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Ann Thorac Surg 2004;77:254-259
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

Positron emission tomography scanning poorly predicts response to preoperative chemotherapy in non-small cell lung cancer

^a Department of Cardiothoracic Surgery, Weill-Cornell Medical Center, New York, New York, USA

Accepted for publication July 17, 2003.

^* Address reprint requests to Dr Altorki, Department of Cardiothoracic Surgery, Suite M404, Weill Medical College of Cornell University, 525 East 68th St, New York, NY 10021, USA.
e-mail: nkaltork{at}med.cornell.edu

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
BACKGROUND: The ability to accurately predict pathologic response to preoperative chemotherapy may have a significant impact on the treatment strategy for non-small cell lung cancer (NSCLC). The purpose of this study was to examine the accuracy of positron emission tomography (PET) scanning in predicting the pathologic response to preoperative chemotherapy in the primary tumor and draining lymph nodes.

METHODS: A total of 25 patients were enrolled in two separate phase II trials investigating induction chemotherapy for NSCLC. All patients underwent pre-treatment and post-treatment PET scans followed by surgical resection. A significant PET scan response was defined as a reduction in the standard uptake value by 50% or more. We defined a major pathologic response as either no disease or microscopic disease only in the primary tumor. The percentage change in standard uptake value was then calculated and correlated with pathologic response in the primary tumor. In addition, the presence or absence of nodal metastases as determined by the postchemotherapy PET scan was compared with final pathologic nodal stage.

RESULTS: The positive and negative predictive values for PET detection of major pathologic response in the primary tumor were 43% and 100%, respectively. Positron emission tomography did not accurately predict nodal status in 52% of patients. The positive and negative predictive values of PET to detect node-positive disease were 73% and 64%, respectively. For N2 disease the positive predictive value of PET scans was less than 20%.

CONCLUSIONS: Positron emission tomography scanning does not reliably predict pathologic response to preoperative chemotherapy in NSCLC in either the primary tumor or the draining lymph nodes.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Positron emission tomography (PET) scanning has been shown to be accurate in predicting the pathologic stage of patients with nonsmall cell lung cancer (NSCLC) undergoing pulmonary resection [1, 2]. Positron emission tomography scanning is superior to conventional computed tomography (CT) scans in staging mediastinal lymph nodes with a reported sensitivity of 87% to 90% and specificity of 85% [3, 4]. In addition PET scanning has demonstrated accuracy in determining the extent of extrathoracic disease such as bone, adrenal, and hepatic metastases [5–7]. Based in large part on these studies PET scanning has become a routine component of the preoperative evaluation of patients with NSCLC along with CT scans and mediastinoscopy.

A significant proportion of patients with nonsmall cell lung cancer who ultimately undergo resection may have received preoperative chemotherapy either for proven N2 disease or within the context of clinical trials investigating preoperative chemotherapy for earlier stage disease. The ability of PET scans to accurately predict response to chemotherapy in this patient population has not been well studied. However evaluation of the response to induction chemotherapy is critical to determine both prognosis and options for additional treatment. Patients who have no residual mediastinal nodal involvement after chemotherapy for proven N2 disease have been shown to have a survival rate as high as 54% compared with 17% for those who do [8, 9]. Similarly, patients with a complete pathologic response in the primary tumor have a significantly increased survival rate compared with those with residual disease [10]. Therefore, accurate documentation of a response to chemotherapy, particularly in the mediastinal nodes, may influence the decision to proceed with either surgical resection or definitive chemoradiation.

In the present study, we prospectively evaluated the ability of PET scanning to predict both the response of the primary tumor and nodal disease to chemotherapy. All patients underwent preoperative chemotherapy, before and after chemotherapy PET scans, and surgical resection irrespective of PET results. Thus the change in PET activity after chemotherapy could be measured and correlated with pathologic response.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Patient selection
Twenty-five patients enrolled in two separate phase II trials investigating the role of preoperative chemotherapy in NSCLC formed the basis of the present study. In each trial patients were eligible for inclusion if they had biopsy-proven NSCLC that was clinical stage IB–IIIA. Nineteen of 25 patients were staged with a mediastinoscopy before treatment. Each patient was evaluated with a CT scan as well as a PET scan utilizing F-18-fluorodeoxyglucose before and after induction chemotherapy. All PET scans were performed on a dedicated PET scanner. The post-treatment scans were performed 2 weeks after the final course of chemotherapy. Four weeks after the final course of chemotherapy all patients underwent anatomic pulmonary resection and complete mediastinal lymph node dissection (levels 2, 4, 7, 8, and 9 on the right side and levels 5, 6, 7, 8, and 9 on the left side).

In the first study, patients were treated with two cycles of carboplatin and paclitaxel in conjunction with celecoxib, a selective COX-2 inhibitor. The results of this study have been reported elsewhere [11]. In the second trial patients were treated with two cycles of irinotecan and paclitaxel as well as celecoxib. This trial is currently accruing patients. Seven patients from that study who have been surgically staged are included in this report.

Data analysis
Data regarding the primary tumor and response to chemotherapy were collected prospectively. In addition, the standard uptake values measured in the primary tumor on the pre- and post-chemotherapy PET scans were recorded and the percent change in the standard uptake value calculated. A major PET scan response was defined as a reduction in the standard uptake value by 50% or more. The percent change in standard uptake value of the primary tumor was correlated with presence or absence of a major pathologic response. A major pathologic response was defined as either no tumor or residual microscopic disease only.

In addition, the clinical nodal stage of the post-chemotherapy PET scan was determined and compared with the final pathologic stage. Hilar or mediastinal nodal stations were considered to be positive on the PET scan if a standard uptake value of 2.5 or greater was measured [12, 13]. This standard uptake value level was chosen since it approximates the typical standard uptake values of the mediastinal blood pool [14].

The ability of PET scanning to predict both a major pathologic response and final nodal stage was determined in the following manner. A major PET scan response without a major pathologic response was considered a false-positive study. A major pathologic response without a major PET scan response was considered a false-negative study. PET scan documentation of mediastinal disease without evidence of N2 nodes in the surgical specimen was also considered to be a false-positive study, and positive N2 nodes without evidence of mediastinal disease on the post-treatment PET scan considered a false-negative study. Sensitivity, specificity, accuracy, and positive and negative predictive values were then calculated.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Patient characteristics are listed in Table 1. Seven of 19 patients who underwent mediastinoscopy were documented to have N2 disease before induction chemotherapy. Six patients with clinical IB disease declined mediastinoscopy before induction therapy, all of whom had no PET activity in the mediastinum.

View larger version (34K): [in this window] [in a new window]   Fig 1. Percent change in standard uptake value (SUV) in 25 patients undergoing induction chemotherapy. A 50% reduction in SUV (dashed line) was defined as a major positron emission tomography (PET) scan response. Each column represents a single patient. Black columns represent patients with a major pathologic response and gray columns represent patients without a major pathologic response.

PET scan staging of nodal disease
The results of nodal staging are presented in Tables 2 and 3. Overall the post-chemotherapy PET scan accurately predicted nodal stage in only 12 patients (48%). Among 12 patients with pN0 disease, 9 were accurately predicted by preoperative PET scans for a specificity 75%. Among the 13 patients with either pN1 or pN2 disease, only 8 were predicted to be node-positive by PET scan. Thus the sensitivity of PET scanning for residual nodal disease at any nodal station was 61%. The positive and negative predictive values for residual nodal disease (pN1 or pN2) at any station were 73% and 64% respectively. When the PET scan was evaluated for accuracy in predicting mediastinal nodal involvement only, 1 of 5 patients was correctly predicted by PET to have N2 disease. The sensitivity and specificity for pN2 were 20% and 70% respectively. The positive predictive value, negative predictive value, and overall accuracy were 14%, 77%, and 60%, respectively.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Techniques currently available to restage lung cancer patients after chemotherapy include repeat CT scans as well as invasive procedures such as mediastinoscopy and thoracoscopy. Unfortunately, these modalities have several drawbacks. Documentation of residual disease by CT scanning is based solely on morphology. It is well established that patients may demonstrate complete fibrosis of their primary tumor without an appreciable change in overall size. As expected, the accuracy of CT scanning in the setting of induction therapy is reported to be quite low [15, 16]. Although mediastinoscopy is a proven tool in the initial staging of patients with lung cancer it is slightly more difficult to perform after induction chemotherapy. Patients have often undergone the procedure once before and the dense fibrosis associated with prior surgery may render the normal anatomic planes difficult to visualize. Small studies have shown that redo mediastinoscopy after induction therapy is technically feasible and safe; however the accuracy of this procedure is lower than that of the initial mediastinoscopy [17, 18].

Positron emission tomography would seem to be an ideal tool to restage patients after induction chemotherapy. Positron emission tomography scans are able to differentiate benign from malignant tissues based on their metabolic rate rather than size criteria. Malignant cells have been shown to have an increased rate of glucose metabolism compared with nonmalignant tissue [19]. Residual disease after induction therapy therefore would be expected to accumulate the FDG tracer and allow patients to be restaged on a physiologic basis.

To date, three studies have reported the accuracy of PET scans to restage patients in this setting. The first reported on 9 patients who underwent surgical staging after pre-chemotherapy and post-chemotherapy PET scans [20]. In this small pilot study PET scanning was shown to be 100% accurate in predicting the mediastinal nodal stage. In the second study, the records of 56 patients who had undergone PET scans after a variety of induction chemotherapy and chemoradiotherapy regimens were retrospectively reviewed [13]. Positron emission tomography scans were shown to accurately predict pathologic response in the primary tumor but predicted nodal status in only 52% of patients. However, only the post-treatment PET scans were available for review in this study and therefore it was not possible to quantitate the change in PET scan activity before and after chemotherapy and investigate its significance.

In the most recent study, 34 patients who had undergone preoperative chemotherapy were prospectively followed up [21]. Each patient was imaged with both CT and PET scans before and after induction therapy. Twenty-five patients ultimately underwent resection with lymph node dissection. Nine additional patients had either persistent N2 disease or a T4 lesion discovered at the time of thoracaotomy and did not undergo resection. The authors found that PET scanning was both 100% sensitive and specific for documenting involvement of N2 paratracheal nodes. Three issues may limit the validity of these results. First, the patient population was heterogeneous; 7 patients were treated with concurrent radiation therapy and the time from the final course of chemotherapy to PET scanning varied from 2 weeks to 2 years. In addition, nodal stations rather than patient number were used as the denominator in the analysis. Finally, a distinction was made in the analysis between paratracheal and other N2 nodes. The clinical significance of this distinction is unclear and when other N2 nodes are considered the sensitivity of PET decreased to only 50%.

Unfortunately, the present study does not confirm the hope that PET scans may replace CT scans and mediastinoscopy to restage patients after induction treatment for NSCLC. In 25 patients undergoing preoperative chemotherapy, PET scans were found to have a high sensitivity (100%) but a low specificity (58%) in predicting response of the primary tumor to induction chemotherapy. Only 6 of 14 of patients who exhibited a significant reduction in PET activity had a major pathologic response in the resected specimen, 5 of whom had residual microscopic disease. Based on these data PET scanning of the primary tumor may be useful in identifying nonresponders in whom other treatment strategies may be considered. More importantly, a significant reduction in PET activity (more than 50% in this study) after chemotherapy is often not associated with a complete tumoricidal effect in the primary lesion. Even when the reduction of standard uptake values approaches 100%, residual microscopic disease may still be present. In this study, 2 patients had no PET activity at the primary tumor site after chemotherapy despite residual microscopic disease in one and gross residual disease in the other.

The ability of PET scanning to accurately predict nodal stage was also disappointing. More than 50% of patients were inaccurately staged with PET scans and the false-positive and false-negative rates were unacceptably high. However, the critical question in restaging after induction therapy is the presence or absence of residual N2 disease. Although the number of N2 patients in this study was small, the ability of PET scans to predict residual N2 disease was poor. Positron emission tomography scans were found to have a positive predictive value of only 16% and therefore consistently overstaged the mediastinum. It is true that a significant minority of patients in this study had large, central tumors that required pneumonectomy for complete resection. It would be expected that the ability of PET scanning to distinguish mediastinal nodal disease from the primary tumor in this setting would be poor. In fact, the accuracy of PET scans in this subset of patients was a disappointing 20%. However, when the subset of patients with peripheral tumors was considered separately, the overall accuracy of nodal staging improved to only 66% (data not shown).

Although the accuracy of CT scans to restage patients after induction therapy is reported to be low, PET scanning performed no better when the two modalities were compared directly. Computed tomography scans had an accuracy of 92% in predicting a major pathologic response in the primary tumor (versus 68% for PET scans) and accurately staged nodal disease in 56% of patients (versus 48% for PET scans).

There are several potential limitations of our conclusions. For example, all patients in this study underwent repeat PET scans 2 weeks after the last dose of chemotherapy. This schedule was followed to allow patients to undergo resection in a timely manner after the conclusion of chemotherapy. It is possible that delaying the PET scan for an additional 2 to 4 weeks may have increased the accuracy of the PET scans; however, the practicality and clinical utility of that approach is questionable.

Another potential limitation of the study is the threshold at which a significant PET response was defined. In this study, a threshold of a 50% reduction in standard uptake values was chosen. Certainly this threshold could be altered to increase the specificity of the test. However, if a decline in standard uptake values of 60% were to be used, 1 patient with a major pathologic response would be falsely considered a nonresponder. If a 75% reduction was designated 2 responders to chemotherapy would be misidentified, lowering the sensitivity of PET scans to only 66% (see Fig 1). Although a response to chemotherapy is not currently used to determine which patients should be offered resection, it seems reasonable that the sensitivity of a test to document response should be as high as possible. In this way, the false-negative rate would be low, preventing patients who have a false-negative PET scan from being denied surgery.

Another limitation is the standard uptake value at which we considered nodal metastases to be present, in this case a standard uptake value of 2.5. There appears to be limited information in the literature regarding the appropriate standard uptake value to indicate nodal disease. We selected a standard uptake value of 2.5 as a cut-off value as it is reportedly typical of tracer uptake in the mediastinal blood pool. Most investigators have suggested a standard uptake value in the 2.5 to 4.4 range [14, 22]. Higher standard uptake values would perhaps be more appropriate in areas with a higher prevalence of granulomatous mediastinal disease.

It is unclear why PET scans are able to accurately predict pathologic stage in patients who have undergone surgical resection and yet are poor in staging patients who have received induction chemotherapy. It is possible that the cytotoxic effect of chemotherapy would lead to tumor cell death as well as an influx of metabolically active immune cells such as macrophages and tumor infiltrating lymphocytes. Cell turnover and migration of immune cells into the primary tumor would have opposite effects on measurements of overall metabolism and thus the accuracy of PET scans in this setting may be diminished.

Refinements in the technique of positron emission tomography may improve its ability to determine response to induction chemotherapy in the future. The standard uptake value is considered to be only a semiquantitative determination of glucose uptake. The glucose metabolic rate is a more quantitative indicator and has been shown in a single study to correlate with pathologic response in the primary tumor [23]. However this measurement requires more complex mathematical modeling than is routinely performed. At the present time we consider PET scanning to have limited accuracy both in determining the response of the primary tumor and extent of nodal disease after induction chemotherapy for nonsmall cell lung cancer.

	References

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