Hand Surgery
1st Edition

93
Vascular Disorders: Arteriovenous Malformations
Joe Upton
Jennifer J. Marler
Stephen A. Pap
Vascular malformations (VMs) in the upper extremity represent very challenging problems in hand surgery. With adequate experience, these are treatable problems with predictable outcomes (1).
In 1982, Mulliken and Glowacki (1a) proposed a classification of vascular anomalies that described vascular tumors based on cellular biology and natural history (Tables 1 and 2). Compared with vascular tumors, malformations do not involute, and they are classified by the aberrant vessel type and by their flow speed. Change in size can be affected by mechanical factors and cellular changes with aging and hormonal modulation. They may be associated with skeletal overgrowth, and fast-flow lesions, in particular, can cause very challenging, occasionally life-threatening, clinical problems.
PATHOGENESIS
VMs arise from errors in embryogenesis (2). Current research efforts are beginning to provide insight into the pathogenesis of abnormal blood vessel formation, and genetic studies are starting to identify particular chromosome changes in syndromes that include arteriovenous malformations (AVMs), such as Osler-Rendu-Weber syndrome (3).
CUTIS MARMORATA TELANGIECTASIA CONGENITA
Cutis marmorata telangiectasia congenita is a rare vascular anomaly that presents with extensive cutaneous marbling exacerbated by exposure to lower temperatures or when the patient is crying. These skin lesions are depressed, may have ulcerations, and are most frequently found unilaterally in the trunk and extremities. They have a distinctive purple color.
Cutis marmorata telangiectasia congenita must be distinguished from cutis marmorata, in which normal vascularity causes skin mottling when exposed to low temperatures but disappears on rewarming. Almost all affected children with cutis marmorata telangiectasia congenita show some degree of improvement of the skin changes during the first year of life into adolescence (3,4). However, atrophy and pigmentation often persist into adulthood, in association with ectasia of the superficial veins in the involved limb (Fig. 1).
CAPILLARY MALFORMATIONS
Clinical Features
Capillary malformations are capillary- to venule-sized vessels in the superficial and deep dermis of skin and owe their color to erythrocytes. They have also been called “port-wine stain,” “angel kiss,” and “stork bite” (Fig. 2). These dilated vessels lack a normal smooth muscle layer within their walls and vasa nervorum (5). Extensive cutaneous capillary malformations can be associated with soft tissue and bone hypertrophy. In the upper extremity, capillary malformations are often associated with a deeper VM or lymphatic malformation (LM) (1). They must be distinguished from other benign, common birthmarks of infancy.
Treatment
The tunable pulsed-dye laser can decrease the color of the cutaneous blush, and more dramatic results are obtained on the face and neck than on the trunk and extremities (6). Soft tissue debulking and skeletal procedures required with overgrowth are particular to the other associated VMs, LMs, and AVMs.
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VENOUS MALFORMATIONS
Clinical Features
Most VMs are sporadic, although a genetic pattern of susceptibility for certain types of VMs has been suggested. VMs of the upper extremity are all present at birth but may not become clinically evident until school age. They grow commensurately with the child and slowly expand during the adolescent growth spurt.
TABLE 1. VASCULAR ANOMALIES OF THE UPPER LIMB
Vascular tumors
   Hemangiomas
      Congenital
         Rapidly involuting congenital hemangioma
         Noninvoluting congenital hemangioma
      Infantile
      Hemangiomatosis
   Pyogenic granuloma
   Kaposiform hemangioendothelioma
   Rare tumors
      Hemangiopericytoma
      Hemangioendothelioma
      Giant cell angioblastoma
      Angiosarcoma
Vascular malformations
   Cutis marmorata telangiectasia congenita
   Capillary malformations
   Venous malformations
   Lymphatic malformations
   Arteriovenous malformations
   Combined (eponymous) malformations
They most commonly present as a mass, swelling, or cutaneous discoloration. These slow-flow malformations engorge with the limb in a dependent position and decompress with the limb held above the level of the heart. Most VMs are located in the subcutaneous tissue planes external to the muscular fascia in the axilla, arm, and forearm (Fig. 3). Most are solitary lesions, and a small number of patients have extensive lesions that may extend into the axilla and ipsilateral chest wall (Fig. 3C).
FIGURE 1. Cutis marmorata telangiectasia congenita. The characteristic features of cutis marmorata telangiectasia congenita include a reticulated, marblelike appearance with a typical deep purple color. Involved limbs may have both soft tissue and skeletal atrophy.
TABLE 2. COMPARISON OF TYPICAL INFANTILE HEMANGIOMAS AND VASCULAR MALFORMATIONS
  Hemangioma Vascular malformation
Present at birth No in 70% of cases. Yes (may not be clinically evident).
30% of cases have premonitory spot.
Growth characteristics Rapid growth during first year of life followed by spontaneous involution. Growth commensurate with child.
Subject to extrinsic modulation by hormonal and other factors.
Female to male ratio 3:1 1:1
Pain and paresthesias are usually the result of local inflammation around intralesional thrombi or nerve compression (1). Areas with phlebothrombosis are swollen, firm, and very painful when compression garments are applied. Most symptoms are aggravated after exercise in which repetitive movements such as lifting, gripping, or pinching are involved.
Intramuscular VMs are found within the flexor and extensor muscles and compartments of the forearm as well as within the hand in the dorsal interossei, thenar, and hypothenar intrinsic muscles. In the absence of phleboliths, nerve compression, or intralesional bleeding, most VMs are asymptomatic. Subtle deficiencies in grip and pinch strength may be measured with extensive intramuscular involvement; however, these generally seem minimal. Despite significant involvement, function of the involved muscles remains surprisingly good.
VMs occasionally involve skeletal structures, showing cortical lucencies where vessels penetrate medullary canals, but no large areas of osteolysis. Pathologic fractures can occur in upper limbs with large diffuse lesions. VMs do not progress from a slow-flow to high-flow state. Enlargement after partial resections represents redirection of flow into adjacent anomalous channels. There is a hormonal modulation in females with medium- and large-sized VMs and lymphatic venous malformations (LVMs), which may
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increase in size during adolescence, menses, and pregnancies and with oral contraceptives.
Large VMs can be coagulopathic, and a coagulation profile should be obtained in all patients. Platelet counts are usually in the range of 100,000 to 150,000 per microliter. Prothrombin time may be increased, with normal activated partial thromboplastin, low fibrinogen levels (150 to 200 mg per dL), and increased fibrin split products.
FIGURE 2. Diverse presentations of capillary malformation (CM). CMs can involve any portion of the upper extremity and do not necessarily follow a segmental or dermatologic pattern. A: An extensive circumferential lesion of the arm, forearm, and hand. Note the less intense CM of the ipsilateral chest and abdomen. B: Diffuse enlargement of the hand is noted in the patient shown in A. C: CM involving the C3 to C5 distribution of the upper limb.
Evaluation
Magnetic resonance imaging scans provide the gold standard for the evaluation of VMs (Fig. 4). These lesions can involve all tissue layers. On T1-weighted sequences, VMs are isointense, whereas gradient-weighted images show diffuse, homogeneous enhancement. T2-weighted images show septation within the soft tissue mass and signal voids characteristic of phleboliths. Flow-sensitive gradient-weighted sequences show no evidence of high flow. Magnetic resonance venography is very helpful for evaluation of large VMs anywhere in the upper limb. Direct puncture phlebography obtains a more detailed evaluation of the intrinsic anatomy of a VM and visualizes the extrinsic drainage of the limb and is usually obtained before sclerotherapy.
Arterial anatomy is normal in limbs with VMs, LVMs, and capillary-lymphatic-venous malformations, although there may be some distortion due to a mass effect. Abnormalities on the venous side show puddling of contrast and delayed flow out of the VM. Angiograms are helpful in the preoperative evaluation of large VMs or of lesions in very difficult areas for dissection.
Treatment
Observation
The initial treatment for all VMs is conservative (Fig. 5). Most large and small lesions are asymptomatic. Compression garments are very helpful to control the enlargement of the VM during or after exercise. Low-dose aspirin therapy is helpful in reducing thrombus formation.
Sclerotherapy
The authors’ second line of treatment is provided by the interventional radiologist for all but the small, well-localized lesions in the upper limb that can be easily resected. Sclerotherapy is used for functional or aesthetic considerations and is most successful in lesions with large saccular channels. Absolute alcohol (100%) is the preferred sclerosant in the United States (7); Ethibloc (Ethicon, Hamburg, Germany) is used outside of the United States (8).
The passage of sclerosant into the general circulation can be potentially very dangerous if a proximal tourniquet is
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not used. The authors’ radiologists prefer to treat specific areas in multiple bimonthly intervals (7) and have the best outcomes with large VMs in the arm and proximal forearm (Fig. 6).
Complications extend from ecchymosis, blistering, and, occasionally, full-thickness loss of overlying skin to damage of adjacent soft tissue structures (Fig. 7). Extensive hemolysis may lead to renal toxicity. Excessive intravenous sclerosant may cause cardiac compromise (7). The inflammatory reaction and scar formation after sclerotherapy are significant and cross tissue planes. The surgeon must be available when the interventional radiologist plans to sclerose extensive VMs.
FIGURE 3. Diverse presentations of venous malformation (VM). A: An isolated VM along the palmar surface of a digit is symptomatic if intralesional thrombi compress digital nerves. B: This dorsal lesion is soft and compressible and symptomatic. C: Extensive VMs may involve the entire extremity and chest wall. This patient is septic from an infected phlebothrombosis in the anterior axillary region. D: This diffuse VM involves every soft tissue structure of the hand and distal forearm. Surgery is indicated only for symptomatic regions.
Surgery
The indications for surgical treatment are primarily functional but can be aesthetic (1,9). Judicious resections of VMs are both safe and predictable. Small, well-localized lesions anywhere in the subcutaneous tissue planes, on the dorsum of the hand, or along the sides of a digit or thumb are easily removed.
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FIGURE 4. Imaging of a venous malformation (VM) in an adult patient with a forearm lesion. A–C: Transverse magnetic resonance images of the forearm that are differently weighted highlight characteristic findings of a VM. On a T1-weighted sequence (A), the VM is isointense to adjacent skeletal muscle. On a T1-weighted sequence with gadolinium enhancement (B), there is diffuse enhancement of the VM. On a T2-weighted sequence (C), there is a high signal with signal voids within the VM that represents phleboliths. D: Intravenous injection of contrast at the time of sclerotherapy reveals abnormal collection of saccular venous structures. E: Phleboliths are seen in soft tissues on a lateral plain radiograph. F: T2-weighted sagittal magnetic resonance imaging sequence.
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FIGURE 5. Treatment algorithm for slow-flow vascular malformations. ASA, aspirin; AVM, arteriovenous malformation; LM, lymphatic malformation; MRI, magnetic resonance imaging; Rx, treatment; VM, venous malformation.
FIGURE 6. Sclerotherapy of an upper extremity venous malformation. A: Venous malformation involving the superficial flexor and extensor compartments of the forearm. B: T1-weighted magnetic resonance imaging sequence demonstrates the extent of involvement. Physical examination alone may be deceiving. C: Injection of contrast material at the time of sclerotherapy demonstrates the abnormal venous vessels. D: Arterial phase angiogram after sclerotherapy demonstrates a normal arterial circulation. E: Venous phase angiogram after sclerotherapy shows lack of contrast at the site of the sclerosed venous malformation (white arrow).
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FIGURE 7. Sclerotherapy complication. An acute compartment syndrome developed within hours after this venous malformation was injected. The lesion ran along the interosseous membrane, involving all four superficial flexor muscle bellies and the terminal flexor to the thumb. Clots and thrombi are seen during the fasciotomy. Involved portions of muscles were excised. The only residuum 4 years later was a weak thumb flexor.
Any resection involving the neurovascular structures in the antecubital fossa, pronator tunnel, and deep palmar spaces of the hand requires careful planning. Single or staged debulking on the dorsum of the hand may extend through the intermetacarpal spaces into the deep palmar spaces, a difficult area in which to control bleeding. Loupe magnification is used at all times, and the authors do not hesitate to use the operating microscope if needed (Table 3).
The authors avoid intramuscular dissections unless that particular area is very symptomatic due to phlebothrombosis. Within the arm or forearm, it is often better to completely resect the affected muscle(s) and to restore its function with tendon transfers or replacement. It is impossible to completely excise large, diffuse lesions with or without muscular involvement. Symptomatic, enlarged digits can be debulked in two stages with incisions placed in the midlateral line. Microscopic preservation of digital arteries, including individual vincular branches and nerves, is important (Fig. 8). In dorsal digital debulking, it is unwise to proceed beyond Cleland’s ligaments on the opposite side of the digit. Forearm debulkings are completed in the same two-staged fashion (Fig. 9). Fortunately, extensive VMs rarely extend through the brachial plexus, a structure that precludes dissection with the aid of a tourniquet. These resections should be avoided in asymptomatic patients with normal distal radial, ulnar, and median nerve function.
TABLE 3. OPERATIVE PRINCIPLES FOR RESECTION OF UPPER EXTREMITY VASCULAR MALFORMATIONS
Maintain absolute hemostasis under tourniquet control.
Carefully plan dissection within a well-defined region.
Preserve nerves, arteries, and joint cavities. Avoid intraneural dissection.
Avoid reoperation in a previously scarred region by performing a thorough initial dissection.
Avoid combined dorsal and palmar dissections.
Use separate procedures for debulking of digit, hand, forearm, and arm. Debulk axilla and chest wall together.
Perform joint synovectomies and tendon dissections within the digital sheath sparingly.
Large VMs extending along the entire arm into the axilla and ipsilateral chest wall are challenging, especially when the patient may be septic from localized phlebothrombosis (Fig. 3C). Coagulopathies are often present. Surgical aids include catheters in the subclavian artery and vein, cell saver, hypotensive anesthesia, pneumatic tourniquet for the most distal portion of the VM, and experienced assistants who can compress the lesion while the primary surgeon dissects it off the muscular fascia. One unit of fresh frozen plasma must be replaced with every three units of blood. The authors try to limit total blood replacement to one blood volume in these children.
The complication rate after partial or complete removal of slow-flow VMs is less than 10%. Patients with complications usually have more than one problem directly proportional to the size and specific location of the VM (1). Because postoperative hematomas are common, the authors have used delayed primary closures at 24 to 72 hours postresection after removal of large VMs. Hematomas can be avoided in the upper limb with elevation and good compression dressings and drains. The most common long-term problems have been neuromas-in-continuity, loss of function and contracture after intramuscular resections, and soft tissue losses (1).
LYMPHATIC MALFORMATIONS
Clinical Features
Lymphatic anomalies are usually present at birth, with smaller lesions in less conspicuous regions becoming evident by 4 years of age. In contrast to VMs, these lesions have a rubbery consistency and do not decompress easily. These two characteristics clearly define LMs from VMs. Males and females are affected equally. LMs are most commonly found in the cervicofacial region, where large lesions are often detected by prenatal ultrasound. Although thoracic duct anomalies can occur, they are rarely seen with isolated upper extremity and chest wall LMs.
Clinically, LMs have the appearance of a sponge with large, small, or combined spaces, also referred to as channels. In the upper limb, solitary or diffuse lesions in the arm, axilla, and chest wall have both macroscopic and microscopic channels (Fig. 10). Distal to the elbow, almost all LMs are predominantly microscopic, a characteristic that makes them less amenable to sclerotherapy. Diffuse lesions involving the dorsum of the hand, wrist, and forearm usually contain microcystic spaces with large amounts
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of adjacent adipose tissue. Histologically, the walls of lymphatic spaces contain both smooth and skeletal muscle cells and are of variable thickness. The lumens and cystic spaces are filled with protein-rich fluid. In all upper extremity locations, LMs are accompanied by large amounts of fat within the subcutaneous tissue plane.
FIGURE 8. Surgical resection of a venous malformation involving the palm and long and ring digits. A: Preoperative appearance. The extent of involvement is always much greater than is estimated on physical examination. B: The first of multiple staged procedures consisted of debulking one-half of each of the long and ring fingers. Microscopic dissection is invaluable for preservation of neurovascular structures. C: The radial digital nerve and artery are seen after microscopic dissection. D: All neurovascular structures (except the venae comitantes) are preserved during a full palmar dissection.
LMs in the upper limb can also present a dermal capillary malformation component. The skin is thick and may have deep cutaneous puckering as well as a bluish discoloration. LMs in the superficial layers present as single or coalesced vesicles that often weep and provide a portal of entry for bacterial flora. Dark blue or red nodules represent vesicles filled with blood. Skin involvement is usually patchy in the presence of extensive deep LMs. One variant of LM has a venous component termed LVM.
Lymphatic anomalies in the upper limb are most commonly isolated to a specific region in a digit, the hand, forearm, or arm. Axillary LMs typically extend onto the ipsilateral chest wall and into the supraclavicular space and neck. Fortunately, most LMs are confined to the subcutaneous tissue planes and skin and do not penetrate the intermuscular fascia into muscle but can spread along
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these fascial planes. Most symptoms in larger lesions are related to the size, weight, and noncompressibility of the lesion or the weeping, maceration, and ulcers of infected regions. Nerve compression and phlebothrombosis are uncommon.
FIGURE 9. Persistent venous malformation after surgical resection. A: A 9-year-old boy presented after an unsuccessful excision of a symptomatic venous malformation at another institution, during which the surgeons found themselves “operating in an inkwell.” At the time of reoperation at our institution, the skin flaps have been reflected and scarred muscular fascia exposed. B: Excision included the interosseous membrane and all involved soft tissue, as well as several distal muscle bellies. C: Before closure, gelatin sponge has been placed within the dead space, along with drainage catheters. D: An intradermal subcutaneous closure should always be performed on the exposed dorsal surface of the forearm.
LMs in the upper and lower extremity can be associated with both skeletal and soft tissue overgrowth that can progress to gigantism. In most of these limbs, there is an accompanying adipose overgrowth, and there is no invasion of the LM into the bone or muscle.
Lymphangiomatosis refers to unique patients who have evidence of disseminated LM. This constellation typically includes diffuse thoracic duct anomalies with recurrent pleural effusions, together with pathognomonic osteolytic bony lesions. These bony lesions were originally described as “Gorham-Stout syndrome,” “disappearing bone disease,” or “phantom bone disease” (10).
Evaluation
Magnetic resonance imaging T1-weighted images are hypointense, and secondary to the high water content, T2-weighted sequences are hyperintense (Fig. 11). Large macrocysts may have high fluid levels due to protein or blood. Contrast administration may reveal absent or slight rim enhancement, and gradient-weighted sequences show no evidence of high-flow voids (11).
Treatment
Observation
Small lesions and involved areas of skin are easily observed and treated with local wound care. The two major problems with LMs are infection and intralesional bleeding. Bleeding within a pure LM is not necessarily indicative of a coagulopathy, but a hematologic workup is advised. Bleeding causes the LM to enlarge and to become bluish in color and sometimes painful. Cold compression, elevation, rest, and empiric antibiotic therapy provide effective treatment.
Infection is a more serious problem. Bacteria from a systemic infection may seed channels within an LM. A rapidly progressing cellulitis in children is usually secondary to an upper respiratory infection. Beta-streptococcal organisms are the major pathogens and respond to the prompt administration of penicillin or a broad-spectrum antibiotic. These wildfire infections usually resolve as rapidly as they progress.
Simple aspiration of large cysts provides only temporary relief. Sustained, intermittent compression of large lesions in the upper extremity adequately decompresses one region,
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displacing fluid into adjacent portions of the LM. Without continuous wear of an elastic garment, the fluid eventually reaccumulates.
FIGURE 10. Diverse presentations of lymphatic malformations. A: Hard, rubbery semimobile mass on the dorsum of the ring finger in an 18-month-old male. B: Gross involvement of the upper limb, ipsilateral chest, mediastinum, and neck in a 2-year-old girl. C: Lymphatic malformation involving the right hand and wrist of a neonate who was erroneously diagnosed as having an amniotic band syndrome on a prenatal ultrasound, resulting in unnecessary fetal surgery at another institution. The tissue is rubbery and minimally compressible. D: The forearm and dorsum of the hand and digits are common presentations for more extensive lymphatic malformations.
Sclerotherapy
The second line of treatment is sclerotherapy by direct injection into the cystic cavities (Fig. 11). Macrocystic LMs respond much more favorably than microcystic lesions, and for this reason, sclerosants are rarely used around the wrist, hand, or digits. Pure ethanol, sodium tetradecyl sulfate, and doxycycline are the most frequently used sclerosants (11). OK-432, derived from group A Streptococcus pyogenes, has been used for LMs.
Surgery
Surgical resection is the most predictable way to control LMs. Operative indications for both LMs and LVMs include pain, intralesional thrombi (venous component present), episodic bleeding, recurrent infection, chronic ulceration and maceration, or functional problems. Local resections in the arm, axilla, and chest wall are often necessary to control excessive drainage (Fig. 5).
Expertise and knowledge of neural and vascular anatomy are essential for dissections of the brachial plexus, antecubital fossa, and palmar spaces of the hand (including the carpal and ulnar tunnels) and along the digits and thumb. The authors have noted most difficulty with extensive lesions within the antecubital fossa and the pronator tunnel, where the multiple motor branches of the ulnar and median nerves must be preserved. Within the palm of the hand, both superficial and deep palmar arches must be preserved with the common digital vessels and all motor branches to intrinsic muscles along the deep motor branch of the ulnar nerve.
The digits and thumb should be approached through midaxial incisions, avoiding zigzag incisions in the glabrous skin,
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as they may hypertrophy. One neurovascular bundle should be left untouched during each of two staged debulkings of a massively enlarged digit (Fig. 12). Cleland’s ligaments represent important landmarks during dissection. Dorsal debulking should not extend beyond this ligament to the opposite side of the digit. The adventitia around digital arteries and the epineurium of digital nerves can help to indicate the location of neurovascular structures. All closures must be tension-free. Early use of self-adherent wrapping and continuous passive motion machines decreases postoperative swelling and the residual scar that often develops postoperatively.
FIGURE 11. Radiologic characteristics of lymphatic malformation. A: Multiple macrocysts within a large cervical lymphatic malformation are seen in this T2-weighted magnetic resonance image sagittal view. B: In a more anterior T1-weighted coronal plane, the extension of this lesion through the axilla along the chest wall can be appreciated. The areas of high signal intensity represent abnormal fat. C: The large macrocysts are the most amenable to sclerotherapy. D: The largest cyst is demonstrated on fluoroscopy just before injection of the sclerosant.
The dorsal surfaces of the hand and wrist should be debulked in stages with incisions along the borders of the hand or through a single incision parallel to the third metacarpal (Figs. 12 and 13). When this skin contains deep dermal LM and epidermal vesicles, consider total excision and replacement with either a full-thickness skin graft or a thin fasciocutaneous flap. The tissue over the thumb and thenar muscles and that over the hypothenar muscles are easy to debulk. In contrast, a thorough dissection of LM within the palm is one of the most difficult procedures in all of hand surgery. Postoperative swelling is very difficult to control.
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The forearm is ideally approached through a straight medial incision, extending from wrist to elbow. Each stage can extend no more than 200 degrees around the circumference of the forearm. The elbow and arm are best approached medially, and extensive LMs or LVMs are removed in two or more stages. The use of continual compression garments and compression pumps preoperatively and postoperatively makes a tremendous difference in achieving a satisfactory result. Although fluid collection can be partially controlled with compression, most resections proximal to the elbow drain for weeks postoperatively.
FIGURE 12. A: Digital resection of lymphatic malformation. The digital and palmar dissections of this lymphatic malformation are performed separately. One side of the digit is debulked at a time. B: The radial neurovascular bundle, including vincular branches of the artery, has been preserved. An excess amount of fat is admixed with the microcystic lymphatic malformation. The ulnar neurovascular bundle is untouched. C: Excess skin is excised through dorsal skin creases. A 2-mm skin bridge is preserved on the distal fingertip for suturing of the palmar flap. Flaps are raised through a high midaxial incision. Estimated regions of skin excision include a large portion of the pulp tissue. There is significant scar tissue from a previous excision. D: Postoperative appearance of dorsal surface. E: Postoperative appearance of palmar surface. F: Dorsal surface closure.
After performing separate resections of the chest wall and axilla for many years, the authors now perform this in a single stage during which all neurovascular structures can
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be clearly identified (Fig. 14). A thorough preoperative preparation of the entire surgical and anesthesia team is essential for these long, meticulous operations.
FIGURE 13. Volar hand resection of lymphatic malformation. A: This girl is seen at age 6 years after debulking of the index and long digits. Resection of the dorsum of the hand and thumb is planned in two additional procedures. B: Postoperative result, 24 years later. C: Result 30 years after resection. D,E: Regions over the radial side of the index finger and the palmar pulp of the thumb continue to be swollen and hyperhidrotic due to intradermal lymphatic malformation.
The principle of “performing as thorough a resection as possible” is more important in the resection of an LM than with any other vascular anomaly. Hypertrophic scars are common, and swelling may be difficult to control. The bleeding and fibrosis encountered on reentry of these previously dissected regions are unique and profound. Dissect these areas in such a way that reentry is not necessary.
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Compression pumps augment circumferential wrapping of the wrist, forearm, and axillary regions. With extensive LMs or LVMs, these modalities displace fluid into the mediastinal LM. Thick skin with dermal involvement (either with or without vesicles) contains lymphatic channels and invariably fissures, ulcerates, or becomes infected; it invariably requires surgical replacement. Hypertrophic scar formation can be expected wherever there is LM within the dermis on either side of the wound closure.
FIGURE 14. Natural history and resection of extensive lymphatic malformation. A: At birth, this baby had a rubbery mass with peau d’orange and a bluish hue within the arm and axilla. The diagnosis of lymphatic malformation can be made on physical examination alone. B: Over the next 3 months, the mass enlarged and was not compressible. C: By 20 months of life, the size and weight of the lesion had become problematic. D: The lesion along the chest wall, the axilla including the brachial plexus and arm, was dissected and resected during one procedure. E: The chest and arm with residual malformation have been well controlled with compression wrappings at age 5 years. F: Despite three additional debulkings of the forearm and arm, it has been difficult to control swelling in this region. Bleeding and maceration from direct dermal involvement within the axilla have necessitated antibiotic treatment for an average of 3 months per year.
The outcomes of aggressive surgery are quite satisfactory, with a complication rate of 22% (1,12). Scar revisions, resection of neuromas, and replacement of drains for persistent drainage in the proximal portions of the limb and chest wall were the most common complications (12). Amputation is often elected for massively enlarged digits, hands, or portions of the arm or after unsuccessful limb salvage attempts. During the past 3 years, the authors have effectively used continuous passive motion machines to maintain motion in released joints at all levels from fingertip to glenohumeral joint.
ARTERIOVENOUS MALFORMATIONS
AVMs are believed to result from errors of vascular development between the fourth and sixth weeks of embryonic gestation. One hypothesis holds that they result from failure of arteriovenous channels in the primitive retiform plexus to regress (13).
Tissue from the epicenter of an AVM, termed the nidus, demonstrates close juxtaposition of medium-sized arteries, veins, and vessels. The veins become “arterialized” and exhibit intimal thickening, increased smooth muscle within the media, and dilatation of the vasa vasorum (14). There is also progressive dilatation of the proximal arteries, with fibrosis, thinning of the media, and diminished elastic tissue (14).
Several mechanisms have been proposed to account for the tendency of AVMs to expand to involve previously virgin adjacent tissue. Reid believed that the thin-walled arteries and veins could rupture into one another secondary to increased pressure and flow, forming new fistulous connections (14). Other authors have proposed that local ischemia plays a role, as seen in the “steal phenomenon,” producing both pain and ulceration. It is well known that an AVM can enlarge rapidly after proximal ligation (15,16 and 17).
Fast-flow malformations are usually present at birth but visible only as a red blush that may be mistaken for a port-wine stain. During childhood, a thrill or bruit and a mass that does not respond to elevation develop. The adolescent growth spurt stimulates growth and expansion by an unknown mechanism; thrills, bruits, and warmth beneath the cutaneous stain become clinically obvious. The pain does not always respond to elevation, especially after exercise. In females, the lesion size increases during the adolescent growth spurt and with menses, oral contraceptives, and pregnancy; it does not regress to its previous size after delivery. Symptoms of distal ischemia and discoloration of digits progressing to ulceration may develop with increased shunting through proximal arteriovenous fistulas (AVFs). Children with large lesions with extensive AVFs may go into congestive heart failure. These are the most symptomatic of all vascular anomalies. Severe pain usually precipitates surgery.
Clinical Classification
Type A
Type A malformations are fast-flow anomalies and include single or multiple AVFs, aneurysms, or ectasias on the arterial side of the circulation (Fig. 15) (1). They primarily involve either the radial or ulnar system with or without shunting. Symptoms occur only with exercise.
Type B
Type B malformations consist of more extensive AVMs localized primarily to one axial arterial system in the forearm, hand, or digit (Fig. 16). These fast-flow AVMs have stable flow characteristics and provoke minimal or no distal symptoms. A steal phenomenon can develop after exercise early in life.
Type C
Type C malformations are more diffuse, involving at least two of the three axial systems, with microfistulous and macrofistulous AVFs involving all tissue of the extremity. They are usually evident at a very early age and expand into previously uninvolved areas of the hand. Increased warmth, pain, hyperhidrosis, and a progressive distal steal phenomenon are present.
Radiologic Evaluation
The clinical diagnosis and presence of fast flow are confirmed by ultrasonography and color Doppler studies. Ultrasound of large lesions shows high-flow voids with a low arterial resistance. Arteriovenous shunts are well demonstrated. Type A and B lesions can be easily followed with yearly ultrasound examinations.
Magnetic resonance imaging scans are obtained to gain a baseline with large lesions or lesions involving the palmar spaces of the hand (Fig. 16). Scans are not obtained of AVMs isolated to a single digit. Soft tissue thickening and flow voids are easily detected by T1- and gradient-weighted sequences.
Angiograms are the best way to demonstrate the specific abnormal anatomy of the malformation. Superselective angiography is not used until interventional or surgical treatment is planned. Sequential images demonstrate the size and location of the feeding arteries, the AVM nidus, and early opacification of draining veins (Figs. 15, 16, and 17B).
FIGURE 15. Types of fast-flow arteriovenous malformations. A,B: Type A consists of single or multiple arteriovenous fistulas, aneurysms on the arterial side of the circulation. C,D: Type B lesions are more extensive but localized primarily to one or two of the three axial systems on the arterial side (radial, interosseous, or ulnar). The discoloration of the long fingertip is secondary to the steal phenomenon. E,F: Type C malformations are very extensive, involve all three systems, and are very symptomatic. The many microarteriovenous fistulas involve all tissues of the wrist and hand.
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Treatment
Observation
Early in life, observation and compression garments are the mainstays of treatment (Fig. 18). The authors have followed a 67-year-old man conservatively with compression wraps for a type C macrofistulous AVM with multiple AVFs (Figs. 15B, 15E, and 17). Most patients with type B and C lesions develop pain as a result of distention of the lesion and progression of a distal steal phenomenon.
FIGURE 16. Type B fast-flow malformation. A: An 8-year-old girl presented with a persistent mass with thrills and bruits over the distal third of the right forearm. B: T1-weighted magnetic resonance imaging sequences show flow voids and a mass involving all soft tissue structures dorsal to the interosseous membrane of the forearm. C: Early views during angiography demonstrate the many microshunts and arteriovenous fistulas along the interosseous system. D: The nidus of the arteriovenous malformation remains along the interosseous membrane, with diffuse extension into the adjacent soft tissue mass. E: After preoperative embolization the mass is well visualized. F: Resection included the interosseous membrane and involved periosteum of both the radius and ulna. Normal digital and thumb extension was restored postoperatively.
Sclerotherapy
Sclerotherapy can be used to obliterate large tortuous arteries if ligated feeding arteries prevent passage of an embolization catheter. Some well-localized AVMs have been successfully
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treated with a combination of embolization followed by sclerotherapy (11,18), most of these in the head and neck and lower extremity. The risks and morbidity after this combined approach are high (19). The authors have not used this combination in the treatment of upper limb AVMs.
FIGURE 17. Arteriovenous malformation type C, fast-flow. A: This 67-year-old executive noted a gradual swelling and pulsation in his hand since his teenage years. Earlier in life, surgical removal of symptomatic regions was aborted due to bleeding that could be controlled only with elevation and pressure. B: Early angiographic sequences show macrofistulous shunts involving the radial and ulnar arteries and both palmar arches. With aging, these vascular channels have dilated and become quite tortuous. C: He experiences a persistent steal phenomenon in the long and index fingers, and the mass within the palm partially obstructs a functional grasp unless he wears his compression glove. Extrinsic flexion and extension have remained normal. The distorted nail matrix of the index finger has been the source of a chronic paronychia.
Embolization
The decision to use embolization with or without surgery is made jointly by the surgeon and the interventional radiologist. For minimal to moderately symptomatic type A or B AVMs, embolization is the less traumatic procedure (Fig. 19). Indications include rapid growth of the AVM with increased flow of AVFs, pain, distal discoloration
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and ulceration, cardiac overload/congestive heart failure, and failure to thrive. The most common symptoms are well localized to specific areas of microfistulous or macrofistulous shunting; these are best controlled with superselective embolization using various types of particles, coils, gelatin sponge packs, and the like. For type C lesions, palliative embolization is often used before surgery (Figs. 20 and 21).
FIGURE 18. Treatment algorithm for fast-flow malformations.
FIGURE 19. Arteriovenous malformation type B, fast-flow. A: The angiogram of a 6-month-old child with a swollen, red, tense fingertip. Localized thrills were consistent with a microfistulous arteriovenous malformation involving only the pulp tissue. B: Superselective embolization was performed through a catheter that was passed into the ulnar digital artery of this small child. C: Follow-up angiography demonstrates complete obliteration of the mass.
FIGURE 20. Embolization and surgery of arteriovenous malformation type B. A: This professional wrestler presented with a painful mass within the thenar muscles. A thrill was first noted during adolescence. There was no history of trauma. B: The nidus of the arteriovenous malformation was demonstrated at the level of superficial palmar arch, supplied by radial, interosseous, and ulnar vessels. Distal digital and thumb arterial architecture was shown to be normal. C: The postembolization study showed obliteration of most of the arteriovenous malformation with large draining veins. D: Two days later, the mass was explored surgically. Yellow vessel loops mark the recurrent motor branch and sensory branches of the median nerve. E: All nerves and flexor tendons were preserved during surgical resection. F: Five years later, he continued to demonstrate good function. Palmar abduction is present through the abductor pollicis, but key pinch is weak due to the resection of the adductor pollicis muscle.
FIGURE 21. Embolization, surgery, and repeat embolization of arteriovenous malformation type B. A: A pulsatile mass within the hypothenar eminence of this young woman became larger and painful when she started antiovulant medication. B: Early angiographic sequences showed a macrofistulous arteriovenous malformation in Guyon’s canal fed by both ulnar and interosseous vessels. C: A postembolization sequence showed persistence of many shunts. Note the lack of perfusion of the pulp tissue of both ring and long digits, which were most symptomatic. The caliber of the ulnar artery was twice normal. D: Surgical excision included removal of ulnar artery and common digital vessel to the fourth web space. Sensory and motor nerves and flexor tendons were preserved and revascularization to the ulnar side of the ring and both sides of the fifth digit performed with autogenous vein grafts. E: Normal flexion and extension without claw posturing were noted 2 years postoperatively. F: Five years later, she presented with a painful mass at the base of the ring finger. This represented some residual arteriovenous malformation at the margin of the previous resection within the intermetacarpal space and was easily embolized without the need for more surgery.
TABLE 4. CLINICAL STAGING SYSTEM FOR ARTERIOVENOUS MALFORMATIONS
Stage Description
I Quiescence Pink-bluish stain, increased warmth, arteriovenous shunting detectable on 20-MHz Doppler
II Expansion Stage I plus enlargement, pulsations, thrill, and bruits, tortuous/tense veins
III Destruction Stage II plus dystrophic skin changes, ulceration, bleeding, persistent pain, and soft tissue necrosis
IV Decompensation Stage III plus cardiac failure
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Surgery
In all but the least complicated resections, angiography and superselective embolization precede surgical resection by 24 to 72 hours. Under pneumatic tourniquet control, the embolized regions are easy to find and provide excellent landmarks for the surgeon. With large lesions, embolization alone can be palliative for difficult problems such as congestive heart failure, continued bleeding, and localized pain. Surgery is mandated for uncontrolled intralesional bleeding, compartment syndromes, nerve compressions, chronic ulceration, and gangrene. Table 4 describes staging guidelines based on clinical findings.
FIGURE 22. Microfistulous, progressive arteriovenous malformation type C. At age 1 year, this child presented with a capillary malformation of the hand and pulsatile mass of the distal forearm. The diagnosis of Parkes Weber syndrome was made, and she was treated with compression garments. An angiogram at age 6 years showed a progressive microfistulous, painful arteriovenous malformation of the distal forearm. By the time she was 12 years old, she was in continual pain. A: Massively enlarged subclavian and axillary arteries were demonstrated, and at the same time, she showed early signs of cardiac compromise. B: She learned to control her pain by dislocating her glenohumeral joint and compressing her axillary artery, a position in which she often slept. C: Intraarterial balloon catheters were helpful at the time of shoulder disarticulation for removal of her parasitic and extremely painful limb. D: Preservation of the scapula helps drape clothing and makes the appearance of these patients less conspicuous. Within 6 months, she gained 20 pounds, became less morose, and excelled in school and cross-country running.
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Wound dehiscence, bleeding, and infection are common early sequelae, and neuroma-related pain, sympathetic dystrophies, and contracture often follow the unsuccessful resection. Partial resections of type B and C AVMs are doomed to fail. The need for microvascular revascularization of the hand or individual digits must be addressed. Most of the preoperative pain in these patients is steal phenomenon–related.
FIGURE 23. A: A 25-year-old secretary with a known type C arteriovenous malformation presented after embolization of a massive lesion involving the entire forearm and hand. B: An angiogram showed macrofistulous shunting involving all three arterial systems of the hand. The digital vessels to the ulnar three digits were not visualized at any stage of the study. C: The shunts and fistulas with the forearm appeared to be massive. D: Appearance during amputation. E: With a well-healed, nonpainful below-elbow amputation stump, she functioned very well with and without a myoelectric prosthesis. She regretted that she did not have this procedure performed much earlier in life.
The most difficult aspect of these resections lies in defining the limits of the malformation that characteristically cross tissue planes. The authors’ approach has been to preoperatively angiograph and embolize the symptomatic portion of the AVM(s) and to anatomically define the resection margins before an incision has been made. Even in the ideal bloodless field afforded by the tourniquet, the surgeon may not have a clear delineation of the malformation margins (Fig. 21) (1).
Long-term outcomes of type B and C patients after upper extremity resections or amputations are not available. The authors’ preliminary experience with approximately 45 patients is that most showed expansion of residual malformations somewhere near the periphery of the resection within 10 years. The majority followed beyond this time became symptomatic in those areas within 10 years. The spread of the malformation into previously uninvolved portions of the extremity has been much greater for microfistulous AVFs and macrofistulous lesions (Fig. 22).
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It is difficult for the surgeon to know when not to operate. Some categorically refuse to consider any surgical approach after witnessing colleagues trying to “operate in an inkwell” after uncontrolled hemorrhage from macrofistulas. For upper extremity lesions, tourniquets, embolization, careful planning, good surgical technique, aggressive resections, and reconstructions together provide opportunities that are not readily available in other anatomic regions such as the head and neck, trunk, pelvis, and peritoneum. Symptomatic type A and B lesions are the most amenable to surgery.
FIGURE 24. Type C, microfistulous and macrofistulous, congestive heart failure, and below-elbow amputation. A: Both this teenager with a type C arteriovenous malformation and his parents wanted to save this hand. The index ray had been resected for uncontrollable pulsatile bleeding. The thumb then became ulcerated and congested, and the patient became suicidal because of the unrelenting pain. B: Angiography showed massively tortuous and enlarged axial vessels feeding microfistulous shunts within the forearm and hand. C: A later sequence demonstrated the extent of the shunting and lack of distal digital perfusion. D: Chest radiograph and electrocardiogram were consistent with congestive heart failure. A below-elbow amputation was followed by a predictable recovery and normal adolescent growth spurt.
The recommendation to amputate is both difficult for the surgeon and exasperating for the patient and his or her parents who, in desperation, often seek multiple additional opinions. If the patient is requesting amputation, he or she is usually right, and the request should not be denied by the surgeon. Pain, impending gangrene, symptoms secondary to severe steal, early cardiac compromise, and a failure of young children and adolescents to maintain normal growth parameters are all indications for selective amputation (Figs. 22, 23, and 24). The authors’ outcome study of type C patients showed an amputation rate of more than 90% over a 30-year period of time. In retrospect, with nine of 17 patients eventually requiring amputation at the forearm, arm, or shoulder level, the authors prolonged the inevitable amputation for a
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number of reasons. The recovery after ablation of the parasitic part and elimination of the chronic pain are both remarkable and predictable. Rapid weight gain, improved disposition, and increased level of activity are all notable.
REFERENCES
1. Upton J, Coombs CJ, Mulliken JB, et al. Vascular malformations of the upper limb: a review of 270 patients. J Hand Surg [Am] 1999;24:1019–1035.
1a. Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 1982;69:412–422.
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3. Guttmacher AE, Marchuk DA, White RI. Hereditary hemorrhagic telangiectasia. N Engl J Med 1955;333:918–924.
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8. Dubois JM, Sebag GH, De Prost Y, et al. Soft-tissue venous malformations in children: percutaneous sclerotherapy with Ethibloc. Radiology 1991;180:195–198.
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10. Gorham L, Stout A. Massive osteolysis (acute spontaneous absorption of bone, phantom bone, disappearing bone): its relation to hemangiomatosis. J Bone Joint Surg 1955;37:986–1004.
11. Burrows PE, Laor T, Paltiel H, et al. Diagnostic imaging in the evaluation of vascular birthmarks. Dermatol Clin 1998;16:455–488.
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13. Halsted W. Congenital arteriovenous and lymphatico-venous fistulae: unique clinical and experimental observations. Trans Am Surg Assoc 1919;37:262.
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15. Braverman I, Keh A, Jacobson B. Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia. J Invest Dermatol 1990;95:422.
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Appendix
Combined (Eponymous) Malformations
SLOW-FLOW COMBINED MALFORMATIONS
Capillary-Lymphatic-Venous Malformation (Klippel-Trénaunay Syndrome)
A capillary-lymphatic-venous malformation (Fig. 25) is associated with skeletal and soft tissue overgrowth (1–5).
In 80%, only the lower limb is involved, mostly unilateral. Upper extremity lesions can extend into the mediastinum and retropleural space but rarely evoke symptoms. Lymphatic hypoplasia is present in more than half of the patients, and generalized lymphedema is common. Upper extremity capillary-lymphatic-venous malformation presents with skeletal overgrowth of the arm, forearm, or hand (Fig. 25). However, undergrowth can occur. Pulmonary embolism may occur in up to 25% of patients.
Proteus Syndrome
Proteus syndrome is a sporadic, progressive vascular, skeletal, and soft tissue condition that truly lies at the interface of vascular anomalies and overgrowth syndromes. The authors do not consider this syndrome as a vascular anomaly.
The 1998 National Institutes of Health workshop diagnostic criteria include three mandatory general criteria: (a) a mosaic or asymmetric distributions of lesions, (b) a progressive course, and (c) sporadic occurrence (6). In addition, some number of “category signs” must be present. These include verrucous (linear) nevus, lipomas and lipomatosis, macrocephaly (calvarial hyperostoses), asymmetric limbs with partial gigantism of the hands and/or feet, and curious cerebriform plantar thickening (“moccasin” feet). As a rule, Proteus syndrome is not present at birth. These features suggest that this syndrome may be the result of a dominant lethal gene that survives by somatic mosaicism (6).
Maffucci’s Syndrome
Maffucci’s syndrome (Fig. 26) denotes the coexistence of exophytic venous malformations with bony exostoses and enchondromas (7). The osseous lesions appear first, most often in the hands, feet, long bones of the extremity, ribs, pelvis, and cranium (8). There may be a history of recurrent fractures secondary to enchondromatous weakening of bony diaphyses. The VMs involve the subcutaneous tissues and bones and are generally distributed in the extremities (Fig. 26). These patients often develop spindle cell hemangioendotheliomas within the VMs. These are a reactive vascular proliferation rather than a true tumor (9). Malignant transformation, usually chondrosarcoma, occurs in 20% to 30% of patients (10,11). A majority of the chondrosarcomas are of histologically low grade and can often be cured with surgical resection (12,13).
FAST-FLOW EPONYMOUS SYNDROMES
Parkes Weber Syndrome
Parkes Weber syndrome is much less prevalent than capillary-lymphatic-venous malformation. The capillary malformation is usually more diffuse and pink. The major difference is the presence of the AVM with AVFs, which all present early in childhood. These lesions become progressively worse and carry a poor long-term prognosis. With time, the involved regions of the arm and forearm form large macrofistulous shunts. Surgical treatment is helpful only for well-localized symptomatic shunts, compartment syndromes, or compression syndromes. Because many of these upper extremity lesions are so diffuse, surgical resection is unrealistic.
FIGURE 25. Capillary-lymphatic-venous malformation progression. A–D: The progression of a combined capillary-lymphatic-venous malformation is seen at ages 6 months, 3 years, 12 years, and 28 years. Manifestations of upper limb involvement included skeletal and soft tissue overgrowth, macrodactyly, development of extensive lymphatic vesicles, and worsening of joint contractures after multiple operations at another local institution. At age 22, she delivered a normal infant, and 6 years later, she died of suspected pulmonary embolus.
FIGURE 26. Maffucci’s syndrome. A: The unilateral hand of a girl with Maffucci’s syndrome shows the characteristic sessile, pedunculated venous malformations. B: Radiographs demonstrate multiple phalangeal and metacarpal lucencies secondary to enchondromas. Her right distal ulnar has been previously resected.
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REFERENCES
1. Upton J, Coombs CJ, Mulliken JB, et al. Vascular malformations of the upper limb: a review of 270 patients. J Hand Surg [Am] 1999;24:1019–1035.
2. Baskerville PA, Ackroyd JS, Lea Thomas M, et al. The Klippel-Trenaunay syndrome: clinical, radiological and haemodynamic features and management. Br J Surg 1985:72:232–236.
3. Gloviczki P, Stanson AW, Stickler GB, et al. Klippel-Trenaunay syndrome: the risks and benefits of vascular interventions. Surgery 1991;110:469–479.
4. Jacob AG, Driscoll DJ, Shaughnessy WJ, et al. Klippel-Trenaunay syndrome: spectrum and management. Mayo Clin Proc 1998;73:28–36.
5. Samuel M, Spitz L. Klippel-Trenaunay syndrome: clinical features, complications and management in children. Br J Surg 1995;82:757–761.
6. Biesecker LG, Happle R, Mulliken JB, et al. Proteus syndrome: diagnostic criteria, differential diagnosis, and patient evaluation. Am J Med Genet 1999;84:389–395.
7. Maffucci A. Di un caso di encondroma ed angioma multiplo contribuzione al a genesi embrionale dei tumor. Movimento Med Chir (Naples) 1881;3:399.
8. Lewis R, Ketcham A. Maffucci’s syndrome: functional and neoplastic significance. J Bone Joint Surg Am 1979;55:1469.
9. Perkins P, Weiss SW. Spindle cell hemangioendothelioma. An analysis of 78 cases with reassessment of its pathogenesis and biologic behavior. Am J Surg Pathol 1996;20:1196–1204.
10. Kaplan RP, Wang JT, Amron DM, et al. Maffucci’s syndrome: two case reports with a literature review. J Am Acad Dermatol 1993;29:894–899.
11. Sun TC, Swee RG, Shives TC, et al. Chondrosarcoma in Maffucci’s syndrome. J Bone Joint Surg Am 1985;67:1214–1219.
12. Coley B, Higinbotham N. Secondary chondrosarcoma. Ann Surg 1954;139:1954.
13. Cook P, Evans P. Chondrosarcoma of the skull in Maffucci’s syndrome. Br J Radiol 1977;50:833.