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(Chest. 1999;115:714-719.)
© 1999 American College of Chest Physicians

Detection of Brain Metastasis in Potentially Operable Non-small Cell Lung Cancer*

A Comparison of CT and MRI

Kohei Yokoi, MD; Noriki Kamiya, MD; Haruhisa Matsuguma, MD; Suguru Machida, MD; Takashi Hirose, MD; Kiyoshi Mori, MD and Keigo Tominaga, MD

* From the Divisions of Thoracic Surgery (Drs. Yokoi, Kamiya, and Matsuguma), and Thoracic Diseases (Drs. Machida, Hirose, Mori, and Tominaga), Tochigi Cancer Center, Utsunomiya, Japan.


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To compare the usefulness of MRI and CT in the detection of brain metastases during preoperative evaluation and postoperative follow-up.

Design: A prospective and sequential comparison.

Patients and methods: Of 332 patients with potentially operable non-small cell lung cancer who were free of neurologic signs and symptoms, brain CT was performed preoperatively on 155 patients (CT group) and brain MRI on 177 patients (MRI group). Patient characteristics in both groups were comparable. In 279 patients with complete resection of the primary lung tumor, intensive follow-up with CT and MRI was performed in the respective groups. The preoperative detection of brain metastases, postoperative intracranial recurrence rates, and characteristics of detected brain tumors were compared between the two groups. The survival of patients with brain metastases was also compared.

Results: From the first evaluation to 12 months after surgery for primary lung cancer, brain metastases were observed in 11 patients (7.1%) from the CT group and 12 patients (6.8%) from the MRI group. MRI detected brain metastases preoperatively in 6 of the 12 patients (3.4% of the total MRI group), whereas CT detected brain metastases preoperatively in 1 of the 11 patients (0.6% of the total CT group). MRI showed a tendency toward a higher preoperative detection rate of brain metastases than CT (p = 0.069). Furthermore, the mean (± SD) maximal diameter of the brain metastases was significantly smaller in the MRI group (12.8 ± 9.1 mm) than in the CT group (20.3 ± 7.0 mm) (p = 0.041). However, the median survival time and 2-year survival rate after treatment of detected brain metastases, respectively, were 10 months and 27% in the CT group and 17 months and 28% in the MRI group. There was no significant difference between the groups in survival time.

Conclusions: Preoperative evaluation and intensive follow-up with MRI could facilitate early detection of brain metastases in patients with potentially operable lung cancer. However, further studies on detection and treatment of the metastatic tumors are considered necessary.

Key Words: brain metastasis • CT • lung cancer • MRI


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Brain metastases are a common mode of general dissemination of lung cancer.1 ,2 Patients with those metastases at their initial staging are generally considered to have a contraindication for resection of their primary lung tumors. And even in the patients who have undergone curative surgery for the primary tumors, brain metastases are frequently considered an initial treatment failure.3

CT of the brain has a well-documented accuracy in detecting metastatic tumors4 and has been described as being of value in the preoperative staging of patients with non-small cell lung cancer who were free of neurologic symptoms.4 ,5 ,6 In our previous study, intensive follow-up with CT was suggested to facilitate the early detection and effective treatment of brain metastases in patients with resected lung cancer.7 Recently, MRI has also started to be used for diagnosing brain tumors,8 and contrast-enhanced MRI has been demonstrated to be very sensitive to small lesions.9

To assess the usefulness of preoperative evaluation and postoperative follow-up with MRI of the brain for the early detection and effective treatment of brain metastases, we prospectively studied 177 patients with potentially resectable non-small cell lung cancer. The results were compared with those of our previous study encompassing 155 patients who had undergone CT.7


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Between January 1989 and December 1995, 332 patients with primary non-small cell lung cancer who were free of neurologic signs and symptoms were listed for surgical treatment. All patients underwent a clinical examination, routine blood test, chest radiography, chest CT, abdominal CT or ultrasonography, and bone scintigraphy, and all were certified as having resectable lung tumors without distant metastases other than those in the brain. For the evaluation of the brain, 155 patients were examined with CT (CT group) between January 1989 and September 1992, and 177 patients were examined with MRI (MRI group) between October 1992 and December 1995 during the 2-week period before thoracic surgery (Table 1 ). Intensive follow-up with CT7 and MRI was also performed on those patients from each group who underwent complete resection of the primary tumors. The study protocols of the examinations are shown in Table 2 . The patients were also scheduled for checkups every 1 to 3 months for 2 years after lung resection.10 Furthermore, when brain metastases were suspected on examination or by the appearance of neurologic symptoms, additional scans were performed more frequently. All patients gave informed consent for preoperative evaluation and postoperative follow-up with brain CT or MRI.


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  		Table 1. Patient Characteristics

 

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  		Table 2. Study Programs With CT and MRI in Evaluation of Brain Metastases

 
CT scans were obtained using a scanner (model 9800; General Electric Medical Systems; Milwaukee, WI) with a 2-s scanning time. The brain was examined from the cranial base to the calvarium using 5- to 10-mm contiguous slices after IV injection of 50 mL of contrast material (iopamidol 300; Schering; Osaka, Japan). MR images from throughout the brain were acquired with an imaging device (MRT-200/RX; Toshiba; Tokyo, Japan) at 1.5 T. Precontrast T1-weighted ([repetition time/echo time] 600 ms/15 ms) and T2-weighted (3,000 ms/80 ms) spin-echo axial sequences were obtained. The field of view was 20 x 20 cm. All sections were 9 mm with 1.6-mm spacing between adjacent sections, and the matrix was 256 x 256. After administering 0.2 mmol/kg gadopentetate dimeglumine (Schering), T1-weighted sequences were repeated.

Treatment for patients with brain metastases that were preoperatively detected depended on the individual physician's order. Metastatic tumors detected postoperatively were usually treated by surgical resection and radiotherapy or radiosurgery for single lesions, and by radiotherapy alone for multiple lesions.

The preoperative demonstration of brain metastases and intracranial recurrence rates within 12 months after operation for primary lung carcinoma and the characteristics of the detected brain tumors were compared between the two groups. The survival of patients with brain metastases was also compared. For comparison of the two groups, we used the unpaired Student's t test for continuous variables and {chi}2 or Fisher's exact test for categorical data. The survival curves were calculated by the Kaplan-Meier method, and comparisons among the curves were made by means of the log-rank test. Values of p < 0.05 were considered to be statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
There were no statistically significant differences between patients examined by CT and MRI with respect to gender, age, histologic type of primary tumor, or clinical stage (Table 1 ).

From the first evaluation to 12 months after surgery for primary lung cancer, brain metastases were observed in 11 patients (7.1%) from the CT group and 12 patients (6.8%) from the MRI group (Table 3 ); the incidence of brain metastases was the same in both groups. Of those patients with brain metastases, MRI detected 6 of 12 patients (3.4% of the total MRI group) preoperatively, whereas CT detected 1 of 11 patients (0.6% of the total CT group). However, about 80% of all detected metastatic tumors in patients from both groups were detected within 6 months after surgery for primary lung cancer. MRI showed a tendency toward a higher preoperative detection rate of brain metastases than CT (p = 0.069).


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  		Table 3. Detectability of CT and MRI in Evaluation of Brain Metastases

 
The clinical data of patients with brain metastases are presented in Table 4 . Single metastases were discovered in 5 of the 11 patients (46%) in the CT group and in 7 of the 12 patients (58%) in the MRI group. The ratios of single and multiple metastases in both groups were almost the same. Seven patients whose brain metastases were detected preoperatively were free of neurologic signs and symptoms. Furthermore, after surgery for the primary lung tumors, six patients from the CT group and four from the MRI group were discovered to have brain metastases in the neurologically asymptomatic state. Those tumors were detected during scheduled follow-up examinations. The remaining four patients from the CT group and two from the MRI group had neurologic signs or symptoms when the brain metastases were found, and their metastases were diagnosed with an extra brain CT or MRI. There was no significant difference between the number of neurologically asymptomatic and symptomatic patients in the two groups.


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  		Table 4. Clinical Data for Patients With Brain Metastases

 
The maximal diameters of brain metastases detected by CT and MRI ranged from 15 to 37 mm and from 4 to 37 mm, respectively. The mean maximal size of brain tumors was significantly smaller in the MRI group than in the CT group (p = 0.041). Of the 23 patients with primary lung tumors who had brain metastases, adenocarcinoma was the most frequent histologic type encountered in both groups. By TN staging, T1/2N0/1 lesions were observed in two patients from the CT group and six from the MRI group, although many other primary tumors were locally more advanced.

Of the 12 patients with a single metastasis, 6 were treated with surgical resection and radiotherapy with or without chemotherapy, 2 were treated with stereotactic radiosurgery with or without chemotherapy, 1 was treated with chemotherapy and radiotherapy, and 3 were treated with radiotherapy alone. Almost all patients with multiple metastases were treated with whole-brain irradiation. For the primary lung tumors in the seven patients with brain metastases that were detected preoperatively, two were treated with surgical resection and chemotherapy with or without radiotherapy, two were treated with chemotherapy and radiotherapy, two were treated with chemotherapy, and one was treated with radiotherapy.

Five patients with a single metastasis and two with multiple metastases survived > 2 years after treatment for their brain tumors (Table 5 ). Regarding the characteristics of those long-term survivors, five patients had N0 lesions, and the remaining two had lymph node metastases. All the patients were discovered to have brain metastases in the neurologically asymptomatic state. The sizes of the brain tumors were < 20 mm in all but one patient. Four of the five patients with a single lesion underwent surgical resection or stereotactic radiosurgery and had a complete response. Of the three patients whose brain tumors were preoperatively detected, patients 1 and 3 in the MRI group underwent pulmonary resection for the primary tumors, and patient 2 received radiation therapy.


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  		Table 5. Survival >2 Yr After Treatment of Brain Metastases*

 
The median survival time after the treatment of brain metastases was 10 months in the CT group and 17 months in the MRI group. The 1- and 2-year survival rates in the CT group were both 27%, whereas in the MRI group the rates were 62% and 33%, respectively (Fig 1 ). The overall median survival time from the beginning of treatment in all patients was 11 months in the CT group and 20 months in the MRI group. The 1- and 2-year overall survival rates in the CT group were 45% and 27%, respectively, whereas in the MRI group they were 87% and 33% (Fig 2 ). There was no significant difference in survival time between the two groups.



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  		Figure 1. Survival curves for patients after the treatment of brain metastases.

 


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  		Figure 2. Overall survival curves for patients from the start of therapy for primary lung tumors or brain metastases.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The incidence of brain metastases in the initial staging of patients with primary lung cancer has been reported to be between 12% and 18%.1 ,2 Furthermore, even after complete resection of primary lung tumors, the occurrence rate has been documented as 1% to 15% of cases, depending on the stage and histologic classification.3

CT has become the radiologic procedure of choice for the diagnosis of brain metastases. Some authors have reported that CT was valuable in the preoperative staging of neurologically intact patients with locally advanced or nonsquamous cell lung carcinoma because these patients have a high risk of metastases.4 ,5 ,6 Moreover, in our follow-up study of patients with completely resected lung cancer, CT has been suggested to be worthwhile for the early detection and effective treatment of brain metastases.7 Recently, MRI has also begun to be used for detection of brain metastases and has been documented to have a higher sensitivity than CT.8 We therefore conducted this prospective study with MRI for pre- and postoperative evaluation of brain metastases in patients with potentially resectable lung cancer, and compared the results with those of a cohort from our previous study using CT.7

Brain metastases occurred at the same incidence in comparable patients from both study populations, that is, about 7% of patients with operable non-small cell lung carcinomas who were free of neurologic symptoms had a risk of brain metastases; this occurrence rate was comparable with those of previous reports.5 ,6 However, although metastases in previous reports were usually detected in patients with locally advanced diseases, one third of our patients with brain metastases had localized primary tumors such as T1/2N0/1 lesions.

Notwithstanding the fact that contrast-enhanced MRI has been demonstrated to be very sensitive for small lesions,9 the ratios of single and multiple metastases detected in both groups were equivalent in our study. When the brain tumors were discovered, the proportions of asymptomatic and symptomatic patients were also the same in the two groups. Nevertheless, MRI was considered to be more sensitive than CT in detecting brain metastases because of the higher preoperative detection rate and significantly smaller mean maximal diameter.

The median survival time after treatment of brain metastases and the 1-year survival rate in the MRI group were slightly longer than those in the CT group. However, the 2-year survival rates of both groups were the same. Similar results were found in overall survival time after the initiation of treatment with all patients. These results are considered to be a result of the fact that MRI is more sensitive for small lesions and can facilitate early detection of brain metastases, creating a lead-time bias that causes the median survival time to appear longer. Meanwhile, despite including patients with multiple lesions, these median survival times after treatment of brain metastases in both groups were similar to those of reported results in surgically resected single brain metastases from lung cancer.12 ,13 Furthermore, seven of our patients were alive > 2 years after treatment for brain tumors. We believe that the treatment results were improved by earlier detection through routine repetitive examinations and consequent improvement of the control of brain metastases.

Of the 12 patients who had a single metastasis, 1 patient from the CT group and 3 from the MRI group were treated with whole-brain irradiation with or without chemotherapy. Only one of those four patients was alive > 2 years after treatment of the metastasis. On the other hand, four of the remaining eight patients who were treated with surgical resection or radiosurgery survived for 2 years. In therapy for brain metastases, stereotactic radiosurgery has recently been advocated because of its effectiveness in treating surgically inaccessible metastases or multiple foci.14 ,15 Moreover, for resectable single metastases, the advantages of radiosurgery over surgical resection have been shown in terms of cost, hospitalization, and wider applicability.16 Surgical treatment of multiple brain metastases has also been reported to be useful in selected patients.17 If more appropriate treatment such as these advanced methods had been aggressively applied to our patients, especially to smaller lesions in the MRI group, we might have obtained better survival statistics.

Preoperative evaluation and follow-up with diagnostic imaging for brain metastases in asymptomatic patients remain controversial issues.18 ,19 Several authors have recommended that brain CT be performed in the staging approach to lung cancer because of its usefulness in the detection of occult metastases, although the stage or histologic type of the primary tumors that is considered necessary for brain evaluation differs between investigators.2 ,4 ,5 ,6 ,20 Some authorities have advocated that the routine use of brain CT or MRI is not warranted in patients without neurologic signs or symptoms because of the marginal cost-effectiveness.21 ,22 There are a few reports about the follow-up of lung cancer patients after curative surgery.7 ,23 ,24 A retrospective study by Virgo and colleagues23 showed that the intensity of follow-up was not significantly related to patient outcome. Walsh et al24 also found that screening for asymptomatic recurrence in patients with resected lung cancer was unlikely to be cost-effective. In both studies, however, it was demonstrated that asymptomatic patients or those patients followed intensively who had recurrences lived longer than symptomatic patients or those patients not followed intensively. Furthermore, as shown in our previous report,7 some patients with asymptomatic brain metastases were cured or had a well-maintained quality of life for a longer period. Therefore, novel studies for specifying high-risk populations for brain metastases from lung cancer are considered necessary, concurrent with discussion of the cost-effectiveness of imaging modalities.

In conclusion, we consider that preoperative evaluation and intensive follow-up with MRI could facilitate early detection of brain metastases in patients with potentially operable lung cancer. Nevertheless, a survival benefit would not be obtained unless more appropriate treatment is applied to the brain metastases. Further studies and discussion of the issue of detecting occult brain metastases in patients with resectable lung cancer is warranted.


   Acknowledgements
 
ACKNOWLEDGMENT: We are grateful to the Divisions of Diagnostic Imaging and Radiation Therapy of Tochigi Cancer Center for their cooperation.


   Footnotes
 
Correspondence to: Kohei Yokoi, MD, Division of Thoracic Surgery, Tochigi Cancer Center, 4–9-13 Yohnan, Utsunomiya, Tochigi 320-0834, Japan; e-mail: kyokoi@tcc.pref.tochigi.jp

Received for publication April 9, 1998. Accepted for publication September 15, 1998.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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