Skip to main content

Advertisement

Log in

Tumour and pelvic lymph node metabolic activity on FDG-PET/CT to stratify patients for para-aortic surgical staging in locally advanced cervical cancer

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

The aim of our study was to comprehensively evaluate the most valuable metabolic parameters of cervical tumours and pelvic lymph nodes (PLN) by FDG-PET/CT to predict para-aortic lymph node (PALN) metastasis and stratify patients for surgical staging.

Methods

The study included patients with locally advanced cervical cancer, negative PALN uptake on preoperative FDG-PET/CT, and para-aortic lymphadenectomy. Two senior nuclear medicine physicians expert in gynaecologic oncology reviewed all PET/CT exams, and extracted tumour SUVmax, MTV, and TLG, as well as PLN. Prognostic parameters of PALN involvement were identified using ROC curves and logistic regression analysis.

Results

One hundred and twenty-five consecutive locally advanced cervical cancer patients were included. The FDG-PET/CT false-negative rate was, respectively, 27.7% (13/47) and 5.1% (4/78) in patients with and without FDG-PET/CT PLN uptake. The AUC of cervical tumour size, SUVmax, MTV, and TLG was, respectively, 0.75 (0.62–0.87), 0.59 (0.44–0.76), 0.75 (0.60–0.90), and 0.71 (0.56–0.86). The AUC of PLN size, SUVmax, SUVmean, PLN SUVmax/Tumour SUVmax ratio, MTV, and TLG was, respectively, 0.57 (0.37–0.78), 0.82 (0.68–0.95), 0.77 (0.61–0.94), 0.85 (0.72–0.98), 0.69 (0.51–0.87), and 0.74 (0.57–0.91). The metabolic parameter showing the best trade-off between sensitivity and specificity to predict PALN involvement was the ratio between PLN and tumour SUVmax.

Conclusion

The risk of PALN metastasis in FDG-PET/CT negative PLN patients is very low, so para-aortic lymphadenectomy does not seem justified. In patients with preoperative PLN uptake on FDG-PET/CT, surgical staging led to treatment modification in more than 25% of cases and should therefore be performed. Patients with more than one positive PLN and high PLN metabolic activity are at high risk of para-aortic extension and recurrence. Further prospective evaluation is required to consider intensified treatment modalities without prior PALN dissection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Global Cancer Observatory, OMS. Estimated number of incident cases, worldwide ( top 10 cancer sites ) in 2012. Dispon. sur http//gco.iarc.fr/today/online-analysis-multi-bars?mode=cancer&mode_population=continents&population=900&sex=2&cancer=16&type=0&statistic=0&prevalence=0&color_palette=default. Accessed 2017. p. 2012

  2. Quinn M a, Benedet JL, Odicino F, Maisonneuve P, Beller U, Creasman WT, et al. Carcinoma of the cervix uteri. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet. 2006;95(Suppl 1):S43–103.

    Article  Google Scholar 

  3. Marth C, Landoni F, Mahner S, McCormack M, Gonzalez-Martin A, Colombo N. Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28:iv72–83.

    Article  CAS  Google Scholar 

  4. Chuang LT, Temin S, Camacho R, Feldman S, Gultekin M, Gupta V, et al. Management and care of women with invasive cervical cancer: American Society of Clinical Oncology resource-stratified clinical practice guideline. J Glob Oncol. 2016;2:1–30.

    Article  Google Scholar 

  5. Yu W, Kou C, Bai W, Yu X, Duan R, Zhu B, et al. The diagnostic performance of PET / CT scans for the detection of para-aortic metastatic lymph nodes in patients with cervical cancer : a meta-analysis. PloS One. 2019;14(7):e0220080. https://doi.org/10.1371/journal.pone.0220080.

  6. Gouy S, Morice P, Narducci F, Uzan C, Gilmore J, Kolesnikov-Gauthier H, et al. Nodal-staging surgery for locally advanced cervical cancer in the era of PET. Lancet Oncol. 2012;13:e212–20.

    Article  Google Scholar 

  7. Gouy S, Morice P, Narducci F, Uzan C, Martinez A, Rey A, et al. Prospective multicenter study evaluating the survival of patients with locally advanced cervical cancer undergoing laparoscopic para-aortic lymphadenectomy before chemoradiotherapy in the era of positron emission tomography imaging. J Clin Oncol. 2013;31:3026–33.

    Article  Google Scholar 

  8. Cibula D, Pötter R, Planchamp F, Avall-lundqvist E, Fischerova D, Haie C, et al. The European Society of Gynaecological Oncology / European Society for Radiotherapy and Oncology / European Society of Pathology guidelines for the management of patients with cervical cancer. Radiother Oncol. 2019;127:404–16 Available from: https://doi.org/10.1016/j.radonc.2018.03.003.

    Article  Google Scholar 

  9. Brockbank E, Kokka F, Bryant A, Pomel C, Reynolds K. Pre-treatment surgical para-aortic lymph node assessment in locally advanced cervical cancer ( review ). Cochrane Database Syst Rev. 2013;(3):CD008217. https://doi.org/10.1002/14651858.CD008217.pub3.

  10. Kidd EA, Siegel BA, Dehdashti F. The standardized uptake value for F-18 fluorodeoxyglucose is a sensitive predictive biomarker for cervical cancer treatment response and survival. Cancer. 2007;110(8):1738–44. https://doi.org/10.1002/cncr.22974.

  11. Sarker A, Im H-J, Cheon GJ, Chung HH, Kang KW, Chung J-K, et al. Prognostic implications of the SUVmax of primary tumors and metastatic lymph node measured by 18F-FDG PET in patients with uterine cervical cancer. A meta-analysis. Clin Nucl Med. 2016;41(1):34–40. https://doi.org/10.1097/RLU.0000000000001049.

  12. Voglimacci M, Gabiache E, Lusque A, Ferron G, Ducassou A, Querleu D, et al. Chemoradiotherapy for locally advanced cervix cancer without aortic lymph node involvement : can we consider metabolic parameters of pretherapeutic FDG-PET / CT for treatment tailoring ? Eur J Nucl Med Mol Imaging. 2019;46(7):1551–9. https://doi.org/10.1007/s00259-018-4219-5.

  13. Onal C, Reyhan M, Parlak C, Guler OC, Oymak E. Prognostic value of pretreatment F-18-fluorodeoxyglucose uptake in patients with cervical cancer treated with definitive chemoradiotherapy. Int J Gynecol Cancer. 2013;23:1104–10.

    Article  Google Scholar 

  14. Vural GU, Akkas BE, Demirel BB. Standardized uptake value and metabolic tumor volume measured by 18 F FDG PET / CT are sensitive biomarkers for the presence of lymph node metastasis in patients with cervical carcinoma. Rev Esp Med Nucl Imagen Mol. 2014;33:268–73.

    CAS  PubMed  Google Scholar 

  15. Kidd EA, Siegel BA, Dehdashti F, Grigsby PW. Pelvic lymph node F-18 fluorodeoxyglucose uptake as a prognostic biomarker in newly diagnosed patients with locally advanced cervical cancer. 2010;116(6):1469–1475. https://doi.org/10.1002/cncr.24972.

  16. Onal C, Guler OC, Reyhan M, Fuat A. Prognostic value of 18 F-fluorodeoxyglucose uptake in pelvic lymph nodes in patients with cervical cancer treated with definitive chemoradiotherapy. Gynecol Oncol. 2015;137:40–6.

    Article  Google Scholar 

  17. Chung HH, Cheon GJ, Kang KW, Kim JW, Park N-H, Song YS. Preoperative PET / CT FDG standardized uptake value of pelvic lymph nodes as a significant prognostic factor in patients with uterine cervical cancer. Eur J Nucl Med Mol Imaging. 2014;41(4):674–81.

  18. Sonoda Y, Leblanc E, Querleu D, Castelain B, Papageorgiou TH, Lambaudie E, et al. Prospective evaluation of surgical staging of advanced cervical cancer via a laparoscopic extraperitoneal approach. Gynecol Oncol. 2003;91:326–31.

    Article  CAS  Google Scholar 

  19. Boellaard R, Delgado-Bolton R, Oyen WJG, Giammarile F, Tatsch K, Eschner W, et al. FDG PET / CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42:328–54.

    Article  CAS  Google Scholar 

  20. Gold MA, Tian C, Whitney CW, Rose PG, Lanciano R. Surgical versus radiographic determination of para-aortic lymph node metastases before chemoradiation for locally advanced cervical carcinoma. Cancer. 2008;112(9):1954–63. https://doi.org/10.1002/cncr.23400.

  21. Havrilesky LJ, Kulasingam SL, Matchar DB, Myers ER. FDG-PET for management of cervical and ovarian cancer. Gynecol Oncol. 2005;97:183–91.

    Article  Google Scholar 

  22. Marth C, Landoni F, Mahner S, McCormack M, Gonzalez-Martin A, Colombo N. Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28:iv72–83.

    Article  CAS  Google Scholar 

  23. Leblanc E, Gauthier H, Querleu D, Ferron G, Zerdoud S, Morice P, et al. Accuracy of 18-Fluoro-2-deoxy-d-glucose positron emission tomography in the pretherapeutic detection of occult para-aortic node involvement in patients with a locally advanced cervical carcinoma. Ann Surg Oncol. 2011;18:2302–9.

    Article  CAS  Google Scholar 

  24. Gouy S, Morice P, Narducci F, Uzan C, Martinez A, Rey A, et al. Prospective multicenter study evaluating the survival of patients with locally advanced cervical cancer undergoing laparoscopic para-aortic lymphadenectomy before chemoradiotherapy in the era of positron emission tomography. J Clin Oncol. 2013;31(24):3026–33. https://doi.org/10.1200/JCO.2012.47.3520.

  25. Vergote I, Tsolakidis D, Mortier D, Neven P, Amant F, Mottaghy F, et al. Value of positron emission tomography of the para-aortic lymph nodes in cervical carcinoma stage IB2-IIIB. J Clin Oncol. 2008;26:5654–5 Available from: http://ascopubs.org/doi/10.1200/JCO.2008.19.5883. Accessed 2008

    Article  Google Scholar 

  26. Imaging PPPET, Leblanc E, Katdare N, Narducci F, Bresson L, Gouy S, et al. Should Systematic Infrarenal Para-aortic Dissection Be the Rule in the Pretherapeutic Staging of Primary or Recurrent Locally Advanced Cervix Cancer Patients With a Negative Preoperative Para-aortic PET Imaging?. Int J Gynecol Cancer. 2016;26:169–75.

    Article  Google Scholar 

  27. Han X, Wen H, Ju X, Chen X, Ke G. Predictive factors of para-aortic lymph nodes metastasis in cervical cancer patients: a retrospective analysis based on 723 para-aortic lymphadenectomy cases. Onctarget. 2017;8:51840–7.

    Google Scholar 

  28. Chung HH, Kim JW, Han KH, Eo JS, Kang KW, Park N-H, et al. Prognostic value of metabolic tumor volume measured by FDG-PET/CT in patients with cervical cancer. Gynecol Oncol. 2011;120:270–4 Available from: https://linkinghub.elsevier.com/retrieve/pii/S0090825810007985. Accessed 2011.

    Article  Google Scholar 

  29. Hong JH, Min KJ, Lee JK, So KA, Jung US, Kim S, et al. Prognostic value of the sum of metabolic tumor volume of primary tumor and lymph nodes using 18F-FDG PET/CT in patients with cervical cancer. Medicine (Baltimore). 2016;95:e2992 Available from: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00005792-201603010-00074. Accessed 2016.

    Article  CAS  Google Scholar 

  30. Chung HH. Prognostic importance of lymph node-to-primary tumor standardized uptake value ratio in invasive squamous cell carcinoma of uterine cervix. Eur J Nucl Med Mol Imaging. 2017;44(11):1862–9. https://doi.org/10.1007/s00259-017-3729-x.

  31. Brunette LL, Bonyadlou S, Ji L, Groshen S, Shuster D, Mehta A, et al. Predictive value of FDG PET / CT to detect lymph node metastases in cervical cancer. Clin Nucl Med. 2018;43:793–801.

    Article  Google Scholar 

  32. Shen W-C, Chen S-W, Liang J-A, Hsieh T-C, Yen K-Y, Kao C-H. [18]Fluorodeoxyglucose positron emission tomography for the textural features of cervical cancer associated with lymph node metastasis and histological type. Eur J Nucl Med Mol Imaging. 2017;44:1721–31 Available from: http://link.springer.com/10.1007/s00259-017-3697-1.

    Article  Google Scholar 

  33. Varia MA, Bundy BN, Deppe G, Mannel R, Averette HE, Rose PG, et al. Cervical carcinoma metastatic to para-aortic nodes: extended field radiation therapy with concomitant 5-fluorouracil and cisplatin chemotherapy: a gynecologic oncology group study. Int J Radiat Oncol. 1998;42:1015–23 Available from: https://linkinghub.elsevier.com/retrieve/pii/S0360301698002673.

    Article  CAS  Google Scholar 

  34. Pomel C, Martinez A, Bourgin C, Beguinot M, Benoit C, Naik R, et al. Survival effect of laparoscopic para-aortic staging in locally advanced cervical cancer : a retrospective cohort analysis. BJOG. 2017;124(7):1089–94. https://doi.org/10.1111/1471-0528.14492.

  35. Lai C, Huang K, Hong J, Lee C, Chou H, Chang T, et al. Randomized trial of surgical staging ( extraperitoneal or laparoscopic ) versus clinical staging in locally advanced cervical cancer. Gynecol Oncol. 2003;89:160–7.

    Article  Google Scholar 

  36. Uzan C, Souadka A, Gouy S, Debaere T, Duclos J, Lumbroso J, et al. Analysis of morbidity and clinical implications of laparoscopic para-aortic lymphadenectomy in a continuous series of 98 patients with advanced-stage cervical cancer and negative PET-CT imaging in the para-aortic area. Oncologist. 2011;16:1021–7 Available from: http://theoncologist.alphamedpress.org/cgi/doi/10.1634/theoncologist.2011-0007.

    Article  Google Scholar 

  37. Manders DB, Sims TT, Bailey A, Hwang L, Richardson DL, Miller DS, et al. The Significance of Para-Aortic Nodal Size and the Sole of Adjuvant Systemic Chemotherapy in Cervical Cancer: An Institutional Experience. Am J Clin Oncol. 2018;41:1225–30.

    Article  Google Scholar 

  38. Sapienza LG, Fernando V, Jr MML, Baiocchi G, Janeiro D, Sloan M, et al. HHS Public Access 2018;144:312–7.

  39. Duen A. Phase III, Open-label, randomized study comparing concurrent gemcitabine plus cisplatin and radiation followed by adjuvant gemcitabine and cisplatin versus concurrent cisplatin and radiation in patients with stage IIB to. J Clin Oncol. 2019;29(13):1678–85. https://doi.org/10.1200/JCO.2009.25.9663.

Download references

Acknowledgements

Martina Aida Angeles acknowledges grant support from “La Caixa” Foundation, Barcelona, Spain. We would also like to thank Dr. Gail Taillefer, a native English speaker experienced in scientific publication, for her review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Martinez.

Ethics declarations

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. Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Oncology – Genitourinary

Electronic supplementary material

ESM 1

(DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinez, A., Voglimacci, M., Lusque, A. et al. Tumour and pelvic lymph node metabolic activity on FDG-PET/CT to stratify patients for para-aortic surgical staging in locally advanced cervical cancer. Eur J Nucl Med Mol Imaging 47, 1252–1260 (2020). https://doi.org/10.1007/s00259-019-04659-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00259-019-04659-z

Keywords

Navigation