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Eur J Cardiothorac Surg 2008;34:892-897. doi:10.1016/j.ejcts.2008.07.023
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Clinical implication and prognostic significance of standardised uptake value of primary non-small cell lung cancer on positron emission tomography: analysis of 176 cases

Nael Al-Sarrafa,b,*, Kathy Gatelya, Julie Luceyc, Rashid Aziza, Kishore Doddakulaa, Lorraine Wilsonc, Eillish McGoverna, Vincent Younga

a Department of Cardiothoracic Surgery, St. James's Hospital, Dublin 8, Ireland
b Department of Thoracic Surgery, Chest Disease Hospital, Kuwait
c Department of Nuclear Medicine, Blackrock Clinic, Dublin, Ireland

Received 6 March 2008; received in revised form 7 July 2008; accepted 14 July 2008.

* Corresponding author. Address: Department of Thoracic Surgery, Chest Disease Hospital, Al-Deya, P.O. Box 15179, 35452 Kuwait, Kuwait. Tel.: +965 6600543; fax: +965 4741504. (Email: trinityq8{at}hotmail.com).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Limitations of the...
 6. Conclusion
 References
 
Objective: We sought to assess the clinical implication and prognostic significance of maximum standardised uptake value (SUVmax) of primary non-small cell lung cancer (NSCLC) staged by integrated PET-CT. Methods: A retrospective review was carried out on 176 consecutive patients with histologically proven NSCLC who underwent staging with integrated PET-CT prior to curative intent surgical resection. SUVmax of primary NSCLC were measured and correlated with tumour characteristics, lymph node involvement, surgical stage, type of surgical resection and survival following resection. Results: SUVmax was significantly higher in centrally located tumours, tumours ≥4.0 cm, squamous cell subtype, poorly differentiated tumours, advanced T stage, advanced nodal stage, pleural invasion, and patients requiring complex surgical resection. SUVmax value of 15 was the best discriminative cut-off value for survival generated by log-rank test. When patients were stratified based on this value, those with SUVmax >15 were more likely to have centrally located tumours, squamous cell subtype, advanced T stage, advanced nodal stage, advanced American Joint Committee on Cancer (AJCC) stage, larger tumour size and required more advanced surgical resections than a simple lobectomy. Overall survival was significantly longer for patients with SUVmax ≤15 than those with SUVmax >15. Furthermore, nodal stage specific survival following resection (i.e. non-N2 and N2) were significantly better in patients with SUVmax ≤15 than SUVmax >15. Conclusion: SUVmax correlates with tumour characteristics, surgical stage and prognosis following resection. SUVmax may be a useful preoperative tool, in addition to other known prognostic markers, in allocating patients with potentially poor prognosis preoperatively to neoadjuvant chemotherapy prior to resection in order to improve their overall survival. Prospective and randomised trials are warranted.

Key Words: Positron emission tomography • Non-small cell lung cancer • Standardized uptake value • Survival


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 5. Limitations of the...
 6. Conclusion
 References
 
Lung cancer remains the leading cause of death from all cancer-related mortalities and carries a dismal prognosis. Despite great advances in chemotherapy, surgery remains the only curative method. Therefore, adequate preoperative staging should be emphasised to determine the best treatment approach and to avoid inappropriate thoracotomies. Positron emission tomography (PET) is superior to conventional radiological staging such as CT in the preoperative staging of non-small cell lung cancer (NSCLC) [1]. In PET studies, tumour metabolism is reflected by a semi quantitative measurement referred to as standardised uptake value (SUV) which is calculated by a standard formula [2]. In this paper, we sought to assess the clinical implication and prognostic significance of maximum standardised uptake value (SUVmax) of primary NSCLC patients undergoing curative intent surgical resection. The advantage of preoperatively identifying patients with poor prognostic indicators is that these cases could be treated more aggressively in the first instance by neo-adjuvant chemotherapy prior to aggressive type surgical resection in the hope of improving their poor long-term outcome.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 5. Limitations of the...
 6. Conclusion
 References
 
2.1 Patients
Between September 2004 and January 2007, 176 consecutive patients with histologically proven NSCLC who underwent lung resection and systematic lymph node dissection (SLND) in the department of cardiothoracic surgery at St. James's hospital were retrospectively reviewed. All these patients underwent staging with integrated PET-CT (as an adjunct to CT) 4 weeks prior to lung resection. All clinical, operative, radiological and pathological findings were analysed retrospectively through the review of patients charts, pathological reports and radiological imaging. SUVs were measured prospectively in all patients. Histological classification of NSCLC was based on that of WHO classification. Pre- and postoperative staging was based on the tumour-node metastasis (TNM) staging system [3]. Diabetic patients with BM ≥ 8 mmol l–1 (n = 16) and those who received neo-adjuvant/induction chemotherapy (n = 18) over the study period were excluded. Only patients who underwent surgical resection were enrolled. This study was approved by the institutional review board.

2.2 PET-CT
We have previously reported our technique in PET-CT scanning [4,5]. 18FDG-PET-CT was performed using integrated PET-CT scanner (Discovery ST, GE Medical systems). Patients were fasting for 6 h prior to the procedure and the images were obtained 1 h after intravenous administration of 18FDG. Patients remained resting for an uptake period of 1 h. Images were obtained from base of the skull to mid-thigh level. Attenuation corrected images were obtained and interpreted by an experienced nuclear medicine physician. Primary lesions were considered pathological (i.e. positive) if a definite localised area of higher 18FDG uptake than the surrounding normal tissue exists (excluding physiological uptake).

Nodal uptake with a standardised uptake value (SUVmax) >2.5 were considered positive. For determination of SUV, a cylindrical region of interest (ROI) was manually placed over the tumour site on the hottest trans-axial slice. The activity concentration within the ROI was determined and expressed as the SUV, where SUV is the ratio of the activity in the tissue to the decay corrected activity injected into the patient. All SUV measurements were normalised for patient body weight. The maximum SUV within a region of interest (SUVmax) was used as our reference measurement.

2.3 Surgical resection and pathological examination
Lung resection with SLND was carried out through posterolateral thoracotomy. The extent of SLND was previously reported [5,6]. Cervical mediastinoscopy was employed in cases where positive uptake is detected in mediastinal nodes (N2 or N3) with nodal SUVmax >2.5 as previously reported [5,6]. Resected lung tissue and lymph nodes were examined by pulmonary histopathologist for the presence or absence of malignancy using standard techniques with immunohistochemistry performed as per pathologist discretion. Vascular invasion refers to the presence of malignant cells in the blood vessel lumen detected histologically following resection.

2.4 Data analysis
The relationship between SUVmax of primary NSCLC and the different variables were analysed using appropriate non-parametric statistics namely, the Mann–Whitney, Kruskal–Wallis, Fisher's exact test, or the chi-square test. ANOVA was used where appropriate. The log-rank test was used to assess the best discriminative cut-off value of SUVmax for survival. Survival curves were generated using Kaplan–Meier method and were measured from the date of resection. The software package SPSS version 11.0 (SPSS Inc., Chicago, IL, USA) was used to perform the statistical analysis. Results were considered statistically significant when a p value was <0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 5. Limitations of the...
 6. Conclusion
 References
 
Our cohort consisted of 105 men and 71 women. Age ranged from 41–83 years with a mean (±1SD) of 65.1 years (±8.8). The mean SUVmax of primary NSCLC (±1SD) in our series was 11.8 (±5.9). Tumour size ranged from 1 cm to 12 cm with a mean (±1SD) of 3.9 cm (±1.9). A summary of patient characteristics, pathological characteristics and type of surgical resection with relation to SUV max is outlined in Tables 1–3 . Two types of analysis were performed. The first examined the relation of different variables to SUVmax (Tables 1–3). The second analysis stratified patients into two groups based on the result of the log-rank test (Fig. 1 ) which identified SUVmax of 15 as a cut-off value for survival and is summarised in Table 4 . Survival curves using Kaplan–Meier methods (Fig. 2 ) were generated and stratified based on this cut-off value (i.e. SUVmax of 15). Survival curves for nodal specific stage (i.e. non-N2 and N2) are shown in Fig. 3 (parts A and B, respectively).


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  		Table 1 Patient population and tumour characteristics with relation to SUVmax
 

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  		Table 2 Pathological characteristics of primary NSCLC with relation to SUVmax
 

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  		Table 3 Operative procedures and vascular invasion with relation to SUVmax
 

Figure 1
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  		Fig. 1. Log-rank analysis for the best cut-off value of SUVmax for survival.

 

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  		Table 4 Variables stratification based on cut-off SUVmax of 15
 

Figure 2
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  		Fig. 2. Kaplan–Meier survival curve for all patients under the study (n = 176).

 

Figure 3
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  		Fig. 3. (A) Kaplan–Meier survival curve for non-N2 patients (n = 139). (B) Kaplan–Meier survival curve for N2 patients (n = 37).

 
3.1 SUVmax and tumour characteristics
Centrally located tumours had a higher mean SUVmax than peripheral ones (16.4 vs 10.5, p < 0.0001). There was no significant difference in SUVmax and the lobar distribution of tumours or their site (i.e. right vs left) (Table 1). Tumour size showed a correlation with SUVmax. Larger tumours (≥4 cm) had a higher mean SUVmax than smaller (<4 cm) tumours (14.4 vs 9.7, p < 0.0001). Adenocarcinoma subtype had a lower mean SUVmax than squamous cell subtype (8.6 vs 14.8) and other subtypes (8.6 vs 11.8, p < 0.0001). Poorly differentiated tumours had higher mean SUVmax than moderately and well-differentiated ones (12.8 vs 11.5 vs 8.8, p = 0.045).

3.2 SUVmax and tumour stage
T1 lesions had lower mean SUVmax than T2 (8.2 vs 12.9) and a lower mean SUVmax than T3/T4 lesions (8.2 vs 14.2, p < 0.0001). Primary NSCLC with negative nodal disease had a lower mean SUVmax than tumours with positive lymph node involvement (10.9 vs 13.1, p = 0.006). In addition, there was a trend of a steady increase in mean SUVmax of primary NSCLC in N0 versus N1 (10.9 vs 14.2) and in N2 versus N0 (12.09 vs 10.9, p = 0.004). When applying the AJCC classification, stage I NSCLC had lower mean SUVmax than stage II (10.7 vs 13.2) and III/IV (10.7 vs 12.9, p = 0.014).

3.3 SUVmax and operative procedures
Tumours requiring complex surgical resections (including sleeve resection and pneumonectomy) had higher mean SUVmax than those requiring simple lobectomy (15.2 vs 10.3, p < 0.0001). Open/close thoracotomy (by virtue of invasion into unresectable structures) occurred in four patients overall in our series, and their mean SUVmax was significantly higher than patients requiring simple lobectomy (15.0 vs10.3, p < 0.0001). Chest wall resection was employed in seven cases overall and the distribution of SUVmax in relation to chest wall invasion showed no significant difference.

3.4 SUVmax and prognostic indicators
We found no significant difference in mean SUVmax in tumours with vascular invasion than those without it (Table 3). Parietal pleural invasion had higher mean SUVmax than tumours with uninvolved pleura (14.2 vs 11.6, p = 0.018). Log-rank test was used to assess the best discriminative SUVmax value in relation to survival (Fig. 1).

Based on this analysis, a cut-off value of 15 was used. Survival curves of overall survival following resection showed that patients with SUVmax ≤15 had significantly longer survival than those with SUVmax >15 (Fig. 2). Furthermore, survival curves based on nodal stages (non N2 and N2) also showed a similar pattern when the cut-off value is used (Fig. 3 A and B, respectively).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
5. Limitations of the...
 6. Conclusion
 References
 
Recent evidence showing improved survival in NSCLC patients treated with neoadjuvant chemotherapy has emerged [7]. This might be the way of replacing the conventional practice of adjuvant chemotherapy following resection. However, no data are currently available on preoperative prognostic indicators that might dictate when patients should receive adjuvant or neoadjuvant chemotherapy. The rationale for identifying NSCLC patients with poor prognostic indicators is that these patients could be treated more aggressively in the first instance with neo-adjuvant chemotherapy while those with favourable prognostic indicators could be treated postoperatively with adjuvant type chemotherapy based on their surgical pathological stage. PET-CT has proved useful in the preoperative staging of NSCLC. The prognostic significance of SUV has been widely studied with most data supporting its role (Table 5 ). The cut-off values in SUV measurements however vary widely reflecting a variety of tumour types, surgical resection, follow-up times and the influence of neo-adjuvant chemotherapy [8–18].


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  		Table 5 Previous studies correlating SUV to outcome
 
SUVmax is a semi-quantitative method of measuring 18FDG uptake by tumour cells. Tumour subtype reflects the differential avidity of 18FDG uptake by the cancer cells. Adenocarcinomas have lower expression of Glut-1 transporters which in turn have lower 18FDG uptake and lower SUVmax measurements than squamous cell type [19]. The advancing T stages and the recorded increase in SUVmax can be explained in part by tumour size and volume. AJCC classification also correlated with SUVmax whereby the most curable stage (stage I) had lowest mean SUVmax than the other stages. This is a combination of factors such as size, local invasion and nodal involvement. NSCLC with pleural invasion showed a higher mean SUVmax than those without it. Pattern of surgical resection correlated with mean SUVmax as patients requiring more aggressive and technically demanding resection had lower mean SUVmax than patients requiring a simple lobectomy. This in part is dependant on tumour size and central location as opposed to peripherally located tumours. Survival following resection is dependant on inherent biological aggressiveness of the tumours and the stage which in turn depends on lymph node involvement and local invasion.

Our overall survival was better for patients with SUVmax ≤15 than those with SUVmax >15 (Fig. 2). The same finding was also observed when patients were stratified into various lymph nodal stages (non-N2 and N2, Figs. 3A and 3B). All these prognostic factors do correlate with the degree of 18FDG uptake by cancer cells.

Our data remains consistent with previously published work, a summary of which is depicted in Table 5. One interesting point shown in this table is the difference in the cut-off values used for survival. This has varied across all the studies and various reasons can potentially explain it. First, the different prevalence of NSCLC subtype and whether or not carcinoids have been studied as well. Second, the pattern of surgical resection might have been the same, but the means whereby lymph nodes were surgically staged differed (i.e. sampling vs SLND, preoperative mediastinoscopy selectively vs routinely). Third, different studies used different follow-up time frames and some have included neo-adjuvant chemotherapy which in itself could have altered both the staging and the prognosis. In our work we relied only on patients with documented NSCLC diagnosis who underwent a curative intent surgical resection and we intentionally excluded all neoadjuvant chemotherapy patients, patients with diabetes and those with carcinoids (which can interfere with SUVmax measurements). In addition, we relied on SLND as a gold standard technique for pathological assessment of lymph nodes following resection thus giving us a higher standard of pathological staging than sampling would normally give.

Various conventional prognostic indicators have been previously described [20,21]. A major limitation of these was their postoperative nature. The difficulty arises when attempting to use them preoperatively and since SUVmax of primary NSCLC does correlate with survival and is of prognostic significance, one might argue the case of using SUVmax preoperatively in allocating patients to different treatment strategies such as neoadjuvant versus adjuvant versus no chemotherapy at all.

However, the best cut-off value that could be used universally remains unknown. Such a strategy certainly warrants a multicentre collaboration in a prospective randomised controlled trial.


   5. Limitations of the study
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Limitations of the...
6. Conclusion
 References
 
Our study remains a retrospective work and as such we can only report an association. We also elected to exclude diabetics and patients who received neoadjuvant chemotherapy which in itself might have caused a selection bias. However, due to the relatively large number of patients studied, such bias may not become significant.


   6. Conclusion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Limitations of the...
 6. Conclusion
References
 
Integrated PET-CT is a valuable investigation tool in preoperative staging of NSCLC. In addition to its superiority to CT in the preoperative staging, it provides additional information regarding tumour characteristics, aggressive tumour behaviour and serves as a prognostic indicator. Such information may help in selecting patients preoperatively into receiving neoadjuvant chemotherapy or not. Prospective and randomised trials are warranted.


   Acknowledgments
 
We are grateful for the assistance of Ms Rita Luddy and Ms Mary Devlin in the data acquisition.


   Footnotes
 
{star} Presented in a poster form at the18th WSCTS World Congress, Kos Island, Greece, April 30–May 3, 2008.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Limitations of the...
 6. Conclusion
 References
 

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