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Soft-Tissue Venous Malformations in Pediatric and Young Adult Patients: Diagnosis with Doppler US¹

¹ From the Departments of Medical Imaging (I.T., J.D., L.G., A.G., H.P., L.A.G.) and Dermatology (C.M.), Hôpital Sainte-Justine, 3175 Côte-Sainte-Catherine, Montréal, Québec, Canada H3T 1C5. Received July 17, 1998; revision requested August 27; final revision received November 13; accepted February 22, 1999. Address reprint requests to J.D. (e-mail: joseedubois@compuserve.com).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To describe the diagnostic features, appearance, and vascularization pattern of venous malformations (VMs) at Doppler ultrasonography (US).

MATERIALS AND METHODS: Between February 1991 and May 1997, 51 soft-tissue VMs were studied with Doppler US in patients between 1 day and 21 years of age (mean age, 9 years). These VMs were located in the maxillofacial region (n = 19), trunk (n = 5), and upper (n = 10) and lower (n = 17) extremities. Twenty–three VMs had venographic confirmation, seven had only histologic confirmation, and 21 had both venographic and histologic confirmation. US was performed with 7.5- or 7–10-MHz linear transducers, a low pulse repetition frequency (mean, 1,680 Hz), and the lowest wall filter (25–50 Hz).

RESULTS: At gray-scale US, VMs appeared as hypoechoic, heterogeneous lesions in 82% of cases. All lesions displayed compressibility. In eight lesions (16%), phleboliths were identified, thus confirming the diagnosis of VM. Analysis of vascular flow revealed monophasic, low-velocity flow in 40 VMs (78%), with an average flow velocity of 0.22 kHz. Biphasic flow was noted at the periphery of three lesions, which is indicative of a mixed capillary-venous malformation. The remaining eight lesions did not display any flow.

CONCLUSION: In pediatric patients, Doppler US is a noninvasive, easily available, and rapid mode of investigation of vascular lesions and can help confirm the diagnosis of VM when it shows a characteristic flow pattern.

Index terms: Arteriovenous malformations, 9_*.14² • Neoplasms, in infants and children, 9_*.14, 9_*.83 • Soft tissues, neoplasms, 9_*.14, 9_*.83 • Soft tissues, US, 9_*.12983 • Veins, US, 9_*.12983 • Venography, 9_*.124

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Venous malformations (VMs) are part of a spectrum of benign vascular lesions commonly found in the pediatric population. These lesions occasionally may be difficult to distinguish solely on the basis of their clinical appearance. In 1982, Mulliken and Glowacki (1) classified congenital vascular anomalies into true hemangiomas and various vascular malformations on the basis of their histologic features.

Vascular malformations are true congenital lesions, which by definition are always present at birth, although they are not always detected (2). They are classified according to the main channel type present: capillary, lymphatic, arterial, venous, or mixed (1). These lesions do not occur in one sex more than the other. They often grow in proportion to the child and can display periods of active growth. Vascular lesions have been categorized further into low- and high-flow types (3) on the basis of the hemodynamic characteristics of the lesions, a distinction that is important in the choice of management strategies. By definition, vascular malformations do not regress spontaneously.

VMs often can be diagnosed on the basis of clinical characteristics: They are bluish, easily compressible, cold, and increase in size with maneuvers aimed at increasing venous pressure (2). However, malformations occasionally may manifest atypical features, and ancillary studies are needed to confirm the diagnosis. A precise diagnosis will lead to the most appropriate treatment; the standard for the diagnosis of VM is venography or biopsy. To our knowledge, the role of Doppler ultrasonography (US) has not been reported. The aim of this study, therefore, is to emphasize the value of Doppler US in the diagnosis of soft-tissue VMs in pediatric and young adult patients.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Between February 1991 and May 1997, 51 VMs in 51 patients (31 female patients, 20 male patients; age range, 1 day to 21 years; mean age, 9 years) were examined by means of gray-scale US and Doppler US in our institution. The lesions were distributed as follows: 19 in the maxillofacial region, five in the trunk, 10 in the upper extremities, and 17 in the lower extremities. Twenty-seven (53%) of the VMs reviewed had been noticed from birth. Eight additional lesions appeared during the first 2 years of life. The remaining 16 VMs appeared at an older age, often in relation to puberty (n = 10) or an episode of trauma (n = 6). At the conclusion of the study period, all examinations were reviewed retrospectively and independently by two investigators (J.D., I.T.). Cases of discrepancy (few) were resolved by a third investigator (L.G.).

Children were referred from our dermatology and vascular malformations clinics by the attending clinician dermatologist, with a presumptive clinical diagnosis of VM. We excluded the patients with Klippel-Trénaunay-Weber syndrome. Our series included patients with VMs only. Patients were referred routinely for US evaluation of a soft-tissue mass clinically suspicious for VM. This diagnosis was proved in all patients: Twenty-three VMs had confirmation only by direct puncture for venography, seven had only histologic confirmation, and 21 had both venographic and histologic confirmation.

Venography was performed percutaneously with direct intralesional puncture and administration of iohexol ([180 mg of iodine per milliliter] Omnipaque; Nycomed, Brampton, Ontario). The venographic criteria used for the diagnosis of VM were those described by Burrows et al (3): ectatic, dilated vascular spaces that demonstrate prolonged pooling of contrast material, with dilated draining veins without arteriovenous shunting or enlarged arterial feeders. Tissue staining was absent or faint and brief.

Biopsy was performed in 28 lesions. For 13 patients, this was performed in an attempt to excise the lesion before referral to our service. Seven patients underwent excision of their lesion after sclerotherapy for treatment of cosmetic and functional impairments. Eight patients had biopsy performed secondary to the treating surgeon's decision (most of these were at the beginning of the study). Histologic analysis confirmed the presence of the ectatic, dilated venous channels characteristic of VM.

US examinations were performed with color Doppler equipment: a Quantum II machine (Siemens, Issaquah, Wash) with a 7.5-MHz linear gray-scale and Doppler transducer or an Ultramark 9 HDI unit (Advanced Technology Laboratories, Bothell, Wash) with a 7–10-MHz linear transducer. A 1-cm-thick standoff pad was used when judged necessary. Examinations were performed by pediatric radiologists (J.D., A.G., L.A.G., H.P.).

All lesions were analyzed according to the following feature characteristics. Echogenicity was assessed as hypo-, iso-, or hyperechoic in comparison with the surrounding subcutaneous tissue. The presence of echogenic shadowing elements, characteristic of calcifications, was noted (Fig 1). Internal architecture was classified as homogeneous or heterogeneous, and the presence of anechoic cavities was noted. In addition, the length, width, and depth were measured by using electronic calipers for all lesions with well-defined borders. Finally, the presence of compressibility was assessed for all lesions, first by means of gentle and then more firm manual probe pressure.

View larger version (144K): [in this window] [in a new window]   Figure 1. Transverse gray-scale US image of a VM in the thigh in a 12-year-old girl shows isoechoic, heterogeneous architecture with a phlebolith (arrow).

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
At gray-scale US, VMs appeared as hypoechoic, heterogeneous lesions in all (Fig 2) but nine patients (42 of 51 [82%]). The nine atypical VMs appeared isoechoic (n = 4 [8%]) or hyperechoic (n = 5 [10%]) with respect to the surrounding subcutaneous tissue but displayed a heterogeneous echo texture in all but one patient (98%). When possible (n = 28), lesions were measured; factors that precluded measurement include the presence of very irregular, infiltrative borders and the presence of very large lesions that could not be imaged entirely at once on the screen (eg, a 25 x 9-cm trunk lesion in a 9-year-old girl). At US, the average volume of measured lesions was 7.4 cm³ (volume range, 0.06–71.3 cm³). Hyperechoic foci with posterior acoustic shadowing, which represented calcifications as confirmed by means of a conventional radiograph or computed tomographic (CT) scan, could be detected in eight lesions (16%). Tubular, anechoic structures, suggestive of vascular channels, were identified within two lesions (4%). All lesions were compressible at testing. The echogenicity was independent of the presence or absence of flow.

View larger version (136K): [in this window] [in a new window]   Figure 2a. Transverse US images of an anterior VM in the neck in an 8-year-old girl. (a) Gray-scale US image displays characteristic hypoechoic, heterogeneous architecture (arrow). The margins of the lesion are delineated by the electronic calipers. (b) Pulsed Doppler US image reveals monophasic (arrow) venous flow diagnostic of VM.

View larger version (131K): [in this window] [in a new window]   Figure 2b. Transverse US images of an anterior VM in the neck in an 8-year-old girl. (a) Gray-scale US image displays characteristic hypoechoic, heterogeneous architecture (arrow). The margins of the lesion are delineated by the electronic calipers. (b) Pulsed Doppler US image reveals monophasic (arrow) venous flow diagnostic of VM.

View larger version (132K): [in this window] [in a new window]   Figure 3a. Images of a VM in the heel in a 4-year-old girl. (a) Transverse gray-scale US image displays atypical architecture with zones of hyperechogenicity (arrowheads) relative to the surrounding subcutaneous tissue. The margins of the VM are delineated by arrows. (b) Transverse pulsed Doppler US image reveals monophasic (arrow) venous flow of 0.1 kHz, which is diagnostic of VM. (c) Oblique direct intralesional venogram outlines numerous venous lakes (arrows), with well-demonstrated draining veins (arrowheads). No arterial structures are visible.

View larger version (101K): [in this window] [in a new window]   Figure 3b. Images of a VM in the heel in a 4-year-old girl. (a) Transverse gray-scale US image displays atypical architecture with zones of hyperechogenicity (arrowheads) relative to the surrounding subcutaneous tissue. The margins of the VM are delineated by arrows. (b) Transverse pulsed Doppler US image reveals monophasic (arrow) venous flow of 0.1 kHz, which is diagnostic of VM. (c) Oblique direct intralesional venogram outlines numerous venous lakes (arrows), with well-demonstrated draining veins (arrowheads). No arterial structures are visible.

View larger version (121K): [in this window] [in a new window]   Figure 3c. Images of a VM in the heel in a 4-year-old girl. (a) Transverse gray-scale US image displays atypical architecture with zones of hyperechogenicity (arrowheads) relative to the surrounding subcutaneous tissue. The margins of the VM are delineated by arrows. (b) Transverse pulsed Doppler US image reveals monophasic (arrow) venous flow of 0.1 kHz, which is diagnostic of VM. (c) Oblique direct intralesional venogram outlines numerous venous lakes (arrows), with well-demonstrated draining veins (arrowheads). No arterial structures are visible.

View larger version (186K): [in this window] [in a new window]   Figure 4a. Transverse US images of a VM in the neck of a 12-year-old girl. (a) Gray-scale US image demonstrates the isoechoic architecture of the lesion. A hyperechoic focus (solid arrow) with posterior acoustic shadowing is identified and represents a phlebolith. The margins of the lesions are delineated by open arrows. (b) Pulsed Doppler US image of the center of the lesion displays monophasic (arrow) venous flow, with an average velocity of 0.4 kHz. (c) Doppler US image obtained at the periphery of the lesion reveals the presence of biphasic flow, both systolic (arrow) and diastolic (arrowhead), which indicates the presence of a capillary component to the VM.

View larger version (151K): [in this window] [in a new window]   Figure 4b. Transverse US images of a VM in the neck of a 12-year-old girl. (a) Gray-scale US image demonstrates the isoechoic architecture of the lesion. A hyperechoic focus (solid arrow) with posterior acoustic shadowing is identified and represents a phlebolith. The margins of the lesions are delineated by open arrows. (b) Pulsed Doppler US image of the center of the lesion displays monophasic (arrow) venous flow, with an average velocity of 0.4 kHz. (c) Doppler US image obtained at the periphery of the lesion reveals the presence of biphasic flow, both systolic (arrow) and diastolic (arrowhead), which indicates the presence of a capillary component to the VM.

View larger version (125K): [in this window] [in a new window]   Figure 4c. Transverse US images of a VM in the neck of a 12-year-old girl. (a) Gray-scale US image demonstrates the isoechoic architecture of the lesion. A hyperechoic focus (solid arrow) with posterior acoustic shadowing is identified and represents a phlebolith. The margins of the lesions are delineated by open arrows. (b) Pulsed Doppler US image of the center of the lesion displays monophasic (arrow) venous flow, with an average velocity of 0.4 kHz. (c) Doppler US image obtained at the periphery of the lesion reveals the presence of biphasic flow, both systolic (arrow) and diastolic (arrowhead), which indicates the presence of a capillary component to the VM.

View larger version (133K): [in this window] [in a new window]   Figure 5. Transverse gray-scale US image of a VM of the lip in a 10-year-old boy demonstrates typical hypoechoic, heterogeneous architecture. No Doppler flow was recorded from the lesion. Arrows demonstrate the margins of the lesion.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

Because deep vascular lesions produce no repercussion on the overlying skin, it often is impossible to assess adequately, on the basis of clinical grounds alone, the presence or the absence of pulsatile flow. The identification of pulsatile flow indicates the presence of a strong arterial component and thereby supports diagnoses such as hemangioma or arteriovenous malformation and rules out the diagnosis of VM. Neoplastic lesions, especially rhabdomyosarcoma and neuroblastoma metastases in this young population, also display an arterial component in most instances.

When not clearly diagnosed at physical examination alone, vascular malformations can be investigated with various imaging modalities. Conventional radiographs, though generally of little use, are invaluable if they demonstrate the presence of phleboliths, as these are pathognomonic of VM (3). CT and magnetic resonance (MR) imaging provide good anatomic detail, with precise delineation of the extent of lesions and the relation to surrounding structures (5). CT is more sensitive than conventional radiography in the depiction of calcifications. MR imaging is helpful in that it can further characterize the type of flow present when flow void is identified (5,6). Despite their great sensitivity, however, neither of these modalities provide information specific enough to allow a precise diagnosis.

Angiography can be invaluable in delineating the feeding and draining vessels and in defining the hemodynamics of vascular lesions. However, angiography is noncontributory in the diagnosis of VM, as findings are generally normal (3). The characteristic features of VM are noted after direct intralesional puncture and lesion opacification, with the demonstration of tortuous, dilated venous channels, without arteriovenous communication (3). Thus, angiography can help rule out high-flow vascular malformations, with their arterial components.

Gray-scale US can help in the diagnosis of VMs and other soft-tissue masses in various ways (7,8). As mentioned previously, the detection of phleboliths will provide a precise diagnosis of VM. However, few VMs display intralesional calcifications (eight lesions [16%] in this study), which diminishes the usefulness of this criterion.

Echo texture also can help in narrowing the differential diagnosis. The majority of venous lesions (82%) that we studied were hypoechoic relative to the surrounding subcutaneous tissue and manifested heterogeneous architecture. Echogenicity alone will not be helpful in eliminating vascular malformations or hemangiomas, as these lesions also are hypoechoic and heterogeneous relative to surrounding tissue (7,8). Such a pattern, however, is different from that of lymphangiomas and allows differentiation.

Lymphangiomas come in two forms: macrocystic and microcystic. Macrocystic lymphangiomas appear as large, anechoic cavities separated by septa at US (8). None of the VMs that we reviewed demonstrated such cystic cavities; only two of the 51 lesions showed evidence of elongated, anechoic structures that easily could be demonstrated to represent vascular structures.

Conversely, microcystic lymphangiomas consist of a myriad of microscopic cavities, which give rise to a hyperechoic texture in relation to the surrounding subcutaneous tissue, owing to the large number of interfaces encountered by the ultrasound beam (8). Only five (10%) of the lesions that we reviewed manifested a hyperechoic texture when compared with surrounding tissue. All of the nine atypical VMs displayed monophasic flow at Doppler US; lymphangiomas, on the other hand, are globally avascular, apart from the septa, from which a mixed type of vascular flow, both venous and arterial, occasionally can be recorded (8).

Doppler US offers great promise in the differentiation of soft-tissue vascular lesions (9–11). We recently have reported the Doppler features characteristic of hemangiomas (12): high vessel density (defined as more than five structures per square centimeter) and a peak arterial Doppler shift of 2 kHz or more. The application of these criteria resulted in a sensitivity of 84% (59 of 70 hemangiomas) and a specificity of 98% (45 of 46 hemangiomas) in the Doppler diagnosis of hemangiomas. Hübsch et al (10) described the appearance of arteriovenous malformations at pulsed and color-coded Doppler US and demonstrated that US can be of great help in the diagnosis of soft-tissue vascular lesions.

Three (6%) of the 51 lesions in our series showed a biphasic component to their vascular flow. In lesions with biphasic vascular flow, a mixed vascular malformation is likely, such as capillary-venous or lymphatic-capillary-venous malformations (1). Pure monophasic flow often can be recorded from other sites within the lesion. The arterial signal remains of low velocity, and there is no confusion possible with the high-flow vascular malformations.

In 16% (eight of 51) of the VMs reviewed, no detectable flow was recorded. The absence of flow may reflect thrombosis of the malformation at the time of thrombophlebitis, usually accompanied clinically by pain. The absence of recordable flow also could be an indication of the limitations of the equipment.

Other entities that can mimic VMs clinically include hematomas. A history of trauma and the absence of venous flow will help separate the two entities in the majority of cases. It also is easy to exclude the diagnoses of rhabdomyosarcoma and neuroblastoma metastases, because soft-tissue neoplastic lesions are not compressible (7). Furthermore, Doppler analysis often can demonstrate the presence of arterial and venous flow, with arteriovenous fistulas, in these malignancies.

In conclusion, US can help in the diagnosis of clinically atypical VMs. We suggest the following criteria for the US diagnosis of VM. At gray-scale US, VMs are hypoechoic, heterogeneous lesions in which phleboliths may be detected (pathognomonic if present), and they display compressibility. At Doppler analysis, monophasic, low-velocity venous signal is encountered. The presence of slow arterial flow can suggest a mixed form of vascular malformation. In the future, it will be interesting to perform a prospective study to determine the sensitivity and specificity of the various imaging modalities in the diagnosis of hemangiomas and vascular malformations.

	Footnotes

 
9_*. Vascular system, location unspecified

Abbreviation: VM = venous malformation

Author contributions: Guarantors of integrity of entire study, J.D., I.T.; study concepts, J.D.; study design, I.T., J.D., L.A.G., H.P.; definition of intellectual content, I.T., J.D.; literature research, I.T., J.D.; clinical studies, all authors; data acquisition, I.T., J.D., L.G., A.G.; data analysis, I.T., J.D., L.G.; manuscript preparation, I.T., J.D., L.A.G., H.P.; manuscript editing, I.T., J.D., L.A.G., H.P., C.M.; manuscript review, all authors

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

1. Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 1982; 69:412-420.[Medline]
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4. Letson GD, Greenfield GB, Heinrich SD. Evaluation of the child with a bone or soft-tissue neoplasm. Orthop Clin North Am 1996; 27:431-451.[Medline]
5. Totty WG, Murphy WA, Lee JKT. Soft-tissue tumors: MR imaging. Radiology 1986; 160:135-141.[Abstract/Free Full Text]
6. Meyer JS, Hoffer FA, Barnes PD, Mulliken JB. Biological classification of soft-tissue vascular anomalies: MR correlation. AJR 1991; 157:559-564.[Free Full Text]
7. AbiEzzi SS, Miller LS. The use of ultrasound for the diagnosis of soft-tissue masses in children. J Pediatr Orthop 1995; 15:566-573.[Medline]
8. Sintzoff SA, Jr, Gillard I, Van Gansbeke D, Gevenois PA, Salmon I, Struyven J. Ultrasound evaluation of soft-tissue tumors. J Belge Radiol 1992; 75:276-280.[Medline]
9. Foley WD, Erickson SJ. Color Doppler flow imaging. AJR 1991; 156:3-13.[Abstract/Free Full Text]
10. Hübsch P, Trattnig S, Kainberger FM, Barton P, Karnel F. Imaging of peripheral arteriovenous malformations using color-coded Doppler sonography. Ultraschall Med 1991; 12:87-90[German].[Medline]
11. Bruns J, Lussenhop S, Behrens P. Ultrasound imaging of soft tissue tumors of the extremities and para-articular soft tissue changes. Ultraschall Med 1994; 15:74-80[German].[Medline]
12. Dubois J, Patriquin HB, Garel L, et al. Soft-tissue hemangiomas in infants and children: diagnosis with Doppler sonography. AJR 1998; 171:247-252.[Abstract/Free Full Text]

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Trop, I. Articles by Garel, L. A. Search for Related Content PubMed PubMed Citation Articles by Trop, I. Articles by Garel, L. A.