a central focus, as seen in the stellate branches of the cutaneous perforating veins of the limbs.
In general, venous anatomy parallels arterial anatomy ( Fig. 23.13 ). From dermal and subdermal venous plexuses, the veins collect either into horizontal large-caliber veins, where they often relate to cutaneous nerves and a longitudinal system of chain-linked arteries, or alternatively in centrifugal or stellate fashion into a common channel that passes vertically down in company with the cutaneous arteries to pierce the deep fascia. Thereafter, the veins travel with the direct and indirect cutaneous arteries, draining ultimately into the venae comitantes of the source arteries in the deep tissue.
In general, the origin, course, and distribution of the deep veins (vena comitantes) are a mirror image of the deep source arteries, but they are larger and more plentiful. Although the anatomy of the veins is subject to considerable variation between sides in the same individual as well as between other individuals, the pattern of venous arcades is evident throughout. These arcades generally become smaller and more numerous as the periphery of the region or the tissue is reached. The superficial veins, however, are independent of the deep arteries (e.g., greater saphenous vein, cephalic vein) and may have a different area of drainage. For example, in the forearm there are paired vena comitantes to the radial and ulnar arteries but a separate system of large-caliber subcutaneous veins, including cephalic, basilic, and antebrachial veins.
The site and density of the valves within the deep venous network are variable. The deep veins follow the bony skeleton of the body or the intermuscular septa with their associated arteries. In some regions, these veins are single; in others, they are duplicated as venae comitantes. In the limbs, the veins commence distally in the hands and feet as single channels linked by venous arcades. These arcades become progressively larger as they approach the wrist and ankle. The veins are duplicated in the forearm and leg, and each pair of veins is linked by a rich stepladder of venous channels that are usually free of valves. These venae comitantes then reunite to form single channels. In the lower limb, this occurs in the popliteal fossa, but in the upper limb, the union is most commonly in the proximal arm or even as high as the axilla.
In the torso, the pattern of arcades is conspicuous (see Fig. 23.13 ); the parent veins are oriented as longitudinal and transverse arcades that match the pattern of the source artery. Distinct territories are evident. Where choke arteries define the arterial territories, they are matched by oscillating veins in the venous network. The existence of venae comitantes is variable.
Within the muscle, the intramuscular venous network mirrors that of the arterial side. Where arterial territories are linked by choke arteries or true anastomotic arteries without changing caliber, the venous territories of the muscles, which drain in opposite directions, are linked by avalvular oscillating veins. Broadly, the muscles can be classified into three types on the basis of their venous architecture. Type I muscles have a single venous territory that drains in one direction. Type II muscles have two territories that drain from the oscillating vein in opposite directions. Type III muscles consist of three or more venous territories that drain in multiple directions ( Fig. 23.14 ).
The extramuscular veins are of two types. The first group consists of the efferent veins. They contain valves and drain the muscles to their parent veins. The other group consists of the afferent veins. They are derived from the overlying integument as musculocutaneous perforators or from adjacent muscles (see Fig. 23.14 ).
In our anatomical studies of neurovascular territories, fresh human cadavers were injected with a radiopaque lead oxide mixture, and the nerves were dissected and labeled with fine computer wire. The nerves and vessels were then segregated by subtraction angiography.
The most obvious feature seen throughout the skin and muscle is the linear arrangement of the nerves and their branches, compared with the looping arcades of the interconnecting vessel network, with the nerves taking the shortest route between two points. In general, the orientation of cutaneous nerves is longitudinal in the limbs, transverse or oblique in the torso, and radiating from loci in the head and neck. Of particular note is that the cutaneous nerves, like the arteries, pierce the deep fascia at fixed skin sites.
Each cutaneous nerve is accompanied by an artery, but the relationship is variable. Some of the arrangements seen in the integument are shown in Fig. 23.15 . In each case, either a long artery or a chain-linked system of arteries “hitchhikes” with the nerve.
When the cutaneous nerve and artery appear at the deep fascia together, their relationship is often established early (e.g., the lateral intercostal neurovascular perforators on the torso or the saphenous system in the lower limb). However, the nerve sometimes pierces the deep fascia at a point remote from the emergence of its associated artery (e.g., the lateral cutaneous nerve of the thigh and the superficial circumflex iliac artery below the inguinal ligament; Fig. 23.16 ). Alternatively, the nerve leaves one vascular system with which it is traveling in parallel to cross the path of another (e.g., the lateral intercostal nerve, which courses initially with its artery and then leaves it to meet the superficial inferior epigastric vessel). In many of these cases, secondary or tertiary branches of the artery often peel off to accompany the nerve (see Fig. 23.16 ). Sunderland noted that each peripheral nerve is abundantly vascularized by a “vascular net” of a series of nutrient arteries entering the nerve at different levels.
The vascular architecture of the intramuscular veins and arteries is almost identical for each muscle. Therefore, to simplify the description of the nervous supply to the muscles, only the arterial relations of the nerves are discussed and illustrated. The intramuscular branches of the nerves were dissected to, but not within, the individual muscle bundles. The following observations were made:
The nerves follow the connective tissue framework. Dissection showed the motor nerves coursing in the connective tissue sheath from its origin at the nerve trunk to the neurovascular hilum of the muscle. Thereafter, the nerve and its branches follow the intramuscular connective tissue to reach the muscle bundles.
The nerves are economical. As in the integument, the direct course of the motor nerves is in stark contrast to the wandering pattern of the vessels. The nerves take the shortest extramuscular and intramuscular routes compatible with the function of each muscle.
Neurovascular relations vary with the muscle, the extramuscular course, and the intramuscular branching of the nerves and the vessels. Some muscles have a single nerve supply; others receive multiple motor branches. All receive multiple arterial pedicles. However, despite the variables, certain observations can be made:
Each motor nerve is accompanied by a vascular pedicle, but the reverse does not apply.
The motor nerve is usually accompanied by the dominant vascular pedicle. There are exceptions to this, however. For example, the nerve supply to sternocleidomastoid is usually accompanied by a minor vascular pedicle.
The nerve may enter the muscle before branching.
Once within the muscle, the nerve divides early, and its branches sweep rapidly into position, parallel to the muscle fibers. The vessels, however, branch and form primary and secondary arcades, often crossing the muscle bundles and nerves before tertiary and quaternary branches are provided to the muscle fibers.
Ultimately, the terminal branches of the vessels and nerves come into close contact and course together in the connective tissue framework parallel to the muscle bundles.
Several methods have been used to classify muscles on the basis of morphology, function, blood supply, or nerve supply ( Table 23.1 ). We have classified muscles of the body according to their most common pattern of innervation ( Fig. 23.17 ). The pattern of neurovascular anatomy of the muscles influences the way a whole muscle or segment of muscle can be harvested as a functioning muscle microvascular transfer. It is possible to subdivide certain muscles, based on the neurovascular anatomy, into separate neurovascular units if each segment has an individual vascular pedicle. Clinically, serratus anterior, latissimus dorsi, gracilis, and rectus femoris are often used in this way, taking a portion of the muscle with their motor nerve and blood supply.
Type I. The muscle is supplied by a single motor nerve that divides after entering the muscle ( Fig. 23.18 ). Multiple vascular pedicles supply each muscle and form a continuous network throughout the tissue. It is possible in each case to remove a vascularized segment of muscle with its nerve supply and yet leave viable muscle in situ .
Type II. A single motor nerve supplies each of the muscles in this group, but the nerve divides before entering the muscle. Muscles in this group include the deltoid (see Fig. 23.18 ), gluteus maximus, trapezius, vastus lateralis, serratus anterior, and flexor carpi ulnaris.
Type III. Multiple motor nerve branches derive from the same nerve trunk (see Fig. 23.18 ). Once again, it is possible to subdivide each muscle into separate functional units because of the multiple vascular pedicles as well as the several nerve branches. Gastrocnemius is often split in this way, taking one head for reconstruction, leaving behind the other functional unit with its neurovascular supply attached.
Type IV. Multiple motor nerves are derived from different nerve trunks (see Fig. 23.18 ). It is apparent that each muscle can be subdivided anatomically into several functional units because of the multiple, often segmental neurovascular pedicles. Indeed, several of these muscles are formed developmentally by the fusion of adjacent somites (e.g., rectus abdominis and internal oblique).
Type I | Type II | Type III | Type IV |
---|---|---|---|
|
|
|
|
Following a review of the works by Manchot and Salmon, along with the results of our total body studies of blood supply to the skin and the underlying deep tissues, it has been possible to divide the body anatomically into three-dimensional vascular territories named angiosomes. Each of these three-dimensional angiosomes is supplied by a source (segmental or distributing) artery and its accompanying vein or veins ( Figs. 23.22–23.24 ). Each angiosome can be subdivided into matching arteriosomes (arterial territories) and venosomes (venous territories) or into further subunits based on individual perforators to the skin. Forty of these territories were initially described, but subsequent investigation has led to many of these territories being subdivided further into smaller composite units and revealed some that do not reach the skin surface. In a later study, 61 vascular territories were identified. Recent work has illustrated no fewer than 13 angiosomes of the head and neck, originally mapped as eight supplied by branches of the external carotid, internal carotid, and subclavian arteries. The angiosome concept indicates that the three-dimensional block of tissue is supplied by a major source artery and its accompanying vein(s), but it is important to note that the angiosome itself may be divisible depending on the branching pattern of the source vessel.
These composite blocks of skin, bone, muscle, and other soft tissues fit together like the pieces of a jigsaw puzzle, to make up the vascular supply of the body. In some of the angiosomes, there is a large overlying cutaneous area and a relatively small deep tissue region; in others, the reverse pattern exists. Each angiosome is linked to its neighbor at every tissue level, either by a true (simple) anastomotic arterial connection without change in caliber of the vessel or by a reduced-caliber choke anastomosis. A similar pattern with avalvular (bidirectional or oscillating) veins on the venous side links adjacent venosomes (see Fig. 23.24 ).
The angiosome concept has several important clinical implications:
Each angiosome defines the safe anatomic boundary of tissue in each layer that can be transferred separately or combined on the underlying source vessels as a composite flap (e.g., skin and muscle, muscle and bone, etc.). Also, the anatomic territory of each tissue in the adjacent angiosome can usually be captured with safety when it is included in the flap design based on one of the source vessels.
Because the junctional zone between adjacent angiosomes usually occurs within muscles of the deep tissue, rather than between them, these muscles provide an important anastomotic detour (bypass shunt) if the main source artery or vein is obstructed.
Because most muscles span two or more angiosomes and are supplied from each territory, one is able to capture the skin island from one angiosome by muscle supplied in the adjacent territory. As we shall see later, this fact provides the basis for the design of many musculocutaneous flaps.
In the course of parallel investigations to describe animal models for vascular studies, it was noted that there are close similarities in vascular anatomy between animal species. However, there are also important differences of which investigators should be aware. The purpose of this section is to provide a more complete picture of the vascular territories. As we shall see, the angiosome concept can be applied equally to other members of the animal kingdom as well as to humans.
In plastic surgical research, selection of various animals for the study of flap physiology is based on cost, convenience, availability, and/or ethical considerations rather than on a profound knowledge of their vasculature. The pig, for example, is a fixed-skin animal, and because human integument is also fixed in many areas, it has been assumed that this animal is therefore most ideally suited for experiments on skin flaps. It is important to understand the vascular basis of the experimental animal model since results may not be generalizable to humans.
Study of these animals also leads us to gain further insight into the development and arrangement of the vascular system. It may aid in identification of the ideal animal for other experiments, such as investigation of the delay phenomenon, use of tissue expansion, programming of vessels, and prefabrication of flaps – whether they are skin, other tissues, or combinations of tissues.
When the radiographs of four animals are reviewed ( Fig. 23.19 ), it is obvious there is a marked dissimilarity in the vasculature of the integument between them and that of the human (see Fig. 23.7 ). Surprisingly, however, this is in marked contrast to the dramatic similarity of the radiographs of deep tissue of the mammalian torsos ( Fig. 23.20 ).
The pattern of the cutaneous vasculature of the integument ranges from the fixed skin of the pig (supplied by a large number of small vessels over most of the hemitorso) to the mobile skin of the rabbit, in which four large vessels supply the majority of this area. The duck, not surprisingly, shows considerable diversity in the vasculature of its integument. Nevertheless, basic patterns are evident, having been modified by the growth and functional demands of the species.
The similarity in vasculature of the deep tissue is not confined to the anterior torso. Certain muscles between species have a remarkably similar vascularity, as can be seen in Fig. 23.21 .
It appears that the vascular blueprint of the deep tissues of the torso of mammals remains relatively constant. It is simply enlarged from the fetus to the adult and from small to large mammals. The reason for this may be that the functional requirements of the torso are the same in each mammal, that is, respiration, protection of the viscera, and aid in removal of the contents. Beyond the deep tissues of the torso, it appears that the vasculature of the overlying integument, the head and the neck, and the limbs has been modified to meet the functional demands of each species, as Hunter predicted more than 200 years ago.
Similarities are also seen in comparing the torso studies of mammals with those of other species, for example, the bird. In each case, vascular arcades arise from three basic sites: cranially from the subclavian and axillary vessels (aortic arch), laterally from the aorta (descending part), and caudally from the iliac and femoral vessels (terminal aorta). These three arcades form the basic vascular loops in the body that are common throughout the animal kingdom, including the human.
An underlying theme of the vascular architecture is that of vascular loops and arcades. Comparison of the vascular architecture in the human with that of other animals and other species reveals a similar arrangement. In loose-skinned animals, the arcades in the integument are stretched over long distances (see Fig. 23.18 ). In the wings of insects and in the leaves of plants, the “veins” assume a pattern of interconnecting arcades similar to those of the intestinal mesentery.
The angiosome concept provides a framework to understand the vascular anatomy of the human body. Plastic surgeons tend to focus on the vascular anatomy of skin but the angiosome concept applies equally to all tissues. The main vascular trunks that supply each angiosome are relatively consistent in size and position, however the individual cutaneous perforators are highly variable in size and position. Each individual cutaneous perforator territory fits together with its neighboring territories like a giant jigsaw puzzle ( Fig. 23.25 ). The arterial connection between adjacent cutaneous perforators may be through reduced caliber choke anastomotic vessels or through vessels that are not reduced in caliber (true anastomoses). True anastomoses occur variably throughout the body, most commonly along cutaneous nerves or in areas where the skin is mobile.
The importance of true anastomoses relates to the clinical territory of an individual cutaneous perforator. Generally, it has been found in experimental work on a series of animals including pig, dog, guinea pig and rabbit that the limit of viability of a skin flap is related to the anatomy of the pedicle of the flap and the surrounding perforator angiosomes. Based on the flap perforator, it is possible to reliably capture an adjacent cutaneous territory in any direction. In about 80% of the animal studies, the limit of flap survival was at the junction between second and third territory.
However, if there are true anastomoses between vascular territories, the third territory potentially could be captured based on an individual perforator. This would be analogous to a delay procedure (see Fig. 23.53 ) in which the choke anastomotic vessels dilate between vascular territories, increasing flap survival. Thus, it is the vascular anatomy of individual perforators and the vascular connections between perforators which govern the survival of flaps based on the perforator. A novel technique using dynamic thermography to preoperatively map cutaneous perforators and their interconnections has been reported which is non-invasive and non-irradiating and shows promise as a tool to predict flap survival.
The angiosome concept has led to the segregation of the body anatomically into three-dimensional vascular territories. Further work has led to the investigation and detailing of angiosomes in certain parts of the body. Some of these regions are highlighted to expand and to clarify the concept. The description of vascular territories is important to the design of flaps throughout the body.
The forearm is an important flap donor site due to the high incidence of hand and upper extremity injuries around the world.
The cutaneous perforators arise directly from the source arteries or from their muscular branches, and then they follow the intermuscular septa distally. Proximally, perforators pierce the muscle bellies near where the muscles are fixed at their origins from bone or from the intermuscular septa. The perforators become more numerous but smaller distally, with the maximum number of small perforators being seen in the palm, where the skin is most rigidly fixed. The cutaneous perforators on both the anterior and posterior surfaces of the forearm emerge in rows along the course of the radial and ulnar arteries ( Fig. 23.26 ).
In general, muscles are supplied by vascular pedicles from each angiosome that they span. These can be divided into the anterior group and the posterior group.
The anterior group of forearm muscles can be further subdivided into the superficial and deep muscles. The superficial muscles proximally receive branches from the brachial artery, the ulnar artery, or the ulnar recurrent artery. Distally, they receive branches from the radial artery or ulnar artery ( Fig. 23.27 ).
The deep anterior muscles are supplied by the radial artery, the anterior interosseous artery, and the ulnar artery. Note in Fig. 23.27 that the junctional zone between angiosomes occurs primarily within the muscles and that most muscles span at least two angiosomes.
The posterior group again can be divided into superficial and deep muscles. The superficial muscles receive blood from the radial recurrent artery, which supplies the proximal and lateral halves of their muscle bellies. The distal and medial halves of these muscles receive their blood supply from the posterior interosseous and the interosseous recurrent arteries ( Fig. 23.28 ). The deep muscles receive their blood supply from the radial recurrent artery, interosseous recurrent artery, posterior interosseous artery, and anterior interosseous artery.
When cross-sectional studies of the forearm are reviewed, it becomes clear that the angiosomes of each source artery span between the skin and the bone ( Fig. 23.29 ). It is noteworthy that the proportional representation of each source artery varies between levels in the forearm. Although the angiosome of the anterior interosseous artery does not reach the skin in Fig. 23.29 , it eventually surfaces in the distal forearm posteriorly or where the anterior interosseous artery provides a dominant median branch. In the latter case, it supplies the skin on the volar surface.
The bones of the forearm also conform to the angiosome concept. The radius is supplied mainly by the radial artery by means of several large proximal branches and by very small distal septoperiosteal and musculoperiosteal branches. In the middle, it receives a nutrient branch from the anterior interosseous artery. Distally, it also receives one or two small septoperiosteal branches from the anterior interosseous artery, and there is another blood supply from the posterior interosseous artery through the muscles that are attached to the bone.
The ulna is supplied predominantly by the ulnar artery, again through several large proximal and several small distal septoperiosteal branches. In the middle, it receives a nutrient branch from the posterior interosseous artery. Again, as with the radius, another blood supply enters through muscles attached to the ulna, derived from branches of the anterior interosseous artery.
From these data, it is evident that the radius and ulna, and nearly every muscle in the forearm, receive a contribution from at least two source arteries. Also, there are intramuscular and extramuscular anastomoses around the elbow that are usually well developed, especially on the radial side. In addition to the connections within the muscles and skin, particularly well-developed anastomoses occur between vessels that travel on and within the deep and cutaneous nerves.
When the radial artery flap is harvested, the only muscles that lie solely within this angiosome are the brachioradialis, extensor carpi radialis longus, and extensor carpi radialis brevis, supplied by its radial recurrent branch. However, this branch has an excellent anastomosis with the profunda brachii artery. Experience confirms this observation and has shown that dissection of the radial forearm flap can proceed safely right up to the origin of the radial artery from the brachial artery, with either division of its recurrent branch or inclusion of this vessel with one or more of “the mobile mass” muscles.
A proximal dissection of the ulnar artery to its origin from the brachial artery, however, especially if the radial artery is smaller than usual, may lead to problems.
The flexor digitorum profundus and flexor carpi ulnaris are the only muscles supplied solely by the ulnar artery and its anterior interosseous or recurrent interosseous branches (see Fig. 23.27 ). If these branches (or the common interosseous artery itself) are divided at their origin while a skin flap is harvested on the ulnar artery, survival of part or all of the flexor carpi ulnaris and flexor digitorum profundus will then rely on: (1) the anastomosis between the ulnar recurrent and the ulnar collateral vessels proximally, an anastomosis that may not be so well developed in some; (2) the anastomosis between branches of the radial artery and the anterior interosseous artery in the mid-forearm, especially within the flexor pollicis longus; or (3) the connections between the anterior interosseous and a reconstituted posterior interosseous artery in the distal forearm.
In contrast to the flexor digitorum profundus, the flexor digitorum superficialis is better protected because it has an additional contribution from the radial artery angiosome.
From the angiosome concept, and applying the anatomic knowledge in the previous sections, various tissues can be combined or raised separately on the forearm on the various source arteries and their accompanying veins. It has been shown clinically that the dimensions of a flap designed in one angiosome can be extended to include the anatomic territory of the adjacent angiosome in each tissue layer.
In the proximal forearm, the cutaneous blood supply from the radial and particularly the ulnar artery is often musculocutaneous. This is seen especially where muscles are fixed to bone or where they have a common fascial attachment, often before the muscles separate. In these circumstances (e.g., where the muscles arise from the common flexor or common extensor origin), the cutaneous vessels are derived usually from muscle branches and emerge from the muscles near these fixed attachments to bone or fascia.
In the lower leg, the source arteries and their respective venae comitantes travel adjacent to, but not within, the rigid fascial envelopes of the leg. Here they are invested in loose connective tissue.
The cutaneous vessels in the lower leg, as in the forearm, arise from the source arteries or their muscle branches. They pierce the deep fascia in longitudinal rows in the vicinity of the intermuscular septa or beside tendons. They supply branches to each tissue they pass of the lower leg proximally, whether bone, muscle, nerve, fat, tendon, or fascia. There tends to be a line of cutaneous perforators over the anterior tibial, posterior tibial, and peroneal vessels. These perforators provide the vascular basis of local perforator or “propeller” flaps for lower leg reconstruction. On the anterior surface proximally, these perforators usually emerge between the tibialis anterior and extensor digitorum longus, where they are derived from the anterior tibial artery, or between the flexor digitorum longus and soleus muscles, where they arise from the posterior tibial artery ( Fig. 23.30 ). Branches are seen also emerging between the tibia and tibialis anterior muscle and between the extensor digitorum longus and the peroneal muscles, these being derived from the anterior tibial artery. Distally, the vessels appear between the muscle bellies or between the tendons of the extensor digitorum longus, extensor hallucis longus, or peronei, obtaining their supply from the anterior tibial artery. Over the subcutaneous surface of the tibia where the skin is fixed, the deep fascia is continuous with the periosteum of the bone. In this area, branches of the anterior tibial and posterior tibial arteries anastomose freely over the surface of the periosteum.
In the posterior aspect of the leg, vessels pierce the deep fascia around the perimeter of muscles and tendons or from intramuscular septa. On occasion, they have a long intramuscular course and appear as terminal branches of a muscle artery; this is seen especially in the proximal perforators of the peroneal artery.
In the lower leg, a picture similar to that in the forearm is seen, with muscles being supplied by vascular pedicles from each angiosome territory they span.
The muscles in this compartment are supplied exclusively by the anterior tibial artery ( Fig. 23.31 ). A common vessel frequently passes through one muscle belly to supply the next as well as providing a cutaneous perforator.
This group of muscles is particularly vulnerable to ischemia because they are housed in a compartment with rigid walls across which vascular connections are sparse. This is particularly so medially, where the tibia is subcutaneous. Here the only connections between the anterior tibial and posterior tibial arteries are by means of the periosteum of the bone and from within the cutaneous network. As can be seen from Table 23.2 , all the muscles of this compartment lie in one territory.
One territory |
|
Two territories |
|
Three territories |
|
The peroneus longus and peroneus brevis are supplied by the anterior tibial and peroneal arteries, thus forming an important, albeit tenuous, intramuscular connection between their two source arteries (see Fig. 23.31 ). These muscles are situated within a tight compartment bordered by the fibula, the anterior and posterior intermuscular septa, and the deep fascia. As with the anterior group muscles, the blood supply frequently passes through one peroneal muscle to reach the next, often hugging the fibula during its course.
Become a Clinical Tree membership for Full access and enjoy Unlimited articles
If you are a member. Log in here