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| ORIGINAL ARTICLE |
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| Year : 2012 | Volume
: 60
| Issue : 2 | Page : 154-159 |
Risk factors, clinical profile, and long-term outcome of 428 patients of cerebral sinus venous thrombosis: Insights from Nizam's Institute Venous Stroke Registry, Hyderabad (India)
Deekshanti Narayan1, Subhash Kaul1, K Ravishankar2, T Suryaprabha1, V. C. S. Srinivasarao Bandaru3, K Rukmini Mridula1, SA Jabeen1, Suvarna Alladi1, AK Meena1, Rupam Borgohain1
1 Department of Neurology, Nizam's Institute of Medical Sciences, Panjagutta, Hyderabad, India
2 Department of Neurology, City Neurocenter, Vijayawada, India
3 Department of Clinical Research, Yashoda Superspeciality Hospital, Hyderabad, India
| Date of Submission | 11-Dec-2011 |
| Date of Decision | 03-Jan-2012 |
| Date of Acceptance | 04-Mar-2012 |
| Date of Web Publication | 19-May-2012 |
Correspondence Address:
Subhash Kaul
Department of Neurology, Nizam's Institute of Medical Sciences, Panjagutta, Hyderabad 500082
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0028-3886.96388
Background: With the widespread use of neuroimaging and hematological workup, many of the previously held concepts about cerebral sinus venous thrombosis (CSVT) are changing. Objective: The objective of this study was to investigate the risk factors, clinical profile, and outcome of the fully investigated cases of CSVT from a major university referral hospital in South India. Materials and Methods: Consecutive patients of CSVT confirmed by definite neuroimaging criteria and fully investigated for prothrombotic states, between June 2002 and September 2010, were prospectively studied in the Venous Stroke Registry of Nizam's Institute of Medical Sciences, Hyderabad, South India. Results: Of the 428 patients, 230 (53.7%) were men and the mean age was 31.3 years (range 8-65 years). Seizures were noted in 126 (29.4%) patients, stroke like presentation was found in 122 (28.5%) patients, and benign intracranial hypertension like presentation was found in 78 (18.2%) patients. Common risk factors were anemia in 79 (18.4%), hyperhomocysteinemia in 78 (18.2%), alcoholism in 67 (15.6%), oral contraceptive pill intake in 49 (11.4%), postpartum state in 42 (9.8%), anticardiolipin antibodies in 31 (7.2%), and protein S deficiency in 53 (12.3%) patients. Good outcome at 90 days (modified Rankin Scale £ 2) was observed in 273 (71.2%) of 383 patients available for follow-up. In-house mortality was noted in 33 (7.7%) and recurrence in 22 (5.1%) patients. Conclusions: Compared to the previous studies, prevalence of CSVT was higher in men. Anemia, hyperhomocysteinemia, alcoholism, oral contraceptive use, and postpartum state were the most common risk factors. Overall prognosis was good, but a small percentage of patients died or showed recurrence.
Keywords: Cerebral sinus venous thrombosis, India, outcome, risk factors
How to cite this article:
Narayan D, Kaul S, Ravishankar K, Suryaprabha T, Bandaru VS, Mridula K R, Jabeen S A, Alladi S, Meena A K, Borgohain R. Risk factors, clinical profile, and long-term outcome of 428 patients of cerebral sinus venous thrombosis: Insights from Nizam's Institute Venous Stroke Registry, Hyderabad (India). Neurol India 2012;60:154-9 |
How to cite this URL:
Narayan D, Kaul S, Ravishankar K, Suryaprabha T, Bandaru VS, Mridula K R, Jabeen S A, Alladi S, Meena A K, Borgohain R. Risk factors, clinical profile, and long-term outcome of 428 patients of cerebral sinus venous thrombosis: Insights from Nizam's Institute Venous Stroke Registry, Hyderabad (India). Neurol India [serial online] 2012 [cited 2023 Jun 9];60:154-9. Available from: https://www.neurologyindia.com/text.asp?2012/60/2/154/96388 |
| » Introduction | |  |
Cerebral sinus venous thrombosis (CSVT) is a common cause of stroke in India. With the widespread use of magnetic resonance imaging (MRI), many more cases of CSVT are being diagnosed than before. It is important to be aware of the varied clinical presentation and course of CSVT, as most of these patients have an excellent outcome if treated early and appropriately. Previous studies from India on CSVT were done before the widespread availability of MRI and procoagulant workup. [1],[2],[3] The aim of the present study was to investigate the risk factors, clinical presentation, course, the response to treatment, and follow-up in patients of CSVT in a prospective manner. This is probably the largest single centre series on this subject to date from the Indian subcontinent.
| » Materials and Methods | | |
This study was conducted on the patients diagnosed as CSVT between June 2002 and September 2010 in the Department of Neurology, Nizam's Institute of Medical Sciences, Hyderabad, South India. Patients from all the strata of society were either referred or came by themselves to this hospital. The disease pattern seen in this major university hospital is representative of Andhra Pradesh, a province in South India. All the patients suspected to have CSVT were subjected to thorough clinical evaluation by neurologists. The clinical diagnosis was confirmed by at least one of the following radiological investigations: brain computer tomography (CT) scan, brain MRI (1.5 T) scan [T1-, T2-weighted axials, T1-weighted sagittal sequences, and MR Venography (MRV)] and digital subtraction angiography (DSA) done on Universal Angiogram System (Axiom Artis FA; Platinum Siemens Medical System, Erlangan, Germany). In some cases, more than one radiological investigation was done. The diagnosis of CSVT was based on appropriate clinical setting supported by radiological evidence in the form of partial or complete absence of filling of one or more dural sinuses or thrombosis of cortical veins. All the confirmed cases of CSVT were investigated with complete blood count, erythrocyte sedimentation rate (ESR), blood urea, sugars, serum creatinine, Human Immunodeficiency Virus (HIV), collagen profile like antinuclear antibody (ANA), antiphospholipid antibodies, prothrombin time, activated partial thromboplastin time, procoagulant states like protein C, protein S, antithrombin III (AT III), and serum homocysteine, with an aim to detect the underlying etiology. Hyperhomocysteinemia was defined as serum homocysteine >15 mg/100 ml in those below 60 years, [4] and >20 mg/100 ml in those above 60 years. [5] Anemia was defined as hemoglobin level <13 g/dl in males and <12 g/dl in females. [6]
Patients were treated with adjusted dose intravenous unfractionated heparin with an approximate dose of 1000 units/h, with the target activated partial thromboplastin time (APTT) of 2-2.5 times the control, or subcutaneous low molecular weight heparin (LMWH) in approximate dose of 0.1 mg/10 kg body weight for a duration of 10 days, intrasinus urokinase, or decompression craniotomy, as per the judgment of the attending doctor. All patients were treated with oral anticoagulation therapy with a target International Normalized Ratio (INR) of 2-3 for a period of 6 months after which it was continued indefinitely in patients with persistent hypercoagulable states. Detailed information about the patients was recorded which included: demographic data, type and duration of symptoms, time since the onset of symptoms elapsed at presentation: acute (<48 h), subacute (48 h to <30 days), and chronic (>30 days), Glasgow Coma Scale (GCS) score at admission, imaging modalities used, location and size of parenchymal lesions, location of thrombus, blood investigations, treatment given, and the response to treatment. Follow-up visits were performed at 6, 9, 12 months, and every 6 months thereafter by direct interview. For all patients, the condition recorded at the time of last follow-up was taken as the final follow-up. The data recorded during follow-up were disability according to modified Rankin Scale (mRS), death, recurrent symptomatic sinus thrombosis, seizures, severe visual loss, and the ongoing treatment. Outcome was assessed using mRS comprising complete recovery (mRS 0-1), partial recovery but independent (mRS = 2), dependent (mRS 3-5), and death (mRS 6).
Statistical analysis
Statistical analysis was performed using Statistical Package for Social Sciences (SPSS) 16.0 window software (SPSS Inc Chicago, Illinois (IL) 60606 USA). Continuous variables were presented in titer of mean and ± SD. Categorical variables were expressed as proportions and chi square test was used to study the association in proportions. We estimated odds ratio (OR) and the resulting 95% CI for the matched good and poor outcome pairs. Multiple logistic regression was performed before and after adjustment for potential confounders. All tests were two sided and P value equal to or less than 0.05 was considered statistically significant.
| » Results | | |
A total of 428 patients (men 230, women 198; 1.17:1) were included in this study. The age range was 8-65 years (mean 31.3 years). Mean duration of symptoms before admission was 16.1 days. Presentation was acute in 61 (14.2%), subacute in 312 (72.8%), and chronic in 53 (12.3%) patients. Headache, vomiting, and seizures were the most common clinical features found in 378 (88.3%), 298 (69.6%), and 171 (39.9%) patients, respectively [Table 1].
In terms of clinical syndromes, stroke like presentation was observed in 122 (28.5%), presentation as isolated seizures in 126 (29.4%), benign intracranial hypertension (BIH) like presentation in 78 (18.2%), presentation as encephalopathy in 108 (25.2%), and presentation as psychosis was observed in 8 (1.8%) patients. Normal neurological examination was found in 31 (7.2%) patients. Common risk factors identified were anemia in 79 (18.4%), hyperhomocysteinemia in 78 (18.2%), alcoholism in 67 (15.6%), oral contraceptive pill (OCP) intake in 49 (11.4%), postpartum state in 42 (9.8%), anticardiolipin antibodies in 31 (7.2%), and protein S deficiency in 53 (12.3%) patients. Multiple risk factors (two or more) were seen in 78 (18.2%) patients. No risk factor could be identified in 69 (16.1%) patients [Table 2].
CT scan brain was done in 293 patients and the findings included: hemorrhagic infarction in 172 (58.7%), empty delta sign in 56 (19.1%), and cord sign in 9 (3%) patients [Table 3]. MRI was done in 392 patients and CSVT diagnosis was made by hemorrhagic infarct in 179 (45.6%), hyperdense sinuses in 145 (36.9%), empty delta sign in 80 (20.4%), and cord sign in 13 (3.3%) patients. In MRV done in 412 patients, superficial venous system was involved in 403 (97.8%) and deep venous system in 24 (5.8%) patients [Figure 1]a, b, [Figure 2]a, b and [Figure 3]a, b. | Figure 1: CT Brain showing hyperdense superior sagittal sinus with bilateral haemorrhagic infarcts in high parietal regions
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 | Figure 2: T1 weighted MRI brain sagittal image showing thrombus in superior saggital sinus
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 | Figure 3: (a-b) MRV phase contrast showing left transverse and superior sagittal sinus thrombosis
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Three hundred and ninety-six (92.5%) patients received unfractionated heparin for 7 days overlapping with oral anticoagulants for 3 days which was continued for a minimum period of 6 months. LMWH was given in 41 (9.5%) of our patients, who had massive hemorrhagic infarcts with midline shift. Six patients (1.4%) not showing a satisfactory response to unfractionated heparin were administered intrasinus urokinase under catheter guidance via the transfemoral route. Decompression craniotomy was done in 16 (3.7%) patients who had midline shift and mass effect.
Information on outcome at discharge was available for all patients. Mean hospital stay was 16.1 days. In-hospital mortality was noted in 33 (7.7%) patients. Death in all cases was caused by raised intracranial pressure leading to cerebral herniation in the acute phase and also due to underlying complications like septicemia. At 90 days information on 416/428 patients (97%)was available. Two hundred and twenty-six (52.8%) patients became normal (mRS: 0-1), 47 (10.9%) patients became functionally independent (mRS = 2), and 110 (25.7%) remained dependent (mRS ³3-5) at the end of 3 months [Table 4]. | Table 4: Difference between good outcome and poor outcome with various risk factors at 90 days
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The independent predictors of poor outcome were fever (OR: 10.3, 95% CI: 2.3-38.9), deep venous thrombosis (OR: 9.9, 95% CI: 3.5-40.8), seizures (OR: 6.9, 95% CI: 3.8-12.4), focal neurological deficit (OR: 6.1, 95% CI: 3.2-11.6), and unconsciousness (OR: 3.4, 95% CI: 1.8-8.4) [Table 5].
Follow-up ranging from 6 months to 5 years was available for 258 patients (60.2%), with a mean follow-up of 33 months. Chronic headache was the most common complication on follow-up seen in 18 (4.2%) patients. Other complications were recurrent seizures in 6 (1.1%), chronic intracranial hypertension in 4 (0.9%), deep venous thrombosis in lower limbs in 4 (0.9%), pulmonary thromboembolism in 2 (0.4%), and arterial thrombosis in 3 (0.7%) patients.
Recurrence of CSVT was seen in 22 patients (5.1%). All the recurrences occurred after 6 months and occurred up to 4.5 years after the initial episode. Risk factors for recurrence were persistent alcohol intake in 3 (13.6%), persistent OCP usage in 5 (2.7%), anemia in 3 (13.6%), hyperhomocysteinemia in 7 (31.8%), retroviral disease in 2 (9%), protein C deficiency in 1 (4.5%), abortion in 1 (4.5%), pregnancy in 1 (4.5%) and unknown in 4 (18.1%) patients. After adjustment of variables by multiple regression analysis, hyperhomocysteinemia (OR: 3.7, 95% CI: 1.5-9.0) and OCP usage (OR: 2.6, 95% CI: 1.0-7.0) were found to be independent risk factors for recurrence. The sinuses involved in the recurrent CSVT cases were Superior sagittal sinous (SSS) in 15/22 (68%), Straight Sinus (SS) in 7/22 (33%), and multiple sinuses in 14/22 (66%).
| » Discussion | | |
Previous studies from India have shown CSVT to be highly prevalent and generally associated with postpartum state. [7],[8],[9],[10] Most of these studies were done before the widespread use of modern neuroimaging [1],[2],[3],[7],[10] and had limitations of having small numbers and incomplete investigations. [1],[3],[7],[8],[9],[10] The largest international multicentric trial of CSVT in 2004 included very few patients from Asia and Africa. [11] With the greater availability of MRI, CSVT is being increasingly diagnosed in both genders and at an early stage in India. Many new risk factors are being identified due to more complete workup. Due to the large sample size, uniform risk factor workup, and regular follow-up, the observations from the present study are most up-to-date and valid. In the present study, CSVT was found more frequently in men. Previous studies found 60-79% of CSVT patients to be women [7],[10],[12] and reported it as the commonest cause of stroke in young women in India. [13] The main reason for this was believed to be high prevalence of postpartum hypercoagulable state, precipitated by dehydration and consumption of high fat food in the developing countries during peripartum period. [12] The high frequency of CSVT in men in this study is probably due to rising consumption of alcohol by men, improvement in obstetric care, and higher level of clinical suspicion and detection of CSVT at an early stage.
The mean age in the present study was 31.3 years. However, it is not uncommon in children. Pediatric population constituted 9.4% of the study population, and the most common risk factor was anemia and infections like otitis media. Other studies showed various risk factors like infection, dehydration, renal failure, trauma, cancer, and hematological disorders, alone or in combination. [14],[15],[16],[17] Main clinical features in children in this study were headache and seizures. Other studies have shown that toddlers frequently present with seizures and focal signs, whereas older children present with headache and altered sensorium. [14] The elderly (>60 years) constituted only five patients (1.2%) among whom two were alcoholics and others had no identifiable risk factors. Most common presenting features in the present study were headache, vomiting, and seizures, as was shown in the previous studies. [11],[18],[19],[20] Papilledema was the most frequent sign. Like the previous studies, we encountered four distinct clinical syndromes, i.e. stroke like presentation, encephalopathy, seizures, and BIH like presentation. We did not encounter any case of puerperal psychosis as described in previous studies, probably due to better postpartum care. Non-puerperal psychiatric manifestations were seen in 8 (1.9%) patients out of whom 3 (0.7%) were using OCP and 5 (1.2%) consumed alcohol. Alcoholism and hyperhomocysteinemia were the main risk factors in men. Alcohol contributes to thrombosis by dehydration, hypercoagulability, and reactive thrombocytosis. [21] Overall, 42 (9.8%) patients were postpartum, which was equal to that reported in most western studies [22],[23] and less than 31-86% as reported from a few Asian studies. [24],[25] Less cases of postpartum CSVT in this study probably represent better women healthcare. While postpartum state, anemia, and OCP use were the most common risk factors in women, newly identified risk factors like protein C, protein S, AT III, and antiphospolipid antibodies (APLA) were also detected more frequently in them than in men. These abnormalities were also detected in some women of postpartum and OCP induced CSVT. It is possible that the presence of these procoagulant states triggers the thrombotic state during such exposure due to their additive effects. Rare etiologies in the present study included acute lymphoid leukemia on l-asparginase therapy, [26] drug-induced protein S deficiency, HIV infection, nephrotic syndrome, Coombs positive hemolytic anemia, carcinoma tongue, and chicken pox. Multiple risk factors were seen in 72 (17.9%) patients. Both arterial and venous thrombosis was seen in six patients, the etiology of which was anti-cardiolipin antibodies syndrome in one patient and the etiology of rest of the cases was unknown. Presence of empty delta sign and cord sign on CT scan brain suggests the diagnosis of CSVT, but these were found only in 56 (11.2%) and 9 (3%) patients, respectively. MRI was found to be better than CT in identification of these findings. As reported by others, we found MRV to be the most effective noninvasive technique to confirm the diagnosis. [27] However, DSA was required for 20 (4.9%) patients to confirm the diagnosis in this study and remains the gold standard for establishing the diagnosis of CSVT. [28] Superior sagittal sinus was the most frequent sinus involved. However, other sinuses can also be involved alone or in combination. Most of the patients were treated with unfractionated heparin. Six patients (1.4%) who did not respond to heparin were treated with intrasinus urokinase, as has been done elsewhere. [29] Successful recanalization with improvement of symptoms was achieved in all cases except one who subsequently died. Decompressive craniotomy was done in 15 (4%) patients of whom 2 patients expired while others had good outcome. Others have had a similar experience. [30] The predictors of good outcome were high GCS at presentation and superficial venous system involvement. Poor outcome was seen in patients with fever, low GCS at presentation, deep venous system involvement, and focal deficits. Association of CSVT and deep venous thrombosis in lower limbs was seen in 14 (3.4%) patients. The etiology of these patients was hyperhomocysteinemia in four, puerperium in two, protein C deficiency in one, malignancy in one, and unknown in six patients.
In majority of the patients, outcome was good and the patients were functionally independent (73.8%) at 3 months in contrast to arterial stroke where more patients remain dependent and bed bound. However, despite a good outcome, we did have an in-house mortality rate of 7.7%. Death was mainly caused by raised intracranial pressure leading to cerebral herniation in the acute phase, along with complications like septicemia.
Recurrence of CSVT was noted in 22 (5.4%) patients after being asymptomatic for a period of at least 6 months and occurred as late as 4.5 years after the initial event. This emphasizes the need for regular and prolonged follow-up in the patients of CSVT.
| » Conclusion | | |
CSVT is an important and treatable cause of stroke affecting both the genders almost equally. Headache associated with raised intracranial pressure and seizures are the common presenting features. Risk factors like anemia, hyperhomocysteinemia, OCP use, alcoholism, and procoagulant state are being increasingly identified, while conventional risk factors like postpartum state are decreasing.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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