Cerebral vein thrombosis
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1 Intern Emerg Med (2010) 5:27 32 DOI /s IM - REVIEW Cerebral vein thrombosis Francesco Dentali Walter Ageno Received: 24 March 2009 / Accepted: 3 October 2009 / Published online: 1 December 2009 Ó SIMI 2009 Abstract Advances in neuroimaging have modified our knowledge on cerebral vein thrombosis (CVT). This disease is now diagnosed more frequently, and increasing evidence as to what are the most common risk factors and on the natural history of the disease is becoming available. Most patients with CVT have a benign prognosis: only a minority of patients die during the acute phase or in the following months. Most patients surviving CVT recover completely, or have only mild functional or cognitive deficits. Unfractionated or low-molecular weight heparin is widely used as a first-line therapy of CVT, despite the absence of conclusive evidence about the safety and efficacy in this setting. Vitamin K antagonists are usually prescribed for secondary prevention, but the optimal duration of treatment remains unknown. Because most patients with CVT have partial or complete recanalization of the vessels within the first few months after the index event, and because recurrences of CVT after a first episode appear to be uncommon, routine use of long-term therapy or event life-long secondary prevention seem to be unnecessary. Keywords Cerebral vein thrombosis F. Dentali W. Ageno Department of Clinical Medicine, Research Center on Thromboembolic Disorders and Antithrombotic Therapies, University of Insubria, Varese, Italy W. Ageno (&) U.O. Medicina I, Ospedale di Circolo, Viale Borri 57, Varese, Italy agewal@yahoo.com Introduction Cerebral venous thrombosis (CVT) has long been considered a rare type of cerebrovascular disease with an estimated annual incidence of five to seven cases per million/children and three to four cases per million/adults accounting for 05% of all strokes [1]. Until a few years ago, systemic or local infections commonly affecting the superior sagittal sinus were identified as the most common causes of CVT [2, 3]. The CVT was frequently diagnosed only at autopsy, usually showing concomitant haemorrhagic lesions, which suggested a potential contraindication to the use of heparin [4]. The recent introduction of non-invasive and highly sensitive diagnostic techniques such as magnetic resonance imaging (MRI), magnetic resonance angiography, and computed tomography (CT) angiography has changed our knowledge of CVT. Thanks to the diffusion of these noninvasive techniques, in the last few years, CVT has been diagnosed more frequently, and less clinically severe cases of CVT have been detected. Despite substantial improvements, the diagnosis of CVT often remains overlooked because of the remarkable variability of clinical presentations and neuroimaging signs. Furthermore, existing studies on CVT patients are often limited by small numbers, their retrospective nature and shortterm follow-up periods. Thus, CVT remains a diagnostic and therapeutic challenge, and scant information still exists on the natural history and long-term prognosis of this disease. The purpose of this review is therefore to summarize recent insights into the pathogenesis, risk factors, and clinical and radiologic diagnosis of CVT, and to discuss the current evidence and controversies about best treatment strategies in these patients.
2 28 Intern Emerg Med (2010) 5:27 32 Aetiology Several conditions can cause, or predispose patients to CVT. Among others, these include genetic and acquired prothrombotic disorders, cancer, haematological diseases, vasculitis, and other inflammatory systemic disorders, pregnancy and puerperium, infections, surgery, presence of jugular vein catheters, use of oral contraceptives (OC) and of hormonal replacement therapy as well as several local causes such as brain tumours, arteriovenous malformations, head trauma, CNS infections, and infections of the ear, sinus, mouth, face, or neck [5]. Because the prevalence of CVT is highest in women in the third decade of age [5], a number of small case control studies have explored the possibility that thrombophilic abnormalities and the use of OC are among the leading causes of CVT. In a recent systematic review of the literature and meta-analysis, we compared the prevalence of OC use and the prevalence of the most common thrombophilic abnormalities in patients with CVT and in healthy controls [6]. The use of OC is significantly associated with the risk of CVT [OR 5.59; 95% confidence interval (CI) ]. Similarly, the presence of factor V Leiden mutation (OR 3.38; 95% CI ), mutation G20210A of prothrombin (OR 9.27; 95% CI ), and hyperhomocysteinemia (OR 4.07; 95% CI ) are also significantly associated with an increased risk of CVT. Other studies have assessed the role of new genetic risk factors with contrasting results [7, 8]. In the International Sinus Cerebral Vein Thrombosis (ISCVT) trial [5], a collaborative study that enrolled more than 600 patients with CVT providing the largest available cohort of patients with this disease in the literature, the most common causes are thrombophilia, OC, pregnancy, and puerperium, infections, and cancer. Most of all, this study shows that CVT is a multifactorial disease, since as many as 44% of the patients have more than one identified cause or predisposing factor. Two recent case control studies [9, 10] have compared the prevalence of major risk factors in patients with CVT, and in patients with deep vein thrombosis (DVT) of the lower limbs or pulmonary embolism (PE). In both studies, DVT and PE are more frequently defined as idiopathic, whereas the use of OC is more commonly associated with CVT. However, these results are influenced by the younger age and by the higher prevalence of females in the group of CVT patients, and no significant differences are observed when groups of comparable age are considered. Clinical manifestations Cerebral vein thrombosis presents a remarkably wide spectrum of signs and modes of onset, thus potentially mimicking numerous other disorders. Clinical presentations include headache, seizures, focal neurological deficits, altered consciousness, and papilloedema, which can present in isolation or in association with other symptoms. Clinical presentation in the two largest series of CVT patients is presented in Table 1 [5, 11]. The most frequent, but least specific clinical presentation of CVT is headache, which is present in 75 90% of adult patients [5, 11]. It usually increases gradually over a couple of days, but can also start rapidly, mimicking a subarachnoid haemorrhage [12]. According to the grouping of symptoms and signs, four main patterns have been identified: isolated intracranial hypertension, focal syndrome, cavernous sinus syndrome, and subacute encephalopathy [13]. Patients with a chronic course or a delayed clinical presentation may show papilloedema on funduscopy, but this finding is less common in acute cases [14]. Isolated thrombosis of the different sinuses and veins results in diverse clinical pictures. When the deep cerebral venous system is occluded, the clinical picture is usually more severe with coma, mental Table 1 Clinical presentation in the two largest series of CVT patients Ferro et al.: 624 patients Headache 88.8% Visual loss 13.2% Papilledema 28.3% Diplopia 13.5% Stupor or coma 13.9% Aphasia 19.1% Mental status disorders 22% Any paresis 37.2% Any seizure 39.3% Sensory symptoms 5.4% Other focal cortical sign 3.4% Wasay et al.: 182 patients Headache 71% Generalized weakness 54% Focal motor or sensory deficit 36% Nausea/vomiting 35% Seizures 32% Walking difficulty 30% Drowsiness 28% Visual blurring 23% Dizziness 21% Behavioural symptoms 18% Slurred speech/inability to speak 16% Coma 15% Fever 14%
3 Intern Emerg Med (2010) 5: troubles, and bilateral motor deficits [15]. More limited thrombosis of the deep venous system can cause relatively mild symptoms [15]. In patients with parenchymal lesions, the clinical picture is also more severe. Focal or generalized seizures are more common than in other stroke types. Seizures are more typical in patients with parenchymal lesions, sagittal sinus, and cortical vein thrombosis, and motor or sensory defects [16]. Diagnosis Although the clinical presentation is highly variable, and may thus be misleading, CVT should be suspected in young and middle-aged patients with recent unusual headache or with stroke-like symptoms in the absence of the usual vascular risk factors. Possible clues to the presence of CVT are more specific risk factors in patients with intracranial hypertension, and in patients with CT evidence of haemorrhagic infarcts, especially if multiple and not confined to the arterial vascular territories. There are currently no pre-test clinical probability scores that have been validated to assist clinicians in the diagnostic approach to CVT. The use of D-dimer has been explored in small studies, but the results are non-conclusive [17, 18]. A CT scan is commonly performed as the first-line diagnostic test. In most cases, the CT scan shows indirect signs such as cerebral oedema, ischaemic or haemorrhagic lesions, or signs of venous stasis. Direct signs such as delta or cord sign can be detected in approximately one-third of CT scans, whereas as many as 30% of scans are negative [2, 19]. CT venography is a promising new technique for creating images of the cerebral venous system [20]. Magnetic resonance is now widely used when a CVT is suspected. The consequences of venous thrombosis on brain parenchyma are highly variable. With T1- and T2- weighted images, a localized or diffuse brain swelling with normal or abnormal signals suggestive of oedema, infarction, or haemorrhage is frequently observed [13]. However, magnetic resonance may be normal in up to 30% of cases. Cytotoxic or vasogenic oedema may be visible using diffusion-weighted images, although, given the wide spectrum of parenchymal changes, various patterns have been reported with this technique. Interestingly, the overall diffusion-weighted imaging and apparent diffusion coefficient pattern is different from that of arterial infarcts, and is mostly suggestive of vasogenic oedema and far less commonly of cytotoxic oedema [21, 22]. The most sensitive examination technique is MRI to visualize the thrombosed vessel in combination with MRV to detect the non-visualization of the same vessel [23, 24]. MRI alone is limited by flow artefacts that can lead to false positives and the absence of hyperintense signal on T1- and T2-weighted images at the onset of acute thrombosis. The diagnostic yield of MRV alone is limited by the fact that, as with all other angiographic techniques, it does not differentiate between thrombosis and hypoplasia, which is extremely frequent in lateral sinuses [19, 25]. Some studies have highlighted the value of echoplanar susceptibility-weighted images (T2*), which, in contrast to T1 and T2, show the thrombosis as a hypointense signal associated with the magnetic susceptibility effect, similar to that reported for intracerebral haemorrhages [26 28]. The diagnostic yield of the combination of MRI (T1, T2, FLAIR and T2*) and MRV is such that conventional angiography is nowadays very rarely required. Treatment of CVT Most patients with objectively diagnosed CVT are treated with anticoagulant drugs. The efficacy of heparin has been evaluated only in two randomized controlled trials with adequate diagnostic imaging tests [29, 30]. In the first study, Einhaupl et al. [29] compared intravenous UFH with placebo. This study was prematurely stopped after the enrollment of 20 patients since an interim analysis showed a significant benefit of heparin. At 3 months, eight of the heparin-treated patients had a complete clinical recovery and two had slight residual neurological deficits. In the placebo group, only one patient had a complete recovery, six patients had neurological deficits, and three patients died (P \ 0.01). A further analysis of this trial, however, did not confirm these results. de Bruijn and Stam [30] compared therapeutic doses of nadroparin with placebo in 60 patients with CVT. This study shows a non-significant benefit of the LMWH: after 3 weeks, 20% of patients in the nadroparin group and 24% in the placebo group have a poor outcome (risk reduction -4%; 95% CI, -25, 17%). A meta-analysis of these studies confirms these results showing a non-significant reduction in the relative risk of death or dependency [31]. In the ISCVT trial the overall use of heparin does not appear to be associated with a better outcome. The authors report a non-statistically significant trend towards a reduction in the rates of adverse events in patients who receive full therapeutic doses of heparin during the acute phase (66/520 vs. 19/104; hazard ratio 0.73; 95% CI, ). However, the design of the study does not allow any meaningful conclusion on the efficacy of treatments. A major concern with the use of anticoagulant drugs in the acute phase of CVT is caused by the frequent detection of haemorrhagic lesions at diagnosis. Because haemorrhagic lesions are secondary to venous stasis provoked by the thrombus, and because there is no evidence to suggest
4 30 Intern Emerg Med (2010) 5:27 32 that the use of anticoagulants worsens haemorrhagic lesions and patients prognosis, it is commonly recommended that CVT patients be treated with anticoagulants regardless of the presence of haemorrhagic lesions [32]. Treatment of CVT with thrombolytics has been reported in cases with a deteriorating clinical course despite anticoagulant therapy. However, the authors of a Cochrane systematic review could not find any randomized controlled trial that evaluates the efficacy of thrombolysis in acute CVT [33]. In a prospective trial, Wasay et al. [34] analysed 40 consecutive patients with superior sagittal sinus thrombosis treated with local urokinase or UFH. In this study, local thrombolysis with urokinase is well tolerated, and only two patients (10%) had a major bleeding complication. In a more recent prospective series, 20 CVT patients with an altered mental status, coma, straight sinus thrombosis, or large space-occupying lesions were treated with endovascular thrombolysis [35]. In this group of patients considered to have a poor prognosis, thrombolysis is generally effective. However, some patients may deteriorate because of increased cerebral haemorrhage, and patients with large infarcts and impending herniation do not appear to have a benefit. Thus, until better evidence is available, endovascular thrombolysis should be restricted only to patients with a very poor prognosis. Vitamin K antagonists (VKA) remain the drugs of choice for the long term, secondary prevention of CVT, and VKA are usually started in the first days after the acute event. The American College of Chest Physician Guidelines recommend the use of VKA for up to 12 months [36] and other recent guidelines suggest continuation of anticoagulation for a period variable from 3 to 12 months [32, 37, 38]. Unfortunately, there are no trials comparing different durations of oral anticoagulant treatment following CVT. Extending secondary prevention beyond a period of 6 12 months should be considered in the presence of permanent risk factors for CVT. In the absence of permanent risk factors, available data show low recurrence rates and high recanalization rates (see following paragraph), suggesting that more prolonged treatment may be unnecessary. Finally, prophylaxis with antiepileptic drugs is suggested for CVT patients with supratentorial lesions presenting with seizures [39]. Clinical history Information on mortality and residual disability following CVT is based on the results of a limited number of studies [5, 40, 41]. In the ISCVT trial [5], patients were followed up for a median of 16 months. Information on the clinical outcome was collected at discharge from the hospital and after follow-up visits that were performed at 6 and 12 months. Twenty-seven patients (4.3%) died during the acute phase. Of note, 11 deaths were caused by an underlying condition. At the end of follow-up, a total of 52 patients (8.3%) had died, whereas 32 patients (5.1%) were moderately or severely impaired. These findings are comparable to the results of the VENOPORT study, in which 142 CVT patients were recruited in 20 Portuguese hospitals [40]. Overall, 11 patients (8%) had died at the end of follow-up, whereas 112 patients (79%) had a complete recovery. In a recently published systematic review of the literature [42], in which we summarized the results of 19 studies on CVT patients, we estimate a 5.6% rate of acute phase mortality (range %) and a mortality at the end of follow-up of 9.4% (range 0 39%). In summary, all these studies confirm that most patients with CVT have a substantially benign prognosis. Mortality rates appear to be low and, interestingly, many patients do not die as a result of their CVT, but as a consequence of an underlying condition such as cancer. Most surviving patients recover completely, or present only mild functional or cognitive deficits; fewer than one in five surviving patients is dependent or has a permanent disability at the end of the follow-up period. Several studies evaluated potential factors associated with a poor outcome after CVT [43 46]. The validity of these findings, however, is often limited by the modest sample size and by the single-centre design or single-country setting of the studies. Some studies find that intracranial haemorrhage at the time of diagnosis of CVT is a predictor of poor outcome [43 45]. This finding should be considered relevant since many CVT patients present with intracerebral haemorrhage at the time of diagnosis. Also, epileptic seizures seem to be associated with an increased risk of poor outcome. Of note, in the ISCVT study, epileptic seizures are significantly more common in patients with intracerebral haemorrhage than in CVT patients without intracerebral haemorrhage (55 vs. 29%; P \ ) [45]. These findings are confirmed by Masuhr et al. [46] in a study of 194 consecutive patients with acute CVT. In this study, mortality is three times higher in patients with epileptic seizures than in patients without (36.4 vs. 12.0%). Furthermore, intracranial haemorrhage, presence of motor deficits and cortical vein thrombosis are independent predictors of early epileptic seizures in this study. In our systematic review [42], other potential predictors of poor outcome include older age, male sex, coma, mental status disorders, deep CVT, right intracranial haemorrhage, posterior fossa lesion, worsening of previous focal or de novo focal deficits, cerebral nervous system infection and cancer. Information on recurrence rates of CVT is ascertained from several studies [5, 40, 41, 43, 47]. The duration of
5 Intern Emerg Med (2010) 5: follow-up, however, varies widely among studies ranging from 12 to 145 months. Only few studies assess the incidence of thromboembolic events occurring in sites other than cerebral veins [5, 41]. In our systematic review of the literature, we find an overall recurrence rate of CVT of 2.8%, while 3.7% of patients have a thromboembolic event in a different venous segment during follow-up [42]. In summary, the rate of recurrent CVT and of other thromboembolic complications after a first episode of CVT is low. There is no adequate information on the risk of recurrence associated with the presence or absence of specific risk factors for CVT, and no information on the risk of recurrence associated with the duration of secondary prophylaxis with oral anticoagulant drugs. Women who develop a CVT during pregnancy or puerperium seem to have a low risk of recurrence during subsequent pregnancies. Spontaneous abortion, however, is a common complication in these patients. Mehraein et al. [48] studied the risk of recurrence in 39 women who had a CVT during childbearing age. During a mean follow-up of 10.2 years, 14 women had 22 pregnancies. Low-dose heparin was given subcutaneously during only five of these pregnancies. No recurrence of CVT occurred during pregnancy or puerperium. There were, however, only 19 births since one pregnancy occurred during oral anticoagulation, and was interrupted, and two pregnancies ended with spontaneous abortions. In the ISCVT study, there were 77 episodes of CVT related to pregnancy or puerperium [5]. In the 34 women who became pregnant after CVT, there was only one recurrent CVT. There were, however, nine abortions (four spontaneous and five voluntary), one lower limb and one pelvic vein thrombosis. Finally, only a few studies with a small sample size and a relatively short follow-up investigate the recanalization of CVT [49, 50]. Results of these studies show that many patients have a partial or complete recanalization at 6 months follow-up, and the rate of recanalization is not different at 1 year [42]. Furthermore, no correlation between recanalization and clinical outcome is found. Conclusion Infections have become less common causes of CVT after the widespread advent of antibiotics, and, in more recent series, other risk factors, such as thrombophilia or the use of OC, are increasingly reported to be associated with CVT. Most patients with CVT appear to have a benign prognosis. Anticoagulant therapy is now largely used as the first-line treatment for most patients, despite the fact that evidence of their safety and efficacy in CVT patients cannot be deemed as conclusive. Intracranial haemorrhage at the time of presentation, and epileptic seizures during the acute phase are associated with an increased risk of death or residual disability. 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