PRINCIPLES, TECHNIQUES, AND BASIC SCIENCE
CHAPTER 4 THE BLOOD SUPPLY OF THE SKIN AND SKIN FLAPS
GEOFFREY IAN TAYLOR, RUSSELL J. CORLETT, AND MARK W. ASHTON
Knowledge of the anatomy of the cutaneous arteries and veins is fundamental to the design of skin flaps and incisions. Although detailed studies of these vessels were performed by Manchot,1,2Spalteholz,3 Pieri,4 Esser,5 and Salmon,6,7 they were published in either German, Italian, or French. In the English-speaking world, little attention was paid to the precise anatomy of the cutaneous vessels so that surgeons designed skin flaps randomly on whatever vessels happened to be in the area, assigning rigid length-to-breath ratios to the flaps. It was not until the last four decades, with the introduction of the microsurgical free skin flap,8,9 the revival of the musculocutaneous flap,10 the description of the fasciocutaneous flap,11,12 and the use of tissue expansion13 and flap prefabrication,14that surgeons and anatomists have returned to the anatomic dissecting room to search and research the intricacies of the vascular pathways to and from the skin. This has been and still is an exciting period of anatomic renaissance, especially with the emergence of “perforator flaps.”15-22
Although much original data have been provided, there has been a concurrent bewildering explosion of new terms and attempts to classify the cutaneous circulation, often based on flap design rather than vascular anatomy. It is worth stating, however, that many of the “new” flaps, whether island, fascial, neurocutaneous, direct, indirect, axial, random, super, septal, arterial, musculocutaneous, perforator, or otherwise, are each simply the product of a surgical insult inflicted on the same basic vascular pattern that exists throughout the body, though viewed through different eyes. Converse23stated that “there is no simple and all encompassing system which is suitable for classifying skin flaps.” He went on to state that “it is now generally agreed that the anatomical vascular basis of the flap provides the most accurate approach for classification.” Time has supported the veracity of this statement, emphasized by the recent refocus of attention on the anatomy of the cutaneous perforators as the basis for skin flap design.15,17,18,20-22,24-27
The skin is the largest organ of the body. Temperature regulation to maintain homeostasis is one of its major roles. This important function is provided by a rich network of cutaneous arteries and veins, especially in the dermal and subdermal plexi, which supply the sweat glands and allow for heat exchange by convection, conduction, and radiation. Although the cutaneous circulation is rich and vast, the metabolic demands of the skin elements are low so that only a small fraction of the potential cutaneous circulation is necessary for skin viability—a fact that is pertinent to the design and survival of various skin flaps.
The cutaneous arteries arise directly from the underlying source (segmental or distributing) arteries or indirectly from branches of those source arteries to the deep tissues, especially the muscles (Figures 4.1 and 4.2). From here the cutaneous arteries follow the connective tissue framework of the deep tissues, either between or within the muscles, and course for a variable distance beneath the outer layer of the enveloping “body suit” of deep fascia. They then pierce that structure, usually at fixed skin sites as cutaneous perforators. After emerging from the deep fascia, the arteries course on its superficial surface for a variable distance, supplying branches to it and the deep surface of the fat. They then worm their way between the lobules of the subcutaneous fat, ultimately reaching the subdermal plexus, where they again travel for variable distances to supply the overlying skin, being longest where the skin is mobile.26 During their subcutaneous course, the cutaneous arteries (and veins) often travel with the cutaneous nerves, either as long channels or as a chain-linked system of vessels.28,29
The density, size, and direction of the cutaneous perforators vary from region to region, being modified by growth, differentiation, and the functional demands of the body part, factors that provide the basis for the various anatomic concepts that follow. In general, the vessels of the head, neck, torso, and proximal limbs are larger and more widely spaced than their counterparts in the forearms, legs, hands, and feet (see Figure 4.1). Although the size and length of the cutaneous perforators may vary, they all interconnect to form a three-dimensional “body carpet” that has a particularly well-developed horizontal strata of vessels in the dermis, in the subdermis, on the undersurface of the subcutaneous fat, and on the outer surface of the deep fascia (Figure 4.2).
The connections between adjacent cutaneous arteries are either by true anastomoses, without change in caliber, or by reduced-caliber choke anastomotic vessels (Figure 4.3). The latter are plentiful in the integument (skin and subcutaneous tissues) and may be important in regulating the blood flow to the intact skin (Figure 4.1C). These choke vessels play an important role in skin flap survival, where, like resistors in an electrical circuit, they provide an initial resistance to blood flow between the base and the tip of the flap. When a skin flap is delayed by the strategic division of cutaneous perforators along its length, these choke vessels dilate to the dimensions of true anastomoses (see later), thus enhancing the circulation to the distal flap. Although some dilatation of the choke vessels occurs because of the relaxation of sympathetic tone, the major effect is seen between 48 and 72 hours after surgery.30,31 This is due to an active process resulting in hypertrophy and hyperplasia of the elements of the vessel wall and a permanent increase in diameter of its lumen.30
The cutaneous veins also form a three-dimensional plexus of interconnecting channels with dominant strata in the subdermis (Figures 4.4–4.7). Although many of these veins have valves that direct the blood in a particular direction, they are often connected by avalvular veins.32 These avalvular (oscillating) vessels allow bidirectional flow between adjacent venous territories whose valves may be oriented in opposite directions, thus providing for the equilibration of flow and pressure (Figure 4.6). 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. The superficial inferior epigastric veins (SIEVs) that drain the lower abdominal integument toward the groin are good examples. In some regions, valved channels direct flow radially away from a plexus of avalvular veins as, for example, in the venous drainage from the vertex of the scalp or the nipple-areolar summit of the breast. In other areas, valved channels direct flow toward a central focus, seen in the groin or in the stellate limbs of the cutaneous perforating veins (Figures 4.4 and 4.6).
In general, the cutaneous veins partner the arteries. However, the venous drainage of the skin is established in the embryo in two stages, which interconnect but which are separated in time by approximately 1 week of development (Figure 4.5).25,33-35
FIGURE 4.1. A. Montage of the cutaneous arteries of the body. The skin has been incised along the ulnar border in the upper extremities, and the integument has been removed with the deep fascia on the left side and without it on the right. B. A closer view of the vessels of the head and neck from the side. C. The angiosome territory of a single cutaneous perforator (perforator angiosome) defined by a perimeter of reduced-caliber “choke” anastomotic vessel. Note (1) the direction, size, and density of the perforators, which are large on the torso and head and get progressively smaller and more numerous toward the periphery of the limbs; (2) the reduced-caliber (choke) anastomotic arteries, which link the perforators into a continuous network, with an area highlighted (arrow) and enlarged in (C). (Reproduced with permission from Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: experimental study and clinical applications. Br J Plast Surg. 1987;40:113).
FIGURE 4.2. A schematic diagram shows a single direct septocutaneous perforator (B) and various indirect musculocutaneous perforators of varying sizes that pierce the muscle (or other specialized deep tissues) early (C) or late (A and D) to supply the overlying integument. In each case, the perforator supplies all adjacent tissues between the source artery and the skin.
FIGURE 4.3. Schematic representation of choke anastomoses (A) and true anastomoses (B) between adjacent arteries. (Reproduction with permission from Taylor GI, Minabe T. The angiosomes of the mammals and other vertebrates. Plast Reconstr Surg. 1992;89:181).
FIGURE 4.4. The venous network of the integument of a female subject. (Reproduced with permission from Taylor GI, Caddy CM, Watterson PA, Crock JG. The venous territories (venosomes) of the human body: experimental study and clinical implications. Plast Reconstr Surg. 1990;86:185).
FIGURE 4.5. Diagram of developing arteries and veins in the forelimb of one of our quail embryos where approximately 1 day in the quail equates to 1 week in the human embryo. Note the primary venous system that develops first, drains the ectoderm (later the dermis) and the deep tissues along the surface of the embryo, whereas the secondary venous system develops centrally, connects with the primary system, and drains areas of the ectoderm (dermis) radially and then axially along the limb in company with the arteries. (Reproduced with permission from Taylor GI. The Angiosome Concept and Tissue Transfer, Publisher Quality Medical Publications (QMP) Jul 2013).
The primary system of veins develops first in the human embryo at about 5 weeks in the subectodermal region and is represented in the adult by large-caliber veins, such as the cephalic, saphenous, and external jugular. These veins course often at some distance from the cutaneous arteries, they are accompanied frequently by cutaneous nerves,28,33,34 and they travel for long distances before piercing the deep fascia (Figures 4.4, 4.5, and 4.6).
The secondary system of veins develops approximately 1 week later in the embryo. This network consists of central axial source veins that accompany the axial source arteries and receive perforating veins from the subectodermal region that accompany the developing cutaneous arteries (Figure 4.5D). In the adult, they are represented by the venae comitantes of the cutaneous perforating arteries with which they travel in close proximity (Figures 4.2 and 4.4–4.7). Thus, from the dermal and subdermal venous plexi, the veins collect into a horizontal “freeway” of large-caliber veins, where they are often related to the cutaneous nerves and a longitudinal system of chain-linked arteries, or alternatively they collect in centripetal or stellate fashion into a common channel that passes vertically down in company with the cutaneous arteries to pierce the deep fascia (Figures 4.6 and 4.7). Thereafter, these perforating veins remain in company with the direct and indirect cutaneous arteries, draining ultimately into the venae comitantes of the source arteries in the deep tissue.
FIGURE 4.6. Schematic diagrams of the basic venous module (A), its modified arrangement in different areas (B), and how these modules interconnect to form a continuous network (C). In the integument, this network of venous perforators of the secondary venous system is connected in the subdermal plexus with the longitudinal channels of the primary venous system (D). The valved segments in blue and the avalvular oscillating veins in yellow are highlighted. (Reproduced with permission from Taylor GI, Caddy CM, Watterson PA, Crock JG. The venous territories (venosomes) of the human body: experimental study and clinical implications. Plast Reconstr Surg. 1990;86:185).
Importantly, these two systems interconnect, especially in the subdermal plexus. This explains why, for example, the radial forearm free flap will survive on either the secondary system of venae comitantes of the radial artery or the primary cephalic or basilic veins.
Thus, the skin is fed and drained by a continuous network of arteries and of veins formed by vessels whose size, shape, density, and direction vary from region to region in the body. The following observations provide for a better understanding of this variation in vessel anatomy.
FIGURE 4.7. Composite diagram of the integument and underlying muscle (shaded) illustrating the primary superficial (S) and secondary deep (D) venous systems with their interconnections in the superficial and the deep tissues. A large vena communicans (C) connects these systems, and the alternative pathways of four venae comitantes of the perforating arteries are shown. Note the bidirectional system of veins (yellow) within the superficial fascia and the muscle (small arrows) and the diverging direction of flow of the muscular veins as determined by the orientation of their valves. (Reproduced with permission from Taylor GI, Caddy CM, Watterson PA, Crock JG. The venous territories (venosomes) of the human body: experimental study and clinical implications. Plast Reconstr Surg. 1990;86:185).
The Angiosome Concept
A review of the works of Manchot1,2 and Salmon6,7 combined with our own studies of the blood supply to the skin and the underlying deep tissues enabled us to segregate the body anatomically into three-dimensional vascular territories that we named “angiosomes.”26 These three-dimensional anatomic territories are supplied by a source (segmental or distributing) artery and its accompanying vein(s) that span between the skin and the bone (Figures 4.8–4.11). Each angiosome v can be subdivided into matching arteriosomes (arterial territories) and venosomes (venous territories). Initially we described 40 angiosomes, but this was an intentional oversimplification as many of these territories can and have been subdivided further into smaller composite units, for example, the intercostal and lumbar angiosomes, and we took this concept down to the final branches in the vascular tree, which in the skin is the cutaneous perforator (Figure 4.1C).26,29 In the same way, we subdivided the deep tissues, for example, the muscles, into their component anatomical territories.
These composite blocks of skin, bone, muscle, and other soft tissue fit together like the pieces of an intricate jigsaw puzzle. In some angiosomes, there is a large, overlying cutaneous “crust” and a relatively small deep tissue region; in others the reverse pattern exists. In some regions, the territory does not reach the skin and is confined to the deep tissues as seen, for example, in more recent studies of the head and neck.36 Each angiosome is linked to its neighbor, in each tissue, by a fringe of either true (simple) anastomotic arteries without change in caliber or by reduced-caliber choke (retiform) anastomotic vessels (Figure 4.1C). On the venous side, avalvular (bidirectional or oscillating) veins often match the anastomotic arteries and define the boundaries of the angiosome, especially in the deep tissues.
FIGURE 4.8. The sites of emergence of an average of 376 direct and indirect cutaneous arterial perforators of 0.5 mm or greater averaged from all studies. Note their concentration near the dorsal and ventral midlines, around the base of the skull, and over or near the intermuscular septa. Direct perforators are more common in the limbs, whereas indirect perforators predominate in the torso. The vessels were color coded to match their underlying source arteries and to correlate with the angiosomes of the body. Compare with Figure 4.10.
FIGURE 4.9. Schematic diagram of the cutaneous perforators (left) and their interconnections. The underlying source arteries, their interconnections, and the sites of origin of the cutaneous vessels (dots) are shown on the right of the diagram. Only the major perforators are illustrated. The vascular territories of the source arteries have then been defined in the integument (left) and in the deep tissues (right) by lines drawn around their perimeter, across the choke, or true connecting arteries and arterioles. Note how the territories correspond in each layer. When taken together they constitute the angiosomes.
Clinical Applications. The angiosome concept has many implications. For example:
(1) Each angiosome defines the safe anatomic boundary of tissue in each layer that can be transferred separately or combined together on the underlying source artery and vein as a composite flap. Furthermore, the anatomic territory of each tissue in the adjacent angiosome can usually be captured with safety when combined in the flap design.22,30,31,37,38
In the skin, the anatomical territory of each cutaneous perforator forms a basic angiosome module, defined by a perimeter of anastomotic vessels that connects it with its neighbor in all directions (Figures 4.1C and 4.11), and we charted an average of 376 such vessels of 0.5 mm or greater.26 In the skin and subcutaneous tissues, these connections were usually, but not always, by reduced-caliber vessels that we named “choke” because of their narrowed lumen. Alternatively, these connections were “true” anastomoses without change in caliber, especially where vessels accompanied cutaneous nerves, but seen more commonly in other tissues, especially the muscles and the nerve trunks, or after a flap has been delayed.30,31,37,38
These basic skin modules (cutaneous perforator angiosomes) link together like a patchwork quilt to form a continuous network of vessels that surfaces the entire body (Figure 4.11). In our original article where we charted 376 of these skin modules supplied anatomically by 40 bilateral (total 80) source arteries, there was an average of 4.7 cutaneous angiosomes per source artery.26 However, the size and number of these skin modules vary within and between source arteries. In some angiosomes, the cutaneous portion of the source artery was represented by multiple skin perforators (defined as vessels that pierce and emerge from the outer layer of the deep fascia), for example, the perforators of the internal thoracic and the deep inferior epigastric artery, whereas in other source artery angiosomes just one, usually large, cutaneous vessel was represented, for example, the superficial inferior epigastric artery (SIEA), superficial circumflex iliac artery (SCIA), and the lateral thoracic perforator (Figure 4.12). It should be noted that in each case the cutaneous perforator supplied not only the skin but also a block of tissue between the outer layer of the deep fascia and the epidermis. In the chest, it includes the breast tissue and in the neck the platysma muscle, for example, as well as the subcutaneous fat.
This brings us to the next point—the clinical territory of a cutaneous perforator. In a number of experiments, and in a range of animals that included the pig,39 dog,37 guinea pig,31 and rabbit,30 as well as observations in patients undergoing various surgical procedures,19,38,40 especially those that involved flap delay, we have observed and concluded on many occasions that one adjacent anatomicalcutaneous perforator territory (skin module) can be captured with safety radially in any direction on the perforator at the flap base. We have noted that necrosis, when it occurs, does so usually in the choke zone between this captured territory and the one beyond, but sometimes an additional territory in the series will survive (Figure 4.13).
The safe length of such a flap depends, therefore, on the size, direction, and span of the anatomical territory of each perforator—the perforator on which the flap is based and the next in the series. This is, therefore, the reliable clinical territory of the cutaneous perforator at the flap base where the anastomotic connections are by usually reduced-caliber choke arteries (Figures 4.13–4.15). However, if the connections are by “true” anastomoses without change in caliber, then the survival length of the flap will be longer with function similar to a flap that has been delayed,38,40 seen especially in the skin where vessels accompany the cutaneous nerves.28
(2) Because the junctional zone between adjacent angiosomes in deep tissues occurs usually within the muscles, rather than between them, these muscles provide a vital anastomotic detour if a main source artery or vein is obstructed.
(3) Similarly, 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 via the muscle supply in the adjacent territory.
This anatomic fact provides the basis for the design of many musculocutaneous flaps.
FIGURE 4.10. The three-dimensional vascular territories—angiosomes—encompassing all tissues between skin and bone from (1) thyroid, (2) facial, (3) buccal (internal maxillary), (4) ophthalmic, (5) superficial temporal, (6) occipital, (7) deep cervical, (8) transverse cervical, (9) acromiothoracic, (10) suprascapular, (11) posterior circumflex humeral, (12) circumflex scapular, (13) profunda brachii, (14) brachial, (15) ulnar, (16) radial, (17) posterior intercostals, (18) lumbar, (19) superior gluteal, (20) inferior gluteal, (21) profunda femoris, (22) popliteal, (22A) descending geniculate (saphenous), (23) sural, (24) peroneal, (25) lateral plantar, (26) anterior tibial, (27) lateral femoral circumflex, (28) adductor (profunda), (29) medial plantar, (30) posterior tibial, (31) superficial femoral, (32) common femoral, (33) deep circumflex iliac, (34) deep inferior epigastric, (35) internal thoracic, (36) lateral thoracic, (37) thoraco-dorsal, (38) posterior interosseous, (39) anterior interosseous and (40) internal pudendal source territories.
Vessels Follow the Connective Tissue Framework of the Body
The fact that vessels follow the connective tissue framework is fundamental to the design of all flaps, especially the “fasciocutaneous” and “septocutaneous” perforator flaps.
Developmentally, the vascular system appears in the mesoderm of the embryo as a continuous network of vessels. The specialized tissues develop within the interstices of that vascular network. As growth and differentiation progress, vessels become encased within the various tissues and are continuous with vessels coursing between the tissues by way of vascular pedicles at various sites. These sites, in turn, are determined by the relative mobility of those tissues. The connective tissue can be regarded as what is “left over” after the specialized tissues have developed.41 Like a honeycomb, the connective tissues house and support the specialized tissues and in so doing support the vascular system of the body, with which they have developed an intimate relationship.
It is important to differentiate between the superficial and the deep fascia as these terms are often confused (Figure 4.16). The superficial fascia is a loose connective tissue honeycomb that connects the dermis to the outer layer of the deep fascia. It houses the subcutaneous fat, the breast, and remnants of the panniculus carnosus where it still exists (for example, the muscles of facial expression in the head, the platysma in the neck, the palmaris brevis in the hand, and the dartos muscle in the scrotum). In the lower abdomen, it is separated into two layers by the fascia of Scarpa.
The deep fascia is also a honeycomb of connective tissue that is usually more rigid that its superficial counterpart. It has a tough outer layer that surrounds and sometimes provides origin to the muscles as a sheath on the torso and a stocking in the limbs. Often referred to as the deep fascia, this is only the outer layer. Radiating intermuscular septa of the deep fascia, dense in some areas and looser in other, anchor the outer layer to the skeleton where the deep fascia becomes continuous with the periosteum. From these septa and from the periosteum, the deep fascia is continued into the muscles as intramuscular septa.
FIGURE 4.11. Schematic representation of the cutaneous perforator angiosomes showing the basic skin module (left) and several modules of different sizes combined to represent the cutaneous territory of a source artery (right).
FIGURE 4.12. The angiosome territories of the anterior chest and abdominal regions of the torso—each territory mapped to match the underlying source arteries with lines drawn through the perimeter of usually choke anastomotic arteries. Note that the SIEA and the lateral thoracic angiosomes are supplied by a single large cutaneous perforator compared, for example, with the internal thoracic, lateral intercostal, and DIEA angiosomes that have multiple cutaneous perforators, each of which could be subdivided further into individual cutaneous (angiosome) territories. This has been done on one side of the internal thoracic–superior epigastric territory to illustrate this point. SIEA, superficial inferior epigastric artery; DIEA, deep inferior epigastric artery.
In the adult, the major arteries are closely related to the bones of the axial skeleton. Their branches follow the intermuscular connective tissues, where they divide to supply the muscles, bones, tendons, nerves, and deep fat deposits, in each instance following the connective tissue framework of that structure down to the cellular level.
The cutaneous perforators exhibit the same pattern. They usually arise from the source artery or from one of its muscle branches, either before or after entering the muscle, and follow the intermuscular or intramuscular connective tissues of the deep fascia as direct or indirect cutaneous perforating vessels, respectively, as they pierce the outer layer of the deep fascia (Figures 4.2, 4.16, and 4.17). Some cutaneous perforators, however, are derived from branches to other deep structures, such as the nerves, the periosteum of bones, the joints, and some glands. After emerging from the deep fascia, the cutaneous vessels follow the connective tissue framework of the superficial fascia to reach another connective tissue structure, the dermis of the skin.
In some regions, the connective tissue is loose areolar, in which case the vessels travel within the connective tissue to allow the arteries to pulsate and the veins to dilate, for example, within the carotid sheath. In other regions, the connective tissue forms dense fibrous sheets, such as the outer layer of the deep fascia, some intermuscular septa, and the periosteum of the bone. In these cases, the vessels course beside or on the dense fasciae, not within them.
Clinical Applications. This vessel relationship to the different types of connective tissue achieves special significance when the surgeon raises a cutaneous flap that includes the outer layer of the deep fascia (termed fasciocutaneous flap) or when the design is extended to include the intermuscular or intramuscular septa (the septocutaneous flaps).
In the former case, the deep fascia should be included in the design of the fasciocutaneous flap in those sites where the skin is relatively fixed to the deep fascia, for example, in the limbs or the scalp (Figures 4.16 and 4.17B). In these instances, the dominant cutaneous vessels course on, or lie adjacent to, the deep fascia. Although they can be dissected free in some cases, it is safer or more expedient to include the deep fascia with the flap. However, where the skin and subcutaneous tissues are mobile over the deep fascia, for example, in the iliac fossa or the breast, it is unnecessary to include this fascial layer as the major cutaneous vessels have already left its surface (Figure 4.17A).
FIGURE 4.13. Skin from the torso of the dog that was removed by midline dorsal incision after the raising of a large island flap on one side (outlined) 1 week previously on a single arteriovenous pedicle (arrow). Comparable vessels are identified with dots and arrows on each side of the ventral midline. Note the anatomical territory of this perforator (shaded yellow) and that (1) the choke vessels have enlarged to the size of true anastomoses within the flap, (2) the scalloped necrosis border is evident inside the flap margins (dotted), and (3) at least one adjacent vascular territory has been captured radially on the artery in the flap pedicle to define the clinical territory of this perforator. (Reproduced with permission from Callegari PR, Taylor GI, Caddy CM, Minabe T. An anatomical review of the delay phenomenon: 1. Experimental studies. Plast Reconstr Surg. 1992;89:397).
The term septocutaneous is sometimes misleading, especially when used to describe a surgically created entity rather than a true anatomic structure. This may occur, for example, when the cutaneous perforators of a radial or an ulnar flap are dissected within an envelope of loose areolar tissue between the flexor tendons. Furthermore, the septocutaneous flap may provide traps for the unwary surgeon. In some cases, the cutaneous artery and its accompanying vein leave the underlying source vessels and course toward the surface in a surgically favorable position, adjacent to a true white fibrous intermuscular septum. This is typical of the blood supply to the skin of the lateral arm flap, where cutaneous perforators arise from descending branches of the profunda brachii vessels and follow the lateral intermuscular septum toward the skin. This pattern of supply usually exists where the muscles glide on either side of the intermuscular septum. However, if the muscles attach to either side of the intermuscular septum, then the course of the cutaneous perforator may be quite variable.
FIGURE 4.14. Schematic representation of the safe clinical territory of a cutaneous perforator (arrow) where anatomical territories of adjacent perforators are captured radially. Note beyond the captured perforators the irregular circumference of the necrosis line. (Compare with Figure 4.17).
FIGURE 4.15. Diagrammatic representation of the same flap raised with and without a surgical delay to illustrate the necrosis line and the changes in the choke vessels—in the choke-vessel interface with vessel “b” or the one beyond. In B, vessel “a” has been delayed by a previous operation before raising the flap. Note the effect on the choke vessels and the site of the necrosis line.
FIGURE 4.16. Cross-sectional studies to illustrate the origin and the course of the cutaneous perforators from their source arteries in the deep tissues. A. Oblique section of the anterior abdominal wall showing the supply to the integument and the underlying muscle, derived laterally from a posterior intercostal artery (i) and medially from vessels arising in the groin. The latter vessels are the superficial inferior epigastric artery (e) and the ascending branch of the deep circumflex iliac artery (D). Note the choke vessels that connect these angiosomes and that they correspond in position in the superficial and the deep layers. B–E. Schematic diagrams and radiographic study at mid-thigh level of (B). The connective tissue network of the superficial and deep fascia (C). The same as (B) but the vessels have been added that follow this connective tissue framework, (D) the angiosomes supplied by each of the source vessels and (E) the lead oxide cadaver injection study that corresponds with (C). Note the large direct cutaneous perforators that follow the intermuscular septa (s) and the large and small indirect musculocutaneous perforators (m). (Reproduced with permission from Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: experimental study and clinical applications. Br J Plast Surg. 1987;40:113).
This variability of anatomy is evident, for example, in the lateral aspect of the upper calf. If a compound skin and bone flap is designed over the lateral intermuscular septum, based on the cutaneous perforators of the peroneal vessels, these skin vessels may course directly to the surface, traveling in a favorable position, adjacent to the septum. Alternatively, they may arise indirectly from branches to the soleus muscle as terminal twigs of muscle branches that have arisen from the peroneal vessels at considerable distance from the lateral intermuscular septum. In these instances, a painful and laborious intramuscular dissection of the cutaneous supply awaits the unfortunate surgeon. These two pathways provide the basis for classifying the various “perforator flaps.”
Vessels Radiate from Fixed to Mobile Areas
Vessels cross tissue planes at or near their fixed margins and radiate to mobile areas. This concept is well illustrated in the blood supply to the skin since vessels emerge from the deep fascia where the skin is fixed or tethered. From here, they travel for variable distances depending on the mobility of the skin. The more mobile the integument, the longer the vessels. These fixed skin sites are seen in a well-muscled individual at skin crease lines, over intermuscular septa, or near the fixed attachments of muscles to bone (see Figures 4.8, 4.9, and 4.17).
Clinical Applications. It follows that long robust flaps should be based where the skin is fixed, with their axes oriented along the lines of maximal skin mobility. The further the distance between fixed points, the longer the safe dimensions of the flap. There are many instances in which this applies in practice. For example, long flaps can be based at the groin, the paraumbilical region of the abdomen, or the parasternal region of the chest (Figures 4.12 and 4.18). Additional precision to flap design can be obtained before surgery by the use of Doppler ultrasonic probe to locate these perforators19 in thin individuals as they emerge from the deep fascia or more recently with CT angiography.42 In this way, a viable flap can be designed by basing it on a significant perforator that is located with the probe, by finding the next dominant perforator along the desired flap axis and then simply joining these two points, since we have found experimentally that one adjacent vascular territory can be captured with safety (Figure 4.13).22,30,31,37,38
FIGURE 4.17. Sectional strip radiographic studies from above down, of the breast (A), thigh (B), sole of the foot (C), and buttock (D). D includes the underlying gluteus maximus muscle. The schematic diagram illustrates the dominant horizontal axis of the vessels, which provides the primary supply to the skin in each case and its relationship to the deep fascia (arrow). In type A, they predominate in the subdermal plexus. Note from left to right the internal thoracic perforator and lateral thoracic artery converging on the nipple (arrow) in the radiograph of the loose skin region of the torso. In type B, they are seen coursing on the surface of the deep fascia in this relatively fixed skin area. In type C, the source artery itself is the dominant horizontal vessel supplying the skin, coursing beneath the deep fascia in this rigidly fixed skin region. In type D, the horizontal vessel is again the source artery (inferior gluteal), but this time its branches have to pierce muscle indirectly to reach this fixed skin region. Small arrows define the deep fascia, and the large arrow indicates the large fasciocutaneous branch of the gluteal artery, which descends with the posterior cutaneous nerve of the thigh. (Reproduced with permission from Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: experimental study and clinical applications. Br J Plast Surg. 1987;40:113).
Vessels Hitchhike with Nerves
Our research has confirmed that the intimate relationship between nerves and blood vessels that is known to exist in the deep tissues and in some areas of the integument is in fact present in all regions of the skin and subcutaneous tissues of the body.28 The cutaneous nerves are accompanied by a longitudinal system of arteries and veins that are often the dominant blood supply to the region. The veins in company with the nerves are frequently large “primary” venous freeways, such as the cephalic, basilic, long saphenous, and short saphenous systems. The arteries are either long vessels—for example, the supraorbital, lateral intercostal, or saphenous arteries—or they exist as a chain-linked system of cutaneous perforators, often joined in series by true anastomoses without change in caliber (Figure 4.18).
Whether the nerves pierce the deep fascia together with the vessels, emerge separately and cross the vessels at an angle, or approach the vessels from opposite directions, in each case, as if drawn by a magnet, the main trunk of the vessel or some of its branches “peel off” to course parallel to the nerve. These vessels either course in close proximity to the nerve or they travel nearby (Figure 4.18).
Clinical Applications. This neurovascular relationship presents the basis for designing long flaps with the added potential for sensation at the repair site. Many of the current “axial” or “fasciocutaneous” flaps are in fact neurovascular flaps. The original long and short saphenous flaps in the calf described by Ponten12 are cases in point.
Vessel Size and Orientation Are a Product of Tissue Growth and Differentiation
More than two centuries ago, John Hunter43 suggested that at some stage of fetal development, and certainly at birth, an individual has a fixed number of arteries in the body, the size, length, and direction of which are modified by subsequent growth and differentiation of the parts. This helps explain why long vessels radiate from the skull base toward its vertex as the brain and skull expand, why long vessels course on the torso as the lungs expand and the fetus extends from the flexed position, and why long vessels converge on the nipple from the periphery as the breast develops in the female (Figure 4.19).
Clinical Applications. This information provides the basis for the logical planning of the various breast reduction operations. Each technique revolves around the design of a flap of skin and subcutaneous tissue (including breast) that is based on one or more vessels as they pierce the deep fascia around the perimeter of the pectoralis major muscle. Tissue expansion is another example. Here existing vessels in the skin and subcutaneous tissues, like the vessels in the abdominal wall during pregnancy, hypertrophy and elongate as the fluid is introduced into the expander. Therefore, if possible, the expander should be placed beneath mobile skin and between fixed skin sites to take maximal advantage of the inherent vascular anatomy of the region.
FIGURE 4.18. Arterial injection studies of the (A) right upper limb and (B) torso. Note the chain-linked systems of arteries (arrows) that course with the cutaneous nerves in the upper limb. On the torso, the nerves are marked green on the arterial study. They either course with the cutaneous arteries, cross them at angles, and collect arterial branches or approach the arteries from opposite directions (arrows). (Reproduced with permission from Taylor GI, Gianoutsos MP, Morris SF. The neurovascular territories of the skin and muscles: anatomic study and clinical implications. Plast Reconstr Surg. 1994;94:1).
Vessels Obey “The Law of Equilibrium”
This concept was described by Debreuil-Chambardel and is referred to constantly by Michel Salmon6,7 in his description of the cutaneous arteries. Basically, this states that “the anatomical territories of adjacent arteries bear an inverse relationship to each other yet combine to supply the same region.” If one vessel is small, its partner is large to compensate and vice versa. This is well illustrated in the variability in size between each of the parasternal perforators of the internal mammary artery and between the internal mammary perforators and the cutaneous perforator of the adjacent angiosome: the thoracoacromial (see Figure 4.1). It is likely that the same relationship occurs between the cutaneous veins, for example, between the venous perforators of the deep inferior epigastric venae comitantes (DIEV) and the usually large SIEV. This may be critical in the design of a deep inferior epigastric perforator flap where the DIEV perforating vein is unexpectedly small. Hence the reason for preserving the SIEV, especially on the contralateral side, as a potential “lifeboat.”
Clinical Applications. The deltopectoral flap of Bakamjian is an excellent example. It is based medially over the second to fourth intercostal spaces so as to embrace the variable size of the internal thoracic (internal mammary) perforators. Designed below and parallel to the clavicle, it is usually dissected in a medial direction from its tip at the shoulder. If small perforators are noted over the deltoid muscle, and in particular from the deltopectoral groove, the dissection is continued to the flap base on the assumption that the internal thoracic perforators will be large. If, however, a large cutaneous perforator is seen emerging from the deltopectoral groove, then this pedicle is usually ligated and further dissection of the flap is delayed for 1 week because of the possibility that the adjacent internal thoracic perforators will be small. This delay procedure is employed because of the risk of flap necrosis, especially if the flap tip spans beyond the point of the shoulder.
Figure 4.19. Schematic diagram to illustrate John Hunter’s hypothesis of a fixed number of cutaneous arteries in the fetus and how growth and differentiation of the tissues could modify the definitive size and relationship of the arteries x and y in different regions of the body after they pierce the deep fascia. A. The “resting state.” B. The vessels are stretched by expansion of structures beneath the deep fascia, for example, the skull and brain. C. The vessels are stretched and compressed toward the dermis by the developing breast above the deep fascia. D. The vessels are stretched apart by the developing long bones but still retain a dominant relationship to the deep fascia. E. Growth again stretches the vessels apart, but this time a gliding plane develops between the deep fascia and the subcutaneous fat in this loose skin area, for example, the iliac fossa.
Vessels Have a Relatively Constant Destination but May Have a Variable Origin
This is typical of the vessels that emanate from the groin to supply the skin of the lower abdomen and upper thigh. The SIEA and the SCIAs, for example, may arise separately from the common femoral artery, as a combined trunk from that vessel, or from one of its branches.28 Whichever is the case, their destination is constant to supply the integument of the lower abdomen and the hip (see Figures 4.1and 4.12).
Clinical Application. Although this variability in vessel origin may not be important when designing a pedicled flap at the groin, it certainly becomes so if the flap is to be isolated on its feeding vessels for microvascular transfer.8,9,44
The Vessels Form a Continuous Unbroken Network
This fact has been referred to already but is highlighted because it is fundamental to the understanding of the various skin flap designs where, for example, the same area of skin and subcutaneous tissuecan be raised as a “cutaneous” flap, a “fasciocutaneous” flap, a “septocutaneous” flap, a “musculocutaneous” flap, or a “perforator flap.” In each case, regardless of the flap design, the vessels that enter the flap at its base connect into the same vascular network. What may vary between flap designs, however, are the size and site of entry of the cutaneous perforators, thus influencing flap survival (seeFigure 4.2).
Clinical Applications. There are numerous instances whereby the surgeon knowingly or unwittingly takes advantage of this anatomic fact. For example, the skin and subcutaneous fat over the pectoralis major muscle can be designed (1) as a musculocutaneous flap on small perforators emerging from the underlying muscle, (2) as a fasciocutaneous flap based either medially on the large internal thoracic (internal mammary) perforators or laterally on the dominant perforator(s) of the thoracoacromial axis, or (3) as a neurovascular fasciocutaneous flap when based superiorly on the supraclavicular neurovascular pedicles that flow down over the clavicle from the neck.
Other important considerations are the anastomotic vascular “keystones” usually formed by reduced-caliber choke arteries that link adjacent perforating cutaneous perforators to form the arterial network. When a flap is elevated, these choke vessels, which initially impede flow from one arterial territory to the next along the flap, enlarge to the caliber of the cutaneous arteries they connect (Figure 4.13).30,31,37,38 However, this process of vessel enlargement is an active event and takes time. It involves multiplication and elongation of the cells in each layer of the vessel wall, with its maximal effect occurring between 48 and 72 hours after operation.30
Experimentally and clinically, it has been noted that one adjacent anatomic vascular territory can be safely captured in any direction on the cutaneous artery at the flap base that defines its reliable clinical territory (Figures 4.13–4.15).30,31,37 If necrosis occurs, it usually does so at the level of the next choke anastomosis in the arterial network or the one beyond. Surgically, flap survival can be extended by the strategic division of vascular pedicles at various time intervals along the length of the proposed flap—the “flap delay” procedure (Figure 4.15).
CLASSIFICATION OF THE CUTANEOUS BLOOD SUPPLY
We have left the contentious subject of classification of the cutaneous blood supply until the end, as we believe it is more important to understand the pure and the applied (functional) anatomy of the cutaneous arteries than to be concerned about which classification is the best. It is essential, however, to differentiate between classifications based correctly on the anatomy and physiology of the cutaneous supply rather than those that focus on flap design, such as axial, random, cutaneous, fasciocutaneous, septocutaneous, and musculocutaneous, each of which describes the method by which the flap is planned and dissected.
One of the oldest, simplest, and best classifications was offered by Spalteholz3 in 1893. He subdivided the cutaneous vessels into two groups, depending on whether they were the main (dominant) supply to the area or whether they had a relatively minor (supplementary) role (see Figure 4.2). Recently this classification has been modified, stimulated by the resurgence of interest on the anatomically based “perforator flaps.”22,24,27,42
Direct Cutaneous Perforator Vessels
These vessels contribute to the primary (dominant) cutaneous supply to the area and are particularly well developed in the limbs. They arise from the underlying source artery or from one of its muscle branches before they enter the muscle. They pass between the muscles and other deep structures in the intermuscular septa and rapidly reach and perforate the outer layer of the deep fascia where their main destination is the skin (Figures 4.2, 4.7, and 4.16). They are usually large and spaced well apart in the torso, head, neck, arms, and thighs, especially where the skin is mobile. They are smaller and more numerous in the forearms and legs except where they accompany cutaneous nerves. In the palms of the hands and the soles of the feet, they are evident as a dense network of small vessels (Figures 4.1 and 4.18).
In each case, these direct cutaneous vessels follow the connective tissue framework of the deep tissue to the skin. They pass between the muscles and tendons supplying branches to them as they pass, sometimes closely related to true intermuscular septa, as “septocutaneous vessels.” If the source artery is close to the surface, for example, the radial, ulnar, or common femoral arteries, then their course to the outer layer of the deep fascia may be short. Conversely, if the source artery is deeply situated then their length is longer, for example, the direct cutaneous perforators of the profunda brachii, lateral femoral circumflex, and peroneal arteries.
When the cutaneous perforators are traced to the underlying source vessels to provide “septocutaneous” perforator flaps, the septum may be well formed, as seen in the lateral arm and thigh, or consist of loose areolar tissue as occurs in the forearm over the radial or ulnar vessels.
Indirect Cutaneous Perforator Vessels
These vessels arise from the source arteries and penetrate the deep tissues, usually muscle, vertically or obliquely before piercing the outer layer of the deep fascia (Figures 4.2, 4.7, and 4.16). They may be quite large and contribute to the primary (dominant) blood supply to the skin and are particularly well developed on the torso (for example, the internal thoracic, intercostal, and deep inferior epigastric musculocutaneous perforators). Alternatively, they may emerge as small “spent” terminal branches to provide the secondary (supplementary) supply to the skin. These are small vessels, often quite numerous, which emerge as terminal twigs of vessels whose predominant supply is to the various deep tissues, especially the muscles.
Whatever their origin and size, these indirect cutaneous perforators provide the basis for the musculocutaneous perforator flaps that require a more tedious dissection with the potential to preserve muscle function. Large or small, they enter, and become continuous with, the same vascular network that is formed by the direct cutaneous arteries. Often the smaller indirect cutaneous vessels are the main blood supply to some musculocutaneous flaps, especially where the skin island is sited over muscle to which it is loosely attached. For example, the gracilis and the gastrocnemius musculocutaneous flaps.
Knowledge of the basic anatomy of the cutaneous vessels coupled with an appreciation of the factors that influence its structure in different regions of the body provides for the logical planning of flaps and incisions. In the sage words of Michel Salmon, “Entre l’anatomie et la physiologie, il y a place pour une anatomie de fonction, pour une anatomie physologique”—“Between anatomy and physiology there is room for a functional anatomy, for a physiologic anatomy.”
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