Clinical value of classification of venous malformations with contrast-enhanced MR Angiography

Abstract

Aim

To classify venous malformations based on contrast-enhanced MR angiography that may serve as a basis for treatment plan.

Patients and methods

A retrospective analysis was performed in 58 patients with venous malformations who underwent contrast-enhanced MR angiography. Venous malformations were classified according to their venous drainage into: type I, isolated malformation without peripheral drainage; type II, malformation that drains into normal veins; type III, malformation that drains into dilated veins; and type IV, malformation that represents dysplastic venous ectasia. Image analysis was done by two reviewers. Intra and inter-observer agreement of both reviewers and intra-class correlation was done.

Results

The intra-observer agreement of contrast-enhanced MR angiography classification of venous malformations was excellent for the first reviewer (k = 0.83, 95% CI = 0.724–0.951, P = 0.001) and substantial for the second reviewer (K = 0.79, 95% CI = 0.656-0.931, P = 0.001). The inter-observer agreement of contrast-enhanced MR angiography classification of venous malformations was excellent for both reviewers at the first time (K = 0.96, 95% CI = 0.933–1.000, P = 0.001) and second time (k = 0.81, 95% CI = 0.678–0.942, P = 0.001). There was high intra-class correlation of both reviewers for single measure (ICC = 0.85, 95% CI = 0.776–0.918, P = 0.001) and for average measures (ICC = 0.96, 95% CI = 0.933–0.978, P = 0.001).

Conclusion

Contrast-enhanced MR angiography classification of venous malformations may be a useful, simple and reliable tool to accurately classify venous malformation and this topographic classification helps for better management strategy.

Keywords

Venous malformation MR angiography

Introduction

Venous malformations are the most common vascular malformations (60%). Venous varicosities or dysplastic small and large venous channels exist as soft and compressible lesions associated with bluish skin discoloration that distended with a Valsalva maneuver or venous compression.^1–6 Choice of appropriate treatment is challenging because of multiplicity of available modalities. Knowledge of pattern of the venous drainage is essential to select proper treatment plan and to avoid complications of sclerotherapy.^7–12 Different imaging modalities are used for assessment of venous malformations.^13–16 Color Duplex ultrasound is used for initial evaluation of venous malformations, but it cannot define its venous drainage.¹⁷ Phlebography and direct cisternography can detect venous drainage of venous malformations. However, these modalities are invasive, technically difficult, and carry hazards of radiation exposure.¹⁸ Routine and advanced MR imaging such as diffusion-weighted and dynamic susceptibility MR cannot detect venous drainage of venous malformations.^19–21 The conventional non-contrast MRA techniques such as time of fight and phase contrast MR angiography produce static images with prolonged acquisition time and cannot detect small vessels.^13–15

Contrast-enhanced MRA (CE-MRA) accentuated the signal from inflowing blood via the T1-shortening effect of gadolinium, resulting in improved MRA. It can assess AVMs, but it is associated with high dose of contrast medium and early venous filling. The CE-MRA adds information about the presence or absence of deep and superficial conducting veins and their morphology, as well as the presence or absence of primitive venous channels.^22–26 To our knowledge, there is no previous study that discusses the role of CE-MRA in assessment of venous malformations.

The aim of work is to classify venous malformations based on CE-MRA that may serve as a basis for treatment plan.

Patients and methods

Patients

The study was approved by the institutional review board and informed consent from the patients was waived because this is a retrospective study. The inclusion criteria were patients with suspected clinically venous malformations who underwent CE-MRA. We excluded five patients from the study because of missing scans and different diagnosis on case revision. The final patients included in this study were 58 patients (23 females and 35 males; age range from 2 years to 16 years) with venous malformations. The patients clinically presented with soft tissue mass that increases in size and coloration during a Valsalva maneuver, with dependent position (n = 42), bluish skin discoloration (n = 31), cosmetic disfigurement (n = 25), and pain (n = 21).

Contrast MR angiography

All patients received MR imaging examination using 1.5T machine (Magnetom Symphony, Siemens, Version VA12 A, Siemens Medical systems, Erlangen, Germany). Axial localizer image at the affected region and then coronal and sagittal images were obtained with the following parameters: TR/TE = 15/5 ms, flip angle = 25°, slice thickness = 0.8–1 mm, field of view = 15–25 cm, matrix = 104 × 256, band width = 260 Hz/Px and number of average = 1. The time of acquisition ranged from 40 to 60 s. The 3D-MRA slab was positioned over the affected region. The above parameters were fixed at pre- and post-contrast scans. After localization and slab positioning, a complete pre-contrast fast 3D-gradient echo sequence at the desired level was performed with the above parameters. Injection of 0.1 mmol/kg body weight of gadolinium-DTPA was followed by 30 ml saline with MR compatible automatic injector at the rate of 2 ml/s. The sequence was performed after 30, 60, 90, and 120 s after injection of contrast medium to ensure visualization of the contrast material bolus in the venous phases. The pre-contrast dataset is then subtracted from each of the post-contrast datasets. The resultant subtracted images manipulated with a maximum intensity-projections algorithm to produce 3D image of the venous system.

Image analysis

Analysis of CE-MRA images was performed by two radiologists (AA and AG) who are expert in vascular radiology for more than 25 and 15 years, respectively. Both reviewers were blinded to the clinical presentation and final diagnosis. The image analysis was performed independently by each reviewer at two different sessions and then by both reviewers in two different sessions. Both reviewers classified venous malformations according to their draining veins in a way similar to the classification based on phlebography²⁷: type I was isolated malformation without peripheral venous drainage; type II was malformation that drains into normal veins; type III was malformation that drains into dilated veins; and type IV malformation represents dysplastic venous ectasia.

Statistical analysis

The statistical analysis of data was done by using SPSS program (Statistical package for social science version 21, 2012). The weighted kappa statistic (K) including 95% confidence interval (CI) with percentage agreement was made to estimate the proportion of agreement for both raters for CE-MRA classification. The K values were interpreted as follows: k values between 0.01 and 0.20 represented slight agreement; k values between 0.21 and 0.40 fair agreement; k values between 0.41 and 0.60 represented moderate agreement; k values between 0.61 and 0.80 represented substantial agreement; k values between 0.81 and 1.00 represented excellent agreement. A P < 0.05 indicated a statistically significant difference. Intra-observer agreement was estimated from the agreement between both readings from each reviewer at two sessions and inter-observer agreement estimated from agreement of readings from both reviewers at two sessions. Intra-class correlation coefficients (ICC) with the 95% confidence intervals (CI) were calculated for single and average measures to test the reliability of CE-MRA classification system. The classification used for the interpretation of the obtained ICC less than 0.40 represented poor reliability; 0.40–0.75 represented good reliability, and more than 0.75 represented excellent reliability.

Result

The venous malformations were located in the head and neck in 25 (43%) patients, upper limb in 10 (17%) patients, and the lower limb in 22 (36.2%) patients and only one venous malformation was detected in the abdominal wall.

Table 1 shows CE-MRA classification of venous malformation by two reviewers. The venous malformations were classified by first reviewer in the two sessions into type I (Figure 1), isolated venous malformations with no drainage to veins (n = 20, 18), type II (Figure 2) drainage venous malformations into normal veins (n = 21, 22), type III (Figure 3) drainage venous malformations into dilated veins (n = 11, 12), and type IV (Figure 4) drainage venous malformations into ectatic dysplastic veins (n = 6, 6). The intra-observer agreement for CE-MRA classification was excellent for the first reviewer (K = 0.83, 95% CI = 0.724–0.951, P = 0.001) and substantial for the second reviewer (K = 0.79, 95% CI = 0.656 to 0.931, P = 0.001) (Table 2).

Table 1.

CE-MRA classification of venous malformation by two reviewers.

subtypes	CE-MRA appearance	Reviewer 1		Reviewer 2
subtypes	CE-MRA appearance	First time	Second time	First time	Second time
Type 1	Isolated venous malformation with no drainage to veins	20 (34.5%)	18 (31%)	19 (32.7%)	22 (38%)
Type II	Drainage of venous malformation into normal veins	21 (36.2%)	22 (38%)	20 (34.5%)	19 (32.7%)
Type III	Drainage of venous malformation into dilated veins	11 (19%)	12 (20.7%)	12 (20.7%)	10 (17.2%)
Type IV	Drainage of venous malformation into ectatic dysplastic veins	6 (10.3%)	6 (10.3%)	7 (12.1%)	7 (12.1%)

Figure 1.

Venous malformation type I: CE-MRA shows venous malformation with no apparent venous drainage.

Figure 2.

Venous malformation type II: CE-MRA shows venous malformation communicating with normal draining veins.

Figure 3.

Venous malformation type III: CE-MRA shows venous malformation draining into the dilated veins.

Figure 4.

Venous malformation type IV: CE-MRA shows venous malformation draining into the ectatic venous channels.

Table 2.

Intra-observer and inter-observer agreement for CE-MRA classification of venous malformations.

	K	95% CI	P value
Intra-observer agreement
Reviewer 1	0.838	0.724–0.951	0.001
Reviewer 2	0.794	0.656–0.931	0.001
Inter-observer agreement
First time	0.900	0.930–1.000	0.001
Second time	0.810	0.678–0.942	0.001

Venous malformations were classified by both reviewers in the two sessions into type I (n = 20, 19), type II (n = 21, 20), type III (n = 11, 12), and type IV (n = 6, 7). The inter-observer agreement for CE-MRA of both reviewers was excellent (K = 0.90, 95% CI = 0.933–1.000, P = 0.001) (Table 2). There was high intra-class correlation of both reviewers for single measure (ICC = 0.85, 95% CI = 0.776–0.918, P = 0.001) and for average measures (ICC = 0.96, 95% CI = 0.933–0.978, P = 0.001).

Thirteen venous malformations refused to undergo treatment. Sixteen patients with venous malformations type I underwent laser therapy, and 17 patients with venous malformations type II were referred for sclerotherapy. Combined sclerotherapy and surgery were done for eight patients with venous malformations type III, and surgery alone was done for four patients with type IV.

Discussion

The main finding in this study is that CE-MRA is a simple and reliable non-invasive imaging modality that can classify venous malformations into four patterns according to the morphology of their draining veins. There is excellent inter-observer agreement and substantial intra-observer agreement of both reviewers for assessment of the four proposed patterns with high intra-class correlation for single and average measures.

In this study, patients presented with bluish skin discoloration, cosmetic disfigurement, and pain. The most common presenting symptoms of patients with venous malformations include: swelling, pain secondary to mass effect on the adjacent structures, infection, ulceration and thrombophlebitis, and intralesional hemorrhage.^1–5

There are different morphological and hemodynamic classifications of venous malformations. Morphological classifications of venous malformations depend upon the shape, the margin, maximum diameter, location and volume of the lesion.^28–30 The hemodynamic classifications of venous malformations depend upon the pattern of draining veins. The hemodynamic pattern of the draining veins has influence upon the method of treatment and has impact on response of venous malformation to the therapy.^18,27

In this study, we classified venous malformations into four patterns according to their draining veins. This classification system based on anatomical and homodynamic features of venous malformations was developed based upon phlebogrpahy findings.²⁷ This system includes four types of venous malformations. It can be used for therapy planning and suggests a higher risk of complications during percutanenous sclerotherapy in venous malformations type III and type IV as compared to type I and type II lesions.

In this study, there was excellent inter-observer and intra-observer agreement of CE-MRA in classification of venous malformations. Other studies reported that CE-MRA shows excellent inter-observer agreement in classification and characterization of arteriovenous malformations. One study reported that the inter-observer agreement of both readers was excellent for the arterial feeders (k = 0.81), excellent for the nidus (k = 0.91), and good for the venous drainage (k = 0.77) of ateriovenous malformations.²⁴

In this study, there is high intra-class correlation of both reviewers for single measure (ICC = 0.79) and for average measures (ICC = 0.90). One study reported that CE-MRA visualized venous drainage pattern in 16 of 18 patients (89%) (CI = 0.65–0.98) of arteriovenous malformations and the interobserver agreement was good (0.86; CI = 0.6–1.0).³¹

The management of venous malformations is challenging. Currently, there is no consensus on the selection of an appropriate treatment approach. The main goal of treatment of venous malformations is complete eradication of their venous drainage.^7–12 Vascular mapping is essential for evaluation of venous drainage for better direction of the treatment choice towards laser therapy, sclerotherapy, surgery or combination of these modalities.^13–16 In this study, we suggested that CE-MRA may have an impact on patient management in the future as it may help the clinician to select the appropriate methods of treatment. The data obtained from CE-MRA helped for selection of the best method of treatment. We suggest that venous malformations type I can be treated with laser therapy, type II treated with sclerotherpay, and types III and IV can be treated with sclerotherapy, surgery, or combination of the these modalities.

Application of advanced MR techniques improves the spatial resolution of CE-MRA. Application of high 3 tesla scanner using higher strength of the gradient systems provides a higher signal from the blood and suppression of the background that can be used to obtain images with higher spatial resolution.²² The use of parallel imaging improves the image quality and spatial resolution by increasing the anatomic coverage and removing the aliasing artifact.^9,10 Applications of four-dimensional MRA accelerate the dynamic MRA scans up to 60 times with a sub-second temporal sampling rate and follow contrast hemodynamics with the near-isotropic spatial resolution of 1–1.5 mm that helps for better delineation of venous drainage.³²

There are few limitations of this study. First, this study included small number of patients. Further studies upon large number of patients with multi-center studies enhanced the accuracy of this technique. Second, there is no follow-up CE-MRA of venous malformations after therapy. Further studies upon venous malformations after therapy are recommended to evaluate the impact of different management methods upon venous malformations and prediction of success of different treatment. Third, there is no correction with conventional venography. Further studies compared CE-MRA with conventional venography in classification of venous malformations.

Conclusion

CE-MRA classification of venous malformations may be a useful, simple and reliable tool to accurately classify venous malformation and this topographic classification helps for better management strategy.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

References

Lee

Baumgartner

Berlien

et al.

Diagnosis and treatment of venous malformations consensus document of the International Union of Phlebology (IUP): updated 2013. Int Angiol 2015; 34: 97–149.

Dasgupta

Patel

. Venous malformations. Semin Pediatr Surg 2014; 23: 198–202.

Judith

Ulrike

Siegmar

et al.

Current concepts in diagnosis and treatment of venous malformations. J Craniomaxillofac Surg 2014; 42: 1300–1304.

Lee

Laredo

. Venous malformation: treatment needs a bird's eye view. Phlebology 2013; 28: 62–63.

Lee

. Venous malformation and haemangioma: differential diagnosis, diagnosis, natural history and consequences. Phlebology 2013; 28: S176–S187.

Razek

. Vascular neurocutaneous disorders: neurospinal and craniofacial imaging findings. Jpn J Radiol 2014; 32: 519–528.

Richter

Braswell

. Management of venous malformations. Facial Plast Surg 2012; 28: 603–610.

Lee

Laredo

. Venous malformation: treatment needs a bird's eye view. Phlebology 2013; 28: 62–63.

Heit

Prestigiacomo

et al.

Guidelines and parameters: percutaneous sclerotherapy for the treatment of head and neck venous and lymphatic malformations. J Neurointerv Surg 2016; Epub ahead of print. DOI: 10.1136/neurintsurg-2015-012255.

10.

Aronniemi

Castrén

Lappalainen

et al.

Sclerotherapy complications of peripheral venous malformations. Phlebology 2016; 31: 712–722.

11.

Rabe

Pannier

. Sclerotherapy in venous malformation. Phlebology 2013; 28: 188–191.

12.

McCafferty

. Management of low-flow vascular malformations: clinical presentation, classification, patient selection, imaging and treatment. Cardiovasc Intervent Radiol 2015; 38: 1082–1104.

13.

Olivieri

White

Restrepo

et al.

Low-flow vascular malformation pitfalls: from clinical examination to practical imaging evaluation – Part 2, Venous malformation mimickers. AJR Am J Roentgenol 2016; 206: 952–962.

14.

Legiehn

Heran

. Venous malformations: classification, development, diagnosis, and interventional radiologic management. Radiol Clin North Am 2008; 46: 545–597.

15.

Abdel Razek

Denewer

Hegazy

et al.

Role of computed tomography angiography in the diagnosis of vascular stenosis in head and neck microvascular free flap reconstruction. Int J Oral Maxillofac Surg 2014; 43: 811–815.

16.

Razek

Huang

. Soft tissue tumors of the head and neck: imaging-based review of the WHO classification. Radiographics 2011; 31: 1923–1954.

17.

Eivazi

Fasunla

Hundt

et al.

Low flow vascular malformations of the head and neck: a study on brightness mode, color coded duplex and spectral Doppler sonography. Eur Arch Otorhinolaryngol 2011; 268: 1505–1511.

18.

Kishi

Morita

Terada

et al.

Physiological interpretations of radiographic findings on malformations of small veins: seriality of cisterns, communications to systemic veins and relationship to muscles. Phlebology 2014; 29: 9–15.

19.

Navarro

. Magnetic resonance imaging of pediatric soft-tissue vascular anomalies. Pediatr Radiol 2016; 46: 891–901.

20.

Abdel Razek

Gaballa

Elhawarey

et al.

Characterization of pediatric head and neck masses with diffusion-weighted MR imaging. Eur Radiol 2009; 19: 201–208.

21.

Razek

Elsorogy

Soliman

et al.

Dynamic susceptibility contrast perfusion MR imaging in distinguishing malignant from benign head and neck tumors: a pilot study. Eur J Radiol 2011; 77: 73–79.

22.

Krishnamurthy

Malone

Lyons

et al.

Body MR angiography in children: how we do it. Pediatr Radiol 2016; 46: 748–763.

23.

Chavhan

Babyn

John

et al.

Pediatric body MR angiography: principles, techniques, and current status in body imaging. AJR Am J Roentgenol 2015; 205: 173–184.

24.

Razek

Gaballa

Megahed

et al.

Time resolved imaging of contrast kinetics (TRICKS) MR angiography of arteriovenous malformations of head and neck. Eur J Radiol 2013; 82: 1885–1891.

25.

Romeih

Al-Sheshtawy

Salama

et al.

Comparison of contrast enhanced magnetic resonance angiography with invasive cardiac catheterization for evaluation of children with pulmonary atresia. Heart Int 2012; 7: e9–e9.

26.

Razek

Saad

Soliman

et al.

Assessment of vascular disorders of the upper extremity with contrast-enhanced magnetic resonance angiography: pictorial review. Jpn J Radiol 2010; 28: 87–94.

27.

Puig

Aref

Chigot

et al.

Classification of venous malformations in children and implications for sclerotherapy. Pediatr Radiol 2003; 33: 99–103.

28.

Jin

Lin

Chen

et al.

Craniofacial venous malformations: magnetic resonance imaging features that predict treatment outcome. J Oral Maxillofac Surg 2009; 67: 2388–2396.

29.

Goyal

Causer

Armstrong

. Venous vascular malformations in pediatric patients: comparison of results of alcohol sclerotherapy with proposed MR imaging classification. Radiology 2002; 223: 639–644.

30.

Caty

Kauffmann

Dubois

et al.

Clinical validation of semi-automated software for volumetric and dynamic contrast enhancement analysis of soft tissue venous malformations on magnetic resonance imaging examination. Eur Radiol 2014; 24: 542–551.

31.

Nishimura

Hirai

Sasao

et al.

Evaluation of dural arteriovenous fistulas with 4D contrast-enhanced MR angiography at 3T. AJNR Am J Neuroradiol 2010; 31: 80–85.

32.

Krishnamurthy

Bahouth

Muthupillai

. 4D contrast-enhanced MR angiography with the keyhole technique in children: technique and clinical applications. Radiographics 2016; 36: 523–537.