Magnetic Resonance Imaging of Facial Vascular Anomalies
JOHN HUSTON III, M.D., GLENN S. FORBES, M.D., DANIEL A. RUEFENACHT, M.D.,* CLIFFORD R. JACK, M.D., Department ofDiagnostic Radiology; J. T. LIE, M.D.,t Section ofMedical Pathology; RICKY P. CLAY, M.D., Division of Plastic Surgery
In 36 patients, facial vascular anomalies were studied with 46 magnetic resonance (MR) examinations, 9 angiograms, and 5 computed tomographic scans. All lesions were categorized into classic pathologic groups on the basis of radiologic and pathologic studies, clinical examination, and behavior. Overall,2 juvenile hemangiomas, 3 capillary malformations (port-wine stains), 18 venous malformations, 9 lymphatic malformations, and 4 arteriovenous malformations were found. MR imaging was superior to computed tomography and angiography for demonstrating the precise anatomic extent of the facial vascular. anomalies and their relationship to the adjacent soft tissues but was inferior to computed tomography for demonstrating radiopaque structures such as trophic bone changes and phleboliths, MR imaging was also inferior to angiography in determining the nidus and the exact nature of collateral vascular structures in arteriovenous malformations. MR studies confirmed the clinically suspected diagnosis of facial vascular anomalies and demonstrated typical characteristics for each type of lesion. MR imaging is an ideal initial technique to triage patients with facial vascular anomalies for appropriate management, including observation, endovascular therapy, or surgical excision.
The purpose of this study was to examine the utility of magnetic resonance (MR) imaging for the evaluation and classification of facial vascular anomalies. The classification of facial vascular lesions is controversial, and the pathologic terminology is complex. I We prefer to use a classification system (Table 1) that combines cellular features with clinical behavior. 2-6 This classification is based on the endothelial characteristics of vascular anomalies.' The term "hemangioma" is limited to lesions that show increased endothelial mitotic activity and have a biphasic growth pattern that consists of early enlargement and later regression. Vascular anomalies that have normal endothelial mitotic activity and fail to regress are termed "malformations." Thus, this classification system includes juvenile hemangio*Current address: University of Minnesota, Minneapolis, Minnesota. tCurrent address: University of California, Davis, Medical Center, Sacramento, California. Address reprint requests to Dr. John Huston III, Department of Diagnostic Radiology, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 67:739-747,1992
mas, capillary malformations (port-wine stains), venous malformations, lymphatic malformations, arteriovenous malformations, and a combination of the malformations. On the basis of this classification system, a clinical diagnosis can be confirmed, and therapeutic planning can be formulated after radiographic evaluation.v'? HEMANGIOMAS Juvenile hemangiomas have a tumorlike appearance and a biphasic growth behavior-rapid expansion during infancy (from to 6 to 10 months of age) and delayed, usually spontaneous involution during the preschool age.9,10 Rarely, such lesions are present at birth. Tense and tender on palpation, juvenile hemangiomas in the proliferative phase may show pulsations and warmth, depending on the size, amount of arteriovenous shunting, and anatomic site.":" Cutaneous juvenile hemangiomas have a strawberry appearance with red, well-delineated discoloration of the skin, whereas subcutaneous juvenile hemangiomas manifest as tumors with bluish discoloration of the overlying skin. If the hemangiomas are deep, they may have no color. Juvenile hemangio739
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Table I.-Classification of Vascular Anomalies Based on Endothelial Characteristics* Hemangiomas-juvenile Malformations Capillary (port-wine stain) Venous Lymphatic Arteriovenous Mixed *See text for further discussion.
mas are more focal and tumorlike than other vascular anomalies; their boundaries are usually confined to an anatomic compartment. These lesions can manifest in conjunction with hematologic disorders, a profound thrombocytopenia (Kasabach-Merritt syndrome)" being the most severe. VASCULAR MALFORMATIONS Capillary malformations (port-wine stains) are present at birth but do not show spontaneous involution.v" They are flat, sharply demarcated, pink to deep red, cutaneous lesions. Occasionally, port-wine stains of the head may be associated with a deeper vascular lesion (such as the Sturge-Weber syndrome or arteriovenous malformation) or may accompany other developmental defects of the neural axis (meningoencephalocele). Venous malformations are present at birth and usually grow proportionally with the child. They do not undergo spontaneous involution, but the common occurrence of phlebothrombosis leads to temporary swelling and tenderness and later to the formation of phleboliths. Rapid enlargement may be noted after injury or partial surgical resection. Anatomically, a wide variety of sizes, extensions, and delineations is observed. Usually, venous malformations are not well delineated, do not respect boundaries of anatomic compartments, and have little continuity with the adjacent normal venous system. 9,lO,I5 Extension within bone is possible. They are not pulsatile but are soft and compressible, and they characteristically expand with a Valsalva maneuver. Localized intravascular coagulopathy may manifest as a major hematologic disorder. Lymphatic malformations are present at birth and expand by accumulation of fluid. Sudden expansion is usually due to hemorrhage within cysts. Lymphatic malformations manifest as a multitude of small cutaneous or mucosal bullae (for example, lymphatic malformation of the tongue) or as large cystic lesions beneath the skin. 4 ,9,l O,16 The most common site of the cystic variant is the neck, where transillumination of the lesion may be performed. Arteriovenous malformations are rarely noted at birth. Usually, a quiescent lesion expands rapidly after local
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trauma, a surgical procedure, or hormonal changes (for example, during puberty or pregnancyj.v'? Because of the presence of arteriovenous shunts, flow is rapid, and the adjacent vascular structures enlarge. Pulsatility and warmth are present, and eventually a bruit and pain may be perceived.'? Venous hypertension and arterial steal in the adjacent normal tissues may leadto trophic changes, and necrosis and hemorrhage may ensue. Disseminated intravascular coagulation as a result of thrombotic consumption may be present as a hematologic complication. Direct arteriovenous fistulas may develop after trauma alone, typically in an area where veins closely parallel arteries (for example, the superficial temporal artery)." The combination of several vascular lesions or the presence of a vascular tumor should be considered when the clinical manifestations do not correspond to one of the aforementioned pattems.v'" In this report, we describe our experience with facial vascular anomalies in 36 patients. The MR findings and the correlated computed tomographic, angiographic, clinical, surgical, and histologic characteristics are presented. PATIENTS AND METHODS In 36 patients (24 female and 12 male patients) who ranged in age from 2 months to 79 years (median age, 14 years), 46 MR examinations were performed. Previous surgical procedures had been performed in 27 patients, 1 of whom had undergone 10 prior operations. Of the 36 patients, 33 underwent imaging between October 1985 and 1988, during which time a multidisciplinary treatment program was available. These studies were done before gadolinium was available. Three additional patients underwent MR imaging between 1988 and May 1990. Of the 46 MR examinations, 41 were performed with use of a 1.5-T superconducting magnet (Signa, General Electric, Milwaukee, Wisconsin) and 5 with use of a 0.15- T resistive magnet (Picker, Highland Heights, Ohio). At the discretion of the examining radiologist, sequences were obtained in the axial, coronal, and sagittal planes, typically with a Tlweighted sagittal and a T2-weighted axial imaging sequence. Spin echo imaging included a repetition time of 400 to 600 ms, an echo time of 20 to 30 ms, and 2 to 4 excitations and also a repetition time of 1,500 to 2,200 ms, an echo time of 30 to 40 and 80 ms, and 1 excitation. In three cases, gradient echo imaging was performed with use of 30° flip angle, a repetition time of 50 to 200 ms, and an echo time of 15 to 50 ms. Examinations were performed with use of a 30-cm standard head coil or, in selected cases, a 7.6- or 12.7-cm (3- or 5-inch) surface coil placed over the area of clinical interest. Five patients were examined with intravenous contrastenhanced computed tomographic scans in an axial plane (model 9800, General Electric). Selective angiographic
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Table 2.-Magnetic Resonance Characteristics of Facial Vascular Anomalies in 36 Patients* Total
Juvenile hemangioma Capillary malformation Venous malformationt Lymphatic malformation Arteriovenous malformationt
Mixed Low
T2
Proton density
T1
Type of anomaly
Iso
High
Mixed Low Iso
High
Mixed Low
Iso High
Flow void None Small Large
0
2
0
0
2
0
0
0
0
2
0
0
0
2
3
0
0
3
0
0
0
0
3
0
0
0
3
2
16
0
0
0
16
0
0
16
5
11
2
18
0
9
4
2
3
0
5
0
0
4
2
0
0
7
8
1
0
4
4:j:
0
0
0
3:j:
0
0
0
3:j:
0
0
0
0
0
4
*"Iso" == magnetic resonance signal isointense with adjacent muscle. tOne patient underwent Tl imaging only. :j:Predominant magnetic resonance appearance was of flow voids.
studies were performed in nine patients. Diagnostic venographic studies, performed with use of a femoral vein approach or a direct puncture (or both), were conducted in seven patients. 10 The lesions were classified into one of six types (Table 1), as outlined in the introductory material.v" RESULTS The MR characteristics of the facial vascular anomalies are summarized in Table 2. Most lesions demonstrated a Tl signal that was isointense with adjacent muscle and an increased signal in comparison with muscle on the proton density and T2-weighted scans in their solid nonflowing portions. The hemodynamic nature of the lesions was characterized by the presence or absence of flow voids on MR imaging. Small flow voids were defined as loss of signal consistent with a vascular structure less than or equal to twice the expected diameter of normal vessels in the anatomic region of the lesion. Large flow voids were defined as signal loss greater than twice the diameter of normal vessels in the region of the lesion that could be traced to feeding arteries or draining veins on contiguous MR images.
The anatomic extent of the facial vascular anomalies as detected on MR images is presented in Table 3. The deepest extension of each lesion was characterized as subcutaneous, superficial, deep, or parapharyngeal. Subcutaneous lesions involved the skin and subcutaneous fat. Superficial lesions included the superficial parotid gland and facial muscles. Deep lesions extended to the deep parotid gland, masticatory space, and carotid space. Parapharyngeal lesions involved the tongue, parapharyngeal space, and prevertebral space. Juvenile hemangiomas were present in two patients (2 months and 1 year of age) and demonstrated typical biphasic growth patterns. In the 2-month-old patient, a small cutaneous lesion of the upper lip completely resolved spontaneously, a finding consistent with the clinical diagnosis of a juvenile hemangioma. On MR examination, this lesion had isointense T1 signal (Fig. 1 A) and increased proton density and T2 signal. In the l-year-old child, a large posterior superficial lesion also demonstrated isointense Tl signal and increased proton density and T2 signal (Fig. 1 B and C). Most likely because of its large size (7 em in maximal diameter), this lesion contained small flow voids and slightly crossed the midline. This hemangioma had enlarged during the child's first 9 months of life and then stabilized in size.
Table 3.-Anatomic Findings in 36 Patients With Facial Vascular Anomalies Type of anomaly
Total
Subcutaneous
Juvenile hemangioma Capillary malformation Venous malformation Lymphatic malformation Arteriovenous malformation
2 3 18 9 4
1 2 3 1 0
Deepest extension SuperParatidal Deep pharyngeal
1 1 2 2 1
0 0 5 2 3
0 0 8 4
0
Airway obstruction Yes No
0 0 3 2 0
2 3 15 7 4
Crossed midline Yes No 1 0 8 4
1
1 3 10 5 3
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When the patient was between 9 months and 1 year of age, the lesion decreased slightly in size and elective resection was performed. Port-wine capillary malformations were present in three patients, who had typical port-wine stains. One such lesion, which occurred in association with the Sturge-Weber syndrome, extended into the superficial facial muscles and demonstrated small flow voids. The other two lesions were confined to the skin. All three capillary malformations had isointense TI signal and increased proton density and T2 signal. The lesion was pathologically confirmed in one patient, who underwent a partial resection. Venous malformations were found on histologic examination in 18 patients, 16 of whom had lesions that were characterized as isointense T1 signal and increased proton density and T2 signal. In 11 lesions, small flow voids were detected within the substance of the lesion. Three venous malformations demonstrated substantial venous pooling; in two additional lesions, angiograms showed a mass effect and only a minimal vascular blush (Fig. 2). Computed tomography clearly demonstrated calcified phleboliths in two of the three patients with venous malformations in whom this study was performed (Fig. 3). On the MR scan, the phleboliths were seen as focal areas of decreased signal that simulated flow voids, but they could not be traced on contiguous images. In all three patients, the extent of the vascular lesion was more easily determined with MR imaging than with computed tomography. Venous malformations resulted in airway obstruction (Fig. 4) in three patients, two of whom required tracheostomies. One patient had orbital extension of the lesion, and another patient had sinus involvement. Four patients had multiple lesions. The patient with the most numerous discrete bilateral lesions had overgrowth of the right arm from a combined capillary-venous-lymphatic malformation (Klippel-Trenaunay syndrome). Lymphatic malformations demonstrated the most varied MR appearance (Fig. 5). Four of the nine lesions had mixed TI signal, with areas of increased Tl signal consistent with hemorrhagic degradation products. Two patients had predominantly low Tl signal, and three patients with mixed TI signal also had areas of decreased TI signal. These five patients with decreased T1 signal had MR findings consistent with 'cystic spaces. One lymphatic malformation had orbital extension. Two patients who underwent gradient
Fig. 1. Magnetic resonance images of juvenile hemangiomas. A, Hemangioma of upper lip of 2-month-old patient; lesion subsequently resolved spontaneously. B, Tl-weighted axial image of7em hemangioma with small flow voids in l-year-old child. C, T2weighted axial image of same lesion as shown in B.
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echo imaging had no evidence of flow. Computed tomography, performed in one patient, clearly demonstrated the lesion, but the complex nature of the lesion and its full extent were more readily delineated on the MR scan. In all nine patients, the lesions were characterized histopathologically. Arteriovenous malformations were present in four patients and demonstrated large flow voids on MR imaging. Three of these patients underwent arteriography, which disclosed high-flow vessels that corresponded to the MR flow voids (Fig. 6). These lesions consisted primarily of flow voids with little solid tissue; therefore, they were predominantly characterized as mixed signal on Tl, proton density, and T2 images. One patient underwent Tl-weighted imaging only. Gradient echo imaging, performed in one patient, demonstrated evidence of flow. In one patient, contrastenhanced computed tomography was superior to MR imaging in disclosing the bony changes from the mandibular involvement and the destruction by the arteriovenous malformation but equivalent to MR imaging in demonstrating the extent of the lesion. DISCUSSION On the basis of a thorough clinical evaluation of a lesion, including the growth characteristics, physical appearance, compressibility, and presence or absence of pulsations, and the patient's history, a presumptive diagnosis of facial vascular anomalies is frequently possible. Those patients who do not have a history or physical findings that are characteristic of a particular type of lesion often can be categorized as having a more general diagnosis, such as congenital lesions or neoplasms. Both of these groups-the vascular anomalies and the unknown lesions-are best further evaluated with MR studies. If the physical examination and MR imaging show the typical features of a particular vascular anomaly and treatment is nonsurgical, a biopsy is unnecessary to confirm the diagnosis.' In those patients with even the slightest possibility of the presence of a tumor after the MR examination, however, a biopsy is indicated for further evaluation. In this study, the MR signal characteristics of most lesions were of isointense Tl signal and increased T2 signal.
Fig. 2. Right facial venous malformation. A, Tl-weighted coronal magnetic resonance image, depicting isointense lesion without evidence of flow void (curved arrows). B, Right external carotid arteriogram, showing a minimal vascular blush (arrow) and substantial displacement of normal-sized arteries due to the mass effect. C, Right jugular venogram, demonstrating no retrograde filling of venous malformation and normal size of tributaries of external jugular vein.
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Fig. 3. Venous malformation involving right pterygoid muscles. A, Contrast-enhanced computed tomogram, showing enhancing lesion with several phleboliths (arrow). B, T2-weighted magnetic resonance image, demonstrating signal loss (arrow) that corresponds to the phleboliths, which should not be confused with flow voids.
Fig. 4. Diffuse venous malformation, predominantly involving base of tongue and right parapharyngeal space. Coronal Tl-weighted (A) and axial T2-weighted (B) magnetic resonance images, demonstrating severe tracheal narrowing and displacement to the left (arrows) that resulted in airway compromise. Flow voids were not evident within the lesion.
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Fig. 5. Lobulated cystic lymphatic malformation involving right side of face and upper aspect of neck and extending into parapharyngeal space. Proton density (A) and T2-weighted (B) magnetic resonance images, showing mixed signal intensities and a hemorrhagic fluid-fluid level (arrow).
Therefore, the T 1 and T2 signal characteristics were not helpful in distinguishing most of the vascular lesions except the lymphatic malformations. The lymphatic malformations demonstrated a mixed signal intensity, which was related to the proteinaceous fluids within the cystic cavities and the hemorrhagic degradation products. An important physiologic feature that MR imaging can delineate is the flow characteristics of the facial vascular anomalies. The presence or absence of flow voids6.19.2o and their relationship to the lesion are characteristic of the various vascular lesions. The numerous large flow voids of arteriovenous malformations have a distinctive MR appearance. Although MR imaging can clearly identify arteriovenous malformations, it cannot distinguish between the feeding arteries and the draining veins or precisely locate the nidus. In this situation, angiography is necessary for determining the area of the arteriovenous shunt for subsequent treatment. Most imaging procedures in this study were performed before the availability of gradient echo imaging, gadolinium contrast, and MR angiography. These recent advances in MR imaging have the potential to enhance imaging results." Because of its superior delineation of soft tissues, MR imaging clearly depicted the topographic relationship of the venous malformations to adjacent structures better than did computed tomography or angiography. MR studies can distinguish between a well-defined and an apparent infiltrative margin. The apparent infiltrative nature of these lesions is due to irregular extension of vascular channels into adjacent tissues. The multiplanar capability of MR examination,
including oblique scanning angles, facilitates the precise delineation of lesions and their relationship to adjacent normal structures. In our study, MR imaging was superior to computed tomography in depicting the extent of three venous malformations and one lymphatic malformation. In addition, MR imaging more clearly demonstrated the complex internal nature of the lymphatic malformation than did computed tomography. The size and location of an arteriovenous malformation were demonstrated equally well by MR studies and computed tomography. On computed tomography, the large vascular channels showed intense enhancement with intravenously administered contrast medium. MR examination more clearly identified the internal vascular nature of the lesion than did computed tomography. Other than arteriovenous malformations, entire vascular lesions were not opacified by angiography. MR imaging was superior to angiography in depicting the extent of the lesions. Computed tomography remains a valuable technique for evaluating vascular malformations; however, for maximal benefit, an iodinated contrast agent must be administered. Computed tomography demonstrated radiopaque structures, including bony changes and phleboliths, more clearly than I did MR studies. Lack of signal within a venous malformation, similar to a flow void but not present on contiguous adjacent slices, was typical of phleboliths on MR imaging. The mandibular bony erosion of one arteriovenous malformation was much more clearly demonstrated with computed tomography than with MR imaging. MR studies can identify vascular anomalies that necessitate angiography before invasive treatment is planned.
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Fig. 6. A, Right external carotid arteriogram, demonstrating arteriovenous malformation of right inferior orbital rim with high flow attributable to a large shunt. Arterial supply is an enlarged right facial artery (arrow). Venous drainage is predominantly through superficial facial veins and right superior ophthalmic vein (curved arrow). B, Tl-weighted axial magnetic resonance image obtained with use of a 12.7-cm (5-inch) surface coil, showing multiple large flow voids (arrow), which on contiguous images could be traced to feeding arteries and draining veins demonstrated on the angiogram.
With arteriovenous malformations, arteriography must be performed to delineate the nidus or identify the presence of an arteriovenous fistula before surgical treatment. If embolization is planned, preliminary diagnostic studies, including selective injection of the internal and external carotid arteries bilaterally, will facilitate rating for risk and success. Venography by direct puncture can confirm the diagnosis of a venous malformation but will fail to demonstrate the full extent of the lesion.'? This result is similar to our experience with venous-phase studies during selective arteriography. CONCLUSION MR imaging is a powerful technique for characterizing facial vascular anomalies. Noninvasively, it can determine the extent and the type of facial vascular anomalies better than computed tomography or angiography. Before treatment of arteriovenous malformations, angiography must be performed to delineate the hemodynamic characteristics and to map the associated arteries and veins. When a facial lesion does not conform to the classic appearance of a vascular anomaly and a neoplasm cannot be excluded, pathologic examination of a biopsy specimen is necessary. ACKNOWLEDGMENT We thank Cynthia P. Rausch for expert preparation of the submitted manuscript.
REFERENCES 1. Enzinger FM,.Weiss SW: Soft Tissue Tumors. St. Louis, CV Mosby Company, 1983, pp 379-421 2. Malan E, Puglionisi A: Congenital angiodysplasias of the extremities. Note I: Generalities and classification; venous dysplasias. J Cardiovasc Surg 5:87-130,1964 3. Malan E, Puglionisi A: Congenital angiodysplasias of the extremities. Note II: Arterial, arterial and venous, and haemolymphatic dysplasias. J Cardiovasc Surg 6:255-345, 1965 4. Grabb WC, Dingman RO, Oneal RM, Dempsey PD: Facial hamartomas in children: neurofibroma, lymphangioma, and hemangioma. Plast Reconstr Surg 66:509-527,1980 5. Mulliken JB: Classification of vascular birthmarks. In Vascular Birthmarks: Hemangiomas and Malformations. Edited by JB Mulliken, AE Young. Philadelphia, WB Saunders Company, 1988, pp 24-37 6. Meyer JS, Hoffer FA, Bames PD, Mulliken JB: Biological classification of soft-tissue vascular anomalies: MR correlation. AJR Am J Roentgenol 157:559-564, 1991 7. Mulliken JB, Glowacki J: Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 69:412-420, 1982 8. Merland 11, Tricot JF, Hadjean E, Riche MC, Engelras 0: Les malformations vasculaires cervico-cephaliques: protocole actuel de traitement; a propos de 230 cas. Phlebologie 33:95-103,1980 9. Merland 11, Natali J, Drouet L, Engelras 0, Hadjean E, Lemarchand-Venencie F, Riche MC, Tricot JF: Les angiomes et malformations vasculaires. Medicorama (Paris) 255:5-56, 1982
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10.
Mulliken 18: Vascular malformations of the head and neck. In Vascular Birthmarks: Hemangiomas and Malformations. Edited by 18 Mulliken, AE Young. Philadelphia, WB Saunders Company, 1988, pp 301-342 11. Azzolini A, Rossi L, Ghinelli C: The angiographic features of immature angiomas in infancy. Minerva Chir 28:14201445, 1973 12. Burrows PE, Mulliken 18, Fellows KE, Strand RD: Childhood hemangiomas and vascular malformations: angiographic differentiation. AJR Am J Roentgeno1 141:483-488, 1983 13. Kasabach HH, Merritt KK: Capillary hemangioma with extensive purpura: report of a case. Am J Dis Child 59:10631070, 1940 14. Mulliken 18: Capillary (port-wine) and other telangiectatic stains. In Vascular Birthmarks: Hemangiomas and Malformations. Edited by JB Mulliken, AE Young. Philadelphia, WB Saunders Company, 1988, pp 170-195
15.
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Boxt LM, Levin DC, Fellows KE: Direct puncture angiography in congenital venous malformations. AJR Am J Roentgeno1 140:135-136,1983 16. Ninh TN, Ninh TX: Cystic hygroma in children: a report of 126 cases. J Pediatr Surg 9:191-195,1974 17. Coleman CC Jr, Hoopes JE: Congenital arteriovenous anomalies of the head and neck. Plast Reconstr Surg 47:354364, 1971 18. Gelbert F, Riche M-C, Reizine D, Merland J-J, Cormier J-M: Direct arteriovenous fistula of the external carotid artery: treatment with detachable balloon. Ann Vase Surg 2:358361, 1988 19. Bradley WG Jr, Waluch V: Blood flow: magnetic resonance imaging. Radiology 154:443-450,1985 20. Mills CM, Brant-Zawadzki M, Crooks LE, Kaufman L, Sheldon P, Norman D, Bank W, Newton TH: Nuclear magnetic resonance: principles of blood flow imaging. AJR Am J Roentgenol 142:165-170,1984
JOHN HUSTON III, M.D., GLENN S. FORBES, M.D., DANIEL A. RUEFENACHT, M.D.,* CLIFFORD R. JACK, M.D., Department ofDiagnostic Radiology; J. T. LIE, M.D.,t Section ofMedical Pathology; RICKY P. CLAY, M.D., Division of Plastic Surgery
In 36 patients, facial vascular anomalies were studied with 46 magnetic resonance (MR) examinations, 9 angiograms, and 5 computed tomographic scans. All lesions were categorized into classic pathologic groups on the basis of radiologic and pathologic studies, clinical examination, and behavior. Overall,2 juvenile hemangiomas, 3 capillary malformations (port-wine stains), 18 venous malformations, 9 lymphatic malformations, and 4 arteriovenous malformations were found. MR imaging was superior to computed tomography and angiography for demonstrating the precise anatomic extent of the facial vascular. anomalies and their relationship to the adjacent soft tissues but was inferior to computed tomography for demonstrating radiopaque structures such as trophic bone changes and phleboliths, MR imaging was also inferior to angiography in determining the nidus and the exact nature of collateral vascular structures in arteriovenous malformations. MR studies confirmed the clinically suspected diagnosis of facial vascular anomalies and demonstrated typical characteristics for each type of lesion. MR imaging is an ideal initial technique to triage patients with facial vascular anomalies for appropriate management, including observation, endovascular therapy, or surgical excision.
The purpose of this study was to examine the utility of magnetic resonance (MR) imaging for the evaluation and classification of facial vascular anomalies. The classification of facial vascular lesions is controversial, and the pathologic terminology is complex. I We prefer to use a classification system (Table 1) that combines cellular features with clinical behavior. 2-6 This classification is based on the endothelial characteristics of vascular anomalies.' The term "hemangioma" is limited to lesions that show increased endothelial mitotic activity and have a biphasic growth pattern that consists of early enlargement and later regression. Vascular anomalies that have normal endothelial mitotic activity and fail to regress are termed "malformations." Thus, this classification system includes juvenile hemangio*Current address: University of Minnesota, Minneapolis, Minnesota. tCurrent address: University of California, Davis, Medical Center, Sacramento, California. Address reprint requests to Dr. John Huston III, Department of Diagnostic Radiology, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 67:739-747,1992
mas, capillary malformations (port-wine stains), venous malformations, lymphatic malformations, arteriovenous malformations, and a combination of the malformations. On the basis of this classification system, a clinical diagnosis can be confirmed, and therapeutic planning can be formulated after radiographic evaluation.v'? HEMANGIOMAS Juvenile hemangiomas have a tumorlike appearance and a biphasic growth behavior-rapid expansion during infancy (from to 6 to 10 months of age) and delayed, usually spontaneous involution during the preschool age.9,10 Rarely, such lesions are present at birth. Tense and tender on palpation, juvenile hemangiomas in the proliferative phase may show pulsations and warmth, depending on the size, amount of arteriovenous shunting, and anatomic site.":" Cutaneous juvenile hemangiomas have a strawberry appearance with red, well-delineated discoloration of the skin, whereas subcutaneous juvenile hemangiomas manifest as tumors with bluish discoloration of the overlying skin. If the hemangiomas are deep, they may have no color. Juvenile hemangio739
740
FACIAL VASCULAR ANOMALIES
Table I.-Classification of Vascular Anomalies Based on Endothelial Characteristics* Hemangiomas-juvenile Malformations Capillary (port-wine stain) Venous Lymphatic Arteriovenous Mixed *See text for further discussion.
mas are more focal and tumorlike than other vascular anomalies; their boundaries are usually confined to an anatomic compartment. These lesions can manifest in conjunction with hematologic disorders, a profound thrombocytopenia (Kasabach-Merritt syndrome)" being the most severe. VASCULAR MALFORMATIONS Capillary malformations (port-wine stains) are present at birth but do not show spontaneous involution.v" They are flat, sharply demarcated, pink to deep red, cutaneous lesions. Occasionally, port-wine stains of the head may be associated with a deeper vascular lesion (such as the Sturge-Weber syndrome or arteriovenous malformation) or may accompany other developmental defects of the neural axis (meningoencephalocele). Venous malformations are present at birth and usually grow proportionally with the child. They do not undergo spontaneous involution, but the common occurrence of phlebothrombosis leads to temporary swelling and tenderness and later to the formation of phleboliths. Rapid enlargement may be noted after injury or partial surgical resection. Anatomically, a wide variety of sizes, extensions, and delineations is observed. Usually, venous malformations are not well delineated, do not respect boundaries of anatomic compartments, and have little continuity with the adjacent normal venous system. 9,lO,I5 Extension within bone is possible. They are not pulsatile but are soft and compressible, and they characteristically expand with a Valsalva maneuver. Localized intravascular coagulopathy may manifest as a major hematologic disorder. Lymphatic malformations are present at birth and expand by accumulation of fluid. Sudden expansion is usually due to hemorrhage within cysts. Lymphatic malformations manifest as a multitude of small cutaneous or mucosal bullae (for example, lymphatic malformation of the tongue) or as large cystic lesions beneath the skin. 4 ,9,l O,16 The most common site of the cystic variant is the neck, where transillumination of the lesion may be performed. Arteriovenous malformations are rarely noted at birth. Usually, a quiescent lesion expands rapidly after local
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trauma, a surgical procedure, or hormonal changes (for example, during puberty or pregnancyj.v'? Because of the presence of arteriovenous shunts, flow is rapid, and the adjacent vascular structures enlarge. Pulsatility and warmth are present, and eventually a bruit and pain may be perceived.'? Venous hypertension and arterial steal in the adjacent normal tissues may leadto trophic changes, and necrosis and hemorrhage may ensue. Disseminated intravascular coagulation as a result of thrombotic consumption may be present as a hematologic complication. Direct arteriovenous fistulas may develop after trauma alone, typically in an area where veins closely parallel arteries (for example, the superficial temporal artery)." The combination of several vascular lesions or the presence of a vascular tumor should be considered when the clinical manifestations do not correspond to one of the aforementioned pattems.v'" In this report, we describe our experience with facial vascular anomalies in 36 patients. The MR findings and the correlated computed tomographic, angiographic, clinical, surgical, and histologic characteristics are presented. PATIENTS AND METHODS In 36 patients (24 female and 12 male patients) who ranged in age from 2 months to 79 years (median age, 14 years), 46 MR examinations were performed. Previous surgical procedures had been performed in 27 patients, 1 of whom had undergone 10 prior operations. Of the 36 patients, 33 underwent imaging between October 1985 and 1988, during which time a multidisciplinary treatment program was available. These studies were done before gadolinium was available. Three additional patients underwent MR imaging between 1988 and May 1990. Of the 46 MR examinations, 41 were performed with use of a 1.5-T superconducting magnet (Signa, General Electric, Milwaukee, Wisconsin) and 5 with use of a 0.15- T resistive magnet (Picker, Highland Heights, Ohio). At the discretion of the examining radiologist, sequences were obtained in the axial, coronal, and sagittal planes, typically with a Tlweighted sagittal and a T2-weighted axial imaging sequence. Spin echo imaging included a repetition time of 400 to 600 ms, an echo time of 20 to 30 ms, and 2 to 4 excitations and also a repetition time of 1,500 to 2,200 ms, an echo time of 30 to 40 and 80 ms, and 1 excitation. In three cases, gradient echo imaging was performed with use of 30° flip angle, a repetition time of 50 to 200 ms, and an echo time of 15 to 50 ms. Examinations were performed with use of a 30-cm standard head coil or, in selected cases, a 7.6- or 12.7-cm (3- or 5-inch) surface coil placed over the area of clinical interest. Five patients were examined with intravenous contrastenhanced computed tomographic scans in an axial plane (model 9800, General Electric). Selective angiographic
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Table 2.-Magnetic Resonance Characteristics of Facial Vascular Anomalies in 36 Patients* Total
Juvenile hemangioma Capillary malformation Venous malformationt Lymphatic malformation Arteriovenous malformationt
Mixed Low
T2
Proton density
T1
Type of anomaly
Iso
High
Mixed Low Iso
High
Mixed Low
Iso High
Flow void None Small Large
0
2
0
0
2
0
0
0
0
2
0
0
0
2
3
0
0
3
0
0
0
0
3
0
0
0
3
2
16
0
0
0
16
0
0
16
5
11
2
18
0
9
4
2
3
0
5
0
0
4
2
0
0
7
8
1
0
4
4:j:
0
0
0
3:j:
0
0
0
3:j:
0
0
0
0
0
4
*"Iso" == magnetic resonance signal isointense with adjacent muscle. tOne patient underwent Tl imaging only. :j:Predominant magnetic resonance appearance was of flow voids.
studies were performed in nine patients. Diagnostic venographic studies, performed with use of a femoral vein approach or a direct puncture (or both), were conducted in seven patients. 10 The lesions were classified into one of six types (Table 1), as outlined in the introductory material.v" RESULTS The MR characteristics of the facial vascular anomalies are summarized in Table 2. Most lesions demonstrated a Tl signal that was isointense with adjacent muscle and an increased signal in comparison with muscle on the proton density and T2-weighted scans in their solid nonflowing portions. The hemodynamic nature of the lesions was characterized by the presence or absence of flow voids on MR imaging. Small flow voids were defined as loss of signal consistent with a vascular structure less than or equal to twice the expected diameter of normal vessels in the anatomic region of the lesion. Large flow voids were defined as signal loss greater than twice the diameter of normal vessels in the region of the lesion that could be traced to feeding arteries or draining veins on contiguous MR images.
The anatomic extent of the facial vascular anomalies as detected on MR images is presented in Table 3. The deepest extension of each lesion was characterized as subcutaneous, superficial, deep, or parapharyngeal. Subcutaneous lesions involved the skin and subcutaneous fat. Superficial lesions included the superficial parotid gland and facial muscles. Deep lesions extended to the deep parotid gland, masticatory space, and carotid space. Parapharyngeal lesions involved the tongue, parapharyngeal space, and prevertebral space. Juvenile hemangiomas were present in two patients (2 months and 1 year of age) and demonstrated typical biphasic growth patterns. In the 2-month-old patient, a small cutaneous lesion of the upper lip completely resolved spontaneously, a finding consistent with the clinical diagnosis of a juvenile hemangioma. On MR examination, this lesion had isointense T1 signal (Fig. 1 A) and increased proton density and T2 signal. In the l-year-old child, a large posterior superficial lesion also demonstrated isointense Tl signal and increased proton density and T2 signal (Fig. 1 B and C). Most likely because of its large size (7 em in maximal diameter), this lesion contained small flow voids and slightly crossed the midline. This hemangioma had enlarged during the child's first 9 months of life and then stabilized in size.
Table 3.-Anatomic Findings in 36 Patients With Facial Vascular Anomalies Type of anomaly
Total
Subcutaneous
Juvenile hemangioma Capillary malformation Venous malformation Lymphatic malformation Arteriovenous malformation
2 3 18 9 4
1 2 3 1 0
Deepest extension SuperParatidal Deep pharyngeal
1 1 2 2 1
0 0 5 2 3
0 0 8 4
0
Airway obstruction Yes No
0 0 3 2 0
2 3 15 7 4
Crossed midline Yes No 1 0 8 4
1
1 3 10 5 3
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When the patient was between 9 months and 1 year of age, the lesion decreased slightly in size and elective resection was performed. Port-wine capillary malformations were present in three patients, who had typical port-wine stains. One such lesion, which occurred in association with the Sturge-Weber syndrome, extended into the superficial facial muscles and demonstrated small flow voids. The other two lesions were confined to the skin. All three capillary malformations had isointense TI signal and increased proton density and T2 signal. The lesion was pathologically confirmed in one patient, who underwent a partial resection. Venous malformations were found on histologic examination in 18 patients, 16 of whom had lesions that were characterized as isointense T1 signal and increased proton density and T2 signal. In 11 lesions, small flow voids were detected within the substance of the lesion. Three venous malformations demonstrated substantial venous pooling; in two additional lesions, angiograms showed a mass effect and only a minimal vascular blush (Fig. 2). Computed tomography clearly demonstrated calcified phleboliths in two of the three patients with venous malformations in whom this study was performed (Fig. 3). On the MR scan, the phleboliths were seen as focal areas of decreased signal that simulated flow voids, but they could not be traced on contiguous images. In all three patients, the extent of the vascular lesion was more easily determined with MR imaging than with computed tomography. Venous malformations resulted in airway obstruction (Fig. 4) in three patients, two of whom required tracheostomies. One patient had orbital extension of the lesion, and another patient had sinus involvement. Four patients had multiple lesions. The patient with the most numerous discrete bilateral lesions had overgrowth of the right arm from a combined capillary-venous-lymphatic malformation (Klippel-Trenaunay syndrome). Lymphatic malformations demonstrated the most varied MR appearance (Fig. 5). Four of the nine lesions had mixed TI signal, with areas of increased Tl signal consistent with hemorrhagic degradation products. Two patients had predominantly low Tl signal, and three patients with mixed TI signal also had areas of decreased TI signal. These five patients with decreased T1 signal had MR findings consistent with 'cystic spaces. One lymphatic malformation had orbital extension. Two patients who underwent gradient
Fig. 1. Magnetic resonance images of juvenile hemangiomas. A, Hemangioma of upper lip of 2-month-old patient; lesion subsequently resolved spontaneously. B, Tl-weighted axial image of7em hemangioma with small flow voids in l-year-old child. C, T2weighted axial image of same lesion as shown in B.
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echo imaging had no evidence of flow. Computed tomography, performed in one patient, clearly demonstrated the lesion, but the complex nature of the lesion and its full extent were more readily delineated on the MR scan. In all nine patients, the lesions were characterized histopathologically. Arteriovenous malformations were present in four patients and demonstrated large flow voids on MR imaging. Three of these patients underwent arteriography, which disclosed high-flow vessels that corresponded to the MR flow voids (Fig. 6). These lesions consisted primarily of flow voids with little solid tissue; therefore, they were predominantly characterized as mixed signal on Tl, proton density, and T2 images. One patient underwent Tl-weighted imaging only. Gradient echo imaging, performed in one patient, demonstrated evidence of flow. In one patient, contrastenhanced computed tomography was superior to MR imaging in disclosing the bony changes from the mandibular involvement and the destruction by the arteriovenous malformation but equivalent to MR imaging in demonstrating the extent of the lesion. DISCUSSION On the basis of a thorough clinical evaluation of a lesion, including the growth characteristics, physical appearance, compressibility, and presence or absence of pulsations, and the patient's history, a presumptive diagnosis of facial vascular anomalies is frequently possible. Those patients who do not have a history or physical findings that are characteristic of a particular type of lesion often can be categorized as having a more general diagnosis, such as congenital lesions or neoplasms. Both of these groups-the vascular anomalies and the unknown lesions-are best further evaluated with MR studies. If the physical examination and MR imaging show the typical features of a particular vascular anomaly and treatment is nonsurgical, a biopsy is unnecessary to confirm the diagnosis.' In those patients with even the slightest possibility of the presence of a tumor after the MR examination, however, a biopsy is indicated for further evaluation. In this study, the MR signal characteristics of most lesions were of isointense Tl signal and increased T2 signal.
Fig. 2. Right facial venous malformation. A, Tl-weighted coronal magnetic resonance image, depicting isointense lesion without evidence of flow void (curved arrows). B, Right external carotid arteriogram, showing a minimal vascular blush (arrow) and substantial displacement of normal-sized arteries due to the mass effect. C, Right jugular venogram, demonstrating no retrograde filling of venous malformation and normal size of tributaries of external jugular vein.
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Fig. 3. Venous malformation involving right pterygoid muscles. A, Contrast-enhanced computed tomogram, showing enhancing lesion with several phleboliths (arrow). B, T2-weighted magnetic resonance image, demonstrating signal loss (arrow) that corresponds to the phleboliths, which should not be confused with flow voids.
Fig. 4. Diffuse venous malformation, predominantly involving base of tongue and right parapharyngeal space. Coronal Tl-weighted (A) and axial T2-weighted (B) magnetic resonance images, demonstrating severe tracheal narrowing and displacement to the left (arrows) that resulted in airway compromise. Flow voids were not evident within the lesion.
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Fig. 5. Lobulated cystic lymphatic malformation involving right side of face and upper aspect of neck and extending into parapharyngeal space. Proton density (A) and T2-weighted (B) magnetic resonance images, showing mixed signal intensities and a hemorrhagic fluid-fluid level (arrow).
Therefore, the T 1 and T2 signal characteristics were not helpful in distinguishing most of the vascular lesions except the lymphatic malformations. The lymphatic malformations demonstrated a mixed signal intensity, which was related to the proteinaceous fluids within the cystic cavities and the hemorrhagic degradation products. An important physiologic feature that MR imaging can delineate is the flow characteristics of the facial vascular anomalies. The presence or absence of flow voids6.19.2o and their relationship to the lesion are characteristic of the various vascular lesions. The numerous large flow voids of arteriovenous malformations have a distinctive MR appearance. Although MR imaging can clearly identify arteriovenous malformations, it cannot distinguish between the feeding arteries and the draining veins or precisely locate the nidus. In this situation, angiography is necessary for determining the area of the arteriovenous shunt for subsequent treatment. Most imaging procedures in this study were performed before the availability of gradient echo imaging, gadolinium contrast, and MR angiography. These recent advances in MR imaging have the potential to enhance imaging results." Because of its superior delineation of soft tissues, MR imaging clearly depicted the topographic relationship of the venous malformations to adjacent structures better than did computed tomography or angiography. MR studies can distinguish between a well-defined and an apparent infiltrative margin. The apparent infiltrative nature of these lesions is due to irregular extension of vascular channels into adjacent tissues. The multiplanar capability of MR examination,
including oblique scanning angles, facilitates the precise delineation of lesions and their relationship to adjacent normal structures. In our study, MR imaging was superior to computed tomography in depicting the extent of three venous malformations and one lymphatic malformation. In addition, MR imaging more clearly demonstrated the complex internal nature of the lymphatic malformation than did computed tomography. The size and location of an arteriovenous malformation were demonstrated equally well by MR studies and computed tomography. On computed tomography, the large vascular channels showed intense enhancement with intravenously administered contrast medium. MR examination more clearly identified the internal vascular nature of the lesion than did computed tomography. Other than arteriovenous malformations, entire vascular lesions were not opacified by angiography. MR imaging was superior to angiography in depicting the extent of the lesions. Computed tomography remains a valuable technique for evaluating vascular malformations; however, for maximal benefit, an iodinated contrast agent must be administered. Computed tomography demonstrated radiopaque structures, including bony changes and phleboliths, more clearly than I did MR studies. Lack of signal within a venous malformation, similar to a flow void but not present on contiguous adjacent slices, was typical of phleboliths on MR imaging. The mandibular bony erosion of one arteriovenous malformation was much more clearly demonstrated with computed tomography than with MR imaging. MR studies can identify vascular anomalies that necessitate angiography before invasive treatment is planned.
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Fig. 6. A, Right external carotid arteriogram, demonstrating arteriovenous malformation of right inferior orbital rim with high flow attributable to a large shunt. Arterial supply is an enlarged right facial artery (arrow). Venous drainage is predominantly through superficial facial veins and right superior ophthalmic vein (curved arrow). B, Tl-weighted axial magnetic resonance image obtained with use of a 12.7-cm (5-inch) surface coil, showing multiple large flow voids (arrow), which on contiguous images could be traced to feeding arteries and draining veins demonstrated on the angiogram.
With arteriovenous malformations, arteriography must be performed to delineate the nidus or identify the presence of an arteriovenous fistula before surgical treatment. If embolization is planned, preliminary diagnostic studies, including selective injection of the internal and external carotid arteries bilaterally, will facilitate rating for risk and success. Venography by direct puncture can confirm the diagnosis of a venous malformation but will fail to demonstrate the full extent of the lesion.'? This result is similar to our experience with venous-phase studies during selective arteriography. CONCLUSION MR imaging is a powerful technique for characterizing facial vascular anomalies. Noninvasively, it can determine the extent and the type of facial vascular anomalies better than computed tomography or angiography. Before treatment of arteriovenous malformations, angiography must be performed to delineate the hemodynamic characteristics and to map the associated arteries and veins. When a facial lesion does not conform to the classic appearance of a vascular anomaly and a neoplasm cannot be excluded, pathologic examination of a biopsy specimen is necessary. ACKNOWLEDGMENT We thank Cynthia P. Rausch for expert preparation of the submitted manuscript.
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