Advertisement

Clinical and Translational Imaging

, Volume 7, Issue 4, pp 237–253 | Cite as

Detection rate of radiolabelled choline PET or PET/CT in hepatocellular carcinoma: an updated systematic review and meta-analysis

  • Giovanni Signore
  • Marie Nicod-Lalonde
  • John O. Prior
  • Francesco Bertagna
  • Barbara Muoio
  • Luca Giovanella
  • Caterina Furlan
  • Giorgio TregliaEmail author
Meta-Analysis
  • 42 Downloads
Part of the following topical collections:
  1. Gastrointestinal tract

Abstract

Background

Different imaging methods have been used to detect hepatocellular carcinoma (HCC). As there are increasing literature data about the role of radiolabelled choline PET/CT in this setting, we aimed to perform an updated meta-analysis about the detection rate (DR) of this imaging method in HCC.

Methods

A comprehensive computer literature search of studies published through December 2018 in PubMed/MEDLINE, Embase and Cochrane library databases regarding the DR of radiolabelled choline PET or PET/CT in patients with HCC was carried out. Pooled DR were calculated on a per patient- and on a per lesion-based analysis. Subgroup analyses taking into account the radiopharmaceutical used were performed.

Results

Nine studies (283 HCC patients) were included in the pooled analysis. The pooled DR of radiolabelled choline PET or PET/CT on a per patient- and on a per lesion-based analysis was 83% [95% confidence interval (95% CI) 75–89%] and 79% (95% CI 72–86%), respectively. A significant heterogeneity among the studies was found on a per lesion-based analysis only. No significant publication bias was found. The subgroup analysis demonstrated a trend towards a higher DR when using 18F-choline compared to 11C-choline, without a statistically significant difference. Pooled DR of HCC using dual-tracer PET/CT (radiolabelled choline and 18F-FDG) on a per patient- and a per lesion-based analysis was 91% (95% CI 87–95%) and 89% (95% CI 80–95%), respectively, without significant heterogeneity.

Conclusions

Radiolabelled choline PET/CT demonstrated good ability in detecting HCC. The DR increased when dual-tracer PET/CT was performed. Large multicenter studies and cost-effectiveness analyses are warranted.

Keywords

PET Positron emission tomography Choline Hepatocellular carcinoma Liver Meta-analysis 

Notes

Funding

The authors declare that they have no financial or non-financial competing interests.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest relevant to this article.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Kulik L, El-Serag HB (2019) Epidemiology and management of hepatocellular carcinoma. Gastroenterology 156(2):477–491CrossRefGoogle Scholar
  2. 2.
    Lange N, Dufour JF (2019) Changing epidemiology of HCC: how to screen and identify patients at risk? Dig Dis Sci.  https://doi.org/10.1007/s10620-019-05515-8 Google Scholar
  3. 3.
    Ronot M, Purcell Y, Vilgrain V (2019) Hepatocellular carcinoma: current imaging modalities for diagnosis and prognosis. Dig Dis Sci 1:1.  https://doi.org/10.1007/s10620-019-05547-0 Google Scholar
  4. 4.
    Kornberg A, Friess H (2019) (18)F-fludeoxyglucose positron emission tomography for diagnosis of HCC: implications for therapeutic strategy in curative and non-curative approaches. Therap Adv Gastroenterol. 19(12):1756284819836205.  https://doi.org/10.1177/1756284819836205 Google Scholar
  5. 5.
    Treglia G, Sadeghi R, Del Sole A, Giovanella L (2014) Diagnostic performance of PET/CT with tracers other than F-18-FDG in oncology: an evidence-based review. Clin Transl Oncol 16(9):770–775CrossRefGoogle Scholar
  6. 6.
    Haug AR (2017) Imaging of primary liver tumors with positron-emission tomography. Q J Nucl Med Mol Imaging. 61(3):292–300Google Scholar
  7. 7.
    Treglia G, Giovannini E, Di Franco D, Calcagni ML, Rufini V, Picchio M, Giordano A (2012) 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(6):451–461CrossRefGoogle Scholar
  8. 8.
    Bertagna F, Bertoli M, Bosio G, Biasiotto G, Sadeghi R, Giubbini R, Treglia G (2014) Diagnostic role of radiolabelled choline PET or PET/CT in hepatocellular carcinoma: a systematic review and meta-analysis. Hepatol Int 8(4):493–500CrossRefGoogle Scholar
  9. 9.
    Treglia G, Piccardo A, Imperiale A, Strobel K, Kaufmann PA, Prior JO, Giovanella L (2019) 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(3):751–765CrossRefGoogle Scholar
  10. 10.
    Treglia G, Ceriani L, Sadeghi R, Giovacchini G, Giovanella L (2014) Relationship between prostate-specific antigen kinetics and detection rate of radiolabelled choline PET/CT in restaging prostate cancer patients: a meta-analysis. Clin Chem Lab Med 52(5):725–733CrossRefGoogle Scholar
  11. 11.
    McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, The PRISMA-DTA Group, Clifford T, Cohen JF, Deeks JJ, Gatsonis C, Hooft L, Hunt HA, Hyde CJ, Korevaar DA, Leeflang MMG, Macaskill P, Reitsma JB, Rodin R, Rutjes AWS, Salameh JP, Stevens A, Takwoingi Y, Tonelli M, Weeks L, Whiting P, Willis BH (2018) Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA 319(4):388–396CrossRefGoogle Scholar
  12. 12.
    Simera I, Moher D, Hoey J, Schulz KF, Altman DG (2010) A catalogue of reporting guidelines for health research. Eur J Clin Invest 40:35–53CrossRefGoogle Scholar
  13. 13.
    Sadeghi R, Treglia G (2017) Systematic reviews and meta-analyses of diagnostic studies: a practical guideline. Clin Transl Imaging 5:83–87CrossRefGoogle Scholar
  14. 14.
    Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155(8):529–536CrossRefGoogle Scholar
  15. 15.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558CrossRefGoogle Scholar
  16. 16.
    Harbord RM, Egger M, Sterne JA (2006) A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 25:3443–3457CrossRefGoogle Scholar
  17. 17.
    Chalaye J, Costentin CE, Luciani A, Amaddeo G, Ganne-Carrié N, Baranes L, Allaire M, Calderaro J, Azoulay D, Nahon P, Seror O, Mallat A, Soussan M, Duvoux C, Itti E, Nault JC (2018) Positron emission tomography/computed tomography with 18F-fluorocholine improve tumor staging and treatment allocation in patients with hepatocellular carcinoma. J Hepatol 69(2):336–344CrossRefGoogle Scholar
  18. 18.
    Tulin PE, Dolgushin MB, Odzharova AA, Mikhaylov AI, Medvedeva BM, Shiryaev SV, Dolgushin BI (2017) Perfusion CT and PET with 18F-FDG and 18F-FCh in the complex diagnosis of hepatocellular carcinoma. Eur J Hybrid Imaging 1(1):13CrossRefGoogle Scholar
  19. 19.
    Kwee SA, Sato MM, Kuang Y, Franke A, Custer L, Miyazaki K, Wong LL (2017) [(18)F]Fluorocholine PET/CT imaging of liver cancer: radiopathologic correlation with tissue phospholipid profiling. Mol Imaging Biol 19(3):446–455CrossRefGoogle Scholar
  20. 20.
    Kwee SA, Okimoto GS, Chan OT, Tiirikainen M, Wong LL (2016) Metabolic characteristics distinguishing intrahepatic cholangiocarcinoma: a negative pilot study of (18)F-fluorocholine PET/CT clarified by transcriptomic analysis. Am J Nucl Med Mol Imaging 6(1):73–83Google Scholar
  21. 21.
    Castilla-Lièvre MA, Franco D, Gervais P, Kuhnast B, Agostini H, Marthey L, Désarnaud S, Helal BO (2016) Diagnostic value of combining 11C-choline and 18F-FDG PET/CT in hepatocellular carcinoma. Eur J Nucl Med Mol Imaging 43(5):852–859CrossRefGoogle Scholar
  22. 22.
    Chotipanich C, Kunawudhi A, Promteangtrong C, Tungsuppawattanakit P, Sricharunrat T, Wongsa P (2016) Diagnosis of hepatocellular carcinoma Using C11 Choline PET/CT: comparison with F18 FDG, contrast enhanced MRI and MDCT. Asian Pac J Cancer Prev 17(7):3569–3573Google Scholar
  23. 23.
    Kwee SA, Wong LL, Hernandez BY, Chan OT, Sato MM, Tsai N (2015) Chronic liver disease and the detection of hepatocellular carcinoma by [(18)F]fluorocholine PET/CT. Diagnostics (Basel) 5(2):189–199CrossRefGoogle Scholar
  24. 24.
    Lopci E, Torzilli G, Poretti D, de Neto LJ, Donadon M, Rimassa L, Lanza E, Sabongi JG, Ceriani R, Personeni N, Palmisano A, Pedicini V, Comito T, Scorsetti M, Chiti A (2015) Diagnostic accuracy of 11C-choline PET/CT in comparison with CT and/or MRI in patients with hepatocellular carcinoma. Eur J Nucl Med Mol Imaging 42(9):1399–1407CrossRefGoogle Scholar
  25. 25.
    Bieze M, Klümpen HJ, Verheij J, Beuers U, Phoa SS, van Gulik TM, Bennink RJ (2014) Diagnostic accuracy of (18) F-methylcholine positron emission tomography/computed tomography for intra- and extrahepatic hepatocellular carcinoma. Hepatology 59(3):996–1006CrossRefGoogle Scholar
  26. 26.
    Fartoux L, Balogova S, Nataf V, Kerrou K, Huchet V, Rosmorduc O, Talbot JN (2012) A pilot comparison of 18F-fluorodeoxyglucose and 18F-fluorocholine PET/CT to predict early recurrence of unifocal hepatocellular carcinoma after surgical resection. Nucl Med Commun 33(7):757–765CrossRefGoogle Scholar
  27. 27.
    Wu HB, Wang QS, Li BY, Li HS, Zhou WL, Wang QY (2011) F-18 FDG in conjunction with 11C-choline PET/CT in the diagnosis of hepatocellular carcinoma. Clin Nucl Med 36(12):1092–1097CrossRefGoogle Scholar
  28. 28.
    Talbot JN, Fartoux L, Balogova S, Nataf V, Kerrou K, Gutman F, Huchet V, Ancel D, Grange JD, Rosmorduc O (2010) Detection of hepatocellular carcinoma with PET/CT: a prospective comparison of 18F-fluorocholine and 18F-FDG in patients with cirrhosis or chronic liver disease. J Nucl Med 51(11):1699–1706CrossRefGoogle Scholar
  29. 29.
    Yamamoto Y, Nishiyama Y, Kameyama R, Okano K, Kashiwagi H, Deguchi A, Kaji M, Ohkawa M (2008) Detection of hepatocellular carcinoma using 11C-choline PET: comparison with 18F-FDG PET. J Nucl Med 49(8):1245–1248CrossRefGoogle Scholar
  30. 30.
    Talbot JN, Gutman F, Fartoux L, Grange JD, Ganne N, Kerrou K, Grahek D, Montravers F, Poupon R, Rosmorduc O (2006) PET/CT in patients with hepatocellular carcinoma using [(18)F]fluorocholine: preliminary comparison with [(18)F]FDG PET/CT. Eur J Nucl Med Mol Imaging 33(11):1285–1289CrossRefGoogle Scholar
  31. 31.
    Lanza E, Donadon M, Felisaz P, Mimmo A, Chiti A, Torzilli G, Balzarini L, Lopci E (2017) Refining the management of patients with hepatocellular carcinoma integrating 11C-choline PET/CT scan into the multidisciplinary team discussion. Nucl Med Commun 38(10):826–836CrossRefGoogle Scholar
  32. 32.
    Kolthammer JA, Corn DJ, Tenley N, Wu C, Tian H, Wang Y, Lee Z (2011) PET imaging of hepatocellular carcinoma with 18F-fluoroethylcholine and 11C-choline. Eur J Nucl Med Mol Imaging 38(7):1248–1256CrossRefGoogle Scholar
  33. 33.
    Fraum TJ, Ludwig DR, Hope TA, Fowler KJ (2018) PET/MRI for gastrointestinal imaging: current clinical status and future prospects. Gastroenterol Clin N Am 47(3):691–714CrossRefGoogle Scholar

Copyright information

© Italian Association of Nuclear Medicine and Molecular Imaging 2019

Authors and Affiliations

  1. 1.School of MedicineSapienza University of RomeRomeItaly
  2. 2.Department of Nuclear Medicine and Molecular ImagingLausanne University HospitalLausanneSwitzerland
  3. 3.Faculty of Biology and MedicineUniversity of LausanneLausanneSwitzerland
  4. 4.Department of Nuclear MedicineUniversity of Brescia and Spedali Civili di BresciaBresciaItaly
  5. 5.Department of Internal MedicineEnte Ospedaliero CantonaleBellinzonaSwitzerland
  6. 6.Clinic of Nuclear Medicine and PET/CT Center, Imaging Institute of Southern SwitzerlandEnte Ospedaliero CantonaleBellinzona/LuganoSwitzerland
  7. 7.Faculty of MedicineUniversity of ZürichZurichSwitzerland
  8. 8.Department of Clinical MedicineSapienza University of RomeRomeItaly
  9. 9.Health Technology Assessment UnitEnte Ospedaliero CantonaleBellinzonaSwitzerland
  10. 10.Department of Tropical and Infectious DiseasesPoliclinico Umberto IRomeItaly

Personalised recommendations