FDG-PET/CT findings in systemic mastocytosis: a French multicentre study
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1 DOI /s ORIGINAL ARTICLE FDG-PET/CT findings in systemic mastocytosis: a French multicentre study S. Djelbani-Ahmed 1,2 & M. O. Chandesris 3,4,5 & A. Mekinian 6 & D. Canioni 3,5,7 & C. Brouzes 3,5,8 & K. Hanssens 3,9 & G. Pop 1 & I. Durieu 10 & S. Durupt 10 & B. Grosbois 11 & S. Besnard 11 & O. Tournilhac 12 & O. Beyne-Rauzy 13 & P. Agapé 14 & A. Delmer 15 & D. Ranta 16 & P. Y. Jeandel 17 & S. Georgin-Lavialle 18 & L. Frenzel 3,4,5 & G. Damaj 3,19 & V. Eder 1 & O. Lortholary 3,5,20 & O. Hermine 3,4,5 & O. Fain 6 & M. Soussan 1,2 Received: 2 April 2015 /Accepted: 10 June 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract Introduction Mastocytosis is a clonal haematological disease characterized by uncontrolled proliferation and the activation of mast cells. The value of FDG-PET/CT (FDG-PET) in mastocytosis has yet to be determined. Methods We retrospectively identified patients with an established diagnosis of systemic mastocytosis (SM), according to the WHO criteria, who underwent PET using the French Reference Centre for Mastocytosis database. Semi-quantitative and visual analysis of FDG-PET was performed and compared to the clinico-biological data. Results Our cohort included 19 adult patients, median age 65 years [range 58 74], including three with smouldering SM (SSM), three with aggressive SM (ASM), 10 with an S. Djelbani-Ahmed and M. O. Chandesris contributed equally to this work. * M. Soussan michael.soussan@avc.aphp.fr 10 Department of Internal and Vascular Medicine, Hospices Civils de Lyon, Groupe Hopitalier Sud, Université de Lyon, Pierre-Bénite, France 1 Department of Nuclear Medicine, Avicenne Hospital, Assistance Publique-HôpitauxdeParis(APHP),Bobigny,France 11 Department of Internal Medicine, Rennes University Hospital, Rennes, France Sorbonne Paris Cité, Paris 13 University, Bobigny, France French Reference center for Mastocytosis (Centre de Référence des Mastocytoses, CEREMAST), Necker Children s Hospital, APHP, Department of Haematology, Necker Children s Hospital, APHP, Sorbonne Paris Cité, Imagine Institute, Paris Descartes University, Department of Internal Medicine and Inflammation-Immunopathology-Biotherapy Department (DHU i2b), AP-HP, Saint Antoine Hospital, Department of Pathology, Necker Children s Hospital, APHP, Laboratory of Haematology, Necker Children s Hospital, APHP, INSERM U1068, Centre de Recherche en Cancérologie de Marseille (Signaling, Hematopoiesis and Mechanism of Oncogenesis), Paoli Calmettes Institute, Aix-Marseille University, Marseille, France Department of Internal Medicine, Clermont-Ferrand University Hospital, Clermont-Ferrand, France Department of Internal Medicine, Purpan University Hospital, Toulouse, France Department of Oncology and Haematology, Saint-Denis University Hospital, Saint-Denis de la Réunion, France Department of Haematology, Reims University Hospital, Reims, France Department of Haematology, Brabois University Hospital, Vandoeuvre les Nancy, France Department of Internal Medicine, Nice University Hospital, Nice, France Department of Internal Medicine, Tenon Hospital, Department of Haematology, Caen University Hospital, Caen, France Department of Infectious Diseases and Tropical Medicine, Necker Children s Hospital, APHP, Pasteur Institute,
2 associated clonal haematological non-mast-cell lineage disease (SM-AHNMD), and three with mast cell sarcoma (MCS). FDG-PET was performed at the time of the SM diagnosis (15/19), to evaluate lymph node (LN) activity (3/19) or the efficacy of therapy (1/19). FDG uptake was observed in the bone marrow (BM) (9/19, 47 %), LN (6/19, 32 %), spleen (12/19, 63 %), or liver (1/19, 5 %). No significant FDG uptake was observed in the SSM and ASM patients. A pathological FDG uptake was observed in the BM of 6/10 patients with SM-AHNMD, appearing as diffuse and homogeneous, and in the LN of 5/10 patients. All 3 MCS patients showed intense and multifocal BM pathological uptake, mimicking metastasis. No correlation was found between the FDG-PET findings and serum tryptase levels, BM mast cell infiltration percentage, and CD30 and CD2 expression by mast cells. Conclusions FDG uptake does not appear to be a sensitive marker of mast cell activation or proliferation because no significant FDG uptake was observed in most common forms of mastocytosis (notably purely aggressive SM). However, pathological FDG uptake was observed in the SM-AHNMD and in MCS cases, suggesting a role of FDG-PET in their early identification and as a tool of therapeutic assessment in this subgroup of patients. Keywords FDG PET/CT. Systemic mastocytosis Introduction Mastocytosis is a heterogeneous group of diseases characterized by the uncontrolled clonal proliferation of mast cells, their accumulation in one or more organs (mainly the skin and hematopoietic organs), and their autonomous and unregulated activation, leading to the excessive and inappropriate release of mast cell mediators. The CKIT D816V mutation is the molecular hallmark of the disease; however, in rare cases (less than 20 %), either a different mutation or no mutation is detected. Mastocytosis is considered systemic (systemic mastocytosis, SM) in cases of organ involvement other than the skin (bone marrow, gastro-intestinal tract, liver, and any other organ) [1]. Differentiation between the two major groups of the disease is most important in adult patients. Indolent mastocytosis is one type. Additionally, there are advanced types that present with very different clinical pictures and are associated with a radically different prognosis [2 4]. The indolent type includes cutaneous mastocytosis, indolent systemic mastocytosis (ISM), and smoldering systemic mastocytosis (SSM). This group is by far the most frequent (accounting for approximately 80 % of all cases of mastocytosis), which is characterized by frequent skin lesions (urticaria pigmentosa) and the absence of organ dysfunction (absence of C-Findings) with frequent mast cell mediator releasing symptoms. The advanced types of mastocytosis (accounting for approximately 15 % of all cases) include aggressive SM (ASM), mast cell leukaemia (MCL), SM with an associated clonal haematological non-mast-cell lineage disease (SM-AHNMD), and mast cell sarcoma (MCS). Those advanced forms of the disease are characterized by major organ infiltration that notably affects the hematopoietic organs (bone marrow, liver, and spleen) and the gastro-intestinal (GI) tract with dysfunction of one or more consecutive organs (C- Findings according to the WHO criteria); they are also rapidly life-threatening [4]. The SM-AHNMD picture and prognosis depend not only on the type of SM (most frequently ASM) but also on the type of AHNMD, usually of the myeloid type (myelodysplastic and myeloproliferative syndromes and acute myeloblastic leukaemia). With regards to prevalence, 880 patients are regularly followed up at the national French Reference Centre located at Necker Children s Hospital. We estimate a total of about 2000 cases of mastocytosis in France with 80 % of cutaneous mastocytosis or ISM, % ASM or SM-AHNMD, less than 1 % MCL, and an unknown prevalence of SSM (CEREMAST, national database, unpublished data). The usefulness of positron emission tomography/computed tomography with 2-[fluorine-18]-fluoro-2-deoxy-D-glucose (FDG-PET) in lymphoid malignancies has been validated for the grading, therapeutic monitoring and prognosis [5 7]. Few case reports on myeloid diseases showed diffuse and homogeneous bone marrow FDG uptake in patients with myelodysplastic syndromes [8], chronic myeloid leukaemia [9], and myelofibrosis [10]. With respect to the usefulness of PET in mastocytosis, a single series of five cases (three ASM, oneism,andonesm-ahnmd),usinganon-hybridpet, showed the absence of pathological FDG uptake [11], whereas two cases reports showed cutaneous, bone marrow, and lymph node FDG uptake in two patients with SM-AHNMD [12, 13]. Hence, the PET findings and interest of PET in SM remain to be determined. In this paper, we aimed to (i) analyse the FDG-PET findings in the different types of mastocytosis, (ii) evaluate the potential correlations with prognostic markers, and (iii) appreciate the relevance of FDG-PET in clinical practice. Patients and methods Patient inclusion The CEREMAST national computer database was authorized by the French National Data Protection Commission; CEREMAST authorization: CNIL: N (October 29, 2010). This database is used to store personal information and helped retrospectively to identify patients with mastocytosis who performed FDG-PET. Overall, 23 regional
3 centres affiliated with the CEREMAST and homogeneously distributed in France were contacted to obtain more information on potential cases. We retrospectively identified, through the CEREMAST, all adult patients with a confirmed diagnosis of mastocytosis (including genetics) according to the WHO criteria [4] who underwent FDG-PET over a period from January 2009 to February Clinical, biological, and radiological data were recorded at the time of SM diagnosis and at the time of FDG-PET. The classification of mastocytosis was based on signs of organ infiltration, with or without organ enlargement (B-Findings: liver and spleen enlargement, adenopathy) and dysfunction (C-Findings: cytopenia, portal hypertension, hypersplenism, malabsorption, pathological fracture) according to the WHO criteria [3, 4]. One C-Finding is sufficient to classify mastocytosis as aggressive, whereas two B-Findings without C-Finding lead to a diagnosis of smouldering mastocytosis. FDG-PET/CT Methodology PET studies were performed in 17 French sites on different PET cameras (Philips Medical Systems: n=7, General Electric Medical Systems: n=7 and Siemens Medical Systems: n=5). The median and range of time post-injection was 60 min (46 90) following the intravenous injection of FDG (median: 280 MBq, range ). The examined FDG-PET areas ranged from the middle of the head to the middle of the thigh. At the time of injection, the median capillary glycaemia was 6.8 mmol/l (range: mmol/ L). In all cases, a low-dose CT scan without iodine contrast agent was performed for attenuation correction, localization, and interpretation. Image analysis For all FDG-PET scans, a centralized re-reading was performed. Two independent nuclear medicine physicians (one junior and one senior) separately interpreted the scans. Both readers were blinded to clinical, histological, and biological data. Visual and semi-quantitative analyses were performed on an Extended Brilliance Workstation (EBW) (Philips Medical System). In case of discordant results, a common rereading was performed for each scan alone, leading to a single interpretation that had consensus. A visual interpretation of the PET scans was performed looking at pathological uptake, especially in usual locations of SM: bone marrow, lymph node (LN) chains, liver and spleen, skin, gastrointestinal tract. Pathological bone marrow uptake was defined as an uptake superior to the liver. Pathological LN uptake was defined as an uptake superior to the mediastinum. Pathological spleen uptake was defined as an uptake equal or more intense than the liver uptake. Pathological liver uptake was defined as a diffuse or multifocal intense uptake. Pathological skin uptake was defined as an uptake higher than background. Pathological gastrointestinal uptake was defined as a focal uptake. In addition, all scans were assessed semi-quantitatively using the SUVmax (normalized for the body weight) at each site. The SUVmax was also defined on a per-patient basis and corresponded to the maximum SUVmax of all sites. Low-dose CT scan was used to correlate pathological uptake to anatomical findings. Immunohistochemical analysis A systematic, centralized re-analysis of each biopsy (bone marrow or any other organ) was required and performed by a CEREMAST-affiliated French reference pathologist for mastocytosis from the Department of Pathology at Necker Children s Hospital (DC). Immunohistochemical analysis with anti-tryptase, anti-cd117 (= anti-ckit), and anti- CD25 antibodies was performed to confirm the diagnosis of SM according to the WHO criteria [4, 14]. The estimated pathological mast cell infiltration as the percentage of CKIT positive cells from the total cell population, as well as of the percentage of CD30-expressing mast cells (= percentage of CKIT positive cells expressing CD30) was recorded. When available, data from the flow cytometric immunophenotypic analysis of bone marrow infiltrating mast cells, using the CD117, CD2, and CD25 phenotypic markers, were collected. Molecular analysis of c-kit gene to screen the D816V mutation was performed from the skin and/or bone marrow sample. Statistical analysis Quantitative variables were expressed as the median with ranges, and qualitative variables were expressed as numbers with frequencies. The interobserver reproducibility of PET interpretations was assessed by calculating the kappa statistic between both observers (Cohen s κ). The Fisher test was used for qualitative variables and the Mann Whitney test for continuous variables. The Kruskal-Wallis test was used to evaluate differences in the FDG-PET parameters according to the SM types. Correlations between the FDG-PET values (global score, SUV max) and tryptase levels, mast cell infiltration percentage, and CD30 and CD2 expression by mast cells were evaluated using the Pearson correlation coefficient. A p value<0.05 was considered statistically significant. All statistical analyses were performed using GraphPad Prism Software version 5.1 (GraphPad Software, San Diego, CA, USA, 2007).
4 Results Patient s clinical, biological and histological data Nineteen patients (17 men, 89 %) with a median age of 65 years (58 74) were included. In 15/19 patients, FDG- PET was performed for diagnostic investigations at the time of the SM diagnosis, before any cytoreductive treatment. In 3/19 patients (all with a smouldering form of the disease), FDG-PET was performed to investigate progression of previously known LN. In one patient (1/19), FDG-PET was performed at the time of relapse following a first line of cytoreductive therapy (cladribine). The patient characteristics are shown in Table 1. Three patients had SSM (16 %), three patients had ASM (16 %), ten patients had SM-AHNMD (52 %), and three patients had MCS (16 %). The AHNMD cases were myelodysplastic syndrome (MDS) (4/10), myeloproliferative syndrome (MPS) (2/10), mixed myeloproliferative/myelodysplastic syndrome (MPS/MDS) (2/10), monoclonal gammopathy of undetermined significance (MGUS) (1/10), and marginal-zone lymphoma (MZL) (1/10). All patients except one had a bone marrow biopsy (BMB), and 7/19 had another organ biopsy/ histology (gastrointestinal tract n=2, LN n=2, spleen n=1, nasopharynx n=1, and epidural space n=1). The median serum tryptase level was 200 ng/ml (32 975); 11/19 patients had a tryptase level up to 200 ng/ml. Furthermore, 15/19 patients presented with at least 1 C-Finding (organ dysfunction sign), and they had a median of 3 C-findings (range 1 4). BMB analysis revealed a median mast cell infiltration level of 30 % (range %). CD30 and CD2 staining of the bone marrow mast cells is described in Table 1. A CKIT D816V mutation was found in 15/18 patients (83 %), a mutation in exon 11 in 1 patient and no mutation (CKIT wild-type) in three patients (16 %). Cytoreductive therapy was required for all except one patient with SSM, and it included steroids (n=11), cladribine (n=5), tyrosine kinase inhibitors (n=13) and 5-azacytidine (n=2). One patient with ASM-AHNMD died before treatment. At the final follow-up (median time 2.6 years [ ]), 12 deaths were recorded from MSA (n=1), SM- AHNMD (n=9), or MCS (n=2). The median survival time was 4 years. FDG-PET findings On a per-patient basis, a pathological FDG uptake was observed in 15/19 patients (79 %), with a median SUVmax at 4.3 [1 12.2]. The per-site analysis showed pathological uptake in the bone marrow, spleen, LN, and liver (Table 2). Pathological FDG uptake was observed in the bone marrow in 9/19 patients (47 %) with a median SUVmax at 4.6 [2 12.2] (Table 2). The overall agreement between the both observers was κ=0.69 (95 % Confidence Interval: 0.24; 1.13) for assessing pathological bone marrow uptake. Bone marrow uptake appeared as diffuse and homogenous in 6/9 patients; it was located in the axial and proximal appendicular skeletons and was associated with a pattern of osteosclerosis at CT scan (defined as an increase bone density) in 4/6 patients. Bone marrow uptake was multifocal in 3/9 patients and was associated with a mixed pattern of lytic and osteosclerotic lesions at CT scan. Of note, two patients (2/19) had a fracturerelated focal vertebral uptake. Pathological FDG uptake was observed in the spleen in 12/ 19 patients (63 %), with a median SUVmax of 3.3 [2 4.4], appearing as diffuse in all 12 patients. Pathological liver diffuse uptake was observed in one patient (SUVmax=4.3). Pathological LN uptake was seen in 6/19 patients (32 %), with a median SUVmax at 3.7 [ ]) (Table 2), and the uptake was located in the cervical (n=4), thoracic (n=4), and abdomino-pelvic areas (n=4). All hypermetabolic LN were supra-centimetric on CT scan. The overall agreement between the both observers was κ=0.87 (95 % Confidence Interval: 0.43; 1.32) for assessing pathological lymph node uptake. We did not observe any pathological uptake in the skin or in the gastrointestinal tract. Correlations between FDG-PET findings and SM characteristics There was no pathological bone marrow uptake in either SSM or ASM cases. Yet, a slight FDG bone marrow uptake (inferior or equal to the liver) was observed in 2/3 patients with ASM. No LN uptake was observed in either SSM or ASM cases, in spite of the presence of enlarged LNs in half of these patients (3/6). In patients with SM-AHNMD, pathological FDG uptake in the bone marrow was observed in 6/10 patients. These six patients had MDS (n=2), mixed MPS/MDS (n=2), MPS (n=1), and MZL (n=1). Splenic FDG uptake was observed in 8/10 patients (80 %). LN uptake was observed in half of the cases (5/10: MDS n=1, MPS n=1, MGUS n=1, MZL n=1, and MPS/MDS n=1). Finally, all MCS patients showed intense and multifocal abnormal uptake located in the bone marrow (Fig. 1). MCS patients exhibited also a dorsal intramuscular hypermetabolic lesion in one case, and an aggressive vertebral lesion with epidural extension in another case. On a per-patient basis, the median SUVmax values in the ASM, SM-AHNMD, and MCS cases were 2.8 [ ], 4.6 [2 5.8] and 7.3 [ ] (p=0.05), respectively, showing a trend to an association of the FDG uptake with the type of SM (Fig. 2, Table 2). No association was found between the PET findings and tryptase serum levels, either with the percentage of
5 Table 1 Clinical and biological parameters of the 19 patients Mastocytosis type a n (%) Total population 19 (100) SSM ASM SM-AHNMD 10 (52) MCS Ageinyears,median(range) 65(58 74) 58 (58 63) 77 (73 79) 67 (49 84) 58 (42 65) PET timing At the time of SM diagnosis, n (%) 15 (79) 1 (33) 3 (100) 9 (90) 2 (67) During SM follow-up, n (%) 4 (21) 2 (67) 0 (0) 1 (10) 1 (33) Main clinic-biological featuresskin involvement b, n (%) 10 (53) 2 (66) 3 (100) 4 (40) 1 (33) H/SMG, n (%) 15 (79) 1 (33) 3 (100) 9 (90) 2 (66) LN enlargement, n (%) 4 (21) 2 (66) 0 (0) 2 (20) 0 (0) C-Findings c, median [range] 2 [0 4] 0 3 [2 4] 3.5 [1 4] 1 [0 3] Tryptase d, median [range] 200 [32 975] 182 [ ] 467 [ ] 180 [32 482] 319 [ ] C-KIT D816V, n (%) 15/18 (83) 2/2 (100) 3/3 (100) 10/10 (100) 0/3 (0) e Bone marrow mast cell infiltration f,medianin%[range] 30[10 80] 40 [20 80] 30 [30 40] 35 [10 60] 30 [30 30] CD30 expression g, n (%) 9/16 (56) 1/3 (33) 2/3 (66) 4/8 (50) 2/2 (100) Median in % [range] <10 [<10 80] 0 [0 30] <10 [0 <10] 0 [0 20] 50 [20 80] Reduced / loss of CD2 expression h, n (%) 8/15 (53) 1/2 (50) 0/2 (0) 4/8 (50) 3/3 (100) Abbreviations: AHNMD associated clonal haematological non-mast cell lineage disease, ASM aggressive SM, H/SMG hepato- and/or splenomegaly, LNs lymph nodes, MCS mast cell sarcoma, n number, SM systemic mastocytosis, and SSM smoldering SM The classification of mastocytosis was based on the presence/absence and number of B (organ infiltration) and C (organ dysfunction) findings according to the WHO classification [4] a b Urticaria pigmentosa C-Findings or signs of organ dysfunction that indicate the aggressiveness of mastocytosis and include the following: one or more cytopenia, Hypersplenism, Portal hypertension and liver insufficiency, Malabsorption with consecutive cachexia The normal value of tryptase is <13.5 ng/ml Two patients were C-KIT wild-type (WT), and the last had a mutation on codon 560 of exon 11 c d e Defined as the percentage of CKIT expressing cells using immunohistochemistry (IHC) on bone marrow biopsy (BMB) f g h IHC on BMB Flow cytometry on fresh bone marrow aspirate
6 Table 2 Results of the FDG-PET findings Mastocytosis type a n (%) Total population 19 (100) SSM 3(16) ASM SM-AHNMD 10 (52) MCS Per-patient analysis Pathological uptake, n (%) 15 (79) 0 (0) 2 (13) 10 (100) 10 (100) SUV max, median [range] 4.3 [1 12.2] 2.8 [ ]* 4.6 [2 5.8]* 7.3 [ ]* Per-site analysis Bone Marrow b Pathological uptake, n (%) 9 (47) 0 (0) 0 (0) 6 (60) 3 (100) SUV max, median [range] 4.6 [2 12.2] 4[2 5] 7.8 [ ] Lymph Nodes c Pathological uptake, n (%) 6 (32) 0 (0) 0 (0) 5 (50) 1 (33) SUV max, median [range] 3.7 [ ] 3.7 [ ] 3.8 Spleen d Pathological uptake, n (%) 12 (63) 0 (0) 2 (66) 8 (80) 2 (66) SUV max, median [range] 3.3 [2 4.4] 2.8 [ ] 3.4 [2 4.4] 3.3 [3 3.5] Liver e Pathological uptake, n (%) 1 (5) 0 (0) 0 (0) 1 (10) 0 (0) SUV max, median Abbreviations: AHNMD associated clonal haematological non-mast cell lineage disease, ASM aggressive SM, H/SMG hepato and/or splenomegaly, LN lymph nodes, MCS mast cell sarcoma, n number, SM systemic mastocytosis, and SSM smoldering SM a The classification of mastocytosis was based on the presence/absence and number of B (organ infiltration) and C (organ dysfunction) findings according to the WHO classification [4] b Pathological bone marrow uptake was defined as an uptake superior to the liver c Pathological LN uptake was defined as an uptake superior to the mediastinum d A pathological splenic uptake was defined as more intense than liver uptake e A pathological liver uptake was defined as a diffuse and intense uptake * Comparison between the ASM, SM-AHNMD and MCS patients, p=0.05 (Kruskal-Wallis test) Fig. 1 Illustrative cases of the FDG-PET patterns. a No significant bone marrow FDG uptake was observed in the smoldering form of SM. b In the aggressive form of SM, a slight bone marrow FDG uptake can be observed equal, but not superior to the liver. c In contrast, intense and diffuse bone marrow FDG uptake (> liver uptake) is seen in SM with associated haematological disorders (patient with MDS). d A patient with mast cell sarcoma exhibiting a singular pattern with multifocal and intense bone marrow FDG uptake
7 Fig. 2 SUVmax results according to the type of systemic mastocytosis. Abbreviations: AHNMD associated clonal haematological non-mast cell lineage disease, ASM aggressive SM, MCS mast cell sarcoma mast cell infiltration in BMB or with the CD2 or CD30 expression by mast cells (p>0.05). Discussion In this study, we aimed to evaluate the potential usefulness of FDG-PET in systemic mastocytosis, especially in the evaluation of aggressive types, which have the worst prognosis and require efficient treatment monitoring. Our results showed that there are no significant differences in the FDG- PET findings between the smoldering (SSM) and purely aggressive (ASM without AHNMD) types of mastocytosis. Indeed, no pathological uptake was observed in SSM and none was observed in ASM, where only moderate and inconstant FDG uptake could be seen in spite of the rapid tumour growth that was responsible for massive tumour infiltration, including hematopoietic organ enlargement and dysfunction. Therefore, these observations showed the limited usefulness of FDG-PET for estimating the prognosis and assessing the therapeutic effects in ASM. FDG-PET could, however, reveal abnormal findings in SM-AHNMD with intense and diffuse pathological bone marrow uptake in 60 % of the patients (6/10), which was mostly from myelodysplastic syndromes, and lymph node uptake in 50 % of patients. In those cases, the associated haematological disorder was probably the major contributor of the high bone marrow uptake [15, 8]. In addition to histological and cytological analysis as well as cytogenetics, FDG-PET could contribute to the early identification of patients with AHNMD because morphological features of myelodysplasia on the bone marrow smear are frequent in mastocytosis and are not always synonymous of authentic MDS, delaying diagnosis and treatment. In contrast, a very particular FDG-PET pattern was observed in mast cell sarcoma, where multifocal and intense bone marrow uptake was observed. This pattern mimicking multifocal metastases from a solid malignancy was only observed in MCS, suggesting the value of FDG-PET for the diagnosis and therapeutic assessment of this extremely rare, usually highly proliferative (illustrated by high Ki67 expression levels) and pejorative type of mastocytosis. The exact origin of FDG uptake is a tricky question. In solid tumours, it is well established that beyond the tumour glucose consumption, tumour infiltrating inflammatory cells also participate in FDG uptake [16]. In mastocytosis, FDG uptake could be due to activated mast cells themselves, AHNMD-related tumour cells, osteoblastic activation in the case of bone condensing type lesions and medullar regeneration [17]. Our results, including the absence of marked pathological uptake in the purely aggressive form of SM (ASM), suggest that mast cell activation and infiltration are not well delineated by FDG-PET. In this study, there was no correlation between the FDG-PET/CT data and known markers of proliferation and aggressiveness. This is confirmed by the absence of a correlation between the intensity of the uptake and (i) the circulating tryptase levels, reflecting that the degree of mast cell infiltration is an authentic tumour marker in the aggressive types [3]; (ii) the CD30 expression by mast cells, which is an immunochemistry marker that is associated with a poor prognostic value in aggressive forms [14]; (iii) and the loss of expression of CD2, another poor prognosis factor in aggressive forms (CEREMAST, unpublished data). The thymidine analogue 3-deoxy-3-18 F-fluorothymidine ( 18 F-FLT), a tracer that undergoes the same first metabolic step as thymidine, can be used to image cell proliferation. Increased 18 F-FLT uptake in the bone marrow has been observed in patients with haematological disorders, such as MDS and MPD [18]. Therefore, it is worth testing 18 F- FLT to evaluate its specificity and sensitivity with respect to mast cell proliferation and activation [19, 18]. Others tracers, such as labelled amino acids (tyrosine or methionine), could also lead to another research direction for imaging the amino acid activity in highly proliferative tissues, such as bone marrow [20]. Our study has several limitations. The SUV results should be interpreted with caution considering that the FDG-PET scans were conducted at different sites with different techniques (variety of injected doses, image acquisition delays, type of machine and reconstruction modes). To overcome this issue, we performed a complementary visual analysis, which we based on the scale used for the PET evaluation of lymphomas therapy [5]. This visual analysis appeared reproducible; the interobserver agreements were 0.69 and 0.87, which is consistent with results from previous studies [21]. The overrepresentation of FDG-PET performed in SM-AHNMD patients is another limitation to appreciate the relevance of FDG- PET in clinical practice for the field of mast cell diseases. In conclusion, we found that FDG-PET cannot distinguish between indolent and purely aggressive SM, suggesting that
8 FDG is not a sensitive marker of mast cell activation and proliferation. By contrast, diffuse and intense bone marrow uptake efficiently raised the possibility of AHNMD, while a pattern mimicking solid tumour metastasis was highly suggestive of MCS; therefore, FDG-PET could be an interesting tool for following the treatment efficacy in this setting. Acknowledgments We would like to thank Isabelle Hirsch and Laure Cabaret from CEREMAST for their work as clinical trial associates. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required. Informed consent was obtained from all individual participants included in the study Sources of support References No financial support was received. 1. Fain O, Stirnemann J, Lortholary O. Systemic mastocytosis. Rev Prat. 2005;55(15): Gotlib J, Pardanani A, Akin C, Reiter A, George T, Hermine O, et al. International Working Group-Myeloproliferative Neoplasms Research and Treatment (IWG-MRT) & European Competence Network on Mastocytosis (ECNM) consensus response criteria in advanced systemic mastocytosis. Blood. 2013;121(13): Valent P, Akin C, Arock M, Brockow K, Butterfield JH, Carter MC, et al. Definitions, criteria and global classification of mast cell disorders with special reference to mast cell activation syndromes: a consensus proposal. Int Arch Allergy Immunol. 2012;157(3): Valent P, Horny HP, Escribano L, Longley BJ, Li CY, Schwartz LB, et al. Diagnostic criteria and classification of mastocytosis: a consensus proposal. Leuk Res. 2001;25(7): Biggi A, Gallamini A, Chauvie S, Hutchings M, Kostakoglu L, Gregianin M, et al. International validation study for interim PET in ABVD-treated, advanced-stage Hodgkin Lymphoma: Interpretation Criteria and Concordance Rate Among Reviewers. J Nucl Med Hutchings M. How does PET/CT help in selecting therapy for patients with Hodgkin lymphoma? Hematol Am Soc Hematol Educ Program. 2012;2012: Moskowitz CH. Interim PET-CT in the management of diffuse large B-cell lymphoma. Hematol Am Soc Hematol Educ Program. 2012;2012: Inoue K, Okada K, Harigae H, Taki Y, Goto R, Kinomura S, et al. Diffuse bone marrow uptake on F-18 FDG PET in patients with myelodysplastic syndromes. Clin Nucl Med. 2006;31(11): Nakajo M, Jinnouchi S, Inoue H, Otsuka M, Matsumoto T, Kukita T, et al. FDG PET findings of chronic myeloid leukemia in the chronic phase before and after treatment. Clin Nucl Med. 2007;32(10): Burrell SC, Fischman AJ. Myelofibrosis on F-18 FDG PET imaging. Clin Nucl Med. 2005;30(10): Zettinig G, Becherer A, Szabo M, Uffmann M, Dudczak R, Valent P, et al. FDG positron emission tomography in patients with systemic mastocytosis. AJR Am J Roentgenol. 2002;179(5): Kim Y, Weiss LM, Chen YY, Pullarkat V. Distinct clonal origins of systemic mastocytosis and associated B-cell lymphoma. Leuk Res. 2007;31(12): Tomihama RT, McEachen JC, Kuo PH. Imaging of systemic mastocytosis by FDG-PET/CT demonstrates increased activity in cortical bone. Clin Nucl Med. 2008;33(3): Valent P, Sotlar K, Horny HP. Aberrant expression of CD30 in aggressive systemic mastocytosis and mast cell leukemia: a differential diagnosis to consider in aggressive hematopoietic CD30- positive neoplasms. Leuk Lymphoma. 2011;52(5): Dong A, Wang Y, Gao L, Zuo C. 18F-FDG PET/CT findings in a patient with sweet syndrome associated with myelodysplastic syndrome. Clin Nucl Med Brown RS, Leung JY, Fisher SJ, Frey KA, Ethier SP, Wahl RL. Intratumoral distribution of tritiated fluorodeoxyglucose in breast carcinoma: I. Are inflammatory cells important? J Nucl Med. 1995;36(10): Fritz J, Fishman EK, Carrino JA, Horger MS. Advanced imaging of skeletal manifestations of systemic mastocytosis. Skeletal Radiol. 2012;41(8): Agool A, Glaudemans AW, Boersma HH, Dierckx RA, Vellenga E, Slart RH. Radionuclide imaging of bone marrow disorders. Eur J Nucl Med Mol Imaging. 2010;38(1): Vanderhoek M, Juckett MB, Perlman SB, Nickles RJ, Jeraj R. Early assessment of treatment response in patients with AML using [(18)F]FLT PET imaging. Leuk Res. 2010;35(3): Dankerl A, Liebisch P, Glatting G, Friesen C, Blumstein NM, Kocot D, et al. Multiple myeloma: molecular imaging with 11Cmethionine PET/CT initial experience. Radiology. 2007;242(2): Itti E, Meignan M, Berriolo-Riedinger A, Biggi A, Cashen AF, Vera P, et al. An international confirmatory study of the prognostic value of early PET/CT in diffuse large B-cell lymphoma: comparison between Deauville criteria and DeltaSUVmax. Eur J Nucl Med Mol Imaging. 2013;40(9):
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