Abstract
Introduction
In primary hyperparathyroidism (PHPT), the localization of hyperfunctioning parathyroid gland (HPTG) allows tailored surgery. Although Four-Dimensional Contrast-enhanced Computed Tomography (4DCeCT) and 18F-choline Positron Emission Tomography/Computed Tomography (PET/CT) are reported to be promising second-line imaging procedures, no meta-analysis of their comparison exists.
Design
we conducted a systematic review and meta-analysis to find original papers reporting the head-to-head comparison of 4DCeCT, 18F-choline PET/CT and integrated 18F-choline-PET/4DCeCT.
Methods
this systematic review was conducted according to PRISMA. PubMed, CENTRAL, Scopus, and Web of Science were searched until January 2021. Studies comparing the ability of 4DCeCT, 18F-choline PET/CT and 18F-choline PET/4DCeCT to identify HPTG in patients with PHPT were selected. A per patient-based analysis of the three procedures was conducted in all patients (detection rate, DR) and in those with histologically confirmed HPTG (sensitivity).
Results
Of the 78 records identified, five articles (153 PHPT patients) published between January the 1st, 2018 and January the 31st, 2021 were included. The pooled DR of 18F-choline PET/CT, 4DCeCT and 18F-choline PET/4DCeCT was 0.86, 0.69, and 0.86, respectively, while their pooled sensitivity was 0.89, 0.77 and 0.93, respectively. The analysis of pooled discrepancy showed that the sensitivity of 18F-choline PET/CT and 18F-choline PET/4DCeCT was higher than that of 4DCeCT by 0.11 and 0.13, respectively, the sensitivity of 18F-choline PET/4DCeCT being 0.06 higher than that of 18F-Choline PET/CT.
Conclusions
This meta-analysis suggests that the sensitivity of 18F-choline PET/CT and 18F-choline PET/4DCeCT is higher than that of 4DCeCT, while only a slight difference was observed between 18F-choline PET/CT and 18F-choline PET/4DCeCT.
Similar content being viewed by others
References
S.J. Silverberg, Natural history of primary hyperparathyroidism. Endocrinol. Metab. Clin. North Am. 29, 451–64 (2000). https://doi.org/10.1016/s0889-8529(05)70145-6
N.M. Singh Ospina, R. Rodriguez-Gutierrez, S. Maraka et al. Outcomes of parathyroidectomy in patients with primary hyperparathyroidism: a systematic review and meta-analysis. World J. Surg. 40, 2359–77 (2016). https://doi.org/10.1007/s00268-016-3514-1
J.P. Bilezikian, M.L. Brandi, R. Eastell et al. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the Fourth International Workshop. J. Clin. Endocrinol. Metab. 99, 3561–9 (2014). https://doi.org/10.1210/jc.2014-1413
G. Noussios, P. Anagnostis, K. Natsis, Ectopic parathyroid glands and their anatomical, clinical and surgical implications. Exp. Clin. Endocrinol. Diabetes 120, 604–10 (2012). https://doi.org/10.1055/s-0032-1327628
G. Treglia, R. Sadeghi, C. Schalin-Jäntti et al. Detection rate of (99m) Tc-MIBI single photon emission computed tomography (SPECT)/CT in preoperative planning for patients with primary hyperparathyroidism: A meta-analysis. Head. Neck 381, E2159–72 (2016). https://doi.org/10.1002/hed.24027
C.Y. Lo, B.H. Lang, W.F. Chan et al. Prospective evaluation of preoperative localization by technetium-99m sestamibi scintigraphy and ultrasonography in primary hyperparathyroidism. Am. J. Surg. 193, 155–9 (2007). https://doi.org/10.1016/j.amjsurg.2006.04.020
A. Harari, E. Mitmaker, R.H. Grogan et al. Primary hyperparathyroidism patients with positive preoperative sestamibi scan and negative ultrasound are more likely to have posteriorly located upper gland adenomas (PLUGs). Ann. Surg. Oncol. 18, 1717–22 (2011). https://doi.org/10.1245/s10434-010-1493-2
G. Treglia, P. Trimboli, M. Huellner et al. Imaging in primary hyperparathyroidism: focus on the evidence-based diagnostic performance of different methods. Minerva Endocrinol. 43, 133–143 (2018). https://doi.org/10.23736/S0391-1977.17.02685-2
S. Minisola, C. Cipriani, D. Diacinti et al. Imaging of the parathyroid glands in primary hyperparathyroidism. Eur. J. Endocrinol. 174, D1–8 (2016). https://doi.org/10.1530/EJE-15-0565.
L.F. Starker, A. Mahajan, P. Björklund et al. 4D parathyroid CT as the initial localization study for patients with de novo primary hyperparathyroidism. Ann. Surgical Oncol. 18, 1723–8 (2011). https://doi.org/10.1245/s10434-010-1507-0
M. Mekel, R. Linder, B. Bishara et al. 4-dimensional computed tomography for localization of parathyroid adenoma. Harefuah 152, 710–712 (2013)
M. Hamidi, M. Sullivan, G. Hunter et al. 4D-CT is superior to ultrasound and sestamibi for localizing recurrent parathyroid disease. Ann. Surg. Oncol. 25, 1403–1409 (2018). https://doi.org/10.1245/s10434-018-6367-z
Y. Tian, S.T. Tanny, P. Einsiedel et al. Four-dimensional computed tomography: clinical impact for patients with primary hyperparathyroidism. Ann. Surg. Oncol. 25, 117–121 (2018). https://doi.org/10.1245/s10434-017-6115-9
E. Quak, S. Lheureux, Y. Reznik et al. F18-choline, a novel PET tracer for parathyroid adenoma? J. Clin. Endocrinol. Metab. 98, 3111–2 (2013). https://doi.org/10.1210/jc.2013-2084
M. Hodolic, V. Huchet, S. Balogova et al. Incidental uptake of (18)F-fluorocholine (FCH) in the head or in the neck of patients with prostate cancer. Radio. Oncol. 48, 228–34 (2014). https://doi.org/10.2478/raon-2013-0075
T. Cazaentre, F. Clivaz, F. Triponez, False-positive result in 18F-fluorocholine PET/CT due to incidental and ectopic parathyroid hyperplasia. Clin. Nucl. Med 39, e328–30 (2014). https://doi.org/10.1097/RLU.0b013e3182a77b62
G. Treglia, E. Giovannini, D. Di Franco et al. The role of positron emission tomography using carbon-11 and fluorine-18 choline in tumors other than prostate cancer: a systematic review. Ann. Nucl. Med. 26, 451–61 (2012). https://doi.org/10.1007/s12149-012-0602-7
L. Michaud, A. Burgess, V. Huchet et al. Is 18F-fluorocholine-positron emission tomography/computerized tomography a new imaging tool for detecting hyperfunctioning parathyroid glands in primary or secondary hyperparathyroidism? J. Clin. Endocrinol. Metab. 99, 4531–6 (2014). https://doi.org/10.1210/jc.2014-2821
M. Orevi, N. Freedman, E. Mishani et al. Localization of parathyroid adenoma by 11C-choline PET/CT: Preliminary results. Clin. Nucl. Med 39, 1033–8 (2014). https://doi.org/10.1097/RLU.0000000000000607
L. Lezaic, S. Rep, M.J. Sever et al. 18F-Fluorocholine PET/CT for localization of hyperfunctioning parathyroid tissue in primary hyperparathyroidism: a pilot study. Eur. J. Nucl. Med. Mol. Imaging 41, 2083–9 (2014). https://doi.org/10.1007/s00259-014-2837-0
L. Michaud, S. Balogova, A. Burgess et al. A pilot comparison of 18f-fluorocholine PET/CT, ultrasonography and 123i/99mtc-sestamibi dual-phase dual-isotope scintigraphy in the preoperative localization of hyperfunctioning parathyroid glands in primary or secondary hyperparathyroidism: Influence of thyroid anomalies. Med. (Baltim.) 94, e1701 (2015). https://doi.org/10.1097/MD.0000000000001701
G. Treglia, A. Piccardo, A. Imperiale et al. L. Diagnostic performance of choline PET for detection of hyperfunctioning parathyroid glands in hyperparathyroidism: a systematic review and meta-analysis. Eur. J. Nucl. Med Mol. Imaging 46, 751–765 (2019). https://doi.org/10.1007/s00259-018-4123-z
E. Quak, D. Blanchard, B. Houdu et al. F18-choline PET/CT guided surgery in primary hyperparathyroidism when ultrasound and MIBI SPECT/CT are negative or inconclusive: the APACH1 study. Eur. J. Nucl. Med Mol. Imaging 45, 658–66 (2018). https://doi.org/10.1007/s00259-017-3911-1
Grimaldi S, Young J, Kamenicky P et al. Challenging pre-surgical localization of hyperfunctioning parathyroid glands in primary hyperparathyroidism: the added value of (18)F-Fluorocholine PET/CT. Eur J Nucl Med Mol Imaging. 2018. https://doi.org/10.1007/s00259-018-4018-z
S.K. Taywade, N.A. Damle, A. Behera et al. Comparison of 18F-Fluorocholine positron emission tomography/computed tomography and four-dimensional computed tomography in the preoperative localization of parathyroid adenomas-initial results. Indian J. Endocrinol. Metab. 21, 399–403 (2017). https://doi.org/10.4103/ijem.IJEM_536_16
W.P. Kluijfhout, J.D. Pasternak, J.E. Gosnell et al. (18)F Fluorocholine PET/MR imaging in patients with primary hyperparathyroidism and inconclusive conventional imaging: a prospective pilot study. Radiology 284, 460–467 (2017). https://doi.org/10.1148/radiol.2016160768.
A. Piccardo, P. Trimboli, M. Rutigliani et al. Additional value of integrated 18F-choline PET/4D contrast-enhanced CT in the localization of hyperfunctioning parathyroid glands and correlation with molecular profile. Eur. J. Nucl. Med Mol. Imaging 46, 766–775 (2019). https://doi.org/10.1007/s00259-018-4147-4
Giovanella L, Bacigalupo L, Treglia G et al. Will 18F-fluorocholine PET/CT replace other methods of preoperative parathyroid imaging? Endocrine. 2020 6. https://doi.org/10.1007/s12020-020-02487-y. Epub ahead of print.
M.D.F. McInnes, D. Moher, B.D. Thombs et al. The PRISMA-DTA group. preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA 319, 388–396 (2018). https://doi.org/10.1001/jama.2017.19163
P.F. Whiting, A.W. Rutjes, M.E. Westwood et al. QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann. Intern. Med. 155, 539–36 (2011). https://doi.org/10.7326/0003-4819-155-8-201110180-00009
R. Sadeghi, G. Treglia, Systematic reviews and meta-analyses of diagnostic studies: a practical guideline. Clin. Transl. Imaging 5, 83–87 (2017). https://doi.org/10.1007/s40336-016-0219-2
C. Amadou, G. Bera, M. Ezziane et al. 18F-fluorocholine PET/CT and parathyroid 4D computed tomography for primary hyperparathyroidism: the challenge of reoperative patients. World J. Surg. 43, 1232–1242 (2019). https://doi.org/10.1007/s00268-019-04910-6
I. Christakis, S. Khan, G.P. Sadler et al. 18Fluorocholine PET/CT scanning with arterial phase-enhanced CT is useful for persistent/recurrent primary hyperparathyroidism: first UK case series results. Ann. R. Coll. Surg. Engl. 101, 501–507 (2019). https://doi.org/10.1308/rcsann.2019.0059
L.A. Boccalatte, N.L. Gómez, M. Musumeci et al. 18F-choline PET/4D CT in hyperparathyroidism: correlation between biochemical data and study parameters. Rev. Esp. Med Nucl. Imagen Mol. 39, 273–278 (2020). https://doi.org/10.1016/j.remn.2020.03.017
V. Pretet, M. Rotania, M. Helali et al. 18F-Fluorocholine PET and multiphase CT integrated in dual modality PET/4D-CT for preoperative evaluation of primary hyperparathyroidism. J. Clin. Med 9, 2005 (2020). https://doi.org/10.3390/jcm9062005. Jun 26
L.A. Boccalatte, F. Higuera, N.L. Gómez et al. Usefulness of 18F-Fluorocholine positron emission tomography–computed tomography in locating lesions in hyperparathyroidism: a systematic review. JAMA Otolaryngol. Head. Neck Surg. 145, 743–750 (2019). https://doi.org/10.1001/jamaoto.2019.0574
G. Treglia, P. Trimboli, M. Huellner et al. Imaging in primary hyperparathyroidism: focus on the evidence-based diagnostic performance of different methods. Minerva Endocrinol. 43, 133–143 (2018). https://doi.org/10.23736/S0391-1977.17.02685-2
S. Fakhran, B.F. Branstetter, D.A. Pryma, Parathyroid imaging. Neuroimaging Clin. N. Am. 18, 537–549 (2008). https://doi.org/10.1016/j.nic.2008.03.006
Author contributions
A.P.: contributed to the conception of the study, acquired and analyzed data, drafting the manuscript. G.B.: contributed to the conception of the study, analyzed data, drafting the manuscript. L.B.: contributed to the acquisition and analysis of data. C.C.: contributed to the acquisition and analysis of data. M.M.: contributed to the acquisition and analysis of data. L.B.: contributed to design of the study and revised the manuscript. C.C.: contributed to the acquisition and analysis of data. M.U. contributed to the acquisition and analysis of data. F.F.: contributed to design of the study and revised the manuscript. P.T. revised the manuscript critically for important intellectual content.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Piccardo, A., Bottoni, G., Boccalatte, L.A. et al. Head-to-head comparison among 18F-choline PET/CT, 4D contrast-enhanced CT, and 18F-choline PET/4D contrast-enhanced CT in the detection of hyperfunctioning parathyroid glands: a systematic review and meta-analysis. Endocrine 74, 404–412 (2021). https://doi.org/10.1007/s12020-021-02798-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12020-021-02798-8