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Annals of Oncology Advance Access originally published online on August 22, 2007
Annals of Oncology 2007 18(10):1685-1690; doi:10.1093/annonc/mdm265
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© 2007 European Society for Medical Oncology

hematologic malignancies

FDG-PET in T-cell and NK-cell neoplasms

S. Kako1, K. Izutsu1, Y. Ota4, Y. Minatani2, M. Sugaya2, T. Momose3, K. Ohtomo3, Y. Kanda1, S. Chiba1, T. Motokura1 and M. Kurokawa1,*

1 Department of Hematology & Oncology
2 Department of Dermatology
3 Department of Radiology, Graduate School of Medicine, University of Tokyo
4 Department of Pathology, Toranomon Hospital, Tokyo, Japan

* Correspondence to: Mineo Kurokawa, Department of Hematology & Oncology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. Tel: +81-3–5800–9092; fax: +81-3–5840–8667; e-mail address: kurokawa-tky{at}umin.ac.jp.


   Abstract
Top
 Abstract
introduction
 patients and methods
 results
 discussion
 References
 
Background: A growing number of studies demonstrate the utility of 18fluoro-2-deoxyglucose positron emission tomography (FDG-PET) in the management of malignant lymphoma. The results of FDG-PET, however, have not been studied extensively for T-cell and natural killer (NK)-cell neoplasms.

Patients and methods: We retrospectively evaluated pretreatment FDG-PET scans in 41 patients with T/NK-cell neoplasms diagnosed according to the World Health Organization (WHO) classification. Histological subtypes frequently included were peripheral T-cell lymphoma, unspecified (PTCLu, n = 11), extranodal NK/T-cell lymphoma, nasal type (ENKL, n = 8), primary cutaneous anaplastic large cell lymphoma (C-ALCL, n = 5), and angioimmunoblastic T-cell lymphoma (AILT, n = 4).

Results: FDG-PET detected a lymphoma lesion in at least one site in 36 out of 41 patients. The positive rate was equally high in most histological subtypes except for cutaneous lymphomas: PTCLu 91%, ENKL 100%, C-ALCL 60%, AILT 100%. All the patients without an FDG-avid lesion had lesions restricted to skin. Among patients who had cutaneous lesions, only 50% had FDG-avid cutaneous lesions, all of which were tumorous. The positive rate of FDG-PET for bone marrow involvement was only 20%.

Conclusion: T/NK-cell neoplasms incorporated in this study were generally FDG-avid except for cutaneous lesions and bone marrow involvement.

Key words: FDG-PET, T/NK-cell neoplasms, cutaneous lesions


   introduction
Top
 Abstract
 introduction
patients and methods
 results
 discussion
 References
 
Standard procedures for the pretreatment evaluation of patients with malignant lymphoma include physical examination, computed tomography (CT) scanning and bone marrow (BM) examination. Nuclear medicine imaging has been frequently used as an adjunctive method in staging, adding information as to functional or metabolic characteristics of lymphoma. Recently, a prominent role for 18fluoro-2-deoxyglucose positron emission tomography (FDG-PET) in the management of lymphoma has been established. Many studies have demonstrated the utility of FDG-PET for staging [1, 2] and the therapeutic response assessment of lymphoma [3–5], and currently, more attention is being paid to the role of PDG-PET after two to three cycles of chemotherapy as an early prognostic predictor [6, 7]. Moreover, the incorporation of FDG-PET findings into response criteria of lymphoma has been proposed [8]. On the other hand, several studies have shown the different intensity of FDG uptake among each subtype of lymphomas [9], which could be explained by the histological profile such as the proliferating nature of tumor cells or the proportion of viable tumor cells and reactive non-malignant cells [10, 11]. These results, however, have been obtained mainly in patients with B-cell neoplasms [12], and the extent of FDG uptake in T-cell and natural killer (NK)-cell neoplasms or the role of FDG-PET in the management of T/NK-cell neoplasms has not been described. Thus, we retrospectively reviewed the results of FDG-PET in patients with T/NK-cell neoplasms diagnosed according to the World Health Organization (WHO) classification, and examined the positive rate of pretreatment FDG-PET.


   patients and methods
Top
 Abstract
 introduction
 patients and methods
results
 discussion
 References
 
patients
All patients with a pathological diagnosis of T/NK-cell neoplasm who underwent FDG-PET scanning in our institute between July 2003 and December 2006 were selected in this study. Pathological diagnoses were made according to the WHO classification. All FDG-PET scans performed at initial diagnosis, at relapse or at progression were included and retrospectively analyzed. FDG-PET scans were performed prior to systemic chemotherapy in all patients at initial diagnosis. The time from the last systemic chemotherapy to the FDG-PET scanning was at least 4 weeks in patients at relapse and at least 3 weeks in patients at progression.

FDG-PET scanning
FDG-PET scans were performed on a high-resolution, dedicated, whole-body PET camera, GE ADVANCE (GE Medical Systems, Waukesha, WI). Patients fasted for 4 hours. Emission data were acquired in 5–7 bed positions, for 2.5 minutes at each position, typically from the top of the skull to the proximal thighs, approximately 60 minutes after the intravenous administration of 296 MBq of F-18 FDG. Ge-68 transmission scans were used to generate the transmission map. A segmented attenuation map was then generated. PET images were reconstructed using Ge-68 for attenuation correction with the ordered subsets expectation maximization algorithm and an 8 mm Gaussian filter, and were displayed in a 128 by 128 matrix. Two experienced radiologists scrutinized all scans. Interpretation of the PET images was in line with the recommendations in the recent publication from the International Harmonization Project [13]. Briefly, focal or diffuse FDG uptake above background in a location incompatible with normal anatomy or physiology was interpreted as abnormal and was considered to be indicative of a lymphoma lesion. In areas with abnormal FDG accumulation, the standard uptake value (SUV) was calculated according to the standard formula. However, we did not use SUV as a specific cutoff value. For the present study, we defined that the result of FDG-PET was positive if FDG-PET detected a lymphoma lesion in at least one site detected by physical examination, CT or BM examination on the basis of the definition in previous reports [12]. In CT scans, a nodule with more than 1.5 cm in their long axis at any site was considered to be a lymphoma lesion.

Comparison between FDG-PET and iliac crest BM biopsy and/or aspiration was performed separately. Samples of biopsy and/or aspiration were examined for BM involvement by pathologists. FDG-PET results of BM were evaluated by radiologists, and we defined that the result of FDG-PET was positive if there was an FDG-avid lesion in BM of patients whose BM involvement was confirmed by biopsy.

We also examined whether FDG-PET detected each lesion that was detected by physical examination or CT and whether each area with FDG uptake was detected by such conventional procedures as a lymphoma lesion site by site. In this analysis, multiple affected lymph nodes in one nodal region were counted as one lesion. Lesions in skin or BM were not included in this analysis.


   results
Top
 Abstract
 introduction
 patients and methods
 results
discussion
 References
 
patient characteristics
A total of 41 patients with a pathological diagnosis of T/NK-cell neoplasm underwent the FDG-PET scanning in our institute between July 2003 and December 2006. FDG-PET scans were performed at initial diagnosis in 31 patients and at relapse or progression in 10 patients. The histological subtypes frequently included were peripheral T-cell lymphoma, unspecified (PTCLu, n = 11), extranodal NK/T-cell lymphoma, nasal type (ENKL, n = 8), primary cutaneous anaplastic large cell lymphoma (C-ALCL, n = 5), angioimmunoblastic T-cell lymphoma (AILT, n = 4), anaplastic large cell lymphoma (ALCL, n = 3), and mycosis fungoides and Sezary syndrome (MS/SS, n = 3) according to the WHO classification. Patient characteristics of each histological subtype are summarized in Table 1.


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  		Table 1. Patient characteristics

 
FDG-PET scan results in T/NK-cell neoplasms
FDG-PET detected a lymphoma lesion in at least one site in 36 out of 41 patients. The positive rate of FDG-PET according to histological subtypes was 100% in patients with ENKL, AILT and ALCL, and 91% in patients with PTCLu. However, the positive rate of FDG-PET was only 66% in patients with C-ALCL and 33% in patients with MF/SS (Table 2). The maximum SUV (SUV max) was recorded in patients with FDG-avid lesions. SUV max varied widely even among patients with the same histological subtype (Figure 1).


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  		Table 2. Positive rate of FDG-PET in T/NK-cell neoplasms

 

Figure 1
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  		Figure 1. SUV max according to histological subtypes. Scattergram of the maximum standard uptake value (SUV max) according to histological subtypes. SUV max varied widely within the same histological subtype. Abbreviations: PTCLu, peripheral T-cell lymphoma, unspecified; ENKL, extranodal natural killer/T-cell lymphoma, nasal type; C-ALCL, primary cutaneous anaplastic large cell lymphoma; AILT, angioimmunoblastic T-cell lymphoma; ALCL, anaplastic large cell lymphoma; MF/SS, mycosis fungoides and Sezary syndrome.

 
In the present study, FDG-PET could not detect any lesion in five patients, two at diagnosis and three at relapse or progression. All these patients, including one with PTCLu, two with C-ALCL and two with MF/SS, had lesions restricted to skin. Therefore, we analyzed the results of FDG-PET in 14 patients who had primary or secondary cutaneous lesions confirmed by biopsy (Table 3). FDG-PET detected a cutaneous lesion in at least one site in seven out of 14 patients. FDG-avid cutaneous lesions were all tumorous, and FDG-PET could not detect patches, plaques or even erythrodermic lesions regardless of the extent of the involved area. The positive rate of FDG-PET for cutaneous lesions according to histological subtypes was only 67% in patients with PTCLu and 40% in patients with C-ALCL. In three patients with MF/SS, FDG-PET could not detect any cutaneous lesion. None of these three patients had tumorous lesions (Table 3).


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  		Table 3. Positive rate for cutaneous lesions in T/NK-cell neoplasms

 
detection of BM involvement by FDG-PET
Iliac crest BM biopsy and/or aspiration was performed at least unilaterally in 35 patients within 6 weeks of the FDG-PET scanning. Five patients with relapsed or progressive lymphoma did not undergo BM study at the time of the FDG-PET scanning, and another patient with MF had never undergone BM study. In 35 patients analyzed, BM involvement was detected pathologically by biopsy in five patients. However, FDG-PET detected BM involvement in only one patient out of these five patients (Table 4). In one patient with ENKL, FDG-PET showed focal uptake in BM. BM biopsy and aspiration, however, showed hemophagocytosis, but involvement of lymphoma was not detected. The second biopsy directed at the site of focal uptake was not performed in this patient.


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  		Table 4. Detection of bone marrow (BM) involvement by FDG-PET

 
FDG-avidity of lymphoma lesions
We analyzed FDG-avidity of each lesion according to histological subtypes. To this end, we examined whether FDG-PET detected each lesion that was detected by conventional procedures site by site. In this analysis, lesions in skin or BM were not included because FDG-PET had limitations in detecting lesions in these sites, as described above. As shown in Table 5, the majority of lesions were uniformly FDG-avid in most histological subtypes with some exceptions. In one patient with AILT, only three out of eight nodal lesions were FDG-avid. In another patient with C-ALCL, FDG-PET could not detect a nodular lesion in spleen, while it detected all nodal lesions in eight regions. In one patient with SS, no nodal lesion was FDG-avid. FDG-avidity was observed only in BM in this patient. Conversely, most of FDG-avid areas were detected by conventional procedures (Table 6).


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  		Table 5. FDG-avidity of lesions detected by conventional procedures (CP)

 

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  		Table 6. Results of conventional procedures (CP) in FDG-avid areas

 

   discussion
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
References
 
While many studies have demonstrated the utility of FDG-PET in the management of malignant lymphoma, several reports indicated diverse intensity of FDG uptake among different histological subtypes of lymphoma. Hoffmann et al. showed the lower detection ability of FDG-PET for extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT-lymphoma) [14], and another report showed that SUV was useful in distinguishing between aggressive and indolent lymphoma [9]. These results imply that the histological subtype should be taken into account in interpreting the results of FDG-PET. Several subtypes of T/NK-cell neoplasms have distinct pathological features such as prominent inflammatory background in AILT and frequent tissue necrosis in ENKL [15], which might affect the results of FDG-PET. In addition, T/NK-cell neoplasms have distinct clinical features, such as the higher frequency of advanced-stage disease and extranodal lesions and the poorer prognosis, compared to common B-cell neoplasms [16–18]. Therefore, the potential role of FDG-PET in the management of T/NK-cell neoplasms should be confirmed separately.

The present study showed the high positive rate of pretreatment FDG-PET in most subtypes of T/NK-cell neoplasms as reported in B-cell neoplasms [7, 12], in spite of the different pathological and clinical characteristics. In nodal lesions and extranodal lesions other than skin and BM, the positive rate was almost 100% in all histological subtypes (Table 2). In the present study, however, there were several lesions detected only by conventional procedures without FDG uptake, and, conversely, there were several FDG-avid areas which were not confirmed as lymphoma lesions by conventional procedures, even in sites other than skin and BM. We were not able to determine that these results of FDG-PET were false-negative and false-positive, respectively because biopsies directed at such sites or follow-up FDG-PET scans after therapies were not necessarily performed. Among T/NK-cell neoplasms, we could not find any relation between SUV max values and histological subtypes in this study.

Although T/NK-cell neoplasms involve skin more often than B-cell neoplasms [16], the positive rate of FDG-PET for cutaneous lesions was only 50% in this study, indicating a limited role of FDG-PET in the detection of cutaneous lesions of T/NK-cell neoplasms. It is worth noting that discordant FDG-PET results between cutaneous lesions and lesions other than skin were observed in some patients. Similar results were also demonstrated in other reports [19, 20]. One explanation for the low positive rate of FDG-PET for cutaneous lesions may be the partial volume averaging effect due to the limited spatial resolution of the PET system [21]. In support of this is the fact that FDG-PET detected only tumorous cutaneous lesions rather than erythroderma with large involved area, as shown in this study. Recently, the high sensitivity of FDG-PET to detect cutaneous lesions of lymphoma was reported [22]. However, that study included patients with various types of lymphoma, and the characteristics of each cutaneous lesion were not described in details. Concerning cutaneous lesions of B-cell neoplasms, six patients had FDG-avid lesions out of nine patients reported individually in sporadic reports to date [12, 22–25]. It is of note that four patients out of those six had tumorous cutaneous lesions of diffuse large B-cell lymphoma. In the present study, the positive rate of FDG-PET might be somewhat lower in patients at relapse or progression (70%; 95% confidence interval [CI], 35–93%) than in patients at diagnosis (94%; 95% CI, 79–99%). However, this could be attributed to the fact that the proportion of patients whose lesions were restricted to skin was higher in the former (40%; 95% CI, 12–74% versus 27%; 95% CI, 13–46%), and this was because several patients with localized cutaneous lymphoma underwent FDG-PET scans after their lymphoma progressed to the larger areas. Concerning extracutaneous lesions, the positive rate was equally high in both groups (Table 2, right columns).

The present study demonstrated the very limited role, if any, of FDG-PET to detect BM involvement of T/NK-cell neoplasms. To date, several studies have examined the role of FDG-PET in assessing BM involvement of lymphoma, with inconsistent results. Pakos et al. demonstrated, with a meta-analysis, that only half of BM lesions detected by biopsy were detected by FDG-PET [26], and this result was compatible with our data as to T/NK-cell neoplasms. In the present study, one patient was diagnosed as having FDG uptake in BM in spite of the absence of pathological evidence of BM involvement. The second biopsy directed at the site of focal uptake might reveal BM involvement as shown in several reports [26, 27]. However, FDG uptake in BM in this case might reflect hemophagocytosis, which was occasionally seen with several T/NK-cell neoplasms such as ENKL. Thus, more caution is needed when assessing BM involvement by FDG-PET in T/NK-cell neoplasms.

In conclusion, our study showed that T/NK-cell neoplasms were generally FDG-avid as B-cell neoplasms. Although a careful interpretation should be carried out for each patient, this result could support further evaluation of clinical significance of FDG-PET in T/NK-cell neoplasms. However, the ability of FDG-PET to detect cutaneous lesions, except for tumorous ones, and BM involvement may not be reliable.

Received for publication February 13, 2007. Revision received April 21, 2007. Accepted for publication April 27, 2007.


   References
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
 References
 
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