Abstract
BACKGROUND AND PURPOSE: Various MR techniques have been used to assess CSF flow and to image the subarachnoid spaces and ventricles. Anecdotal reports describe the use of intrathecal and intraventricular gadolinium-based contrast agents in humans and animals. We sought to determine the clinical usefulness of gadolinium-enhanced MR ventriculography for assessing CSF flow in patients with various neurologic conditions.
METHODS: Five patients (three female and two male patients aged 6 months to 65 years) were included in the study. After performing sagittal, coronal, and axial T1-weighted MR imaging of the brain, 0.02–0.04 mmol of gadodiamide was injected into the lateral ventricle. Sagittal, coronal, and axial T1-weighted imaging was repeated soon after the injection. We were specifically looking for the site of obstruction to CSF flow in those patients with hydrocephalus, communication between cysts and ventricles, elucidation of suspicious intraventricular lesions, and patency of third ventriculostomies.
RESULTS: MR ventriculography showed good delineation of the ventricular system in all patients. In one patient with carcinomatosis and hydrocephalus, a block to contrast material flow was detected at the right foramen of Luschka. In another patient with hydrocephalus, partial block to the flow of contrast material was demonstrated at the right foramen of Monro. In a patient with hydrocephalus and a posterior fossa cyst, flow of contrast material was blocked between the third ventricle and the cyst, with a thin streak of contrast material in the aqueduct. As an assessment of the patency of a third ventriculostomy, MR ventriculography showed flow of contrast material into the suprasellar cisterns from the third ventricle in one patient and absence of flow in another.
CONCLUSION: MR ventriculography is a safe technique for assessing CSF flow, with application in determining the site of obstruction in hydrocephalus, in assessing communication between cysts and the ventricle, and in determining the functioning status of endoscopic third ventriculostomies.
Both conventional spin-echo MR imaging and directional flow determination with cine phase-contrast MR imaging have been used to describe flow of CSF in the brain, in a variety of clinical situations (1–10). These studies are noninvasive; however, the spin-echo techniques are less accurate and the cine format when used alone is subjective. The addition of velocity measurements in the phase-contrast technique has improved the accuracy (11, 12). Recently, the 3D constructive interference in steady-state (CISS) sequence has been used for evaluating intraventricular lesions (13). The usefulness of MR imaging with intraventricular or cisternal injections of a gadolinium-based contrast agent to study CSF flow has been reported in animals and humans (14–19). The purpose of our study was to determine the value of MR ventriculography as an adjunct to routine imaging in determining the functional status of third ventriculostomies, in assessing communication between cysts and the ventricles, and in determining the site of CSF block in noncommunicating hydrocephalus.
Methods
We studied five, nonconsecutive patients (three female and two male patients; age range, 6 months to 49 years) with the MR ventriculographic technique between June 2001 and November 2002. All patients and families were explained that this was a new technique with certain risks of central nervous system injury, infection, and contrast material reaction. Permission was obtained from the Fluid Research Grant Committee, Christian Medical College Hospital, Vellore, India, to study the technique. All patients underwent either CT or MR imaging to establish the clinical diagnosis. On the morning of the procedure, an external ventricular drain was inserted into the right frontal horn in the intensive care unit. Subsequently, routine MR imaging was performed and consisted of sagittal, coronal, and axial T1-weighted images. Gadodiamide ([1 mL containing 287 mg, 0.5 mmol/mL] Omniscan; Nycomed Ireland Ltd, Cork, Ireland) was diluted (1:50) to a concentration of 0.01 mmol/mL. Two milliliters of CSF was withdrawn by the external ventricular drain, and 2–4 mL of the 1:50 diluted gadodiamide solution (0.02–0.04 mmol) was injected into the ventricle, following which sagittal, coronal, and axial T1-weighted imaging was repeated. The sagittal images were obtained in the prone position for the two patients who had undergone third ventriculostomy. In all patients, the head was gently rotated from side-to-side to allow uniform distribution of the contrast agent. Two patients underwent MR ventriculography while under general anesthesia and were then transported to the operating room while under the same anesthesia for the definitive intracranial procedure.
MR ventriculography was performed with a 0.5-T Gyroscan TS-NT MR imager (Phillips Medical Systems, Best, the Netherlands), with the following parameters: 2D spin-echo sequence was routinely performed with 475/18/1 (TR/TE/NEX), 6-mm section thickness, 0.6-mm section gap, and 90° flip angle.
Results
Patient 1 was a 65-year-old woman who presented with headache and lethargy of 2 months’ duration. She had neck stiffness. Contrast material-enhanced CT of the brain showed right frontal and left cerebellar contrast-enhancing tumors with ventriculomegaly (Fig 1A–C). The differential diagnosis was tuberculoma or metastatic tumor. The locations of the tumors did not explain the presence of the hydrocephalus, which included dilatation of the lateral, third, and fourth ventricles. Therefore, the possibility of a carcinomatous meningitis or meningitis due to tuberculosis was considered as a cause of the hydrocephalus. Her sensorium, which continued to deteriorate after admission, improved with external ventricular drainage. To ascertain whether this was a communicating or noncommunicating hydrocephalus, MR ventriculography was performed. The MR ventriculogram demonstrated free communication among the lateral, third, and fourth ventricles (Fig 1D–F). However, while contrast material exited the fourth ventricle via the left foramen of Luschka and foramen of Magendie, no contrast material could be seen in the right foramen of Luschka (Fig 1G and F). The next day, a CT-guided stereotactic biopsy was performed of the right frontal mass, and the findings were reported as metastatic adenocarcinoma. Carcinomatous meningitis was concluded to be the cause of the basal arachnoiditis, and the external ventricular drain was converted to a ventriculoperitoneal shunt. The patient was advised to undergo radiation therapy.
Patient 2 was a 9-year-old girl who presented with headache, vomiting, and two episodes of decerebration of 1 week’s duration. She had papilledema with no lateralizing neurologic deficits. The CT scan of the brain showed dilatation of all ventricles (Fig 2A). A suspicious lesion was noted in the fourth ventricle, raising the possibility of a fourth ventricular cysticercus cyst causing the hydrocephalus (Fig 2B). The sagittal MR ventriculogram showed evidence of a syrinx in the cervical and thoracic cord with no tonsillar herniation (Fig 2E). At MR ventriculography, contrast material injected into the right frontal horn demonstrated a partial block to the flow of CSF at the right foramen of Monro despite turning the head 90° to the left to present the contrast material to that region (Fig 2C–E). To determine if the left foramen of Monro was patent, we inserted a left frontal ventricular catheter and injected 4 mL of contrast material into the left frontal horn. The time gap between the studies was 100 minutes. The repeat MR ventriculography showed good flow of contrast material from the left lateral ventricle through the foramen of Monro into the third ventricle. Contrast material from the first injection into the right frontal horn was now more uniformly distributed (Fig 2F–H). It is possible that the layered contrast material in the right lateral ventricle had now diffused more uniformly or that contrast material injected into the left frontal horn refluxed up into the right frontal horn from the third ventricle. There was no obvious lesion within the fourth ventricle. No contrast material was seen exiting the fourth ventricle, and no communication was noted between the fourth ventricle and the cervical syrinx. The patient was taken to the operation room, and a left frontal burr hole was placed. Third ventriculostomy was performed after negotiating the endoscope through the patent left foramen of Monro. In addition, fenestration of the septum pellucidum was performed to establish communication between the lateral ventricles, thus providing drainage for the right lateral ventricle.
The third patient was a 6-month-old girl who presented with an enlarging head since birth. The CT scan of the brain showed hypoplasia of the vermis with a large posterior fossa cyst. There was dilatation of the third and lateral ventricles. MR ventriculography (Fig 3) demonstrated intense contrast in the left lateral ventricle and third ventricle, with contrast of less intensity in the right lateral ventricle (Fig A–C). A thin trickle of contrast material was seen entering the cerebral aqueduct, indicating an aqueductal narrowing (Fig 3A and D). Therefore, shunt tubes were placed in the posterior fossa cyst and in the lateral ventricle (ventriculocystoperitoneal shunt). In this case of a Dandy-Walker malformation, MR ventriculography clearly demonstrated that there was an associated aqueductal stenosis; this information helped in the surgical decision-making process.
Patient 4 was an 8-year-old boy who presented with headache and vomiting of 3 months’ duration. He had bilateral papilledema, sixth nerve palsies, and cerebellar signs. A CT scan of the brain showed an enhancing midline posterior fossa mass causing hydrocephalus. Since he was symptomatic and time was not available on the elective operating list for removal of the posterior fossa mass, an endoscopic third ventriculostomy was performed. Although he had complete relief of raised intracranial symptoms, a subgaleal collection of CSF at the burr-hole site after 5 days prompted us to ascertain patency of the third ventriculostomy. He was scheduled for posterior fossa surgery the next day, and MR ventriculography was planned while the patient was under the general anesthesia for surgery. MR ventriculography demonstrated that the third ventriculostomy was not functioning (Fig 4). The patient was taken directly to the operation room. Intraoperatively, the tumor had not infiltrated the floor of the fourth ventricle, and after radical excision, the cerebral aqueduct was completely open with free flow of CSF. The biopsy findings were reported as medulloblastoma. The postoperative contrast-enhanced CT scan (Fig 4F) showed no residual tumor. He was given a course of postoperative craniospinal radiation therapy.
The fifth patient was a 49-year-old man who presented with headache and neck pain for 3 months’ duration. There was papilledema, bilateral sixth nerve palsies, and cerebellar signs with no lower cranial nerve palsies. MR imaging showed a midline cyst in the posterior fossa with a solid, enhancing component at C1–2, causing hydrocephalus. After third ventriculostomy, symptoms of raised intracranial pressure were relieved. MR ventriculography performed 6 days later (Fig 5) demonstrated a functioning third ventriculostomy. He underwent total excision of the mass, which was reported to be a cystic neurofibroma at histopathologic examination.
Discussion
Special radiologic studies are required to assess relative or absolute obstruction to CSF flow in various clinical conditions. Assessing communication between cysts and the ventricular system, patency of third ventriculostomies, and the site of obstruction in obstructive hydrocephalus, as well as detection of intraventricular cysticerci has relevance in directing appropriate therapy. Although conventional x-ray ventriculography (20), metrizamide CT ventriculography or cisternography, and isotope cisternography (21) are relatively inexpensive, their poor spatial resolution, lack of multiplanar imaging capability, and exposure to radiation are drawbacks.
With the introduction of MR imaging, newer techniques for assessing flow without these disadvantages were possible. These included CSF flow studies by using spin-echo sequences, cine phase-contrast MR imaging for directional flow determination, and the 3D Fourier transform sequence, CISS (1–8, 10–12, 21–23). Jack and Kelly (6), in an assessment of third ventriculostomy patency, described a CSF flow void in the floor of the third ventricle on T2-weighted images. Although this could signify rapid, turbulent flow through a perforation, the presence of the basilar artery in the vicinity of the expected third ventriculostomy flow void made interpretation difficult, with false-positive results. Moreover, they found that the absence of a flow void did not preclude adequate function, as the use of flow-compensation techniques may have yielded the false-negative results.
Subsequently, cine 2D phase-contrast MR imaging methods were used to assess CSF flow and patency of third ventriculostomies. Lev et al (3) used a cine phase-contrast MR imaging technique to measure actual flow velocities and velocity ratios between the third ventricular floor and cervical subarachnoid space in six patients with third ventriculostomies and 12 control subjects. They found higher velocities at the third ventricular floor and prepontine cistern in the patients compared with velocities in the control subjects, indicating a patent ventriculostomy. However, even in the control subjects, flow was detectable in the floor of the third ventricle. Therefore, modest flow in the region is inconsequential and does not indicate patency of the third ventriculostomy. This was corroborated by Fukuhara et al (8) who compared cine phase-contrast MR imaging and direct endoscopic exploration of the third ventriculostomy orifice in 12 patients. In five patients with no flow on phase-contrast MR images, the ventriculostomies were closed with a membrane or clot. However, in four patients in whom flow was considered “subtle” before exploration, all had membranes across the orifice, requiring fenestration.
Compared with the standard MR images, a 3D Fourier transform sequence—CISS—produces greater detail of the ventricular system and basal cisterns, with excellent CSF-to-brain contrast and superior spatial resolution (22, 23). Moreover, this technique may define cyst walls and septations better since the adjacent flow patterns can enhance the visualization of these septations. Govindappa et al (13) found CISS more sensitive and specific than routine spin-echo sequences in the diagnosis of intraventricular cysticercal cysts. Aleman et al (23) used the CISS technique with T2-weighted imaging before and after fenestration procedures for loculated or multiloculated hydrocephalus, aqueductal stenosis or obstruction, and intracranial cysts by using a flexible endoscope in 14 consecutive patients. The preoperative CISS images demonstrated intracystic and intraventricular septa not observed with conventional T2-weighted imaging in 11 of 15 procedures. Both CISS and T2-weighted imaging demonstrated flow voids through third ventriculostomies. Although CISS could clearly demonstrate the fenestration performed for six of nine intracranial cysts, no flow void through the fenestration was observed. This was possibly because the pressure gradient between cysts and ventricle was too small to produce a high CSF flow and flow voids.
The use of slow-flow pulse sequences based on a 3D steady-state free precession (SSFP) scheme with additional gradient pulses in the read-out axis provides a very high sensitivity to fluid motion, down to flow velocities of 0.5–1.0 mm/s in phantom studies (24). This sequence has provided valuable information on CSF flow in head and spine disorders (24, 25). In the assessment of spinal stenosis, the slow-flow sequence detected a distinct flow pattern in high-grade stenoses; however, in intermediate- and low-grade stenoses, it was less reliable (25). These flow sensitive and diffusion-weighted MR imaging sequences were useful in the study of clinically suspected CSF leaks (26). In the evaluation of 24 sacral meningeal cysts, Davis et al (24) found that flow sensitive MR imaging was useful in detecting communication between the cysts and the subarachnoid space in those patients who were symptomatic, whereas the asymptomatic cysts were noncommunicating. The CISS technique is not readily available and is dependent on a correct gradient strength.
The technique of MR ventriculography involves the acquisition of T1-weighted sequences after injection of a gadolinium-based contrast agent into the ventricles (MR ventriculography) or into the lumbar subarachnoid space (MR cisternography). There have been a few reports showing that the technique is safe and provides accurate information regarding obstruction to CSF flow (14–19). In studies on rats by Ray et al (17, 18), gadopentetate dimeglumine and gadodiamide or caldiamide at low doses adequate for imaging purposes, caused no histologic or behavioral changes. In another study by Skalpe and Tang (19), who used these two preparations of gadolinium-based contrast agents in eight pigs, marked enhancement of the CSF was obtained with concentrations from 10 to 0.625 mmol/L. They concluded that both these gadolinium-based compounds were remarkably well tolerated in the subarachnoid space and in doses relevant for imaging purposes; no adverse effects were seen. Siebner et al (14) reported on two cases of leptomeningeal carcinomatosis studied with MR ventriculography with use of 0.01 mmol of gadopentetate dimeglumine. They found excellent contrast between ventricular CSF and brain and a high safety index. Zeng et al (16) performed MR cisternography with intrathecal lumbar injection of gadopentetate dimeglumine at doses ranging from 0.1 to 0.5 mmol in 11 patients. No complications were noticed in any of the 11 patients during a 9–15 month follow-up. The imaging was helpful in identifying disk herniation, posttraumatic spinal stenosis, postsurgical noncommunicating cyst, myelitis, intradural extramedullary mass, and vascular malformation.
In our report of five patients, we evaluated the usefulness of MR ventriculography in an assortment of clinical situations. MR ventriculography showed unequivocal block at the foramen of Luschka in the first patient, evidence of patency of third ventriculostomy in the fourth patient, and a nonfunctioning ventriculostomy in the fifth patient. It also showed a lack of communication between dilated ventricles and a posterior fossa cyst in the third patient and partial obstruction at the right foramen of Monroe in the second patient. In these latter two patients, the surgical procedures performed were based on the imaging findings. The administration of intraventricular contrast material in such low doses (0.02–0.04 mmol giving a dose of 0.01–0.02 mmol/g of brain) appears to be safe, and no complications occurred after its use in our study.
The primary advantage of MR flow studies and flow sensitive sequences over MR ventriculography is related to the potential for repeated imaging for follow-up studies since they are noninvasive. MR ventriculography, being invasive, would primarily find its use for diagnostic purposes, aiding in clinical decision making. In the case of intermittent obstructions to flow, assessment of ventricular or cyst wall compliance and the possible detection of one-way or bidirectional flow, SSFP studies would be advantageous.
CT cisternography has been shown to predict surgical outcome in patients with normal-pressure hydrocephalus; patients with persistent ventricular stasis had an unsatisfactory response to shunt surgery (27). Radionuclide CSF flow studies have been used in assessing CSF flow patterns in the spinal and cranial subarachnoid spaces. These findings were used to predict homogeneous distribution of intrathecal chemotherapy for patients with leptomeningeal metastasis (28). Unlike CT cisternography, MR ventriculography and MR cisternography do not have the problems related to radiation. Although radionuclide cisternography imparts a lower radiation exposure, it may involve a longer duration of examination. MR cisternography would therefore be a superior technique in the evaluation of ventricular stasis and in documenting CSF flow patterns for homogeneous distribution of intrathecal chemotherapy. Furthermore, with MR ventriculography, there is better delineation of adjacent soft-tissue characteristics, and it is possible to perform additional physiologic studies, such as cerebral blood flow and diffusion. Other applications of MR ventriculography and MR cisternography may include evaluation of CSF flow across the craniospinal junction in syringomyelia. In the evaluation of CSF dural fistulas, T2-weighted MR images have been found to be more sensitive than CT cisternography and radionuclide cisternography (25). The latter techniques deliver a high dose of radiation, are cumbersome and invasive, and in the absence of an active leak may have high false-negative rates. However, CT defines bone very well and would be a useful additional tool to detect bone defects in CSF dural fistulas and to describe bone anomalies at the craniovertebral junction. Further studies may indicate a role for MR cisternography in defining with greater detail the CSF pathways in relation to adjacent soft tissues, thus enabling detection of CSF dural fistulas.
Conclusion
Apart from the noninvasive MR flow studies available, MR ventriculography is a safe additional technique that may be used to ascertain patency of third ventriculostomies. It is likely to help in differentiating between intracranial cysts and enlargement of CSF spaces and in the assessment of intraventricular masses. MR cisternography can provide excellent detail of the contrast material pathways in relation to adjacent soft tissues and the ventricular system. Both MR ventriculography and MR cisternography maybe used in the setting of a routine MR imaging examination including T1-weighted, T2-weighted, diffusion, perfusion, and contrast-enhanced studies. We foresee the greater use of MR ventriculography or MR cisternography in understanding CSF flow dynamics in physiologic and pathologic states.
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