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Computed Tomography Response, But Not Positron Emission Tomography Scan Response, Predicts Survival After Neoadjuvant Chemotherapy for Resectable Non–Small-Cell Lung Cancer

Tawee Tanvetyanon, Edward A. Eikman, Eric Sommers, Lary Robinson, David Boulware, Gerold Bepler

From the Division of Thoracic Oncology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL

Corresponding author: Tawee Tanvetyanon, MD, 12902 Magnolia Dr, Tampa, FL 33612; e-mail: tanvett{at}moffitt.org

	ABSTRACT

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Purpose Tumor response is considered a surrogate marker of survival. We investigated whether tumor response based on computed tomography (CT) scan or whole-body [¹⁸F]fluorodeoxyglucose positron emission tomography (PET) scan after neoadjuvant chemotherapy for resectable non–small-cell lung cancer (NSCLC) is prognostic of survival.

Patients and Methods Two consecutive phase II clinical trials were jointly analyzed. Patients underwent CT and PET scans before and after completion of neoadjuvant chemotherapy, followed by surgery.

Results Eighty-nine patients were included. Patients with a partial or complete response based on Response Evaluation Criteria in Solid Tumors categories (n = 33) had a better overall survival than those with stable or progressive disease (n = 56; median survival time, not reached v 36 months, respectively; P = .04). Of all patients, those with response in the highest quartile had 1- and 2-year survival rates of 100% and 81%, respectively, compared with 77% and 61%, respectively, among patients in the lowest quartile. However, on the basis of visual analysis of PET scan, patients with a metabolic response (n = 28) had no significant difference in survival compared with patients without response (n = 61; median survival time, 35.6 months v not reached, respectively; P = .94). In addition, on the basis of a semiquantitative analysis of PET scan, using at least 30% reduction in tumor metabolism as a response (n = 59), we also found no significant difference in survival among those with or without response.

Conclusion Among patients with resectable NSCLC treated with neoadjuvant chemotherapy, we found no evidence that tumor response by PET scan after chemotherapy is prognostic of survival; however, response by CT scan was associated with better survival.

	INTRODUCTION

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Tumor response after chemotherapy is a surrogate marker of survival. Response, as manifested by shrinkage of lesions seen by a computed tomography (CT) scan, reflects a reduction of tumor load and generally translates into a survival benefit.¹ Previous studies conducted in patients with advanced or metastatic non–small-cell lung cancer (NSCLC) have shown that response to chemotherapy as determined by CT scan after 8 weeks of treatment is a strong predictor of subsequent survival.² In addition, for patients with nonmetastatic cancer, response early in the course of disease often facilitates subsequent effective treatments, resulting in favorable overall survival as well.³

Besides the response as seen by CT scan, recent data suggest that a response by [¹⁸F]fluorodeoxyglucose (FDG) positron emission tomography (PET) after chemotherapy may have a significant correlation with survival in NSCLC.⁴ Among patients with unresectable (but nonmetastatic) NSCLC receiving definitive radiation or chemoradiotherapy, it has been reported that tumor response from PET scan is a better survival predictor than tumor response from CT scan.⁵ Among those with advanced or metastatic disease, tumor response by PET scan—defined as 20% reduction of tumor metabolic activity after the first cycle of chemotherapy—is also associated with an improved survival.⁶

Although tumor response by both CT scan and PET scan seems to have prognostic significance among patients with advanced NSCLC, this association is less clear among patients who have earlier stages of disease and undergo neoadjuvant chemotherapy. Most available data are derived from patients with stage III NSCLC. For example, in patients with stage III NSCLC who underwent neoadjuvant chemotherapy followed by surgery, the median overall survival was almost four times longer among patients with no significant residual glucose metabolism detected than those with residual glucose hypermetabolism.⁷ In patients with stage III NSCLC, a greater than 50% decrease in the metabolic activity of the tumor by PET scan after three cycles of induction chemotherapy was associated with an improved survival.⁸

To date, however, limited data are available on patients who have early, resectable stages of NSCLC (ie, stages IB and II and resectable stage III). One study has suggested that tumor response by CT scan after neoadjuvant chemotherapy is prognostic of survival,⁹ but limited information is currently available with regard to the prognostic value of a response by PET scan. In this article, we investigated the prognostic value of tumor response, assessed by CT scan and PET scan, after neoadjuvant chemotherapy for patients with resectable NSCLC.

	PATIENTS AND METHODS

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Patients and Treatments
Patients were included from two prospective clinical trials of neoadjuvant chemotherapy followed by surgical resection. Both clinical trials enrolled patients with histologically confirmed NSCLC who had resectable disease, including stages IB, II, IIIA, or IIIB (T4 with two lesions in one lobe).^10,11 Patients with N2 disease were eligible if surgically resectable without multistation or bulky mediastinal lymph node involvement. Staging procedures included mediastinoscopy in all patients. Preoperative chemotherapy consisted of gemcitabine 1,000 mg/m² and vinorelbine 25 mg/m² administered on days 1, 8, 22, and 29 or gemcitabine 1,500 mg/m² and pemetrexed 500 mg/m² administered on days 1, 15, 29, and 43. Patients had thoracotomy between days 50 and 70 in the first study and between days 64 and 77 in the second study.

Imaging Studies
PET and CT scans were required before and after neoadjuvant chemotherapy. The first tests were performed before enrollment to confirm protocol eligibility; the second tests were to confirm resectability after chemotherapy. The second tests were performed between days 43 and 50 in the first study and between days 50 and 63 in the second study. For patients who had PET scans performed at our institution, semiquantitative analysis was recalculated by an independent nuclear radiologist (E.A.E.) who was not aware of the previous interpretation. These scans were performed on a Siemens Biograph PET-CT scanner that provided PET images with CT images for lesion localization (Model CTI 3201958-00; Siemens Medical Solution, Malvern, PA). After an overnight fast, the patients received FDG, and the scan started approximately 90 minutes after the injection. Fusion PET-CT images were obtained in all patients. Semiquantitative evaluation was based on the standardized uptake value (SUV), which is calculated as the ratio of measured activity concentration over an assumed homogeneous distribution of the applied radioactivity in the whole body. The maximum SUV in the tumor site (SUV_max) was measured using a volumetric region-of-interest technique with standard image analysis software (SynGo VX49b-Leonardo VD30B; Siemens AG, Berlin, Germany).

Response
Radiographic response was determined using Response Evaluation Criteria in Solid Tumors (RECIST), which considers a 30% or greater reduction in the sum of unidimensional tumor measurement as a response.¹² Metabolic response was evaluated based on visual analysis in all patients. For patients with multiple lesions, the most hypermetabolic lesion was taken as an index lesion. PET response was defined as the presence of a significant decrease in the metabolism of the index lesion by direct comparison of the pre- and postchemotherapy scans as determined by a reading nuclear radiologist or the resolution of hypermetabolic area in part or all of the known malignant lesions. In a group of patients with available data on SUV_max, PET response was also determined by a semiquantitative analysis. Response was defined as a 30% or greater reduction in the SUV_max to correspond with the radiographic response criteria. In addition, an exploratory analysis based on a 50% or greater reduction in the SUV_max was performed.

Statistical Considerations
Survival was estimated using the Kaplan-Meier method, and survival curves stratified by PET response and CT response were generated. Overall survival was measured from the date of first chemotherapy to the date of death or last follow-up. The generalized Wilcoxon test was performed to test for a difference in overall survival between groups. To further examine survival for PET response, a multivariable, stepwise Cox proportional hazards regression analysis was performed using backwards elimination (significance level to stay at P = .15). Kendall's and Spearman's correlation coefficient were also used in the correlation analysis. All statistical analyses were performed using SAS statistical software (Version 9.1; SAS Institute, Cary, NC).

	RESULTS

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Patient Characteristics and Treatments
There were 114 patients; 62 were from the gemcitabine plus vinorelbine study, and 52 were from the gemcitabine plus pemetrexed study. Of these, 89 patients (78%) completed both pre- and postchemotherapy CT and PET scans (Table 1). All CT scans were performed with the use of intravenous nonionic contrast. The median thickness of CT slice was 5 mm in both pre- and postchemotherapy scans (range, 4 to 8 mm and 5 to 8 mm, respectively). For PET scanning, the median administered dosages of FDG were 12.7 and 12.0 µCi in pre- and postchemotherapy scans, respectively (range, 7 to 30 µCi and 8.7 to 14.9 µCi, respectively). The median serum glucose levels in these patients, immediately before pre- and postchemotherapy PET scans, were 116 and 107 mg/dL, respectively (range, 85 to 208 mg/dL and 79 to 214 mg/dL, respectively). Chemotherapy was well tolerated, and the toxicity profile has been previously reported.^10,11 All but eight patients underwent a surgical resection of lung cancer. Of the patients who underwent resection, 71 of 81 patients had a complete resection. To date, 34 patients have died. The median survival time of the entire cohort has not been reached. The 1-year and 2-year survival rates are 85% (95% CI, 76% to 91%) and 71% (95% CI, 60% to 79%), respectively.

View larger version (19K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Plots demonstrating responses by computed tomography (CT) and positron emission tomography (PET) scan of each patient.

View larger version (10K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Overall survival stratified by Response Evaluation Criteria in Solid Tumors (RECIST) category (patients with a complete or partial response v patients with a stable or progressive disease). CT, computed tomography.

View larger version (12K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 3. (A) Survival stratified by positron emission tomography (PET) response category based on visual analysis (patients with a response v patients without a response. (B) Survival stratified by PET response category based on semiquantitative analysis with 30% metabolic reduction cutoff (patients with a response v patients without a response).

To parallel the radiographic criteria, we first considered a 30% or greater reduction in the SUV_max as a response. We found no significant difference in survival between patients who achieved (n = 24) and who did not achieve response (n = 35; median survival time, not reached in both groups; P = .70; Fig 3B). We then explored the use of a 50% or greater reduction in the SUV_max as a metabolic response. Again, we found no significant difference in the survival between patients who responded (n = 10) and patients who did not (n = 49; median survival time, 26.9 months v not reached, respectively; P = .57).

Impact of Clinical Stage, Tumor Size, and Completeness of Surgical Resection on Survival
We performed analyses incorporating the influences of stage, tumor size, and completeness of resection on survival. In this cohort, we did find a survival difference among stages, but no significant difference in the CT or PET responses among stages was observed. The median survival times for patients with stage I, II, and III disease were not reached, not reached, and 27 months, respectively (P = .005). We also found a survival difference between patients who had complete and incomplete surgical resection (median survival time, not reached v 14 months, respectively; P = .03). Finally, we factored in the tumor size because measurements on CT scans were unreliable for small lesions.¹³ To adjust for these confounders, we performed a Cox multivariable regression analysis.

In the first analytic model, we took stage, tumor size, completeness of surgical resection, and response by RECIST into consideration. After adjusting for stage and completeness of surgical resection, the response by CT scan remained a significant survival predictor (hazard ratio = 0.25; 95% CI, 0.07 to 0.94; P = .04). In this model, stage was also a significant survival predictor (P = .05). Tumor size was of borderline significance (P = .07). However, the completeness of resection was not a significant survival predictor (P = .14). We also found that the effect of CT scan response on survival was clearest among patients with stage III disease; CT responders (n = 11) had a median survival time of 35.6 months compared with 15.5 months in nonresponders (n = 25; P = .02; Fig 4C). However, the prognostic value of CT scan response was unclear among patients with stage I and II disease. In these patients, median survival times were not reached in both the responder groups and the nonresponder groups. Overall, we found no significance differences among responders versus nonresponders who had stage I or II disease (P = .74 and P = .27, respectively; Figs 4A and 4B).

View larger version (10K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 4. Influence of tumor stage on the survival as stratified by Response Evaluation Criteria in Solid Tumors (RECIST) category. Survival of patients with (A) stage I, (B) stage II, and (C) stage III disease. CT, computed tomography.

Correlation Between PET and CT Responses
To understand whether there was a close relationship between PET and CT response, we first examined the PET response by visual analysis and the CT response in 89 patients. In all, there were 28 patients with a PET response and 33 patients with a complete or partial response by CT scan. PET response by visual reading and CT response demonstrated a weak, although significant, correlation; on the basis of a correlation coefficient in which the values of 1.0 or –1.0 were the strongest correlation and 0 was the weakest, the Kendall's was 0.28 (P = .008).

Second, we examined the correlation between PET response by semiquantitative reading and the CT response in 59 patients. Again, PET response showed a weak but significant correlation with CT response; Spearman's correlation coefficient was –0.34 (P = .008). Finally, we investigated whether the use of SUV_max after neoadjuvant chemotherapy alone would be predictive of survival. Using a Cox regression model adjusting for stage and completeness of resection, the postchemotherapy SUV_max by itself was not predictive of survival (P = .44).

	DISCUSSION

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On the basis of data from our two prospective trials of neoadjuvant chemotherapy followed by surgery in resectable NSCLC, we found that the tumor response by CT scan correlated with survival, especially for patients with stage III disease. However, the tumor response by PET scan was not predictive of survival. These findings remained true after adjusting for completeness of subsequent surgical resection, tumor size, and stage. Because neoadjuvant chemotherapy followed by surgery has now been shown to provide a survival benefit over surgery alone¹⁴ and because CT scan and PET scan are recommended tests before surgery, clinicians may become more likely to face the daunting task of interpreting a response from PET scans and CT scans in this clinical setting.¹⁵

The observation that patients with a tumor response from CT scan had a superior survival is not surprising; a reduction in tumor size might have facilitated a complete surgical resection, resulting in a favorable survival. However, the observation that patients with a tumor response from PET scan did not have an improved survival is quite unexpected. What could have accounted for this finding?

First, it may help to interpret this in the context of existing literature on PET response and survival among patients with nonmetastatic NSCLC. Our search of the MEDLINE database identified nine pertinent studies—three from induction chemotherapy trials, four from chemoradiotherapy trials, and two from mixed approaches (Table 2). Among the trials of induction chemotherapy, the observed response rate by PET scan was high, ranging from approximately 50% to 60%. In two of these trials in which a 50% or greater reduction in SUV_max was considered as a response, the response by PET scan was found to be a significant predictor of survival. In our trial, if considering 50% or greater reduction in SUV_max as response, the response rate was 17%, which is relatively low. It seemed that our chemotherapy regimens were less active. It is possible that this has masked any potential prognostic value of a response by PET scan.

Third, the lack of prognostic value of the PET scan may stem from the determination of PET scan response based on visual analysis that was used in our study. Although response based on visual analysis has been used in previous studies and is perhaps the most widely used criteria in clinical practice, this approach is subjected to an interpretation by radiologists, who may vary in the stringency of interpretation.²³ In addition, out of a research setting, this problem can be further exacerbated by scans performed at different facilities. Interfacility technical variability, including time from injection of radioactive glucose until scan is performed, can further limit its prognostic accuracy.²⁴

Our study has a number of limitations. First, the patient sample size may be too small to detect subtle differences between groups, although our report constitutes one of the largest numbers of patients with early-stage NSCLC receiving neoadjuvant chemotherapy (Table 2). Second, data on PET scan by semiquantitative analysis were not available in all patients, although the group of patients with available data seemed to be representative of the entire cohort, and it seems unlikely that a major prognostic value of a response by PET scan exists based on current data. Finally, it is possible that the results from visual analysis of PET scan in our study may not be generalizable, although the PET scan reports in our studies emanated from various radiologic facilities in diverse locations, and we believe that these are representative of what clinicians are facing in current practice.

In summary, for patients with resectable NSCLC undergoing neoadjuvant chemotherapy, the tumor response based on CT scan seems to have a prognostic value on survival, but the tumor response by PET scan, either by visual analysis or semiquantitative reading, does not necessarily portend a good prognosis. Clinicians should use caution in interpreting a tumor response by PET scan in this clinical setting.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Conception and design: Tawee Tanvetyanon, Edward A. Eikman, Gerold Bepler

Financial support: Gerold Bepler

Administrative support: Gerold Bepler

Provision of study materials or patients: Tawee Tanvetyanon, Edward A. Eikman, Eric Sommers, Lary Robinson, Gerold Bepler

Collection and assembly of data: Tawee Tanvetyanon, Edward A. Eikman, Gerold Bepler

Data analysis and interpretation: Tawee Tanvetyanon, Edward A. Eikman, Lary Robinson, David Boulware, Gerold Bepler

Manuscript writing: Tawee Tanvetyanon, Edward A. Eikman, Lary Robinson, David Boulware, Gerold Bepler

Final approval of manuscript: Tawee Tanvetyanon, Edward A. Eikman, Eric Sommers, Lary Robinson, David Boulware, Gerold Bepler

	NOTES

 
Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted February 27, 2008; accepted June 10, 2008.

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