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I3riri.

d Gourd ofP/asric Surgery (1987),40, 113-141


Q 1987 The Trustees of British Association of Plastic Surgeons

The vascular territories (angiosomes) of the body:


experimental study and clinical applications
G. I. TAYLOR and J. H. PALMER
Department of Plastic and Reconstructive Surgery, Royal Melbourne Hospital and Department of Anatomy,
~n~~~ers~yof ~efbo~rne

Summary-The blood supply to the skin and underlying tissues was investigated by ink injection
studies, dissection, perforator mapping and radiographic analysis of fresh cadavers and isolated
limbs. The results were correlated with previous regional studies done in this department.
The blood supply is shown to be a continuous three-dimensional network of vessels not only in
the skin but in all tissue layers. The anatomical territory of a source artery in the skin and deep tissues
was found to correspond in most cases, giving rise to the angiosome concept.
Arteries follow closely the connective tissue framework of the body. The primary supply to the skin
is by direct cutaneous arteries which vary in calibre, length and density in different regions. This
primary supply is reinforced by numerous small indirect vessels, which are “spent” terminal branches
of arteries supplying the deep tissues.
An average of 374 major perforators was plotted in each subject, revealing that there are still many
more potential skin flaps. Our arterial roadmap of the body provides the basis for the logical planning
of incisions and flaps. The angiosomes defined the tissues available for composite transfer.

Sir Harold Gillies wrote that “Plastic Surgery perforators, assigned them to their underlying
is a constant battle between blood supply and source vessels and charted the cutaneous vascular
beauty’* (Gillies and Millard, 1957)-a struggle territories of the body.
which has not yet been resolved. The speciality of The next major work was performed by Michel
Plastic Surgery evolved in Europe and North Salmon in the 1930s and was published in French
America to improve the lot of the victims of the (1936a). With the aid of X-rays he reappraised the
two Great Wars. With artistic flair and geometrical work of Manchot. He injected entire cadavers with
precision tissues were advanced and rotated. They a mixture containing lead oxide and mapped not
were transposed locally and dispatched to a distant only the entire cutaneous circulation but also the
site on a limb carrier-only to be rebuffed on blood supply of every muscle in the body (1936b).
occasions by necrosis. Gradually rigid length to His work has recently been rediscovered and will
breadth ratios were formulated, because the major- soon be available in English (Salmon, 1987, in
ity o’f these flaps were designed without a precise press).
knowledge of the vessels upon which they were Early this century advances on the clinical front
based. gave significance to the work of these great
This anatomical info~ation was available but anatomists. Tansini reported a latissimus dorsi flap
as is often the case it was hidden in texts in foreign supplied by the thoracodorsal artery in 1906. In
languages, In 1889 Manchot, at the age of 23 1921 Blair described a forehead flap based on the
completed his treatise, Die Hautarterien des Men- superficial temporal vessels and in 1929 Esser
schli~he~ Korpens-the Skin Arteries of”the Body, in published his book, Artery Flaps. In 1937 Webster
the incredible time of 6 months. This anatomical cited the work of Manchot when he described a
landmark has recently been made available in long bipedicled thoraco-epigastric flap based on
English (1983). Since Roentgen was not to make named arteries which extended from the groin to
his discovery until several years later, Manchot did the axilla. Shaw and Payne (1946) utilised the
not have the advantage of radiography. Neverthe- information in wartime to provide one stage direct
less, with an accuracy which has mostly stood the flaps for hand reconstruction. Then in 1965,
test of time, Manchot identified the cutaneous Bakamjian drew attention to the long paramedian
113
114 BRITISH JOURNAL OF PLASTIC SURGERY

perforators of the internal thoracic system. The (iii) Integration of this information with that of
significance of the cutaneous circulation was about other workers.
to emerge into a new era.
Considering the results of our own work and that
The 1970s saw the beginning of the “anatomical
of others, some important anatomical concepts
revolution”. In 1973 McGregor and Morgan differ-
have emerged. They will be listed at this stage as
entiated between large flaps based on a known axial
they provide the basis for a better understanding of
blood supply and those based on random vessels in
the arterial network.
the area. Daniel and Williams (1973) reappraised
the work of Manchot and others, and on an (9 The blood supply of the body courses within
embryological and anatomical basis segregated the or adjacent to the connective tissue framework,
cutaneous arteries into direct cutaneous and mus- whether it is bone, septa or fascia.
culocutaneous vessels. (ii) Vessels course from fixed loci to mobile areas.
“The free flap” (Taylor and Daniel; Daniel and (iii) The vascular outflow is a continuous system of
Taylor) was published in 1973 and in the same year arteries linked predominantly by reduced
the musculocutaneous flap was revived by McGraw calibre vessels-the choke arteries and arter-
and co-workers (McGraw, 1980). Both procedures ioles.
demanded a precise knowledge of the cutaneous (iv) The body is a three-dimensional jigsaw made
vasculature. In the search for new donor sites for up of composite blocks of tissue supplied by
tissue transfer, surgeons scurried back to the named source arteries. The arteries supplying
dissection room. Many new and exciting techniques these blocks of tissue are responsible for the
were developed. However, there was a tendency for supply of the skin and the underlying struc-
these new techniques to neglect the aesthetic side tures. These composite units we have named
of Plastic Surgery. The results could sometimes be ANGIOSOMES.
what the late Frank McDowell (1979) has described
It is hoped that this paper will provide the reader
as “globs and blobs”.
with a basic understanding of the vascular anatomy
To escape from the hamburger of muscle and
which will help clarify nomenclature, aid in the
skin, surgeons soon rediscovered that blood vessels
planning of flaps and incisions and provide the
follow fascial planes. In the 1980s a sleek new
basis for explaining certain pathological processes,
model emerged-the fasciocutaneous flap (Ponten,
1981). Together with this there has been an
explosion of new terms and new classifications of
the cutaneous circulation. These are still in a state The background
of flux, and the thesaurus of flaps includes a The research of this department into the vascular
bewildering array of terms such as axial, random, territories of the body commenced in 1972. Since
direct cutaneous, musculocutaneous, fasciocuta- then over 2000 fresh cadaver studies have been
neous, super and septocutaneous. Indeed there has performed involving dissection, injection and ra-
been a recent attempt to classify flaps into no less diography of various regions, tissues and combina-
than 10 types and subtypes based on the origin of tions of tissues. In each case our anatomical studies
the cutaneous perforators (Nakajima ef al., 1986). were problem orientated. They were designed to
Are these terms all justified, or are they just a provide a surgical solution to patients’ needs.
different expression of the basic cutaneous vascu- Initially the investigations involved an analysis
lature that Manchot and Salmon told us about a of various arteriovenous systems to define possible
century and 50 years ago? donor sites for free skin flap transfer (Taylor and
This paper attempts to answer these questions. Daniel, 1975). Next the studies focused on other
It presents a review of the vascular territories of the tissues and included the anatomical basis for the
body based on : transfer of bone (Taylor et al., 1975) nerve (Taylor
and Ham, 1976) and certain muscles (Taylor et al.,
(9 A reappraisal of the works of Manchot and 1983). Encouraged by the success of some of the
Salmon by a detailed series of dissections and resulting clinical procedures, the research expanded
radiographic studies, performed after total to investigate composite units of tissue, supplied by
body injections in fresh cadavers. a single vascular system. Units of skin and tendon
(ii) A correlation with our previous detailed (Taylor and Townsend, 1979), muscle with nerve
studies of isolated areas of the body. (Taylor 1978) and skin, muscle and bone (Taylor
THE VASCULARTERRITORIES L~NOI~~~MES)OFTHE BODY 115

and Watson, 1978; Taylor et al., 1979a and b) were neous perforators. Initially we used barium sulphate
analysed. It was jiom this work that the angiosome but often the results were unsuitable for publication.
concept germinated. Various regions including the Since 1983 our radiography has been greatly
anterior abdominal wall (Boyd et al., 1984; Taylor improved by using a modification of Salmon’s
et a/., 1984), the anterior thorax (Reid and Taylor. injection mixture (Rees and Taylor, 1986). Both
1984; Palmer and Taylor, 1986), the lower limb and regional and total body studies have produced
the upper limb were then studied. The results added excellent results.
strength to the angiosome concept of the blood Our results in general agree with those of Salmon
supply and revealed the interconnections that exist and Manchot. However, our method differed in
at all levels between adjacent vascular territories, a many respects and our investigations were more
relationship which is evident throughout the body. extensive.
Our methods evolved in three stages. Initially
dissection was used to define vascular anatomy. It
also showed the considerable variability that exists Materials and methods
between individuals and between opposite sides in
This study involved dye injections in 50 fresh
the same individual. It revealed a reciprocity
cadavers, and radiographic investigations in 6
between adjacent arterial territories. When the
whole bodies, 2 amputated upper limbs and 4
vessels in one area were small those in the adjacent
area were large. This has been referred to by amputated lower limbs after each had been injected
in the fresh state with a mixture containing lead
Salmon (1936a) as the “law of equilibrium”.
oxide. Particular attention was paid to those regions
Next, techniques of dye injection were employed.
not previously studied.
The:y were validated in the experimental pig and
then used extensively in fresh cadavers (Taylor and
Dye injection studies
Corlett, 1981). They defined the cutaneous terri-
torie:s and the supply to deeper tissues. Macroscopic An average of four vascular territories were
staining of the tissues and microscopic extent of examined in each cadaver with a range of 1 to 30.
tissue perfusion were assessed. When the vessel of Usually regions were investigated by injecting the
a known flap was injected in the intact body, the source artery (the main distributing artery) of
adjacent territories alternately with red, black or
perimeter of cutaneous staining never extended
purple ink (Fig. 1). The skin staining was recorded
beyond the expected area of survival of the potential
photographically at various stages of the injection
flap. This is explained as follows by “the overflow
and then the deeper tissues were dissected, noting
phenomenon” (Taylor and Corlett, 1981; Taylor,
the course of the vessels and the staining of the
1983).
underlying muscle and bone.
When large volumes of ink were used, the dye
would appear often from the cannula inserted into
Radiographic and perforator mapping studies
an adjacent artery or be seen to escape into the
This was a time consuming exercise and, unlike
major arteries and appear at a remote site such as
Manchot, it took us 2 years to complete. It evolved
the viscera. The reason for this phenomenon is
in four stages : preliminary investigations, whole
revealed in our radiographic studies which illustrate
body studies, examination of isolated limbs and
the reduced calibre choke arterial connections that
cross section assays.
link adjacent vascular territories (Taylor, 1983).
Beca.use there is no pressure buffer effect (McGregor 1. Preliminary investigations. Because of the limited
and Morgan. 1973) from adjacent arteries in the availability of fresh cadavers and the length of each
cadaver, the dye simply follows the line of least study, three important problems had to be solved.
resistance. It is distributed via the branches of the The first was to find a suitable preservative which
artery under investigation until it reaches these could be combined with our lead oxide-gelatin
choke connections. Then it overflows into the mixture and would retain the normal colour and
branches of the adjacent vessels and escapes in texture of the tissues. Various substances were
retrograde fashion via their main trunk. rather than tried, including Salmon’s original mixture, and
perfusing a successive series of linked vascular ultimately chlorocresol was selected. The details of
territories. this study are to be published separately.
Finally, radiography was used to define the exact Next a large radiolucent platform was required
course, distribution and connections of the cuta- which would support the weight of the body and
BRITISH JOURNAL OF PLASTIC SURGERY

Fig. I
Figure l-Fresh cadaver ink injection studies of various source arteries: (A) Internal thoracic and deep inferior epigastric systems.
(B) The same territories on the opposite side injected with different colours plus the deep circumflex iliacs. (C) Two intercostal
vessels injected. (D) Muitiple territories stained (compare with Fig. 16). (E) Right suprascapular, thpraco-dorsal and profunda
territories. (F) Same subject with left posterior circum~ex humeral and circumflex scapular vessels injected.

beneath which X-ray cassettes could be passed cassettes at regular intervals. The grid system was
without moving the subject. This was necessary in designed so that the radiographs overlapped by
order to produce an accurate montage of the area 5 cm around their perimeter. The distance between
under investigation. Various materials were tested the tube of the X-ray machine and the specimen
and 5 mm thick perspex was selected. A supporting was determined to give maximum definition and
platform was constructed by the authors with minimum magnification. It was fixed at 57 inches.
longitudinal parallel rails to guide the X-ray Most radiographs of the integument were exposed
cassettes accurately beneath a grid system marked at 55 to 60 KV, 100 mA for 0.3 seconds.
on the perspex (Fig. 2A). Transverse removable Finally, when planning our incisions, it was
rods were included to interrupt the travel of the important that the skin and attached subcutaneous
THE VASCULAR TERRITORIES (ANGIOSOMES) OF THE BODY

Fig. 2
Figure l--(A) Authors‘ designed piatfor~l with sliding perspex grid to allow radiography without disturbing the subject. Note
parallel rail systems, x-ray cassette and transverse removable rods. (B) Model used to plan one of the methods of skin removal.

tissue could be laid fiat without overlap and that as we wanted to preserve as many of them as possible.
wide an expanse of integument as possible could be We experimented first by removing simulated skin
examined. Previous workers, including Salmon, from plastic models coated with a latex rubber
had made topographical boundary incisions to solution (Fig. 2B). Each pattern of incisions was
remove areas of skin, particularly in the lines of the tested on such a model before the fresh cadaver was
groins, axillae, neck and limb joints. These junc- dissected.
tional regions are of great clinical importance and 2. Total hod~~~t~~~~~.Three adult males and three
118 BRITISH JOURNAL OF PLASTIC SURGERY

females were examined. Those who were very


elderly, had extensive cardiovascular or metastatic
disease, or who had more than 2 surgical scars,
were rejected. Each subject took approximately 3
months to examine. An average of 109 radiographs
were taken in each case and an average of 374
perforators were mapped and traced to their
underlying source vessels. In every study the body
was injected within 24 hours of death and cooled.
The important body landmarks, previous scars
and our proposed incisions were marked with
indelible inks of different colours and photographed
(Fig. 3). The subjects were chosen and the incisions
were planned: to provide a comparison between
sexes; to obtain anterior, posterior, lateral, “bird’s-
eye” and “worm’s-eye” views of the blood supply
to the integument (skin and subcutaneous fat); and
finally, in the last subject, cross-sections of the body
were made to retain continuity of the vessels
between the deep tissues and the skin.
The body was injected via a T-tube placed in one
femoral artery sited at the apex of the femoral
triangle. This left undisturbed the cartwheel of
cutaneous vessels that radiate from this artery in
the groin. The substance was injected in a pulsatile
manner to avoid small vessel rupture (Reid and
Taylor, 1984).
At first 3 to 4 litres of 0.3 per cent chlorocresol
preservative was injected until the superficial veins
became distended. The venous sytem was then
decompressed via cannulae inserted into the exter-
nal jugular veins. Next the lead oxide gelatin
mixture was introduced until its orange colour was
noted in the conjunctival vessels, as mottled patches
in the skin, and within small incisions made in the
pulps of the toes and finger tips. This took
approximately 1 hour. The most difficult areas to
perfuse were the pressure points in contact with the Fig. 3
dissection table. In the first 3 cadavers we massaged
Figure 3-Cadaver with body landmarks and incision lines
these areas during injection but the perfusion was marked.
not complete. Subsequently we adopted the tech-
nique described by Last and Tompsett (1962) and
floated the bodies in a bath. Finally 10% formalin to its outer layer on the other. It must be remembered
was introduced into the cranial, thoracic and that the palmar and plantar aponeuroses are part
abdominal cavities since chlorocresol is relatively of the deep fascia.
ineffective in preserving the viscera. The cutaneous perforators were measured as they
Dissection was deferred until the next day to pierced the deep fascia. In keeping with our
allow the orange radio-opaque mixture to set to a previous studies (Boyd et al., 1984; Palmer and
firm rubbery consistency. The integument was Taylor, 1986) those vessels of 0.5 mm or greater
removed usually as 2 halves in order to preserve in were tagged with lead beads and divided to leave
continuity as wide an area of cutaneous vasculature the lead markers on the surface of the deep fascia.
as possible. In the limbs the integument was raised The perforators were not tagged on the undersurface
superficial to the deep fascia on one side and deep of the integument as their stumps were easily
THE VA~C~.JI_ARTERRITORIES(ANGI~S~MES) OF THEBODY

Fig.4
Figure I---Perforator mapping pins on dorsal aspect of subject.

identified on X-ray. When a long vessel was noted possible and always within S days. While the
it was sutured in the correct orientation. The integument was being studied the body was placed
integument was spread on the perspex platform. in a deep freeze or an alcohol bath. Additional
The cutaneous “carpet” was X-rayed and a montage radiographic studies were made of the pancreas,
of its arterial circulation was constructed using liver, spleen, renal tract, gall bladder with bile
contact photographic prints of the carefully labelled ducts, and representative samplesof bowel, individ-
radiographs (Figs 5,6,7 and 8). ual muscles and nerves. This was done to compare
Next the deep tissues were X-rayed and dissected, the arterial framework of these tissues with each
tracing the tagged cutaneous perforators to their other and with the skin.
underlying source vessels (Fig. 9). The lead beads
3. Isolated limb studies. Four upper limbs and two
were removed and replaced with coloured mapping
lower limbs, amputated for trauma and tumour in
pins, assigning a different colour to the perforators
young individuals, also became available for
of each source artery (Fig. 4). The results were
analysis in the fresh state. They were injected and
photographed and recorded on a master diagram
analysed as described. Because of the age of the
of the body in each case (Fig. 15). The coloured
patients there was no evidence of vascular disease
pins were then matched to the perforators in the
and excellent studies were obtained, especially of
radiographic studies of the integument. The vascu-
the hands and the feet (Fig. 8).
lar territory of the perforator, or cluster of perfora-
tors, arising from each source artery was charted. 4. Cross-section studies. Our radiographs of the
This was done by drawing a line around the integument provided us with a two-dimensional
perimeter of the territories, across the choke vessels “plan” picture of the cutaneous vascular network.
which linked them together (Figs 11, 12, 14 and To define the course of vessels between the deep
16). fascia and the skin, strips were taken from the
Because of the lengthy nature of the investiga- integument of each subject along the axes of
tions, certain steps were taken to deiay tissue decay. selected cutaneous arteries. Particular attention
The body cavities were eviscerated as early as was paid to those areas where the skin was mobile
120 BRITISH JOURNAL OF PLASTIC SURGERY

Fig. 5
Figure 5--Gne of the montages of the cutaneous circulation revealing the continuous network of arteries and arterioles, their origin,
size, orientation and density in different regions of the body. Several pressure areas on the back did not perfuse in this subject. Note
the large perforators in the head, neck, torso and proximal limbs compared with the small closely packed perforators in the forearms
and legs. Note also the long axial vessels radiating from the groins and popliteal fossae.
THE VASCULAR TERRITORIES (ANGIOSOMES) OF THE BODY 121

Fig. 6
Figure &Lateral view of one female subject (A) and anterior view of another (B). The arm has been removed in study (A). Note
the nebvork of large vessels which sweep laterally from the ventral and dorsal midlines, ascend from the groins, descend from the
shoulder girdle and converge on the summits of the scalp and the breasts. This demonstrates the principle that vessels radiate from
fixed concave zones and radiate to mobile convex areas, A lower midline scar interrupts the vessels in subject(B) with compensatory
opening of a large choke vessel above the umbilicus (arrow) to re-establish the flow across the midline.
122 BRITISH JOURNAL OF PLASTIC SURGERY

Fig. 7
Figure ?--“Birds-eye” view of scalp and shoulder epaulette. Note rich choke interconne~ti(~ns between vessels which converge on
the convexity of the scalp (A) and radiate from the concavity at the root of the neck (B). Arrows indicate the elbow joints. and the
clavicle is outlined. The platysma muscle was not included on the right side of the subject which explains the poverty of perforators
in this area.
A

D
Fig. 8
Figure X--Radiographs of the integument of the hands removed with the palmar aponeurosis (A) and without it (B). The blood
supply around the right knee. the distal legs and the feet (C and DJ are shown. The position of the patella is represented (shaded
area). NOZP The high density of perforators in the palm and sole skin. the convergence of vessels over the loose-skinned areas of the
extensor surface of the knee and interphalangeal joints of the fingers. and longitudinal orientation of large vessels which accompanv
the sensory nerves (arrows).
Fig. 9
Figure 9-Radiographs of deep tissues with lead beads locating the dominant cutaneous perforators. Note: (A) The perpendicular
supply to the quadriceps of the thigh versus the oblique supply to the hamstrings. This is due to the different range of movement
between these muscle groups. (B) The continuous arch formed between the anterior and posterior tibia1 arteries. (C) The choke
vessels above the umbilicus which connect the internal thoracic-superior epigastric arteries with the deep inferior systems to
establish the ventral vascular railroad between the clavicles and the groins. Branches of these systems radiate laterally to connect-in
approximately the mid-clavicular line from above down with the acromiothoracic, lateral thoracic, posterior intercostals, lumbar
and ascending branches of the deep circumflex iliac arteries. The territory of one DIEA is defined.
n-

Fig. 1U
Figure IO--- Sectional strip radiographic studies from above down of the breast (A), thigh (B), sole of foot (C) and buttock (D). The fatter includes the ynderlying gluteus
maximus muscle. Schematic diagram illustrates the dominant horizontal axis of vessels which provides the primary supply to the skm m each case and tts relationshtp to
the deep fascia. In Type A they predominate in the subdermal plexus. Note from left to right the internal thoracic perforator and lateral thoracic artery converging on
nipple (arrow) rn the radiograph of this loose skin region of the torso. fn Type B they are seen coursing on the surface of the deep fascia m this relatively tixed 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 glutealf but this time its branches have to pierce muscle directly to reach this tixed skin region. Smalt arrows define the
deep fascia and the large arrow indicates the large fasciocutaneous branch of the &teal artery which descends with the posterior cutaneous nerve of the thigh. E
126 BRITISH JOURNAL OF PLASTIC SURGERY

Fig. 11

Figure 1 l-Sectional studies selected from the abdomen, thorax and thigh revealing the course of the cutaneous and muscular
branches derived from the source arteries in the deep tissues, Note: (top left) The section is taken obliquely along the intercostal-
femoral artery axis showing 2 angiosomes linked by choke vessels at corresponding levels in the integument and deep tissues
(arrows). The cutaneous (i) and muscular branches of the posterior intercostal (I) angiosome connect with the superficial inferior
epigastric (e) and ascending branch of the deep circumflex iliac artery (D). The source artery on the right is the external iliac-
femoral artery trunk. (Bottom left) The internal thoracic artery (arrow) with its anterior intercostal, muscular and cutaneous
branches which sweep laterally to meet the posterior intercostal artery and its lateral cutaneous perforator (arrow). Posteriorly
branches of the posterior intercostal artery anastomose with the circumflex scapular artery at this level (arrows). (Top and centre
right) The dominant cutaneous perforators which arise from the superficial femoral (F), profunda (P) and descending branch of the
lateral circumflex femoral (L) arteries. They reach the skin via the intermuscular septa. (Bottom right) The angiosomes of these 3
source arteries which supply skin, muscle and bone (compare with Fig. 14).
THE VASCULAR TERRITORIES (AN~IOSOMES) OF THE BODY

Fig. 12
Figure I ?---Radiographs of selected regions of the integument and muscles. More: (A) Dotted line drawn around perimeter of choke
connecting vessels of a large acromiothoracic perforator to define its anatomical territory {compare with Figure 5 front view, left
side of body). (B) Chain-linked system of perforators anatomising without change in calibre (arrows). They accompany lateral
cutaneous nerve of arm (compare also with Figure 5 front view, right arm). (C) Trapezius muscle with transverse cervical (above)
and posterior intercostal (below) territories defined. (Compare with their angiosomes in Figure 16.) (D) Latissimus dorsi muscle
with thoracodorsal (above), posterior intercostal (middle) and lumbar territories (below) outlined which again correspond to their
respec%ive angiosomes.
128 BRITISH JOURNAL OF PLASTIC!SURGERY

Fig. 13
Figure 134chematic diagram of a source artery with direct and indirect cutaneous perforators. The direct vessel (D) courses here
in the intermuscular septum to reach the integument, supplying muscle and other deep tissues en route. The smaller indirect
perforators (i) arise as terminal twigs of large arteries to the muscles. Both systems communicate within the connective tissue
framework of the muscles, on the surface of the deep fascia (arrow) and within the integument to form a continuous three-
dimensional network of vessels.

over the deep fascia and to where it was fixed. The studies in order to define the angiosomes of the
strips were cooled until rigid, placed on their side body (vide infra). The ink also outlined the course
and X-rayed to give an elevation view of the vessels of the arteries during dissection. This was of
(Fig. 10). particular benefit when tracing the course of the
Finally, in one body composite blocks of integu- vessels in the integument, as the dye penetrated
ment and underlying deep tissue were sectioned further than the lead oxide-gelatin mixture and
from the torso, the buttocks and from the limbs at reached the capillary bed.
5 cm intervals. This was done to define the course
of the cutaneous perforators from their source Dissection and perforator mapping
arteries as well as the supply to the deeper tissues. The bright orange colour of the lead oxide-gelatin
The specimens were again X-rayed (Fig. 11). mixture facilitated dissection. Perhaps the most
striking feature was the relationship ofthe vessels to
the connective tissue framework of the body. They
Results
followed it closely as if for support and protection.
Our ink injection, dissection, perforator mapping Wherever the connective tissue was rigid they
and radiographic studies complemented each other. hugged its surface. Where the connective tissue was
The results were correlated and then compared loose they travelled within it.
with our previous anatomical studies in fresh No matter which part of the body was studied,
cadavers. This provided an overview of the blood certain principles became clear. Few vessels crossed
supply of the entire body. Some results verify the mobile tissue planes. They crossed where those
observations of other workers, others vary from planes were fused. The vessels radiated from fixed
published material, some confirm our previous to mobile areas. Where mobility existed between
concepts, others offer new ideas. Therefore only the tissues the vessels coursed parallel to the surface for
important anatomical observations which have long distances, usually separated from the plane of
particular surgical significance will be presented. mobility by a sheet of connective tissue of variable
thickness. Sometimes the vessels travelled in a
Injection studies fibrous sheath, but always this tunnel contained
These outlined the cutaneous territories of the loose areolar tissue. Gray’s Anatomy (1980) states
source arteries (compare Figs 1 and 16) as well as the reason for this-it is to allow the veins to dilate
their supply to the deep tissues. This information and the arteries to pulsate.
was coupled with our dissection and radiographic The pattern of supply is well illustrated if the
THE VASCULAR TERRITORIES (ANGIOSOMES) OF THE BODY 129

-._ ._*
/

Fig. 14

Figure 14.- Schematic diagrams showing


how we detined the angiosom~s. IA) The cutaneous perforators with their choke
connectionsare depicted on the left. The origin of these perforators from their underlying source arteries and their muscular
branches is shown on the right. (Bj The vascular territories of each source artery are illustrated in the integument (left) and deep
tissues fright) by lines drawn through the choke connecting vessels. Note that the territories correspond in these 2 layers and ho%
they appear as sectors in the limbs.

arterial network is traced from the heart to the the bones, the nerves and the deep fat deposits, As
periphery. The major arteries are closely related to these vessels divide and subdivide within the
the blones of the axial skeleton, a fact which is specialised tissues, their branches follow the con-
cIearl:y illustrated by the corosion cast studies of nective tissue framework to reflect the architecture
Last and Tompsett (Fig. ISA). Their branches at of the tissue in question,
first radiate from fixed locations to reach the
viscera, or follow the intermuscular septa to supply
Classification of the cutaneous blood supply
the musculo-skeletal tissues and the integument.
In the deep tissues the branches penetrate the The course of the cutaneous perforators depends on
muscles, usually on their deep surface, the tendons, the proximity of the source artery to the undersur-
BRITISH JOURNAL OF PLASTIC SURGERY

Figure 1S-The dominant cutaneous perforators emerging from the deep fascia with different colours identifying their corresponding
source arteries in the deep lavers (compare with Figure 16). Note their relationship to the intermuscular and the intramuscular
septa. This result was aveiageh from all-our studies. -

face of the deep fascia. In each case they follow the purpose is to supply the muscles and other deep
inte~us~ular and the intramuscular septa, supply- tissues. They reinforce and interconnect with the
ing branches to each tissue as they pass by. They primary supply to the skin. They are sparse where
fall broadly into two groups: (i) direct and the muscle pistons beneath the deep fascia and are
(ii) indirect (Fig. 13). This classification was de- plentiful where the muscle is fixed to that structure.
scribed originally by Spalteholtz (1893) and has The direct cutaneous vessels arise:
been reviewed recently by Timmons (1985). (i) From the source artery as it courses just
Direct vessels beneath the deep fascia-for example the
The direct vessels constitute the primary cutaneous superior ulnar collateral artery; the superficial
supply. Whether they follow the intermuscular inferior epigastric artery; and the cutaneous
septa, or pierce muscles en route, their main perforators of the transverse cervical, radial
destination is the skin. and plantar arteries.
(ii) As a direct continuation of the source artery-
I~d~reet vessels for example the cutaneous branches of the
The indirect vessels constitute the secondary cuta- internai and external carotid vessels, such as
neous supply. They emerge from the deep fascia as the superficial temporal and the supratrochlear
terminal spent branches of arteries whose main arteries.
3 (Anti :OSOMES) OF THE BODY

Figure L&-The angiosomes of the source arteries of the body coloured to correspond with Figure 14. They are: (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, (I I) Posterior circumflex humeral. (12) Circumflex scapular. (13) Profunda
brachii, t 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) Surai, (24) Peroneal. (25) Lateral plantar,
(26) Anterior tibial, (27) Lateral femoral circumflex, (28) Adductor (profunda), (29) Medial plantar. (30) Posterior tibia],
(31) Superficial femoral, (32) Common femoral, (33) Deep circumflex iliac, (34) Deep inferior epigastric, (35) Internal thorncic.
(36) Lareral thoracic, (37) Thoraco-dorsaf, (38) Posterior interosseous, (39) Anterior interosseous, (40) Internal pudendal

{iii) From a deeply situated source artery, or one of The direct cutaneous perforators pierce the outer
its branches to a muscle. They follow the layer of the deep fascia near where it is anchored to
intermuscular septa to the surface-for exam- bone or to the intermuscular and large intramuscu-
ple the cutaneous branch or branches of the lar septa (Figs 4, 5 and 15). These lines and zones
circumflex scapular and lateral circumflex of fixation also correspond to the fixed skin areas of
femoral vessels. the body. They are easily seen in a thin, well
(iv) From the source artery as it courses on the muscled individual as grooves and valleys around
undersurface of a muscle. A single large vessel the perimeter of muscles-especially where they
olr a number of vessels are given off and each interdigitate, over well developed intermuscular
pierces the muscle vertically or obliquely to and intramuscular septa, over the flexor surface of
reach and penetrate the deep fascia. For joints, adjacent to the dorsal and ventral midlines
example the cutaneous perforators of the of the body, around the base of the skull and in the
internal thoracic, intercostals, deep inferior region of some bony prominences.
epigastric and the gluteal vessels. From these grooves and valleys in the deep fascia
132 BRITISH JOURNAL OF PLASTIC SURGERY

The size and density of the direct perforators


vary in different regions. In the head, neck, torso,
arm and thigh the vessels are larger, longer and less
numerous. In the forearm, leg, dorsum of the hands
and feet, the vessels are generally smaller, shorter
and more numerous. In the palms of the hands and
the soles of the feet, perhaps the most fixed skin
areas of the body, the density of perforators is at a
maximum. Thus the primary supply to each
cutaneous territory varies between source arteries.
It ranges from a small number of large direct
perforators to a large number of smaller direct
vessels (Figs 5, 6, 7 and 8). Each territory is
reinforced by indirect perforators.
The course of the cutaneous vessels between the
deep fascia and the skin also varies in different
regions. Nevertheless they follow the connective
tissue framework of the superficial fascia, intercon-
necting at al1 levels. They ramify on the undersur-
face of the subcutaneous fat adjacent to the deep
fascia and then branch and course towards the
subdermal plexus, worming their way between the
fat locules. The smaller vessels in general course
vertically towards the skin. The larger vessels either
E branch in all directions in stellate form or course in
a particular axis, branching as they pass parallel to
the skin surface.
Fig. 17 In the scalp and in the extremities where the skin
Figure 17-Diagram showing how the size and course of the is relatively or rigidly fixed to the deep fascia the
direct cutaneous perforators X and Y. which emerge from fixed larger vessels hug that surface. They course on the
points in the deep fascia. couId be rn~~~ed by growth either deep fascia for a considerable distance in the loose
before or after birth. In (A) the perforators, which are fixed in
number and position, form a major connecting network on the
areofar Iayer that separates it from the subcutaneous
surface of the deep fascia in the “resting state”. In (B) they are fat (Figs IO and 11). This is evident particularly
stretched with the deep fascia by the expansion of underlying where the perforator accompanies a cutaneous
tissues-for example the scalp vessels as the brain and skull nerve. Frequently several vessels interconnect in
expand during foetal development. In (C)as the breast develops chain link fashion to follow a nerve, anastomosing
~ifhj~ the integument the vessels are displaced towards the
dermis and lengthened as they converge on the nipple. In (D) without change in calibre (Figs 8 and 12).
they are stretched apart in the limbs as the long bones graw, but In the loose skin areas of the body, especially
stili retain their original relationship to the deep fascia. In (E) over the pectoralis major muscle, the iliac fossa and
the vessels are again stretched apart by growth but the mobile the extensor surface of joints, the direct cutaneous
relationship between the under surface of the integument and
the deep fascia is responsible for their oblique course. This is
vessels course for a variable distance parallel to the
characteristic of the loose skin areas of the torso. deep fascia. However, they are more intimately
related to the undersurface of the su~utaneous fat
and are plastered to it by a thin glistening sheet of
the vessels flow towards the convexities of the body fascia which separates them on their deep surface
surface, branching within the integument. The from a plexus of smaller vessels. This plexus of
wider the distance between the concavities and the smaller vessels lies in loose areolar tissue on the
higher the summit, the longer the vessel. For surface of the deep fascia. It is formed by branches
example: the blood supply of the breast, nose, ears, which arise from the direct perforators as they
genitalia, the extensor surface of the joints and over pierce the deep fascia, and the connections these
the surface of bulging muscles. This pattern of branches make with smaller indirect perforators
supply is clearly shown in our radiographic studies (Fig 17). The large direct perforators then pierce
(Figs 5 to 11). the subcutaneous layer. They ascend obliquely
THE VASCULAR TERRITORIES (ANGIOSOMES) OF THE BODY

Fig. 18
Figure I8-_( A) Tompsett‘s corrosion cast of the arteries in a stillborn baby. Note how the major vessels relate to the bony skeleton
of the body. Reproduced by kind permission from the Department of Anatomy, Royal College of Surgeons of England. (B) The
wing of a moth with its superstructure of “veins” which interconnect and nourish the part. Note the resemblance to the mesenteric
vessels in the human gut

within the superficial fascia to reach the rich linked to form a continuous network of t)essels
subdermal plexus, where they travel for considera- regardless of the tissue. Some connections are true
ble distances (Figs 10 and 11). anastomoses without change in calibre, for example
between the dorsalis pedis and the posterior tibia1
Radiographic studies artery, between some posterior and anterior inter-
These investigations provide the basis for a three- costal arteries (Fig. 9) and to a lesser extent in the
dimensional arterial atlas of the body (Figs 5 to 12). muscles and in the integument. More commonly
They confirm the origin and course of the direct the connections are formed by reduced calibre
cutaneous perforators (vide supra) as well as vessels-the choke arteries and arterioles (Fig. 12).
demonstrating their density in different areas of the As the calibre of the arteries decreases the number
body. The most striking observation, however, is of connections increases.
that adjacent source arteries and their branches are The blood supply to the integument is revealed
134 BRITISH JOURNAL OF PLASTIC SURGERY

as a continuous three-dimensional mesh of vessels, artery. The latter 2 groups of arteries are
contributed to at fixed skin sites by the entry of derived from the internal maxillary artery but
cutaneous perforators. It spans the entire body like all 3 are derived directly or indirectly from the
a national map of roadways and subways made up terminal bifurcation of the external carotid
of interconnecting channels of all sizes. It is system. In other words, the angiosome is the
subdivided into anatomical vascular territories by composite block of integument, muscle, peri-
the perimeter of choke arteries which connect the cranium, bone and dura supplied by the distal
perforators of a source artery with those of its part of the external carotid artery-the terminal
neighbour (Figs 12 and 14). external carotid artery angiosome.
In the deep tissues a similar pattern exists. The (ii) The territory of the superficial inferior epigas-
branches of the source arteries are linked within tric artery (SIEA). The common femoral angio-
the various tissues, usually by choke vessels. In the some (Figure 16) can be subdivided into smaller
muscles they often exhibit a characteristic cork- angiosomes. The ascending branch of the deep
screw appearance (Figs 9, 11 and 14). circumflex iliac artery (DCIA) is the deep tissue
counterpart of the SIEA (Fig 11 top left). The
The angiosome concept continuation of the DCIA is the counterpart of
the superficial circumflex iliac artery (SCIA).
We compared the territory supplied by a source Unfortunately the deep vessels arise from the
artery in the deep tissues with its territory in the terminal part of the external iliac artery and
overlying integument and found that their per- the cutaneous perforators arise from the begin-
imeters often coincided (Figs 11 and 14). This ning of the common femoral artery. Terminol-
composite unit of skin and underlying deep tissue, ogy again obscures the angiosome concept.
supplied by a source artery, we have named an
ANGIOSOME*. The angiosomes of the body were Other important observations from our radiog-
then plotted, based upon the combined results of raphy studies should be noted. The first is the dense
our ink injection, dissection, perforator mapping network of vessels in the scalp, face, axillae, breasts,
and radiographic studies (Figs 14, 15 and 16). paraumbilical region, perineum, palms of the
Though the boundaries of these anatomical hand and soles of the feet. Many of these corre-
territories are shown as lines, they represent the spond to the areas that sweat most profusely
middle of choke zones. They outline the vascular (Figs 5 to 8).
territories of the integument and the deep structures, The second observation is that there is a dominant
e.g. muscles, nerves and peritoneum. It is clear axis of vessels coursing parallel to the body surface
from our studies that some muscles will be wholly which supplies direct vessels to the skin. The depth
contained within one angiosome, e.g. thenar; many of this arterial axis varies in different regions and is
span at least two angiosomes, e.g. rectus abdominis fundamental to skin flap design (Figs 10 and 11). It
and gluteus maximus; but the majority traverse may be seen :
more than two, e.g. the latissimus dorsi, pectoralis (9 In the subdermal plexus. This is characteristic
major and sartorius muscles. of the loose skinned areas (see Figs 10A and
There is a close correlation between the angio- 11 top left).
somes and the neurological dermatomes on the (ii) On the surface of the deep fascia. This is
torso and in the head. In the extremities this is less typical of the blood supply to the scalp, the
evident where the angiosomes appear as sectors thighs and the arms, where the skin is fixed to
(Figs 11 and 14). Sometimes the angiosomes concept the deep fascia (Fig. 10B).
is clouded by nomenclature. For example : (iii) Beneath the deep fascia. This is apparent
(i) The territory of the superficial temporal artery. where the source artery itself is the dominant
This fan-shaped territory overlies a similar vessel which courses parallel to the skin surface
territory supplied by the deep temporal vessels. and gives off a series of perforators. It may
This in turn overlies a comparable territory in course just beneath the deep fascia, e.g. medial
the dura supplied by the middle meningeal plantar artery (Fig. lOC), beneath or within
an intermuscular septum (for example the
radial and ulnar arteries), or beneath a muscle
*From the Greek angio- meaning vessel, and somite meaning which intervenes between it and the deep
segment or sector of the body (derived from soma, body) fascia (Fig. 1OD).
THE VASCULAR TERRITORIES (AN~IDSOMES~ OF THE BODY 135

tissues of the adjacent angiosome can be captured


We did not inject the venous system in this study. with safety. Necrosis tends to occur in the next or
However in each instance during dissection venae subsequent angiosome. This presumably is due to
commitantes were noted accompanying the cuta- the pressure gradient that must occur as blood flows
neous arteries. A further investigation is under way across the choke vessels that link adjacent arterial
to complete the picture, prompted by the work of territories. We have noted in our pig experiments
Costa et al. (1987). that it is these choke connecting arteries and
arterioles which dilate when a skin flap is delayed.
In the developing embryo the vascular system is
Discussion
the first tissue to differentiate in the mesoderm. It
Carl Manchot (1889) defined 40 cutaneous terri- commences as a syncytium of interconnecting
tories in his study of the blood supply to the skin. vascular channels. Although modified by the differ-
He did this with remarkable accuracy considering entiation, growth and migration of the specialised
that he did not have the advantage of X-rays. He tissues, this network arrangement of vessels is
excluded the head, neck, hands and feet in his retained into adulthood. Some vessels obviously
chart. Salmon (1936a) defined more than 80 skin have disappeared and others have enlarged.
territories which covered the entire body. Both GraqlS Anatomy (1958) states that the connective
gave very accurate descriptions of the origin and tissue is what is left of the mesoderm, after the
course of the cutaneous vessels and Salmon revealed specialised tissues have developed from it. It is
the interconnections that exist between ‘adjacent interesting that the connective tissue framework
cutaneous arteries. Salmon (1936b) also went a step and the vascular system co-exist as an interconnect-
further and in a separate study examined the ing network in the adult. If the specialised tissues
individual muscles. He showed that each muscle is such as muscle, nerve, fat and bone have developed
supplied by a variable number of source arteries within this mesh of connective tissue and vessels,
which interconnect within it. then this would explain why vessels have become
However. neither of these workers illustrated the captured within, and compressed between, the
course of the arteries between the deep tissues and specialised tissues. It would explain why they follow
the skin, they did not define the vascular territories the intermuscular septa, the intramuscular septa,
of the source arteries in the deep tissues, nor did the deep fascia and the connective tissue scpta of
they correlate these territories with their counter- the superficial fascia to reach the skin. As mobility
parts in the overlying integument. Salmon hinted develops between tissue planes then presumably
that a relationship existed between these layers, but some of the interconnections between vessels would
neither he nor Manchot could have envisaged the have been lost, with a compensatory enlargement
anatomical demands of modern flap surgery with of vessels at fixed tissue sites. However, this requires
the need to correlate the blood supply between the further research since most of the studies of human
integument and the deep tissues. development have been inferred from data obtained
Our studies have gone this stage further. The from the developing chick embryo.
angiosomes are the composite blocks of tissue Another concept which was suggested by John
supplied by named source arteries which span Hunter two centuries ago (1794) is that at some
between the skin and the bone. Crock (1967) has stage of foetai development, and certainly at birth,
demonstrated the connections that occur in the the body has a fixed number of arteries. This has
bones. Each tissue in an angiosome is supplied by been our impression when comparing the number
branches of the source artery. We have described of cutaneous perforators seen in children and in
40 angiosomes, but many can be subdivided into adults when raising various flaps. If this is so, and
smaller segments; for example the common fem- remembering that thecutaneousperforators emerge
oral, popliteal and posterior intercostal territories. from the deep fascia at predetermined sites. then
Adjacent angiosomes are interconnected in each the orientation of the cutaneous arteries is the
tissue layer. whether it be skin, fat, muscle, nerve product of the differential growth that has occurred
or bone, usually by reduced cafibre choke arteries. in that area from some stage in foetal development
When we consider these anatomical territories in to adulthood. It explains why vessels radiate from
the light of clinical experience it can be seen that in concavities and converge on convexities and why
most cases when a flap is based on the vessels of the vessels in some areas are small and close
one angiosome, then the corresponding tissue or together while in others they are large and spaced
136 BRITISH JOURNAL OF PLASTIC SURGERY

well apart (Figs 5,6,7 and 8). There are numerous 1. The axes of skin jups. Our arterial atlas of the
examples which support this hypothesis (Fig. 17). integument details the origin, course, size, density
The sternomastoid and trapezius muscles split from and interconnections of the cutaneous perforators.
the same somite (Patten, 1968). The trapezius It therefore provides for the logical planning of the
“drags” its supplying transverse cervical artery base and the axis of a flap. It is obvious from our
(and nerve) across the root of the neck to the back, studies that there are many more axial flaps
together with a large band of skin which the artery available for transfer than have been described to
nourishes. Manchot suggested that the long course date. Several of these are included in Figure 20 with
of the superficial superior and inferior epigastric the known flaps.
arteries is the result of extension of the torso of the The cross-sectional studies confirm the reason
foetus. The expansion of the brain stretches the for including the outer layer of the deep fascia with
scalp vessels from the base of the skull towards the flaps raised in the scalp and in the extremities, for
vertex. Similarly the vessels converge on the nipple in these situations the vessels hug the fascia for
from all directions as the breast develops. The considerable distances. If a flap is designed along
pattern is seen also in the limbs. As the epiphyses the course of a cutaneous nerve, such as the
of the long bones grow the arteries are stretched saphenous or the sural nerves, then very long safe
apart. Notably they radiate from the flexor surface flaps can and have been elevated. Ponten’s (1981)
of joints, an observation well illustrated in our original flaps were designed in this way and we
studies (Figs 5 and 8). planned our saphenous neurovascular flap in a
A final concept was documented again by John similar manner (Acland et al., 198 1).
Hunter (1794). He noted the anastomoses that In the loose-skinned areas of the torso, which can
occur between arteries, quoting the vascular arcades be gauged by the pinch test, it is unnecessary to
in the hands and feet as examples, and stated that include the deep fascia as the cutaneous arteries
the arcades occur more frequently as the arteries course at an early stage within the integument.
become more distal. The arterial arcades in the Frequently they correspond with the course of a
bowel mesentery are a classic example. They are cutaneous nerve (Badran et al., 1984). By comparing
smaller and more numerous as they approach the our radiographic studies of the vessels in the
intestine. This basic pattern exists in all tissues and integument with the course of the cutaneous nerves
is modified by the function of that tissue. Even as depicted in Grant’s Atlas of Anatomy (1958), a
during tissue repair the pattern of vascular arcades remarkable resemblance in orientation of the
is reproduced in granulation tissue. cutaneous arteries and nerves is evident.
Comparison of the vascular architecture in the Finally, if it is retnembered that the large
human with that of other animals and other species cutaneous vessels emerge from the deep fascia
reveals a similar arrangement of arcades. In the predominantly around the perimeter of muscles,
loose-skinned animals the arcades in the integu- we have found in lean individuals that the Doppler
ment are stretched over long distances (Fig. 19). In probe is a useful aid to locate these perforators. If a
the wings of insects and in the leaves of plants the line is drawn to join two such perforators and the
“veins” assume a similar pattern of interconnecting skin between is mobile, then in our experience a
arcades to those of the intestinal mesentery (Fig. safe flap can be planned along this axis. This is of
18B). particular use on the torso and especially on the
back.

Clinical applications 2. Skin flap dimensions. Since the blood supply of


the integument has been shown to be a continuous
It would be presumptuous of us to suggest that the
system of linked vascular territories, the survival
anatomical information that we have provided is
length of a skin flap must depend upon :
completely original or a definitive work on the
blood supply to the skin and underlying tissues. (i) The calibre and length of the dominant vessel
Rather it is an attempt to correlate the efforts of upon which the flap-is based
many workers, to provide some concepts which will (ii) The calibre and span of the adjacent captured
stimulate further research, to aid in the design of artery or arteries
skin flaps and incisions, and to simplify nomencla- (iii) The calibre and length of the connecting choke
ture. Some of the applications of the anatomical vessels
information will be considered briefly : (iv) An adequate venous return
THE VASCULAR TERRITORIES (ANGIOSOMES) OF THE BODY 13:

B
A

Fig. 19
Figure 19-The cutaneous blood supply of the rabbit. Note the large long vessels which course in the loose-skinned area of the torso,
their choke connections, and their origin from the fixed skin areas of the axillae and the groins.

In most instances the skin flap is endowed with tered, for example, with island neurovascular flaps
a rich dual system of superficial and deep veins. raised from a digit.
Problems may arise, however, with an island skin If the arterial perforators are large and widely
flap. The superficial veins are disconnected and the separated, the territory of each is big and a long
venous return may be thrust upon a diminutive flap can be raised with safety. These flaps are
deep system. This problem is sometimes encoun- characteristic of the loose-skinned areas of the torso
138 BRITISH JOURNAL OF PLASTIC SURGERY

Fig. 20
Figure 20-Some of the large axial cutaneous Aaps which have been used, or are available, as defined by our radiographic studies of
the integument. In the scalp and the limbs they should include the deep fascia. (Compare with Figures 5-8 and 14.)

and of the scalp. Conversely if the perforators are the dominant axis of vessels which course parallel
diminutive and close together, the territory of each to the skin surface in different areas of the body.
is small. The viable length of the flap is short unless However, the concept of septocutaneous vessels is
the underlying source vessel is included in the not original and is illustrated by many of the early
design. This is very evident in the fixed skin area of anatomists (Quain and Wilson, 1842; Grant, 1958).
the sole of the foot. Cormack and Lamberty (1984) have added much
Where very large flaps are required, or where to the knowledge of the anatomy of the cutaneous
vessels of a large calibre are necessary for microvas- perforators and have suggested a classification of
cular anastomoses, these requirements can be fasciocutaneous flaps.
satisfied by chasing the perforators via the inter-
muscular septaor the intramuscular septa to include 3. Fasciocutaneousjups. It is interesting how these
the underlying source vessels. The intelligent use-of flaps have evolved. In many ways we have
a delay will also allow safe capture of adjacent historically come full circle. The senior author was
vascular territories. Many studies of these septocu- taught by Sir Benjamin Rank, as a dictum from Sir
taneous vessels have been made and have resulted Harold Gillies, always to take the deep fascia with
in various flap designs (Shanahan and Gingrass, a skin flap in the extremities, and especially in the
1979; Song&al., 1982; Carriquicyetal., 1985). The lower limb. The flap was safer if you did so. The
principles are outlined in Figure 10 which highlights precise vascular basis, however, was not known.
THE VASCULAR TERRITORIES (ANGIOSO~ES) OF THE BODY 139

We then laboured through many bulky musculocu- perforators of the feeding artery or those in the
taneous flaps, some of which have been major adjacent muscular territory. Attempts to capture
contributions. Now thanks to Ponten we have territories beyond that in either muscle or skin,
returned to rediscover an old friend. However, this without prior delay, frequently result in vascular
time we know why the flaps are safer in the limbs insufficiency. This situation may prevail for exam-
when the deep fascia is included. ple in the pectoralis major and the lower transverse
Nevertheless too much emphasis has been placed rectus abdominis (TRAM) flaps.
on the intrinsic value of the blood supply of the
deep fascia. Every experienced surgeon knows that 5. Composite japs. A knowledge of the supply of
when the deep fascia is exposed it desiccates, all of the tissues which constitute each angiosome
sloughs and granulates with reluctance. Our studies provides the basis for the transfer of composite
show that the dominant vessels course adjacent to units of skin, muscle, nerve, tendon and bone
the surface of the deep fascia, not within it. With supplied by a single arteriovenous system. This
care they can be dissected free. Inclusion of the knowledge has been applied extensively in free
deep fascia with the overlying integument simply composite tissue transfer.
avoids such a tedious dissection. It also preserves The vessels within the angiosome interconnect
the a.djacent subfascial course of arteries in some between the various layers. This interconnection is
situations. well illustrated with the transfer of composite tissue
The term “fasciocutaneous” flap is the subject of from the groin region. The direct cutaneous
much debate. PontCn included the deep fascia in perforators of the SCIA interconnect with the
his description of the flap. It is a well defined sheet indirect perforators of the DCIA. When a compos-
in the limbs but in certain regions is continued as ite osteocutaneous flap is based on the deep system,
the periosteum of the tibia, the ligaments of joints, the perforators of the DCIA capture the territory
the external oblique aponeurosis, the lumbar fascia of the SCIA to perfuse the skin (Taylor et al, 1979a).
and the rectus sheath-to cite just a few examples When the superficial system is utilised the reverse
where its structure is modified. Therefore we must applies to perfuse the anterior segment of iliac crest
be careful when we apply the term fasciocutaneous and the attached muscles (Taylor and Watson,
to these regions. 1978).
We must also remember that there is a superficial 6. Hypervascular and hypovascular planes. These
fascia, stuffed with fat pellets, which connects the have been referred to in considerable detail by
dermis to the deep fascia. Perhaps then we should Michel Salmon. The fixed skin areas of the body,
name flaps raised above the deep fascia as superjicial which mark the sites of emergence of the dominant
fasciocutaneous flaps and those which include the
cutaneous perforators, constitute the hypervascular
deep fascia as deep fasciocutaneous$aps. We are zones. Where the skin is mobile over the deep
reluctant to suggest new terminology but it would fascia or skull, or where muscles slide freely beneath
certa:inly clarify the structure of the many new the deep fascia, few small vessels cross these gliding
“fasciocutaneous” flaps which are appearing in the planes. These are the hypovascular planes which
literature. are often used by surgeons to minimise blood loss.
The placement of a breast prosthesis beneath the
4. Musculocutaneousj?aps. It is apparent from our mammary gland or the pectoralis major muscle
studies that in many situations the cutaneous paddle takes advantage of this fact.
of a musculocutaneous flap is fed by small indirect
perforators. Where the skin and deep fascia are 7. The venous drainage ofjlaps. The anatomy of the
firmly bound to the underlying muscle, for example deep venous system was noted during our dissec-
the gluteus maximus and the latissimus dorsi tions, but the veins were not injected and studied
muscles, the blood supply to the skin is ensured. At radiographically. Costa et al. (1987) have studied
each fixed site over the muscle vessels emerge, some the venous drainage of the TRAM flap. They have
large and some small, to supply the integument. highlighted the fact that there are choke veins as
However where the muscle is mobile beneath the well as arteries connecting corresponding territories
deep fascia, for example the gracilis muscle, the in the muscle. They have also revealed that the
cutaneous supply is at best tenuous. initial venous return from the skin paddle is against
In general, musculocutaneous flaps can be raised the valves when the skin paddle is based distally.
safely if the skin paddle is placed over the This is due to the fact that the venous drainage of
140 BRITISH JOURNAL OF PLASTIC SURGERY

the captured territory is in the opposite direction to Costa, M. A. C., Carriquiry, C., Grottiag, J. C., Herrera, R. H.,
Vaxoaez, L. 0. and Wiadle, B. H. (1987). An anatomical
that of the vein in the ilap pedicle. This opens a studyofthevenousdrainageofthe transverserectusabdominis
new avenue of research. musculocutaneous flap. Plastic and Reconstructive Surgery, In
Press.
Crock, H. I. (1967). The Blood Supply of the Lower Limb Bones.
Conclusion Edinburgh: E. and S. Livingston Ltd.
Daniel, R. K. and Taylor, G. I. (1973). Distant transfer of an
Our ink infusion and total body injection, dissection island flap by microvascular anastomoses. Plastic and Recon-
and radiographic studies provide an overview of structive Surgery, 52, III.
the blood supply of the integument and the Daniel, R. K. and Williams, H. B. (1973). The free transfer of
underlying tissues. They confirm the works of skin flaps by microvascular anastomoses. Plastic and Recon-
structive Surgery, 52, 16.
Manchot and Salmon and go a stage further to
Esser, J. F. S. (1929). Artery Flaps. Antwerp: De Vos-van Kleef.
develop the concept of the angiosome which is GiUies, H. D. and Miiard, D. R. (1957). The Principles and Arr of
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We are grateful to Professor Gordon Clunie and Professor
Translated by Ristic, J. and Morain, W. D. New York:
Graham Ryan for their guidance and for the assistance given by
Springer-Verlag.
their respective Depa~ments of Surgery and Anatomy at The
University of Mel~ume; to Mr Douglas McManamny, Mr M&raw, J. B. (1980). The recent history of my~utaneous flaps.
Russell Corlett and Dr Gary Crossthwaite for their assistance Clinicf in Pfastic Surgery, 7, 3.
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The Royal Australasian College of Surgeons and The Buckland Nakajima, H., Fqjino, T. and Adachi, S. (1986). A new concept
Foundation for their grants to fund our research. of vascular supply to the skin and classification of skin flaps
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The Authors
Taylor, G. I. and Watson, N. (1978). One stage repair of G. I. Taylor, FRACS, FRCS, Consultant Plastic Surgeon, Royal
compound leg defects with revascularised flaps of groin skin Melbourne Hospital.
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Requests for reprints to: Mr G. Ian Taylor, 766 Elizabeth Street.
Superiority of the deep circumflex iliac vessels as the supply
Melbourne 3000, Australia.
for free groin flaps: experimental work. Plasticand Reconstruc-
tive Surgery, 64, 595. Received 30 August 1986.

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