Incidence and clinical characteristics of spinal arteriovenous shunts: hospital-based surveillance in Okayama, Japan

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  • 1 Department of Neurological Surgery, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama;
  • | 2 Department of Neurosurgery, Kurashiki Central Hospital, Kurashiki;
  • | 3 Department of Epidemiology, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama;
  • | 4 Department of Neurosurgery, Kawasaki Medical School, Kurashiki; and
  • | 5 Department of Neurosurgery, Okayama City Hospital, Okayama City General Medical Center, Okayama, Japan
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OBJECTIVE

There have been no accurate surveillance data regarding the incidence rate of spinal arteriovenous shunts (SAVSs). Here, the authors investigate the epidemiology and clinical characteristics of SAVSs.

METHODS

The authors conducted multicenter hospital-based surveillance as an inventory survey at 8 core hospitals in Okayama Prefecture between April 1, 2009, and March 31, 2019. Consecutive patients who lived in Okayama and were diagnosed with SAVSs on angiographic studies were enrolled. The clinical characteristics and the incidence rates of each form of SAVS and the differences between SAVSs at different spinal levels were analyzed.

RESULTS

The authors identified a total of 45 patients with SAVSs, including 2 cases of spinal arteriovenous malformation, 5 cases of perimedullary arteriovenous fistula (AVF), 31 cases of spinal dural AVF (SDAVF), and 7 cases of spinal epidural AVF (SEAVF). The crude incidence rate was 0.234 per 100,000 person-years for all SAVSs including those at the craniocervical junction (CCJ) level. The incidence rate of SDAVF and SEAVF combined increased with advancing age in men only. In a comparative analysis between upper and lower spinal SDAVF/SEAVF, hemorrhage occurred in 7/14 cases (50%) at the CCJ/cervical level and in 0/24 cases (0%) at the thoracolumbar level (p = 0.0003). Venous congestion appeared in 1/14 cases (7%) at the CCJ/cervical level and in 23/24 cases (96%) at the thoracolumbar level (p < 0.0001).

CONCLUSIONS

The authors reported detailed incidence rates of SAVSs in Japan. There were some differences in clinical characteristics of SAVSs in the upper spinal levels and those in the lower spinal levels.

ABBREVIATIONS

AVF = arteriovenous fistula; AVM = arteriovenous malformation; AVS = arteriovenous shunt; CCJ = craniocervical junction; DSA = digital subtraction angiography; IQR = interquartile range; mRS = modified Rankin Scale; OCSS = Okayama Cranial and Spinal A-V Shunts; PAVF = perimedullary AVF; SAVM = spinal AVM; SAVS = spinal arteriovenous shunt; SDAVF = spinal dural AVF; SEAVF = spinal epidural AVF.

OBJECTIVE

There have been no accurate surveillance data regarding the incidence rate of spinal arteriovenous shunts (SAVSs). Here, the authors investigate the epidemiology and clinical characteristics of SAVSs.

METHODS

The authors conducted multicenter hospital-based surveillance as an inventory survey at 8 core hospitals in Okayama Prefecture between April 1, 2009, and March 31, 2019. Consecutive patients who lived in Okayama and were diagnosed with SAVSs on angiographic studies were enrolled. The clinical characteristics and the incidence rates of each form of SAVS and the differences between SAVSs at different spinal levels were analyzed.

RESULTS

The authors identified a total of 45 patients with SAVSs, including 2 cases of spinal arteriovenous malformation, 5 cases of perimedullary arteriovenous fistula (AVF), 31 cases of spinal dural AVF (SDAVF), and 7 cases of spinal epidural AVF (SEAVF). The crude incidence rate was 0.234 per 100,000 person-years for all SAVSs including those at the craniocervical junction (CCJ) level. The incidence rate of SDAVF and SEAVF combined increased with advancing age in men only. In a comparative analysis between upper and lower spinal SDAVF/SEAVF, hemorrhage occurred in 7/14 cases (50%) at the CCJ/cervical level and in 0/24 cases (0%) at the thoracolumbar level (p = 0.0003). Venous congestion appeared in 1/14 cases (7%) at the CCJ/cervical level and in 23/24 cases (96%) at the thoracolumbar level (p < 0.0001).

CONCLUSIONS

The authors reported detailed incidence rates of SAVSs in Japan. There were some differences in clinical characteristics of SAVSs in the upper spinal levels and those in the lower spinal levels.

ABBREVIATIONS

AVF = arteriovenous fistula; AVM = arteriovenous malformation; AVS = arteriovenous shunt; CCJ = craniocervical junction; DSA = digital subtraction angiography; IQR = interquartile range; mRS = modified Rankin Scale; OCSS = Okayama Cranial and Spinal A-V Shunts; PAVF = perimedullary AVF; SAVM = spinal AVM; SAVS = spinal arteriovenous shunt; SDAVF = spinal dural AVF; SEAVF = spinal epidural AVF.

In Brief

The objective in this paper was to investigate the epidemiology of spinal arteriovenous shunts and the differences in characteristics between these lesions occurring at different spinal levels by using multicenter hospital-based surveillance as an inventory survey. The crude incidence rate was 0.234 per 100,000 person-years for all spinal arteriovenous shunts, and there were some differences in the clinical characteristics between the upper and lower spinal levels. The present study is the first reported inventory survey of spinal arteriovenous shunts.

Spinal arteriovenous shunts (SAVSs) are abnormal connections between arteries and veins of the spinal cord or adjacent structures that present with a wide variety of neurological symptoms. They are reported to be a rare disease,1–5 but to date there has been no inventory surveillance of their incidence rate. There have, however, been some recent reports on the clinical characteristics and anatomical details of specific types of SAVS lesions, such as craniocervical junction (CCJ) AVSs and thoracolumbar spinal epidural arteriovenous fistulas (SEAVFs).6,7

In the present study, we conducted multicenter hospital-based surveillance as an inventory survey to investigate the epidemiology of SAVSs and the differences in clinical characteristics between SAVSs occurring at different spinal levels.

Methods

Study Settings

Patient data were derived from the Okayama Cranial and Spinal A-V Shunts (OCSS) study database obtained through multicenter hospital-based surveillance.8 Our institutional ethics committees approved this study. Written informed consent had been obtained from all patients prior to angiography, endovascular treatment, or direct surgery, but written informed consent for this study was not required because of the retrospective noninvasive study design. Patients in this study were recruited from 8 institutions in Okayama Prefecture, a province in the western part of Honshu Island in Japan with a population of approximately 1.9 million. There are more than 150 hospitals in Okayama Prefecture. Due to the rarity of these diseases, only neuroendovascular specialists diagnose and treat almost all cases of intracranial and spinal AVSs in Okayama Prefecture. During the study period, the 8 core hospitals in Okayama Prefecture that employ neuroendovascular specialists certified by the Japanese Society for Neuroendovascular Therapy received all cases of these disorders that occurred anywhere in the catchment area. Thus, we concluded that multicenter hospital-based surveillance at these 8 centers would be suitable as an inventory survey in Okayama Prefecture. The collaborating centers and doctors other than the coauthors of this study are listed in the Acknowledgments.

The OCSS study database registered all consecutive cases of intracranial or spinal AVSs that were initially diagnosed by digital subtraction angiography (DSA) between April 2009 and March 2019. The database and this study included cases that were observed conservatively without treatment. The following patients were excluded from the database: patients living outside Okayama Prefecture; patients who were diagnosed prior to the start of the study period; patients with conditions other than AVSs, such as cavernous angioma or venous angioma; and patients who did not receive angiography. A total of 393 patients were included in the OCSS study database. We previously reported that among a total of 393 cranial and spinal AVSs, 201 (51.1%) cases of cranial dural AVF including those at the CCJ region, 155 (39.4%) cases of cranial arteriovenous malformation (AVM), and 34 (8.7%) cases of SAVS excluding those at the CCJ level were identified. We reported the crude incidence rates were 2.040 per 100,000 person-years for all AVSs, 0.805 for cranial AVM, 1.044 for intracranial dural AVF including those at the CCJ level, and 0.177 for SAVS excluding those at the CCJ level.8 In the present study we analyzed 45 patients (11.5%) with SAVSs, including those at the CCJ level.

Data Collection

The data set of the OCSS study included the following parameters: basic information (institution, year of diagnosis, age at diagnosis, patient age and sex, patient address, family history, and personal medical history); detailed information on lesions (chief complaint, initial clinical presentation, MRI findings, angiography findings, disease name, disease location, and preoperative modified Rankin Scale [mRS] score); treatment information (disease duration before treatment, treatment methods, treatment results, intraoperative complications, and postoperative delayed complications); and follow-up results (mRS score 3 months after the final treatment, last mRS assessment, duration of follow-up, final treatment results, recurrence, and retreatment). Regarding MRI and angiography findings, there are no standardized imaging or analysis methods. Therefore, equipment, techniques, and analyses of imaging depended on each hospital.

Shunt Types and Lesion Levels

We classified SAVSs into four shunt types as follows: spinal AVM (SAVM), perimedullary AVF (PAVF), spinal dural AVF (SDAVF), and SEAVF. We chose these categories based on the classification proposed by Takai.9 SDAVF and SEAVF are similar diseases that have a draining vein into the perimedullary vein and often present with progressive congestive myelopathy. We differentiated between SEAVF and SDAVF based on the description of angioarchitecture by Kiyosue et al.7 We defined intramedullary glomus and juvenile AVM as SAVM due to their rarity. We classified the locations of lesions into four spinal levels: CCJ, cervical other than CCJ, thoracic, and lumbar levels. The CCJ level was defined as the level of the first and second cervical vertebrae.

Evaluation

We investigated the characteristics, clinical presentation, and incidence rate of each type of SAVS at each level during the study period. For a comparative analysis between lesions at the upper and lower spinal levels, we assessed clinical characteristics, treatment results, and follow-up results in all patients divided according to lesion location: CCJ/cervical level and thoracolumbar level. We excluded cases of SAVM and PAVF from these analyses because of their rarity and because they are distinct from SDAVF and SEAVF in various ways.

Statistical Analysis

We performed all calculations using JMP 14 software (SAS Institute). Descriptive statistics were expressed as the mean ± SD for continuous variables, median (interquartile range [IQR]) for ordinal variables, and numbers (percentages) for categorical variables. We calculated crude incidence rates per 100,000 person-years during the 10-year study period using the monthly population survey in Okayama Prefecture.10 We calculated 95% confidence intervals (CIs) of crude incidence rates based on the Poisson distribution. Age-adjusted incidence rates were calculated according to the direct method, using the population of Okayama Prefecture from the 2015 census as a standard.10 Two-group comparison was assessed using Fisher’s exact test or the Wilcoxon signed-rank test. We presented our results as relative risk with 95% CIs. The significance level was set at p < 0.05.

Results

Baseline and Clinical Characteristics of Each Shunt Type

We identified a total of 45 patients with SAVS during the study period. These included 2 cases of SAVM, 5 cases of PAVF, 31 cases of SDAVF, and 7 cases of SEAVF. The baseline and clinical characteristics of each shunt type are described in Table 1. The mean age at diagnosis was 66 ± 13 years, and 36 patients (80%) were male. Twenty-one patients (47%) presented with moderate or severe disability (mRS score > 2) at diagnosis. Hemorrhage and venous congestion were reported in 7 (16%) and 29 (64%) patients, respectively. All patients with hemorrhage had upper SDAVF, 5 with CCJ lesions and 2 with cervical lesions. Of all 45 lesions, 11 (24%) were at the CCJ level, 3 (7%) were at the cervical level, 19 (42%) were at the thoracic level, and 12 (27%) were at the lumbar level. All CCJ and cervical lesions were SDAVFs.

TABLE 1.

Baseline and clinical characteristics of each disease

CharacteristicTotal, n = 45SAVM, n = 2PAVF, n = 5SDAVF, n = 31SEAVF, n = 7
Age at Dx in yrs (mean ± SD)66 ± 1343 ± 3661 ± 1068 ± 1273 ± 6
Male36 (80)1 (50)3 (60)25 (81)7 (100)
Comorbidities
Hypertension17 (38)0 (0)0 (0)15 (48)2 (29)
Diabetes mellitus7 (16)0 (0)0 (0)6 (19)1 (14)
Dyslipidemia7 (16)0 (0)1 (20)6 (39)0 (0)
Medical history
Family history of SAVS or hereditary disease0 (0)0 (0)0 (0)0 (0)0 (0)
Trauma or op near lesion2 (4)0 (0)0 (0)0 (0)2 (29)
Cancer or venous thrombosis4 (9)0 (0)0 (0)2 (6)2 (29)
Median disease duration in mos prior to Dx (IQR)9 (2–18)NA11 (4–18)8 (2–18)4 (2–18)
mRS score >2 at Dx21 (47)2 (100)1 (20)11 (35)7 (100)
Clinical presentation
Hemorrhage7 (16)0 (0)0 (0)7 (23)0 (0)
Myelopathy due to venous congestion29 (64)2 (100)3 (60)17 (55)7 (100)
Others7 (16)0 (0)2 (40)5 (16)0 (0)
Asymptomatic2 (4)0 (0)0 (0)2 (6)0 (0)
Spinal level
CCJ11 (24)0 (0)0 (0)11 (35)0 (0)
Cervical3 (7)0 (0)0 (0)3 (10)0 (0)
Thoracic19 (42)2 (100)1 (20)15 (48)1 (14)
Lumbar12 (27)0 (0)4 (80)2 (6)6 (86)

Dx = diagnosis; NA = not available.

Unless otherwise indicated, values are expressed as the number of patients (%).

Incidence Rates of SAVSs

According to a monthly population survey, Okayama Prefecture’s average population during the study period was 1,926,103, and the cumulative population during the same period was 231,132,350 person-months.

The crude incidence rates for the conditions under study were 0.234 (95% CI 0.172–0.309) per 100,000 person-years for all SAVSs including those at the CCJ level, 0.177 (95% CI 0.124–0.243) for all SAVSs excluding those at the CCJ level, 0.036 (95% CI 0.016–0.070) for SAVM and PAVF combined at all levels, 0.197 (95% CI 0.141–0.267) for SDAVF and SEAVF combined at all levels, and 0.125 (95% CI 0.081–0.181) for SDAVF and SEAVF combined at the thoracolumbar level (Table 2). Figure 1 shows the age-specific incidence rates of SDAVF and SEAVF combined at all levels in all patients and in patients grouped according to sex. The incidence rate of male sex increased in an age-dependent manner.

TABLE 2.

Crude and age-adjusted incidence rates of SAVSs per 100,000 person-years

VariableNo. of PtsCrude Incidence Rate (95% CI)Age-Adjusted Incidence Rate (2015 census, Okayama)
Total including CCJ level450.234 (0.172–0.309)0.216
Total excluding CCJ level340.177 (0.124–0.243)0.163
SAVM & PAVF at all levels70.036 (0.016–0.070)0.024
SDAVF & SEAVF at all levels380.197 (0.141–0.267)0.182
SDAVF & SEAVF at thoracolumbar level240.125 (0.081–0.181)0.114

Pts = patients.

FIG. 1.
FIG. 1.

Age-specific incidence rates of SDAVFs and SEAVFs at all spinal levels in all patients, in male patients, and in female patients.

Comparison Between Upper and Lower Spinal Levels

For SDAVF and SEAVF, we performed a comparative analysis between lesions at the CCJ/cervical level and those at the thoracolumbar level (Table 3). Neurological symptoms appeared in 9 cases (64%) at the CCJ/cervical level and in 24 cases (100%) at the thoracolumbar level (p = 0.004). All instances of hemorrhage occurred in patients with lesions at the CCJ/cervical levels. Myelopathy due to venous congestion occurred in 1 case (7%) at the CCJ/cervical level and in 23 cases (96%) at the thoracolumbar level (p < 0.0001). The median disease duration before diagnosis was significantly longer for lesions at the thoracolumbar level than for those at the CCJ/cervical level (13 months vs 1 month, respectively, p = 0.0009). Shunts at the CCJ/cervical level were completely obliterated in 1 case (7%) by embolization and in 9 cases (64%) by direct surgery. Shunts at the thoracolumbar level, in contrast, were completely obliterated in 10 cases (42%) by embolization and in 13 cases (54%) by direct surgery. There were no differences in complication rates or follow-up results. We present representative cases of CCJ-level (Fig. 2) and thoracic-level (Fig. 3) SDAVF.

TABLE 3.

Comparative analysis of SDAVF/SEAVF at the CCJ/cervical and thoracolumbar levels

VariableCCJ/Cervical Level, n = 14Thoracolumbar Level, n = 24Relative Risk (95% CI)p Value
Clinical characteristics
Age >70 yrs at Dx7 (50)13 (54)1.08 (0.57–2.05)>0.99
Male10 (71)22 (92)1.28 (0.90–1.83)0.17
Any neurological symptoms9 (64)24 (100)1.56 (1.05–2.30)0.004
Hemorrhage7 (50)0 (0)NA0.0003
Myelopathy due to venous congestion1 (7)23 (96)13.42 (2.03–88.86)<0.0001
Preop mRS score >25 (36)13 (54)1.41 (0.65–3.07)0.50
Median disease duration prior to Dx, in mos (IQR)1 (1–6)13 (4–19)0.0009
Tx results
Complete obliteration by embolization1 (7)10 (42)5.83 (0.83–40.88)0.03
Complete obliteration by direct surgery9 (64)13 (54)0.84 (0.49–1.44)0.74
Procedural complications1 (7)0 (0)NA0.38
Delayed complications1 (7)2 (8)1.17 (0.12–11.73)>0.99
FU results at >2 mos*
mRS score >2 at 3 mos after final Tx2 (15)6 (30)1.95 (0.46–8.23)0.43
mRS score >2 at last FU2 (15)5 (25)1.63 (0.37–7.17)0.50
Median FU duration after Tx (IQR)21 (7–42)9 (5–38)

FU = follow-up; Tx = treatment.

Unless otherwise indicated, values are expressed as the number of patients (%).

Follow-up results were available in 13 patients in the CCJ/cervical level group and in 20 patients in the thoracolumbar level group.

FIG. 2.
FIG. 2.

A: A 66-year-old man with an SDAVF at the CCJ level presented with a sudden-onset headache. Sagittal CT image shows subarachnoid hemorrhage in front of the brainstem and upper cervical cord. B: The anteroposterior (AP) view of the CT angiography sequence shows an abnormal vessel from the right vertebral artery (VA). C: The AP view of the angiogram of the right VA shows the shunt point (black arrow) and intradural drainage into the median anterior medullary vein. D: The AP view of the 3D DSA of the right VA shows the shunt point (white arrow) and intradural drainage. E: We performed a suboccipital craniotomy and C1 hemilaminectomy to clip the intradural draining vein without complication. F: The AP view of the angiogram of the right VA after treatment shows disappearance of the AVF.

FIG. 3.
FIG. 3.

A: A 66-year-old male with an SDAVF at the thoracic level presented with motor and sensory disturbance of the lower extremities for 2 years. Sagittal T2-weighted MR image shows a high-intensity lesion in the spinal cord and perimedullary flow void signals behind the spinal cord. B: The AP view of the spinal angiogram of the left T6 segmental artery shows the shunt point (black arrow) and intradural drainage of AVF. C: The oblique view of the 3D DSA of the left T6 segmental artery shows the shunt point (white arrow) and intradural drainage of AVF. D: We performed transarterial embolization using 20% N-butyl-2 cyanoacrylate (NBCA) without complication. Note that the NBCA cast penetrated to the draining vein via the shunt point (black arrow). E: The AP view of the spinal angiogram of the left T6 segmental artery after embolization shows the disappearance of the AVF. F: Sagittal T2-weighted MR image obtained 3 months after the embolization shows the disappearance of the intramedullary high-intensity lesion and no perimedullary flow void signals.

Discussion

This detailed inventory survey of SAVSs reveals that the crude incidence rate of all SAVSs, including those at the CCJ level, was 0.234 per 100,000 person-years. The most common SAVS type was SDAVF/SEAVF at the thoracolumbar level, with a crude incidence rate of 0.125 per 100,000 person-years. We also present the results of a comparative analysis of lesions at different spinal levels. To the best of our knowledge, this is the first reported inventory survey of SAVSs.

Epidemiology

To date, there has been no well-organized inventory survey of SAVSs. Some authors1–3 refer to the work of Thron as a source for the incidence rate of SDAVF. Thron has reported that, although exact figures on the frequency of this rare disease are not available, careful consideration suggests an estimated 5–10 SDAVF cases/year per 1 million inhabitants.5 From this, we calculate his estimated incidence rate as 0.5–1.0 per 100,000 person-years, a figure that exceeds the previously reported incidence rates of intracranial dural AVFs, which ranged from 0.15 to 0.51 per 100,000 person-years.4,11–13 Kuwayama has reported nationwide questionnaire surveillance data for dural AVF in Japan between 1998 and 2002.4 His database consisted of 1815 cases of dural AVFs, including 105 SDAVFs. Kuwayama estimated that the detection rate for all dural AVFs was 0.29 per 100,000 persons per year. From this, we can calculate the detection rate of SDAVF as 0.017 per 100,000 person-years. A Spanish cohort study of patients treated between 1972 and 2008 reported that the incidence of nontraumatic spinal cord injury was 1.21 per 100,000 person-years.14 In this cohort, 15.5% of nontraumatic spinal cord injuries consisted of vascular disease. This allows us to calculate the incidence rate of spinal vascular disease as 0.19 per 100,000 person-years; unfortunately, however, this figure includes aneurysms, AVMs, and cord infarctions. In our study we reported the crude incidence rates based on inventory surveillance. Consequently, our results are more precisely limited to SAVSs and are therefore more reliable.

The most distinctive epidemiological characteristic of SAVSs is the high incidence of SDAVF and SEAVF in older men. Several case series with large numbers of patients have shown that the proportion of men among patients with SDAVF is 72%–85%, with a mean age of 60–67 years.1,7,15–22 Among patients with SEAVF, the proportion of men is 63%–73%, with a mean age of 67–68 years.7,21,23,24 Jellema et al. found 6 thoracic arteriovenous anastomoses in 10 human cadavers who were not known to have suffered from spinal disease during life. The mean age of these cadavers was 78 years.25 This demonstrates that subclinical AVSs may occur in healthy older people more often than we suspect. The tendency of these shunts to manifest at advanced ages, as Thron has suggested, may be due at least in part to an acquired triggering mechanism like hypertension, inflammation, thrombosis, or microtrauma.26

In the present study, the proportions of men among patients with SAVS were 81% for SDAVF and 100% for SEAVF. The mean ages were 68 years for SDAVF and 73 years for SEAVF. Compared to the case series mentioned above, our results demonstrate an even older mean age for both of these SAVSs, indicating that the incidence of these diseases is continuing to increase among older men. We presume that the reasons for this ongoing increase are the aging of the overall population and therefore of the patient population, and the small number of patients in our database. One possible explanation for the higher incidence rates in men is the embryological background of the spinal dural membrane, which is composed only of dura propria derived from the neural crest cells.27 Intracranial dural AVFs with the same embryological background of the dural membrane, such as tentorial or falx dural AVFs, also have higher incidence rates in men.4,27

Differences Between Upper and Lower Spinal Levels

Most SDAVFs occur at the thoracolumbar level.1,7,15,18–20,22 The most frequent clinical presentation of SDAVF and SEAVF at the thoracolumbar level is progressive myelopathy due to venous congestion,1,7,18–20,22 but this is not so for all SAVSs: AVFs at the CCJ and cervical levels may present with progressive myelopathy or hemorrhage, with hemorrhage reported to be the most common clinical presentation.6,28–30 Likewise, two systematic review articles about CCJ AVFs have mentioned that 37.5%–43.1% of patients present with subarachnoid hemorrhage.31,32 In the present study, hemorrhage occurred only in patients with CCJ and cervical lesions.

Disease duration prior to diagnosis is one of the significant differences between the upper and lower spinal levels. The diagnosis of SDAVF at the thoracolumbar level tends to be delayed due to its nonspecific symptoms. Previous literature records that the mean and median times to diagnosis were 19–24 months and 7–12 months, respectively.1,16,18–20 SDAVFs at the CCJ and cervical levels, in contrast, may be diagnosed sooner after their onset due to presentation with hemorrhage or brainstem dysfunction.

In the present study, nearly all thoracolumbar SDAVFs and SEAVFs were obliterated, and this was achieved through embolization and direct surgery in approximately equal proportions. In CCJ/cervical SDAVFs and SEAVFs, in contrast, a larger proportion of patients were asymptomatic or had nonneurological symptoms and therefore were observed conservatively; in those cases in which lesions were obliterated, this was achieved primarily through direct surgery. Another study on a large series of intracranial dural AVFs reported that nonsinus-type AVF, including that at the CCJ level, was one of the independent risk factors for overall complications after embolization.33 According to the results of a Japanese nationwide registry of SDAVF, compared to noncervical SDAVF, cervical SDAVF was characterized by higher rates of hemorrhage onset, incomplete obliteration of the shunt, and embolization-related complications.22 Therefore, embolization of these lesions has a higher risk of brainstem or spinal cord infarction. In the present study, we treated these lesions mostly by direct surgery, which enabled our low complication rate.

Limitations

The present study has some methodological limitations. First, the possibility of excluding patients who were treated outside of Okayama Prefecture or in other departments without angiography may have affected our results. Second, we may have missed some patients who were misdiagnosed with other spinal diseases and therefore not included in this database. Third, medical checkup of asymptomatic patients for spinal disease is not performed in general, and there can be undiagnosed patients. Fourth, no standardized imaging or analysis methods were applied to all patients at all participating centers. Moreover, advances in neuroimaging technology may influence the increasing number of cases. As a result of these four limitations, we may be underestimating the incidence. Meanwhile, we believe we can say that the incidence rate of all SAVSs is no less than 0.234 per 100,000 person-years, and these data are more accurate and specific than previous studies as described in the Discussion section. Fifth, because we performed this study in only one prefecture in Japan, the number of patients with each shunt type was small. Previously, two nationwide studies of SAVSs have been conducted in Japan, but these were registries rather than inventory surveys.22,34 In the future, nationwide population-based or hospital-based inventory surveys are warranted.

Conclusions

We conducted a multicenter hospital-based inventory survey in Okayama Prefecture and reported our findings on the clinical characteristics and incidence rates of SAVSs. The crude incidence rate of all SAVSs including those at the CCJ level was 0.234 per 100,000 person-years. The incidence rate of SDAVF and SEAVF combined increased in an age-dependent manner in men only. Most SDAVF and SEAVF cases at the thoracolumbar level presented with myelopathy, whereas those at the CCJ/cervical level presented with hemorrhage or myelopathy.

Acknowledgments

We express our heartfelt thanks to the collaborating doctors who devoted their time to this investigation: Kazuki Kobayashi, Department of Neurosurgery, Tsuyama Chuo Hospital, Okayama; Ayumi Nishida and Shun Tanimoto, Department of Neurosurgery, Japanese Red Cross Okayama Hospital, Okayama; Toshinari Meguro and Miki Taniguchi, Department of Neurosurgery, Kawasaki Medical School General Medical Center, Okayama; and Sanami Kawada and Michiari Umakoshi, Department of Neurosurgery, Okayama Kyokuto Hospital, Okayama, Japan. We received a commendation for this study from the Japanese Society for Neuroendovascular Therapy.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Hiramatsu, Ishibashi, Suzuki. Acquisition of data: Hiramatsu, Ishibashi, Miyazaki, Murai, Takai, Takasugi, Yamaoka, Nishi, Takahashi, Haruma. Analysis and interpretation of data: Hiramatsu, Ishibashi, Suzuki. Drafting the article: Hiramatsu. Critically revising the article: Ishibashi, Suzuki, Miyazaki, Murai, Takasugi, Hishikawa, Yasuhara, Sugiu, Date. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Hiramatsu. Statistical analysis: Hiramatsu. Administrative/technical/material support: Chin, Matsubara, Uno, Tokunaga, Sugiu, Date. Study supervision: Hishikawa, Yasuhara, Chin, Matsubara, Uno, Tokunaga, Sugiu, Date.

Supplemental Information

Previous Presentations

Portions of this work were presented orally at the 35th annual meeting of the Japanese Society for Neuroendovascular Therapy, which was held November 21–23, 2019, in Fukuoka, Japan.

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    • Export Citation
  • 7

    Kiyosue H, Matsumaru Y, Niimi Y, Takai K, Ishiguro T, Hiramatsu M, et al.JSNET Spinal AV Shunts Study Group. Angiographic and clinical characteristics of thoracolumbar spinal epidural and dural arteriovenous fistulas. Stroke. 2017;48(12):32153222.

    • Search Google Scholar
    • Export Citation
  • 8

    Murai S, Hiramatsu M, Suzuki E, Ishibashi R, Takai H, Miyazaki Y, et al. Trends in incidence of intracranial and spinal arteriovenous shunts: hospital-based surveillance in Okayama, Japan. Stroke. 2021;52(4):14551459.

    • Search Google Scholar
    • Export Citation
  • 9

    Takai K. Spinal arteriovenous shunts: Angioarchitecture and historical changes in classification. Neurol Med Chir (Tokyo). 2017;57(7):356365.

    • Search Google Scholar
    • Export Citation
  • 10

    Okayama Prefectural Monthly population survey. Okayama Prefecture Web site. Accessed August 13, 2021. https://www.pref.okayama.jp/page/detail-14029.html

    • Search Google Scholar
    • Export Citation
  • 11

    Brown RD Jr, Wiebers DO, Torner JC, O’Fallon WM. Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992. Neurology. 1996;46(4):949952.

    • Search Google Scholar
    • Export Citation
  • 12

    Al-Shahi R, Bhattacharya JJ, Currie DG, Papanastassiou V, Ritchie V, Roberts RC, et al. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke. 2003;34(5):11631169.

    • Search Google Scholar
    • Export Citation
  • 13

    Piippo A, Niemelä M, van Popta J, Kangasniemi M, Rinne J, Jääskeläinen JE, Hernesniemi J. Characteristics and long-term outcome of 251 patients with dural arteriovenous fistulas in a defined population. J Neurosurg. 2013;118(5):923934.

    • Search Google Scholar
    • Export Citation
  • 14

    van den Berg ME, Castellote JM, Mahillo-Fernandez I, de Pedro-Cuesta J. Incidence of nontraumatic spinal cord injury: a Spanish cohort study (1972-2008). Arch Phys Med Rehabil. 2012;93(2):325331.

    • Search Google Scholar
    • Export Citation
  • 15

    Gross BA, Albuquerque FC, Moon K, McDougall CG. Validation of an ‘endovascular-first’ approach to spinal dural arteriovenous fistulas: an intention-to-treat analysis. J Neurointerv Surg. 2017;9(1):102105.

    • Search Google Scholar
    • Export Citation
  • 16

    Jablawi F, Schubert GA, Hans FJ, Mull M. Anticoagulation therapy after surgical treatment of spinal dural arteriovenous fistula. Effectiveness and long-term outcome analysis. World Neurosurg. 2018;114:e698e705.

    • Search Google Scholar
    • Export Citation
  • 17

    Koch MJ, Stapleton CJ, Agarwalla PK, et al. Open and endovascular treatment of spinal dural arteriovenous fistulas: a 10-year experience. J Neurosurg Spine. 2017;26(4):519523.

    • Search Google Scholar
    • Export Citation
  • 18

    Narvid J, Hetts SW, Larsen D, Neuhaus J, Singh TP, McSwain H, et al. Spinal dural arteriovenous fistulae: clinical features and long-term results. Neurosurgery. 2008;62(1):159167.

    • Search Google Scholar
    • Export Citation
  • 19

    Saladino A, Atkinson JL, Rabinstein AA, Piepgras DG, Marsh WR, Krauss WE, et al. Surgical treatment of spinal dural arteriovenous fistulae: a consecutive series of 154 patients. Neurosurgery. 2010;67(5):13501358.

    • Search Google Scholar
    • Export Citation
  • 20

    Sasamori T, Hida K, Yano S, Asano T, Seki T, Houkin K. Long-term outcomes after surgical and endovascular treatment of spinal dural arteriovenous fistulae. Eur Spine J. 2016;25(3):748754.

    • Search Google Scholar
    • Export Citation
  • 21

    Takai K, Endo T, Yasuhara T, Seki T, Watanabe K, Tanaka Y, et al. Microsurgical versus endovascular treatment of spinal epidural arteriovenous fistulas with intradural venous drainage: a multicenter study of 81 patients. J Neurosurg Spine. 2020;33(3):381391.

    • Search Google Scholar
    • Export Citation
  • 22

    Tsuruta W, Matsumaru Y, Iihara K, Satow T, Sakai N, Katsumata M, et al. Clinical characteristics and endovascular treatment for spinal dural arteriovenous fistula in Japan: Japanese Registry of Neuroendovascular Therapy 2 and 3. Neurol Med Chir (Tokyo). 2019;59(12):492497.

    • Search Google Scholar
    • Export Citation
  • 23

    Nasr DM, Brinjikji W, Clarke MJ, Lanzino G. Clinical presentation and treatment outcomes of spinal epidural arteriovenous fistulas. J Neurosurg Spine. 2017;26(5):613620.

    • Search Google Scholar
    • Export Citation
  • 24

    Takai K, Shojima M, Imai H, Saito N, Taniguchi M. Microsurgical and endovascular treatments of spinal extradural arteriovenous fistulas with or without intradural venous drainage. World Neurosurg. 2018;111:e819e829.

    • Search Google Scholar
    • Export Citation
  • 25

    Jellema K, Bleys RL, Tijssen CC, Koudstaal PJ, van Gijn J. Thoracic radicular vessels by simultaneous intra-arterial and intravenous injection of araldite. Clin Anat. 2007;20(5):524529.

    • Search Google Scholar
    • Export Citation
  • 26

    Thron AK. Applications in spinal dural AV fistulas. In: Vascular Anatomy of the Spinal Cord, Radioanatomy as the Key to Diagnosis and Treatment. 2nd ed. Springer;2016:161163.

    • Search Google Scholar
    • Export Citation
  • 27

    Tanaka M. Embryological consideration of dural AVFs in relation to the neural crest and the mesoderm. Neurointervention. 2019;14(1):916.

    • Search Google Scholar
    • Export Citation
  • 28

    Kai Y, Hamada J, Morioka M, Yano S, Mizuno T, Kuratsu J. Arteriovenous fistulas at the cervicomedullary junction presenting with subarachnoid hemorrhage: six case reports with special reference to the angiographic pattern of venous drainage. AJNR Am J Neuroradiol. 2005;26(8):19491954.

    • Search Google Scholar
    • Export Citation
  • 29

    Kinouchi H, Mizoi K, Takahashi A, Nagamine Y, Koshu K, Yoshimoto T. Dural arteriovenous shunts at the craniocervical junction. J Neurosurg. 1998;89(5):755761.

    • Search Google Scholar
    • Export Citation
  • 30

    Sato K, Endo T, Niizuma K, Fujimura M, Inoue T, Shimizu H, Tominaga T. Concurrent dural and perimedullary arteriovenous fistulas at the craniocervical junction: case series with special reference to angioarchitecture. J Neurosurg. 2013;118(2):451459.

    • Search Google Scholar
    • Export Citation
  • 31

    Wang JY, Molenda J, Bydon A, Colby GP, Coon AL, Tamargo RJ, Huang J. Natural history and treatment of craniocervical junction dural arteriovenous fistulas. J Clin Neurosci. 2015;22(11):17011707.

    • Search Google Scholar
    • Export Citation
  • 32

    Zhao J, Xu F, Ren J, Manjila S, Bambakidis NC. Dural arteriovenous fistulas at the craniocervical junction: a systematic review. J Neurointerv Surg. 2016;8(6):648653.

    • Search Google Scholar
    • Export Citation
  • 33

    Hiramatsu M, Sugiu K, Hishikawa T, Nishihiro S, Kidani N, Takahashi Y, et al. Results of 1940 embolizations for dural arteriovenous fistulas: Japanese Registry of Neuroendovascular Therapy (JR-NET3). J Neurosurg. 2020;133(1):166173.

    • Search Google Scholar
    • Export Citation
  • 34

    Tsuruta W, Matsumaru Y, Miyachi S, Sakai N. Endovascular treatment of spinal vascular lesion in Japan: Japanese Registry of Neuroendovascular Therapy (JR-NET) and JR-NET2. Neurol Med Chir (Tokyo). 2014;54(1):7278.

    • Search Google Scholar
    • Export Citation
  • View in gallery

    Age-specific incidence rates of SDAVFs and SEAVFs at all spinal levels in all patients, in male patients, and in female patients.

  • View in gallery

    A: A 66-year-old man with an SDAVF at the CCJ level presented with a sudden-onset headache. Sagittal CT image shows subarachnoid hemorrhage in front of the brainstem and upper cervical cord. B: The anteroposterior (AP) view of the CT angiography sequence shows an abnormal vessel from the right vertebral artery (VA). C: The AP view of the angiogram of the right VA shows the shunt point (black arrow) and intradural drainage into the median anterior medullary vein. D: The AP view of the 3D DSA of the right VA shows the shunt point (white arrow) and intradural drainage. E: We performed a suboccipital craniotomy and C1 hemilaminectomy to clip the intradural draining vein without complication. F: The AP view of the angiogram of the right VA after treatment shows disappearance of the AVF.

  • View in gallery

    A: A 66-year-old male with an SDAVF at the thoracic level presented with motor and sensory disturbance of the lower extremities for 2 years. Sagittal T2-weighted MR image shows a high-intensity lesion in the spinal cord and perimedullary flow void signals behind the spinal cord. B: The AP view of the spinal angiogram of the left T6 segmental artery shows the shunt point (black arrow) and intradural drainage of AVF. C: The oblique view of the 3D DSA of the left T6 segmental artery shows the shunt point (white arrow) and intradural drainage of AVF. D: We performed transarterial embolization using 20% N-butyl-2 cyanoacrylate (NBCA) without complication. Note that the NBCA cast penetrated to the draining vein via the shunt point (black arrow). E: The AP view of the spinal angiogram of the left T6 segmental artery after embolization shows the disappearance of the AVF. F: Sagittal T2-weighted MR image obtained 3 months after the embolization shows the disappearance of the intramedullary high-intensity lesion and no perimedullary flow void signals.

  • 1

    Kirsch M, Berg-Dammer E, Musahl C, Bäzner H, Kühne D, Henkes H. Endovascular management of spinal dural arteriovenous fistulas in 78 patients. Neuroradiology. 2013;55(3):337343.

    • Search Google Scholar
    • Export Citation
  • 2

    Koch C. Spinal dural arteriovenous fistula. Curr Opin Neurol. 2006;19(1):6975.

  • 3

    Krings T, Geibprasert S. Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2009;30(4):639648.

  • 4

    Kuwayama N. Epidemiologic survey of dural arteriovenous fistulas in Japan: clinical frequency and present status of treatment. Acta Neurochir Suppl. 2016;123:185188.

    • Search Google Scholar
    • Export Citation
  • 5

    Thron A. Spinal dural arteriovenous fistulas. Article in German. Radiologe. 2001;41(11):955960.

  • 6

    Hiramatsu M, Sugiu K, Ishiguro T, Kiyosue H, Sato K, Takai K, et al. Angioarchitecture of arteriovenous fistulas at the craniocervical junction: a multicenter cohort study of 54 patients. J Neurosurg. 2018;128(6):18391849.

    • Search Google Scholar
    • Export Citation
  • 7

    Kiyosue H, Matsumaru Y, Niimi Y, Takai K, Ishiguro T, Hiramatsu M, et al.JSNET Spinal AV Shunts Study Group. Angiographic and clinical characteristics of thoracolumbar spinal epidural and dural arteriovenous fistulas. Stroke. 2017;48(12):32153222.

    • Search Google Scholar
    • Export Citation
  • 8

    Murai S, Hiramatsu M, Suzuki E, Ishibashi R, Takai H, Miyazaki Y, et al. Trends in incidence of intracranial and spinal arteriovenous shunts: hospital-based surveillance in Okayama, Japan. Stroke. 2021;52(4):14551459.

    • Search Google Scholar
    • Export Citation
  • 9

    Takai K. Spinal arteriovenous shunts: Angioarchitecture and historical changes in classification. Neurol Med Chir (Tokyo). 2017;57(7):356365.

    • Search Google Scholar
    • Export Citation
  • 10

    Okayama Prefectural Monthly population survey. Okayama Prefecture Web site. Accessed August 13, 2021. https://www.pref.okayama.jp/page/detail-14029.html

    • Search Google Scholar
    • Export Citation
  • 11

    Brown RD Jr, Wiebers DO, Torner JC, O’Fallon WM. Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992. Neurology. 1996;46(4):949952.

    • Search Google Scholar
    • Export Citation
  • 12

    Al-Shahi R, Bhattacharya JJ, Currie DG, Papanastassiou V, Ritchie V, Roberts RC, et al. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke. 2003;34(5):11631169.

    • Search Google Scholar
    • Export Citation
  • 13

    Piippo A, Niemelä M, van Popta J, Kangasniemi M, Rinne J, Jääskeläinen JE, Hernesniemi J. Characteristics and long-term outcome of 251 patients with dural arteriovenous fistulas in a defined population. J Neurosurg. 2013;118(5):923934.

    • Search Google Scholar
    • Export Citation
  • 14

    van den Berg ME, Castellote JM, Mahillo-Fernandez I, de Pedro-Cuesta J. Incidence of nontraumatic spinal cord injury: a Spanish cohort study (1972-2008). Arch Phys Med Rehabil. 2012;93(2):325331.

    • Search Google Scholar
    • Export Citation
  • 15

    Gross BA, Albuquerque FC, Moon K, McDougall CG. Validation of an ‘endovascular-first’ approach to spinal dural arteriovenous fistulas: an intention-to-treat analysis. J Neurointerv Surg. 2017;9(1):102105.

    • Search Google Scholar
    • Export Citation
  • 16

    Jablawi F, Schubert GA, Hans FJ, Mull M. Anticoagulation therapy after surgical treatment of spinal dural arteriovenous fistula. Effectiveness and long-term outcome analysis. World Neurosurg. 2018;114:e698e705.

    • Search Google Scholar
    • Export Citation
  • 17

    Koch MJ, Stapleton CJ, Agarwalla PK, et al. Open and endovascular treatment of spinal dural arteriovenous fistulas: a 10-year experience. J Neurosurg Spine. 2017;26(4):519523.

    • Search Google Scholar
    • Export Citation
  • 18

    Narvid J, Hetts SW, Larsen D, Neuhaus J, Singh TP, McSwain H, et al. Spinal dural arteriovenous fistulae: clinical features and long-term results. Neurosurgery. 2008;62(1):159167.

    • Search Google Scholar
    • Export Citation
  • 19

    Saladino A, Atkinson JL, Rabinstein AA, Piepgras DG, Marsh WR, Krauss WE, et al. Surgical treatment of spinal dural arteriovenous fistulae: a consecutive series of 154 patients. Neurosurgery. 2010;67(5):13501358.

    • Search Google Scholar
    • Export Citation
  • 20

    Sasamori T, Hida K, Yano S, Asano T, Seki T, Houkin K. Long-term outcomes after surgical and endovascular treatment of spinal dural arteriovenous fistulae. Eur Spine J. 2016;25(3):748754.

    • Search Google Scholar
    • Export Citation
  • 21

    Takai K, Endo T, Yasuhara T, Seki T, Watanabe K, Tanaka Y, et al. Microsurgical versus endovascular treatment of spinal epidural arteriovenous fistulas with intradural venous drainage: a multicenter study of 81 patients. J Neurosurg Spine. 2020;33(3):381391.

    • Search Google Scholar
    • Export Citation
  • 22

    Tsuruta W, Matsumaru Y, Iihara K, Satow T, Sakai N, Katsumata M, et al. Clinical characteristics and endovascular treatment for spinal dural arteriovenous fistula in Japan: Japanese Registry of Neuroendovascular Therapy 2 and 3. Neurol Med Chir (Tokyo). 2019;59(12):492497.

    • Search Google Scholar
    • Export Citation
  • 23

    Nasr DM, Brinjikji W, Clarke MJ, Lanzino G. Clinical presentation and treatment outcomes of spinal epidural arteriovenous fistulas. J Neurosurg Spine. 2017;26(5):613620.

    • Search Google Scholar
    • Export Citation
  • 24

    Takai K, Shojima M, Imai H, Saito N, Taniguchi M. Microsurgical and endovascular treatments of spinal extradural arteriovenous fistulas with or without intradural venous drainage. World Neurosurg. 2018;111:e819e829.

    • Search Google Scholar
    • Export Citation
  • 25

    Jellema K, Bleys RL, Tijssen CC, Koudstaal PJ, van Gijn J. Thoracic radicular vessels by simultaneous intra-arterial and intravenous injection of araldite. Clin Anat. 2007;20(5):524529.

    • Search Google Scholar
    • Export Citation
  • 26

    Thron AK. Applications in spinal dural AV fistulas. In: Vascular Anatomy of the Spinal Cord, Radioanatomy as the Key to Diagnosis and Treatment. 2nd ed. Springer;2016:161163.

    • Search Google Scholar
    • Export Citation
  • 27

    Tanaka M. Embryological consideration of dural AVFs in relation to the neural crest and the mesoderm. Neurointervention. 2019;14(1):916.

    • Search Google Scholar
    • Export Citation
  • 28

    Kai Y, Hamada J, Morioka M, Yano S, Mizuno T, Kuratsu J. Arteriovenous fistulas at the cervicomedullary junction presenting with subarachnoid hemorrhage: six case reports with special reference to the angiographic pattern of venous drainage. AJNR Am J Neuroradiol. 2005;26(8):19491954.

    • Search Google Scholar
    • Export Citation
  • 29

    Kinouchi H, Mizoi K, Takahashi A, Nagamine Y, Koshu K, Yoshimoto T. Dural arteriovenous shunts at the craniocervical junction. J Neurosurg. 1998;89(5):755761.

    • Search Google Scholar
    • Export Citation
  • 30

    Sato K, Endo T, Niizuma K, Fujimura M, Inoue T, Shimizu H, Tominaga T. Concurrent dural and perimedullary arteriovenous fistulas at the craniocervical junction: case series with special reference to angioarchitecture. J Neurosurg. 2013;118(2):451459.

    • Search Google Scholar
    • Export Citation
  • 31

    Wang JY, Molenda J, Bydon A, Colby GP, Coon AL, Tamargo RJ, Huang J. Natural history and treatment of craniocervical junction dural arteriovenous fistulas. J Clin Neurosci. 2015;22(11):17011707.

    • Search Google Scholar
    • Export Citation
  • 32

    Zhao J, Xu F, Ren J, Manjila S, Bambakidis NC. Dural arteriovenous fistulas at the craniocervical junction: a systematic review. J Neurointerv Surg. 2016;8(6):648653.

    • Search Google Scholar
    • Export Citation
  • 33

    Hiramatsu M, Sugiu K, Hishikawa T, Nishihiro S, Kidani N, Takahashi Y, et al. Results of 1940 embolizations for dural arteriovenous fistulas: Japanese Registry of Neuroendovascular Therapy (JR-NET3). J Neurosurg. 2020;133(1):166173.

    • Search Google Scholar
    • Export Citation
  • 34

    Tsuruta W, Matsumaru Y, Miyachi S, Sakai N. Endovascular treatment of spinal vascular lesion in Japan: Japanese Registry of Neuroendovascular Therapy (JR-NET) and JR-NET2. Neurol Med Chir (Tokyo). 2014;54(1):7278.

    • Search Google Scholar
    • Export Citation

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