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Brain Tumors: Complications of Cerebral Angiography Accompanied by Intraarterial Chemotherapy¹

¹ From the Departments of Radiology (M.G., D.W.C.) and Neurology (H.B.N.), Ohio State University Medical Center, S-255 Rhodes Hall, 450 W 10th Ave, Columbus, OH 43210. From the 1998 RSNA scientific assembly. Received June 22, 1998; revision requested August 4; final revision received January 12, 1999; accepted March 26. Address reprint requests to D.W.C.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate the rate of complications associated with diagnostic cerebral angiography accompanied by intraarterial chemotherapy for the treatment of primary and metastatic brain tumors.

MATERIALS AND METHODS: Three hundred ninety-two consecutive transfemoral cerebral angiographic procedures accompanied by intraarterial chemotherapy were performed in 48 patients (28 men, 20 women), and complications were evaluated.

RESULTS: The most common local complications were groin hematomas, which occurred in 10 (2.6%) of the 392 procedures and none of which required therapy. Two carotid arterial dissections (0.5%) were reported in two patients who were asymptomatic and did not require further treatment. Both improved at follow-up examinations. Only one patient required surgery for a delayed popliteal embolus. Systemic transient complications occurred five times (1.3%). There were seven (1.8%) transient neurologic events, which were paresis and visual disturbances. Six (1.5%) transient seizure events were recorded. There were no permanent neurologic complications.

CONCLUSION: Intraarterial chemotherapy for brain tumors is a safe procedure with a low complication rate.

Index terms: Angiography, complications, 10.124, 10.441, 10.442, 10.445 • Brain neoplasms, 10.363, 10.38 • Brain neoplasms, therapy, 10.124, 10.1266 • Chemotherapeutic infusion, 10.1266 • Chemotherapy, complications, 10.1266, 10.441, 10.442, 10.445

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The management of and therapy for both primary and metastatic malignant brain tumors remain a difficult area of oncology (1–4). For most patients, the standard method of treatment has been a combination of surgery and irradiation. More recently, chemotherapy has begun to play an important role in brain tumor therapy (5). Although chemotherapy typically is administered intravenously, regional intraarterial administration may increase tumor uptake of drug, with improvement in efficacy and patient survival (6). The departments of neurology and radiology at our institution have established a dedicated brain tumor program in which many patients receive internal carotid and vertebral intraarterial chemotherapy (7,8). To our knowledge, however, the rate and severity of complications associated with these intraarterial chemotherapeutic procedures have not been evaluated systematically. Patients with brain tumors represent a special population, with a spectrum of medical problems and morbidity cofactors that differ from those in the types of patients previously described in the angiography literature (9–17).

We evaluated the complications in 48 patients in whom 392 consecutive diagnostic cerebral angiographic procedures with concomitant intraarterial chemotherapy were performed for the treatment of primary and metastatic brain tumors. Many of these patients underwent multiple procedures throughout their full course of treatment, far more than would be encountered in typical diagnostic angiography. To our knowledge, this type of analysis has not been performed previously in a cohort of patients with brain tumors. If intraarterial chemotherapy is to become a standard neuro-oncologic treatment approach, it is important to document its complication rate.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
From January 1995 through May 1997, 392 transfemoral cerebral angiographic procedures, accompanied by intraarterial chemotherapy administered through the cervical internal carotid and vertebral arteries, were performed and complications evaluated in 48 patients (28 men, 20 women; age range, 23–80 years; mean age, 50 years). All of the patients in the study were included in the intraarterial carboplatin (Paraplatin; Bristol-Myers Squibb, Princeton, NJ) and intravenous etoposide (Vepesid; Bristol-Myers Squibb) protocol for the treatment of primary or metastatic brain tumors, except one patient who was treated with an intraarterial methotrexate (Lederle, Carolina, Puerto Rico) protocol for primary central nervous system lymphoma. Patients who were undergoing blood-brain barrier disruption accompanied by intraarterial chemotherapy were excluded from this analysis. Each patient had measurable, enhancing tumor at the time of protocol initiation, which indicated substantial residual disease after surgery and irradiation or documented tumor progression. All of the procedures were performed under the direct supervision of a staff neuroradiologist at a single institution. Written informed consent in accordance with our institutional review board was obtained prior to the initiation of the protocol. Written informed consent was also obtained before each procedure.

All patients underwent baseline ophthalmologic and audiologic evaluations before the onset of treatment, as well as complete blood cell count, liver function, renal panel, and electrolyte tests. The protocol consisted of intraarterially infused carboplatin 200 mg/m²/d and intravenously infused etoposide 100 mg/m²/d on days 1 and 2 every 3–4 weeks; the majority of patients were on a 4-week cycle. A white blood cell count above 2,000/mm³ and a platelet count above 100,000/mm³ were the goals before the performance of each procedure, though a few patients did not meet these goals. Follow-up ophthalmologic and audiologic examinations were performed every two cycles.

At the first examination only, most patients were evaluated with arch aortography followed by biplane angiography of the territories to be treated. The arch aortogram was obtained to define the anatomy of the arch and to avoid potential complications. The selection of the vessel to be treated was made by the neuro-oncologist (H.B.N.) on the basis of the predominant vascular supply of the tumor as judged from magnetic resonance images or computed tomographic scans obtained every 8 weeks or as needed. One vascular territory would be treated the 1st day, and a second territory would be treated the following day. We never encountered primary vascular disease (ie, aneurysm or stenosis) to a degree that prevented us from performing chemotherapeutic infusion. We did encounter a few noncritical carotid bifurcation plaques that were traversed.

Internal carotid diagnostic angiograms were completed initially, followed directly by intraarterial chemotherapeutic infusions. To avoid potential carotid dissections, this approach was altered to a diagnostic common carotid injection, followed by fluoroscopic documentation of internal carotid position for the infusion of the chemotherapeutic agent. After the initial biplane study, only a single-plane diagnostic angiogram was completed at subsequent examinations for documentation. For the carotid territory, after evaluation of the anatomy, the catheter was placed at approximately the C4-5 through C1-2 level for the infusion. In patients with high-risk abnormalities (ie, stenosis, aneurysm of the cervical internal carotid artery), the level of catheter placement was variable. For the vertebral injections, the catheter was placed approximately at the C4 to C7 level. If possible, the dominant or ipsilateral vertebral artery to the lesion was chosen.

All of the patients received 5–10 mg of orally administered diazepam (Mylan Pharmaceuticals, Pittsburgh, Pa) on-call to the angiography suite. The examinations were all performed by means of the transfemoral approach. An attempt usually was made to alternate between the right and left groin for the 2-day protocol, except in a few of the early patients in whom a 5-F vascular sheath was left in the femoral artery overnight. Use of the sheaths was discontinued to avoid possible complications, including hemorrhage, thrombosis, patient discomfort, and infection. An additional factor was the increased patient care involved, considering that at our institution, patients who have arterial catheters cannot be observed in a standard hospital room. In some patients, one groin was used predominately owing to venous thrombosis problems, lack of a good contralateral pulse, or patient preference.

Standard catheter and guide wire techniques were used. Various catheters were used, including 5-F standard pigtail, JB1, JB2, Berenstein, H1H, and Simmons catheters (Cook, Bloomington, Ind). The catheters were flushed with 3,000 U of heparin sodium (Elkins-Sinn, Cherry Hill, NJ) per 1,000 mL of normal saline solution at a keep-open drip rate. Iohexol, a nonionic, water-soluble contrast medium (Omnipaque 300; Nycomed Amersham, Princeton, NJ), was used for angiographic injections. The procedures were performed with a Neurostar or Angiostar (Siemens Medical Systems, Iselin, NJ) or a Fluoricon LU (GE Medical Systems, Milwaukee, Wis) system.

After the diagnostic angiogram obtained with use of a 5-F catheter, the chemotherapeutic agent, carboplatin or methotrexate, dissolved in 150 mL dextrose 5% water solution (Baxter, Deerfield, Ill), was infused during a 15-minute period by means of intravenous tubing with an in-line disk filter and a standard mechanical pump. The infusion was made through a three-way stopcock. After completion of the study, the catheter was removed, and pressure was applied to the puncture site, usually by using a mechanical compression device, until hemostasis was achieved. The patients were monitored by nurses for 1 hour in the angiography recovery room. The patients were then transferred to their rooms and monitored for another 4 hours with the ipsilateral lower extremity kept straight to expedite healing of the groin wound. All patients underwent a neurologic examination before and after the procedure, as well as continuous monitoring during the procedure by a radiology nurse specialist. In addition, neurologic evaluations were performed by the neuro-oncology service at the time of admission (usually just before the procedure), after each intraarterial procedure, and before discharge.

Age, sex, type of tumor (primary or metastatic), and number of procedures performed were tabulated for each patient. Complications were divided into several groups. Local complications included any localized abnormality related to the puncture site or to a direct effect of the catheter in the cerebral circulation. Systemic complications were nonneurologic complications affecting the patient as a consequence of the procedure. Neurologic complications were subdivided into the following categories: transient, or having complete resolution during the first 24 hours; reversible, or having resolution between the first 24 hours and 7 days; and permanent, or having developed during the first 24 hours after the procedure but without resolution after 7 days.

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
We evaluated 392 procedures performed in 48 patients (Table 1). Thirty-three patients had primary brain tumors; glioblastoma multiforme was the most common diagnosis. Other frequent tumors included oligodendroglioma, anaplastic astrocytoma, and gliosarcoma. Fifteen patients had metastatic brain tumors, lung cancer being the most common primary site.

Procedural catheter complications included two episodes (0.5%) of vasospasm. The vasospasm occurred at the tip of the catheter and was seen only in the right internal carotid catheterizations. The catheter was pulled back slightly and the spasm resolved following the administration of nitroglycerin skin paste in the first case and spontaneously in the second. The chemotherapy protocol was completed with a slower than routine flow rate. Both episodes of vasospasm were neurologically asymptomatic.

Two asymptomatic arterial dissections (0.5%) occurred, both after diagnostic internal carotid angiograms were obtained. One dissection involved the proximal right internal carotid artery; there was a residual pseudoaneurysm at initial follow-up, but it subsequently disappeared. A second dissection occurred in a different patient and involved the left internal carotid artery approximately 2 cm proximal to the petrous segment. The stenosis initially was estimated at 90%, but a follow-up angiogram showed only a 50% stenosis. A few weeks later, only a small residual pseudoaneurysm was noted, and the patient remained asymptomatic.

A few neurologic complications occurred during the procedures. There were seven transient non–seizure-related neurologic complications (1.8%). Five involved focal paresis (1.3%). One patient developed numbness on the left side of the face on one occasion and during a different procedure noted numbness in the left arm. In both cases, the symptoms resolved in less than 30 minutes. One patient complained of left-sided dysesthesias during the infusion of the chemotherapeutic agent, but these resolved by the end of the procedure. Another patient had an episode of right-sided weakness and aphasia, which resolved in 30 minutes. One patient developed left hemiparesis approximately 12 hours after a procedure; the patient was readmitted and observed, and the hemiparesis completely resolved in less than 24 hours.

One patient developed visual symptoms twice (0.5%); on both occasions, the left vertebral artery was catheterized. During the first episode, the patient experienced bright dots and dark spots in his field of view, but this resolved during the next 12 hours. The second episode involved complete occipital cortical blindness accompanied by mental status changes and transient global amnesia; complete recovery occurred in less than 24 hours.

Six (1.5%) transient seizure events were recorded. Four of the seizures were focal episodes; two of these involved the facial musculature. One patient had focal seizures of the right extremities on two different occasions during the chemotherapeutic infusion. One patient had a generalized tonic-clonic seizure and was treated with a low level of phenytoin (Dilantin; Parke-Davis, a Warner-Lambert Company, Morris Plains, NJ). The other patient with a generalized seizure episode had frequent seizures at home, and these were poorly controlled despite medication.

No permanent neurologic complications (eg, vessel occlusion, brain infarct) were observed related to the angiographic procedures. In addition, the rate of chemotherapy-induced complications and toxicity was negligible. There were no cases of nephrotoxicity, ototoxicity, retinopathy, or leukoencephalopathy. The most common side effects of chemotherapy were mild to moderate leukopenia and thrombocytopenia.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
There have been many approaches to the treatment of brain tumors; the majority of these therapies are relatively ineffective (1,2). Multiple surgical procedures can be undertaken, but most gliomas will still recur locally. Direct tumor ablation with lasers, cryoprobes, and other energy sources also have been attempted with limited success. Whole brain, stereotactic, and interstitial irradiation can be used; however, there are many potential problems associated with irradiation, including dementia, white matter changes, atrophy, delayed tumor induction, necrosis, and alopecia (18,19).

A recent meta-analysis by Fine and colleagues (5) suggests that the use of chemotherapy confers a survival advantage on adult patients with malignant gliomas. Intravenous chemotherapy has produced a modest improvement in the survival of patients with these tumors by using agents such as carmustine, or BCNU, methotrexate, cisplatin, and cyclophosphamide (20). An alternative approach is intraarterial chemotherapy, which, compared with an equivalent intravenous dose, can augment the local plasma peak drug concentration and local area under the concentration-time curve (6). This method potentially can increase drug concentrations by twofold to fourfold while reducing the risk of systemic toxicity. To standardize and propagate the use of intraarterial chemotherapy, it is important to document its complication rate.

Our preliminary results with use of intraarterial chemotherapy have been encouraging (7,8). Twenty-three patients (age range, 31–68 years; mean age, 50.2 years) were available for evaluation of efficacy. Ten patients had gliomas: glioblastoma multiforme (n = 4), anaplastic astrocytoma (n = 2), oligodendroglioma (n = 2), anaplastic astrocytoma and oligodendroglioma (n = 1), and gliosarcoma (n = 1); and 13 patients had metastatic brain tumors: lung (n = 7), breast (n = 2), colon (n = 2), adenocarcinoma (n = 1), and malignant fibrous histiocytoma (n = 1).

There have been four complete responses and six partial responses; some patients with multifocal metastatic brain tumors had complete responses or partial responses to treatment (7,8). All of the complete responses and four of six partial responses occurred in patients with metastatic tumors. The two partial responses in the glioma cohort developed in patients with anaplastic astrocytoma. Eight patients had stable disease. The mean time to progression was approximately 22.0 weeks for all tumor types. The majority of patients with gliomas died of progressive central nervous system disease, while many of the patients with metastatic tumors died of systemic complications unrelated to intraarterial chemotherapy.

The complications of diagnostic cerebral angiography have been evaluated in previous studies. Earnest et al (9) evaluated 1,517 cerebral angiograms in 1980–1982. They reported an overall incidence of complications of 8.5% and one death. Local complications developed in 4.9% (74 of 1,517) of procedures, while neurologic complications were noted in 2.6% (40 of 1,517), with 2.2% (33 of 1,517) transient, 0.1 % (two of 1,517) reversible, and 0.3% (five of 1,517) permanent. Older age, an increased serum creatinine level, and the use of more than one catheter were all associated with an increased risk of neurologic complications. Waugh and Sacharias (10) evaluated the complication rate in 2,475 patients who underwent diagnostic angiographic procedures—939 carotid or cerebral studies—with use of digital subtraction in 1988–1990. The total complication rate was 10%, with four deaths (0.16%). Local complications occurred in 7.3% (181 of 2,475) of procedures, and 0.96% (nine of 939) were neurologic, with 0.3% (three of 939) reversible and 0.3% (three of 939) permanent.

More recently, Heiserman et al (11) evaluated the rate of neurologic complications associated with modern diagnostic cerebral angiography in 1,000 patients and found an 8.1% rate of nonneurologic complications and a 1.0% (10 of 1,000) overall rate of neurologic complications, with 0.5% (five of 1,000) transient and 0.5% (five of 1,000) permanent. All of the complications developed in patients who were 50 years or older and who had a history of stroke, transient ischemic attack, or carotid bruit.

Horowitz et al (12) evaluated the complications in 1,929 procedures—1,358 diagnostic and 571 interventional—in 1993–1996. The overall rate of complications was 5.5% (105 of 1,926), with a 0.1% (two of 1,358) rate of procedure-related deaths. For diagnostically oriented procedures, the overall complication rate was 2.2% (30 of 1,358). Permanent neurologic complications were noted in 0.4% (five of 1,358), whereas transient neurologic complications developed in 0.3% (four of 1,358) of procedures.

The rate of complications in our study was similar to, or in some cases, lower than that in many of the reported series detailed earlier and compares favorably with the standards of the American College of Radiology and the Society of Cardiovascular and Interventional Radiology (21). We had a 0% rate of irreversible or permanent neurologic deficits and no deaths. There are probably a number of reasons for our low complication rate. One is that the population in our study was not dominated by patients with angiopathy. The patients in our study were not examined for primary vascular disease, nor did they have a history of stroke or transient ischemic attack, factors previously associated with an increased rate of neurologic complications (11,13,17).

A key determinant associated with higher complication rates has been prolonged procedure times (9,10,14,15). In our study, we had not only the advantage of advanced knowledge of the patient's anatomy because patients underwent multiple procedures but also ideal equipment for completing the examination. These factors allowed for shorter vascular examination times, which often took only 30 minutes, including the chemotherapeutic infusion. The patients also were screened well for possible bleeding or metabolic problems. All of our studies were performed with nonionic contrast medium.

Authors of some studies (11,14,16) in which the complication rate with the advent of digital subtraction angiography has been evaluated have claimed a decreased complication rate, presumably related to a decrease in procedure time and in the amount of contrast medium administered. The small amounts of contrast medium we used during the limited single-vessel, single-plane angiogram obtained during each procedure, before the infusion of the chemotherapeutic agent, may have been an advantage. Microcatheter techniques were not used to avoid increased costs, procedure time, and the potential for a higher catheter-related complication rate.

The patients in our study had other risk factors not present in previous study populations, and these might have been expected to increase the rate of complications. This was an interventional procedure rather than a purely diagnostic one. There could have been thrombus development or drug reactions related to the chemotherapy. Bubbles could have been introduced into the vascular system. The catheters were left in place for a relatively long interval, which could have allowed for clot development. None of the patients received anticoagulant therapy, and many had relatively low platelet and white blood cell counts. Despite all of these risk factors, there were no serious hemorrhagic or infectious complications.

We observed a 1.5% rate of procedure-related seizures, most of which can be attributable to the underlying malignancy and not to the procedure itself. One of the patients was known to have frequent grand mal seizures while at home. Most of the patients were receiving an anticonvulsant, usually phenytoin, and on at least one occasion subtherapeutic levels were documented in association with procedural seizure activity.

Many of the patients in our study underwent numerous consecutive groin punctures and angiography. Regardless of this, there did not appear to be a progressive risk of groin complications, and there was only one popliteal embolus. No pseudoaneurysm formation was noted at the puncture sites.

A few patients had pulmonary emboli and venous thrombotic disease. There is a high rate of thrombotic venous disease in patients with brain tumor. Findings of recent studies (22,23) suggest a combined rate of thromboembolic disease of 19%–28% in patients with high-grade gliomas. In light of these, it is difficult to attribute the events noted in our study to the angiographic procedures or intraarterial chemotherapy.

We took certain precautions to avoid complications in the patients in our study. For example, we did not routinely use intraarterial sheaths or leave them in place overnight. Leaving the sheath in the vessel also could have increased the risk of thrombosis, hemorrhage, accidental leak, and infection. We stopped obtaining internal carotid diagnostic angiograms before the infusions because we never encountered a dissection or spasm with common carotid catheterization or injections. We suspect that the trauma associated with the injection was more important than the catheter or wire manipulation. Because we also did not use general anesthesia with these patients, there was a low rate of spasm. We always used a filter for the chemotherapy to avoid emboli and to intercept any air bubbles.

A potential limitation of our study was the presence of underlying neurologic deficits in some of the patients, which was caused by the brain tumor, surrounding edema, and effect of the mass. Thrombosis or embolism might have occurred in neurologically affected regions and remained without clinical manifestation. The fact that no reversible or permanent neurologic complications were observed is reassuring.

Another inherent limitation of the study is that a number of these patients died of their primary disease during the course of treatment, thereby not allowing potential complications of repeated angiography to become clinically apparent. It is encouraging that 50% of the patients in our study underwent seven or more procedures (nine patients underwent 13 or more and four patients underwent 19 or more) without a major complication.

This study demonstrates that intraarterial chemotherapy, even in potentially sensitive vascular territories (ie, cerebral), can be performed with a low complication rate. This implies that intraarterial chemotherapy for brain tumors is not limited by the technical aspects of the catheterization procedure but more by the availability of efficacious and safe chemotherapeutic agents. As more effective agents become available, intraarterial chemotherapy may have an expanded role in the treatment of primary and metastatic brain tumors. Furthermore, these results suggest that intraarterial chemotherapy could play an important role in the treatment of other tumors with accessible vasculature, such as those in the head and neck region.

	Footnotes

 
Author contributions: Guarantors of integrity of entire study, D.W.C., H.B.N.; study concepts, M.G., D.W.C., H.B.N.; study design, M.G., D.W.C.; definition of intellectual content, D.W.C., H.B.N., M.G.; literature research, M.G., D.W.C., H.B.N.; clinical studies, D.W.C., H.B.N.; data acquisition, M.G.; data analysis, M.G., D.W.C.; manuscript preparation, M.G.; manuscript editing and review, H.B.N., D.W.C., M.G.

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gelman, M. Articles by Newton, H. B. Search for Related Content PubMed PubMed Citation Articles by Gelman, M. Articles by Newton, H. B.