Computerized tomography—guided stereotactic surgery for brainstem masses: a risk—benefit analysis in 71 patients

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✓ The benefits of the use of computerized tomography (CT)-guided stereotactic surgical techniques for the management of intrinsic brainstem masses diagnosed from clinical evaluation and imaging studies were evaluated vis-à-vis the risks involved in 71 consecutive patients. Seventy-two procedures were performed. The masses were diffuse, involving two or three contiguous brainstem segments, in 60 patients and focal in 11 patients. On the CT scans, 25 patients had hypodense nonenhancing masses, two had isodense nonenhancing masses, 19 had ring-enhancing masses, and 25 had heterogeneously enhancing masses. A positive biopsy was obtained in 68 of 69 patients (98.5%) undergoing a biopsy procedure. In nine patients (12.6%) with suspected malignant masses a benign pathology was diagnosed (four tuberculomas, two epidermoid cysts, one pyogenic abscess, one epidermal cyst, and one case of encephalitis). Additionally, fluid from cystic masses could be aspirated in eight cases, providing benefit in six (four patients had benign lesions and two had neoplastic lesions). Thereby, a total of 13 patients (18.3%) were deemed to have benefited from the surgery (two patients were included in both categories). Patients with focal masses and ring-enhancing masses had the highest proportion of benign lesions (60% and 36.8%, respectively) and therefore derived the most benefit from histological verification. There was no procedurerelated mortality. One patient (1.4%) suffered permanent morbidity and four others (5.6%) had transient worsening attributable to the procedure. The authors conclude that CT-guided stereotactic surgery of the brainstem is safe and reliable. Histological verification of all enhancing (especially ring-enhancing) and focal brainstem masses should be undertaken to identify patients with benign nonneoplastic lesions. Selected patients with diffuse hypodense nonenhancing masses with atypical clinical or imaging features may also benefit from stereotactic biopsy. Even in these patients the lack of enhancement on a contrast-enhanced magnetic resonance image, rather than the diffuse location of the tumor alone, should form the basis for diagnosing a malignant glioma. The main value of stereotactic surgery lies in the identification of benign masses in a significant proportion of patients with intrinsic brainstem masses and in providing a rapid and safe method for evacuation of the contents of cystic masses.

Abstract

✓ The benefits of the use of computerized tomography (CT)-guided stereotactic surgical techniques for the management of intrinsic brainstem masses diagnosed from clinical evaluation and imaging studies were evaluated vis-à-vis the risks involved in 71 consecutive patients. Seventy-two procedures were performed. The masses were diffuse, involving two or three contiguous brainstem segments, in 60 patients and focal in 11 patients. On the CT scans, 25 patients had hypodense nonenhancing masses, two had isodense nonenhancing masses, 19 had ring-enhancing masses, and 25 had heterogeneously enhancing masses. A positive biopsy was obtained in 68 of 69 patients (98.5%) undergoing a biopsy procedure. In nine patients (12.6%) with suspected malignant masses a benign pathology was diagnosed (four tuberculomas, two epidermoid cysts, one pyogenic abscess, one epidermal cyst, and one case of encephalitis). Additionally, fluid from cystic masses could be aspirated in eight cases, providing benefit in six (four patients had benign lesions and two had neoplastic lesions). Thereby, a total of 13 patients (18.3%) were deemed to have benefited from the surgery (two patients were included in both categories). Patients with focal masses and ring-enhancing masses had the highest proportion of benign lesions (60% and 36.8%, respectively) and therefore derived the most benefit from histological verification. There was no procedurerelated mortality. One patient (1.4%) suffered permanent morbidity and four others (5.6%) had transient worsening attributable to the procedure. The authors conclude that CT-guided stereotactic surgery of the brainstem is safe and reliable. Histological verification of all enhancing (especially ring-enhancing) and focal brainstem masses should be undertaken to identify patients with benign nonneoplastic lesions. Selected patients with diffuse hypodense nonenhancing masses with atypical clinical or imaging features may also benefit from stereotactic biopsy. Even in these patients the lack of enhancement on a contrast-enhanced magnetic resonance image, rather than the diffuse location of the tumor alone, should form the basis for diagnosing a malignant glioma. The main value of stereotactic surgery lies in the identification of benign masses in a significant proportion of patients with intrinsic brainstem masses and in providing a rapid and safe method for evacuation of the contents of cystic masses.

Intrinsic masses of the brainstem have varied pathologies, although a majority of them, especially in children and young adults, are malignant.2,6,7,10,13,15 Management of these lesions is currently the subject of considerable debate. Recognition of the occurrence of benign brainstem lesions such as demyelination, inflammatory granulomas, cavernous angiomas, and pyogenic abscesses has focused on the need to replace empirical radiation therapy with specific therapy directed by a histological diagnosis. The ability of magnetic resonance (MR) imaging to elegantly demonstrate brainstem pathology without the artifacts seen on computerized tomography (CT) has, however, led to a reconsideration of the policy of routine histological verification of all brainstem masses.4

The objectives of the present study were to evaluate the risks and benefits associated with a policy of CT-guided stereotactic surgery for all intrinsic brainstem masses, to determine the proportion of patients in whom such surgery altered the projected management and thereby the outcome, and to identify the subgroup of patients in whom this surgery would yield maximum benefits.

Clinical Material and Methods
Patient Population

All patients undergoing CT-guided stereotactic surgery at our institution for isolated intrinsic brainstem masses (as determined on imaging studies) between May 1987 and December 1993 were included in the study. Seventy-two stereotactic procedures were performed in 71 patients during this time. There were 37 males and 34 females, ranging in age from 2.5 years to 67 years and with a median age of 9 years. Nearly 75% of patients (52 of 71) were in the pediatric age group (< 18 years). A few patients with brainstem masses, most often of the exophytic type, underwent open surgical procedures during the study period. Data were gathered from case records and imaging studies.

Imaging Studies

Contrast-enhanced CT was the chief investigational procedure and was performed in all patients prior to surgery. Magnetic resonance imaging was also obtained in 16 patients. The brainstem lesions were classified into four categories based on their appearance on contrast-enhanced CT: 1) hypodense nonenhancing; 2) isodense nonenhancing; 3) ring enhancing; and 4) heterogeneously enhancing. The location of the brainstem mass was determined on the basis of clinical evaluation and imaging studies and was classified as diffuse if more than one contiguous brainstem segment was involved or if the mass was more than 2 cm in size.9 Masses restricted to one brainstem segment and measuring less than 2 cm in size were designated as focal.

Stereotactic Surgery

The surgery was performed with the patient under general anesthesia in 60 procedures and under local anesthesia in 12. In all patients stereotactic surgery was performed using a Brown-Roberts-Wells CT stereotactic system. A precoronal burr hole was used as the entry point for a transfrontal approach to the brainstem in 70 procedures. In two patients a suboccipital burr hole was used to perform a transcerebellar biopsy. A sheath 1.2 mm in diameter was passed to the target and cup forceps were used to deliver 1 mm3 of tissue from the tumor in cases in which a biopsy was obtained. If a cystic mass was suspected a hand-held syringe was used to gently aspirate the contents through the outer sheath after removing the stylet.

An intraoperative smear diagnosis was obtained on all specimens and the procedure was terminated only when the pathologist confirmed that representative tissue had been obtained. Routine postoperative CT was performed in all cases within 4 hours of the procedure.

Identifying Benefited Patients

Patients were deemed to have benefited from the procedure either when a benign pathology was identified in a case in which a malignant mass was suspected on preoperative imaging studies, or when the contents of a cystic mass could be aspirated and provided immediate (whether transient or long-lasting) improvement in the patient's neurological status.

Results

Table 1 summarizes the CT categorization and location of the masses. A majority of the masses were contrast enhancing (44 of 71, 62%) and most were diffuse (60 of 71, 84.5%).

TABLE 1

Morphology on computerized tomography (CT) and location of masses

FeatureNo. of Patients
morphology on CT
 hypodense nonenhancing25
 isodense nonenhancing2
 ring enhancing19
 heterogeneously enhancing25
location
 diffuse
  pons & medulla16
  pons & midbrain10
  pons, midbrain, & medulla34
 focal
  pons6
  midbrain5
total71

Diagnostic Yield

Table 2 lists the diagnostic pathologies obtained. A positive biopsy was obtained in 68 (98.5%) of 69 biopsy procedures. An etiological diagnosis of tuberculosis could be made in only two of six patients with chronic inflammatory masses. The other four patients with chronic inflammatory masses responded clinically and radiologically to antituberculous therapy.

TABLE 2

Pathology of the brainstem masses

DiagnosisNo. of Patients
astrocytoma Grade 19
astrocytoma Grade 242
astrocytoma Grade 37
ependymoma1
chronic inflammation4
granulomatous inflammation2
 consistent with tuberculosis
epidermoid cyst2
epidermal cyst (?)1
pyogenic abscess2
encephalitis1
normal brain (false negative)1
total72*

One patient underwent two biopsy procedures.

One patient who underwent a transfrontal biopsy of a ring-enhancing mass in the middle cerebellar peduncle (as seen on CT and MR imaging) had a negative biopsy (Fig. 1). This patient then underwent a transcerebellar CT-guided stereotactic biopsy, which was reported as being consistent with the contents of an epidermoid cyst. This was later confirmed on open surgical excision of the mass.

Fig. 1.
Fig. 1.

Magnetic resonance imaging in a 50-year-old woman who presented with left-sided trigeminal neuralgia. Plain axial T1-weighted (left) and T2-weighted (right) images show a ring-enhancing lesion in the left middle cerebellar peduncle. There was no enhancement of the mass on gadolinium-enhanced images. Biopsy revealed an epidermoid cyst.

In three patients a biopsy was not performed. One patient with Fallot's tetralogy and a ring-enhancing mass in the brainstem was suspected of having an abscess and underwent an aspiration procedure only, which yielded 15 ml of pus. No tissue was taken for biopsy. (This patient has been reported previously.23) Another patient, with a previous histological diagnosis of a cerebellopontine angle tuberculoma, underwent aspiration of a tuberculous abscess involving the pons and midbrain. The third patient, with a probable epidermal cyst, is detailed below.

Patients Benefiting From the Surgery

A benign pathology was discovered in nine patients (12.6%) with suspected malignant lesions. Six other patients improved following aspiration of their cystic masses. Two patients were in both these subgroups; therefore a total of 13 patients (18.3%) were ultimately deemed to have benefited from the stereotactic surgery. In three other patients a benign lesion was identified preoperatively (a cardiogenic abscess, a tuberculous abscess, and a tuberculoma). The imaging and pathological features of masses with a benign pathology are outlined in Table 3.

TABLE 3

Appearance on computerized tomography (CT) and pathological data in 12 patients with benign brainstem masses*

Age (yrs)/SexLocation of MassMR FeaturesImaging DiagnosisStereotactic Diagnosis
hypodense nonenhancing
12, F diffuse gliomaencephalitis
5, F diffuseT1; hypo gliomaepidermal cyst (?)
 T2; hyper 
29, F focal gliomaepidermoid cyst
ring enhancing 
67, M focalring lesion metastasisabscess
50, F focalring lesion metastasisepidermoid cyst
18, F focalring lesion tuberculomatuberculoma
5, M diffuse abscessabscess
22, F diffuse tuberculomatuberculous abscess
6, M focal gliomatuberculoma
5, M focal gliomatuberculoma
heterogeneously enhancing
32, F diffuseheterogeneous gliomatuberculoma
11, F diffuse gliomatuberculoma

MR = magnetic resonance; T1 and T2 = T1- and T2-weighted MR images; hypo = hypointense; hyper = hyperintense; — = did not undergo MR imaging.

A 5-year-old girl with clinical features of an intrinsic brainstem mass and a CT picture of a diffuse hypodense mass in the brainstem (Fig. 2 left) was subsequently diagnosed as having a cystic mass anterior to the brainstem (Fig. 2 center and right). The milky contents suggested the possibility of an epidermal cyst.

Fig. 2.
Fig. 2.

Left: Stereotactic contrast-enhanced computerized tomography scan in a 5-year-old girl showing a hypodense mass in the region of the pons as well as the basilar artery appearing anterior to the mass. No tissue was obtained on biopsy, although aspiration yielded 8 ml of milky-white fluid. Center: Magnetic resonance imaging performed after recurrence of symptoms 1 month following aspiration. Sagittal T1-weighted image reveals a well-defined hypointense mass anterior to the pons and medulla, but the basilar artery is anterior to the mass. Right: Magnetic resonance imaging performed 3 months after open surgery and marsupialization of the cyst, revealing normal configuration of the brainstem and resolution of the mass anterior to it.

A 67-year-old man with rapidly progressing clinical symptoms and signs had a ring-enhancing mass in the midbrain (Fig. 3). Differential diagnoses included metastatic disease, tuberculoma, and pyogenic abscess. Stereotactic biopsy and aspiration were diagnostic of a pyogenic abscess and the pus grew enterococci. The patient improved over a period of 2 weeks with antibiotic therapy. No systemic source for the infection was found.

Fig. 3.
Fig. 3.

Left: Contrast-enhanced computerized tomography scan in a 67-year-old man showing a ring-enhancing mass in the midbrain. Right: A T2-weighted axial magnetic resonance image in the same patient showing a ring-enhancing lesion with a hypointense periphery and hyperintense center. Biopsy and aspiration revealed a pyogenic abscess.

In eight patients with a cystic mass fluid could be aspirated from the mass, but improvement was seen in only six patients. Four of these patients had benign lesions: two had pyogenic abscesses, another had a tuberculous abscess, and the fourth, who did not undergo biopsy, probably had an epidermal cyst ventral to the brainstem.

Complications

There was no procedure-related mortality in our series. One patient with an epidermoid cyst indenting the middle cerebellar peduncle suffered morbidity that has not resolved completely. Following the transfrontal biopsy, which was nondiagnostic, this patient had a left lateral gaze palsy, facial palsy, and right hemihypalgesia. Although the facial palsy and the gaze palsy were successfully treated with steroids, she has a persistent left lateral rectus palsy and mild diminution of pain and temperature sensation in the right half of the body.

Four patients (5.6%) experienced transient morbidity. Two patients were drowsy for 24 to 48 hours after surgery. One patient developed aspiration pneumonia 48 hours after surgery but recovered with appropriate therapy. After surgery, one patient had worsening of his ataxia, which recovered to preoperative levels over 1 week.

Discussion
Lack of Imaging and Pathological Correlation

Many benign pathologies such as pyogenic abscess, tuberculoma, cavernous angiomas, demyelination, encephalitis, radiation necrosis, and cysticercus granuloma can produce clinical and imaging characteristics of an intrinsic brainstem mass.1,7,15 Besides these lesions that occur within the brainstem, some lesions closely related to it but not within its bounds can also mimic an intrinsic mass. This was the case in three patients in our series, one with a probable epidermal cyst and two with epidermoid tumor, although MR imaging was available for two of them. Even using MR imaging, a definitive pathological diagnosis is impossible in a large number of cases.1,7,15,18 Kratimenos and Thomas15 estimated that in 10% to 20% of cases the image-based diagnosis is incorrect. Therefore it becomes imperative that benign pathologies be identified histologically in every case so as not to subject patients to inappropriate radiation therapy.

Diffuse Brainstem Masses in Children

The management of pediatric patients is highly controversial. Many authors now believe that MR imaging characteristics are so typical in these patients that a histological diagnosis is not warranted.2–4,9,10,20 Albright, et al.,4 strongly urge neurosurgeons to desist from performing biopsy of diffuse brainstem masses in children. These authors define diffuse tumors as those involving all segments of the brainstem. The diffuse location of the tumor alone, and not the lack of significant contrast enhancement on contrast-enhanced CT or MR scans, was suggested as the crucial identifying feature of a malignant brainstem glioma in children. Others, however, contend that because histological diagnosis is relatively safely obtained with stereotactic techniques, empirical radiation therapy should be avoided.1,7,15 One of our concerns is that plain MR imaging may not distinguish inflammatory masses from gliomas, as happened in one of our cases. Therefore, even for diffuse masses of the brainstem, whether in children or adults, a gadolinium-enhanced MR image should be mandatory if empirical radiation therapy is being advised. Presupposing that all inflammatory masses will enhance with gadolinium injection, this policy may reduce the number of instances in which an inflammatory lesion such as a tuberculoma is mistaken for a glioma. We believe that in addition to the location of the mass (diffuse or focal), its appearance on a contrast-enhanced CT or MR image should be an important determinant of further management strategies.

Our data suggest that obtaining a histological diagnosis in pediatric patients with brainstem lesions may identify the occasional patient with a benign pathology. In our series three children with diffuse masses (two hypodense and one enhancing) benefited from such a policy. In one case even MR imaging was misleading, as an extraaxial cyst had pushed the basilar artery anteriorly, giving it the appearance of an intrinsic brainstem mass. Abernathy, et al.,1 reported a child with a diffuse hypodense mass on CT and MR imaging in whom the biopsy revealed demyelination. Therefore demyelination, radiation necrosis, encephalitis, and a benign cyst adjacent to the brainstem may occasionally mimic a diffuse malignant glioma, even on MR imaging.

Focal Enhancing Masses

Compared to hypodense nonenhancing masses, focal enhancing masses on both CT and MR imaging are more likely to be given a diagnosis other than that of malignant glioma (Fig. 4). In our series, tuberculomas were the second most common cause of an enhancing mass in the brainstem. All focal and enhancing masses of the brainstem deserve a histological diagnosis, because imaging does not differentiate with absolute certainty one pathology from another in these patients.

Fig. 4.
Fig. 4.

Pie charts showing the proportion of benign masses with various appearances on computerized tomography. The shaded segments represent gliomas and the nonshaded segments represent benign nongliomatous masses. Note the high proportion of the latter category of lesions among ring-enhancing and focal lesions. The numbers represent the number of masses in each category. E = enhancing, NE = nonenhancing, HYPO = hypodense, ISO = isodense, HETERO = heterogeneous.

Role of Open Surgery

Open surgery plus radical excision is now a generally accepted mode of treatment for patients with exophytic and cervicomedullary gliomas, but is less so for focal intrinsic gliomas.9–12,20 Even among patients with the former lesions only those with benign glioma have been shown to have longer survival following radical surgery, with or without adjuvant radiation therapy.9,10,12,20 Open surgery for brainstem masses carries considerable risk for morbidity and mortality.5,11,12,16,21,24 Even those who survive the surgical procedure require prolonged postoperative care in an intensive care setting. Pierre-Kahn, et al.,21 recommend that all patients undergoing brainstem surgery should be electively ventilated and have an external ventricular drain for 1 week after the surgery.

Most authors agree that open surgery should not be performed just to obtain a biopsy, as stereotactic methods are safer and more reliable.2,4,10,18 Besides the higher morbidity associated with open surgery, a negative result is more likely when open surgery is used to obtain a histological diagnosis in patients with diffuse intrinsic masses.17,24

Radical excision of focal brainstem masses such as tuberculomas and lymphomas is not indicated. Radical excision also does not prolong survival in patients with malignant glioma of the brainstem.10,12,21 Before embarking on a major surgical procedure for a focal intrinsic brainstem mass, it would therefore seem prudent to identify the nature of the mass with a stereotactic biopsy and avoid open surgery if the lesion is identified as a malignant glioma or a mass that can be treated with other modalities.15

Role of Stereotactic Surgery

Stereotactic surgery of the brainstem is minimally invasive and a number of authors have reported no mortality and a low morbidity rate with this procedure.1,7,13–15 The positive yield rate is also very high, ranging between 94% and 100%.1,7,13–15 An unexpected histological diagnosis has been reported in 25% to 50% of patients undergoing stereotactic biopsy of brainstem masses.1,7,15 An etiological diagnosis is, however, elusive in a majority of patients with inflammatory masses.22 One is often forced to rely on the overall clinical situation and microbiological studies before initiating specific therapy in patients with inflammatory masses.

Stereotactic techniques also help in safely aspirating the contents of cystic masses, both benign and malignant. This usually provides long-lasting benefit in patients with benign cystic masses, such as pyogenic abscesses, neuroepithelial cysts, parasitic cysts, and tuberculous abscesses. Aspiration of cystic gliomas not only provides immediate amelioration of the neurological symptoms, but has also been reported to produce long-term benefits when combined with external beam radiation therapy. Hood and McKeever14 reported good results in 10 patients with cystic brainstem glioma who underwent stereotactic aspiration of the cyst combined with interstitial and externalbeam radiation therapy. Brachytherapy of brainstem gliomas using stereotactically implanted isotopes iodine-131 or iridium-192 has also been reported to be efficacious in prolonging survival of patients with benign glioma.19

Biopsy for Predicting Outcome in Patients With Brainstem Glioma

There are conflicting reports on the value of the histological grade obtained from biopsy of a brainstem glioma in predicting long-term outcome. Early reports suggested that patients with histologically proven low-grade glioma had a better prognosis than those with high-grade glioma.3,5,8,14 Recent reports suggest that although this may be true when the histological diagnosis is based on radically resected specimens, it may not hold true for a diagnosis based on stereotactic biopsy samples. Brainstem gliomas are notorious for their heterogeneity and a small biopsy sample may represent a benign focus in a largely malignant tumor. However, Abernathy, et al.,1 and Kratimenos and Thomas15 documented a good correlation between stereotactic biopsy-based diagnosis and survival in patients with brainstem gliomas. In our series, however, only eight of 59 gliomas were graded as malignant, whereas it is well known that a majority of these tumors would be malignant. We would therefore not recommend stereotactic biopsy to determine the histological grade of an obvious glioma.

Conclusions

Image-guided stereotactic biopsy seems to be the ideal initial procedure for most patients with intrinsic brainstem masses. It carries minimal risk and is beneficial in approximately 18% of patients by either identifying benign pathology or enabling the surgeon to aspirate fluid from a cystic mass. Although all focal and enhancing masses in the brainstem deserve histological verification, the management of patients with diffuse hypodense nonenhancing masses of the brainstem should be individualized. Even in this latter group of patients gadolinium-enhanced MR imaging, rather than plain MR imaging, should form the basis for selection of patients to be treated with radiation therapy.

References

Article Information

Address reprint requests to: Vedantam Rajshekhar, M.Ch., Department of Neurological Sciences, Christian Medical College Hospital, Vellore 632004, India.

© AANS, except where prohibited by US copyright law.

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Figures

  • View in gallery

    Magnetic resonance imaging in a 50-year-old woman who presented with left-sided trigeminal neuralgia. Plain axial T1-weighted (left) and T2-weighted (right) images show a ring-enhancing lesion in the left middle cerebellar peduncle. There was no enhancement of the mass on gadolinium-enhanced images. Biopsy revealed an epidermoid cyst.

  • View in gallery

    Left: Stereotactic contrast-enhanced computerized tomography scan in a 5-year-old girl showing a hypodense mass in the region of the pons as well as the basilar artery appearing anterior to the mass. No tissue was obtained on biopsy, although aspiration yielded 8 ml of milky-white fluid. Center: Magnetic resonance imaging performed after recurrence of symptoms 1 month following aspiration. Sagittal T1-weighted image reveals a well-defined hypointense mass anterior to the pons and medulla, but the basilar artery is anterior to the mass. Right: Magnetic resonance imaging performed 3 months after open surgery and marsupialization of the cyst, revealing normal configuration of the brainstem and resolution of the mass anterior to it.

  • View in gallery

    Left: Contrast-enhanced computerized tomography scan in a 67-year-old man showing a ring-enhancing mass in the midbrain. Right: A T2-weighted axial magnetic resonance image in the same patient showing a ring-enhancing lesion with a hypointense periphery and hyperintense center. Biopsy and aspiration revealed a pyogenic abscess.

  • View in gallery

    Pie charts showing the proportion of benign masses with various appearances on computerized tomography. The shaded segments represent gliomas and the nonshaded segments represent benign nongliomatous masses. Note the high proportion of the latter category of lesions among ring-enhancing and focal lesions. The numbers represent the number of masses in each category. E = enhancing, NE = nonenhancing, HYPO = hypodense, ISO = isodense, HETERO = heterogeneous.

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