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Imaging strategy in recurrent ovarian cancer: a practical review

  • Lucia Manganaro
  • Silvia Gigli
  • Amanda Antonelli
  • Matteo Saldari
  • Federica Tomao
  • Claudia Marchetti
  • Emanuela Anastasi
  • Andrea Laghi
Article

Abstract

Ovarian cancer is one of the most aggressive gynaecologic malignancies in women worldwide. The lack of proper screening programs and the characteristic abdominal spreading with minimal clinical symptoms give rise of its high lethality. Most patients show advanced disease at diagnosis and have a poor prognosis. The surveillance of ovarian cancer patients after initial treatment is a challenging question in clinical practice and there is no consensus in literature about the most appropriate follow-up strategy for these women. The role of Imaging has become increasingly important, allowing to properly monitor patients, distinguishing the different relapse patterns, thus guiding the correct management and therapy. In this review, we report and analyze the scientific evidence about the role of the different imaging modalities now available in the follow-up strategy and management of Epithelial Ovarian Cancer patients with recurrent disease.

Keywords

Recurrent ovarian cancer Ovarian cancer follow-up Recurrent ovarian cancer imaging US CT MRI 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, et al. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:359–386CrossRefGoogle Scholar
  2. 2.
    Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ (2002) Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 20:1248–1259CrossRefPubMedGoogle Scholar
  3. 3.
    Chi DS, Eisenhauer EL, Lang J, et al. (2006) What is the optimal goal of primary cytoreductive surgery for bulky stage IIIC epithelial ovarian carcinoma (EOC)? Gynecol Oncol 103:559–564CrossRefPubMedGoogle Scholar
  4. 4.
    Hennessy BT, Coleman RL, Markman M (2009) Ovarian cancer. Lancet 374:1371–1382CrossRefPubMedGoogle Scholar
  5. 5.
    Heintz APM, Odicino F, Maisonneuve P, et al. (2006) Carcinoma of the ovary. Int J Gynecol Obstet 95:161–192CrossRefGoogle Scholar
  6. 6.
    Dao MD, Alwan LM, Gray HJ, et al. (2013) Recurrence patterns after extended treatment with bevacizumab for ovarian, fallopian tube, and primary peritoneal cancers. Gynecol Oncol 130:295–299.  https://doi.org/10.1016/j.ygyno.2013.04.055 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Tsumura N, Sakuragi N, Hareyama H, et al. (1998) Distribution pattern and risk factors of pelvic and para-aortic lymph node metastasis in epithelial ovarian carcinoma. Int J Cancer 79:526–530CrossRefPubMedGoogle Scholar
  8. 8.
    Kimio U (2009) Treatment for recurrent ovarian cancer—at first relapse. J Oncol 2010:497429Google Scholar
  9. 9.
    Usami T, Kato K, Taniguchi T, et al. (2014) Recurrence patterns of advanced ovarian, fallopian tube, and peritoneal cancers after complete cytoreduction during interval debulking surgery. Int J Gynecol Cancer 24:991–996CrossRefPubMedGoogle Scholar
  10. 10.
    Pignata S, Cannella L, Leopardo D, Bruni GS, Facchini G (2011) Pisano C (2011) Follow-up with CA125 after primary therapy of advanced ovarian cancer: in favor of continuing to prescribe CA125 during follow-up. Ann Oncol 22:viii40–viii44.  https://doi.org/10.1093/annonc/mdr470 CrossRefPubMedGoogle Scholar
  11. 11.
    Mitchell DG, Javitt MC, Glanc P, et al. (2013) American college of radiology. ACR appropriateness criteria staging and follow-up of ovarian cancer. J Am Coll Radiol 10:822–827CrossRefPubMedGoogle Scholar
  12. 12.
    Diaz-Gil D, Fintelmann FJ, Molaei S, et al. (2016) Prediction of 5-year survival in advanced-stage ovarian cancer patients based on computed tomography peritoneal carcinomatosis index. Abdom Radiol 41:2196–2202CrossRefGoogle Scholar
  13. 13.
    Wrobel JK, Toborek M (2016) Blood-brain barrier remodeling during brain metastasis formation. Mol Med .  https://doi.org/10.2119/molmed.2015.00207 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Zola P, Macchi C, Cibula D, et al. (2015) Follow-up in gynecological malignancies a state of art. Int J Gynecol Cancer 25:1151–1164.  https://doi.org/10.1097/IGC.0000000000000498 CrossRefPubMedGoogle Scholar
  15. 15.
    Testa AC, Fruscella E, Ludovisi M, et al. (2005) The role of sonographic examination in the follow-up of gynecological neo- plasms. Gynecol Oncol 99:696–703CrossRefPubMedGoogle Scholar
  16. 16.
    Gadducci A, Cosio S (2009) Surveillance of patients after initial treatment of ovarian cancer. Crit Rev Oncol Hematol 71:43–52CrossRefPubMedGoogle Scholar
  17. 17.
    Zikan M, Fischerova D, Pinkavova I, Dundr P, Cibula D (2010) Ultrasound-guided tru-cut biopsy of abdominal and pelvic tumors in gynecology. Ultrasound Obstet Gynecol 36:767–772CrossRefPubMedGoogle Scholar
  18. 18.
    Kinkel K, Hricak H, Lu Y, Tsuda K, Filly RA (2000) US characterization of ovarian masses: a meta-analysis. Radiology 217:803–811CrossRefPubMedGoogle Scholar
  19. 19.
    Testa AC, Di Legge A, Virgilio B, et al. (2014) Which imaging technique should we use in the follow up of gynaecological cancer? Best Pract Res Clin Obs Gyn 28:769–791CrossRefGoogle Scholar
  20. 20.
    Hanbidge AE, Lynch D, Wilson SR (2003) US of the peritoneum. RadioGraphics 23:663–685CrossRefPubMedGoogle Scholar
  21. 21.
    Woodward PJ, Hosseinzadeh K, Saenger JS (2004) Radiologic staging of ovarian carcinoma with pathologic correlation. RadioGraphics 24:225–246CrossRefPubMedGoogle Scholar
  22. 22.
    Kawamoto S, Urban BA, Fishman EK (1999) CT of epithelial ovarian tumors. RadioGraphics 19:S85–S102CrossRefPubMedGoogle Scholar
  23. 23.
    Urban BA, Fishman EK (1995) Spiral CT of the female pelvis: clinical applications. Abdom Imaging 20:9–14CrossRefPubMedGoogle Scholar
  24. 24.
    Pannu HK, Bristow RE, Montz FJ, Fishman EK (2003) Multidetector CT of peritoneal carcinomatosis from ovarian cancer. RadioGraphics 23:687–701CrossRefPubMedGoogle Scholar
  25. 25.
    Forstner R, Sala E, Kinkel K, Spencer JA (2010) European society of urogenital radiology. ESUR guidelines: ovarian cancer staging and follow-up. Eur Radiol 20:2773–2780CrossRefPubMedGoogle Scholar
  26. 26.
    Kurtz AB, Tsimikas JV, Tempany CM, et al. (1999) Diagnosis and staging of ovarian cancer: comparative values of Doppler and conventional US, CT, and MR imaging correlated with surgery and histopathologic analysis—report of the Radiology Diagnostic Oncology Group. Radiology 212:19–27CrossRefPubMedGoogle Scholar
  27. 27.
    Arai K, Makino H, Morioka T, et al. (1993) Enhancement of ascites on MRI following intravenous administration of Gd-DTPA. J Comput Assist Tomogr 17:617–622CrossRefPubMedGoogle Scholar
  28. 28.
    Kim CK, Park BK, Choi JY, Kim BG, Han H (2007) Detection of recurrent ovarian cancer at MRI: comparison with integrated PET/CT. J Comput Assist Tomogr 6:868–875CrossRefGoogle Scholar
  29. 29.
    Low RN, Duggan B, Barone RM, et al. (2005) Treated ovarian cancer: MR imaging, laparotomy reassessment, and serum CA-125 values compared with clinical outcome at 1 year. Radiology 235:918–926CrossRefPubMedGoogle Scholar
  30. 30.
    Hameeduddin A, Sahdev A (2015) Diffusion-weighted imaging and dynamic contrast-enhanced MRI in assessing response and recurrent disease in gynaecological malignancies. Cancer Imaging 15:3.  https://doi.org/10.1186/s40644-015-0037-1 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Ricke J, Sehouli J, Hach C, et al. (2003) Prospective evaluation of contrast-enhanced MRI in the depiction of peritoneal spread in primary or recurrent ovarian cancer. Eur Radiol 13:943–949CrossRefPubMedGoogle Scholar
  32. 32.
    Sala E, Rockall AG, Freeman SJ, et al. (2013) The Added Role of MR Imaging in Treatment Stratification of Patients with Gynecologic Malignancies: what the Radiologist Needs to Know. Radiology 266:717–740.  https://doi.org/10.1148/radiol.12120315 CrossRefPubMedGoogle Scholar
  33. 33.
    Michielsen KL, Vergote I, Dresen R, et al. (2016) Whole-body diffusion-weighted magnetic resonance imaging in the diagnosis of recurrent ovarian cancer: a clinical feasibility study. Br J Radiol 89(1067):20160468CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Michielsen K, Dresen R, Vanslembrouck R, et al. (2017) Diagnostic value of whole body diffusion-weighted MRI compared to computed tomography for pre-operative assessment of patients suspected for ovarian cancer. Eur J Cancer 83:88–98CrossRefPubMedGoogle Scholar
  35. 35.
    Kyriazi S, Collins DJ, Morgan VA, Giles SL, deSouza NM (2010) Diffusion-weighted imaging of peritoneal disease for noninvasive staging of advanced ovarian cancer. RadioGraphics. 30:1269–1285.  https://doi.org/10.1148/rg.305105073 CrossRefPubMedGoogle Scholar
  36. 36.
    Fehniger J, Thomas S, Lengyel E, et al. (2016) A prospective study evaluating diffusion weighted magnetic resonance imaging (DW-MRI) in the detection of peritoneal carcinomatosis in suspected gynecologic malignancies. Gynecol Oncol 142:169e75CrossRefGoogle Scholar
  37. 37.
    Espada M, Garcia-Flores JR, Jimenez M, et al. (2013) Diffusion-weighted magnetic resonance imaging evaluation of intraabdominal sites of implants to predict likelihood of suboptimal cytoreductive surgery in patients with ovarian carcinoma. Eur Radiol 23(2636):e42Google Scholar
  38. 38.
    Nakai G, Matsuki M, Yn Inada, et al. (2008) Detection and evaluation of pelvic lymph nodes in patients with gynecologic malignancies using body diffusion-weighted magnetic resonance imaging. J Comput Assist Tomogr 32:764–768CrossRefPubMedGoogle Scholar
  39. 39.
    Lin G, Ho KC, Wang JJ, et al. (2008) Detection of lymph node metastasis in cervical and uterine cancers by diffusion-weighted magnetic resonance imaging at 3T. J Magn Reson Imaging 28:128–135CrossRefPubMedGoogle Scholar
  40. 40.
    Kim JK, Kim KA, Park BW, et al. (2008) Feasibility of diffusion-weighted imaging in the differentiation of metastatic from nonmetastatic lymph nodes: early experience. Magn Reson Imaging 28:714–719CrossRefGoogle Scholar
  41. 41.
    Park SO, Kim JK, Kim KA, et al. (2009) Relative apparent diffusion coefficient: determination of reference site and validation of benefit for detecting metastatic lymph nodes in uterine cervical cancer. J Magn Reson Imaging 29:383–390CrossRefPubMedGoogle Scholar
  42. 42.
    Levy A, Medjhoul A, Caramella C, et al. (2011) Interest of diffusion-weighted echo-planar MR imaging and apparent diffusion coefficient mapping in gynecological malignancies: a review. J Magn Reson Imaging 33:1020–1027.  https://doi.org/10.1002/jmri.22546 CrossRefPubMedGoogle Scholar
  43. 43.
    Clavo AC, Brown RS, Wahl RL (1995) Fluorodeoxyglucose uptake in human cancer cell lines is increased by hypoxia. J Nucl Med 36:1625–1632PubMedGoogle Scholar
  44. 44.
    Fularz M, Adamiak P, Czepczyński R, et al. (2010) Clinical value of FDG PET/CT in the diagnosis of suspected recurrent ovarian cancer: is there an impact of FDG PET/CT on patient management? Eur J Nucl Med Mol Imaging 37:1259–1269CrossRefGoogle Scholar
  45. 45.
    Cho SM, Ha HK, Byun JY, et al. (2002) Usefulness of FDG PET for assessment of early recurrent epithelial ovarian cancer. AJR Am J Roentgenol. 179:391–395CrossRefPubMedGoogle Scholar
  46. 46.
    Kim TH, Kim J, Kang YK, et al. (2017) Identification of metabolic biomarkers using serial 18F-FDG PET/CT for prediction of recurrencein advanced epithelial ovarian cancer. Transl Oncol 10:297–303.  https://doi.org/10.1016/j.tranon.2017.02.001 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Gu P, Pan LL, Wu SQ, et al. (2009) CA 125, PET alone, PET-CT, CT and MRI in diagnosing recurrent ovarian carcinoma: a systematic review and meta-analysis. Eur J Radiol 71:164–174CrossRefPubMedGoogle Scholar
  48. 48.
    Satoh Y, Ichikawa T, Motosugi U, et al. (2011) Diagnosis of peritoneal dissemination: comparison of 18F-FDG PET/CT, diffusion-weighted MRI, and contrast-enhanced MDC. AJR 196:447–453CrossRefPubMedGoogle Scholar
  49. 49.
    Suppiah S, Chang WL, Hassan HA, et al. (2017) Systematic review on the accuracy of positron emission tomography/computed tomography and positron emission tomography/magnetic resonance imaging in the management of ovarian cancer: is functional information really needed? World J Nucl Med 16:176–185CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Limei Z, Yong C, Yan X, et al. (2013) Accuracy of positron emission tomography/computed tomography in the diagnosis and restaging for recurrent ovarian cancer: a meta-analysis. Int J Gynecol Cancer 23:598–607.  https://doi.org/10.1097/IGC.0b013e31828a183c CrossRefPubMedGoogle Scholar
  51. 51.
    Yuan Y, Gu ZX, Tao XF, Liu SY (2012) Computed tomography, magnetic resonance imaging, and positron emission tomography or positron emission tomography/computer tomography for detection of metastatic lymph nodes in patients with ovarian cancer: a meta-analysis. Eur J Radiol 81:1002–1006CrossRefPubMedGoogle Scholar
  52. 52.
    Sebastian S, Lee SI, Horowitz NS, et al. (2008) PET–CT vs. CT alone in ovarian cancer recurrence. Abdom Imaging 33:112–118.  https://doi.org/10.1007/s00261-007-9218-0 CrossRefPubMedGoogle Scholar
  53. 53.
    Cook GJR (2010) PET and PET/CT imaging of skeletal metastases. Cancer Imaging 10:153–160.  https://doi.org/10.1102/1470-7330.2010.0022 CrossRefPubMedCentralGoogle Scholar
  54. 54.
    Mangili G, Picchio M, Sironi S, et al. (2007) Integrated PET/CT as a first-line re-staging modality in patients with suspected recurrence of ovarian cancer. Eur J Nucl Med Mol Imaging 34(5):658–666.  https://doi.org/10.1007/s00259-006-0306-0 CrossRefPubMedGoogle Scholar
  55. 55.
    Simcock B, Neesham D, Quinn M, et al. (2006) The impact of PET/CT in the management of recurrent ovarian cancer. Gynecol Oncol 103(1):271–276CrossRefPubMedGoogle Scholar
  56. 56.
    Fulham MJ, Carter J, Baldey A, et al. (2009) The impact of PET-CT in suspected recurrent ovarian cancer: a prospective multi-centre study as part of the Australian PET Data Collection Project. Gynecol Oncol 112(3):462–468.  https://doi.org/10.1016/j.ygyno.2008.08.027 CrossRefPubMedGoogle Scholar
  57. 57.
    Han EJ, Park HL, Lee YS, et al. (2016) Clinical usefulness of post-treatment FDG PET/CT in patients with ovarian malignancy. Ann Nucl Med 30(9):600–607CrossRefPubMedGoogle Scholar
  58. 58.
    Schwenzer NF, Schmidt H, Gatidis S, et al. (2014) Measurement of apparent diffusion coefficient with simultaneous MR/positron emission tomography in patients with peritoneal carcinomatosis: comparison with 18F-FDG-PET. J Magn Reson Imaging 40:1121–1128.  https://doi.org/10.1002/jmri.24497 CrossRefPubMedGoogle Scholar
  59. 59.
    Subhas N, Patel PV, Pannu HK, et al. (2005) Imaging of pelvic malignancies with in-line FDG PET-CT: case examples and common pitfalls of FDG PET. RadioGraphics 25:1031–1043CrossRefPubMedGoogle Scholar
  60. 60.
    Levy T, Weiser R, Boaz M, et al. (2013) The significance of the pattern of serum CA125 level ascent to above the normal range in epithelial ovarian, primary peritoneal and tubal carcinoma patients. Gynecol Oncol 129:165–168CrossRefPubMedGoogle Scholar
  61. 61.
    Song MJ, Lee SH, Choi MR, et al. (2013) Diagnostic value of CA125 as a predictor of recurrence in advanced ovarian cancer. Eur J Gynaecol Oncol 34:148–151PubMedGoogle Scholar
  62. 62.
    Zimny M, Siggelkow W, Schröder W, et al. (2001) 2-[Fluorine-18]-fluoro-2-deoxy-d-glucose positron emission tomography in the diagnosis of recurrent ovarian cancer. Gynecol Oncol 83:310–315CrossRefPubMedGoogle Scholar
  63. 63.
    Sheng XG, Zhang XL, Fu Z, et al. (2007) Value of positron emission tomography-CT imaging combined with continual detection of CA125 in serum for diagnosis of early asymptomatic recurrence of epithelial ovarian carcinoma. Zhonghua Fu Chan Ke Za Zhi 42:460–463PubMedGoogle Scholar
  64. 64.
    Evangelista L, Palma MD, Gregianin M, et al. (2015) Diagnostic and prognostic evaluation of fluorodeoxyglucose positron emission tomography/computed tomography and its correlation with serum cancer antigen-125 (CA125) in a large cohort of ovarian cancer patients. J Turk Ger Gynecol Assoc 16:137–144CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Catalano OA, et al. (2013) Clinical impact of PET/MR imaging in patients with cancer undergoing same-day PET/CT: initial experience in 134 patients—a hypothesis-generating exploratory study. Radiology 269:857–869.  https://doi.org/10.1148/radiol.13131306 CrossRefPubMedGoogle Scholar
  66. 66.
    Drzezga A (2012) First clinical experience with integrated whole body PET/MR: comparison to PET/CT in patients with oncologic diagnoses. J Nucl Med 53:845–855.  https://doi.org/10.2967/jnumed.111.09860 CrossRefPubMedGoogle Scholar
  67. 67.
    Parikh N, Friedman KP, Shah SN, Chandarana H (2015) Practical guide for implementing hybrid PET/MR clinical service: lessons learned from our experience. Abdom Imaging 40:1366–1373.  https://doi.org/10.1007/s00261-015-0444-6 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Grueneisen J, Schaarschmidt BM, Heubner M, et al. (2015) Implementation of FAST-PET/MRI for whole-body staging of female patients with recurrent pelvic malignancies: a comparison to PET/CT. Eur J Radiol 84:2097–2102CrossRefPubMedGoogle Scholar
  69. 69.
    Salani R, Khanna N, Frimer M, et al. (2017) An update on post-treatment surveillance and diagnosis of recurrence in women with gynecologic malignancies: Society of Gynecologic Oncology (SGO) recommendations. Gynecol Oncol 146:3–10CrossRefPubMedGoogle Scholar
  70. 70.
    Morgan RJ, Alvarez RD, Armstrong DK, et al. (2013) Ovarian cancer, version 2.2013. J Natl Compr Cancer Netw 11:1199–1209CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Lucia Manganaro
    • 1
  • Silvia Gigli
    • 1
  • Amanda Antonelli
    • 1
  • Matteo Saldari
    • 1
  • Federica Tomao
    • 2
  • Claudia Marchetti
    • 2
  • Emanuela Anastasi
    • 3
  • Andrea Laghi
    • 4
  1. 1.Department of Radiological, Oncological and Pathological Science, Umberto I Hospital“La Sapienza” University of RomeRomeItaly
  2. 2.Department of Gynaecological, Obstetrical and Urological Science, Umberto I Hospital“La Sapienza” University of RomeRomeItaly
  3. 3.Department of Molecular MedicineUmberto I Hospital, “La Sapienza” University of RomeRomeItaly
  4. 4.Department of Radiological, Oncological and Pathological Science, Sant’Andrea Hospital“La Sapienza” University of RomeRomeItaly

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