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ORIGINAL ARTICLE
Year : 2012  |  Volume : 8  |  Issue : 1  |  Page : 96-102

Correlation of fluorodeoxyglucose uptake and tumor-proliferating antigen Ki-67 in lymphomas


1 Department of Radiology, Changhai Hospital, the Second Military Medical University, Shanghai 200433; PET-CT Center, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200127, China
2 Department of Radiology, Changhai Hospital, the Second Military Medical University, Shanghai 200433, China
3 PET-CT Center, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200127, China

Date of Web Publication19-Apr-2012

Correspondence Address:
Jianping Lu
Department of Radiology, Changhai Hospital, the Second Military Medical University, No. 800 Xiang yin Road, Shanghai 200433
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.95182

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 > Abstract 

Objective: To investigate the correlation between cellular proliferation and the fluorodeoxyglucose (FDG) uptake in positron emission tomography/computed tomography (PET/CT) imaging by comparing 50 cases of different subtypes of lymphoma.
Materials and Methods: Fifty cases of lymphomas were collected. Each case was labeled with Ki-67 stain, a marker of cellular proliferation, and a PET/CT examination was performed. All lymphoma cases were sorted according to the World Health Organization's classification, and the International Non-Hodgkin's Lymphoma Working Formulation was used to differentiate groups of large and small cell non-Hodgkin's lymphoma. The Ki-67 staining was described as slight, mild, middle, or strong according to the nuclear staining of positive cells. FDG uptake by lesions in PET/CT images was semi-quantitatively analyzed to calculate the average standard uptake value. The statistics software SPSS13.0 was used to calculate the mean and standard deviation of the FDG uptake value of the lymphoma subtypes, the difference between the large and small cell lymphoma group with a Student's t-test, and the correlation between the Ki-67 level and FDG uptake of lesion with a Spearman's analysis.
Results: The FDG uptake value of large cell origin lymphoma was significantly higher than that of small cell origin lymphoma (t = 6.19, P < 0.01). The correlation coefficients between the Ki-67 level and FDG uptake value in lymph nodal and extranodal lesions was 0.750 and 0.843, respectively.
Conclusions: Ki-67 staining, a reflection of tumor-proliferation activity, was significantly related to the FDG uptake value in lymphoma lesions.

Keywords: Fluorodeoxyglucose, Ki-67, lymphoma, positron emission tomography/computed tomography


How to cite this article:
Shou Y, Lu J, Chen T, Ma D, Tong L. Correlation of fluorodeoxyglucose uptake and tumor-proliferating antigen Ki-67 in lymphomas. J Can Res Ther 2012;8:96-102

How to cite this URL:
Shou Y, Lu J, Chen T, Ma D, Tong L. Correlation of fluorodeoxyglucose uptake and tumor-proliferating antigen Ki-67 in lymphomas. J Can Res Ther [serial online] 2012 [cited 2020 Jul 9];8:96-102. Available from: http://www.cancerjournal.net/text.asp?2012/8/1/96/95182


 > Introduction Top


Lymphoma is a cancer of many subtypes all of which originate from lymph nodes or extralymphatic tissues. The lymphoma types present in various forms and their pathologic classification is complex. Due to its higher sensitivity and specificity, the most effective imaging technique to diagnose lymphoma is positron emission tomography/computed tomography (PET/CT). However, most studies that report the use of PET/CT for the diagnosis of lymphoma are limited in their discussion to tumor staging, evaluation of therapeutic outcomes and surveillance of recurrences. Although the usefulness of PET/CT across different histological subtypes has been extensively discussed over the last decade, the reasons for differences in 18 F-fluorodeoxyglucose ( 18 F-FDG) uptake in various subtypes of lymphoma are still debated. This article reports 50 cases of lymphoma that underwent PET/CT imaging in combination with complete pathologic and immunohistochemical results. The causes for differences in 18 F-FDG uptake amongst lymphoma types was explored by comparing the expression of Ki-67 (an immunoenzyme-labeled tumor-proliferating antigen) and fluorodeoxyglucose (FDG) uptake of lymphoma lesions, and find the correlation between them.


 > Materials and Methods Top


Case selection

Fifty patients with lymphoma who were admitted between October 2003 and October 2009 were included in this study. The diagnosis was confirmed by pathology and the results of immunoenzyme staining utilizing the proliferating tumor cell marker Ki-67 antigen. The patients underwent routine 18 F-FDG PET/CT scan before or after the pathologic diagnosis. Patients who received radiotherapy or chemotherapy within one month prior to the PET/CT scan were excluded from the study.

Pathologic classification and unification of the results of Ki-67

Pathologic classification was in accordance with that of the World Health Organization (WHO) for lymphomas [1] and the International Non-Hodgkin's Lymphoma Working Formulation [2] for differentiating between large cell lymphoma (LCL) and small cell lymphoma (SCL). The results of Ki-67 enzyme-labeled immunohistochemistry were rated according to the degree of positive nuclear staining for the antigen. Very weak (+/−), weak (+), middle (++) and strong (+++) positive scores were given when 0-5%, 6-20%, 21-50%, and >50% of cells' nuclei showed antigen staining, respectively. Each surgical or biopsy specimen was sampled at 3-5 different sites, proliferating indices were obtained and the mean Ki-67 index was calculated to reflect the overall proliferation level of the entire specimen.

PET/CT images

PET/CT images were collected on an 8-slice GE Discovery LS PET/CT scanner (BGO crystal, GE, USA). 18 F-FDG was injected with a radiochemistry purity of >95%. The patients fasted for ≥6 hours before the examination. After the injection of 0.15 mCi/kg 18 F-FDG, the patients rested for 45 to 60 minutes before the whole body PET/CT scan. The following scan parameters were used: body CT voltage 120 kV, current 140 mA, pitch 5.0 mm, tube rotation time 0.8 s, and thickness 5.0 mm. Images were collected in 2D mode, 15 minutes for each bed position for a mean of 5 to 7 positions. The PET images were calibrated for attenuation correction. Image reconstruction was done by ordered-subsets expectation maximization, with 2 iterations, 8 iteration subsets, and 4.25 mm thickness. Analysis was focused on cross section. Image fusion was performed on a Xeleris work station.

PET/CT imaging diagnosis

The PET/CT images were analyzed semi-quantitatively by two PET/CT radiologists on a Xeleris work station. In cases of high FDG uptake, the maximum FDG uptake image was used for analysis, where the FDG condensed area was drawn manually along the edge of the lesion. In cases of low or no FDG uptake, the areas were drawn roughly according to the location of the lesion. In all cases the mean standardized uptake value (SUV ave ) was calculated automatically by software. All lesions were classified as either nodular or extra-nodular. To eliminate the influence of volume effects on FDG uptake, the diameter of all selected pathologic lymph nodes was greater than 1 cm. For extra-nodular lesions, the SUV ave value was outlined according to lesion and calculated the same way as for lymph nodes. The PET/CT radiologists were blinded to the pathologic and immunohistochemical results before their diagnosis.

Statistical analysis

Data were analyzed with Statistical Package for the Social Sciences (SPSS) 13.0 software. Common lymphoma subtypes, including diffuse large B-cell lymphoma (DLBCL), follicular lymphoma (FL), small lymphocytic lymphoma (SLL), mucosa-associated lymphoid tissue (MALT), B-cell lymphoma, peripheral T-cell lymphoma, unspecified peripheral T-cell lymphoma (PTCL-U), plasmacyte lymphoma and Hodgkin's lymphoma (HL) were used to statistically calculate FDG uptake value. All data are expressed as mean ± SD. The difference between SCL and LCL non-Hodgkin's lymphoma (NHL) was analyzed statistically using a Student's t-test of independent samples. The correlation between FDG uptake and Ki-67 was analyzed using Spearman's method to calculate the rank correlation coefficient, r. A probability value P < 0.05 was considered statistically significant.


 > Results Top


Of the 50 patients (38 men and 12 women; mean age 43 years), 47 were diagnosed with NHL and 3 with HL. Of the 47 cases of NHL, 36 were B-cell lymphoma including 14 cases of DLBCL, 8 cases of FL, 3 cases of SLL, 6 cases of MALT, 2 cases of mantle-cell lymphoma (MCL), one case of nodal marginal zone lymphoma (NMZL), one case of B-cell lymphoblastic lymphoma (B-LBL), one case of non-defined subtype B-cell lymphoma. Eight cases were T-cell lymphoma including 3 cases of PTCL-U, one case of nasal killer (NK)/T-cell lymphoma, one case of anaplastic large cell lymphoma (ALCL), one case of angioimmunoblastic T-cell lymphoma (AITCL), one case of T-cell LBL (T-LBL), and one case of non-defined subtype T-cell lymphoma. Three cases were plasmacytoma including 2 cases of solitary bone plasmacytoma and one case of multiple myeloma. Of the 3 cases of HL, 2 cases were of mixed cellularity (MC), and one case was a nodular sclerosis (NS). Ki-67 staining and FDG uptake values on PET/CT images, of the 50 lymphomas subtypes are shown in [Table 1].
Table 1: Ki-67 immunoenzyme staining and FDG uptake value on PET/CT imaging of the 50 cases of lymphoma

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Statistical results

  1. The mean and standard deviation values for FDG uptake of the common lymphoma subtypes were as follows: 7.9 ± 2.9 for DLBCL; 3.9 ± 1.2 for FL; 3.8 ± 0.7 for SLL; 2.5 ± 0.5 for MALT; 5.3 ± 1.4 for PTCL-U; 2.8 ± 0.1 for plasmacytoma; and 4.6 ± 0.5 for HL.
  2. Of the 47 cases of NHL, FDG uptake of LCL (including DLBCL, T-cell NHL and LBL) was 7.0 ± 2.8 and that of SCL (including FL, SLL, MALT, MCL, NMZL and plasmacytoma) was 3.3 ± 1.0; the difference was statistically significant (t = 6.19, P < 0.01). Furthermore, with T-cell NHL, LBL and plasmacytoma cases excluded, the SUV ave of DLBCL from large B-cell origin was 7.7 ± 2.9, and that of FL, SLL, MALT, MCL and NMZL from small B-cell origin was 3.4 ± 1.0; the difference was statistically significant (t = 6.57, P < 0.01).
  3. There was a positive correlation between FDG uptake and Ki-67 in both nodular lesions (r = 0.750, P < 0.01) and extra-nodular lesions (r = 0.843, P < 0.01). The correlation between the FDG uptake of lymphoma lesion and Ki-67 are shown in [Figure 1] and [Figure 2], respectively. Additionally, some cases of subtypes of lymphomas with PET/CT images and its corresponding Ki-67 staining were illustrated in [Figure 3], [Figure 4], [Figure 5] and [Figure 6].
  4. Figure 1: Correlation of Ki-67 expression and standardized uptake value (SUV) of FDG. Expression of Ki-67 correlates positively with FDG uptake value of nodular lesions. The correlation coefficient r is 0.750

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    Figure 2: Correlation of Ki-67 expression and standardized uptake value (SUV) of FDG in extra-nodular lesions. Expression of Ki-67 correlates positively with FDG uptake value of extra-nodular lesions. The correlation coefficient r is 0.843

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    Figure 3: A 57-year-old woman was diagnosed as DLBCL by endoscopic biopsy. The PET/CT was performed and showed thickening of the stomach wall. Where FDG uptake was abnormally elevated, SUVAVE was 14.5. The Ki-67 staining of specimen was strong positive (+++)

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    Figure 4: A 42-year-old man who had a fever for three months was admitted to hospital. Multiple enlarged regional lymph nodes and splenomegaly were revealed on 18FDG-PET/CT. Axillary lymph node was biopsied and SLL was diagnosed by pathological and Ki-67 staining showed weak positive (+)

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    Figure 5: A 58-year-old man had a long history of persistent abdominal pain and was diagnosed as MALT by surgical pathology. Before surgery, a PET/CT scan was performed and showed extensive mesenteric thickening and intestinal adhesion with slight FDG uptake, where SUVSUV was 2.3. The corresponding Ki-67 staining was very weak positive (+/-) in this case

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    Figure 6: A 57-year-old man who complained of right leg pain. PET/CT showed a region of bone defect on the right upper femur with unclear edge and swelling of surrounding tissue. The lesion revealed slight FDG uptake with a SUVAVE of 2.8. Thereafter, bone lesion was biopsied and plasmacytoma was confi rmed according to pathology. Ki-67 was very weak positive (+/-) in immunochemistry staining

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 > Discussion Top


PET/CT is a relatively new technique for tumor imaging, highly sensitive and specific to lymphoma. It is able to display the extent of lymphoma involvement before presentation by other imaging techniques. [3] Causes for different FDG uptakes in different tumors remain a major confounding problem. Some researchers believe that differences in FDG uptakes are a reflection of the proliferating activities of the tumors. Minn et al. [4] and Higashi et al. [5] found that there was a correlation between cell proliferating activities and FDG uptake in head and neck tumors and non-small cell lung cancer. However, Buck et al. [6] did not find a significant correlation between Ki-67 staining and FDG uptake in pancreatic cancer and pancreatitis cases. Brown et al. [7] pointed out that FDG uptake in different tumors was related to glucose transporters (GLUT), especially GLUT-1. Other researchers believed that it was related to hexokinase activity. [8]

We found in our study that Ki-67 expression was positively correlated with FDG uptake, especially in different subtypes of B-cell lymphoma. FDG uptake was relatively low in tumors of low proliferation, mostly in FL, SLL, MALT, and plasmacyte tumors where karyokinesis was predominantly rare and cell metabolism was at a low level. In contrast, FDG uptake was significantly increased in tumors of high proliferation, mostly in DLBCL, T-cell lymphoma, and lymphoblast lymphoma where karyokinesis was evident and cell metabolism was at a relatively high level. [9],[10] In general, tumor-proliferating activity, hexokinase level, GLUT level and tumor cell density may all affect FDG uptake. However, it is difficult to determine which particular factor plays a critical role in FDG uptake of different tumor types if the influences of other factors are not controlled. Lymphoma is a kind of B- or T-cell monoclonal tumor. [11] It originates from the same cell but presents different proliferating activities. It is therefore easier to exclude the influences of other factors on FDG uptake and display the relationship between proliferating activity and FDG uptake. The results thus obtained are more accurate.

Compared with normal tissues, tumor cells are highly proliferative, and therefore cell division is more rapid, cell metabolism is vigorous, and the need for substrate adenosine for cell division is increased. Glycolysis is the main pathway of producing adenosine, and therefore the glycolytic process of tumor cells increases markedly, and the uptake of substrate glucose or FDG is elevated accordingly. [12] It is therefore understandable that higher Ki-67 levels correlate with higher FDG uptake. Greater proliferating activity of a tumor is the underlying cause for increased FDG uptake, while increases in GLUT and hexokinase may be secondary.

LCL refers to lymphoma with relatively large cells. According to the WHO and Working Formulation classification, large cells refer to large B-cells (including central blasts, immune blasts, and anaplastic large cells), blasts (B- or T-blasts), and moderately large T-cells. These cells also have rich cytoplasm, large nuclei, loose chromatin, and moderate or large nucleoli with greater rate of cell division. In tumors with predominately large cells such as DLBCL, FL-III, and ALCL, Ki-67 staining is mostly positive (++) or strongly positive (+++). [1],[2] Lesions in LCL are often found to be highly condensed on FDG-PET.

In contrast, SCL refers to small B cells, central cells, mononuclear cells, mantle cells, and plasma cells. These cells are small, with small amounts of cytoplasm, small global nuclei, dense or cartwheel nuclei, small and unclear nucleoli, and rarely in the mitotic phase. In tumors with predominately small cells such as FL-I and II, SLL, MZL, and MCL, Ki-67 staining is mostly very weakly positive (+/−) or weakly positive (+). [1],[2] Lesions in SCL often appear mildly condensed on FDG-PET. This study also confirmed that there is an important correlation between tumor-proliferating activity, as reflected by Ki-67 staining, and FDG uptake in lymphoma lesions. [13]

The size of lymphoma cells should be considered a critical factor distinguishing aggressive from indolent groups clinically. Lymphomas with prominent large cells possess significantly stronger proliferative ability than small cell lymphomas. Follicular lymphoma was classified as an indolent subtype according to the WHO and Working Formulation classification, but FL-III, with a greater proportion of large cells (centroblasts) inside the tumor, showed an increased proliferative activity compared to lower-grade FL-I or II, and a more aggressive clinical course. Papajik et al. [14] pointed out that in his study FL as DLBCL, ALCL, LBL and PTCL with high mean and medium SUV max which is obviously different to MCL, MZL, and SLL. Tang et al. [15] studied 23 patients with different grades of FL lymphomas: the BxSUVs (maximum value within a volume of interest over the biopsy region) in 6 cases of grade I, 8 cases of grade II, and 9 cases of grade III were 6.6 ± 4.4, 6.9 ± 3.9, and 9.6 ± 6.3, respectively. In our study, 8 cases of FL were grade I or II, with a relatively lower uptake of FDG (SUV ave : 3.8 ± 0.7). The pathological grade of FL depends on the proportion of central blast cells in the background of small central cells. [16] When the proportion of central blast cells was increased, the lymphoma was graded higher correspondingly. If all small central cells turn into large central blast cells, FL will eventually transform into DLBCL. [16] FL with high FDG uptake in Papajik study was probably due to selected cases of high grade or the emergence of large cell transformation.

Another interesting case is MCL, which is regarded as an aggressive lymphoma with poor prognosis. In our study, 2 cases of MCL presented lower FDG uptakes as SLL, MALT and FL (the SUV ave 's were 3.0 and 3.5). Wong et al. [17] investigated 58 cases of newly diagnosed NHL. The MCL group of 4 cases all exhibited SUV values well below the SUV ave of the aggressive group. In the current case, an ideal interpretation was possible because of the pathologic structure of the mantle cells, which are indolent small cells whose shape and proliferation is similar to other small cells. Indeed the aggressive clinical course of MCL was probably not due to proliferative ability but due to insensitivity to chemotherapy. However, selected case bias could not be excluded from our limited case number, and low FDG uptake of MCL needs further verification by investigating more cases.

Watanabe et al. [18] studied 36 patients with untreated NHL, measured the Ki-67 proliferation indices in biopsy specimens and compared them with the SUV max 's of FDG-PET at the biopsy site. They concluded that there was considerable overlap of SUV max 's between indolent and aggressive lymphomas. Wong et al. [19] studied 102 patients with newly diagnosed NHL and HL who underwent PET and found it difficult to differentiate aggressive and indolent lymphomas using the SUV. A large overlap was observed in this study: SUVs were lower for some aggressive types compared to indolent types, which led to an incorrect discrimination between these two groups. In our study, all subtypes of lymphomas were sorted into LCL or SCL, and the SUV ave 's of the LCL group were significantly higher than that of the SCL; there was relatively little overlap between the groups. The cellular size of lymphoma determines the proliferating activity and the glucose uptake rate. Therefore, the cellular classification (large or small) may be better for correlating with Ki-67, even though it may not be directly correlated with clinical behavior or outcome. This correlation will potentially contribute to better explain the essence of varied FDG uptake in different cellular-constituted lymphomas.

It is still debated whether either SUV ave or SUV max is a valid parameter to measure FDG uptake in lymphomas. Most authors have adopted SUV max to quantify malignant solid tumors. For SUV ave , problems still exist in determining tumors' margins and a scattering effect due to radiotracer activity cannot be excluded. SUV max is a measure of the local maximum uptake value of a single spot in a region of interest. The use of SUV max may lead to a greater bias, while SUV ave reflects the FDG uptake level of the entire lesion involved in the lymphoma. Another reason for choosing SUV ave instead of SUV max is that Ki-67 scores, which were obtained from different sites of one specimen, reflected the overall lesion's proliferating activity. Therefore, the use of SUV ave in association with Ki-67 can be superior to elaborate the correlation between FDG uptake and proliferating activity in lymphomas.

To decide the appropriate chemotherapy regimen, it is most important to know the proliferation potential and to determine the speed of tumor growth by measuring FDG uptake in lymphomas.

Lymphomas in which FDG uptake is intense suggests increased proliferation ability and rapid growth, but they may be sensitive to chemotherapy. Lymphomas with weak FDG uptake imply lower proliferation ability and slow growth, but these may be insensitive to chemotherapy. Thus, the FDG uptake value can be used as a predictor when adopting a chemotherapy regimen. In conclusion, of the various factors that may influence tumor FDG uptake in different subtypes of lymphomas, the proliferation activity of the tumor, as confirmed by Ki-67, may be the most important.

 
 > References Top

1.Jaffe ES, Harris NL, Stein H, Vardiman JW, editors. World Health Organization Classification of tumors: Pathology and Genetics of Tumors of Haematopoietic and Lymphoid Tissues. Lyon: IRAC Press; 2001. p. 125-275.  Back to cited text no. 1
    
2.National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphomas: Summary and description of a working formulation for clinical use. The Non-Hodgkin's Lymphoma Pathologic Classification Project. Cancer 1982;49:2112-35.  Back to cited text no. 2
    
3.Jerusalem G, Hustinx R, Beguin Y, Fillet G. Positron emission tomography imaging for lymphoma. Curr Opin Oncol 2005;17:441-5.  Back to cited text no. 3
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4.Minn H, Joensuu H, Ahonene A, Klemi P. Fluorodeoxyglucose imaging: A method to assess the proliferative activity of human cancer in vivo. Comparison with DNA flow cytometry in head and neck tumors. Cancer 1988;61:1776-81.  Back to cited text no. 4
    
5.Higashi K, Ueda Y, Yagishita M, Arisaka Y, Sakurai A, Oguchi M, et al. FDG PET measurement of the proliferative potential of non-small cell lung cancer. J Nucl Med 2000;41:85-92.  Back to cited text no. 5
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6.Buck AC, Schirrmeister HH, Guhlmann CA, Diederichs CG, Shen C, Buchmann I, et al. Ki-67 immunostaining in pancreatic cancer and chronic active pancreatitis: Does in vivo FDG uptake correlate with proliferative activity? J Nucl Med 2001;42:721-5.  Back to cited text no. 6
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8.Shim HK, Lee WW, Park SY, Kim H, So Y, Kim SE. Expressions of glucose transporter Types 1 and 3 and hexokinase-II in diffuse large B-cell lymphoma and other B-cell non-Hodgkin's lymphomas. Nucl Med Biol 2009;36:191-7.  Back to cited text no. 8
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9.Hoffmann M, Raderer M. Malignant B-cell lymphoma, WHO classification and the respective 18F-fluoro-deoxy-glucose positron emission tomography result. Imaging Decis (Berl) 2007;10:14-21.  Back to cited text no. 9
    
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12.Haberkorn U, Ziegler SI, Oberdorfer F, Trojan H, Haag D, Peschke P, et al. FDG uptake, tumor proliferation and expression of glycolysis associated genes in animal tumor models. Nucl Med Biol 1994;21:827-34.  Back to cited text no. 12
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14.Papajik T, Myslivecek M, Sedova Z, Buriankova E, Prochazka V, Koranda P, et al. Standardised uptake value of 18F-FDG on staging PET/CT in newly diagnosed patients with different subtypes of non-Hodgkin's lymphoma. Eur J Haematol 2011;86:32-7.  Back to cited text no. 14
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1]


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