18F-fluorothymidine (FLT)-PET and diffusion-weighted MRI for early response evaluation in patients with small cell lung cancer: a pilot study

Tine Nøhr Christensen, Seppo W Langer, Katrine Engholm Villumsen, Helle Hjorth Johannesen, Johan Löfgren, Sune Høgild Keller, Adam Espe Hansen, Andreas Kjaer, Barbara Malene Fischer, Tine Nøhr Christensen, Seppo W Langer, Katrine Engholm Villumsen, Helle Hjorth Johannesen, Johan Löfgren, Sune Høgild Keller, Adam Espe Hansen, Andreas Kjaer, Barbara Malene Fischer

Abstract

Background: Small cell lung cancer (SCLC) is an aggressive cancer often presenting in an advanced stage and prognosis is poor. Early response evaluation may have impact on the treatment strategy.

Aim: We evaluated 18F-fluorothymidine-(FLT)-PET/diffusion-weighted-(DW)-MRI early after treatment start to describe biological changes during therapy, the potential of early response evaluation, and the added value of FLT-PET/DW-MRI.

Methods: Patients with SCLC referred for standard chemotherapy were eligible. FLT-PET/DW-MRI of the chest and brain was acquired within 14 days after treatment start. FLT-PET/DW-MRI was compared with pretreatment FDG-PET/CT. Standardized uptake value (SUV), apparent diffusion coefficient (ADC), and functional tumor volumes were measured. FDG-SUVpeak, FLT-SUVpeak, and ADCmedian; spatial distribution of aggressive areas; and voxel-by-voxel analyses were evaluated to compare the biological information derived from the three functional imaging modalities. FDG-SUVpeak, FLT-SUVpeak, and ADCmedian were also analyzed for ability to predict final treatment response.

Results: Twelve patients with SCLC completed FLT-PET/MRI 1-9 days after treatment start. In nine patients, pretreatment FDG-PET/CT was available for comparison. A total of 16 T-sites and 12 N-sites were identified. No brain metastases were detected. FDG-SUVpeak was 2.0-22.7 in T-sites and 5.5-17.3 in N-sites. FLT-SUVpeak was 0.6-11.5 in T-sites and 1.2-2.4 in N-sites. ADCmedian was 0.76-1.74 × 10- 3 mm2/s in T-sites and 0.88-2.09 × 10-3 mm2/s in N-sites. FLT-SUVpeak correlated with FDG-SUVpeak, and voxel-by-voxel correlation was positive, though the hottest regions were dissimilarly distributed in FLT-PET compared to FDG-PET. FLT-SUVpeak was not correlated with ADCmedian, and voxel-by-voxel analyses and spatial distribution of aggressive areas varied with no systematic relation. LT-SUVpeak was significantly lower in responding lesions than non-responding lesions (mean FLT-SUVpeak in T-sites: 1.5 vs. 5.7; p = 0.007, mean FLT-SUVpeak in N-sites: 1.6 vs. 2.2; p = 0.013).

Conclusions: FLT-PET and DW-MRI performed early after treatment start may add biological information in patients with SCLC. Proliferation early after treatment start measured by FLT-PET is a promising predictor for final treatment response that warrants further investigation.

Trial registration: Clinicaltrials.gov, NCT02995902. Registered 11 December 2014 - Retrospectively registered.

Keywords: 18F-fluorothymidine; DW-MRI; Diffusion-weighted MRI; Early treatment evaluation; FLT-PET; PET/MRI; Prediction of response; Response evaluation; SCLC; Small cell lung cancer.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Overview of the inclusion process
Fig. 2
Fig. 2
Correlations of FDG-SUVpeak, FLT-SUVpeak, and ADCmedian in T-sites (a–c) and N-sites (d, e). FDG-SUVpeak vs. FLT-SUVpeak were positive correlated in T-sites (a) and N-sites (d). FDG-SUVpeak vs. ADCmedian was not significantly correlated in T-sites (b), but significantly negative correlated in N-sites (e). ADCmedian vs. FLT-SUVpeak were neither correlated in T-sites (c) nor N-sites (f). Significant correlations (p < 0.05) are marked with *
Fig. 3
Fig. 3
T-site (4-T) with high and heterogeneous FLT-uptake: FDG-PET (axial (a), coronal (b), sagittal (c)), FLT-PET (axial (d), coronal (e), sagittal (f)), and DW-MRI (transversal (g), coronal (h), sagittal (i)), and voxel-by-voxel scatterplot of FDG-SUV vs. FLT-SUV (j) and FLT-SUV vs. ADC (k). This lesion was clearly detectable on FDG-PET (SUVpeak 22.7), detectable but very heterogeneous on FLT-PET (SUVpeak 11.5), and detectable on DW-MRI (ADCmedian 1.43 × 10−3 mm2/s). The most metabolically active region (MTV70) was located caudally, whereas the most proliferative active region (PTV70) was located cranially within the tumor, thus MTV70 and PTV70 showed no overlap. The most water-diffusion restricted regions (DWTV50) were randomly distributed and overlapped partially with both MTV70 and PTV70. The voxel-by-voxel scatter plots (j, k) showed very weak overall correlations. This T-site had no change as response to chemotherapy
Fig. 4
Fig. 4
T-site (1-T) with low FLT-uptake: FDG-PET (axial (a), coronal (b), sagittal (c)), FLT-PET (axial (d), coronal (e), sagittal (f)), and DW-MRI (transversal (g), coronal (h), sagittal (i)), and voxel-by-voxel scatterplot of FDG-SUV vs. FLT-SUV (j). This T-site was clearly detectable on FDG-PET (SUVpeak 16.6); almost indistinguishable from background on FLT-PET (SUVpeak 1.6); and detectable on DW-MRI (ADCmedian 1.22 × 10−3 mm2/s). The low tumor-to-background ratio causes PTV70 to be less convincing, visually. MTV70 and DWTV50 had a partial overlap. The voxel-by-voxel scatter plot of FLT-SUV and FDG-SUV (j) showed an overall moderate positive correlation (r = 0.50), but the very low FLT-SUVs should be noticed, and the correlation may be a result of perfusion to the region rather than a correlation between metabolism and (a very low) proliferation. Voxel-by-voxel analysis was not feasible for FLT-SUV vs. ADC. This T-site had complete response to chemotherapy, and did not relapse during follow up
Fig. 5
Fig. 5
N-site (12-N1): FDG-PET (axial (a), coronal (b), sagittal (c)), FLT-PET (axial (d), coronal (e), sagittal (f)), and DW-MRI (transversal (g), coronal (h), sagittal (i)), and voxel-by-voxel scatterplot of FDG-SUV vs. FLT-SUV (j), and FLT-SUV vs. ADC (k). This N-site were clearly detectable on FDG-PET (SUVpeak 11.6), FLT-uptake was the highest of all N-sites (SUVpeak 2.4), and detectable on DW-MRI (ADCmedian 1.56 × 10−3 mm2/s). The most aggressive regions (MTV70, PTV70, and DWTV50) were located centrally within the tumor on all imaging modalities, and voxel-by-voxel correlations were moderate for FDG-SUV vs. FLT-SUV (r = 0.55) (j) and for FLT-SUV vs. ADC (r = − 0.44) (k). This N-site progressed during chemotherapy
Fig. 6
Fig. 6
FDG-SUVpeak, FLT-SUVpeak, and ADCmedian in lesions with response vs. lesions with no change or progression. T-sites are shown in left panel (a–c) and N-sites in right panel (d–f). Note that no T-sites progressed during chemotherapy, and no N-sites had no change. FLT-SUVpeak was significantly different in T-sites with response vs. no change (b) and in N-sites with response vs. progression (e). Three lesions with response had no signal on DW-MRI and are not included (c). Lesions that were not evaluated for response are included for completeness. NA*: response evaluation was not available due to atelectasis. NA**: The patient died prior to any response evaluation

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