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Incidence and Mortality of Cerebral Venous Thrombosis in a Norwegian Population

Originally publishedhttps://doi.org/10.1161/STROKEAHA.120.030800Stroke. 2020;51:3023–3029

Abstract

Background and Purpose:

There are conflicting figures of the incidence of cerebral venous thrombosis (CVT). The incidence was previously estimated to around 0.5/100 000/y, but more recent studies have suggested 1 to 1.5/100 000/y. The purpose of this study was to explore the incidence and mortality of CVT in a Norwegian population.

Methods:

A retrospective cross-sectional hospital population-based study conducted at Akershus University Hospital serving roughly 10% of the total Norwegian population. Patients were identified through chart reviews based on the relevant International Classification of Diseases(Tenth Revision) codes for new CVT cases in a 7-year period between January 1, 2011, and December 31, 2017. Only inhabitants living in the hospital’s catchment area were included.

Results:

Sixty-two patients aged 0 to 80 years were identified and included. The median age was 46 years and 53% were females. The overall incidence of CVT was 1.75 (95% CI, 1.36–2.23) per 100 000/y with no significant sex differences. The incidence for children and adolescents (<18 years, n=9) was lower than for adults (≥18 years, n=53); 1.08 (0.52–1.97) versus 1.96 (1.49–2.55) per 100 000/y per year, with the highest incidence for those >50 years with 2.10 (1.38–3.07)/100 000/y. Headache was the most prevalent symptom, reported in 83%, followed by nausea, motor deficits, and seizures observed in 45%, 32%, and 32% of the patients. Transverse sinuses and the jugular vein were the most frequent sites of thrombosis. In most patients (61%), thrombosis occurred in multiple sinuses/veins. Risk factors were found in 73% of the patients, and most of the patients had a combination of 2 or more risk factors. The 30-day and 1-year mortality rates were 3% and 6%.

Conclusions:

The incidence of CVT in this population was higher than previously reported. The mortality rate was similar to previous studies.

Introduction

Cerebral venous thrombosis (CVT) is an uncommon form of stroke, which more often affects younger adults and women compared with ischemic and hemorrhagic stroke.1–3

Risk factors of CVT in adults have been suggested to be the same as for venous thromboembolism.3,4 Thus, the most frequent and major risk factors for CVT in adults are hereditary thrombophilia, prothrombotic/hypercoagulability conditions, oral contraceptives, hormonal replacement therapy, pregnancy, puerperium, malignancy, local infections, and head injury.

The incidence was previously estimated to around 0.3 to 0.5/100 000/y, but more recent studies have suggested higher incidences of 1.57 and 1.32 per 100 000 annually.3,5,6 These latter studies combined hospitals incidents with data from the general population. Whether these increased incidence findings are due to methodological differences, more focus on the diagnosis, better access to imaging, or a true increase is not known.

The short-term mortality in CVT has been estimated to 4% to 5%, and a trend with declining mortality among patients with CVT over time has been described.3,7 Most previous studies of CVT are multicenter studies from referral/specialized hospitals with highly selected patient populations.1,8–10 The incidence, clinical presentations, risk factors, and mortality of patients in selected populations compared with more unselected populations from primary hospitals may differ. The purpose of this study was to explore the incidence, mortality, risk factors, and clinical findings in an unselected population diagnosed with CVT in Norway.

Methods

All supporting data are available within the article, and any data related to CVT at our hospital is also available from the corresponding author upon reasonable request.

Study Design, Setting, and Population

This was a retrospective study of all hospital-admitted patients at Akershus University Hospital, the largest primary acute hospital in the Oslo greater metropolitan area, Norway, in the period between January 1, 2011 and December 31, 2017.

Norwegian hospitals are almost exclusively publicly financed. Akershus University Hospital is a public hospital serving both as a primary hospital and a University Hospital. The hospital has the responsibility for most of Akershus county in addition to the eastern part of Oslo, and these catchment areas were included in the present study. The hospital had a catchment area of about 530 000 inhabitants between 2011 and 2017, which is ≈10% of Norway’s total population.

Norway has an all-covering national health insurance, thus, all patients enter the hospital’s emergency ward on the same conditions and with the same threshold for further in-patient admission.

Data from Statistics Norway show that the catchment area is reasonably representative for the total Norwegian population.11,12 All cases in this area with CVT will be in contact with our hospital at the initial admission, as part of the rehabilitation, with a discharge report or death certificate from other hospitals. This makes it possible to estimate accurate population-based incidence figures for CVT.

The data management group at the Research Centre, Akershus University Hospital, searched the hospital’s electronic clinical database to identify patients at all ages with a new CVT diagnosis during a 7-year period between January 1, 2011 and December 31, 2017. All discharge codes and not only the main diagnoses were assessed.

The following International Classification of Diseases, Tenth Revision (ICD-10) codes were searched: G08 Intracranial and intraspinal phlebitis and thrombophlebitis, I636 Cerebral infarction due to cerebral venous thrombosis, nonpyogenic, I676 Nonpyogenic thrombosis of intracranial venous system, O225 Cerebral venous thrombosis in pregnancy, and O873 Cerebral venous thrombosis in the puerperium. All these patients were manually screened (Drs Saxhaug Kristoffersen and Elena Harper).

In addition, all patients with ICD-10 codes of I82 Embolism and thrombosis of unspecified vein or I61 intracerebral hemorrhage from the departments of Neurology, Pediatrics, Geriatrics, General Medicine and Obstetrics were manually screened for potential CVT cases (Dr Saxhaug Kristoffersen). All neuroradiological assessments for the identified CVT cases were reassessed and confirmed by a skilled neuroradiologist (Dr Zarnovicky).

All patients with a new diagnosis of a nontraumatic CVT were included, and the only exclusion criterion was not residing in the hospital’s catchment area. Patients with repeat presentations because of chronic CVT during the study period were counted as one case in the analysis. To avoid too many nonmutually exclusive subgroups patients were not divided into further groups based on underlying or additional pathology. Patients aged 18 and older were defined as adults.

All-cause mortality was calculated at discharge, 30 days, and 1 year. All inhabitants in Norway have a unique 11 digit personal identification number in the National Population Register. The Norwegian Cause of Death Registry collects death certificates for all deaths that occur in the country and link these to the National Population Register. Because all electronic health records in the hospitals are constantly updated from the National Population Register, it is possible to accurately estimate all-cause mortality rates.

Statistics

For descriptive data, absolute numbers, proportions, means, and SDs or 95% CIs are given.

Population figures of the years 2011 to 2017 for the incidence calculations were acquired from Norway Statistics.12 The mean population of the catchment area during these 7 years was 505 000 of whom 76.4% were adults.

Statistical analyses were performed using IBM SPSS Statistics, Version 25.00 (SPSS Inc, Chicago, IL).

Ethics

The Regional Committee for Medical Research Ethics South-East (2017/2446) and the Data Protection Officer at Akershus University Hospital approved the study. In accordance with the approval from the Regional Committee for Medical Research Ethics and the Norwegian law on medical research, the project did not require a written patient consent.

Results

We identified 73 patients with CVT at Akershus University Hospital between 2011 and 2017, of whom 11 were visitors/tourists in the catchment area and thus excluded from the present study. Sixty-two patients were included in the analysis. The patients were on average 43.2 (SD 21.4, range 0–80) years old (median 46) and 53% were women.

In our population of 3 537 288 (person-years 2011–2017), 62 cases give an incidence of 1.75 per 100 000/y (95% CI, 1.36–2.23). The incidence for children and adolescents (<18 years, n=9), 1.08 (95% CI, 0.52–1.97) was lower than for adults (≥18 years, n=53), 1.96 (95% CI, 1.49–2.55) per 100 000/y. The incidence figures for different age groups and sex are given in Table 1. For newborns (<1 year, n=3), the incidence was 7.10 per 100 000/y (95% CI, 2.41–20.8).

Table 1. Incidence of CVT

Age GroupN, Totaln, Womenn, Men
<18 y91.08 (0.52–1.97)40.98 (0.31–2.36)51.17 (0.43–2.59)
≥18 y531.96 (1.49–2.55)292.14 (1.46–3.03)241.79 (1.17–2.62)
18–49 y291.80 (1.22–2.57)182.22 (1.34–3.48)111.39 (0.73–2.42)
≥50 y242.10 (1.38–3.07)111.86 (0.98–3.24)132.35 (1.31–3.92)
50–66 y152.11 (1.23–3.41)51.43 (0.52–3.17)102.78 (1.41–4.95)
≥67 y92.07 (1.01–3.80)62.49 (1.01–5.17)31.55 (0.39–4.23)
Total621.75 (1.36–2.23)331.87 (1.31–2.60)291.64 (1.12–2.32)

Figures are given as cases per 100 000 per year. CVT indicates cerebral venous thrombosis.

Mean time from symptom onset to admission was 11.9 days (median 3, range 0–150), and 47% (n=29) of the patients were admitted within 2 days of symptom debut.

Table 2 shows the demographics, risk factors, clinical, and radiological findings among all patients with CVT. Headache was the most common presenting symptom followed by nausea, paralysis, and seizures. These findings were similar for women, men, children, young adults, and older patients. In total, 61% of the patients had involvement of 2 or more veins/sinuses. The transverse sinus (10%) and the superior sagittal sinus (13%) were the far most common sinuses involved both for children and adults among those with only one vein/sinus involved. Among those with more than one vein/sinus involved, the transverse or sigmoid sinus was affected in almost half of the patients. Forty-five cases were diagnosed based on computed tomographic venography. Parenchymal lesions defined by edema, infarction, and hemorrhage at computed tomography/magnetic resonance imaging were identified in 47%. One out of 4 had a hereditary thrombophilia or a systemic prothrombotic condition. Thirty-two percent of the women at reproductive age (15–49) had recently given birth (puerperium), and no one was pregnant. Only 3 women used oral contraceptives or hormonal replacement therapy. Central nervous system or ear nose throat infections as risk factor were far more common among children (56%) than among adults (15%). One or more risk factors were identified among 78% of the children and adolescents and among 55% of the adults.

Table 2. Demographic, Clinical, and Radiological Data Presented as Total and Percentage

Total, N=620–17 y, N=918 y, N=53
Patient characteristics
 Median age, y (interquartile range)46 (32)7 (15)49 (24)
 Sex, women, n (%)33 (53)4 (44)29 (55)
 History of previous ischemic stroke/transient ischemic attack, n (%)3 (5)0 (0)3 (6)
Clinical presentation, n (%)
 Headache52 (83)6 (67)46 (87)
 Nausea/vomiting28 (45)4 (44)24 (45)
 Motor weakness20 (32)2 (22)18 (34)
 Seizures20 (32)4 (44)16 (30)
 Sensory disturbances17 (27)1 (11)16 (30)
 Speech disturbances16 (26)1 (11)15 (28)
 Visual disturbances16 (26)2 (22)14 (26)
 Cranial nerve palsies15 (24)3 (33)12 (23)
 Cerebellar signs8 (13)1 (11)7 (13)
Radiological findings, n (%)
 Sinus/vein involved
  One sinus involved24 (39)3 (33)21 (40)
   Transverse sinus6 (10)1 (11)5 (10)
   Sigmoid sinus2 (3)1 (11)1 (2)
   Straight (rectus) sinus2 (3)0 (0)2 (4)
   Superior sagittal sinus8 (13)1 (11)7 (13)
   Vena jugularis interna1 (2)0 (0)1 (2)
   Cortical veins5 (8)0 (0)5 (10)
  Two or more sinuses/veins involved37 (61)6 (67)31 (60)
   Transverse sinus26 (43)4 (44)22 (42)
   Sigmoid sinus28 (46)4 (44)24 (46)
   Straight (rectus) sinus9 (15)2 (22)7 (13)
   Superior sagittal sinus13 (21)3 (33)10 (19)
   Vena jugularis interna19 (31)3 (33)16 (31)
   Cortical veins6 (10)1 (11)5 (10)
   Deep venous system4 (7)1 (11)3 (6)
 Parenchymal involvement
  No lesion39 (63)5 (56)34 (64)
  Focal edema/infarction7 (11)1 (11)6 (11)
  Hemorrhage6 (10)1 (11)5 (9)
  Infarction and hemorrhage10 (16)2 (22)8 (15)
Risk factors, n (%)
 History of CVT or venous thromboembolism7 (11)0 (0)7 (13)
 Hereditary thrombophilia9 (15)1 (11)8 (15)
 Systematic/prothrombotic diseases6 (10)1 (11)5 (9)
 Central nervous system/ear nose throat infection13 (21)5 (56)8 (15)
 Malignancy7 (11)1 (11)6 (11)
 Pregnancy0 (0)NA0 (0)
 Puerperium6 (32)NA6 (33)
 Oral contraceptives or hormonal replacement therapy3 (16)1 (100)2 (11)
 Head trauma1 (2)0 (0)1 (2)
 One risk factor24 (39)6 (67)18 (34)
 More than one risk factor12 (19)1 (11)11 (21)
 No risk factor26 (42)2 (22)24 (45)

CVT indicates cerebral venous thrombosis.

All patients were discharged with anticoagulation therapy, 43 with warfarin, 18 with low molecular weight heparin, and one with direct oral anticoagulation.

The all-cause mortality was 3% both at discharge and after 30 days. The long-term mortality (1 year) was 6% for the total sample, however, no children or adolescents died within 1 year after the diagnosis in comparison to 17% of those aged 50 years or older (Table 3).

Table 3. Mortality of CVT at Discharge, 30 Days, and 1 Year

Total, N=620–17 y, N=918 y, N=5350 y, N=24
Discharge, n (%)2 (3)0 (0)2 (4)2 (8)
30 d, n (%)2 (3)0 (0)2 (4)2 (8)
1 y, n (%)4 (6)0 (0)4 (8)4 (17)

CVT indicates cerebral venous thrombosis.

Discussion

In our study population, we found an overall incidence of CVT of 1.75 per 100 000/y. The incidence for adults was 1.96 per 100 000/y, which is much higher than figures previously reported, but we found a similar mortality rate.

The incidence has previously been estimated to be around 0.3 to 0.5 per 100 000/y.3

In a hospital-based study from Portugal, an annual incidence of 0.22/100 000 was reported for the period between 1980 and 1998.13 A study from Hong Kong reported 0.34/100 000/y between 1995 and 1998 and 2 tertiary care clinics in Iran reported 1.23/100 000/y between 2001 and 2004.14,15 More recent studies from Australia and the Netherlands report an annually incidence of 1.57 and 1.32 per 100 000 annually.5,6

Table 4 shows the findings from our study in relation to these previous studies.5,6,13–15

Table 4. Comparison of Different Studies of Incidence and Mortality of CVT5,6,13–15

NorwayAustraliaNetherlandsIranHong KongPortugal
Years2011–20172005–20112008–20102001–20041995–19981980–1998
SettingSingle hospital, only hospital in the region covering 10% of NorwayAll public hospitals in the region of AdelaideAll 19 hospitals in the regions of North-Holland and FlevolandTwo tertiary referral hospitals in the region of IsfahanAll three district hospitals at the Hong Kong island30 centers in Portugal
PopulationPrimary hospitalPrimary hospitalsPrimary hospitalsSelected referral hospitalsPrimary hospitalsSelected centers
Number of CVT cases621059412213142
Age includedAll ages>17 y>17 y>14 y>15 y>14 y
Median age, y46494136 (mean)3035
Proportion women, %535272797772
Incidence per 100 000/y1.751.571.321.230.340.22
Mortality at discharge, %391Not given86

CVT indicates cerebral venous thrombosis.

It is known that the incidence varies with age and probably varies in different parts of the world due to different risk factors, disease spectrums, and health care systems. Our results are probably not comparable to 30-year-old findings from Hong Kong and Portugal, because there has been a shift within medicine towards more focus on imaging-based stroke diagnosis and treatment. Due to the increased availability of prompt treatment for acute stroke, more patients are now referred to hospitals than just 2 to 3 decades ago. Furthermore, the availability, frequency, and quality of imaging/diagnostics have increased over time, also for older patients, and this may at least partly explain some of the increased incidence. However, populations from the Netherlands and Australia are most likely epidemiologically similar to the Norwegian population. The health care system organization is also much the same, but geographic factors, for example, residential patterns and the distance to hospital, could account for some of the difference in incidence. Furthermore, the public health care system and easy access to advanced imaging in Norway may contribute to a lower threshold for imaging in sub-acute headache. It is also important to underline that the study period in our study (2011–2017) was in the subsequent decade compared with the studies from the Netherlands (2008–2010) and Australia (2005–2011). The shift within stroke medicine towards more public awareness and focus on in-hospital treatment may also lead to a lower threshold for seeking medical help and being admitted to hospital even with more diffuse and variable symptoms than in previous decades.

An almost 3 times higher incidence for women is reported in several studies.1,2 The female predominance is found in adults, but not in children or elderly. Thus, the female to male ratio of 3:1 has been suggested to be due to pregnancy, puerperium, oral contraceptives, and hormonal replacement therapy. The median age among adults in the present study was 49 years and 55% were women. This is comparable with the Australian study with a median age of 49 years and 52% women.5 The Dutch study had a slightly younger population (41 years) and a much higher proportion of women (72%).6 In the present study, almost one out of 5 adults were older than 64 years, which is a higher proportion than previously reported in other studies.1,10,16 Whether this finding represents a true increase of CVT among elderly should be investigated in future population-based studies.

We found a very high incidence of CVT with 7.10 per 100 000 newborns compared with previous studies which have reported annual incidences in newborns between 2.60 and 2.69 per 100 000.17,18 The high incidence with a very broad 95% CI found in the present study probably reflects that the sample of newborns was small (<43 000 over 7 years) and does not necessarily represent a huge difference in the incidence for the youngest children. The incidence of CVT (1.08 per 100 000 per year) in our total pediatric population is much more comparable to the previous findings of 0.67 case per 100 000 children per year from the Canadian Pediatric Stroke Registry 1992 to 1997.19

Fifty-eight percent had an identified risk factor. Interestingly, none of the women were pregnant. The Dutch study with its younger women had many more cases under hormonal changes (oral hormones or pregnancy) than the Australian and present study. Whether this is a coincidence or reflects a different or change in treatment traditions of oral contraceptive use is not clear. An identified risk factor was more common among children (78%) than adults (55%). Infections that have been suggested as risk factors for CVT (ie, head, ear, nose, and throat) were far more common among children than adults. Among the adults, 34% had one risk factor and 21% had 2 or more risk factors. These proportions are lower than the suggested 85% in more selected cohorts.1,20 One out of 4 had a hereditary thrombophilia or a systemic prothrombotic condition.21,22

The onset of CVT is highly variable with delays in diagnosis commonly reported.1,23 As in other studies, >8/10 had headache at admission, almost 50% experienced nausea, and 1/3 experienced seizures or motor weakness. Interestingly, in a substantial minority, none of these symptoms were present, underlining the variable clinical presentation of CVT.

All patients started initial anticoagulation therapy in accordance with current guidelines.24

Mortality in the acute phase is estimated to 4% to 5%.3,7 The most common cause of death in the acute phase is transtentorial herniation, while other common causes are status epilepticus and medical complications.3 In the present study, we found a mortality rate of 3% at discharge, increasing with older age. A trend with declining mortality among patients with CVT over time has been described.7 Possible explanations may be the same as commonly discussed for the potential increased incidence, namely shift in risk factors over time, improved diagnostics, increased case assessment, identification of less severe cases, and improved treatment.3,5,6 As in other studies, worse outcome and mortality increased with older age in this Norwegian population.7,18,25

Certain potential limitations should be considered when interpreting the results from our study. The sample size may be regarded as small with 62 cases, but the study extended 7 years and covered >10% of the total Norwegian population. In addition, Norway has an all-covering national health insurance, and the population of our public hospital is reasonably representative for the total Norwegian population. All patients requiring emergency medicine assessment within the catchment area will be admitted directly to our hospital, and all CVT cases will somehow be in contact with our hospital. Thus, selection bias and year-by-year variance are probably of minor importance. We cannot exclude that some cases may have been missed based on wrong ICD-10 code. To minimize this, we manually checked the radiology descriptions and discharge reports for all patients diagnosed with ICD-10 codes of I82 embolism and thrombosis of unspecified vein or I61 intracerebral hemorrhage from relevant departments. It is impossible to ascertain if some people in the general population may have suffered a CVT without symptoms and that the true incidence may be even higher than the figures reported in the literature. However, CVT is not a common incident finding in clinical work, in patients doing MRI for other reasons, or in newer autopsy series, and asymptomatic cases are therefore less likely to affect CVT epidemiology. If any cases were missed with the present methodology, this would give an even higher incidence. The study was retrospective in design, however, we used the original electronic medical reports so selection or reporting bias is unlikely. Furthermore, CVT is relatively uncommon, and a prospective study from unselected primary centers would be highly time- and cost-consuming without necessarily yielding higher data quality. A way to counteract these limitations in the future would be to combine data from well-defined high-quality nationwide health registries with clinical data from hospitals.

In conclusion, the incidence of CVT in Norway is higher than previously reported for adults in other studies. Whether this reflects a genuine increase or simply greater awareness of the condition, as well as better and more accessible diagnostic imaging, is uncertain. However, the incidence among children and the overall mortality are comparable with previous studies. New and larger studies from different countries should combine nationwide population registries and clinical data from hospital charts to confirm these findings.

Nonstandard Abbreviations and Acronyms

CVT

cerebral venous thrombosis

ICD-10

International Classification of Diseases, Tenth Revision

Footnotes

Presented in part at the European Stroke Organisation Conference, Milan, Italy, May 22–24, 2019.

For Sources of Funding and Disclosures, see page 3028.

Correspondence to: Espen Saxhaug Kristoffersen, MD, PhD, Department of General Practice, Institute of Health and Society, University of Oslo, PO Box 1130 Blindern, 0318 Oslo, Norway. Email

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