ABSTRACT
Background
An accurate assessment of tumor viability after first-line treatment is critical for predicting treatment failure in peripheral T-cell lymphomas (PTCLs). 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography/computed tomography (PET/CT) has been adopted as the preferred assessment method in clinical trials, but its impact in clinical practice should be examined. This study aims to determine the prognostic significance of18F-FDG-PET/CT for survival following first-line treatment in PTCL patients.
Research design and methods
Retrospective observational study including 175 patients diagnosed with PTCL between 2008 and 2013 in 13 Spanish sites.
Results
Fifty patients were evaluated with18F-FDG-PET/CT following first-line therapy: 58% were18F-FDG-PET/CT-negative and 42% were18F-FDG-PET/CT-positive. Disease progression occurred in 37.9% of18F-FDG-PET/CT-negative patients and in 80.9% of18F-FDG-PET/CT-positive patients (p = 0.0037). Median progression-free survival and overall survival were 67 and 74 months for18F-FDG-PET/CT-negative patients, and 5 (p < 0.0001) and 10 months (p < 0.0001), respectively, in18F-FDG-PET/CT-positive patients. After multivariate analysis, only B symptoms emerged as a negative predictive factor of complete response (RR 7.08; 95% CI 1.60–31.31; p = 0.001).
Conclusions
18F-FDG-PET/CT identifies high-risk PTCL patients who will have poor prognosis and survival following first-line treatment. However, more research is needed to confirm the best treatment options for PTCL patients.
1. Introduction
Peripheral T-cell lymphomas (PTCLs) are a heterogeneous and rare group of malignancies that account for 10%–15% of all non-Hodgkin lymphomas and 5% of all lymphoid malignancies. They are characterized by aggressive clinical behavior, poor response to chemotherapy, and poor long-term survival compared to the more common B-cell lymphomas [Citation1–4].
The outcome of patients following conventional first-line chemotherapy with cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) or CHOP-like regimens remains poor for the majority of histological subtypes. The overall response rate for PTCL is nearly 70% with 5-year progression-free survival (PFS) and overall survival (OS) rates of 20% and 30%, respectively [Citation5,Citation6]. Anaplastic lymphoma kinase (ALK)-positive anaplastic large-cell lymphoma (ALCL) demonstrated the best 5-year OS (70%), while ALK-negative ALCL had an intermediate 5-year OS of 49%. Five-year failure-free survival was 60% for ALK-positive ALCL and 36% for ALK-negative ALCL [Citation4]. In addition, 30% of PTCL patients are unsuitable for autologous stem cell transplantation (ASCT) or any other consolidation therapy [Citation5]. Therefore, an early imaging-based diagnosis to identify patients who are likely to fail first-line treatment is imperative to design prompt, appropriate, and alternative therapies.
Although there are currently no universal standardized models for predicting the prognosis of PTCL patients, some methods have been shown to be predictive or prognostic for survival outcomes. One example is the Total Metabolic Tumor Volume (TMTV), which can estimate the total tumor burden as predictive of outcome in PTCL [Citation7]. Other models, such as the International Prognosis Index (IPI) and the Prognostic Index for T-cell lymphoma (PIT) have been used in clinical practice to predict the prognosis of PTCL patients [Citation8–10], but these scores cannot predict response to individual therapies.
18F-fluorodeoxyglucose (18F-FDG) positron emission tomography/computed tomography (PET/CT) is a valuable tool for staging and response assessment of both Hodgkin and non-Hodgkin lymphomas [Citation11–13]. Despite the observed high sensitivity of18F-FDG-PET/CT in Hodgkin lymphoma [Citation14–17], results in the different subtypes of non-Hodgkin lymphoma remain somewhat inconsistent [Citation18–22]. Hence, further elucidation of the utility of18F-FDG-PET/CT in PTCL is warranted. Most published studies included either small numbers of PTCL patients and/or other non-PTCL lymphoma types [Citation23–29], so results surrounding the prognostic value of interim or final18F-FDG-PET/CT assessment in PTCL are controversial [Citation30–34]. A few studies have reported that a positive interim18F-FDG-PET/CT was not predictive of poor PFS and OS [Citation30]. However, a Deauville score of three or higher following completion of induction treatment was predictive of poor outcome, suggesting that an intensified chemotherapy regimen could be beneficial in such patients [Citation31]. Therefore, a more accurate assessment of residual tumor viability after first-line therapy for predicting treatment failure in PTCL is critical.
18F-FDG-PET/CT analysis is the preferred assessment method in clinical trials and is routinely used to guide therapy in various lymphoma subtypes. The objective of this study was to assess the prognostic value of18F-FDG-PET/CT for PFS and OS in clinical practice following first-line treatment in PTCL patients.
2. Methods
2.1. Study design and patients
The Real-T study was an observational, retrospective, multicentre study of the clinicopathological features and prognostic factors of patients with PTCL (NCT02788916) [Citation35]. Data presented here are a subanalysis of the Real-T study aimed at determining the role of18F-FDG-PET/CT in PTCL prognosis in clinical practice. Medical records from 13 Spanish centers were retrospectively reviewed to identify patients diagnosed with PTCL between 1 January 2008 and 31 December 2013 using the 2008 WHO classification of lymphoid neoplasms [Citation1]. All patients provided written informed consent prior to inclusion. The study protocol was approved by the ethical committees at all participating sites and it was conducted in accordance with the International Conference on Harmonization Guidelines on Good Clinical Practice and the Declaration of Helsinki.
The main inclusion criteria for the REAL-T study were availability of biopsy specimens from the initial diagnosis (node or 16–18 mm core biopsy in paraffin) and PTCL histologically confirmed by centralized review, involving ALK-positive ALCL, ALK-negative ALCL, angioimmunoblastic T-cell lymphoma (AITL), PTCL-not-otherwise-specified (NOS), or extranodal natural killer/T-cell (NK/T) PTCL subtypes. In addition, 18F-FDG-PET/CT after first-line therapy was required for this subanalysis. Patients whose medical history was unavailable (lost, empty, or unrecoverable) were excluded from the study.
Clinical data collected included age, sex, Ann Arbor disease stage, extranodal lesions, B symptoms, bulky disease, ECOG PS, β2-microglobulin, and LDH. Date of disease progression and/or death were also recorded to calculate PFS and OS. In all cases, 18F-FDG-PET/CT assessment was done at the time of diagnosis, before the initiation of first-line treatment, and also after the completion of treatment (4–6 weeks after last chemotherapy). Semi-quantitative and non-quantitative assessments were performed with maximum standardized uptake value (SUVmax) because data were not available for all patients. No centralized PET reviews were performed, and results were collected and analyzed based on the local PET reports [Citation36].
Patients were followed up by CT following the Lugano 2014 criteria [Citation37]. PET/CT was not used for the follow-up of these patients.
2.2. Statistical analysis
Categorical variables were reported as percentages and analyzed using binomial regression. Continuous variables were reported as mean ± standard deviation (SD) or median (range). Time-to-event analyses (PFS and OS) were performed using the Kaplan–Meier method and the log-rank test. Estimated mean with 95% confidence intervals (95% CIs) was used when the median value was not reached. The Cox proportional hazards model was used for the univariate and multivariate analyses of hazard ratios (HR) with 95% CIs for OS and PFS. Factors with p-value of ≤ 0.1 in the univariate analysis were included in the multivariate analysis (excluding potentially confounding factors that were already included in further variables). Differences were considered statistically significant at p-values of < 0.05 in all cases. All analyses were performed using IBM SPSS software (version 22.0; IBM Corp., Armonk, NY).
3. Results
Of the 175 patients included in the REAL-T study [Citation35], 50 patients (28.9%) had a18F-FDG-PET/CT assessment after first-line therapy. Most patients received therapy with the CHOP regimen (n = 33, 66%), 4 patients received cyclophosphamide, doxorubicin, vincristine, etoposide, and prednisone (CHOEP) (8%), and 13 patients received other CHOP-like regimens (26%). shows the baseline characteristics of these patients at diagnosis according to the18F-FDG-PET/CT result after treatment.
Table 1. Baseline patient characteristics at diagnosis (n = 50) according to18F-FDG-PET/CT result after first-line therapy.
Following first-line therapy, the18F-FDG-PET/CT was negative in 58% of patients (n = 29/50) and positive in 42% (n = 21/50). The best clinical response to first-line therapy achieved in the18F-FDG-PET/CT-negative group was complete response in 26 patients (89.7%) and partial response in three patients (10.3%). These three patients had partial radiological response on CT scan but complete metabolic response, as no abnormal uptake was observed on18F-FDG-PET/CT. In the18F-FDG-PET/CT-positive group, 14 patients (66.7%) achieved partial response and 7 (33.3%) disease progression. After18F-FDG-PET/CT assessment, 37.9% of the18F-FDG-PET/CT-negative patients (n = 11/29) had disease progression, compared to 80.9% of the18F-FDG-PET/CT-positive patients (n = 17/21) (p = 0.0037) ().
Table 2. Rate of disease progression and survival outcomes according to18F-FDG-PET/CT results.
At the end of treatment, 28% of the patients (n = 14/50) were consolidated with ASCT: 34.5% of the18F-FDG-PET/CT-negative patients (n = 10/29) and 19.0% of the18F-FDG-PET/CT-positive patients (n = 4/21). All patients who underwent ASCT achieved complete response. The indication for ASCT was based not only on18F-FDG-PET/CT results, but also on performance status, chemosensitivity or willingness.
After disease progression, patients in the18F-FDG-PET/CT-positive group received a variety of salvage therapies, including brentuximab vedotin (n = 2); cyclophosphamide, mitoxantrone, vincristine, etoposide, bleomycin, and prednisone (VNCOP) (n = 1); gemcitabine plus oxaliplatin (GEMOX) (n = 2); etoposide, methylprednisolone, high-dose cytarabine, and cisplatin (ESHAP) (n = 2); cyclophosphamide plus prednisone (n = 1); bendamustine (n = 1); mesna, ifosfamide, mitoxantrone, and etoposide (MINE) (n = 2); and etoposide, dexamethasone, high-dose cytarabine, and cisplatin (EDHAP) (n = 1). 18F-FDG-PET/CT-negative patients with disease progression received ESHAP (n = 11); MINE (n = 1); etoposide (n = 1); fludarabine, mitoxantrone, and dexamethasone (FMD) (n = 1); metronomic therapy (n = 1); and cyclophosphamide plus prednisone (n = 1).
With a median follow-up of 12.4 months, median PFS in the18F-FDG-PET/CT-negative group was 67 months versus 5 months in the18F-FDG-PET/CT-positive group (p < 0.0001). Median OS in the18F-FDG-PET/CT-negative group was 74 months versus 10 months in the18F-FDG-PET/CT-positive group (p < 0.0001) () ().
Figure 1. Kaplan–Meier survival analysis of progression-free survival (PFS) and overall survival (OS) according to18F-FDG-PET/CT results after first-line treatment.
In the univariate analysis, factors that at the time of diagnosis were found to predict a negative18F-FDG-PET/CT after first-line treatment were as follows: absence of B symptoms (p = 0.0355), normal β2-microglobulin levels (p = 0.025), and normal serum lactate dehydrogenase (LDH) levels (p = 0.0424) (). Neither sex, histologic subtype, Ann Arbor stage, presence of extranodal disease, nor Eastern Cooperative Oncology Group performance status (ECOG PS) showed differences between18F-FDG-PET/CT-positive or negative patients (). In the multivariate analysis, only B symptoms remained as predictive factor of positive18F-FDG-PET/CT with a relative risk (RR) 7.08 (95% CI 1.60, 31.31; p = 0.001).
4. Discussion
In this study, we found that18F-FDG-PET/CT has a prognostic value and can predict PFS and OS after first-line PTCL treatment in clinical practice. This subanalysis demonstrated that patients with negative18F-FDG-PET/CT after first-line treatment have a better prognosis, with significantly longer PFS and OS compared to patients with positive18F-FDG-PET/CT. Moreover, only the absence of B symptoms at PTCL diagnosis was identified as predictive factor for a negative18F-FDG-PET/CT following treatment.
Although18F-FDG-PET/CT is the preferred method to assess response in clinical trials, it has not been used routinely in Spain for PTCL until recently. In fact, of the 175 patients initially included in the REAL-T study [Citation35], 18F-FDG-PET/CT was performed following first-line therapy in only 29%. These observations could be partially explained by the lack of availability of18F-FDG-PET/CT in most of the hospitals during the study period (2008–2013) and the lack of scientific evidence.
Recent studies have reported conflicting results regarding the prognostic significance of18F-FDG-PET/CT findings in PTCL. Gurion et al. in a retrospective analysis evaluated the diagnostic utility of baseline18F-FDG-PET/CT and the prognostic significance of interim and end-of-treatment18F-FDG-PET/CT in 40 newly diagnosed or relapsed PTCL patients using various chemotherapy regimens [Citation27]. Although18F-FDG-PET/CT was positive in 90% of the PTCL patients in this study, these findings were not considered predictive for PFS or OS at any point. In contrast, lymphopenia was the only prognostic factor for predicting survival on the multivariate analysis [Citation27].
Ahn et al. investigated whether interim and post-treatment response assessment by18F-FDG-PET/CT using the Deauville scale had any prognostic value [Citation38]. They found that clinical outcomes of interim and post-treatment18F-FDG-PET/CT did not differ between ASCT and non-ASCT PTCL patients. Moreover, they observed that the clinical and pathological features of PTCL patients who underwent ASCT were similar to those of patients who did not. After a median follow-up period of 60.8 months, only end-of-treatment18F-FDG-PET/CT was found to be an independent prognostic factor of survival outcomes [Citation38]. In our study, 34.5% of the patients with negative18F-FDG-PET/CT findings after first-line treatment underwent ASCT in contrast to 19% of the patients with positive18F-FDG-PET/CT. However, the huge survival advantage observed in18F-FDG-PET/CT-negative patients suggests that the clinical outcome of PTCLs could be mainly reflected by18F-FDG-PET/CT response after first-line chemotherapy, regardless of upfront ASCT.
Abe et al., on the other hand, report positive results for the predictive value of18F-FDG-PET/CT response. Patients whose bone marrow involvement was detected by18F-FDG-PET/CT had a poorer prognosis than patients with negative bone marrow histology, suggesting that18F-FDG-PET/CT may have the potential to improve existing prognostic tools in PTCL [Citation39].
In a large European study, the combination of18F-FDG-PET/CT (both interim and end-of-treatment) findings with baseline TMTV could predict early relapse or refractory disease [Citation40]. This was a retrospective study that included 140 patients with nodal PTCL, who underwent baseline, interim, and post-treatment18F-FDG-PET/CT procedures. These authors concluded that positive interim18F-FDG-PET/CT findings predicted a poor outcome in PTCL patients and that the combination of this with TMTV evaluation could further stratify these high-risk patients. Furthermore, subanalysis showed that18F-FDG-PET/CT findings had an excellent predictive value for PFS and OS in both AITL and PTCL-NOS patients.
The results of the above study are in consonance with the findings of our study. We also found in this retrospective and multicentre study that a post-treatment18F-FDG-PET/CT could accurately predict outcome after first-line PTCL therapy. Our analysis also suggests that the presence of B symptoms at diagnosis could be a good predictor for poor18F-FDG-PET/CT response. Patients with low TMTV, SUVmax, and total lesion glycolysis have also shown significantly better clinical outcomes than those with higher levels [Citation29]. These parameters were associated with PFS and OS. Moreover, SUVmax values and the National Comprehensive Cancer Network International Prognostic Index (NCCN-IPI) scores were independent factors of OS only. The combination of TMTV and NCCN-IPI scores also improved patients’ initial-stage risk stratification, which may contribute to the adjustment of the ongoing treatment or to switch to an appropriate therapeutic regimen [Citation29].
The limitations of our study are similar to those of a retrospective design. Clinical variables were not available for all patients, the cohort of PTCL patients with evaluable18F-FDG-PET/CT assessment after first-line therapy was relatively small, and the range of heterogeneous PTCL subtypes makes it difficult to draw solid conclusions. Moreover, PET/CT review was not centralized, which can introduce bias. Another limitation was that the Deauville score was not available and only the nuclear medicine physician’s final interpretation of positive/negative18F-FDG-PET/CT assessment was recorded. However, in our favor, we should bear in mind that data was collected from multiple centers in Spain and the experience is not limited to a single institute.
5. Conclusions
Our subanalysis of the REAL-T study concluded that positive post-treatment18F-FDG-PET/CT findings can identify high-risk PTCL patients. Our study also suggests that B symptoms at disease diagnosis could identify patients who will have a dismal response to first-line treatment. The use of new predictive factors may help select patients with a poorer prognosis who may benefit from intensified chemotherapy or treatment combinations with new target drugs. However, further studies are needed to confirm the impact of18F-FDG-PET/CT status at the end of first-line treatment and determine the best treatment strategy for PTCL patients.
Declaration of interest
R Cordoba: Speakers bureau, consulting/advisory role for Takeda, and travel and accommodation by Takeda. J Sánchez-García: Research funding by Janssen and Roche. Speakers bureau for Abbvie, Janssen, BSM, Roche, and Takeda. E Domingo-Domenech: Consulting/advisory role for Takeda. Research funding by Bristol-Myers Squibb, Seattle Genetics, Inc., and Takeda. Travel, accommodation and expenses by Bristol-Myers Squibb, Takeda, Roche, and Janssen. J López Jiménez: Research funding by Abbvie, Janssen, MSD, Roche and Takeda. Speakers bureau for Abbvie, Janssen, MSD, Roche, and Takeda. C Carpio: Speakers bureau for Regeneron, Takeda, Celgene, Novartis, and Roche. A Bendaña: Speakers bureau for Roche. S González de Villambrosia: Speakers bureau for Janssen and Roche. G Rodríguez: Consulting/advisory for Roche, Janssen, Celgene, and Takeda. A Naves: Employee of Takeda Farmacéutica España S.A. L Baeza: Employee of Takeda Farmacéutica España. S.A. AM Martín García-Sancho: Research funding by Janssen, Celgene. Consulting/advisory for Roche, Servier, Celgene/BMS, Clinigen, Eusa Pharma, Gilead, Kyowa Kirin, Novartis, and Morphosys. Speakers bureau for Roche, Celgene, Janssen, Servier, Gilead, and Takeda.
Reviewer disclosures
Peer reviewers on this manuscript have no relevant financial or other relationships to disclose.
Author contributions
R Cordoba: designed the research, performed the tests and statistics, and reviewed the manuscript. J Sánchez-García, E Domingo-Domenech, J López Jiménez, A Martínez Pozo, C Carpio, A Bendaña, AJ González, S González de Villambrosia, J Gómez Codina, B Navarro, G Rodríguez, and A Martín García-Sancho reviewed the medical records to identify patients diagnosed with PTCL, recorded the data used in the study, and reviewed the manuscript. A Naves and L Baeza revised the article. All of the authors approved the final version of the manuscript for submission.
Acknowledgments
The authors wish to thank McCann Health and Fernando Sánchez Barbero, PhD, for the support on the preparation of this manuscript.
Data availability statement
All data generated or analyzed during this study are included in this published article.
Additional information
Funding
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