World J Urol DOI 10.1007/s00345-013-1189-x

ORIGINAL ARTICLE

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F-fluorocholine PET/CT compared with extended pelvic lymph node dissection in high-risk prostate cancer

H. Kjo¨lhede • G. Ahlgren • H. Almquist • F. Liedberg • K. Lyttkens • T. Ohlsson • O. Bratt

Received: 15 May 2013 / Accepted: 9 October 2013 Ó Springer-Verlag Berlin Heidelberg 2013

Abstract Purpose To compare 18F-fluorocholine positron-emission tomography/computed tomography (PET/CT) with extended pelvic lymph node dissection (ePLND) for the detection of lymph node metastases in a large cohort of patients with high-risk prostate cancer. Materials and methods Patients with prostate-specific antigen levels between 20 and 99 ng/mL and/or Gleason score 8–10 cancers, planned for treatment with curative intent following a negative or inconclusive standard bone scan, were investigated with 18F-fluorocholine PET/CT followed by an ePLND. None of the patients received hormonal therapy prior to these staging procedures. Results for PET/CT were compared on a per-patient basis with

Electronic supplementary material The online version of this article (doi:10.1007/s00345-013-1189-x) contains supplementary material, which is available to authorized users. H. Kjo¨lhede (&) Section of Urology, Department of Surgery, Va¨xjo¨ Hospital, Lund University, SE-351 85 Va¨xjo¨, Sweden e-mail: [email protected] G. Ahlgren  F. Liedberg Department of Urology, Ska˚ne University Hospital, Lund University, Lund, Sweden H. Almquist  K. Lyttkens Center for Medical Imaging and Physiology, Ska˚ne University Hospital, Lund University, Lund, Sweden T. Ohlsson Radiation Physics, Ska˚ne University Hospital, Lund University, Lund, Sweden O. Bratt Department of Urology, Helsingborg Hospital, Lund University, Lund, Sweden

histopathology from ePLND. Sensitivity, specificity, positive and negative predictive values were calculated. Results PET/CT detected a total of 76 suspected lymph node metastases and four suspected bone metastases in 33 (29 %) of the 112 included patients. Of these, 35 suspected lymph node metastases, only within the anatomical template area of an ePLND, were found in 21 of the patients. Histopathology of the ePLND specimens detected 117 lymph node metastases in 48 (43 %) of the 112 patients. Per-patient sensitivity, specificity, positive and negative predictive values for 18F-fluorocholine PET/CT for lymph node metastases within the ePLND template were 0.33, 0.92, 0.76 and 0.65, respectively. Only 11 patients had lymph nodes larger than 10 mm that would have been reported by CT alone. Conclusions 18F-fluorocholine PET/CT detects lymph node metastases in a significant proportion of patients with high-risk prostate cancer with a high specificity, but low sensitivity. Keywords Prostate cancer  PET and CT  Lymphatic metastasis

Introduction The presence of lymph node metastases is an important prognostic factor for prostate cancer. The standard of reference for determining lymph node metastases is an extended pelvic lymph node dissection (ePLND) [1, 2]. Noninvasive methods such as computed tomography and magnetic resonance imaging (MRI) have been studied, but have poor sensitivity and specificity, relying only on morphology and size [3]. Newer promising methods are MRI with lymphotropic contrast, diffusion-weighted MRI,

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SPECT-CT and positron-emission tomography/computed tomography (PET/CT) with radio-labeled choline, but these have not yet been evaluated thoroughly [4–9]. The published studies on choline PET/CT for lymph node staging have included heterogeneous study populations [10–14]. We previously reported that choline PET/CT indicated metastatic disease in 39 % of patients with highrisk prostate cancer without clear evidence for metastases on a standard bone scan [15]. The metastases were so widespread that the planned curative treatment was abandoned for one-fifth of the patients. All imaging methods yield both false-positive and falsenegative results. In our previous study, the PET/CT findings were not verified histopathologically. The aim of this study was to determine the sensitivity and specificity in detection of lymph node metastases by 18F-fluorocholine PET/CT compared with histopathology from ePLND, in patients with high-risk prostate cancer.

Materials and methods Patients The study protocol was accepted by the research ethical review board at the University of Lund (EPN LU552/ 2007). According to the protocol, urologists in the southern health care region of Sweden were invited to refer patients with biopsy-verified high-risk prostate cancer, eligible for curative treatment after a normal or inconclusive planar 99m Tc-MDP bone scan, for an 18F-fluorocholine PET/CT scan. Diagnostic prostatic biopsies had been performed with 8–12 cores, according to the regional guidelines. High-risk prostate cancer was defined as a prostate-specific antigen (PSA) C20 ng/mL and/or Gleason score 8–10. Patients receiving hormonal therapy before PET/CT or ePLND and patients with PSA [100 ng/mL were excluded from the study. An ePLND, as described by Heidenreich et al. [2], was performed at one of five centers (Halmstad, Helsingborg, Lund, Malmo¨ and Va¨xjo¨), for all patients except those whose PET/CT scans showed extensive metastatic spread. The anatomical extent of the ePLND was defined laterally by the lateral border of the external iliac arteries, medially by the internal iliac arteries and the bladder and cranially by the ureteral crossing of the common iliac arteries, including all the tissues in the obturator fossae. No lymph nodes were dissected outside this standard template, regardless of PET/CT findings. Patients with extensive metastatic spread were not subjected to PLND and therefore not included in the study. Histopathological examination was done at each center according to local routines.

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Imaging protocol 18

F-fluorocholine was synthesized on the TracerLab MXFDG module (GE Healthcare) using the method described by Kryza et al. [16]. A minor modification of the method was performed, producing 18F-fluorobromomethane with the assistance of tetrabutylammonium hydroxide instead of Kryptofix 2.2.2. PET/CT studies were acquired with an integrated PET/ CT system (Philips Gemini TF, Philips Medical Systems, Cleveland, OH, USA) at the Center for Medical Imaging and Physiology, Ska˚ne University Hospital in Lund. Patients were fasting for 4 h before 18F-fluorocholine injection. Whole-body PET (pelvis to neck) was acquired 1–1.5 h after intravenous injection of 4 MBq/kg (max dose 400 MBq) of 18F-fluorocholine with 2 min per bed position. A diagnostic quality CT scan was performed immediately prior to the PET scan with a multidetector spiral CT scanner, with 5 mm reconstructed slice thickness. Sixty minutes before the scan, 1,000 ml oral contrast (Omnipaque, GE Healthcare, Stockholm; Sweden) was given. Three CT scans were obtained. The liver was scanned without intravenous contrast, and then, the thorax was scanned in the arterial phase—both scans during breathhold. The third scan covered the body from the base of the skull to the proximal thigh and was obtained in the portal phase during normal breathing. The PET/CT scans were initially interpreted by at least one nuclear medicine physician and one radiologist. All clinical decisions were based on these primary interpretations. The PET/CT scans were for the purpose of this study reevaluated later by two PET/CT experts, one nuclear medicine physician and one radiologist, who were both blinded to the results of the lymph node dissection and the clinical decisions. Only these reevaluations were used for analysis in this study. Focal 18F-fluorocholine uptake above the background corresponding to a lymph node in the pelvis or para-aorta was reported as positive. A high uptake overruled the lymph node size in this interpretation. Locations were categorized as (1) within the template of an ePLND, (2) within the pelvis up to the level of the aortic bifurcation but outside the ePLND template, (3) within the abdomen above the aortic bifurcation and (4) skeletal sites. Data collection and statistical analysis Clinical stage, PSA levels and Gleason score at the time of referral for PET/CT, and pathology reports from lymph node dissection were confirmed retrospectively from the medical records. Sensitivity, specificity, positive predictive values and negative predictive values were calculated with

World J Urol

95 % confidence intervals, using the VassarStats online calculator.

total of 54 pathology-verified lymph node metastases. The median number of lymph nodes removed by ePLND was 15 (range 6–45) for the 26 patients with false-negative PET/CT.

Results Findings within the template for an ePLND Overall findings From February 2008 to November 2011, 174 patients that met the inclusion criteria performed an 18F-fluorocholine PET/CT. After exclusions, 112 patients from ten referral centers remained for analysis (Fig. 1). Baseline data for these patients are presented in Table 1. PET/CT detected 80 suspected metastases in 33 (29 %) of the 112 patients, 76 in lymph nodes and four in the skeleton (Online Resource 1). Of the suspected lymph node metastases, 35 (46 %) were detected within the ePLND template area, 37 (49 %) within the pelvis but outside the ePLND area and four (5 %) in the abdomen cranial to the aortic bifurcation. For 22 of the 33 (67 %) patients with positive PET/CT findings, the positive lymph nodes were \10 mm and would not have been reported by CT alone. Of the 112 patients who underwent a lymph node dissection, 48 (43 %) had a total of 117 lymph node metastases, including micrometastases, verified by histopathology. These operations were performed at median 41 (range 3–130) days after PET/CT, for 29 patients at the same time as a radical prostatectomy and for 83 patients before external beam radiation. Of the 33 patients with any positive PET/CT finding, 22 (67 %) had a total of 63 lymph node metastases verified by histopathology, and one (3 %) had a solitary bone metastasis verified with MRI. Of the 79 patients with normal PET/CT scans, 53 (67 %) had no metastases detected by ePLND and 26 (33 %) had a

174 patients who performed a choline PET/CT

26 patients excluded due to extensive metastatic findings on PET/CT 4 patients with positive PET/CT did not perform an ePLND due to intercurrent disease or non-prostate related death

32 patients with negative PET/CT did not perform an ePLND due to intercurrent disease or non-prostate related death 112 patients who performed an ePLND available for analysis

Fig. 1 Exclusion diagram

For 21 of the 112 patients, the PET/CT scan indicated a total of 35 lymph node metastases within the ePLND template. The ePLND revealed a total of 57 metastases, including micrometastases, in 16 of these 21 patients. Sensitivity and specificity for per-patient and per-side analyses were within the confidence intervals (Table 2). The median number of removed lymph nodes from the patients with verified metastases was 10.5 (range 3–32). Seven of these 16 patients had additional findings on PET/ CT outside the template area. Findings within the pelvis, but outside the ePLND template For 17 of the 112 patients, the PET/CT scan indicated a total of 37 lymph node metastases within the pelvis, but outside the ePLND area. Eight of the 17 patients also had findings within the template area, and five of these eight patients had pathology-verified metastases. Nine patients with normal PET/CT findings within the ePLND template had a total of 11 suspected lymph node metastases in the rest of the pelvis. Five of them had a total of five metastases verified by histopathology. Findings outside the pelvis The PET/CT scan indicated a total of eight metastases outside the pelvis in seven patients. Three of the patients had findings in lymph nodes in the upper abdomen, and four patients had suspected skeletal metastases. One patient had positive PET/CT findings in two abdominal lymph nodes only, but had a negative ePLND with nine removed lymph nodes. Two patients had positive PET/CT findings in a skeletal site only. One of them had a positive ePLND with six removed lymph nodes, and the other had a negative ePLND with six removed nodes. For the latter patient, an MRI was performed that confirmed the bone metastasis.

Discussion The main objective of our study was to compare the findings of 18F-fluorocholine PET/CT with histopathology from ePLND. We therefore based the calculations of sensitivity, specificity, NPV and PPV on the PET/CT findings

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World J Urol Table 1 Characteristics of the patients All patients n = 112

Negative PET/CT n = 79

Positive PET/CT n = 33

Negative ePLND n = 64

Positive ePLND n = 48

65.6 (±6.2)

65.1 (±6.2)

66.9 (±6.1)

65.8 (±5.9)

65.4 (±6.6)

25 (2.4–95)

28.5 (3.9–91)

22.0 (2.4–95)

25.0 (3.9–91)

28.5 (2.4–95)

5–6

7 (6)

7 (9)

0 (0)

6 (9)

1 (2)

7 8–10

41 (37) 64 (57)

32 (41) 40 (51)

9 (27) 24 (73)

27 (42) 31 (48)

14 (29) 33 (69)

Age (year) Mean (±SD) PSA (ng/mL) Median (range) Biopsy Gleason score

Local clinical tumor stage T1c

23 (21)

18 (23)

5 (15)

15 (23)

8 (17)

T2

35 (31)

26 (33)

9 (27)

25 (39)

10 (21)

24 (38)

30 (62)a

a

35 (44)

Negative

102 (91)

73 (92)

29 (88)

58 (91)

44 (92)

Inconclusive

10 (9)

6 (8)

4 (12)

6 (9)

4 (8)

12.0 (3–47)

13.0 (3–47)

10.0 (3–39)

12.0 (3–47)

13.5 (3–45)

41.0 (3–130)

39.5 (7–130)

42.0 (3–113)

48.0 (3–130)

35.0 (7–112)

T3

54 (48)

19 (58)

a

99m

Tc-MDP bone scan

Lymph nodes dissected (no) Median (range) Time to ePLND (days) Median (range)

Pathological tumor stage (no) pT2

9 (31)

8 (33)

1 (20)

7 (47)

2 (14)

pT3

20 (69)

16 (67)

4 (80)

8 (53)

12 (86)

Values as numbers and percentages in brackets for Gleason score, tumor stages and bone scans. Pathological tumor stage presented for 29 patients who underwent prostatectomy PET/CT positron-emission tomography/computed tomography, ePLND extended pelvic lymph node dissection, PSA prostate-specific antigen a

Including one patient who after PET/CT and PLND was restaged as T4

within the anatomical template of an ePLND, both perpatient and per-side. In our study, per-patient analysis showed that 18F-fluorocholine PET/CT had a high specificity (0.92), but a low sensitivity (0.33). The PPV was 76 % and the NPV 65 %. Per-side analysis showed similar results for sensitivity and specificity (0.31 and 0.94). The present study thus suggests that choline PET/CT cannot predict the presence or absence of lymph node metastases with clinically acceptable accuracy, at least in the absence of extensive metastatic spread. A possible cause for this is the very low detection rate of metastases \5 mm of PET/CT [10]. Choline PET/CT can show positive findings also in benign pathological conditions, such as inflammation, which we also found to be the case [17]. Even in this study population with high-risk cancers and a 42 % prevalence of pathology-verified lymph node metastases, there were five of 21 (24 %) patients with false-positive findings on PET/CT. If choline PET/CT were applied in populations with lower risk of metastases, the proportion of false-positive findings would be even higher.

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Therefore, PET/CT with limited positive findings should not preclude treatment with curative intent, but could possibly indicate the need for adjuvant treatment or extended radiation fields. This needs further study. Our study supports previous observations that the primary route of dissemination of prostate cancer is common not only outside the obturator fossa, but also beyond all the iliac lymph nodes [18]. Meijer et al. [19] reported MRIdetected lymph node metastases outside the ePLND template area in 37 (79 %) of 47 patients with biochemical recurrence after radical prostatectomy with ePLND. According to a study by Mattei et al. [20], as many as onethird of sentinel nodes are located outside the standard anatomical template of an ePLND. The wide anatomical field for lymph node metastases makes ePLND a poor reference test for the assessment of the overall clinical value of PET/CT. Both methods have their strengths and weaknesses, and they could be of complementary clinical value. PET/CT may detect metastases outside the standard ePLND template, and ePLND may detect metastases in

World J Urol Table 2 Per-patient analysis (A) and per-side analysis (B) of 18 F-fluorocholine PET/CT in detecting lymph node metastases PET/CT ?

-

(A) Per-patient analysisa ePLND

? -

16 (16)

32 (27)

5 (5)

60 (65)

18 (18)

41 (36)

9 (9)

150 (155)

(B) Per-side analysisb ePLND

? -

a

Sensitivity was 0.33 (0.21–0.49), specificity was 0.92 (0.82–0.97), positive predictive value was 0.76 (0.52–0.91), and negative predictive value was 0.65 (0.54–0.75) with 95 % confidence intervals in brackets. Results when discounting micrometastases (metastases \2 mm) are shown in brackets. Sensitivity was then 0.37 (0.23–0.53), specificity was 0.93 (0.83–0.97), positive predictive value was 0.76 (0.52–0.91), and negative predictive value was 0.71 (0.60–0.79)

versus 110 min for 18F, is inconvenient and restricts the number of centers using 11C-choline PET/CT. Choline PET/CT has also been evaluated in patients with biochemical relapse after prostatectomy, but with mixed results [23]. The strengths of our study include the homogeneity of the patient population. All had high-risk prostate cancer with PSA \100 ng/mL and no definitive evidence of metastases on bone scan. To our knowledge, no previous study including so many patients with high-risk prostate cancer has been published on this subject. The main limitations of this study are the lack of histopathological data in the 26 patients with extensive metastatic spread and the large proportion of patients that did not have an ePLND due to other factors. The difficulty in exactly defining the template of an ePLND when assessing a PET/CT examination is another limitation of the study.

b

For 109 patients, per-side information was available from pathology reports, giving 218 individual sides to compare. Sensitivity was 0.31 (0.20–0.44), specificity was 0.94 (0.89–0.97), positive predictive value was 0.67 (0.46–0.83), and negative predictive value was 0.79 (0.72–0.84) with 95 % confidence intervals in brackets. Results discounting micrometastases are shown in brackets. Sensitivity was then 0.33 (0.21–0.48), specificity was 0.95 (0.90–0.97), positive predictive value was 0.67 (0.46–0.83), and negative predictive value was 0.81 (0.75–0.86)

patients with normal PET/CT findings, as well as dismiss false-positive findings on PET/CT. Using intraoperative sentinel node detection may further increase the accuracy of the staging [21]. Despite the rather poor performance of PET/CT compared with ePLND in our study, we believe that choline PET/CT may be of clinical value as a staging procedure for patients with high-risk prostate cancer. Certainly, it adds more information than the use of CT alone, which in our study would only have detected suspected lymph node metastases in 11 patients. Our results are in accordance with those of Beheshti et al. [10] who reported sensitivity, specificity, PPV and NPV of 18F-labeled choline PET/CT for 111 patients with intermediate- or high-risk prostate cancer: 45, 96, 82 and 83 %, respectively. The prevalence of metastases was lower (31 %) in their study, as expected with the inclusion of intermediate-risk cancers, which explains their higher NPV. De Jong et al. [11] reported similar results with 11Clabeled choline, but the cancers of the patients in their study were very heterogeneous, and the results are difficult to generalize. No study has yet compared the difference in performance between 18F-labeled choline and 11C-labeled choline, but a meta-analysis suggested that studies with 11 C-choline demonstrate a higher sensitivity than studies with 18F-choline [22]. The much shorter half-life of 11C, 20

Conclusions We compared the findings of 18F-fluorocholine PET/CT with the histopathology from ePLND for patients with high-risk prostate cancer. The PPV was 76 % and the NPV 65 % for PET/CT findings within the anatomical template of the ePLND. PET/CT cannot be used to rule out the presence of lymph node metastases, and signs of limited spread should not preclude attempted curative treatment. On the other hand, 18F-fluorocholine PET/CT may detect metastases outside the template of an ePLND, even in patients with no metastases within the template area. Acknowledgments Grants for this study were received from Cancerstiftelsen i Kronoberg, The Swedish Cancer Society, FoU Kronoberg and Region Ska˚nes FoU-enhet. Conflict of interest The authors declare that they have no conflicts of interest.

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CT compared with extended pelvic lymph node dissection in high-risk prostate cancer.

To compare (18)F-fluorocholine positron-emission tomography/computed tomography (PET/CT) with extended pelvic lymph node dissection (ePLND) for the de...
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