Urological disturbances in patients with the spinal dural arteriovenous fistulas

Spinal dural arteriovenous fistulas (SDAVFs) are the most common vascular malformation of the spinal cord. However, they remain an undiagnosed pathology and, in case of untimely treatment cause significant disability. SDAVFs can debut with urination disorders, erectile dysfunction, and mimic different pathologies. At the same time, the vast majority of cases are difficult to diagnose. The urological aspects of SDAVFs are important for proper evaluation and management of patients with urological disorders. The objective: to analyze the urological disorders in patients with spinal dural arteriovenous fistulas and their course after surgical treatment. Materials and methods. From June 2009 to January 2023, 67 patients with arteriovenous malformations of the spinal cord were surgically treated at the SI «Research and Practical Center for Endovascular Neuroradiology of the National Academy of Medical Sciences of Ukraine». 44 (65.7%) patients were diagnosed with SDAVFs (arteriovenous malformations of the spinal cord type I according to Anson–Spetzler). Among the studied group were 30 (68.2%) men and 14 (31.8%) women aged 32–67 years (average age – 59.6 years). Treatment options for SDAVFs included endovascular embolization, microsurgical debridement, or their combination. A modified Aminoff–Logue scale was used to compare clinical results before and after treatment. After treatment, patients were divided into three categories: patient’s condition was improved, patient’s condition remained unchanged, or worsened. Results. As a result of the study, it was established that SDAVFs of the cervical spine was diagnosed in 6 (13.6%) patients, thoracic one – in 20 (61.9%), lumbar – 15 (21.1%), and sacrum – 3 (6.8%). The main initial symptoms of SDAVFs were gait disturbances, sensory disturbances, and paresthesias. The most common symptoms at the time of the final diagnosis were urination disorders in 36 (81.8%) patients, paraparesis – in 37 (84.1%), sensitivity disorders – in 30 (68.1%), defecation problems – in 17 (38.6%), pain in the back and legs – in 21 (47.8%) patients, erectile dysfunction – in 11 (25.0%) patients. After the total separation of the fistula, a favorable clinical result was observed in 31 (93.9%) of 33 patients. Improvement of urinary problems and erectile dysfunction was determined in 19 (52.7%) patients. Residual symptoms were found in 17 (47.3%) patients. Conclusions. Early intervention and elimination of pathologic arteriovenous shunting is necessary for neurological improvement in patients with SDAVFs, but urination disorders persist in half of patients even after successful treatment.

S pinal dural arteriovenous fistula (SDAVF) is a direct connection between a spinal artery and a vein [1].They belong to type I spinal arteriovenous malformations (AVM) according to Anson -Spetzler classification (1992) and account for 3-4% of spinal cord diseases that cause neurological deficits [2].
Nevertheless, they are uncommon in general population and occur in 5-10 patients per million persons annually [3], but are the most common type of spinal AVM, up to 80% of all cases [4].However, data suggest that SDAVF is seriously under diagnosed [5].
SDAVFs typically occurred between 55 and 60 years with male predominance (male-to-female ratio of 5:1).Less than 1% of patients with a SDAVF were younger than 30 years old [6].
Due to excessive arteriovenous shunting that leads to venous congestion, increased venous pressure, and progressive myelopathy, clinical manifestation of SDAVF has numerous neurologic symptoms, and can mimics different pathology [7], that often postponed correct diagnosis.Mean duration of symptoms according to the most large series in the literature is nearly 2 years and almost never less than 1 year [8].Slow and permanent progression make definitive diagnosis of SDAVF challenging.And it is not a rare for patients with SDAVF being consulted with urologists (urinary retention is mistakenly thought to be associated with prostrate hyperplasia or erectile dysfunction) [8].
Considering that, SDAVF is an extremely rare pathology that is sometimes misdiagnosed for months or years, clinical manifestation of this disease from all perspective should be carefully evaluated to improve early diagnosis and decreased irreversible damage of neuronal tissues.
The objective: to analyze the urological disorders in patients with spinal dural arteriovenous fistulas and their course after surgical treatment.

MATERIALS AND METHODS
Sixty seven patients with a spinal AVM were surgically treated at SI «Scientific-practical Center of endovascular neuroradiology NAMS of Ukraine» between June 2009 and January 2023.Among them 44 (65.7%) patients had SDAVF (Anson -Spetzler Type I spinal AVM), 30 (68.2%) males and 14 (31.8%)females, mean age (32-67 years, mean -59.6) which were retrospectively analyzed.The research protocol was approved by local ethic committee.Presenting signs and symptoms, baseline neurological assessments were evaluated.
Spinal angiography was used for SDAVF diagnosis in every case.Initial MRI was evaluable in 30 of the 44 cases.
Treatment options for SDAVF included endovascular therapy, microsurgical ligation, or both.The main goal of treatment was complete occlusion of the fistula.In case this aim couldn't be achieved without affordable risks, reducing of the blood flow was the second option.For endovascular embolization embolic glue (N-butyl 2-cyanoacrylate) was used with target penetration of the glue till proximal draining veins.In case endovascular approach was seemed difficult, risky or incomplete, microsurgical ligation was conducted.
Postoperative angiogram, which was done right after the treatment were analyzed to assessed result of the procedure (complete occlusion, in case of total resection or successful embolization of fistula, incomplete occlusion, in case of residual shunting of fistula remained).
A modified Aminoff-Logue Scale (Table 1) was used to compare the clinical outcomes before and after the treatment.
Considering modified Aminoff-Logue Scale we divided patients into three categories as improved, unchanged, or worsened.Treatment outcome where neurological deficits improved was considered favorable, while remained unchanged or worsened after the treatment was unfavorable.Patients with urological and erectile disturbances had urological and nephrological consultations for evaluation of concomitant diseases Statistical analyses were done using SPSS v. 24 software («SPSS Inc.», USA).Data are presented as median and range or as mean and standard deviation (±).Mann-Whitney U test was used to compare continuous variables.A value of p<0.05 was considered as statistically significant.
The most common initial sign of SDAVFs ware gait problem, sensory disturbances and paresthesia (burning sensation in the leg), which were seen in 21 (32.5%),11 (25.0%) and 9 (20.5%)patients respectively (Table 2).Micturition problems or erectile dysfunction as manifestation of the disease were seen in 6 (13.6%) cases (Fig. 1).Also, it should be mentioned that one patient with SDAVF and sacral involvement had spontaneous ejaculations after physical load.The time between initial presentation and diagnosis depend upon presentation and varied between 4-29 months (mean 21.2).In patients with sensory disturbances and paresthesia, it lasted 24.2 months and in case of initial motor deficits -5.1 months.
SDAVFs that were completely occluded had favorable clinical outcome in 31 (93.9%)among 33 patients, on the other hand only 6 (54.5%) of patients after incomplete occlusion had favorable results at the time of discharge.
Neurologic evaluation after the treatment according to Modified Aminoff-Logue Scale reveled improvement of all three domain despite the 9 cases where deficits remained the same of worsened (Table 3).
Reduction of urinary disorders depend upon the completeness of SDAVFs occlusion, the duration of symptoms as well as the presence of neurologic complication after procedure, and occurred in 19 (out of 36) patients, erectile dysfunction improved in 6 (out of 11) patients.17 (47.3%)patients had residual urinary and 5 (45.5%) patients -erectile disturbances, and among them 11 (64.7%) had complete fistulas occlusion, that probably is the result of long venous congestion and irreversible neuronal damage.
Our data confirmed that spinal dural arteriovenous fistulas (SDAVFs) are the most frequent spinal vascular malformation, but they are still underdiagnosed conditions that, if left untreated, can cause significant morbidity.Despite widespread introduction of MRI and spinal angiography, mean duration of symptoms was 21.2 months from onset to diagnosis, this status-quo remains among most large series during the last 20 years [8][9][10][11].
SDAVFs are acquired disorders with unknown pathophysiology, and it characterized by the presence of pathological shunt between radiculomeningeal artery, which supplies the nerve root, meninges and sometimes     the spinal cord, with radicular vein near the intervertebral foramen.Persistent arterial shunting into the veins causes the venous congestion with intramedullary edema, which leads to progressive myelopathy [7].Localization of SDAVFs is most common in lower thoracic and lumbar regions and contrary to cervical region with a numerous venous outflow thoracic region [12], venous congestive edema in this region is more likely to spread caudocranially, with initial signs of conus medullaris disorder, including urinal problem, buttocks and perineum anesthesia, gait disturbances etc. [7].
Considering rarity of SDAVFs and non-specific symptoms, especially during the early stages, correct diagnosis is crucial for better outcome as successful occlusion of fistula is important prognostic factor of the treatment outcome [8].Speaking from urological perspective about SDAVFs it is important to mention that sign or symptom of sacral segment involvement-micturition difficulties, fecal incontinence, in-voluntary ejaculation, or sensory loss in perineum are cardinal feature for suspicion of this pathology [6].Unfortunately, definitive diagnosis of this disease is difficult with only MRI, and CT-angiography and MR-angiography is mandatory to rule out the pathological shunting [13].Also, SDAVFs can mimic symptoms of prostate hyperplasia, sensory polyneuropathy, acute or chronic inflammatory demyelinating polyneuropathy, medullary tumor, and disc herniation, and should be ruled out in case of suspicion [14,8].

CONCLUSIONS
SDAVF is a rare vascular spinal disease which should be taken into account in case of bladder dysfunction and progressive myelopathy.

Fig. 1 .
Fig. 1. 33 years-old male with SDAVF of the conus medullaris, which manifest with leg weakness and erectile dysfunction.After 6 months he deteriorated to severe paraparesis, paresthesia of the both legs and perineum, urinal and fecal retention.Diagnosis was proven with MRI (A, arrow) and spinal angiography (B), which also revealed associated aneurysm (B, arrow).Patients underwent endovascular embolization with complete SDAVF and aneurysm occlusion (C, arrow).Postoperative period was associated with significant neurological improvement with reduction of urinal and defecation disturbances and residual slight right leg paresis.Follow-up MRI showed no signs of SDAVF (D, arrow)

Fig. 2 .
Fig. 2. 50 years-old male admitted with paraparesis, paresthesia of the left legs perineum, urinal and fecal retention.MRI (A, arrow) revealed severe venous congestion in the spinal cord and suspicion of SDAVF (B), spinal angiography of the left L2 segmental artery demonstrated the site of fistula (B, arrow).Patients underwent clip ligation (C) with complete SDAVF occlusion (D, arrow), that was confirmed by angiography.Postoperative period was associated with neurological improvement with reduction of urinal and defecation disturbances and residual slight left leg paresis.

Table 1
Assessment of the treatment outcome according to modified Aminoff and Logue Disability Scale

Table 2
Initial manifestation of spinal dural arteriovenous fistulas

Table 3
Assessment of neurological outcome after treatment of spinal dural arteriovenous fistulas