Abstract
An extensive analysis of the reliability of positron emission tomography (PET) after induction treatment in patients with Hodgkin's disease (HD) or aggressive non-Hodgkin's lymphoma (NHL). In all, 75 untreated patients with HD (n=41) or aggressive NHL (n=34) were studied with both PET and CT scans following standard chemotherapy induction therapy (ABVD or MACOP-B) with/without radiotherapy. Histopathological analysis was performed when considered necessary. After treatment, four out of five (80%) patients who were PET+/CT− relapsed, as compared with zero out of 29 patients in the PET−/CT− subset. Among the 41 CT+ patients, 10 out of 11 (91%) who were PET+ relapsed, as compared with 0 out of 30 who were PET−. The actuarial relapse-free survival (RFS) rates were 9 and 100% in the PET+ and PET− subsets, respectively (P=0.00001). All five patients who were PET+/CT− underwent a lymph node biopsy: in four (80%) cases, persistent lymphoma and was confirmed at histopathological examination. Two HD patients who were PET−/CT+ (with large residual masses in the mediastinum or lung) were submitted to biopsy, which in both cases revealed only fibrosis. In HD and aggressive NHL patients, PET positivity after induction treatment is highly predictive for the presence of residual disease, with significant differences being observable in terms of RFS. PET negativity at restaging strongly suggests the absence of active disease; histopathological verification is important in patients who show PET positivity.
Main
Both Hodgkin's disease (HD) and aggressive non-Hodgkin's lymphoma (NHL) are curable malignancies. With standard induction therapies (Armitage et al, 1986; DeVita et al, 1997; Gianni et al, 1997) more than 70% of patients with HD and almost half those with aggressive NHL can be cured. Many prognostic indicators of response to treatment exist based on clinical characteristics at presentation. The International Prognostic Index (IPI) (The International non-Hodgkin's Lymphoma Prognostic Factors Project, 1993), which summarises different clinical prognostic factors at diagnosis, has become an established parameter for risk stratification in NHL. For HD, a specific prognostic score has been devised for the identification different risk subsets (Hasenclever and Diehl, 1998). After selecting correct, specific frontline treatments on the basis of these prognostic scores at the time of presentation, the next important steps are to: (i) distinguish between responders to standard approaches and non-responders who stand to benefit from an early change to an alternative, experimental form of therapy; (ii) monitor and identify any relapses during follow-up. Chemosensitivity and response to treatment is currently assessed on the basis of clinical, radiological and pathological (bone marrow) criteria.
X-ray computed tomography (CT) remains the gold standard for evaluation of nodal disease. However, definition of response criteria based on conventional radiographic characteristics remains difficult, as lymphoma patients treated with chemotherapy often present with residual masses of uncertain significance. These residual masses may consist of fibrotic tissue or active disease and CT scan and magnetic resonance imaging (MRI) cannot reliably differentiate between active disease and fibrosis (Hill et al, 1993; Zinzani et al, 1996). For these purposes, functional imaging with fluorine-18 fluorodeoxyglucose (FDG) positron emission tomography (PET) can reveal decisive metabolic or functional tissue parameters and is more accurate than conventional radiological imaging techniques for restaging after chemotherapy (Jerusalem et al, 1999, 2001; Zinzani et al, 1999a, 1999b; Kostakoglu and Goldsmith, 2000; Dittmann et al, 2001). Several groups, including our own, have evaluated the efficiency of PET for restaging patients after completed therapy (Cremerius et al, 1998, 2001; De Wit et al, 2001; Naumann et al, 2001; Spaepen et al, 2001a, 2001b; Weihrauch et al, 2001, 2003; Zinzani et al, 2002; Fihnont et al, 2003).
Herein, we report an extensive analysis of restaging after induction treatment of patients with HD or aggressive NHL based on PET in conjunction with CT and – in certain selected cases – histopathological analysis.
Patients and methods
Patient population
All patients with HD or aggressive NHL who were treated at our Institute with our standard induction chemotherapy protocols (with/without radiation therapy) between October 2001 and December 2002 were screened for this retrospective analysis. Eligibility criteria were no prior therapy; histological diagnosis of HD or aggressive NHL according to the R.E.A.L. classification (Harris et al, 1994); an ECOG (Oken et al, 1982) performance status score of <3; normal hepatic, renal, and cardiac function. All patients provided informed consent for the study. Ethical approval was not appropriate for this noninvasive study performed in conjunction with routine chemotherapy protocols.
Induction treatment
Patients with HD were treated with four or six cycles of ABVD regimen (Bonadonna et al, 1977), based on initial staging. Patients with aggressive NHL were submitted to the MACOP-B regimen (Klimo and Connors, 1985). Radiotherapy was performed at the clinician's discretion.
Staging
Radiological clinical staging with evaluation of tumour size included CT and PET. CT was performed at diagnosis (before therapy), 1 month after the end of chemotherapy, and 2 months after any radiotherapy. PET was performed at least 1 month after the end of chemotherapy, and 3 months after any radiotherapy. The remaining staging procedures included bone marrow biopsy, haematological and biochemical survey. A mass measuring ⩾10 cm in its longest diameter was considered as bulky.
CT scans of the chest, abdomen, and pelvis were obtained using a third generation General Electric scanner (GE Medical Systems, Milwaukee, WI, USA). All the regions were scanned at 10 × 10 mm2 intervals; scan time was 2 s. Intravenous contrast material (a bolus of 100–150 ml of nonionic contrast medium) was used in all patients.
To optimise FDG uptake in normal and neoplastic tissue, patients were asked to fast for at least 6 h before undergoing PET examination; no patient had a history of diabetes. Fluorine-18 fluorodeoxyglucose (FDG) was produced in our radiopharmacy using standard synthesis techniques. Each patient was i.v. injected with about 6 MBq kg−1 of FDG; PET scan was carried out 70–90 min after tracer injection. Before PET scanning patients were encouraged to void in order to minimise activity in the bladder. FDG-PET scans were carried out using a dedicated tomograph (Advance NX, General Electric Medical Systems, Milwakee, USA). Emission scans were acquired for 4 min at every table positron; 2-min transmission scans were also recorded in all patients. Overall, about six bed positions were required for each patient, with a total scan time of about 40 min. Images were reconstructed with segmented attenuation correction. PET images were evaluated on the basis of image visual inspection by three experienced readers. Areas of focal uptake were interpreted as positive for lymphoma unless they were at the sites of known accumulation, including the kidney and bladder, gastrointestinal tract, skeletal areas showing symmetric joint uptake (especially within the shoulder) were considered as due to arthritis.
Evaluation of response
Complete response (CR) was defined using reported standardised guidelines (Cheson et al, 2000). For the purposes of this report, results of PET were not considered when assigning response status following therapy. The relapse-free survival (RFS) curve was calculated using the Kaplan–Meier method (Kaplan and Meier, 1958). RFS was defined as the period from the end of therapy to the time of first relapse. The statistical significance of differences observed were assessed using the log-rank test (Mantel and Haenzel, 1959).
Results
In total, 75 patients satisfied the eligibility criteria (Table 1). After completion of the respective chemotherapy programs (ABVD for HD, MACOP-B for NHL), 45 out of 75 (60%) patients received radiation therapy with a tumour dose of 30–36 Gy.
Table 2 reports PET and CT restaging findings after induction with respect to outcome. After the treatment, 59 out of 75 (79%) patients were negative at PET, the remaining 16 being positive. In total, 14 of the 16 (88%) patients who were PET+ went on to have local relapse/progression (at a median of 9 months after completing induction therapy, range 3–12 months). By contrast, none of the 59 patients who were PET− had local relapse/progression (P=0.00001). Figure 1 shows the RFS curves for patients who were PET+ went after the induction treatment (P=0.00001).
As regards CT, as many as 41 out of 75 (55%) patients had a positive scan. Of these, 30 out of 41 (73%) were PET−. All 30 (100%) patients in this PET−/CT+ subset are still in CR at a median follow-up of 12 months (range, 6–15 months). Two of these patients, both with HD, were submitted to histopathological evaluation, due to evidence at CT of either diffuse mediastinal residual disease or right lung infiltration. In both cases, the histopathological findings (based on an intrathoracic biopsy and lobectomy, respectively) were negative for lymphomatous infiltration, and revealed only fibrotic and necrotic tissue (Figure 2 shows the negative PET scan of the patient who had suspected pulmonary infiltration at CT). By contrast, in the PET+/CT+ subset 10 out of 11 (91%) patients experienced local relapse/progression within the first 12 months; in the remaining patient, a driven true-cut biopsy guided by abdominal ultrasonography was performed at 3 months (following a second positive PET scan), revealing a pathohistological diagnosis of aggressive NHL.
Among the patients who were CT−/PET+ after treatment, only one out of five (20%) is currently in CR; the remaining four (80%) patients relapsed (after 3, 5, 9, and 12 months). All these five patients were submitted to a lymph node biopsy: in the four patients who relapsed histopathological confirmation was made of either aggressive NHL (three cases) or HD (one case); in the remaining patient, the histopathological diagnosis was follicular hyperplasia. By contrast, all 29 patients in the PET−/CT− subset are now in CR with a median follow-up of 14 months.
It should be noted that biopsies performed in two patients who were PET− but strongly CT+ revealed only fibrotic/necrotic tissue. Figure 3 shows the positive PET scans of patient who had histopathological confirmation of relapse.
Discussion
This extended follow-up analysis strongly reinforces the positive role of PET for optimal restaging of patients with HD or aggressive NHL after induction chemotherapy with/without radiation therapy.
Many lymphoma patients present with residual masses after completing induction therapy, but less than 20% of them will eventually relapse. Thus, detection of residual active lymphoma after induction is of major clinical importance. Before the introduction of PET for clinical evaluation of lymphoma patients, no available tool could reliably predict the course of the disease. None of the morphological characteristics described for CT scan can differentiate active lymphoma from necrosis and fibrosis. MRI has a low sensitivity and is therefore not useful for lymphoma (Hill et al, 1993; Zinzani et al, 1996). Although 67-Gallium scintigraphy is a metabolic imaging technique to detect active tumour tissue, it has drawbacks such as a low spatial resolution and difficulty in identifying residual abdominal masses (Kostakoglu et al, 1992; Setoain et al, 1997; Zinzani et al, 1999a, 1999b). In recent years, a series of reports have shown that PET is the most helpful noninvasive metabolic imaging technique for patients with either HD or aggressive NHL: it can distinguish between active lymphoma and fibrosis, and it has important prognostic value after completion of front-line therapy (Cremerius et al, 1998, 2001; De Wit et al, 2001; Naumann et al, 2001; Spaepen et al, 2001a, 2001b; Weihrauch et al, 2001, 2003; Zinzani et al, 2002; Fihnont et al, 2003).
Our extensive analysis clearly indicates reliability of PET in the post-treatment evaluation of HD and aggressive NHL with respect to specific histopathological evaluation. There were no false-negative results among the 75 PET scans performed and only one false-positive result. Among the 16 patients who had positive PET scans, 14 (88%) relapsed or progressed within 1 year from the end of the treatment. Remarkably, surgical biopsy revealed persistence of active disease in four out of the five (80%) patients in whom a positivity at PET was accompanied by a negative CT scan. The single false-positive PET finding corresponded to a histolopathological diagnosis of follicular hyperplasia. Biopsies were also performed in two patients who were negative at PET due to the large size of residual masses visualised at CT: in either case, histopathological examination revealed only fibrotic/necrotic tissue. The relevant impact of PET positivity on RFS, independently of lymphoma type (HD or aggressive NHL) and presence/absence of a positive CT scan can be clearly seen from Figure 1.
Taken together, these data suggest the need to reach a histopathological diagnosis whenever possible before commencing salvage therapy, rather than relying exclusively on a positive PET result. On the other hand, the apparently strong negative predictive value of PET suggests that biopsy might be reserved for cases of PET positivity.
An interesting development in the role of PET for HD and aggressive NHL patients will be to verify and to confirm the preliminary data reported by Spaepen et al (2002) concerning the possible role of an early PET scan performed after a few courses of induction chemotherapy for identification and stratification of responder and nonresponder patients. This could lead to inclusion of PET in a specific mixed prognostic score including biological, clinical and imaging parameters. In addition, recent reports indicate that PET can be used to predict the clinical outcome after high-dose chemotherapy and stem cell transplantation (Becherer et al, 2002; Cremerius et al, 2002; Spaepen et al, 2003). In both situations, histopathological diagnosis will remain important for deciding further treatment of patients with positive PET scans.
A further step will be evaluation of the utility of combined PET/CT (Visvikis and Ell, 2003). In the last few months, we have initiated a prospective study to assess the possible predictive role of PET/CT during induction chemotherapy (after one-third and two-thirds of the courses) for patients with HD and aggressive NHL in our institutions.
Change history
16 November 2011
This paper was modified 12 months after initial publication to switch to Creative Commons licence terms, as noted at publication
References
A predictive model for aggressive non-Hodgkin's lymphoma (1993) The International Non-Hodgkin's Lymphoma Prognostic Factors Project. N Engl J Med 32: 987–994
Armitage JO, Weisenburger DD, Hutchins M, Moravec DF, Dowling M, Sorensen S, Mailliard J, Okerbloom J, Johnson PS, Howe D (1986) Chemotherapy for diffuse large-cell lymphoma-rapidly responding patients have more durable remissions. J Clin Oncol 4: 160–164
Becherer A, Mitterbauer M, Jaeger U, Kalhs P, Greinix HT, Karanikas G, Potzi C, Raderer M, Dudczak R, Kletter K (2002) Positron emission tomography with [18F]2-flouro-D-2-deoxyglucose (FDG-PET) predicts relapse of malignant lymphoma after high-dose therapy with stem cell transplantation. Leukemia 16: 260–267
Bonadonna G, Zucali R, De Lena M, Valagussa P (1977) Combined chemotherapy (MOPP or ABVD)–radiotherapy approach in advanced Hodgkin's disease. Cancer Treat Rep 61: 769–777
Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, Lister TA, Vose J, Grillo-Lopez A, Hagenbeek A, Cabanillas F, Klippensten D, Hiddemann W, Castellino R, Harris NL, Armitage JO, Carter W, Hoppe R, Canellos GP (2000) Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. (J Clin Oncol 1999; 17: 1244; Erratum in J Clin Oncol 18: 2351)
Cremerius U, Fabry U, Neuerburg J, Zimny M, Osieka R, Bull U (1998) Positron emission tomography with 18F-FDG to detect residual disease after therapy for malignant lymphoma. Nucl Med Commun 19: 1055–1063
Cremerius U, Fabry U, Neuerburg J, Zimmy M, Bares R, Osieka R, Bull U (2001) Prognostic significance of positron emission tomography using fluorine-18-fluorodeoxyglucose in patients treated for malignant lymphoma. Nuklearmedizin 40: 23–30
Cremerius U, Fabry U, Wildberger JE, Zimny M, Reinartz P Nowak B, Schaefer W, Buell U, Osieka R (2002) Pretransplant positron emission tomography (PET) using fluorine-18-fluoro-deoxyglucose (FDG) predicts outcome in patients treated with high-dose chemotherapy and autologous stem cell transplantation for non Hodgkin's lymphoma. Bone Marrow Transplant 30: 103–111
DeVita Jr VT, Mauch PM, Harris NL (1997) Hodgkin's disease. In Cancer, DeVita Jr VT, Hellman S, Rosenberg SA (eds). 5th edn, Vol 224 Philadelphia: Lippincott
de Wit M, Bohuslavizki KH, Buchert R, Bumann D, Clausen M, Hossfeld DK (2001) 18 FDG-PET following treatment as valid predictor for disease-free survival in Hodgkin's lymphoma. Ann Oncol 12: 29–37
Dittmann H, Sokler M, Kollmannsberger C, Dohmen BM, Baumann C, Kopp A, Bares R, Claussen CD, Kanz L, Bokemeyer C (2001) Comparison of 18FDG-PET with CT scans in the evaluation of patients with residual and recurrent Hodgkin's lymphoma. Oncol Rep 8: 1393–1399
Fihnont JE, Czenin J, Yap C (2003) Value of f-18 fluorodeoxyglucose positron emission tomography for predicting the clinical outcome of patients with aggressive lymphoma prior to and after autologous stem-cell transplantation. Chest 124: 608–613
Gianni AM, Bregni M, Siena S, Brambilla C, Di Nicola M, Lombardi F, Gandola L, Tarella C, Pileri A, Ravagnani F, Valagussa P, Bonadonna G (1997) High-dose chemotherapy and autologous bone marrow transplantation compared with MACOP-B in aggressive B-cell lymphoma. N Engl J Med 336: 1290–1297
Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC (1994) A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84: 1361–1392
Hasenclever D, Diehl V (1998) A prognostic score for advanced Hodgkin's disease. International Prognostic Factors Project on Advanced Hodgkin's disease. N Engl J Med 339: 1506–1514
Hill M, Cunningham D, MacVicar D, Roldan A, Husband J, McCready R, Mansi J, Milan S, Hickish T (1993) Role of magnetic resonance imaging in predicting relapse in residual masses after treatment of lymphoma. J Clin Oncol 11: 2273–2278
Jerusalem G, Beguin Y, Fassotte MF, Najjar F, Paulus P, Rigo P, Fillet G (2001) Whole-body positron emission tomography using 18 F-fluorodeoxyglucose compared to standard procedures for staging patients with Hodgkin's diseas. Haematologica 86: 266–273
Jerusalem G, Beguin Y, Fassotte MF, Najjar F, Paulus P, Rigo P, Fillet G (1999) Whole-body positron emission tomography using 18 F-fluorodeoxyglucose for posttreatment evaluation in Hodgkin's disease and non-Hodgkin's lymphoma has higher diagnostic and prognostic value than classical computed tomography scan imaging. Blood 94: 429–433
Kaplan ES, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53: 457–481
Klimo P, Connors JM (1985) MACOP-B chemotherapy for the treatment of diffuse large-cell lymphoma. Ann Intern Med 102: 596–602
Kostakoglu L, Yeh SD, Portlock C, Heelan R, Yao TJ, Niedzwiecki D, Larson SM (1992) Validation of gallium-67-citrate single-photon emission computed tomography in biopsy-confirmed residual Hodgkin's disease in the mediastinum. J Nucl Med 33: 345–350
Kostakoglu L, Goldsmith SJ (2000) Fluorine-18 fluorodeoxyglucose positron emission tomography in the staging and follow-up of lymphoma: is it time to shift gears? Eur J Nucl Med 27: 1564–1578
Mantel H, Haenzel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22: 719–748
Naumann R, Vaic A, Beuthien-Baumann B, Bredow J, Kropp J, Kittner T, Franke WG, Ehninger G (2001) Prognostic value of positron emission tomography in the evaluation of post-treatment residual mass in patients with Hodgkin's disease and non-Hodgkin's lymphoma. Br J Haematol 115: 793–800
Oken MM, Creech RH, Tormey DC, Horton J, Davis TE McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5: 649–655
Setoain FJ, Pons F, Herranz R, Vidal-Sicart S, Lomena F, Ayuso C, Montserrat E, Setoain J (1997) 67 Ga scintigraphy for the evaluation of recurrences and residual masses in patients with lymphoma. Nucl Med Commun 18: 405–411
Spaepen K, Stroobants S, Dupont P, Van Steenweghen S, Thomas J, Vandenberghe P, Vanuytsel L, Bormans G, Balzarini J, De Wolf-Peeters C, Mortelmans L, Verhoef G (2001a) Prognostic value of positron emission tomography (PET) with fluorine-18 fluorodeoxyglucose ([18 F]FDG) after first-line chemotherapy in non-Hodgkin's lymphoma: is [18 F]FDG-PET a valid alternative to conventional diagnostic methods? J Clin Oncol 19: 414–419
Spaepen K, Stroobants S, Dupont P, Thomas J, Vandenberghe P, Balzarini J, De Wolf-Peeters C, Motelmans L, Verhoef G (2001b) Can positron emission tomography with [(18) F]-fluorodeoxyglucose after first-line treatment distinguish Hodgkin's disease patients who need additional therapy from others in whom additional therapy would mean avoidable toxicity? Br J Haematol 115: 272–278
Spaepen K, Stroobants S, Dupont P, Vandenberghe P, Thomas J, de Groot T, Balzarini J, De Wolf-Peeters C, Mortelmans L, Verhoef G (2002) Early restaging positron emission tomography with 18F-fluorodeoxyglucose predicts outcome in patients with aggressive non-Hodgkin's lymphoma. Ann Oncol 13: 1356–1363
Spaepen K, Stroobants S, Dupont P, Vandenberghe P, Maertens J, Bormans G, Thomas J, Balzarini J, De Wolf-Peeters C, Mortelmans L, Verhoef G (2003) Prognostic value of pretransplantation positron emission tomography using fluorine 18-fluorodeoxyglucose in patients with aggressive lymphoma treated with high-dose chemotherapy and stem cell transplantation. Blood 102: 53–59
Visvikis D, Ell PJ (2003) Impact of technology on the utilisation of positron emission tomography in lymphoma: current and future perspectives. Eur J Nucl Med Mol Imaging 30: 106–116
Weihrauch MR, Re D, Scheidhauer K, Ansen S, Dietlein M, Bischoff S, Bohlen H, Wolf J, Schicha H, Diehl V, Tesch H (2001) Thoracic positron emission tomography using 18 F-fluorodeoxyglucose for the evaluation of residual mediastinal Hodgkin disease. Blood 98: 2930–2934
Weihrauch MR, Dietlein M, Schicha H, Diehl V, Tesch H (2003) Prognostic significance of 18F-fluorodeoxyglucose positron emission tomography in lymphoma. Leuk Lymphoma 44: 15–22
Zinzani PL, Zompatori M, Bendandi M, Battista G, Fanti S, Barbieri E, Gherlinzoni F, Rimondi MR, Frezza G, Pisi P, Merla E, Gozzetti A, Canini R, Monetti N, Babini L, Tura S (1996) Monitoring bulky mediastinal disease with gallium-67, CT-scan and magnetic resonance imaging in Hodgkin's disease and high-grade non-Hodgkin's lymphoma. Leuk Lymphoma 22: 131–135
Zinzani PL, Martelli M, Magagnoli M, Pescarmona E, Scaramucci L, Palombi F, Bendandi M, Martelli MP, Ascani S, Orcioni GF, Pileri SA, Mandelli F, Tura S (1999a) Treatment and clinical management of primary mediastinal large B-cell lymphoma with sclerosis: MACOP-B regimen and mediastinal radiotherapy monitored by 67-Gallium scan in 50 patients. Blood 94: 3289–3293
Zinzani PL, Magagnoli M, Chierichetti F, Zompatori M, Garraffa G, Bendandi M, Gherlinzoni F, Cellini C, Stefoni V, Ferlin G, Tura S (1999b) The role of positron emission tomography (PET) in the management of lymphoma patients. Ann Oncol 10: 1181–1184
Zinzani PL, Chierichetti F, Zompatori M, Tani M, Stefoni V, Garraffa G, Albertini P, Alinari L, Ferlin G, Baccarani M, Tura S (2002) Advantages of positron emission tomography (PET) with respect to computed tomography in the follow-up of lymphoma patients with abdominal presentation. Leuk Lymphoma 43: 1239–1243
Acknowledgements
We are grateful to Robin MT Cooke for scientific editing.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
From twelve months after its original publication, this work is licensed under the Creative Commons Attribution-NonCommercial-Share Alike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/
About this article
Cite this article
Zinzani, P., Fanti, S., Battista, G. et al. Predictive role of positron emission tomography (PET) in the outcome of lymphoma patients. Br J Cancer 91, 850–854 (2004). https://doi.org/10.1038/sj.bjc.6602040
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.bjc.6602040
Keywords
This article is cited by
-
Poor prognosis in patients with diffuse large B cell lymphomas with bone marrow involvement possessing chromosomal abnormalities, despite aggressive treatment
Annals of Hematology (2020)
-
Primary mediastinal B-cell lymphoma
Current Respiratory Care Reports (2014)
-
FDG PET/CT predictive role in follicular lymphoma
European Journal of Nuclear Medicine and Molecular Imaging (2012)
-
Postchemotherapy PET evaluation correlates with patient outcome in paediatric Hodgkin’s disease
European Journal of Nuclear Medicine and Molecular Imaging (2011)
-
Primary Mediastinal DLBCL: Evolving Biologic Understanding and Therapeutic Strategies
Current Oncology Reports (2011)