Cardiovasc Intervent Radiol DOI 10.1007/s00270-016-1334-1
TECHNICAL NOTE
18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases from Neuroendocrine Tumours: Technical Note on a Preliminary Experience Roberto Luigi Cazzato1 • Julien Garnon1 • Nitin Ramamurthy2 • Georgia Tsoumakidou1 • Alessio Imperiale3 • Izzie Jacques Namer3 • Philippe Bachellier4 • Jean Caudrelier1 • Pramod Rao1 • Guillaume Koch1 • Afshin Gangi1
Received: 6 February 2016 / Accepted: 26 March 2016 Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2016
Aim To review our preliminary experience with 6-L-18Ffluorodihydroxyphenylalanine (18F-FDOPA) PET/CTguided radiofrequency ablation (RFA) of liver metastases from neuroendocrine tumours (NETs). Materials and Methods Three patients (mean age 51.3 years; range 43–56) with gastro-entero pancreatic NET (GEP-NET) liver metastases underwent 18F-FDOPA PET/CT-guided RFA. Patients were referred with oligometastatic hepatic-confined disease (1–6 metastases; \3 cm) on 18F-FDOPA PET/CT; poor lesion visualisation on US, CT, and MR; and ongoing symptoms. Procedures were performed in an interventional PET/CT scanner under general anaesthesia using a split-dose protocol. Lesion characteristics, procedural duration and technical success (accurate probe placement and post-procedural ablation-
zone photopaenia), complications, patient and operator dose, and clinical outcomes were evaluated. Results Thirteen liver metastases (mean size 11.4 mm, range 8–16) were treated in three patients (two presented with ‘‘carcinoid syndrome’’). Technical success was 100 % with a mean procedural duration of 173.3 min (range 90–210) and no immediate complications. Mean patient dose was 2844 mGycm (range 2104–3686). Operator and radiographer doses were acceptable other than the operator’s right hand in the first case (149 lSv); this normalised in the second case. There was no local tumour or extra-hepatic disease progression at mid-term follow-up (mean 12.6 months; range 6–20); however, two cases progressed with new liver metastases at different sites. There was 100 % clinical success (n = 2) in resolving carcinoid syndrome symptoms.
& Roberto Luigi Cazzato
[email protected]
Guillaume Koch
[email protected] Afshin Gangi
[email protected]
Julien Garnon
[email protected] Nitin Ramamurthy
[email protected]
1
Georgia Tsoumakidou
[email protected]
Department of Interventional Radiology, Nouvel Hoˆpital Civil (Hoˆpitaux Universitaires de Strasbourg, HUS), 1, place de l’Hoˆpital, 67000 Strasbourg, France
2
Alessio Imperiale
[email protected]
Department of Radiology, Norfolk and Norwich University Hospital, Colney Lane, Norwich NR4 7UY, UK
3
Department of Biophysics and Nuclear Medicine, Hoˆpital de Hautepierre (Hoˆpitaux Universitaires de Strasbourg, HUS), Avenue Molie`re, 67200 Strasbourg, France
4
Hepato-Pancreato-Biliary Surgery and Liver Transplantation, Hoˆpital de Hautepierre (Hoˆpitaux Universitaires de Strasbourg, HUS), Avenue Molie`re, 67200 Strasbourg, France
Izzie Jacques Namer
[email protected] Philippe Bachellier
[email protected] Jean Caudrelier
[email protected] Pramod Rao
[email protected]
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R. L. Cazzato et al.: 18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases…
Conclusion 18F-FDOPA PET/CT-guided RFA appears technically feasible, safe, and effective in patients with GEP-NETs and low-burden hepatic metastases. Further prospective studies are required to elucidate its precise role in tailored multimodality management of GEP-NET liver metastases. Keywords Neuroendocrine tumours Liver metastasis Radiofrequency ablation PET/CT
Introduction Neuroendocrine tumours (NETs) constitute a wide range of relatively indolent neoplasms commonly originating from the gastrointestinal tract or pancreas (i.e. GEPNETs) [1]. Presentation may be sporadic or associated with familial syndromes (e.g. multiple endocrine neoplasia type 1). Up to 18 % of small bowel tumours are symptomatic with abdominal pain, diarrhoea, and cutaneous flushing (‘‘carcinoid syndrome’’), usually secondary to liver metastases [2, 3]. Hepatic disease is present in approximately 30 % at diagnosis, causes significant morbidity and mortality, and represents a vital target for therapy [4]. GEP-NET liver metastases are multiple, small, multisegmental lesions, typically unsuitable for surgical resection. Intra-arterial therapies exploit the arterial hyper-vascularity of GEP-NETs to deliver selective therapy, but are best suited to patients with high tumour burden or uncontrolled symptoms. In patients with hepatic-confined disease (\5–6 lesions, \3–3.5 cm), percutaneous image-guided ablation may be proposed [5, 6]. Technical success depends on high-quality imaging guidance; however, routine imaging modalities are limited by suboptimal contrast, spatial resolution, and transient lesion visualisation on contrast-enhanced studies [7]. 18F-FDOPA PET/CT is a novel imaging technique, which uses 6-L-18F-fluorodihydroxyphenylalanine (18FFDOPA) to detect NET lesions poorly visualised on US, CT, and MR [1, 8, 9]. Similar to FDG-PET/CT, it facilitates good lesion conspicuity throughout long procedures, precise targeting using functional–anatomic images, and post-treatment efficacy assessment [7, 10]. It has been applied to guide NET biopsy and radiofrequency ablation (RFA) in a recent report [11] with good outcomes. The purpose of this study is to review our preliminary experience of 18F-FDOPA PET/CT-guided RFA of hepatic GEP-NET metastases and to discuss technical feasibility, clinical success, radiation dose, and mid-term outcomes of this novel procedure.
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Materials and Methods Study Population This retrospective study was undertaken with Institutional Review Board approval and written informed patient consent. Review of electronic records identified three consecutive patients (two female, one male; mean age 51.3 years; range 43–56) with GEP-NET liver metastases who underwent 18F-FDOPA PET/CT-guided hepatic RFA between June 2013 and October 2015. All patients presented sporadic GEP-NETs; and all of them underwent surgical resection of the primary well-differentiated GEP-NETs, located in the distal small bowel. Two patients (Table 1) were symptomatic with ‘‘carcinoid syndrome’’. All cases were discussed in a multidisciplinary tumour board. Patients were included on the basis of pre-procedural diagnostic 18F-FDOPA PET/CT demonstrating oligometastatic hepatic-confined disease (1–6 liver metastases; diameter \3 cm); poor visualisation of target lesions on US, CT, and MR; and ongoing symptoms despite primary tumour resection and maximal systemic therapy. Patients with 18F-FDOPA PET/CT imaging follow-up \6 months following RFA were excluded. FDOPA PET/CT-Guided RFA All patients were treated in a single session on an in-patient basis, under general anaesthesia and sterile conditions by two senior interventional radiologists with C12 months experience in PET/CT-guided interventions and C6 years experience in percutaneous image-guided ablation. Peri-operative octreotide infusion was administered to avoid carcinoid crisis. Peri-procedural management of coagulation status was in accordance to international guidelines [12]. On the procedure day, patients were fasted for 4 h and pre-medicated with 200 mg Carbidopa 90 min prior to 18F-FDOPA injection to increase its bioavailability. A split-dose protocol was used [10]: the calculated dose of 18F-FDOPA according to patient weight (0.21 mCi/kg) was divided into an initial targeting dose (to guide ablation), and a second treatment efficacy dose (to evaluate technical success). Mean injected activity was 386 MBq (range 276–561), distributed approximately equally between each dose. Following 18F-FDOPA injection, patients were positioned supine in a PET/CT unit (Biograph mCT, Siemens, Erlangen, Germany), Fig. 1. A scout CT scan was acquired from head to pelvis, followed by breath-hold spiral CT scan covering the liver. 3D PET scan was acquired at a single
R. L. Cazzato et al.: 18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases… Table 1 Study population Patients (sex, age)
Liver metastases
Size (mm)
Liver segment
DLP (mGycm)
Procedural time (min)
18FFDOPA activity (MBq/ mCi)
Followup (months)
1 (M, 56)
1
12
VIII
2742
90
561/15.1
20
2
10
V
2 (F, 43)
3
11
VIII
4
16
V
No
5
11
V
No
6
14
IV
No
7
8
III
8
8
IV
9
13
IV
No
10 11
12 9
IV IV
No No
12
10
VI
No
13
14
VI
No
3 (F, 55)
Local tumour progression at last PET/ CT
Hepatic tumour progression
Extrahepatic tumour progression
Clinical success
No
Yes
No
N/A
No
No
Yes
Yes
No
Yes
No 2104
220
321/8.6
12
No
No 3686
210
276/7.4
6
No
N/A not applicable (no clinical symptoms)
bed position covering the same axial range, and datasets were fused to create a PET/CT study. This was used to plan trajectory and facilitate cutaneous marking. RFA probes were advanced under intermittent CT fluoroscopy guidance, available on the same PET/CT machine. Adequate pre-ablation position of the probe was confirmed using a second PET/CT acquisition exploiting the initial 18F-FDOPA targeting dose; no additional needle re-positioning was required. RFAs were performed with a straight or multi-tined probe, to ensure a minimum 1 cm ablation margin. Patient 1 was treated with the 4-cm multi-tined RFA probe (LeVeen CoAccess Needle Electrode System, Boston Scientific, USA); the remainder using a 3-cm active-tip straight RFA probe (Cooltip 3 cm, Covidien, Ireland). Ablations were performed according to manufacturer protocol. Following ablation, the second radiotracer bolus was administered and post-treatment PET/CT acquisition of the liver was performed. Efficacy was confirmed by demonstrating photopaenia at the ablation zones. Follow-Up PET/CT was performed at 6–8 month intervals; this also represented the most recent clinical follow-up since patients were interviewed to evaluate symptoms prior to each imaging study.
Data Collection and Analysis Number, size, and location of liver lesions, procedural and general anaesthesia durations, technical success and complications, patient and operator dose, and clinical outcomes (tumour progression and symptomatic resolution) were evaluated using retrospective chart review. Lesion size was measured as the maximum diameter on planning fused PET/CT images. Procedure duration was measured between the first 18FFDOPA injection and the final post-treatment PET/CT. Duration of general anaesthesia was also recorded. Technical success was defined as accurate RFA probe placement in the centre of each lesion on intra-procedural 18F-FDOPA PET/CT and complete ablation-zone photopaenia on final PET/CT. Complications were classified according to the SIR grading system [13]. Patient CT dose was estimated via dose length product (DLP) calculated using proprietary scanner software. Operator dose was measured using thermoluminescent dosimeters (TLDs) attached to bilateral hands and ankles, temporal regions (proxy for lens dose), and to the torso of the interventional radiologists and the assisting radiographer being in the operating room. Tumour progression was defined as local (uptake within ablation zone), hepatic (new liver lesion), or extra-hepatic (new uptake outside liver) on most recent 18-FDOPA PET/
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R. L. Cazzato et al.: 18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases…
Fig. 1 Four of the six metastases treated in patient 3. 18F-FDOPA PET/CT showing hyper-metabolic metastases (arrows) in segments VI (A) and IV (B). Such lesions were treated using a straight 3-cm active-tip RFA probe (C, D) using hydrodissection (hyperdensity in
D, obtained by diluting 5 % of iodinated contrast medium in 5 % dextrose in water) to protect the stomach during ablation of segment IV lesions. Post-procedural 18F-FDOPA PET/CT scan (E, F) demonstrates complete photopaenia at the ablated sites (arrows)
CT examination. Symptom regression was qualitatively defined as either ‘‘partial’’ or ‘‘complete’’. Descriptive statistics were computed using Microsoft Excel 2010 (Microsoft Corporation, Redmond, Washington, USA).
radiologists performed the second procedure and doses were within normal limits [14]. Radiographer dose was within expected limits (Table 2; Figs. 2, 3). At mid-term 18F-FDOPA PET/CT follow-up (mean 12.6 months; range 6–20), there was no local tumour progression in the treated lesions, nor extra-hepatic disease progression. In two cases, there was hepatic disease progression with new liver lesions (one lesion in each patient measuring B1 cm) at different sites from the treated metastases (Table 1); however, both patients were not symptomatic, probably due to the limited extension of such progression. The two patients presenting with ‘‘carcinoid syndrome’’ before RFA reported complete symptom regression (clinical success 100 %).
Results Thirteen liver metastases (mean size 11.4 mm, SD 2.4 mm, range 8–16) were treated in three patients (Table 1) with 2, 5, and 6 lesions, respectively (mean 4.3 lesions treated per session). Technical success was 100 %; mean procedural time 173.3 min (range 90–220); and mean duration of general anaesthesia 283.3 min (range 150–280). No procedure-related or late complications were recorded. Mean patient dose was 2844 mGycm (range 2104–3686). Operator dose was available for the first two procedures only. The first procedure performed by a single radiologist resulted in 149 lSv to the right hand. Two
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Discussion PET/CT represents an emerging imaging guidance technique for percutaneous procedures. Current experience is limited due to restricted availability, but primarily focuses
R. L. Cazzato et al.: 18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases… Table 2 Operators’ dose Left lens (lSv)
Right lens (lSv)
Left hand (lSv)
Right hand (lSv)
Left ankle (lSv)
Right ankle (lSv)
Total body (lSv)
First operator (patient 1)
23
21
43
149
21
14
18
First operator (patient 2)
11
5
8
9
6
5
6
Second operator (patient 2)
5
6
18
14
8
7
6
Assistant radiographer (patient 1)
7
7
8
9
6
5
6
Assistant radiographer (patient 2)
3
7
11
11
8
10
7
Fig. 2 Measured dose to the interventional radiologist performing the procedure
on fluorodeoxyglucose (FDG)-avid tumours. Several studies have illustrated technical feasibility and accuracy of PET/CT-guided procedures [7, 10, 15–22]. In the largest biopsy series, Cornelis et al. reported 100 % diagnostic success in 106 FDG-PET/CT-guided biopsies of lesions in various organs poorly visualised on US, CT, and MR [7]. The largest ablation series by Ryan et al. demonstrated 97 % initial technical success, with 7 % local recurrence at median 155-day follow-up [10]. These studies illustrate the key advantages of PET/CT guidance: (i) precise lesion identification and targeting using combined functional and anatomic imaging; (ii) persistent tracer uptake throughout long procedures enabling treatment of multiple lesions; and (iii) immediate post-procedural assessment of technical success (ablation-zone photopaenia) [10]. The latter feature is analogous to pathologic frozen sections utilised during oncologic surgery, and enables immediate verification of adequate tumour margins [10, 23]. Complete ablation is granted when a safety margin is assured around the target
Fig. 3 Measured dose to the radiographer assisting the interventional radiologist inside the interventional room
lesion and the efficacy of such method is verified with subsequent imaging follow-up. This is not the case with surgery since following tumour resection, margins can be immediately verified on the resected specimen, thus allowing for immediate intra-operatory extension of the resection in case of limited margins. In this perspective, PET/CT photopaenia in the ablation zone may be considered as a surrogate of post-resection pathological analysis of the margins, thus allowing for immediate intra-operative additional ablation in case of limited ablation. GEP-NETs result often in multiple hypervascular liver metastases [24]. Lesion conspicuity appears optimal on DWI and contrast-enhanced MR, but both of them are unsuitable for ablation due to limited spatial resolution and
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R. L. Cazzato et al.: 18F-FDOPA PET/CT-Guided Radiofrequency Ablation of Liver Metastases…
transient enhancement, respectively. Therefore, targeting of multiple lesions during long procedures is not allowed [9]. However, tumour biology may be exploited to improve detection using specific radiotracers [8] such as 18FFDOPA and 68 Ga-DOTA-D-Phe1-Try3-Octreotide (68 Ga-DOTATOC) [8, 9]. We specifically reported about 18F-FDOPA PET/CT imaging guidance using a split-dose protocol similar to that described by Ryan et al. [10] to ablate GEP-NET liver metastases. Procedures were performed in an interventional PET/CT scanner under general anaesthesia. RFA was preferred to radioembolisation due to the low burden of hepatic disease [6] and the limited access available in our institutions to this kind of intra-arterial therapy; moreover, due to the small size of target lesions, RFA was preferred to other techniques such as microwave ablation. We did not use navigation software [16, 17, 21, 22] because it is not available in our department; nevertheless, such tools yield several advantages including reduction of both procedural time and radiation exposure for patients and operators. Our small series demonstrates the feasibility of this novel technique. Lesions were easily targeted, and procedures performed relatively quickly without complications. At mean 12-month follow-up, there was no local tumour progression; and symptoms had completely resolved in the two symptomatic cases. The principal drawbacks of this technique are restricted availability, relatively high dose, and uncertain role in the natural history of the disease. Dose to the patient was significant (approximately 43 mSv [25]). However, operator and assistant doses were within acceptable limits [14], other than high dose to the single operator’s right hand during the first procedure. Such high dose to the operator’s right hand in the first case can be explained by the fact that the procedure was the first PET/CT-guided RFA performed in our Institution; moreover, the right hand was the closest operator’s anatomic part to the patient. Using two operators (one leaving the interventional room after having performed half of the procedure and the other taking over) reduced individual doses to acceptable levels during the second procedure. The split-dose technique, in which operators are exposed to the targeting radiotracer dose only, probably contributed favourably to this outcome. Finally, follow-up PET/CT studies demonstrated hepatic disease progression at different sites in 2/3 cases. Ablation is currently suggested in patients with low-burden hepaticconfined disease [6], unremitting symptoms, and in nonsurgical recurrence [4]; however, the precise role of 18FFDOPA PET/CT-guided ablation remains uncertain given the very low experience available [11] and the progressive behaviour of the disease.
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Study limitations are the small sample size and the retrospective setting. Mean 12-month follow-up is probably adequate for indolent lesions, but longer follow-up would ideally be desirable. In conclusion, 18F-FDOPA PET/CT-guided RFA for patients with GEP-NETs and low-burden hepatic-confined metastases or unremitting symptoms is technically feasible, safe, and clinically effective. The principal advantages are excellent lesion visualisation throughout the procedure and post-procedural assessment of technical success; drawbacks are limited availability and patient dose. Further prospective studies are required to elucidate the precise role of this novel technique in tailored multimodality management of GEP-NET liver metastases. Compliance with Ethical Standards Conflicts of Interest to disclose.
All of the authors have no conflict of interest
Ethical Approval 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 Informed consent was obtained from all individual participants included in the study.
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