Positron Emission Tomography Imaging in Medullary Thyroid Carcinoma: Time for Reappraisal?

Abstract

Medullary thyroid carcinomas (MTC) are rare neoplasms derived from calcitonin-secreting cells of the thyroid. They can occur sporadically or as part of the multiple endocrine neoplasia type 2 syndromes. Overall, successful management of MTC patients heavily relies on the patient's conditions, tumor stage, genetic background, and the medical team's experience. Over the past 10 years, many consensus or near consensus of expert panels have been published for the treatment and follow-up of MTC (e.g., American Thyroid Association [ATA] 2009, ATA 2015, European Society of Medical Oncology [ESMO] 2019, European Association of Nuclear Medicine [EANM] 2020). The recent 2020 EANM guidelines recommend in particular to carry out ¹⁸F-FDOPA (6-18F-fluoro-L-3,4-dihydroxyphenylalanine) positron emission tomography/computed tomography scan (PET/CT scan) in MTC patients with persistent disease; however, this recommendation was not made in the 2015 ATA revised version. 18F-flurodeoxy glucose PET/CT scan is limited to aggressive forms, and PET imaging using ⁶⁸Ga-somatostatin analogs appears suboptimal. This special article focuses on the clinical value of PET imaging in three common clinical scenarios (before initial thyroidectomy, before cervical reoperations for persistent/recurrent disease, and in the follow-up of metastatic cases).

Introduction

Medullary thyroid carcinoma (MTC) is a rare neoplasm of neural crest origin derived from calcitonin-secreting cells of the thyroid (C cells). MTC accounts for 3–10% of all thyroid carcinomas and represents 0.4–1.3% of all thyroid nodules. MTC can occur sporadically (about 70% of the total) or as part of the multiple endocrine neoplasia type 2 (MEN2) syndromes. MEN2 is an autosomal dominant syndrome due to germline activating point mutations in the RET proto-oncogene. MEN2 is divided into two groups depending on their clinical features: MEN2A (95% of MEN2, including the former subgroup of familial MTC) and MEN2B (5%). MTC typically arises from the posterior upper third of the thyroid lobes, where the largest concentration of C cells is found. MEN2-related cases are characterized by diffuse C cell hyperplasia (CCH) and tumor multifocality, CCH being considered as a preneoplastic lesion. Multifocality can also occur in up to 10% of large RET-negative MTC via intrathyroidal diffusion. MTC is characterized by a high propensity for regional lymph node (LN) metastases with an increased risk in MEN2 (due to multifocality) for bilateral cervical nodal metastases.

Patients with MTC can present with a thyroid nodule discovered by neck palpation or thyroid ultrasound (US), less frequently with local symptoms (neck fullness/pain, dysphagia, dyspnea, or hoarseness), or with systemic symptoms (bone pain, flushing, weight loss, and/or diarrhea) due to the presence of distant metastases with highly elevated levels of calcitonin. Of note, MEN2-related MTC occur at a younger age than their sporadic counterparts and can present with a family history of MTC/pheochromocytoma (PHEO) or pathognomonic clinical signs (e.g., notalgia paresthetica in MEN2A with RET 634 codon mutation, mucosal neuromas, and marfanoid habitus in MEN2B). The diagnosis of MTC can be made preoperatively by measurement of serum calcitonin. The tumor stage is a critical prognostic factor in MTC. Recently, new TNM staging has been proposed for a more accurate risk stratification and potential treatment selection (1). One major change involved placing only metastatic disease in stage IV (T4 and N1b being downstaged), which led to a revised 5-year disease-specific survival rate in this group of 40% compared with 82% in the current American Joint Committee on Cancer TNM staging. Recent data have shown that germline RET mutations determine the age of MTC occurrence but has no impact on overall survival or time to developing distant metastatic disease. By contrast, MTC patients who carry M918T somatic RET mutation have a decrease in 10-year survival rate compared with RET mutation-negative cases (45% versus 90%, respectively). Additionally, patients with a shortened serum calcitonin and/or carcinoembryonic antigen (CEA) doubling time (<6–12 months) during follow-up have a dismal prognosis (2).

As other neuroendocrine tumors, MTC overexpress large (L)-type amino acid transporters and therefore can be imaged by 6-18F-fluoro-L-3,4-dihydroxyphenylalanine (¹⁸F-FDOPA) positron emission tomography/computed tomography scan (PET/CT scan). For performance and availability reasons, we have chosen to focus our overview on the role of ¹⁸F-FDOPA PET imaging in three common clinical scenarios (before initial thyroidectomy, before cervical reoperations for persistent/recurrent disease, and in the follow-up of metastatic cases).

¹⁸F-FDOPA PET/CT Scan

¹⁸F-FDOPA is a fluorinated analog of a naturally occurring amino acid, L-DOPA. It is widely accepted that ¹⁸F-FDOPA enters into the cells mainly via LAT-1 and LAT-2 and is retained in the cells after decarboxylation by the aromatic L-amino acid decarboxylase (AADC) that converts ¹⁸F-FDOPA into ¹⁸F-dopamine. ¹⁸F-DOPA is not specific to MTC. Although L-type amino acid transporters and AADC expression has been demonstrated in some other malignancies, there are only a few anecdotal case reports in non-neuroendocrine malignancies, such as solid pseudopapillary tumor of the pancreas, thyroid neoplasm of follicular origin (oncocytoma), squamous cell carcinoma (cervix, epiglottis), poorly differentiated adenocarcinoma, and melanoma. In MEN2 cases, uptake can be related to another primary neuroendocrine tumor such as PHEO.

¹⁸F-FDOPA PET/CT scan acquisition protocol needs to be adapted to patients with MTC since tumor uptake can decrease by 40% between early and delayed images. According to the European Association of Nuclear Medicine (EANM) guidelines, early ¹⁸F-FDOPA images (at 15 minutes after injection) centered over the neck may be acquired in addition to whole-body acquisition. Premedication with carbidopa was previously proposed to improve the tracer's bioavailability, but its impact on the detection rate of ¹⁸F-FDOPA PET/CT scan has not been demonstrated, and therefore, this premedication is not recommended. PET/CT scans are usually performed with co-registered low-dose CT and without contrast-enhanced CT (ceCT) for the evaluation of this tumor because ceCT adds little to cervical LN assessment. The EANM guidelines propose to use PET/ceCT in selected cases when there is suspicion of local invasive disease or vascular invasion or suspicious metastases in sites of physiological tracer uptake.

Radiation dose exposure is estimated to be 0.020 mSv/MBq. Additional exposure originates from the CT scan carried out in PET/CT scan examination (ranging from 2 to 5 mSv). No adverse events have been reported in association with the administration of ¹⁸F-FDOPA.

The clinical value of ¹⁸F-FDOPA in the common clinical scenarios encountered in practice is discussed below. Most importantly, MTC patients should be evaluated and treated by multidisciplinary teams at high-volume centers with appropriate expertise to ensure favorable outcome.

Clinical Scenarios

¹⁸F-FDOPA PET/CT scan is not recommended before initial surgery for MTC

Due to the high penetrance (90%) for MTC in MEN2, early (prophylactic) thyroidectomy is recommended. RET mutations can be classified at highest (M918T RET mutation), high (mainly 634 codon mutations and the rare A883F RET mutation), and moderate (other RET variants) risks. The age at early thyroidectomy is based on these risk groups, from below the age of 1 in the highest risk group to 5 years in the high-risk group. Patients with moderate risk should have thyroidectomy when calcitonin increases or, based on parents decision to avoid a long-term surveillance, during childhood (3). In the latter cases, calcitonin is usually normal or mildly increased, and the MTC, if present, has not spread outside the thyroid gland. Imaging study for staging is thus needless before early thyroidectomy, excluding neck US. Furthermore, the likelihood of primary hyperparathyroidism or PHEO being present at this stage is almost always nil, but biochemical testing should still be undertaken.

By contrast, in sporadic cases or in MEN2 cases for whom the diagnosis could not be made before the recommended age, accurate staging is important before initial therapeutic surgery. In all cases, neck US remains the first-line imaging modality for assessing thyroid nodules and cervical LNs and can also be used to guide fine-needle aspiration cytology.

In cases with preoperative serum calcitonin values of >500 pg/mL, a complete preoperative workup should be performed and include ¹⁸F-FDOPA PET/CT scan (4) (Table 1). In patients with distant metastases, a less extended neck surgery should be considered to avoid local complications and to circumvent complications arising from an extended surgical approach.

Table 1.

Preoperative Imaging Studies Before Initial Surgery According to Different Clinical Scenarios

Presentation	Surgery	Preoperative imaging studies^a
MEN2 diagnosed by genetic screening and no clinical evidence of disease	Prophylactic total thyroidectomy (if no disease on preoperative US)	Neck US
MTC (MEN2 or sporadic) <10 mm without evidence of metastatic nodes on neck US and serum calcitonin <200 pg/mL	Total thyroidectomy and prophylactic central LN dissection	Neck US
MTC (MEN2 or sporadic) ≥10 mm without evidence of LN metastasis on neck US	Total thyroidectomy and central LN dissection, prophylactic ipsilateral (sporadic) or bilateral (MEN2) lateral LN dissection	Neck US, neck and chest CT?, ¹⁸F-FDOPA PET/CT scan?
MTC (MEN2 or sporadic) with abnormal nodes on neck US	Total thyroidectomy and therapeutic central and lateral LN dissection (bilateral in MEN2)	Neck US, neck and chest CT, ¹⁸F-FDOPA PET/CT scan?
MTC (MEN2 or sporadic) with suspicion of distant metastases (calcitonin >500 pg/mL)	In the absence of distant metastases, total thyroidectomy and therapeutic cervico-mediastinal and bilateral lateral LN dissection In the presence of distant metastases, surgery can be performed for preventing locoregional complications	Neck US, neck, chest, and abdomen/pelvis CT (or hepatic MRI), bone scintigraphy and bone marrow MRI, ¹⁸F-FDOPA PET/CT scan?, ¹⁸F-FDG PET/CT scan?

Before thyroidectomy, all patients are required to undergo evaluation for pheochromocytoma with biochemical testing. If metanephrines are elevated, an abdominal computed tomography and/or magnetic resonance imaging is indicated.

?, optional; ¹⁸F-FDG, 18F-flurodeoxy glucose; ¹⁸F-FDOPA, 6-18F-fluoro-L-3,4-dihydroxyphenylalanine; LN, lymph node; MEN2, multiple endocrine neoplasia type 2; MRI, magnetic resonance imaging; MTC, medullary thyroid carcinoma; PET/CT scan, positron emission tomography/computed tomography scan; US, ultrasound.

In MTC with suspected multiple LN metastases on US, a neck and chest CT scan complements neck US for ruling out potential mediastinal nodes that may influence surgical approach. Some patients with positive LNs in the upper mediastinum, but without distant metastases, may benefit from mediastinal dissection.

In MTC with the absence of suspected LN or limited abnormalities on neck US, the value of preoperative imaging for directing cervical LN dissection is still debated and widely depends on the surgical approach. For teams that perform total thyroidectomy with systematic central neck and bilateral lateral lymphadenectomy (including level V), regardless of serum calcitonin levels and imaging results, the added value of ¹⁸F-FDOPA PET/CT scan is probably more limited, even if it may be more accurate than neck US in patients with widespread nodes in the lateral neck compartments (5). In this situation, the main criterion for modifying surgical strategy would be the detection of LNMs in the mediastinum and/or distant metastases. However, the overall yield of finding extracervical metastases in patients with moderately elevated serum calcitonin levels is low. Some centers do not routinely perform prophylactic contralateral lateral lymphadenectomy in sporadic cases because it is free of metastases in more than 60% of cases (depending on the degree of central nodal involvement), and specific complications are not uncommon such as lymphatic leak, spinal accessory nerve paralysis, and other dysfunctions of the lateral neck nerves. A threshold of 200 pg/mL for serum calcitonin has been proposed in sporadic cases for indicating contralateral prophylactic dissection, but this does not accurately predict tumor behavior. In this situation, ¹⁸F-FDOPA PET/CT scan may be relevant. Currently, no guidelines recommend to perform ¹⁸F-FDOPA PET/CT scan before initial surgery due to scarce literature (3,4,6,7). Of note, all patients should undergo genetic testing for RET mutations and have a PHEO excluded preoperatively by measurements of plasma free or 24-hour urinary fractionated metanephrines.

Restaging at the reoperative neck surgery time is an appropriate indication for ¹⁸F-FDOPA PET/CT scan

Although total thyroidectomy with systematic nodal dissection is routinely performed, ∼40% of patients will present with persistent/recurrent disease. Interestingly, the presence of germline RET mutation does not affect the degree of lymphatic spread. Even after adequate initial surgery, the ability to cure patients with LNM (≥3 compartments involved, ≥10 positive nodes) is very unusual. Here, postoperative serum calcitonin measurement plays a central role in detecting persistent or recurrent disease. Except for rare poorly secreting MTC, the level of calcitonin indeed grossly reflects residual tumor volume. In patients with structural disease in the neck, the benefit–risk ratio of reoperation should be balanced in each individual situations (personalized approach). Reoperation with a curative intent is most feasible in patients who have had an inadequate initial operation.

In 2009, the American Thyroid Association (ATA) MTC guidelines recommended performing an ¹⁸F-FDOPA PET/CT scan in MTC patients with persistent/recurrent with serum calcitonin >150 pg/mL (8). However, this recommendation was not made in the 2015 ATA revised version (3) (Table 2). The EANM did not endorse revised recommendations due to contradictions between versions, no new evidence against the use of ¹⁸F-FDOPA PET/CT scan, the body of scientific evidence in the literature, and the certitude of the nuclear medicine community regarding the quality of images that can be obtained with an optimal imaging protocol (9). Based on two meta-analyses and several original articles, ¹⁸F-FDOPA PET can be considered as the best radiopharmaceutical for the detection of persistent/recurrent MTC on both patient- and lesion-based analyses (10,11).

Table 2.

Indication for Positron Emission Tomography Imaging According to Guidelines

	¹⁸F-FDOPA	¹⁸F-FDG	⁶⁸Ga-SSA
ATA 2015 (3)	Not recommended	Not recommended	Not recommended
ESMO 2019 (4)	At initial diagnosis when serum CT >500 pg/mL or suspicion of distant metastasis In persistent/recurrent MTC with serum CT >150 pg/mL	In cases with short serum CT and CEA levels, doubling times (<1 year) or MTC with an aggressive behavior (e.g., CEA levels disproportionately high compared with CT levels)	To assess the feasibility of PRRT
EANM 2020 (7)	In persistent/recurrent MTC with serum CT >150 pg/mL	In cases with short serum CT and CEA levels, doubling times (<1 year) or MTC with an aggressive behavior	In selected cases with inconclusive morphological and functional imaging and to assess the feasibility of PRRT

ATA, American Thyroid Association; CEA, carcinoembryonic antigen; CT, calcitonin; EANM, European Association of Nuclear Medicine; ESMO, European Society of Medical Oncology; PRRT, peptide receptor radionuclide therapy.

Overall, the per patient detection rate of ¹⁸F-FDOPA PET/CT scan is estimated to be 60–70% and heavily depends on serum calcitonin levels and tumor behavior. The main limitation of ¹⁸F-FDOPA PET/CT scan is due to its poor spatial resolution that leads to underestimation of subcentimeter nodes. However, ¹⁸F-FDOPA PET/CT scan performed better than whole-body magnetic resonance imaging (MRI) and whole-body CT scan in one study (12). The cutoff value of 150 pg/mL for calcitonin should not be taken as a strict value that determine ¹⁸F-FDOPA PET/CT scan sensitivity but rather as a clinically relevant value for the timing of reoperative surgery. If reoperation is being considered in a patient with a lower serum calcitonin value, the use of ¹⁸F-FDOPA PET/CT scan can be discussed on an individual basis.

¹⁸F-FDOPA PET/CT scan together with neck US can show the involved neck compartments/levels and help to determine the optimal surgical strategy (extended vs. limited neck dissection). Therefore, there is no evidence to disqualify the use of ¹⁸F-DOPA in countries where ¹⁸F-DOPA is approved and interpreted for patient management in a multidisciplinary approach.

The use of ¹⁸F-FDOPA PET/CT scan in patients with metastatic MTC may be appropriate in selected cases

All imaging modalities underestimate the extent of the disease as illustrated by the high proportion of patients with negative imaging results or minimal abnormalities despite highly elevated serum calcitonin levels. ¹⁸F-FDOPA PET/CT scan often appears less sensitive than MRI for detecting osseous and liver metastases. The added value of ¹⁸F-FDOPA PET/CT scan in the follow-up of patients with metastatic MTC is also of limited value since visualizing of additional small-volume residual disease is unlikely to change patient management. Thus, it appears appropriate to perform ¹⁸F-FDOPA PET/CT scan in selected cases such as unexpected rise in serum calcitonin and/or CEA with stable conventional imaging results or new indeterminate lesion on CT.

Role of Other Radiopharmaceuticals

A meta-analysis showed that the detection rate of 18F-flurodeoxy glucose (¹⁸F-FDG) PET or PET/CT scan in suspected recurrent MTC on a per patient-based analysis is low (59% [95% confidence interval 54–63%]) (13). Therefore, ¹⁸F-FDG PET/CT scan can only be used in addition to neck US and cross-sectional anatomic imaging (CT scan, MRI) in this setting. ¹⁸F-FDG PET/CT scan sensitivity increases in patients with high calcitonin and CEA concentrations and short calcitonin and CEA doubling times, suggesting its usefulness as a prognostic factor.

⁶⁸Ga-somatostatin analogs PET/CT scan appears suboptimal but could be useful in a small number of patients with inconclusive results or for selecting MTC patients who are likely to benefit from peptide receptor radionuclide therapy. CEA targeting using murine or chimeric anti-CEA bispecific antibody and pretargeted haptens peptides labeled with ¹¹¹In or ¹³¹I has initially been developed for radioimmunotherapy in relapsed MTC. More recently, the same approach has been developed for pretargeted immuno-PET with promising preliminary findings (14).

As knowledge regarding tumor biology and pathogenesis will continue to expand, the number of targeted agents will no doubt increase for imaging and disease characterization of MTC. Cholecystokinin 2 receptor (CCK₂R, or gastrin receptor) is overexpressed in several tumor types, including MTC. CCK₂R targeting shows promise for MTC imaging and represents together with somatostatin receptors ligands, potential theranostic approaches in selected cases (15). Many peptide-based radiopharmaceuticals for CCK₂R targeting have been developed, mainly based on short version of gastrin (i.e., minigastrin [MG]). ⁶⁸Ga-labeled DOTA-PP-F11 has shown promising results for PET/CT scan imaging and its therapeutic companion ¹⁷⁷Lu-PP-F11 is currently being evaluated in the setting of clinical trials. To date, there are no prospective clinical studies of CCK₂R targeting vectors labeled with positron-emitting radionuclides available. Recently, a new highly metabolically stable MG analog (DOTA-MGS5) has shown excellent targeting properties in preclinical studies, which support its translation into clinical trials (16).

Conclusion

Robust MTC imaging remains an unresolved clinical unmet need mainly due to MTC biological behavior with a trend toward micrometastatic spread. MTC is also a heterogeneous disease with different phenotypes and variable clinical manifestations (micro and macro cervical LNs vs. widespread distant metastases). If available, ¹⁸F-FDOPA PET/CT scan is the first-choice radiopharmaceutical for restaging at the reoperative neck surgery time. Its value before initial therapeutic surgery would merit further evaluation. The role of ¹⁸F-FDG PET/CT scan is limited to aggressive forms.

Footnotes

Authors' Contribution

F.C. and D.T. wrote the article.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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Positron Emission Tomography Imaging in Medullary Thyroid Carcinoma: Time for Reappraisal?

Abstract

Introduction

18F-FDOPA PET/CT Scan

Clinical Scenarios

18F-FDOPA PET/CT scan is not recommended before initial surgery for MTC

Restaging at the reoperative neck surgery time is an appropriate indication for 18F-FDOPA PET/CT scan

The use of 18F-FDOPA PET/CT scan in patients with metastatic MTC may be appropriate in selected cases

Role of Other Radiopharmaceuticals

Conclusion

Footnotes

Authors' Contribution

Author Disclosure Statement

Funding Information

References

¹⁸F-FDOPA PET/CT Scan

¹⁸F-FDOPA PET/CT scan is not recommended before initial surgery for MTC

Restaging at the reoperative neck surgery time is an appropriate indication for ¹⁸F-FDOPA PET/CT scan

The use of ¹⁸F-FDOPA PET/CT scan in patients with metastatic MTC may be appropriate in selected cases