Advertisement

Journal of Gastrointestinal Surgery

, Volume 22, Issue 4, pp 722–730 | Cite as

The Added Diagnostic Value of 18F-Fluorodihydroxyphenylalanine PET/CT in the Preoperative Work-Up of Small Bowel Neuroendocrine Tumors

  • Pietro Addeo
  • Gilles Poncet
  • Bernard Goichot
  • Loic Leclerc
  • Cécile Brigand
  • Didier Mutter
  • Benoit Romain
  • Izzie-Jacques Namer
  • Philippe Bachellier
  • Alessio Imperiale
Original Article

Abstract

Background

The precise localization of the primary tumor and/or the identification of multiple primary tumors improves the preoperative work-up in patients with small bowel (SB) neuroendocrine tumor (NET). The present study assesses the diagnostic value of 18F-fluorodihydroxyphenylalanine (18F-FDOPA) positron emission tomography/computed tomography (PET/CT) during the preoperative wok-up of SB NETs.

Methods

Between January 2010 and June 2017, all consecutive patients with SB NETs undergoing preoperative 18F-FDOPA PET/CT and successive resection were analyzed. Preoperative work-up included computed tomography (CT), somatostatin receptor scintigraphy (SRS), and 18F-FDOPA PET/CT. Sensitivity and accuracy ratio for primary and multiple tumor detection were compared with data from surgery and pathology.

Results

There were 17 consecutive patients with SB NETs undergoing surgery. Nine patients (53%) had multiple tumors, 15 (88%) metastatic lymph nodes, 3 (18%) peritoneal carcinomatosis, and 9 patients (53%) liver metastases. A total of 70 SB NETs were found by pathology. Surgery identified the primary in 17/17 (100%) patients and recognized seven of 9 patients (78%) with multiple synchronous SB. Preoperatively, 18F-FDOPA PET/CT displayed a statistically significant higher sensitivity for primary tumor localization (100 vs. 23.5 vs. 29.5%) and multiple tumor detection (78 vs. 22 vs. 11%) over SRS and CT. Compared with pathology, 18F-FDOPA PET/CT displayed the highest accuracy ratio for number of tumor detected over CT and SRS (2.0 ± 2.2 vs. 0.4 ± 0.7 vs. 0.6 ± 1.5, p = 0.0003).

Conclusion

18F-FDOPA PET/CT significantly increased the sensitivity and accuracy for primary and multiple SB NET identification. 18F-FDOPA PET/CT should be included systematically in the preoperative work-up of SB NET.

Keywords

Neuroendocrine tumors Small bowel carcinoid 18F-FDOPA PET/CT Multiple tumors 

Notes

Acknowledgements

The authors thank Gerlinde Averous, MD, and Marie Pierrette Chenard, MD, from the Department of Pathology, University Hospitals of Strasbourg, for pathological examinations of surgical specimens.

Author Contribution

Substantial contributions to the conception or design of the work: PA, GP, BG, LL, CB, DM, BR, IJN, PB, and AI.

Acquisition, analysis, or interpretation of data for the work; PA, GP, BG, LL, CB, DM, BR, IJN, PB, and AI.

Drafting the work or revising it critically for important intellectual content: PA, GP, BG, LL, CB, DM, BR, IJN, PB, and AI.

Final approval of the version to be published: PA, GP, BG, LL, CB, DM, BR, IJN, PB, and AI.

Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: PA, GP, BG, LL, CB, DM, BR, IJN, PB, and AI.

References

  1. 1.
    Wang SC, Parekh JR, Zuraek MB, et al. Identification of unknown primary tumors in patients with neuroendocrine liver metastases. Arch Surg. 2010;145:276–280.CrossRefPubMedGoogle Scholar
  2. 2.
    Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9:61–72.CrossRefPubMedGoogle Scholar
  3. 3.
    Capurso G, Rinzivillo M, Bettini R, Boninsegna L, Delle Fave G, Falconi M. Systematic review of resection of primary midgut carcinoid tumour in patients with unresectable liver metastases. Br J Surg. 2012;99:1480–1486.CrossRefPubMedGoogle Scholar
  4. 4.
    Partelli S, Bartsch DK, Capdevila J, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology. 2017;105:255–265.Google Scholar
  5. 5.
    Yantiss RK, Odze RD, Farraye FA, Rosenberg AE. Solitary versus multiple carcinoid tumors of the ileum. A clinical and pathologic review of 68 cases. Am J Surg Pathol. 2003; 27:811–817.CrossRefPubMedGoogle Scholar
  6. 6.
    Bonekamp D, Raman SP, Horton KM, Fishman EK. Role of computed tomography angiography in detection and staging of small bowel carcinoid tumors. World J Radiol. 2015;7:220–235.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Yamagishi H, Fukui H, Shirakawa K, et al. Early diagnosis and successful treatment of small-intestinal carcinoid tumor: useful combination of capsule endoscopy and double-balloon endoscopy. Endoscopy. 2007;39 Suppl 1:E243-E244.CrossRefPubMedGoogle Scholar
  8. 8.
    Pasquier A, Walter T, Hervieu V, et al. Surgical management of small bowel neuroendocrine tumors: specific requirements and their impact on staging and prognosis. Ann Surg Oncol. 2015;22 suppl 3:742–749.CrossRefGoogle Scholar
  9. 9.
    Santhanam P, Chandramahanti S, Kroiss A, et al. Nuclear imaging of neuroendocrine tumors with unknown primary: why, when and how? Eur J Nucl Med Mol Imaging. 2015;42:1144–1155.CrossRefPubMedGoogle Scholar
  10. 10.
    Deroose CM, Hindié E, Kebebew E, et al. Molecular imaging of gastroenteropancreatic neuroendocrine tumors: current status and future directions. J Nucl Med. 2016;57:1949–1956.CrossRefPubMedGoogle Scholar
  11. 11.
    Koopmans KP, de Vries EG, Kema IP, et al. Staging of carcinoid tumours with 18FDOPA PET: a prospective, diagnostic accuracy study. Lancet Oncol. 2006;7:728–734.CrossRefPubMedGoogle Scholar
  12. 12.
    Imperiale A, Rust E, Gabriel S, et al. 18F-fluorodihydroxyphenylalanine PET/CT in patients with neuroendocrine tumors of unknown origin: relation to tumor origin and differentiation. J Nucl Med. 2014;55:367–372.CrossRefPubMedGoogle Scholar
  13. 13.
    Imperiale A, Averous G, Chilinseva-Natorov N, et al. Unknown multifocal ileal carcinoid revealed by (18)F-FDOPA PET/CT. J Clin Endocrinol Metab. 2014;99:1510–1511.CrossRefPubMedGoogle Scholar
  14. 14.
    Helali M, Heimburger C, Rohr S, Goichot B, Imperiale A. Small Bowel Carcinoid: The “Dancing Bowel Sign” on 18FFDOPA PET/CT Clin Nucl Med. 2016;41:944–945.CrossRefPubMedGoogle Scholar
  15. 15.
    Sei Y, Zhao X, Forbes J, et al. A hereditary form of small intestinal carcinoid associated with a germline mutation in inositol polyphosphate multikinase. Gastroenterology. 2015;149:67–78.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Ambrosini V, Tomassetti P, Rubello D, et al. Role of 18F-dopa PET/CT imaging in the management of patients with 111In-pentetreotide negative GEP tumours. Nucl Med Commun. 2007;28:473–477.CrossRefPubMedGoogle Scholar
  17. 17.
    Jager PL, Chirakal R, Marriott CJ, Brouwers AH, Koopmans KP, Gulenchyn KY. 6-L-18F-fluorodihydroxyphenylalanine PET in neuroendocrine tumors: basic aspects and emerging clinical applications. J Nucl Med. 2008;49:573–586.CrossRefPubMedGoogle Scholar
  18. 18.
    Fiebrich HB, de Jong JR, Kema IP, et al. Total (18)F-dopa PET tumour uptake reflects metabolic endocrine tumour activity in patients with a carcinoid tumour. Eur J Nucl Med Mol Imaging. 2011;38:1854–1861.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Sadowski SM, Neychev V, Millo C et al. Prospective study of 68Ga-DOTATATE positron emission tomography/computed tomography for detecting gastro-entero-pancreatic neuroendocrine tumors and unknown primary sites. J Clin Oncol. 2016;34:588–596.7CrossRefPubMedGoogle Scholar
  20. 20.
    Strosberg JR, Weber JM, Feldman M, Coppola D, Meredith K, Kvols LK. Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors. J Clin Oncol. 2013;3:420–425.CrossRefGoogle Scholar
  21. 21.
    Bartlett EK, Roses RE, Gupta M, et al. Surgery for metastatic neuroendocrine tumors with occult primaries. J Surg Res. 2013;184:221–227.CrossRefPubMedGoogle Scholar
  22. 22.
    Hoffman EJ, Huang SC, Phelps ME. Quantitation in positron emission computed tomography: 1. Effect of object size. J Comput Assist Tomogr 1979;3:299–308.CrossRefPubMedGoogle Scholar
  23. 23.
    Pasquer A, Walter T, Rousset P, et al. Lymphadenectomy during small bowel neuroendocrine tumor surgery: the concept of skip metastases. Ann Surg Oncol. 2016;23:804–808.CrossRefPubMedGoogle Scholar
  24. 24.
    Ethun CG, Postlewait LM, Baptiste GG, et al. Small bowel neuroendocrine tumors: a critical analysis of diagnostic work-up and operative approach. J Surg Oncol. 2016;114:671–676.CrossRefPubMedGoogle Scholar
  25. 25.
    Figueiredo MN, Maggiori L, Gaujoux S, et al. Surgery for small-bowel neuroendocrine tumors: is there any benefit of the laparoscopic approach? Surg Endosc. 2014;28:1720–1726.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2017

Authors and Affiliations

  • Pietro Addeo
    • 1
  • Gilles Poncet
    • 2
  • Bernard Goichot
    • 3
  • Loic Leclerc
    • 4
  • Cécile Brigand
    • 5
  • Didier Mutter
    • 6
  • Benoit Romain
    • 5
  • Izzie-Jacques Namer
    • 7
    • 8
  • Philippe Bachellier
    • 1
  • Alessio Imperiale
    • 7
    • 8
  1. 1.Hepato-Pancreato-Biliary Surgery and Liver Transplantation, Pôle des Pathologies Digestives, Hépatiques et de la Transplantation, Hautepierre University Hospital, University Hospitals of StrasbourgUniversity of StrasbourgStrasbourgFrance
  2. 2.Digestive and Oncologic Surgery, Edouard-Herriot University HospitalClaude-Bernard Lyon 1 UniversityLyonFrance
  3. 3.Internal Medicine, Hautepierre University Hospital, University Hospitals of StrasbourgUniversity of StrasbourgStrasbourgFrance
  4. 4.Radiology, Hautepierre University Hospital, University Hospitals of StrasbourgUniversity of StrasbourgStrasbourgFrance
  5. 5.Digestive and General Surgery, Hautepierre University Hospital, University Hospitals of StrasbourgUniversity of StrasbourgStrasbourgFrance
  6. 6.General, Digestive, and Endocrine Surgery, IRCAD-IHUUniversity of StrasbourgStrasbourgFrance
  7. 7.Department of Biophysics and Nuclear Medicine, Hautepierre University Hospital, University Hospitals of StrasbourgUniversity of StrasbourgStrasbourg Cedex 09France
  8. 8.ICube, Faculty of MedicineUniversity of Strasbourg/CNRS (UMR 7357) and FMTSStrasbourgFrance

Personalised recommendations