Pediatr Surg Int (1996) 11:290-295

Springer-Verlag 1996

O. Enjolras J. B. Mulliken

Vascular cutaneous anomalies in children:

malformations and hemangiomas

Abstract The vast majority of cutaneous vascular anoma-

lies in infants and children are either malformations or

hemangiomas. Vascular malformations are subgrouped,
based on channel morphology and rheology: slow-flow
(capillary, lymphatic, venous, or combined-complex
types) and fast-flow malformations (ectasia, aneurysm,
fistula, or arteriovenous anomalies). Noninvasive radiologic
techniques, especially ultrasonography with Doppler flow
studies and magnetic resonance imaging, serve to document
the extent and flow characteristics. Management depends
on the type of malformation: laser for capillary malformations; surgical excision for lymphatic malformations; compression, sclerotherapy, and resection for venous malformations; and embolization and/or surgical resection for arteriovenous fistulae/malformations. Hemangiomas are the
most common tumors of infancy. The life cycle is divided
into three phases: proliferating, involuting, and involuted.
Most hemangiomas do not require treatment, although drug
therapy is indicated for endangering or life-threatening
hemangiomas. Corticosteroids (either systemic or local)
and alpha-2a interferon are currently the most effective
agents. Surgical resection of problematic hemangiomas can
be undertaken during infancy, the preschool years, or childhood.
Key words Vascular malformation Hemangioma MRI
Embolization Sclerotherapy

Introduction
Based on clinical features, hemodynamic characteristics,
natural behavior, and histologic differences, there are two

major categories of superficial vascular anomalies (VA):

vascular malformations (VM) and hemangiomas [1-3].
VMs are composed of dysplastic vessels exhibiting a
normal endothelial turnover. Most of these anomalies are
visible at birth, although some are subtle cutaneous birthmarks that may go unnoticed in early childhood. VMs grow
commensurately with the patient, however, some can enlarge suddenly or progressively worsen over a lifetime.
Hemangiomas are exclusively a pediatric problem.
These benign tumors of the blood capillary networks are
characterized by rapid postnatal growth of endothelial cells,
pericytic nests, and capillaries (the proliferating phase),
followed by slow, spontaneous, invariable regression (the
involuting phase). Hemangiomas are the most common
tumors of infancy and childhood; they always regress,
and never appear in adolescents or adults.
Although VMs and hemangiomas are totally different
pathologic entities, they are often discussed adjacent to one
another in the literature. The aim of this paper is to review
the evolution, differential diagnosis, and therapy of these
two distinct major categories of VAs.

Vascular malformations
Depending on the type of malformed vascular channels and
their flow characteristics, superficial VMs can be separated
clinically into capillary malformations (CM) (port-wine
stains and telangiectases), venous malformations (VeM),
lymphatic malformations (LM), arterial malformations
(AM) (aneurysms, ectasias, stenoses, rare in the skin
area), and various complex combined slow-flow and fastflow forms. In the latter category, arteriovenous malformations (AVM) (with AV fistulae) deserve special commentary).

o. Enjolras (~)
H6pital Cochin, Department of Dermatology, Pavillon Tarnier,
89 rue d'Assas, F-75006 Paris, France

Capillary malformations

J. B. Mulliken
Children's Hospital, Division of Plastic Surgery, Harvard Medical
School, 300 Longwood Avenue, Boston, 02115 MA, USA

Port-wine stains are the most common CM. These are

obvious at birth as red, clearly delineated skin or mucosal

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Fig. 1 Venous malformation in the hand of a 10-year-old girl

Fig. 2 Venous malformation in the knee joint of an adolescent:
operative finding (Dr Claude Lanrian, Paris)
Fig. 3 T2-weighted MRI sequence; bright hypersignals visualize
venous malformation of skin and muscle
Fig. 4a Adolescent male with venous malformation of upper lip;
b 1 year after two injections with 1% sotradecylsulfate and subsequent
contour excision

stains. They consist of ectatic capillaries in the papillary

and upper reticular dermis. They grow commensurately
with the skin and never regress. In time, particularly in
the facial area, some CMs develop a purple or coppery
color with dermal thickening, ectasia, and nodular elevations.
Investigation is not required to diagnose a CM. However, it may be a red flag signalling a more complex
syndrome [1-3]. Therefore, diagnostic examinations are
considered and chosen depending on the following clinical
presentations: complex combined VMs of the limbs and
trunk; Klippel-Trenaunay and Parkes Weber syndromes;
Proteus syndrome; phacomatosis pigmentovascularis; skin
markers for occult spinal dysraphism; or Sturge-Weber
syndrome.
CMs are a cosmetic problem best treated by laser; the
pulsed-dye and continuous-wave lasers are presently the
most efficacious.

Venous malformations
VeMs are present at birth, sometimes as an obvious spongy
blue mass, but more often as bluish patches in the skin.
They progressively enlarge and slowly worsen throughout
childhood and adolescence, and to a lesser degree in
adulthood. Their characteristic blue color is due to ectatic
venous channels in the dermis. There is no increased local
heat, bruit, or thrill on palpation. VeMs are easily compressed manually. Phleboliths are pathognomonic; they are
palpated or seen on plain radiographs.
Specific problems occur depending on the location of
the VeM. In the facial area the lesion swells in dependent
areas, with the Valsalva maneuver, and when the patient
cries or during physical exertion. With time, this swelling
becomes conspicuous. There can be distortion of facial
structures, e.g. periocular VeMs cause progressive orbital
enlargement and proptosis. Enophthalmos can occur when
the patient stands up. A venous lesion can become painful
when the patient is exercising. Localized thrombosis is a
common occurrence.
Pharyngeal, laryngeal and palatal VeMs can cause obstructive sleep apnea syndrome, easily demonstrated by
polysonmographic investigation. Pelvic VeMs enlarge during pregnancy, causing pain and large vulvar varicose veins,
yet rarely impede vaginal delivery. In the limbs, pure VeMs
are less common than complex combined VMs with overgrowth (an older term is Klippel-Trenaunay syndrome).

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Limb VeMs are often extensive; the skin is blue mad
permeated with venous channels and pouches (Fig. 1). They
frequently involve the muscles, and sometimes the joints
(Fig. 2). The limb usually has normal axial growth, but
sometimes there is undergrowth. VeMs frequently bleed
into the muscles and joints. Hematomas and hemarthroses
are painful and cause functional impairment. Multiple
small, blue, dome-shaped cutaneous VeMs of the limbs
can indicate the presence of either familial glomangiomatosis (frequent and purely cutaneous) or "blue rubber bleb
nevus" (Bean) syndrome (rare, cutaneous and visceral). In
the latter a gastrointestinal work-up is advisable.
In extensive VeMs, particularly those located in the
limbs, a blood coagulation profile must be obtained because
these patients frequently have chronic low-grade disseminated intravascular coagulopathy with diminished fibrinogen and elevated D-dimers. VeMs can present anywhere in
the skin, and are frequently more extensive than clinically
appreciated on physical examination. Therefore, investigations are indicated whenever treatment is considered to
define the anatomic boundaries, particularly the depth [4].
Standard arteriography is useless for studies of VeMs
because only hyperselective arteriography demonstrates the
"bunch of grapes" venous staining in the late venous phase;
this does not give a complete representation of the entire
anomaly.
Doppler studies may be performed, although in pure
VeMs they are less useful than in the complex-combined
limb vascular anomalies (the old Klippel-Trenaunay and
Parkes Weber syndromes). Computed tomography (CT)
with contrast enhancement documents the extent of the
VeM. For some limb VeMs this is an excellent way to detect
which muscles are involved.
Magnetic resonance imaging (MRI) is, in our opinion,
the "gold standard" for evaluation of VeMs, particularly at
the cephalic level, but also for limb and truncal VeMs. MRI
gives excellent tissue resolution and provides a selection of
slices in three planes that is particularly useful for demonstrafing the extent of a lesion prior to treatment. VeMs have
a bright hypersignal on T2-weighted sequences, brighter
than that from fat (Fig. 3). There is no need for gadolinium
enhancement to evaluate the extent of an established VeM.
With gadolinium, Tl-weighted sequences alone are usually
obtained because T2-weighted sequences with gadolinium
are difficult to analyze. VeMs are best characterized using
T2-weighted images. Therefore, gadolinium injection is
only performed when there is a question of a deep VeM
versus a malignant tumor, a LM, or a combined lymphaficovenous malformation [5].
Treatment of VeMs is difficult and usually prolonged.
The approach varies depending on the level and extent of
the lesion. Percutaneous sclerotherapy is always possible,
but usually requires multiple therapeutic sessions. Ethibloc
(a mixture of zein, alcohol and additives) is often used in
Europe [6]; 100% ethanol is favored in the United States
[7]. The less destructive sclerosing agents, classically useful for limb varicose veins, may be chosen for small,
superficial VeMs. The aim of this treatment is to shrink
the venous channels, reduce the swelling and pain, mini-

mize the skin color, and diminish the contour deformity.

Percutaneous sclerotherapy under fluoroscopic control has
been used increasingly over the last 12 years for VeMs,
whereas arterial embolization is now performed only rarely.
In the cephalic region percutaneous sclerotherapy makes
surgical resection easier [8] (Fig. 4a and b). Dental malocclusion and an open bite may develop due to a VeM's
mass effect. Correction requires orthodontia and frequently
an orthognathic surgical procedure. Velar and pharyngeal
VeMs that cause sleep apnea are approached by direct
sclerotherapy under fluoroscopic control. A tracheostomy
is often necessary during the period of multiple procedures.
Limb VeMs are often too extensive to be treated completely
by sclerotherapy or surgical correction [9, 10]. Compression by an elastic stocking is always recommended. In some
specific localizations, for example, a thigh VeM in one
muscular group or a VeM in the knee joint synovia causing
bleeding, pain, progressive stiffness, and ankylosis, sclerotherapy and/or surgical excision may be considered for
functional reasons.

Lymphatic malformations
There are two anatomic forms of LM, which are often
intermingled. The microcysfic form manifests as small
vesicles on the skin surface (the old terms are lymphangioma, lymphangioma circumscriptum, and lymphangioendothelioma) [11]. The macrocystic type is composed of
subcutaneous cysts under normal skin (the old terms are
cystic lymphangioma or cystic hygroma). LM is usually
detected at birth, and can be visualized prenatally by
ultrasonography (US) if the cysts are large.
Macrocystic and microcystic LMs typically swell and
enlarge whenever there is a viral or bacterial infection.
Steroidal or non-steroidal anti-inflammatory drugs may be
used if there is a viral infection. Sometimes bacterial
cellulitis occurs, which requires a prolonged course of
antibiotics, normally beginning with IV administration.
Intralesional bleeding within the cyst from the thin wall
of the LM is another frequent occurrence.
The diagnosis of a LM is usually made by physical
examination. If uncertain, US, CT, or MRI is indicated.
Treatment differs according to the type of LM and its
location. Surgical excision is possible if the lesion is well
delineated. The surgical strategy is to focus on an anatomic
region and remove as much, if not all, of the LM in that
area as possible (Fig. 5 a and b). Repetitive excision is made
difficult by scarring and is more likely to result in damage
to nerves. Excision may also be performed after previous
cutaneous expansion to allow wide removal with a better
cosmetic result and diminished chance of recurrence within
the scar. In macrocystic LMs percutaneous sclerotherapy
with Ethibloc or 100% ethanol may be considered alone, or
as an adjunct to surgical removal.
Associated visceral (thorax, abdomen) or skeletal LMs
are very difficult to treat, and in rare cases these forms may
be lethal.

293

Fig. 5a Two-year-old boy with typical cystic cervical lymphatic

malformation; b following surgical excision

Arteriovenous malformations
These are the most dangerous and most difficult VAs to
treat. AVMs are hemodynamically active lesions with AV
shunting. Some are visible at birth; others manifest during
childhood or adolescence. An AVM in its initial quiescent
stage can mimic a port-wine stain or a hemangioma. Rapid
expansion may occur during puberty, pregnancy, trauma, or
after ill-advised surgical treatment, such as arterial ligation
or partial excision. AVMs may worsen at any time throughout life. AVMs in the head and neck region or the pelvic
area are life-endangering; large AVMs may, in time, cause
congestive heart failure.
Clinically, the diagnosis of an AVM is usually straightforward. There are signs of shunting and rapid blood flow.
The pink skin patch or mass is warm; there is a bruit;
dilated veins are seen around the nidus and the epicenter,
and there is a thrill on palpation. With time, with increased
shunting through the AV fistulae, cutaneous ischemia and
dystrophic skin changes develop, e.g., "pseudo-Kaposi
sarcoma" skin alterations; painful ulcers, episodic bleeding,
or massive hemorrhage (Fig. 6).
Complementary investigations confirm the diagnosis
and, moreover, document the precise vascular rheodynamics. Doppler US and color Doppler studies are neces-

Fig. 7 Arteriovenous malformation of scalp: MRI, T1 sequence;

flow voids indicate high-flow
vessels
Fig. 8a Six-year-old boy with an
arteriovenous malformation well
localized to left ala nasi; b 1 year
following resection and immediate reconstruction with microvascular flap from crus of fight
ear (Dr Julian J. Pfibaz, Boston)

Fig. 6a, b Severe arteriovenous malformation of hand in an adolescent female a before and b after elastic compression

sary to localize AV shunting and measure the local output.

MRI demonstrates the typical serpiginous, black "flow
voids" corresponding to the high-flow vessels (Fig. 7),
and magnetic resonance angiographic images portray the
expanding arteries on the abnormal side in comparison with
the normal side. Arteriography must also be performed in
order to clearly delineate the nidus with its early venous
drainage, and to evaluate the therapeutic possibilities.
Treatment of an AVM is always a challenge (8, 11-14);
intervention should never be undertaken by a novice. If an
AVM is in a quiescent stage, a "wait-and-see" attitude with
periodic evaluations is usually preferred. Cure is difficult to
achieve, either by superselective arterial embolization alone
or a combination of arterial embolization and complete
subsequent surgical excision with reconstruction (Fig. 8a
and b).

294

Fig. 10 Six-year-old girl with residual involuted hemangioma of

forehead; b appearance at age 13 years following excision of fibrofatty
residuum

In about one-half of the cases, a birthmark signals the

nascent hemangioma: a congenital red telangiectasia, an
Fig. 9 Good response of facial hemangioma to oral corticosteroid irregular pink stain, a congenital blue patch mimicking a
treatment, in contrast to insufficient shrinkage of laryngeal hemangioma. Due to persistent respiratory obsu'uction patient required a bruise, or a pale, white, "anemic" macule (the so-called
tracheostomy for months (upper left at 15 days, upper right 45 days, anemic nevus). These early signs predict what the surface
lower left 6 months, lower right 2 years)
and extent of the hemangioma will be, however, none
forecasts the eventual volume of the lesion. In rare instances a fully-grown, violaceous, and firm hemangioma is
present at birth. In these cases a biopsy may be indicated in
order to rule out another congenital tumor, e.g., infantile
Hemangiomas
rhabdomyosarcoma, fibrosarcoma, myofibromatosis, or
Hemangiomas appear in 10%-12% of neonates and in- neuroblastoma. The growth of these "intrauterine hemanfants, with a female preponderance, and proliferate over a giomas" is nearly completed during fetal life, and thus, the
variable number of months during the 1st year of life. They involuting phase begins soon after birth.
Treatment is not indicated for a majority of hemangiosubsequently exhibit spontaneous, slow involution over
years. Following involution normal skin is restored in mas, because most of them are small. ("Nature is the best
about 50% of cases, or there may be cosmetic sequelae, cure"). Some (10%-20%), however, grow to cause alarme.g., telangiectases, sagging, scarring, or fibrofatty residua. ing and even life-threatening complications. These include:
Rarely are the underlying structures affected (bone distor- destructive extension, large volume with anatomic distortion due to a mass effect, enlargement of the ear, lip, or tion, obstruction of a vital orifice with functional consequences (e.g., eyelid, orbital, nasal, lip, ear, or perineal
cheek, breast underdevelopment at puberty, etc.).
Most hemangiomas develop in the papillary and reticu- hemangiomas), invasion of a breast bud, necrosis and
lar dermis. These superficial forms appear as bright red, ulceration, visceral localization (laryngeal [16], hepatic
mammillated lesions (the old adjectives are "tuberous" or [17], abdominal cardiac, or cerebral), and thrombocytope"strawberry"); these are easy to diagnose by physical nia (the Kasabach-Merritt phenomenon [18]).
For these endangering or life-threatening lesions, pharexamination. Hemangiomas can also develop in the deep
dermis, hypodermis, and subcutaneous tissue. These lesions macological treatment is necessary to stop the growth phase
appear as a rather compact, warm mass under normal or and accelerate involution. Corticosteroids (oral-systemic or
bluish skin (the old adjective is "cavernous"). In these intralesional) and alfa-interferon (AI) (subcutaneously) are
instances the diagnosis may be unclear, and therefore, both in the front line of treatment for these patients [19, 20].
US, color Doppler, and MRI are determinant. CT is not For corticosteroids, the responses are approximately 30%
as useful as MRI, but nevertheless does document tissue good, 40% equivocal, and 30% none (Fig. 9) [19]. AI acts
involvement. MRI may be necessary to distinguish a sub- more slowly than steroids; the frequency of response is
cutaneous deep hemangioma from a dermoid cyst, a approximately 90%. Arterial embolization of hemangiomas
meningocele, an encephalocele, or a LM. CT, US, and is no longer indicated except in very rare, dangerous
MRI may be necessary to document an associated anomaly situations after failure of pharmacologic treatment, e.g.,
such as a tethered cord or Dandy-Walker malformation for hepatic hemangiomas causing high-output congestive
heart failure.
[15].

295
Pulsed-dye laser treatment for early proliferating hemangiomas is still under evaluation. Investigators believe it
shortens the evolution of a thin h e m a n g i o m a [21], but there
is no evidence that it can affect deep dermal extension.
Early surgical excision m a y be indicated in selected cases,
for. example, in the case of a localized eyelid h e m a n g i o m a
impairing the visual axis and unresponsive to drug therapy
or a "pendulum" lip hemangioma. CO2 laser excision of a
subglottic h e m a n g i o m a causing respiratory distress is considered in cases where there is no response to systemic
corticosteroids. Surgical repair of the skin sequelae is
indicated after involution (Fig. 10a and b).
The.immunohistochemical characteristics of hemangiomas have been defined according to the clinical phases in
the natural history of these lesions [22]. Hemangiomas in
their proliferating phase have a high expression of proliferating-cell nuclear antigen, vascular endothelial growth
factor, type IV collagenase, urokinase, and basic fibroblast
growth factor. These findings document active angiogenesis
and confirm the fact that hemangiomas are completely
different lesions from VMs.

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