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Symptomatic Developmental Venous Anomaly: State-of-the-Art Review on Genetics, Pathophysiology, and Imaging Approach to Diagnosis C.C.-T. Hsu and T. Krings AJNR Am J Neuroradiol 2023, 44 (5) 498-504 This information is current as of June 3, 2023. doi: https://doi.org/10.3174/ajnr.A7829 http://www.ajnr.org/content/44/5/498 REVIEW ARTICLE Symptomatic Developmental Venous Anomaly: State-of-the- Art Review on Genetics, Pathophysiology, and Imaging Approach to Diagnosis C.C.-T. Hsu and T. Krings ABSTRACT SUMMARY: Developmental venous anomalies (DVAs) are the most common slow-ﬂow venous malformation in the brain. Most DVAs are benign. Uncommonly, DVAs can become symptomatic, leading to a variety of different pathologies. DVAs can vary signif- icantly in size, location, and angioarchitecture, and imaging evaluation of symptomatic developmental venous anomalies requires a systematic approach. In this review, we aimed to provide neuroradiologists with a succinct overview of the genetics and categori- zation of symptomatic DVAs based on the pathogenesis, which forms the foundation for a tailored neuroimaging approach to assist in diagnosis and management. ABBREVIATIONS: BRBNS ¼ blue rubber bleb nevus syndrome; CCM ¼ cerebral cavernous malformation; CMMRD ¼ constitutional mismatch repair deﬁ- ciency syndrome; CVMS ¼ cerebrofacial venous metameric syndrome; DVA ¼ developmental venous anomaly; WMH ¼ white matter hyperintensities evelopmental venous anomaly (DVA) is an extreme varia- Neurovascular and Genetic Pathogenesis Dtion of a transmedullary vein composed of a radial complex The neurovascular hypothesis surrounding the etiology of DVA is of medullary veins resembling a “Medusa head,” which converges based on the neurovascular adaptation of the brain venous vascu- into a “collector” vein that ultimately drains into either the deep lature secondary to a nonspecific insult during vasculogenesis, or superficial cerebral venous system. DVAs are the most com- leading to the developmental arrest of medullary veins in the late 2,5 mon form of slow-flow venous malformation in the brain, with first trimester of gestation. The cerebral venous system will cre- an estimated incidence of 2.6%6.4%, and the overwhelming ate compensatory pathways to counter the abnormality in the su- majority are asymptomatic. Histologically, DVAs are composed perficial or deep venous circulation during the period of venous 2,5 of dilated venous channels that are interspersed in the white mat- plasticity in utero and early infancy. This feature is supported ter, with simple or complex variations in venous architecture and by the observation of DVAs both in utero and in the perinatal pe- drainage patterns. DVAs represent a less efficient form of the ve- riod. In recent years, genetic studies have advanced our under- nous drainage route, which is dependent on one or few collector standing of the pathogenesis of DVAs. Genetic analysis of DVAs veins, and with time, the exposure to higher venous pressure may associated with a sporadic cerebral cavernous malformation cause vascular remodeling with vessel wall thickening and micro- (CCM) suggests that DVAs could be an intermediate lesion. vascular hyalinization. Evidence from cohort studies and case se- DVAs may have a somatic activating mutation in the PIK3CA ries suggests a diverse array of clinical manifestations related to gene, leading to a gain of function, which acts as a genetic precur- 3,4 symptomatic DVAs. We performed a comprehensive review of sor to a sporadic CCM. An acquired second-hit mutation in the the pathogenesis of DVAs and discuss imaging and management CCM complex (KRIT1, CCM2, PDCD10)or MAP3K3 then results approaches to symptomatic DVAs. in the formation of a sporadic CCM, supported by the observa- tion that sporadic CCMs often develop within the venous drain- Received October 15, 2022; accepted after revision February 23, 2023. age territory of the DVA. On the other hand, hereditary CCMs From the Division of Neuroradiology (C.C.-T.H.), Department of Medical Imaging, preferentially develop via a mutation in the CCM complex Gold Coast University Hospital, Southport, Queensland, Australia; Division of (CCM1, CCM2, CCM3 gene loci) or the MAP3K3 locus, causing Neuroradiology (C.C.-T.H.), Lumus Imaging, Varsity Lakes, Queensland, Australia; and Division of Neuroradiology (T.K.), Department of Medical Imaging, Toronto multiple quiescent CCMs, which may acquire an additional muta- Western Hospital; University Medical Imaging Toronto and University of Toronto, tion in PIK3CA, driving lesional growth. Ontario, Canada. This review was presented as an education exhibit (NR118-ED-X) at the Radiological Society of North America (RSNA) Annual Meeting in 2016 and received a Certiﬁcate of Merit. Symptomatic DVA Symptomatic DVA is an umbrella term that encompasses a Please address correspondence to Dr. Charlie Chia-Tsong Hsu, MBBS, FRANZCR, Gold Coast University Hospital, Division of Neuroradiology, Department of Medical Imaging, 1 diverse range of DVA-related complications. Systematic review Hospital Boulevard, Southport, Queensland, Australia; e-mail: email@example.com predominately from low-level evidence (ie, case series or case- Indicates open access to non-subscribers at www.ajnr.org http://dx.doi.org/10.3174/ajnr.A7829 control studies) showed that an astounding 61% of DVAs are 498 Hsu May 2023 www.ajnr.org As to the formation of CCMs in DVAs, there is a recently proposed genetic model for the formation of CCMs from a “2-hit hypothesis.” However, a more mechanical model for the de novo formation of a CCM around a DVA is proposed on the ba- sis of a combination of venous conges- tion and venous ischemia due to poor venous outflow leading to a release of local angiogenetic factors and endo- FIG 1. FLAIR (A) shows a mixed-signal-intensity CCM (arrowhead) in the left insular cortex with an internal blood-ﬂuid level and no perilesional edema. A collector vein of a DVA (arrow)is seen thelial proliferation. Newly formed from the ventricular ependyma to the CCM, which is barely visible on the SWI (B) and becomes fragile vessels are prone to bleeding, more conspicuous on the susceptibility-weighted MIP image (C). creating an initial petechial hemor- rhage, and repeat cycles of re-endothe- lialization and hemorrhage eventually lead to the classic multilobulated MR imaging appearance of a CCM. The triggered angiogenesis, which forms fragile vessels prone to hemor- rhage as well as recurrent cycles of angiogenesis and microbleeds ultimately lead to the formation of CCMs. The FIG 2. A patient with right facial pain and dysesthesia. SWI (A) shows a posterior pontine DVA following anatomic factors predispose (arrow) and an associated CCM (arrowhead) involving the intra-axial and cisternal segments of to the development of CCMs within the the right trigeminal nerve. FLAIR (B) demonstrates hyperintense edema along the right lateral as- pect of the pons (arrowhead). Coregistered T2 sampling perfection with application-optimized drainage territory of a DVA: infratento- contrasts by using different ﬂip angle evolutions (SPACE sequence; Siemens) (C)conﬁrms CCM rial DVA location, drainage of the col- involvement of the right trigeminal nerve. lector into a deep vein, torsion of the draining vein, $5 medullary veins asymptomatic: 23% with nonspecific clinical presentation, 6% draining into a collector, stenosis of .55% of the medullary with a focal neurologic deficit, 6% with hemorrhage, 4% with veins, and an acute angle between the medullary and the collector 1 8,11-13 seizures, and ,1% with infarct. However, given our clinical vein of#106.5°. Note that most of the above-mentioned ana- tomic factors contribute to a decreased outflow of the DVA, thus experience, this reported incidence of symptomatic DVAs is very likely overestimated due to reporting bias. In fact, in a pop- supporting a venous congestion model of the formation of CCMs ulation-based study, most DVAs, ie, 98%, were detected inci- in the vicinity of a DVA. Systematic factors such as major infec- dentally, with only 2% of DVAs being symptomatic and tious illness, chronic inflammatory disorders, and radiation expo- 1 12 attributed to hemorrhage or infarct. The natural course of sure/treatment are also implicated in the formation of CCMs. patients with DVA suggests a very low risk of hemorrhage after The proinflammatory state is believed to promote thrombosis the first presentation, ranging from 0% to 1.28% per year. within the DVA, raising the venous pressure to promote an envi- During the past decade, advanced imaging techniques have ronment for CCM formation. Topographical location of CCMs are important as cortical or juxtacortical location or limbic involve- aided our understanding of DVAs. Optimized imaging proto- ment aremoreproneto seizure. Brainstem CCM may cause cra- cols should be applied to investigate symptomatic DVAs, tai- nial neuropathy through the involvement of the cranial nerve lored to clinicopathologic entities. nuclei, intra-axial cranial nerve pathway or even direct extension Coexisting CCM or Capillary Telangiectasia into the cisternal cranial nerves (Fig 2). Hemorrhagic propensity CCMs are vascular sinusoidal lesions lined by a single endothelial of CCM hemorrhage is based on the history of prior hemorrhage layer in a background of a collagenous matrix. CCMs are devoid and this can be quantitatively analyzed through the CCM hemo- of arterial or venous communication. They have a strong associa- siderin burden and its evolution over time on quantitative suscepti- 16,17 tion with sporadic DVAs, with a frequency of coexistence of bility mapping (QSM). Higher mean susceptibility value on between 2%and 33%(Fig 1). Theprevalenceof CCMs with DVAs QSM positively correlates with patient age and prior hemorrhagic also have a positive correlation with increasing age. SWI is the episodes, whilst patients with clinically stable CCM demonstrate 16,17 ideal sequence to detect DVAs with CCMs due to the increased lower mean susceptibility value (Fig 3). contrast conspicuity of the deoxyhemoglobin in the venous blood Less commonly, capillary telangiectasias can be seen in the and the presence of blood products in CCMs. The SWI sequence venous drainage territory of a DVA. Capillary telangiectasia on high-field-strength 7T MR imaging is more sensitive for depict- consists of clusters of dilated capillaries with intervening normal ing smaller-sized DVAs associated with sporadic CCMs, which brain parenchyma and is more commonly located in the brain- may otherwise not be visible on 3T MR imaging. stem but can also be found in the supratentorial brain. Capillary AJNR Am J Neuroradiol 44:498–504 May 2023 www.ajnr.org 499 matter disease) and are more common in a periventricular location of the DVA. WMH associated with DVAs were statistically seen more frequently with coexisting microbleeds, supporting the notion of a common pathogenic (ie, venous congestive) process. Basal ganglia and deep cerebellar nuclei are regions of the brain with higher metabolic demands. The pres- ence of a DVA in these locations across time may lead to increased mineraliza- FIG 3. A middle-aged patient with new-onset ataxia. T1WI (A)and SWI MIP (B)showa CCM in the tion within the affected deep gray matter right superior cerebellar peduncle (arrowheads) and a large left cerebellar DVA with the collector structure (Fig 4). Metabolic abnormal- vein (arrow) draining into the transverse sinus. Quantitative susceptibility mapping (C)analysis of ities can also be encountered in the the CCM shows a high mean susceptibility value of 858 parts per billion (with threshold). An ROI with a red boundary represents the exclusive object boundary, and the purple area represents venous drainage territory of a DVA. A thresholded pixels (150 parts per billion). SWIM (Siemens) parameters: TE ¼ 20.00 ms; TR ¼ 27.00 ms; small case series of 22 patients found ﬂip angle ¼ 15 ;resolution ¼ 0.937 0.937 2.5 mm. Images courtesy of Dr E. Mark Haacke. that 76% of DVAs studied had meta- bolic changes on FDG-PET/CT scans in the form of hypometabolism, which was significantly more common in older patients (Fig 5). Asubsequent larger study with 54 patients with 57 DVAs showed evidence of metabolic abnor- malities in 38% of patients; in this study, hypometabolism was more common in DVAs draining gray matter rather than white matter. Hypometabolism has been reported in regions corresponding to neurologic symptoms; for example, FIG 4. Noncontrast CT of the head (A and B) shows dystrophic calciﬁcation of the anterior right hypometabolism was seeninthe visual putamen and pulvinar of the thalamus (arrows). CTV MIP sagittal image (C) shows a right basal ganglia DVA (arrowheads) with the collector vein draining into the ipsilateral internal cerebral tracts in patients with visual symptoms vein (arrows). and a corresponding DVA. Most interesting, structural abnormalities (ie, telangiectasia has a more benign natural history than CCMs, WMH) were not seen in these patients with abnormalities on 21,22 and its detection requires SWI and a gadolinium-enhanced functional images. Again, this finding is supportive of the T1-weighted sequence for diagnosis. Thus, coexisting capillary notion that DVAs have a less robust venous drainage pathway. telangiectasia with a DVA may be underreported. The relationship between DVA and demyelination is not well-understood. Demyelination is an autoimmune disease with a perivascular pattern of inflammatory response secondary to lym- Parenchymal Abnormalities The brain parenchyma in the venous drainage territory of a DVA phocytic and monocytic infiltration. Brain parenchyma around a DVA may be more vulnerable to the formation of demyelinating can be associated with white matter hyperintensities (WMH), microbleeds, mineralization, metabolic derangements and may plaques in patients with pre-existing demyelinating diseases such even be more prone to the formation of demyelination plaque in as MS (Fig 6). A proposed theory is that venous congestion patients with pre-existing demyelinating diseases such as MS. DVA may lead to a higher and longer duration of lymphocytic infiltra- drainage has a relatively larger venous territory compared with tion and, thus, a greater degree of a neuroinflammatory reaction physiologically normal cortical or medullary veins and is reliant on than a brain with a normal venous drainage pattern. usually #1 collector vein. The venous drainage territory of a DVA Uncommonly, DVAs can be seen in regions of malformation usually has only a deep or a superficial drainage route rather than of cortical development (polymicrogyria, pachygyria, and focal multiple superficial and a deep drainage possibility. With time, the cortical dysplasia). It is uncertain whether the coexistence of the 2 thus-impaired venous hemodynamics may contribute to the pro- entities is incidental or due to a shared common insult in the gressive thickening and hyalinization of the venous walls of DVAs, pathway of cerebral venous development, with interruption of leading to increased resistance, decreased compliance, and venous normal cortical development and of normal cortical and dural ve- hypertension causing focal edema and gliosis in the circumjacent nous sinus development. The true incidence of the association of white matter or mineralization of the adjacent gray matter. WMH polymicrogyria and DVA is not known because the studies were around a DVA have an incidence of 12.5% (an adjusted prevalence based on case series with small sample sizes. However, it is of 7.8% after exclusion of patients with moderate-to-chronic white unlikely that a DVA contributes to epileptogenesis. A case series 500 Hsu May 2023 www.ajnr.org FIG 5. A patient with headache and ataxia. CTA sagittal and axial MIP images (A and B) show a right cerebellar hemisphere DVA (arrowheads) with the collector vein (arrow) draining into the vein of Galen. Corresponding [ F] FDG-PET/CT attenuation-corrected image (C)and a fused PET/CT image (D) show moderate reduction of [ F] FDG uptake in the right cerebellar hemisphere in the venous territory of the large DVA (asterisk). FIG 6. A patient with MS with an SWI (A) demonstrating a DVA. FLAIR at 6-month (B), 1-year (C), and 2-year (D) follow-up shows an enlarging demyelinating plaque (arrows) centered around the DVA. Flow-Related Complications As mentioned above, DVAs are related to a less compliant venous drainage of thebrain becauseeither thedeep or the superficial venous routes are not estab- lished. Thus, a limited number of collec- tor veins drain a relatively large territory of brain parenchyma. Collector veins can, therefore, be overloaded due to the FIG 7. DSA cerebral catheter angiogram in the arterial phase image (A) demonstrates a left occi- multiple, dilated medullary veins feed- pital AVM nidus (arrowhead) supplied by the left posterior cerebral artery (arrow). Subsequent late arterial (B) and early venous (C) images show the AVM nidus (arrowhead) draining into a right ing them. A disturbance in the balance occipital DVA (arrowhead), with an early venous ﬁlling of the collector vein (arrowhead). The between inflow and outflow of blood patient underwent stereotactic radiation treatment with successful obliteration of the AVM can lead to flow-related neurologic com- nidus with preservation of the DVA venous architecture. plications. Flow-related complications were found in up to 71% of sympto- by Striano et al showed only 4 of 1020 patients with epilepsy matic DVAs, though this study was likely biased, given its referral had associated DVAs. It is uncertain whether DVAs and cortical base from a neurovascular center. Flow-related complications dysplasia share a common cerebrovascular pathogenesis; how- include increased flow from an arteriovenous shunt such as a ever, DVAs are unlikely to constitute an epileptogenic focus. DVA draining an AVM (Fig 7)ora “microshunting” phenomenon Nevertheless, it is important to identify the presence of a DVA in from increased arterial blood flow into a DVA, leading to early ve- the area of cortical dysplasia. In the context of neurosurgical nous filling. DVA outflow complications can be attributed to either resection of an focal cortical dysplasia (FCD), unknowing or in- stenosis or thrombosis of the DVA collector vein. A DVA with a advertent resection of the DVA may result in catastrophic venous MicroShunt shows early venous filling of the DVA on angiography infarction due to its vulnerability to hemodynamic changes, fur- secondary to an increased arteriolar inflow of blood. This is a phe- ther highlighting DVAs being “no-touch” lesions. nomenon most commonly seen in large-sized DVAs or DVAs AJNR Am J Neuroradiol 44:498–504 May 2023 www.ajnr.org 501 Venous thrombosis can occur in DVAs, leading to venous ischemia or hemorrhage. The paucity of reports of thrombosed DVAs in the earlier litera- ture may be due to under-recognition and reporting. Marked hyperdensity of the collector vein on noncontrast CT may be a sign of a thrombosed DVA and warrants further investigation with CT or MRV. A literature review of a small number of cases of thrombosed DVAs suggests similar procoagulant risk factors, such as oral contraception, postpartum, or no identifiable risk. There is currently no evidence to sug- gest that DVAs are more prone to thrombosis than normal cerebral veins. However, it is important for the radiol- ogist to identify a thrombosed DVA because treatment is similar to that of venous or dural sinus thrombosis: Anticoagulation is used in the treat- ment of thrombosed DVAs, aiming to FIG 8. A patient with headache and ataxia. Contrast-enhanced T1WI (A–C) shows the DVA prevent the progression of the throm- medusa veins in the cerebellar hemispheres (arrowheads) with a pair of draining veins and ulti- bus, limit new thrombus formation, mately a common collector vein (arrows) draining into the right tentorial venous sinus. DSC MRI perfusion demonstrates a pronounced and asymmetrically increased MTT (D) in the right cerebel- and facilitate recanalization of the col- lar hemisphere, consistent with venous hypertension. CBV (E)and CBF (F)images shows expected lector vein (Fig 9). The standard pre- increased cerebral blood volume and ﬂow in the DVA medusa veins. caution for initiating anticoagulation is unchanged except for the potential risk of bleeding when there is a coexisting CCM. DVAs with ve- nous outflow obstruction due to narrowing or kinking of the collector veins can also lead to increased venous congestion. Neurovascular intervention could be considered in selective cases when conservative treatment fails. Recently, a case of rescue venous stent placement has been reported in a patient with a pon- tomedullary DVA with venous outflow obstruction despite con- servative treatment with anticoagulation. Spontaneous hemorrhage related to a DVA is uncommon and should be attributed to an underlying CCM, venous out- flow obstruction, or flow-related shunt with a microaneurysm FIG 9. A young patient presented with a sudden onset of severe unless proved otherwise, further highlighting DVAs being no- headaches after a marathon race. Presentation CTV (A) shows throm- touch lesions, which should not be removed, irradiated, or em- bosis of a DVA collector vein (arrow) overlying the right frontal cere- bolized. Vascular imaging and recognition of the DVA are par- bral convexity. The patient was placed on antiplatelet medication, amount becauseoften theDVA could be masked or distorted and a follow-up CTV (B) showed a resolution of the thrombus. by the hematoma. When the surgical evacuation of a cerebral with complex angioarchitecture. MR imaging perfusion techniques hematoma is considered, effortshould bemadeto preservethe such as DSC and arterial spin-labeling can better characterize the DVA. 26-29 microcirculation of a DVA. On DSC perfusion, normal DVAs follow the cerebral vein and dural venous sinus hemodynamics, Mechanical Effect with elevated relative CBV and CBF. DVAs with venous outflow The collector vein of a DVA can rarely lead to a mechanical 26-29 impairment may reveal an elevated MTT (Fig 8). In a cohort effect on adjacent structures. In the posterior fossa, collector study, Jung et al demonstrated that the area around a DVA with veins near the root entry zone of cranial nerves can lead to neu- increased signal intensity on T2 and FLAIR showed increased rela- rovascular conflicts such as trigeminal neuralgia. The neurovas- tive CBV and MTT compared with normal white matter. This cular decompression procedure requires more attention because finding is supportive of the hypothesis of symptomatic DVAs with the venous wall of the DVA collector vein is more delicate than a microshunt leading to venous congestion and, with time, perive- an arterial vessel and has to be preserved. Rarely, the DVA nular gliosis around the DVA. collector vein can obstruct CSF flow at the cerebral aqueduct 502 Hsu May 2023 www.ajnr.org DVAs. It is an autosomal recessive bial- lelic (homozygous) germline mutation in the mismatch repair genes (MLH1, MSH2, MSH6,and PMS2). CMMRD manifests as neoplastic and non-neoplas- tic processessuch asa DVA. Oncologic manifestations of the CMMRD are vari- able in the CNS, along with intestinal tumors and hematologic malignancy. There is a robust association of CMMRD with DVAs, which has been suggested to FIG 10. A midline midbrain DVA with the collection vein (arrow) obstructs the cerebral aqueduct be a potential quantifiable factor for leading to ventriculomegaly. SWI (A) shows the radially oriented medullary veins in the midbrain and an associated microbleed in the left anterior thalamus (arrowhead). T2-SPACE (B) and gado- CMMRD, and thisisfurther support for linium-enhanced T1-weighted (C) images depict the location of a large collector vein obstructing agenetic basis for DVAs. In CVMS, fa- the entrance into the cerebral aqueduct. Images courtesy of Dr Arjuna Somasundaram and Dr cial venous malformations have a 20%– Christian Schwindack. 28% association with DVAs, and most of the DVAs are ipsilateral and in the same metamere as the superficial venous mal- 36,37 formation (Fig 11). The association between DVAs and head and neck ve- nous malformations may share a com- mon developmental pathogenesis. CONCLUSIONS Symptomatic DVAs can lead to a diverse array of clinical diseases, which can be categorized on the basis of their patho- physiologic mechanism. Neuroimaging FIG 11. CVMS in a patient with a left orbital venous malformation depicted on the coronal T2- plays a fundamental role in characteriz- weighted fat saturated (A) and coronal post-gadolinium-enhanced T1-weighted fat saturated (B) images, which show an inﬁltrative T2-weighted hyperintense intraconal lesion with avid contrast ing the angioarchitecture of the DVA enhancement (asterisk). Coronal gadolinium-enhanced T1-weighted image (C) reveals a large left and assessment of the parenchyma sur- basal ganglia DVA (arrow) with the collector vein draining in the left superior petrosal sinus. rounding the DVA, using conventional, advanced, or functional imaging techni- (Fig 10). Depending on the degree of obstruction and resultant ques. An accurate depiction of the pathophysiologic mechanism responsible for symptomatic DVAs are crucial for management hydrocephalus, there may be a need for CSF shunting or an endo- and prognosis. scopic ventriculostomy CSF diversion procedure as a treatment. ACKNOWLEDGMENTS Syndromic Association Dr Krings acknowledges the generous support from the Patricia Most DVAs have sporadic and isolated findings; however, DVAs Holt-Hornsby and Dan Andreae Vascular Research Unit and can be part of a syndromic feature in patients with mutations in UMIT (University Medical Imaging Toronto). either shared RAS-MAPK and PI3K/AKT/mTOR intracellular sig- naling pathways, which are drivers of the phenotypic development Disclosure forms provided by the authors are available with the full text and of vascular malformations and tumors. Most notably, syndromes PDF of this article at www.ajnr.org. associated with DVAs include blue rubber bleb nevus syndrome (BRBNS), constitutional mismatch repair deficiency syndrome REFERENCES (CMMRD), and the more recently described cerebrofacial venous 1. Hon JM, Bhattacharya JJ, Counsell CE, et al. The presentation and metameric syndrome (CVMS). 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American Journal of Neuroradiology – American Journal of Neuroradiology
Published: May 1, 2023
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