ORIGINAL ARTICLE
Magnetic Resonance Imaging in Neurocysticercosis Rosa Delia Delgado Hernández, MD,* Bernando Boleaga Durán, MD,† and Perla Salgado Lujambio, MD‡ Abstract: Cysticercosis in one of the most common parasitic infections in the central nervous system. The complex and unpredictable nature of the host immune reaction against cysticercosis as well as the pleomorphism of your injuries make the disease neurocysticercosis interesting and fascinating to study. Imaging studies play an important role in the diagnosis of this disease. Advanced imaging techniques have improved detection and visualization of scolex cysts extraparenchymal spaces. Key Words: cysticercosis, magnetic resonance imaging, diffusionweighted imaging, perfusion-diffusion weighted imaging, spectroscopy, 3D-CISS (Top Magn Reson Imaging 2014;23: 191–198)
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ysticercosis is one of the most common central nervous infections due to parasites. The hosts’ complex and unpredictable immunologic reaction to the cysticerci as well as the pleomorphism of the injuries make neurocysticercosis a fascinating illness to study. The exact prevalence of cysticercosis is unknown; nevertheless, it is estimated that several million people have been infected by the Taenia solium larva. In general, neurocysticercosis is endemic in most Latin-American countries, Subsaharian Africa, and some countries of Asia (Indonesia, Vietnam, Korea, and China). Neurocysticercosis is rare in northern Europe, Canada, Australia, Japan, and New Zeeland with the exception of immigrants. It is occasionally reported in Israel and Muslim countries of Africa and Asia. Neurocysticercosis was a rare illness in the United States and Occidental Europe 30 years ago. Because of the increasing numbers of immigrants from endemic regions together with the local cases, the zoonotic control of this illness is problematic. Some examples are 90% of the reported cases in the south of the United States due to Mexican and Latin-American immigration. A similar problem has been observed in Spain due to the large numbers of South American immigrants this country has received in the last years.1–3 In Brazil, studies have shown that the prevalence of neurocysticercosis varies between 1% and 6%, usually in patients with ages between 20 and 50 years from rural communities and who present partial epilepsy and endocraneal hypertension.4 Epidemiologic data describe the seroprevalence of cysticercosis in Latin-America between 3% and 20% (5%–24% for Peru and 3.7%–12% for Mexico), with the same predilection for rural patients.5 In Mexico, the prevalence of the disease varies by 9% in rural communities. The frequency of hospitalization in a tertiary level
From the *Radiology Department, Manuel Velasco Suarez National Institute of Neurology Neurosurgery, National Institute of Medical Science Nutrition Salvador Zubiran, Mexico City; †Mexican Academy of Surgery, Mérida, Yucatán; and ‡Neuroradiology Department and Teaching Division, National Institute of Neurology and Neurosurgery Manuel Velasco Suarez, Mexico City, Mexico. Reprints: Dra Rosa Delia Delgado Hernández, MD, Departamento de Neuroimagen, Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suárez, Insurgentes Sur 3877, Col La Fama, Delegación Tlalpan, CP 14269, México DF, México (e‐mail: [email protected]). The authors declare no conflict of interest. Copyright © 2014 by Lippincott Williams & Wilkins
has remained stable when comparing the years 1995 (2.4%) and 2001 (1.8%), with no statistically significant changes.6 In the Mexican adult population, the age of presentation of neurocysticercosis ranges in 38.1 years (36.2–41.5 years), predominantly men (51.7%). The consultation had 35.8% for seizures and 27.5% for intracranial hypertension clinic. Vesicular stage predominates (59.6%) and multiple (63.2%) and subarachnoid location ranges in 45.6%.6 Neurocysticercosis in children is lower than in adults, reported to have a frequency between 0.16% and 0.54% in an autopsy study in Mexico.7 The frequency of this disease in hospital concentration decreased in the last decades.8,9 In Mexico, for the current decade, the mean age of presentation of this disease is 10.3 years (range, 5–13 years), with no predominance of sex, referred from peripheral states to Mexico City in 66.7% of cases. The clinical problems are predominantly headache (66.7%) and seizures (33.3%). Among the radiologic findings, the presentation of vesicular (viable) is the most prevalent in 83.3% of the cases with multiple lesions (50%) and predominantly in parenchymal location (100%). In 33% of the patients, parenchymal presentation is accompanied by subarachnoid and intraventricular location. In the last decade, compared with other series, neurocysticercosis in the pediatric population has decreased its prevalence.8,9 Unlike adults, hypertension is usually secondary to intracranial cysticerci encephalitis, which is an exaggerated immune response of the host, secondary to massive infection of cysticerci in the brain parenchyma. The immune response in children for this presentation of the disease is usually active. Except for these patients with cysticercosis encephalitis, the other children with neurocysticercosis usually follow a benign course.8
MORPHOLOGY AND INVOLUTION PHASES OF THE CYSTICERCOID Degeneration of the cysticercoid has been divided in 4 histopathologic phases by Escobar and colleagues10: viable or vesicular, colloidal, nodular-granular, and nodular calcified. After penetration of the central nervous system (CNS), the cysticerci is in the vesicular phase (viable). In this period, the parasite has a transparent membrane with a clear vesicular fluid as well as an invaginated scolex. Brain parenchyma in this phase presents almost no inflammatory reaction to lesions and just creates a thin layer of collagen around the parasite. The cysticercoid can remain viable for several years or as a result of the immunologic attack of the host; it can progress into a degeneration process that transforms it into an inactive nodule. It is possible that the immune attack of the host occurs before the transformation of the metacestode inside the vesicular cysticerci. Independent of this, the metacestode or the vesicular cyst is in the first phase of the cysticerci evolution (colloidal phase), in which the vesicular liquid turns turbid and the scolex shows signs of hyaline degeneration. In this new phase, there is an intense mononuclear inflammatory reaction that includes the parasite itself. After this, the cyst wall will thicken, and the scolex will transform itself into a calcified granule. At this time point, the cysticercoid is no longer viable. This is the granular phase. Nevertheless,
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edema persists, and the adjacent astrocytes to lesions can even increase it. Finally, the remains of the parasite appear as a calcified nodule (calcified phase). By the side of the lesion, intense gliosis and the presence of multinuclear cells can be observed.1,11 Some cysticercoids have several membranes, which together resemble grape bunches. This presentation of the cysticercoids has been named racemose and has been observed in parasites localized in the basal cisterns.12 The mechanisms underlying these transformations are not completely clear, but it has been suggested that the vesicle begins to grow and the scolex disappears as the result of a degenerative process named hydropic degeneration.
NEUROIMAGING OF NEUROCYSTICERCOSIS The different pleomorphism of this illness generates differences with respect to the number and location of lesions as well as severity of the host immune system to the parasite. According to frequency, location, evolution, and treatment, the standard appearance of cysticerci can be divided in the following way: brain parenchyma, subarachnoid space, ventricular, spine channel, occular, and extraneural.11 The inflammatory reaction associated to neurocysticercosis is complex and has not been completely studied. Inflammation is necessary to reduce the size of the lesion and as part of the death process of the parasite, but at the same time, it is associated to shortand long-term complications. In parenchymal neurocysticercosis, the inflammation around the parasite is the principal cause of convulsions and occurs regularly in calcified and cystic degenerative lesions. The inflammatory reaction is minimal in the vesicular phase (viable) but varies in intensity in each patient in the moment the cystic degeneration is present. When the parasites appear out of the parenchyma, inflammation of CSF is frequent and intense, which conditions to arachnoiditis, ependymitis, vasculitis, and cranial pairs involvement.13
Parenchymal Neurocysticercosis The phase of development of the cysticercosis in brain parenchyma is determined by imaging studies. Cysticercosis in vesicular phase shows lesions with viable larvae sizes beside the scolex. These lesions can appear in 2 shapes—one in which lesions are small, round, with properly defined cysts, close to white and gray matter unions (mean size, 4–20 mm), and with a similar T1 and T2 values to that of CSF (Fig. 1)1; another that presents large cysts that can reach mean sizes of 10 cm—due to the absence of larvae inside the lesion and due to hidatidic transformations in which cystic membranes continue growing despite the absorption of the larvae.11 Lesions can also be found in the basal ganglia, cerebellum, and brainstem. The wall in these cases is thin; there is small or no peripheral edema as well as no posterior reinforcement due to the use of contrast agents. Plenty of the vesicular cysts have an eccentric or mural nodule inside, which represents the scolex and appears hyperintense in T1 and hypointense in T2 images and is considered as a pathognomonic sign called hole with dot. In case of doubt diffusionweighted imaging (DWI), apparent diffusion coefficient mapping can be useful to detect the scolex as a hyperintense nodule inside the vesicle. The scolex is the solid component of the structure, and therefore, it can be easily highlighted with DWI imaging.14 Cysticercosis in colloidal states shows degenerated larvae with turbid liquid and thick capsules. The cyst in degenerative phase can be seen as hyperintense in T1 and T2 imaging. In this phase, lesions are not well defined with peripheral edema. Most lesions show an ill-defined ring in the posterior
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FIGURE 1. Vesicular cysticercosis. A, Axial T1WI. B, Sagittal T1WI postcontrast. C, Axial CISS. D, Axial DWI. Note isointense lesion to cerebrospinal fluid, with the hyperintense scolex in DWI sequence (D). Note the eccentric scolex (blade) (D).
region (66% of cases). In some extraordinary cases, the scolex can be observed. Because of intense T2 signal, the scolex can be hidden. The mural module can be better observed with proton density contrast or using the fluid level-attenuated inversion recovery (FLAIR) sequence, in which it will appear as a hyperintense eccentric module inside the cyst (Fig. 2).15 As a differential diagnosis, the presence of lesions with 1 or more rings after contrast intake can be controversial, so other pathologies such as tuberculoma, cerebral abscess due to toxoplasmosis, primary cerebral neoplasms (glioblastoma), or secondary (metastasis) have to be considered as a possibility. For diagnostic imaging, we should use advanced sequences such as DWI, spectroscopy, or even perfusion-weighted imaging. Pyogenic abscess shows a hyperintense signal for DWI sequences; in contrast, neurocysticercosis cysts show a hypointense signal. A mature tuberculoma has a hypointense behavior for a T2 sequence. In toxoplasmosis, the location of the lesions is what has to be considered.14 In some cases, there are hypointense lesions in the center of the lesion and isointense lesions in the periphery, which can resemble tuberculomas, small abscess, and in some cases, metastasis. Some neurocysticercosis cysts show increased signal greater than the CSF, so that the behavior hyperintense on apparent diffusion coefficient maps by neurocysticercosis cyst may be useful in the differential diagnosis with an abscess.4 In vivo spectroscopy of neurocysticercosis shows cytosolic amino acid peaks (valine, leucine, and isoleucine), lactate (Lac), alanine, succinato/pyruvate, N-acetil-aspartato (NAA), creatinine (Cr), and choline (Cho). The NAA, Cr, and Cho peaks are thought to be due to the normal voxel contamination due to parenchyma signal. Pyruvate, a final product of glycolysis, can be metabolized through the aerobic path into acetate or through the anaerobic path to Lac in eukaryotic and parasitic organisms. This metabolite is © 2014 Lippincott Williams & Wilkins
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FIGURE 2. Colloidal cysticercosis. A, Axial T1WI postcontrast. B, Coronal T2WI. C, Sagittal FLAIR. D, Axial DWI. The cyst shows turbid fluid inside with thick wall and hyperintense signal on T2W image (B). Note brain edema (C) and scolex eccentric inside the lesion—colloidal stage (D).
predominant in racemose neurocysticercosis. The presence of pyruvate can be useful to differentiate between racemose neurocysticercosis and cystic gliomas (Fig. 3).4 The tuberculomas have a more elevated peak for lipids and Cho as well as smaller NAA and Cr peaks. The relation of Cho-Cr is larger than for all the tuberculomas, a ratio that changes for neurocysticercosis.16 Spectroscopy is useful for the cases of large cysticercosis without a visible scolex, as it can be used to differentiate them from a cerebral abscess or metastasis. In vivo, the succinate acetate peaks and Lac as well as the presence of keratin are dependent on the lesion being in the vesicular or colloidal phase. It has been described that the liquid obtained from cysts that starts degenerating lacks Cr. Meanwhile, vesicular cysts contain this metabolite because of the presence of muscular fibers in the scolex wall of the cysticercosis cyst.17 Neurocysticercosis is an entity that can generate lesions that resemble a pseudotumoral mass (gigantic cystic neoplasm),
FIGURE 3. Racemose neurocysticercosis. A and B, Sagittal and axial T1WI postcontrast. Observe multiple cysts in the right Sylvan fissure. © 2014 Lippincott Williams & Wilkins
MRI in Neurocysticercosis
so it can be confused with a brain neoplasm (Fig. 4). Perfusionweighted imaging sequences can confirm whether a lesion is of the benign parasitic type as the brain blood volume is low, showing differences with respect to the different grades of neurovascularity that an astrocytoma can show.4,14 In the nodule-granular phase, the larvae dies, the cyst starts collapsing so the scolex starts calcifying, the capsule gets thicker, and less reinforcement in the ring can be observed as well as less perilesional edema. In computerized tomography (CT), the cysticercosis can be seen as a hyperdense nodule after contrast infusion, with small to no perilesional edema. In MRI, the most common is that the lesion is observed with no signal on T1 and T2, with hyperdense ring, thick, and secondary to peripheral gliosis. In other cases, this injury can be identified as isointense in T1 and hypointense on T2 hyperintense center. At this stage, differential diagnosis must be made with tuberculosis and metastasis (Fig. 5, 6). In the calcified phase, the lesion is completely mineralized with inactive response from the host. The CT is the most sensitive imaging technique for this phase. In it, the lesion will appear as a hyperdense nodule without evidence of an edema and without enhancement. When using MRI techniques, sequences sensitive to calcifications should be used. Examples of these are gradient echo or the susceptibility-weighted imaging sequence. These sequences show calcifications and areas with hemorrhage as hypointense. In general, there is no mass effect or anormal enhancement after contrast administration (Fig. 7). Anyway, in this phase, reactivation of neurocysticercosis has been described. In the calcified phase, it has been reported in some chronic lesions that show anormal enhancement or peripheral edema. In patients with recent epileptogenic activity, intermittent inflammatory changes have been reported as a response to the residual antigen that eventually is liberated or reorganized in the host, even during or after the cesticid therapy. The use of T1-weighted sequences can be a sensitive method in the degenerative phase.4,15,18
FIGURE 4. A, Sagittal T1WI. B, Coronal T2WI. C, Axial DWI. D, Macroscopic piece. Note CSF-like lesion in T1WI and T2WI, without evidence of scolex inside the lesion. www.topicsinmri.com
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FIGURE 5. Nodular-granular cysticercosis. A, Axial T1WI. B, Axial T2WI. C, Axial DWI. D, Axial gradient echo. Note adjacent lesion to sulcus parieto-occipital, in the nodular-granular phase. Observe the lesion slightly hyperintense on T1WI and hypointense on T2WI without edema (A and B). In the gradient echo sequence (D), the lesion shows hypointense signal.
3-dimensional constructive interference in steady state (3D-CISS) should be used (Fig. 9). On the other hand, lesions located in the Sylvain fissure or in the base cisterns usually have larger sizes, have a multilobulated appearance (like a bunch of grapes), displace neighboring structures, can behave as space-occupying lesions, and show low or null enhancement of the walls of each cyst. Multilobulated cystic lesions with the appearance of a bunch of grapes receive the name of racemose (Figs. 3, 10).14 For the cystic lesion cases due to neurocysticercosis localized in the pontocerebellar cistern, differential diagnoses of epidermoid cysts, arachnoid cysts, schwannoma, or cystic meningioma must be considered. In these cases, the behavior of the lesion has to be evaluated with a 3D-CISS and with DWI. The 3D-CISS sequence is used to evaluate lesions in the pontocerebellar angle and middle and internal ear and is a useful tool for the discrimination of lesions in ventricles, sulci, and intraventricular spaces. The 3D-CISS must be routinely used in the valuations of lesions by subarachnoid and ventricular neurocysticercosis as it helps to distinguish the walls of the cyst and the scolex (Fig. 11).4,13 Other finding of subarachnoid neurocysticercosis is hydrocephaly due to the occlusion of the Luschka and Magendie holes due to fibrosis arachnoiditis. This can be observed both with CT and MRI imaging and is seen as anormal enhancement of basal leptomeninges in the skull basis (Figs. 11, 12). Arteritis is observed in 53% of the subarachnoid neurocysticercosis cases.14 The most common cerebral complications can find infarction due to occlusion of the principal cerebral
Less Frequent Presentations Miliar neurocysticercosis and pseudotumoral presentation are 2 abnormal presentations of this illness. The miliar form represents a massive infestation of the CNS by cysticercosis and is characterized by several small cysts all over the cerebral parenchyma.4 Massive infestation can cause encephalitic and no encephalitic forms of this illness. Encephalitic neurocysticercosis is more frequent in children and women, which are infested by a large load of eggs of the Taenia solium. In this case, the immune system of the host reacts strongly against the parasites. Clinically, it behaves as acute encephalitis. When using imaging methods, diffuse edemas and compression of the ventricular system are seen. After contrast injection, several nodular or ring-shaped lesions are observed and are distributed all throughout the brain parenchyma. No encephalitic neurocysticercosis is more common with Taenia solium carriers that have developed tolerance to the immune response after invasion of the parasite in the CNS and has started showing chronic epilepsy trends. These patients show multiple vascular lesions apparently viable and without the presence of edema, similar to a “Swiss cheese” (Fig. 8).19
Subarachnoid Neurocysticercosis Cerebral cistern involvement is present in approximately 3.5% of neurocysticercosis cases. Frequently, the subarachnoid cysts are small, unique, or multiple; are localized inside the cerebral sulci; and look similar to those observed in the cerebral parenchyma. These lesions can be difficult to detect because of the similar signal intensity of the cyst liquid content and the CSF. At the same time, the cyst wall is detected in rare occasions, the scolex cannot be seen, and postcontrast enhancement is almost negligible. Because of these factors, sequences such as FLAIR or
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FIGURE 6. Nodular-granular cysticercosis. A, Axial T1WI postcontrast. B, Axial T2WI. C, Axial gradient echo. D, Axial DWI. Different stages of cysticerci in the brain. Observe the lesions in both parietal in the nodule-granular phase, less postcontrast enhancement, and perilesional edema null. On T2WI, gradient echo and susceptibility-weighted imaging, hypointense signal is noted in these same 2 lesions. © 2014 Lippincott Williams & Wilkins
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FIGURE 7. Calcified cysticercosis. A, Axial CT scan. B, Axial T1WI. C, Axial gradient echo. D, Axial T2WI. Note multiple calcified lesions of small size, without peripheral edema.
MRI in Neurocysticercosis
FIGURE 9. Cysternal cysticercosis. A, Axial T1WI postcontrast. B, Axial T2WI. C, Axial CISS. D, Axial DWI. Axial CISS image demonstrates multiple cysts in the basal cisterns (superior cerebellar, ambiens, and suprasellar). Note multiple cysts within the larger lesion, located rostral to the left temporal horn, with eccentric scolex presence (C and D).
arteries (most frequent in the medial cerebral artery), reported between 4% and 6% with any kind of active neurocysticercosis (Fig. 13). These infarctions are associated with the inflammatory reaction that subarachnoid cyst lesions generate (particularly those located in the supraselar ventricle) or, secondary to the arachnoiditis, is observed in the ventricles of the base that at the same time affects the prefrontal basal vessels. Endarteritis should also be considered to be generated by cyst destruction secondary to medical management.1 Endarteritis due to cysticercosis causes severe endothelial disruption that can produce edema and thrombosis and the formation of fusiform aneurisms due to the weakness of affected vessel walls.
FIGURE 8. A, Axial T1WI. B, Axial T2WI. Note multiple vesicular lesions without evidence of edema, similar to Swiss cheese (courtesy of Dr Enrique Palacios, Tulane University School of Medicine, Louisiana). © 2014 Lippincott Williams & Wilkins
FIGURE 10. Racemose neurocysticercosis. A, Axial T1WI postcontrast. B, Coronal T2WI. C, Axial CISS. D, Axial DWI. Observe lesions located within the left Sylvian fissure: larger, multilocular (like cluster of grapes) lesions, which simulate space-occupying lesions. These lesions show no or little reinforcement in the walls of each cyst. www.topicsinmri.com
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FIGURE 13. Vascular complications of neurocysticercosis in a patient aged 11 years. A, Axial T1WI postcontrast. B, Axial DWI. Note the granular nodular lesion lateral to the left putamen and infarction in the territory of the ipsilateral posterior cerebral artery (courtesy of Dr Pilar Dies Suarez, Imaging Department, Hospital Infantil de Mexico Federico Gomez).
FIGURE 11. Subarachnoid cysticercosis and arachnoiditis. A, Axial T1WI. B, Axial CISS. C and D, Axial and sagittal T1WI postcontrast. Observe multiple cysts within basal cisterns and signs of arachnoiditis, more evident in the cistern quadrigerminal (D).
Arteritis due to cysticercosis affects the small- and mediumsized vessels, and on average, 50% of the patients find themselves affected by arachnoiditis.5
Ventricular Neurocysticercosis This is the second most common location (54% of the cases). This variant can appear isolated but, nevertheless, can be
FIGURE 12. Subarachnoid cysticercosis and arachnoiditis. A, Axial CT scan. B-D, Axial, sagittal, and coronal T1WI postcontrast. Observe the reinforcement in the various cisterns of the base.
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associated to parenchyma involvement (24% of the cases) and the subarachnoid.14 It usually affects the ventricle IV (54%– 64%), followed by the ventricle III (23%–27%), the lateral ventricles (11%–14%), and the Sylvain aqueduct (9%) (Fig. 14).4 Ventricular cysticercosis appears in CT imaging as hypodense lesions that distort the ventricular system causing asymmetric obstructive hydrocephaly. In the vesicular phase, vesicular cysts are isodense as well as the CSF, so they are difficult to determine using this technique. On the other hand, most of these lesions can be easily valuated using MRI because of the liquid properties of the liquid inside the vesicles or cysts as well as the scolex, different to those of the CSF (Fig. 15). In some occasions, the cyst is slightly more hyperintense than the CSF when using the FLAIR sequence, and it can show reinforcement after contrast perfusion. In some cases, the use of the sign of the ventricular signal can be useful for differential diagnosis. In it, motion of the cyst inside the ventricular cavity as a response to head motion is studied.20 For other patients, the presence of parasite membranes inside the ventricle or ventriculitis, secondary to the Monro hole occlusion, can be identified. Asymmetric dilation can also be detected of the posterior ventricle after ventricle shunt installation. Double-behavior hydrocephaly exists, where the fourth ventricle is isolated from the
FIGURE 14. Ventricular cysticercosis. A and B, Axial FLAIR. Note dilated supratentorial and infratentorial ventricular system with transependymal migration in a female patient aged 11 years. Observe the dilatation of the ventricles III and IV (courtesy of Dr Pilar Dies Suarez, Imaging Department, Hospital Infantil de Mexico Federico Gomez). © 2014 Lippincott Williams & Wilkins
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MRI in Neurocysticercosis
Sellar Neurocysticercosis Neurocysticercosis is described as the direct involvement of the sella by a vesicle. Twenty-three cases have been described in the literature, with involvement in ophthalmic disorders in 67% of patients and endocrine disorders in 57% of patients.21 This type of injury usually involves the pituitary and moves, compresses, and sometimes, destroys the pituitary stalk or the pituitary itself. This injury may be accompanied by hydrocephalus, involucre subarachnoid cisterns of the base, and chiasmatic arachnoiditis (Figs. 12, 16). As a differential diagnosis, a vesicle by neurocysticercosis may behave like an arachnoid cyst, pituitary adenoma with cystic degeneration, Rathke cleft cyst, epidermoid cyst, sellar craniopharyngioma, or granuloma.21,22
Neurocysticercosis in the Spine FIGURE 15. Intraventricular cysticercosis. A, Sagittal T1WI. B and C, Sagittal and axial CISS. D, Axial DWI. Observe the cystic lesion in the ventricle IV with eccentric scolex presence.
others, due to the presence of granular ependymitis and due to the occlusion of the cerebral aqueduct as well as simultaneous arachnoiditis that blocks the Luschka and Magendie holes. Ependymitis is identified as a hyperintense signal in T2 images at the ependyma level and subependimo as well as increasing contrast of the ventricular wall after infusion of contrast agents.14,19 For these patients, it might be important to install 2 independent derivation systems: one will drain the supratentorial ventricular system; and the other will drain the ventricle IV, which is isolated.1
Orbital Neurocysticercosis Orbital neurocysticercosis appears in a mean of 3% of the cases. The parasites in the ocular ball can affect the anterior and posterior camera and even the subconjunctival region.19 Cysticercosis affects the eye orbit through the choroid vessels localized in the subretinal level.4 After some time, the cysticercoids will need more space and will induce retinal spill and invasion of the vitreous. When using MRI, the parasite looks hyperintense in T1 and hypointense in T2; because of that, it can be confused with a choroid melanoma. Some of the differential diagnostics could be retinoblastoma in pediatric patients and metastasis in adult patients.19 The involvement of an extraocular muscle is the most common case of orbital neurocysticercosis, appearing as myositis. Involvement of the optical nerve is extremely rare but may occur through the hematogen way by branches of the central artery of the retina.4
FIGURE 16. Sellar cysticercosis. A, Sagittal CISS. B, Axial T1WI postcontrast. Note the destruction of the pituitary, coupled condition of the basal cisterns (A). Observe the increased size of the infundibulum sellar and its pathological enhancement (B). © 2014 Lippincott Williams & Wilkins
Spinal cord involvement is unusual and is reported for 1.2% to 5.8% of patients with neurocysticercosis. The appearance in the leptomeningeal (extramedullar) is 6 to 8 times more common than in the intramedullar (0.77%). Extradural presentation is even less common. Intramedullary cysticercosis may occur by hematogenous spread of infection outside the CNS, through the artery of Adamkiewicz.4,23 The low flux of the spinal cord, the type of vascularization of the cord (small caliber and pressure vessels), and the presence of spinal medulla contribute to the low number of intramedullary cases. It is usual to find cysts in the thoracic segment, as this is the region of the spinal cord that receives the higher fluxes (67%), followed by cervical and lumbar.25 The intradural-extramedullar involvement can be due to the scatter of the larvae from the brain to the subarachnoid space of the spine (Fig. 17).4 The MRI, when studying this form of neurocysticercosis, has displaced myelography, as well as CT. In MRI, the
FIGURE 17. Intradural spinal cysticercosis. A and C, Sagittal postcontrast T1WI. B and D, Sagittal and axial T2WI. Identify cystic lesions in intradural-extramedullary situation leading to spinal cord compression. Note syringomyelic cavity. www.topicsinmri.com
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2. Sorvillo F, Wilkins P, Shafir S, et al. Public health implications of implications of cisticercosis acquired in the United States. Emerg Infect Dis. 2011;17:1–6. 3. Más-sesé G, Vives-Pñera I, Fernández-Barreiro A, et al. A descriptive study of neurocysticercosis in a tertiary care hospital. Rev Neurol. 2008;46:194–196. 4. do Amaral LLF, Ferreira RF, da Rocha AJ, et al. Neurocysticercosis. Evaluation with advanced magnetic resonance techniques and atypical forms. Top Magn Reson Imaging. 2005;16:127–144. 5. Marquez JM, Arauz A. Cerebrovascular complications of neurocysticercosis. Neurologist. 2012;18:17–22. 6. Fleury A, Moreno García J, Valdez Aguerrebere P, et al. Neurocysticercosis, a persisting health problem in Mexico. PLoS Negl Trop Dis. 2010;4:e805. 7. Ridaura-Sanz C. Hosp response in childhood neurocysticercosis. Childs Nerv Syst. 1987;3:206–207. 8. Del Brutto. Neurocysticercosis in children: clinical, radiological and prognostic factors in 54 patients. Neurol Rev. 1997;25:1681–1684. 9. Ruiz-Garcia M, González-Astiazarán A, Rueda-Franco A. Neurocysticercosis in children. Clinical experience in 122 patients. Childs Nerv Syst. 1997;13:608–612.
FIGURE 18. Intramedullar cysticercosis. A, Axial T1WI. B, Axial T1WI postcontrast. C and D, Coronal and axial T2WI. Observe the intramedullary lesion, at the granular nodular stage, with peripheral rim enhancement (B).
intramedullar cysticercosis is identified as a round or septed isointense to CSF lesion in T1 and T2 sequences. They can present as an eccentric hyperintense nodule in relation with the scolex. Cyst periphery can reinforce, secondary to reinforcement from cystic wall or rupture of hematoencephalic barrier (Fig. 18). Spinal cord presents expansion and local edema. There is marked thickening and intense inflammatory reaction, suggesting fibrosis focal pachymeningitis.11,19,24 If the scolex cannot be identified, other differential diagnostics should be considered such as neoplasms (astrocytoma vs cystic ependymoma), inflammatory origin, demyelination, vascular, or granulomatous.1,19 Leptomeningeal cysts are easy to identify. These lesions are mobile and can change positions with relation to the patient during an imaging study.1
CONCLUSIONS Host immune response and the disease pleomorphism continue to exert a factor of interest in the study of neurocysticercosis. Using advanced sequences and noninvasive MRI, great progress contributes to the detection of the different stages of the disease, scolex detection, identification of lesions in the subarachnoid space, and better evaluation of the differential diagnoses.
10. Escobar A. The pathology of neurocysticercosis. In: Palacios Palacios E, Rodríguez-Carbajal J, Taveras JM, eds. Cysticercosis of the Central Nervous System. Springfield, IL: Charles C. Thomas; 1983:27–54. 11. Salgado P, Rojas R, Sotelo J. Cysticercosis. Clinical and classification based on imaging studies. Arch Intern Med. 1997;22:1991–1997. 12. Pittella JEH. Neurocyscitercosis. Brain Pathol. 1997;7:681–683. 13. Carpio A, Fleury A, Hauser WA. Neurocysticercosis. Five new things. Neurol Clin Pract. 2013;3:118–123. 14. Abdel-Razed AAK, Watcharakorn A, Castillo M. Parasitic diseases of the central nervous system. Neuroimaging Clin N Am. 2011;21:815–848. 15. Lucato LT, Guedes MS, Sato JR, et al. The role of conventional MR imaging sequences in the evaluation of neurocysticercosis: impact on characterization of the scolex and lesion burden. AJNR Am J Neuroradiol. 2007;28:1501–1504. 16. Pretell EJ, Martinot C Jr, Garcia HH, et al. Differential diagnosis between cerebral tuberculosis and neurocysticercosis by magnetic resonance spectroscopy. J Comput Assist Tomogr. 2005;29:112–114. 17. Gupta RK, Jobanputra KJ, Yadav A. MR spectroscopy in brain infections. Neuroimaging Clin N Am. 2013;23:475–498. 18. Poeschl P, Janzen A, Schuierer G, et al. Calcified neurocysticercosis lesions trigger symptomatic inflammation during antiparasite therapy. AJNR Am J Neuroradiol. 2006;27:653–655. 19. Del Brutto O, Campos X. Massive neurocysticercosis: encephalitic versus non-encephalitic. Am J Trop Med Hyg. 2012;87:381. 20. Garcia HH, Del Brutto O. Imaging findings in neurocysticercosis. Acta Trop. 2003;87;71–78. 21. Del Brutto OH, Del Brutto VJ. Intrasellar cysticercosis: a systematic review. Acta Neurol Belg. 2013;113:225–227.
ACKNOWLEDGMENT The authors thank medical doctors Fernando Robles Ramirez and Salomon Israel González Dominguez for their collaboration in the recollection and selection of clinical cases.
REFERENCES 1. Del Brutto O. Neurocysticercosis. Continuum Lifelong Learn Neurol. 2012;18:1392–1416.
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22. Arriada-Mendicoa N, Celis-López MA, Higuera-Calleja J, et al. Imaging features of sellar cysticercosis. AJNR Am J Neuroradiol. 2003;24:1386–1389. 23. Del Brutto OH, Garcia HH. Intramedullary cisticercosis of the spinal cord: a review of patients evaluated with MRI. J Neurol Sci. 2013;331:114–117 24. Moharty A, Venkatrama SK, Das S, et al. Spinal intramedullary cysticercosis. Neurosurgery. 1997;40:82–87. 25. Muzumbar D, Nadkarni T, Desai K, et al. Thoracic intramedullary cysticercosis. Two cases reports. Neurol Med Chir. 2002;42:575–579.
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Magnetic Resonance Imaging in Neurocysticercosis Rosa Delia Delgado Hernández, MD,* Bernando Boleaga Durán, MD,† and Perla Salgado Lujambio, MD‡ Abstract: Cysticercosis in one of the most common parasitic infections in the central nervous system. The complex and unpredictable nature of the host immune reaction against cysticercosis as well as the pleomorphism of your injuries make the disease neurocysticercosis interesting and fascinating to study. Imaging studies play an important role in the diagnosis of this disease. Advanced imaging techniques have improved detection and visualization of scolex cysts extraparenchymal spaces. Key Words: cysticercosis, magnetic resonance imaging, diffusionweighted imaging, perfusion-diffusion weighted imaging, spectroscopy, 3D-CISS (Top Magn Reson Imaging 2014;23: 191–198)
C
ysticercosis is one of the most common central nervous infections due to parasites. The hosts’ complex and unpredictable immunologic reaction to the cysticerci as well as the pleomorphism of the injuries make neurocysticercosis a fascinating illness to study. The exact prevalence of cysticercosis is unknown; nevertheless, it is estimated that several million people have been infected by the Taenia solium larva. In general, neurocysticercosis is endemic in most Latin-American countries, Subsaharian Africa, and some countries of Asia (Indonesia, Vietnam, Korea, and China). Neurocysticercosis is rare in northern Europe, Canada, Australia, Japan, and New Zeeland with the exception of immigrants. It is occasionally reported in Israel and Muslim countries of Africa and Asia. Neurocysticercosis was a rare illness in the United States and Occidental Europe 30 years ago. Because of the increasing numbers of immigrants from endemic regions together with the local cases, the zoonotic control of this illness is problematic. Some examples are 90% of the reported cases in the south of the United States due to Mexican and Latin-American immigration. A similar problem has been observed in Spain due to the large numbers of South American immigrants this country has received in the last years.1–3 In Brazil, studies have shown that the prevalence of neurocysticercosis varies between 1% and 6%, usually in patients with ages between 20 and 50 years from rural communities and who present partial epilepsy and endocraneal hypertension.4 Epidemiologic data describe the seroprevalence of cysticercosis in Latin-America between 3% and 20% (5%–24% for Peru and 3.7%–12% for Mexico), with the same predilection for rural patients.5 In Mexico, the prevalence of the disease varies by 9% in rural communities. The frequency of hospitalization in a tertiary level
From the *Radiology Department, Manuel Velasco Suarez National Institute of Neurology Neurosurgery, National Institute of Medical Science Nutrition Salvador Zubiran, Mexico City; †Mexican Academy of Surgery, Mérida, Yucatán; and ‡Neuroradiology Department and Teaching Division, National Institute of Neurology and Neurosurgery Manuel Velasco Suarez, Mexico City, Mexico. Reprints: Dra Rosa Delia Delgado Hernández, MD, Departamento de Neuroimagen, Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suárez, Insurgentes Sur 3877, Col La Fama, Delegación Tlalpan, CP 14269, México DF, México (e‐mail: [email protected]). The authors declare no conflict of interest. Copyright © 2014 by Lippincott Williams & Wilkins
has remained stable when comparing the years 1995 (2.4%) and 2001 (1.8%), with no statistically significant changes.6 In the Mexican adult population, the age of presentation of neurocysticercosis ranges in 38.1 years (36.2–41.5 years), predominantly men (51.7%). The consultation had 35.8% for seizures and 27.5% for intracranial hypertension clinic. Vesicular stage predominates (59.6%) and multiple (63.2%) and subarachnoid location ranges in 45.6%.6 Neurocysticercosis in children is lower than in adults, reported to have a frequency between 0.16% and 0.54% in an autopsy study in Mexico.7 The frequency of this disease in hospital concentration decreased in the last decades.8,9 In Mexico, for the current decade, the mean age of presentation of this disease is 10.3 years (range, 5–13 years), with no predominance of sex, referred from peripheral states to Mexico City in 66.7% of cases. The clinical problems are predominantly headache (66.7%) and seizures (33.3%). Among the radiologic findings, the presentation of vesicular (viable) is the most prevalent in 83.3% of the cases with multiple lesions (50%) and predominantly in parenchymal location (100%). In 33% of the patients, parenchymal presentation is accompanied by subarachnoid and intraventricular location. In the last decade, compared with other series, neurocysticercosis in the pediatric population has decreased its prevalence.8,9 Unlike adults, hypertension is usually secondary to intracranial cysticerci encephalitis, which is an exaggerated immune response of the host, secondary to massive infection of cysticerci in the brain parenchyma. The immune response in children for this presentation of the disease is usually active. Except for these patients with cysticercosis encephalitis, the other children with neurocysticercosis usually follow a benign course.8
MORPHOLOGY AND INVOLUTION PHASES OF THE CYSTICERCOID Degeneration of the cysticercoid has been divided in 4 histopathologic phases by Escobar and colleagues10: viable or vesicular, colloidal, nodular-granular, and nodular calcified. After penetration of the central nervous system (CNS), the cysticerci is in the vesicular phase (viable). In this period, the parasite has a transparent membrane with a clear vesicular fluid as well as an invaginated scolex. Brain parenchyma in this phase presents almost no inflammatory reaction to lesions and just creates a thin layer of collagen around the parasite. The cysticercoid can remain viable for several years or as a result of the immunologic attack of the host; it can progress into a degeneration process that transforms it into an inactive nodule. It is possible that the immune attack of the host occurs before the transformation of the metacestode inside the vesicular cysticerci. Independent of this, the metacestode or the vesicular cyst is in the first phase of the cysticerci evolution (colloidal phase), in which the vesicular liquid turns turbid and the scolex shows signs of hyaline degeneration. In this new phase, there is an intense mononuclear inflammatory reaction that includes the parasite itself. After this, the cyst wall will thicken, and the scolex will transform itself into a calcified granule. At this time point, the cysticercoid is no longer viable. This is the granular phase. Nevertheless,
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edema persists, and the adjacent astrocytes to lesions can even increase it. Finally, the remains of the parasite appear as a calcified nodule (calcified phase). By the side of the lesion, intense gliosis and the presence of multinuclear cells can be observed.1,11 Some cysticercoids have several membranes, which together resemble grape bunches. This presentation of the cysticercoids has been named racemose and has been observed in parasites localized in the basal cisterns.12 The mechanisms underlying these transformations are not completely clear, but it has been suggested that the vesicle begins to grow and the scolex disappears as the result of a degenerative process named hydropic degeneration.
NEUROIMAGING OF NEUROCYSTICERCOSIS The different pleomorphism of this illness generates differences with respect to the number and location of lesions as well as severity of the host immune system to the parasite. According to frequency, location, evolution, and treatment, the standard appearance of cysticerci can be divided in the following way: brain parenchyma, subarachnoid space, ventricular, spine channel, occular, and extraneural.11 The inflammatory reaction associated to neurocysticercosis is complex and has not been completely studied. Inflammation is necessary to reduce the size of the lesion and as part of the death process of the parasite, but at the same time, it is associated to shortand long-term complications. In parenchymal neurocysticercosis, the inflammation around the parasite is the principal cause of convulsions and occurs regularly in calcified and cystic degenerative lesions. The inflammatory reaction is minimal in the vesicular phase (viable) but varies in intensity in each patient in the moment the cystic degeneration is present. When the parasites appear out of the parenchyma, inflammation of CSF is frequent and intense, which conditions to arachnoiditis, ependymitis, vasculitis, and cranial pairs involvement.13
Parenchymal Neurocysticercosis The phase of development of the cysticercosis in brain parenchyma is determined by imaging studies. Cysticercosis in vesicular phase shows lesions with viable larvae sizes beside the scolex. These lesions can appear in 2 shapes—one in which lesions are small, round, with properly defined cysts, close to white and gray matter unions (mean size, 4–20 mm), and with a similar T1 and T2 values to that of CSF (Fig. 1)1; another that presents large cysts that can reach mean sizes of 10 cm—due to the absence of larvae inside the lesion and due to hidatidic transformations in which cystic membranes continue growing despite the absorption of the larvae.11 Lesions can also be found in the basal ganglia, cerebellum, and brainstem. The wall in these cases is thin; there is small or no peripheral edema as well as no posterior reinforcement due to the use of contrast agents. Plenty of the vesicular cysts have an eccentric or mural nodule inside, which represents the scolex and appears hyperintense in T1 and hypointense in T2 images and is considered as a pathognomonic sign called hole with dot. In case of doubt diffusionweighted imaging (DWI), apparent diffusion coefficient mapping can be useful to detect the scolex as a hyperintense nodule inside the vesicle. The scolex is the solid component of the structure, and therefore, it can be easily highlighted with DWI imaging.14 Cysticercosis in colloidal states shows degenerated larvae with turbid liquid and thick capsules. The cyst in degenerative phase can be seen as hyperintense in T1 and T2 imaging. In this phase, lesions are not well defined with peripheral edema. Most lesions show an ill-defined ring in the posterior
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FIGURE 1. Vesicular cysticercosis. A, Axial T1WI. B, Sagittal T1WI postcontrast. C, Axial CISS. D, Axial DWI. Note isointense lesion to cerebrospinal fluid, with the hyperintense scolex in DWI sequence (D). Note the eccentric scolex (blade) (D).
region (66% of cases). In some extraordinary cases, the scolex can be observed. Because of intense T2 signal, the scolex can be hidden. The mural module can be better observed with proton density contrast or using the fluid level-attenuated inversion recovery (FLAIR) sequence, in which it will appear as a hyperintense eccentric module inside the cyst (Fig. 2).15 As a differential diagnosis, the presence of lesions with 1 or more rings after contrast intake can be controversial, so other pathologies such as tuberculoma, cerebral abscess due to toxoplasmosis, primary cerebral neoplasms (glioblastoma), or secondary (metastasis) have to be considered as a possibility. For diagnostic imaging, we should use advanced sequences such as DWI, spectroscopy, or even perfusion-weighted imaging. Pyogenic abscess shows a hyperintense signal for DWI sequences; in contrast, neurocysticercosis cysts show a hypointense signal. A mature tuberculoma has a hypointense behavior for a T2 sequence. In toxoplasmosis, the location of the lesions is what has to be considered.14 In some cases, there are hypointense lesions in the center of the lesion and isointense lesions in the periphery, which can resemble tuberculomas, small abscess, and in some cases, metastasis. Some neurocysticercosis cysts show increased signal greater than the CSF, so that the behavior hyperintense on apparent diffusion coefficient maps by neurocysticercosis cyst may be useful in the differential diagnosis with an abscess.4 In vivo spectroscopy of neurocysticercosis shows cytosolic amino acid peaks (valine, leucine, and isoleucine), lactate (Lac), alanine, succinato/pyruvate, N-acetil-aspartato (NAA), creatinine (Cr), and choline (Cho). The NAA, Cr, and Cho peaks are thought to be due to the normal voxel contamination due to parenchyma signal. Pyruvate, a final product of glycolysis, can be metabolized through the aerobic path into acetate or through the anaerobic path to Lac in eukaryotic and parasitic organisms. This metabolite is © 2014 Lippincott Williams & Wilkins
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FIGURE 2. Colloidal cysticercosis. A, Axial T1WI postcontrast. B, Coronal T2WI. C, Sagittal FLAIR. D, Axial DWI. The cyst shows turbid fluid inside with thick wall and hyperintense signal on T2W image (B). Note brain edema (C) and scolex eccentric inside the lesion—colloidal stage (D).
predominant in racemose neurocysticercosis. The presence of pyruvate can be useful to differentiate between racemose neurocysticercosis and cystic gliomas (Fig. 3).4 The tuberculomas have a more elevated peak for lipids and Cho as well as smaller NAA and Cr peaks. The relation of Cho-Cr is larger than for all the tuberculomas, a ratio that changes for neurocysticercosis.16 Spectroscopy is useful for the cases of large cysticercosis without a visible scolex, as it can be used to differentiate them from a cerebral abscess or metastasis. In vivo, the succinate acetate peaks and Lac as well as the presence of keratin are dependent on the lesion being in the vesicular or colloidal phase. It has been described that the liquid obtained from cysts that starts degenerating lacks Cr. Meanwhile, vesicular cysts contain this metabolite because of the presence of muscular fibers in the scolex wall of the cysticercosis cyst.17 Neurocysticercosis is an entity that can generate lesions that resemble a pseudotumoral mass (gigantic cystic neoplasm),
FIGURE 3. Racemose neurocysticercosis. A and B, Sagittal and axial T1WI postcontrast. Observe multiple cysts in the right Sylvan fissure. © 2014 Lippincott Williams & Wilkins
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so it can be confused with a brain neoplasm (Fig. 4). Perfusionweighted imaging sequences can confirm whether a lesion is of the benign parasitic type as the brain blood volume is low, showing differences with respect to the different grades of neurovascularity that an astrocytoma can show.4,14 In the nodule-granular phase, the larvae dies, the cyst starts collapsing so the scolex starts calcifying, the capsule gets thicker, and less reinforcement in the ring can be observed as well as less perilesional edema. In computerized tomography (CT), the cysticercosis can be seen as a hyperdense nodule after contrast infusion, with small to no perilesional edema. In MRI, the most common is that the lesion is observed with no signal on T1 and T2, with hyperdense ring, thick, and secondary to peripheral gliosis. In other cases, this injury can be identified as isointense in T1 and hypointense on T2 hyperintense center. At this stage, differential diagnosis must be made with tuberculosis and metastasis (Fig. 5, 6). In the calcified phase, the lesion is completely mineralized with inactive response from the host. The CT is the most sensitive imaging technique for this phase. In it, the lesion will appear as a hyperdense nodule without evidence of an edema and without enhancement. When using MRI techniques, sequences sensitive to calcifications should be used. Examples of these are gradient echo or the susceptibility-weighted imaging sequence. These sequences show calcifications and areas with hemorrhage as hypointense. In general, there is no mass effect or anormal enhancement after contrast administration (Fig. 7). Anyway, in this phase, reactivation of neurocysticercosis has been described. In the calcified phase, it has been reported in some chronic lesions that show anormal enhancement or peripheral edema. In patients with recent epileptogenic activity, intermittent inflammatory changes have been reported as a response to the residual antigen that eventually is liberated or reorganized in the host, even during or after the cesticid therapy. The use of T1-weighted sequences can be a sensitive method in the degenerative phase.4,15,18
FIGURE 4. A, Sagittal T1WI. B, Coronal T2WI. C, Axial DWI. D, Macroscopic piece. Note CSF-like lesion in T1WI and T2WI, without evidence of scolex inside the lesion. www.topicsinmri.com
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FIGURE 5. Nodular-granular cysticercosis. A, Axial T1WI. B, Axial T2WI. C, Axial DWI. D, Axial gradient echo. Note adjacent lesion to sulcus parieto-occipital, in the nodular-granular phase. Observe the lesion slightly hyperintense on T1WI and hypointense on T2WI without edema (A and B). In the gradient echo sequence (D), the lesion shows hypointense signal.
3-dimensional constructive interference in steady state (3D-CISS) should be used (Fig. 9). On the other hand, lesions located in the Sylvain fissure or in the base cisterns usually have larger sizes, have a multilobulated appearance (like a bunch of grapes), displace neighboring structures, can behave as space-occupying lesions, and show low or null enhancement of the walls of each cyst. Multilobulated cystic lesions with the appearance of a bunch of grapes receive the name of racemose (Figs. 3, 10).14 For the cystic lesion cases due to neurocysticercosis localized in the pontocerebellar cistern, differential diagnoses of epidermoid cysts, arachnoid cysts, schwannoma, or cystic meningioma must be considered. In these cases, the behavior of the lesion has to be evaluated with a 3D-CISS and with DWI. The 3D-CISS sequence is used to evaluate lesions in the pontocerebellar angle and middle and internal ear and is a useful tool for the discrimination of lesions in ventricles, sulci, and intraventricular spaces. The 3D-CISS must be routinely used in the valuations of lesions by subarachnoid and ventricular neurocysticercosis as it helps to distinguish the walls of the cyst and the scolex (Fig. 11).4,13 Other finding of subarachnoid neurocysticercosis is hydrocephaly due to the occlusion of the Luschka and Magendie holes due to fibrosis arachnoiditis. This can be observed both with CT and MRI imaging and is seen as anormal enhancement of basal leptomeninges in the skull basis (Figs. 11, 12). Arteritis is observed in 53% of the subarachnoid neurocysticercosis cases.14 The most common cerebral complications can find infarction due to occlusion of the principal cerebral
Less Frequent Presentations Miliar neurocysticercosis and pseudotumoral presentation are 2 abnormal presentations of this illness. The miliar form represents a massive infestation of the CNS by cysticercosis and is characterized by several small cysts all over the cerebral parenchyma.4 Massive infestation can cause encephalitic and no encephalitic forms of this illness. Encephalitic neurocysticercosis is more frequent in children and women, which are infested by a large load of eggs of the Taenia solium. In this case, the immune system of the host reacts strongly against the parasites. Clinically, it behaves as acute encephalitis. When using imaging methods, diffuse edemas and compression of the ventricular system are seen. After contrast injection, several nodular or ring-shaped lesions are observed and are distributed all throughout the brain parenchyma. No encephalitic neurocysticercosis is more common with Taenia solium carriers that have developed tolerance to the immune response after invasion of the parasite in the CNS and has started showing chronic epilepsy trends. These patients show multiple vascular lesions apparently viable and without the presence of edema, similar to a “Swiss cheese” (Fig. 8).19
Subarachnoid Neurocysticercosis Cerebral cistern involvement is present in approximately 3.5% of neurocysticercosis cases. Frequently, the subarachnoid cysts are small, unique, or multiple; are localized inside the cerebral sulci; and look similar to those observed in the cerebral parenchyma. These lesions can be difficult to detect because of the similar signal intensity of the cyst liquid content and the CSF. At the same time, the cyst wall is detected in rare occasions, the scolex cannot be seen, and postcontrast enhancement is almost negligible. Because of these factors, sequences such as FLAIR or
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FIGURE 6. Nodular-granular cysticercosis. A, Axial T1WI postcontrast. B, Axial T2WI. C, Axial gradient echo. D, Axial DWI. Different stages of cysticerci in the brain. Observe the lesions in both parietal in the nodule-granular phase, less postcontrast enhancement, and perilesional edema null. On T2WI, gradient echo and susceptibility-weighted imaging, hypointense signal is noted in these same 2 lesions. © 2014 Lippincott Williams & Wilkins
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FIGURE 7. Calcified cysticercosis. A, Axial CT scan. B, Axial T1WI. C, Axial gradient echo. D, Axial T2WI. Note multiple calcified lesions of small size, without peripheral edema.
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FIGURE 9. Cysternal cysticercosis. A, Axial T1WI postcontrast. B, Axial T2WI. C, Axial CISS. D, Axial DWI. Axial CISS image demonstrates multiple cysts in the basal cisterns (superior cerebellar, ambiens, and suprasellar). Note multiple cysts within the larger lesion, located rostral to the left temporal horn, with eccentric scolex presence (C and D).
arteries (most frequent in the medial cerebral artery), reported between 4% and 6% with any kind of active neurocysticercosis (Fig. 13). These infarctions are associated with the inflammatory reaction that subarachnoid cyst lesions generate (particularly those located in the supraselar ventricle) or, secondary to the arachnoiditis, is observed in the ventricles of the base that at the same time affects the prefrontal basal vessels. Endarteritis should also be considered to be generated by cyst destruction secondary to medical management.1 Endarteritis due to cysticercosis causes severe endothelial disruption that can produce edema and thrombosis and the formation of fusiform aneurisms due to the weakness of affected vessel walls.
FIGURE 8. A, Axial T1WI. B, Axial T2WI. Note multiple vesicular lesions without evidence of edema, similar to Swiss cheese (courtesy of Dr Enrique Palacios, Tulane University School of Medicine, Louisiana). © 2014 Lippincott Williams & Wilkins
FIGURE 10. Racemose neurocysticercosis. A, Axial T1WI postcontrast. B, Coronal T2WI. C, Axial CISS. D, Axial DWI. Observe lesions located within the left Sylvian fissure: larger, multilocular (like cluster of grapes) lesions, which simulate space-occupying lesions. These lesions show no or little reinforcement in the walls of each cyst. www.topicsinmri.com
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FIGURE 13. Vascular complications of neurocysticercosis in a patient aged 11 years. A, Axial T1WI postcontrast. B, Axial DWI. Note the granular nodular lesion lateral to the left putamen and infarction in the territory of the ipsilateral posterior cerebral artery (courtesy of Dr Pilar Dies Suarez, Imaging Department, Hospital Infantil de Mexico Federico Gomez).
FIGURE 11. Subarachnoid cysticercosis and arachnoiditis. A, Axial T1WI. B, Axial CISS. C and D, Axial and sagittal T1WI postcontrast. Observe multiple cysts within basal cisterns and signs of arachnoiditis, more evident in the cistern quadrigerminal (D).
Arteritis due to cysticercosis affects the small- and mediumsized vessels, and on average, 50% of the patients find themselves affected by arachnoiditis.5
Ventricular Neurocysticercosis This is the second most common location (54% of the cases). This variant can appear isolated but, nevertheless, can be
FIGURE 12. Subarachnoid cysticercosis and arachnoiditis. A, Axial CT scan. B-D, Axial, sagittal, and coronal T1WI postcontrast. Observe the reinforcement in the various cisterns of the base.
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associated to parenchyma involvement (24% of the cases) and the subarachnoid.14 It usually affects the ventricle IV (54%– 64%), followed by the ventricle III (23%–27%), the lateral ventricles (11%–14%), and the Sylvain aqueduct (9%) (Fig. 14).4 Ventricular cysticercosis appears in CT imaging as hypodense lesions that distort the ventricular system causing asymmetric obstructive hydrocephaly. In the vesicular phase, vesicular cysts are isodense as well as the CSF, so they are difficult to determine using this technique. On the other hand, most of these lesions can be easily valuated using MRI because of the liquid properties of the liquid inside the vesicles or cysts as well as the scolex, different to those of the CSF (Fig. 15). In some occasions, the cyst is slightly more hyperintense than the CSF when using the FLAIR sequence, and it can show reinforcement after contrast perfusion. In some cases, the use of the sign of the ventricular signal can be useful for differential diagnosis. In it, motion of the cyst inside the ventricular cavity as a response to head motion is studied.20 For other patients, the presence of parasite membranes inside the ventricle or ventriculitis, secondary to the Monro hole occlusion, can be identified. Asymmetric dilation can also be detected of the posterior ventricle after ventricle shunt installation. Double-behavior hydrocephaly exists, where the fourth ventricle is isolated from the
FIGURE 14. Ventricular cysticercosis. A and B, Axial FLAIR. Note dilated supratentorial and infratentorial ventricular system with transependymal migration in a female patient aged 11 years. Observe the dilatation of the ventricles III and IV (courtesy of Dr Pilar Dies Suarez, Imaging Department, Hospital Infantil de Mexico Federico Gomez). © 2014 Lippincott Williams & Wilkins
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Sellar Neurocysticercosis Neurocysticercosis is described as the direct involvement of the sella by a vesicle. Twenty-three cases have been described in the literature, with involvement in ophthalmic disorders in 67% of patients and endocrine disorders in 57% of patients.21 This type of injury usually involves the pituitary and moves, compresses, and sometimes, destroys the pituitary stalk or the pituitary itself. This injury may be accompanied by hydrocephalus, involucre subarachnoid cisterns of the base, and chiasmatic arachnoiditis (Figs. 12, 16). As a differential diagnosis, a vesicle by neurocysticercosis may behave like an arachnoid cyst, pituitary adenoma with cystic degeneration, Rathke cleft cyst, epidermoid cyst, sellar craniopharyngioma, or granuloma.21,22
Neurocysticercosis in the Spine FIGURE 15. Intraventricular cysticercosis. A, Sagittal T1WI. B and C, Sagittal and axial CISS. D, Axial DWI. Observe the cystic lesion in the ventricle IV with eccentric scolex presence.
others, due to the presence of granular ependymitis and due to the occlusion of the cerebral aqueduct as well as simultaneous arachnoiditis that blocks the Luschka and Magendie holes. Ependymitis is identified as a hyperintense signal in T2 images at the ependyma level and subependimo as well as increasing contrast of the ventricular wall after infusion of contrast agents.14,19 For these patients, it might be important to install 2 independent derivation systems: one will drain the supratentorial ventricular system; and the other will drain the ventricle IV, which is isolated.1
Orbital Neurocysticercosis Orbital neurocysticercosis appears in a mean of 3% of the cases. The parasites in the ocular ball can affect the anterior and posterior camera and even the subconjunctival region.19 Cysticercosis affects the eye orbit through the choroid vessels localized in the subretinal level.4 After some time, the cysticercoids will need more space and will induce retinal spill and invasion of the vitreous. When using MRI, the parasite looks hyperintense in T1 and hypointense in T2; because of that, it can be confused with a choroid melanoma. Some of the differential diagnostics could be retinoblastoma in pediatric patients and metastasis in adult patients.19 The involvement of an extraocular muscle is the most common case of orbital neurocysticercosis, appearing as myositis. Involvement of the optical nerve is extremely rare but may occur through the hematogen way by branches of the central artery of the retina.4
FIGURE 16. Sellar cysticercosis. A, Sagittal CISS. B, Axial T1WI postcontrast. Note the destruction of the pituitary, coupled condition of the basal cisterns (A). Observe the increased size of the infundibulum sellar and its pathological enhancement (B). © 2014 Lippincott Williams & Wilkins
Spinal cord involvement is unusual and is reported for 1.2% to 5.8% of patients with neurocysticercosis. The appearance in the leptomeningeal (extramedullar) is 6 to 8 times more common than in the intramedullar (0.77%). Extradural presentation is even less common. Intramedullary cysticercosis may occur by hematogenous spread of infection outside the CNS, through the artery of Adamkiewicz.4,23 The low flux of the spinal cord, the type of vascularization of the cord (small caliber and pressure vessels), and the presence of spinal medulla contribute to the low number of intramedullary cases. It is usual to find cysts in the thoracic segment, as this is the region of the spinal cord that receives the higher fluxes (67%), followed by cervical and lumbar.25 The intradural-extramedullar involvement can be due to the scatter of the larvae from the brain to the subarachnoid space of the spine (Fig. 17).4 The MRI, when studying this form of neurocysticercosis, has displaced myelography, as well as CT. In MRI, the
FIGURE 17. Intradural spinal cysticercosis. A and C, Sagittal postcontrast T1WI. B and D, Sagittal and axial T2WI. Identify cystic lesions in intradural-extramedullary situation leading to spinal cord compression. Note syringomyelic cavity. www.topicsinmri.com
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2. Sorvillo F, Wilkins P, Shafir S, et al. Public health implications of implications of cisticercosis acquired in the United States. Emerg Infect Dis. 2011;17:1–6. 3. Más-sesé G, Vives-Pñera I, Fernández-Barreiro A, et al. A descriptive study of neurocysticercosis in a tertiary care hospital. Rev Neurol. 2008;46:194–196. 4. do Amaral LLF, Ferreira RF, da Rocha AJ, et al. Neurocysticercosis. Evaluation with advanced magnetic resonance techniques and atypical forms. Top Magn Reson Imaging. 2005;16:127–144. 5. Marquez JM, Arauz A. Cerebrovascular complications of neurocysticercosis. Neurologist. 2012;18:17–22. 6. Fleury A, Moreno García J, Valdez Aguerrebere P, et al. Neurocysticercosis, a persisting health problem in Mexico. PLoS Negl Trop Dis. 2010;4:e805. 7. Ridaura-Sanz C. Hosp response in childhood neurocysticercosis. Childs Nerv Syst. 1987;3:206–207. 8. Del Brutto. Neurocysticercosis in children: clinical, radiological and prognostic factors in 54 patients. Neurol Rev. 1997;25:1681–1684. 9. Ruiz-Garcia M, González-Astiazarán A, Rueda-Franco A. Neurocysticercosis in children. Clinical experience in 122 patients. Childs Nerv Syst. 1997;13:608–612.
FIGURE 18. Intramedullar cysticercosis. A, Axial T1WI. B, Axial T1WI postcontrast. C and D, Coronal and axial T2WI. Observe the intramedullary lesion, at the granular nodular stage, with peripheral rim enhancement (B).
intramedullar cysticercosis is identified as a round or septed isointense to CSF lesion in T1 and T2 sequences. They can present as an eccentric hyperintense nodule in relation with the scolex. Cyst periphery can reinforce, secondary to reinforcement from cystic wall or rupture of hematoencephalic barrier (Fig. 18). Spinal cord presents expansion and local edema. There is marked thickening and intense inflammatory reaction, suggesting fibrosis focal pachymeningitis.11,19,24 If the scolex cannot be identified, other differential diagnostics should be considered such as neoplasms (astrocytoma vs cystic ependymoma), inflammatory origin, demyelination, vascular, or granulomatous.1,19 Leptomeningeal cysts are easy to identify. These lesions are mobile and can change positions with relation to the patient during an imaging study.1
CONCLUSIONS Host immune response and the disease pleomorphism continue to exert a factor of interest in the study of neurocysticercosis. Using advanced sequences and noninvasive MRI, great progress contributes to the detection of the different stages of the disease, scolex detection, identification of lesions in the subarachnoid space, and better evaluation of the differential diagnoses.
10. Escobar A. The pathology of neurocysticercosis. In: Palacios Palacios E, Rodríguez-Carbajal J, Taveras JM, eds. Cysticercosis of the Central Nervous System. Springfield, IL: Charles C. Thomas; 1983:27–54. 11. Salgado P, Rojas R, Sotelo J. Cysticercosis. Clinical and classification based on imaging studies. Arch Intern Med. 1997;22:1991–1997. 12. Pittella JEH. Neurocyscitercosis. Brain Pathol. 1997;7:681–683. 13. Carpio A, Fleury A, Hauser WA. Neurocysticercosis. Five new things. Neurol Clin Pract. 2013;3:118–123. 14. Abdel-Razed AAK, Watcharakorn A, Castillo M. Parasitic diseases of the central nervous system. Neuroimaging Clin N Am. 2011;21:815–848. 15. Lucato LT, Guedes MS, Sato JR, et al. The role of conventional MR imaging sequences in the evaluation of neurocysticercosis: impact on characterization of the scolex and lesion burden. AJNR Am J Neuroradiol. 2007;28:1501–1504. 16. Pretell EJ, Martinot C Jr, Garcia HH, et al. Differential diagnosis between cerebral tuberculosis and neurocysticercosis by magnetic resonance spectroscopy. J Comput Assist Tomogr. 2005;29:112–114. 17. Gupta RK, Jobanputra KJ, Yadav A. MR spectroscopy in brain infections. Neuroimaging Clin N Am. 2013;23:475–498. 18. Poeschl P, Janzen A, Schuierer G, et al. Calcified neurocysticercosis lesions trigger symptomatic inflammation during antiparasite therapy. AJNR Am J Neuroradiol. 2006;27:653–655. 19. Del Brutto O, Campos X. Massive neurocysticercosis: encephalitic versus non-encephalitic. Am J Trop Med Hyg. 2012;87:381. 20. Garcia HH, Del Brutto O. Imaging findings in neurocysticercosis. Acta Trop. 2003;87;71–78. 21. Del Brutto OH, Del Brutto VJ. Intrasellar cysticercosis: a systematic review. Acta Neurol Belg. 2013;113:225–227.
ACKNOWLEDGMENT The authors thank medical doctors Fernando Robles Ramirez and Salomon Israel González Dominguez for their collaboration in the recollection and selection of clinical cases.
REFERENCES 1. Del Brutto O. Neurocysticercosis. Continuum Lifelong Learn Neurol. 2012;18:1392–1416.
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22. Arriada-Mendicoa N, Celis-López MA, Higuera-Calleja J, et al. Imaging features of sellar cysticercosis. AJNR Am J Neuroradiol. 2003;24:1386–1389. 23. Del Brutto OH, Garcia HH. Intramedullary cisticercosis of the spinal cord: a review of patients evaluated with MRI. J Neurol Sci. 2013;331:114–117 24. Moharty A, Venkatrama SK, Das S, et al. Spinal intramedullary cysticercosis. Neurosurgery. 1997;40:82–87. 25. Muzumbar D, Nadkarni T, Desai K, et al. Thoracic intramedullary cysticercosis. Two cases reports. Neurol Med Chir. 2002;42:575–579.
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