Transcranial Doppler ultrasonography to evaluate cerebral hemodynamic changes in neurocysticercosis Ultrasonografía Doppler transcraneal para evaluar cambios hemodinámicos cerebrales en neurocisticercosis

Background Arteritis is a complication of neurocysticercosis (NCC), which is not well known and could trigger strokes. The transcranial Doppler ultrasound (TCD) is a noninvasive method for detecting, staging, and monitoring cerebrovascular diseases. Nonetheless, the utility of TCD to evaluate cerebral hemodynamic changes, suggesting vasculitis associated with NCC remains uncertain. Objective To evaluate cerebral hemodynamic changes


INTRODUCTION
Neurocysticercosis (NCC) is the most common parasitic infection of the central nervous system (CNS) and is present mainly in developing countries, being the cause of around 30% of secondary epilepsies. 1,2In Latin America, approximately 75 million people live in NCC-endemic regions, 400 thousand of whom are affected by the symptomatic disease. 3his infection occurs in parenchymal and extraparenchymal forms, with the latter involving the ventricular and subarachnoid spaces.The clinical presentation of NCC varies depending on the parasitic burden, location, size, degree of degeneration, and immune response of the host.Seizures, chronic headaches and intracranial hypertension are the most frequent manifestations. 2Cerebral cysticercotic vasculitis (CCV) is a less recognized complication of this infection and is predominantly documented in the subarachnoid form,. 4,5having been documented through the use of angiography in 53% (15/28) of patients with subarachnoid NCC. 6urthermore, CCV can result in strokes and, in some cases, brain hemorrhage. 7The frequency of cerebral infarctions associated with NCC varies from 2 to 15%. 8,9The mechanisms discussed that have implications on the cerebrovascular disease are an occlusive endarteritis secondary to basal exudates on the subarachnoid space, thrombosis of the superficial cortical vessels due to chronic meningitis, and segmental vasculitis of blood vessels due to an adjacent cyst. 4,5,8,10,11he transcranial Doppler (TCD) ultrasound is a noninvasive method for evaluating the blood flow velocity of the main intracranial arteries allowing the indirect detection of vasculitis.It is inexpensive and reproducible, even in critically ill patients, making this tool an important test for the detection, staging, and monitoring of cerebrovascular disease.The TCD has been shown to be valuable in different cerebrovascular pathologies, such as intracranial artery stenosis, monitoring of vasospasm, and cerebral circulatory arrest.Furthermore, this ultrasound has a sensitivity and specificity of 95% for detecting intracranial stenosis of major vessels in patients with ischemic stroke, with variations depending on the temporal bone thickness. 12,13In relation to its use in NCC, he information is currently scarce, and the only published prospective study included 9 individuals with was more frequent in the subarachnoid NCC group (9/29, 31.03% vs. 3/24, 12.5%; p ¼ 0.187), although this difference did not reach statistical significance.Conclusion Cerebral hemodynamic changes suggestive of vasculitis are frequent in patients with NCC and can be evaluated using TCD.
subarachnoid NCC and cerebral infarction, and arteritis was detected by TCD in 7 of 10 arterial lesions that were also detected by digital subtraction angiography, suggesting that TCD is a promising tool for the diagnosis and follow-up of CCV. 4 Although TCD is a useful tool in the diagnosis and followup of intracranial vasculitis of various etiologies, 13,14 information is still scarce regarding the use of TCD to detect CCV in patients with subarachnoid and parenchymal NCC.This study aimed to evaluate cerebral hemodynamic changes suggesting vasculitis in patients with subarachnoid and parenchymal neurocysticercosis by using TCD.

METHODS
We conducted a cross-sectional study approved by the Institutional Review Board of Instituto Nacional de Ciencias Neurológicas (INCN), a reference center for neurological diseases in Lima, Peru.A total of 53 consecutive NCC patients were included, 29 with subarachnoid and 24 with parenchymal, who were evaluated at the INCN outpatient clinic before starting antiparasitic treatment.Included subjects had NCC lesions evidenced in magnetic resonance imaging (MRI), confirmed by specific serology using enzyme-linked immunoelectrotransfer blot (EITB), fulfilling the diagnostic criteria. 15The exclusion criteria were history of cerebrovascular disease or intracranial vasculitis attributable to other causes, and focal deficit.The presence of arachnoiditis was assessed using postcontrast MRI.
The sonographic diagnosis of CCV was defined by the identification of stenosis or occlusion along a blood vessel using TCD with a 2-MHz transducer from DWL (Multidopp T. 0801, 2006).The procedure was performed by one vascular neurologist trained in ultrasonography, blinded to the clinical and neuroimaging findings of the participants.The arteries were evaluated in two windows: the middle cerebral artery (MCA), anterior cerebral artery (ACA), and posterior cerebral artery (PCA) were evaluated through the temporal window, while the basilar artery was evaluated through the suboccipital window.Alterations in the mean velocities consistent with stenosis or occlusion have been described in previous studies. 13,16ach artery was evaluated along the blood vessels.For the MCA, 6 segments were considered from 65 to 40 mm in depth; for the ACA, 3 segments, from 65 to 75 mm in depth; the PCA was evaluated in 3 segments, from 55 to 65mm in depth; and the basilar artery, in 6 segments, from 75 to 100 mm in depth.The diagnostic criteria for stenosis of the middle and anterior cerebral arteries were the peak systolic velocity (PSV) greater than 140 cm/s and the mean velocity (MV) greater than 80 cm/s in at least one segment.The criteria for basilar artery and PCA stenosis were mean blood flow velocities greater than 65 cm/s and 70 cm/s respectively. 16,17atient characteristics were described as summary statistics, with categorical variables being expressed as percentages, whereas continuous and discrete variables were expressed using mean AE standard deviation (SD) or median and ranges, respectively.Normality assessment was per-formed using the Shapiro-Wilk test and comparisons between groups was performed by the Student t-test in cases of quantitative variables with normal distribution or by the Mann-Whitney U test.Additionally, the Chi-squared, and Fisher exact tests were used for categorical variables.Statistical significance of the test was set at 0.05.The analysis was performed using Stata (StataCorp LLC., College Station, TX, USA), version 17.0.

DISCUSSION
The NCC is a risk factor of stroke in young and middle-aged individuals. 8Vasculitis occurs in this condition but is not always recognized, with a tendency to be more frequent in the subarachnoid type. 10In this series, we demonstrated sonographic signs of vasculitis in 23% of the patients with NCC, supporting the utility of TCD in the diagnosis of NCCrelated vasculopathy.The vasculopathy found in our group of patients was mostly MCA involvement in 11 cases (91.67%), concordant with previous reports.In 1998, Berrinagarrementería et al. detected cerebral arteritis by angiography in 15/28 (53%) patients with subarachnoid NCC, 8 (53%) of whom had evidence of infarction on MRI, while in the group without arteritis only 1 had an infarction, and the most commonly affected vessels were the MCA and PCA. 6The strong correlation between arteritis and stroke in these patients suggests that early identification of CCV could allow the implementation of preventative measures, potentially decreasing morbidity and mortality.Tools such as TCD, a noninvasive and inexpensive diagnostic exam that can be performed at the bedside, can help in the diagnosis. 13,17nly one study has reported the use of TCD in the evaluation of intracranial arteries in NCC; the exam was performed on 9 patients with subarachnoid NCC and infarction, detecting large vessel arteritis in 7 of 10 arterial lesions demonstrated on cerebral angiography.The findings were occlusive in 2 and stenotic in 5. Furthermore, 4 of the 6 arterial lesions in the follow-up resolved in 3 cases when they were evaluated between 4 and 6 months of follow-up,

Vasculitis and neurocysticercosis
Boluarte et al.  and in one case the stenosis remained at 12 months of evaluation.In the remaining 2 cases, the occlusive pattern remained until 18 months of follow-up. 4The TCD is useful for diagnosis and could be useful for the follow-up, providing information about the progression of the arteriopathy and the risk of strokes in this population.
No patients with stroke were found in our study.However, sonographic signs of vasculitis were documented with a high frequency, which implies the presence of a risk factor in asymptomatic patients and, possibly, the opportunity to detect and prevent strokes.Vasculopathy in NCC more frequently affected those who had arachnoiditis, with approximately 50% previously reported in patients with arachnoiditis. 6he presence of vasculitis and subsequent strokes implies greater morbidity and mortality. 4,8,18It is relevant to account for this entity, to take preventive measures, using tools such as the TCD for the evaluation of vascular compromise, to improve the diagnosis and management.Conventional techniques for neurovascular imaging can fail to distinguish between vessel wall diseases.Therefore, it is necessary to evaluate different diagnostic tools. 19,20e main limitation of this study was that TCD findings were not compared with an angiography, and we could not show the capacity of this tool for diagnosis.Additionally, the small sample size did not allow us to reach definite conclusions.The use of steroids was also a variable that could impact in the evaluation of vasculitis.However, in our study, there was no difference in this variable between the NCC and vasculitis groups.
In conclusion, our study showed that TCD can be used to evaluate cerebral hemodynamic changes, suggesting vasculitis in patients with NCC.Longitudinal follow-up studies must define the role of this exam in monitoring hemodynamic alterations, assessing the burden of stroke associated with CCV, and determining whether early detection of sonographic signs of this condition and subsequent preventative measures can reduce the risk of stroke in patients with NCC.

Table 3
Description of the cases of vasculitis