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 PET/MRI in pancreatic and periampullary cancer: correlating diffusion-weighted imaging, MR spectroscopy and glucose metabolic activity with clinical stage and prognosis

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European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

To correlate the clinical stage and prognosis of pancreatic or periampullary cancer with the imaging biomarkers on diffusion-weighted imaging, magnetic resonance spectroscopy and glucose metabolic activity derived from integrated PET/MRI.

Methods

This prospective study was approved by the institutional review board and informed consent was obtained. The study group comprised 60 consecutive patients with pancreatic or periampullary cancer who underwent PET/MRI before treatment. The imaging biomarkers were the minimal apparent diffusion coefficient (ADCmin), choline levels, standardized uptake values, metabolic tumour volume (MTV), and total lesion glycolysis (TLG) of the tumours. The relationships between these biomarkers and clinical TNM stage were evaluated using the Pearson test and the Mann-Whitney U test. The area under the receiver operating characteristic curve (AUROC) was used to evaluate accuracy. The correlation between the imaging biomarker and progression-free survival (PFS) was investigated using the Cox proportional hazards model.

Results

ADCmin was significantly lower in N1 and TNM stage 3+ tumours. Choline levels significantly higher in T4 tumours. TLG was significantly higher in T4, N1 and TNM stage 3+ tumours. MTV was significantly higher in T4, N1, M1, and TNM stage 3+ tumours (all P < 0.05). The MTV/ADCmin ratio exhibited the highest AUROC for predicting T4, N1, M1, and advanced TNM stages tumours, and was an independent predictor of PFS (P = 0.018) after adjustment for age, sex, tumour size and stage.

Conclusion

The imaging biomarkers from integrated PET/MRI may predict clinical stage and PFS in patients with pancreatic or periampullary cancer.

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References

  1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–30.

    Article  PubMed  Google Scholar 

  2. Ma J, Jemal A. The rise and fall of cancer mortality in the USA: why does pancreatic cancer not follow the trend? Future Oncol. 2013;9:917–9.

    Article  CAS  PubMed  Google Scholar 

  3. Huellner MW, Appenzeller P, Kuhn FP, Husmann L, Pietsch CM, Burger IA, et al. Whole-body nonenhanced PET/MR versus PET/CT in the staging and restaging of cancers: preliminary observations. Radiology. 2014;273:859–69.

    Article  PubMed  Google Scholar 

  4. Fattahi R, Balci NC, Perman WH, Hsueh EC, Alkaade S, Havlioglu N, et al. Pancreatic diffusion-weighted imaging (DWI): comparison between mass-forming focal pancreatitis (FP), pancreatic cancer (PC), and normal pancreas. J Magn Reson Imaging. 2009;29:350–6.

    Article  PubMed  Google Scholar 

  5. Barral M, Taouli B, Guiu B, Koh DM, Luciani A, Manfredi R, et al. Diffusion-weighted MR imaging of the pancreas: current status and recommendations. Radiology. 2015;274:45–63.

    Article  PubMed  Google Scholar 

  6. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11:835–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Penet MF, Shah T, Bharti S, Krishnamachary B, Artemov D, Mironchik Y, et al. Metabolic imaging of pancreatic ductal adenocarcinoma detects altered choline metabolism. Clin Cancer Res. 2015;21:386–95.

    Article  CAS  PubMed  Google Scholar 

  8. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher-Sananikone E, et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell. 2012;149:656–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rakheja R, Chandarana H, DeMello L, Jackson K, Geppert C, Faul D, et al. Correlation between standardized uptake value and apparent diffusion coefficient of neoplastic lesions evaluated with whole-body simultaneous hybrid PET/MRI. AJR Am J Roentgenol. 2013;201:1115–9.

    Article  PubMed  Google Scholar 

  10. Schaarschmidt BM, Buchbender C, Nensa F, Grueneisen J, Gomez B, Kohler J, et al. Correlation of the apparent diffusion coefficient (ADC) with the standardized uptake value (SUV) in lymph node metastases of non-small cell lung cancer (NSCLC) patients using hybrid 18F-FDG PET/MRI. PLoS One. 2015;10, e0116277.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Baba S, Isoda T, Maruoka Y, Kitamura Y, Sasaki M, Yoshida T, et al. Diagnostic and prognostic value of pretreatment SUV in 18F-FDG/PET in breast cancer: comparison with apparent diffusion coefficient from diffusion-weighted MR imaging. J Nucl Med. 2014;55:736–42.

    Article  CAS  PubMed  Google Scholar 

  12. Shih IL, Yen RF, Chen CA, Chen BB, Wei SY, Chang WC, et al. Standardized uptake value and apparent diffusion coefficient of endometrial cancer evaluated with integrated whole-body PET/MR: correlation with pathological prognostic factors. J Magn Reson Imaging. 2015;42:1723–32. doi:10.1002/jmri.24932.

    Article  PubMed  Google Scholar 

  13. Grueneisen J, Beiderwellen K, Heusch P, Buderath P, Aktas B, Gratz M, et al. Correlation of standardized uptake value and apparent diffusion coefficient in integrated whole-body PET/MRI of primary and recurrent cervical cancer. PLoS One. 2014;9, e96751.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yu X, Lee EY, Lai V, Chan Q. Correlation between tissue metabolism and cellularity assessed by standardized uptake value and apparent diffusion coefficient in peritoneal metastasis. J Magn Reson Imaging. 2014;40:99–105.

    Article  PubMed  Google Scholar 

  15. Tozaki M, Hoshi K. 1H MR spectroscopy of invasive ductal carcinoma: correlations with FDG PET and histologic prognostic factors. AJR Am J Roentgenol. 2010;194:1384–90.

    Article  PubMed  Google Scholar 

  16. Yamaguchi T, Lee J, Uemura H, Sasaki T, Takahashi N, Oka T, et al. Prostate cancer: a comparative study of 11C-choline PET and MR imaging combined with proton MR spectroscopy. Eur J Nucl Med Mol Imaging. 2005;32:742–8.

    Article  CAS  PubMed  Google Scholar 

  17. Ma C, Liu L, Li J, Wang L, Chen LG, Zhang Y, et al. Apparent diffusion coefficient (ADC) measurements in pancreatic adenocarcinoma: a preliminary study of the effect of region of interest on ADC values and interobserver variability. J Magn Reson Imaging. 2016;43:407–13. doi:10.1002/jmri.25007.

    Article  PubMed  Google Scholar 

  18. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50 Suppl 1:122S–50.

  19. Romesser PB, Qureshi MM, Subramaniam RM, Sakai O, Jalisi S, Truong MT. A prognostic volumetric threshold of gross tumor volume in head and neck cancer patients treated with radiotherapy. Am J Clin Oncol. 2014;37:154–61.

    Article  CAS  PubMed  Google Scholar 

  20. Chirindel A, Alluri KC, Chaudhry MA, Wahl RL, Pawlik TM, Herman JM, et al. Prognostic value of FDG PET/CT-derived parameters in pancreatic adenocarcinoma at initial PET/CT staging. AJR Am J Roentgenol. 2015;204:1093–9.

    Article  PubMed  Google Scholar 

  21. Larson SM, Erdi Y, Akhurst T, Mazumdar M, Macapinlac HA, Finn RD, et al. Tumor treatment response based on visual and quantitative changes in global tumor glycolysis using PET-FDG imaging. The visual response score and the change in total lesion glycolysis. Clin Positron Imaging. 1999;2:159–71.

    Article  PubMed  Google Scholar 

  22. Shrikhande SV, Kleeff J, Reiser C, Weitz J, Hinz U, Esposito I, et al. Pancreatic resection for M1 pancreatic ductal adenocarcinoma. Ann Surg Oncol. 2007;14:118–27.

    Article  PubMed  Google Scholar 

  23. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.

    Article  CAS  PubMed  Google Scholar 

  24. Muraoka N, Uematsu H, Kimura H, Imamura Y, Fujiwara Y, Murakami M, et al. Apparent diffusion coefficient in pancreatic cancer: characterization and histopathological correlations. J Magn Reson Imaging. 2008;27:1302–8.

    Article  PubMed  Google Scholar 

  25. Wang Y, Chen ZE, Nikolaidis P, McCarthy RJ, Merrick L, Sternick LA, et al. Diffusion-weighted magnetic resonance imaging of pancreatic adenocarcinomas: association with histopathology and tumor grade. J Magn Reson Imaging. 2011;33:136–42.

    Article  CAS  PubMed  Google Scholar 

  26. Hayano K, Miura F, Amano H, Toyota N, Wada K, Kato K, et al. Correlation of apparent diffusion coefficient measured by diffusion-weighted MRI and clinicopathologic features in pancreatic cancer patients. J Hepatobiliary Pancreat Sci. 2013;20:243–8.

    Article  PubMed  Google Scholar 

  27. Niwa T, Ueno M, Ohkawa S, Yoshida T, Doiuchi T, Ito K, et al. Advanced pancreatic cancer: the use of the apparent diffusion coefficient to predict response to chemotherapy. Br J Radiol. 2009;82:28–34.

    Article  CAS  PubMed  Google Scholar 

  28. Kurosawa J, Tawada K, Mikata R, Ishihara T, Tsuyuguchi T, Saito M, et al. Prognostic relevance of apparent diffusion coefficient obtained by diffusion-weighted MRI in pancreatic cancer. J Magn Reson Imaging. 2015;42:1532–7. doi:10.1002/jmri.24939.

    Article  PubMed  Google Scholar 

  29. Lee JW, Kang CM, Choi HJ, Lee WJ, Song SY, Lee JH, et al. Prognostic value of metabolic tumor volume and total lesion glycolysis on preoperative 18F-FDG PET/CT in patients with pancreatic cancer. J Nucl Med. 2014;55:898–904.

    Article  PubMed  Google Scholar 

  30. Shi S, Ji S, Qin Y, Xu J, Zhang B, Xu W, et al. Metabolic tumor burden is associated with major oncogenomic alterations and serum tumor markers in patients with resected pancreatic cancer. Cancer Lett. 2015;360:227–33.

    Article  CAS  PubMed  Google Scholar 

  31. Xu HX, Chen T, Wang WQ, Wu CT, Liu C, Long J, et al. Metabolic tumour burden assessed by 18F-FDG PET/CT associated with serum CA19-9 predicts pancreatic cancer outcome after resection. Eur J Nucl Med Mol Imaging. 2014;41:1093–102.

    Article  CAS  PubMed  Google Scholar 

  32. Choi HJ, Lee JW, Kang B, Song SY, Lee JD, Lee JH. Prognostic significance of volume-based FDG PET/CT parameters in patients with locally advanced pancreatic cancer treated with chemoradiation therapy. Yonsei Med J. 2014;55:1498–506.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Dholakia AS, Chaudhry M, Leal JP, Chang DT, Raman SP, Hacker-Prietz A, et al. Baseline metabolic tumor volume and total lesion glycolysis are associated with survival outcomes in patients with locally advanced pancreatic cancer receiving stereotactic body radiation therapy. Int J Radiat Oncol Biol Phys. 2014;89:539–46.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sakane M, Tatsumi M, Kim T, Hori M, Onishi H, Nakamoto A, et al. Correlation between apparent diffusion coefficients on diffusion-weighted MRI and standardized uptake value on FDG-PET/CT in pancreatic adenocarcinoma. Acta Radiol. 2015;56:1034–41.

    Article  PubMed  Google Scholar 

  35. Soussan M, Cyrta J, Pouliquen C, Chouahnia K, Orlhac F, Martinod E, et al. Fluorine 18 fluorodeoxyglucose PET/CT volume-based indices in locally advanced non-small cell lung cancer: prediction of residual viable tumor after induction chemotherapy. Radiology. 2014;272:875–84.

    Article  PubMed  Google Scholar 

  36. Soret M, Bacharach SL, Buvat I. Partial-volume effect in PET tumor imaging. J Nucl Med. 2007;48:932–45.

    Article  PubMed  Google Scholar 

  37. Davison J, Mercier G, Russo G, Subramaniam RM. PET-based primary tumor volumetric parameters and survival of patients with non-small cell lung carcinoma. AJR Am J Roentgenol. 2013;200:635–40.

    Article  PubMed  Google Scholar 

  38. Chang KP, Tsang NM, Liao CT, Hsu CL, Chung MJ, Lo CW, et al. Prognostic significance of 18F-FDG PET parameters and plasma Epstein-Barr virus DNA load in patients with nasopharyngeal carcinoma. J Nucl Med. 2012;53:21–8.

    Article  CAS  PubMed  Google Scholar 

  39. Dibble EH, Alvarez AC, Truong MT, Mercier G, Cook EF, Subramaniam RM. 18F-FDG metabolic tumor volume and total glycolytic activity of oral cavity and oropharyngeal squamous cell cancer: adding value to clinical staging. J Nucl Med. 2012;53:709–15.

    Article  CAS  PubMed  Google Scholar 

  40. Tesiram YA, Lerner M, Stewart C, Njoku C, Brackett DJ. Utility of nuclear magnetic resonance spectroscopy for pancreatic cancer studies. Pancreas. 2012;41:474–80.

    Article  PubMed  Google Scholar 

  41. Yao X, Zeng M, Wang H, Fei S, Rao S, Ji Y. Metabolite detection of pancreatic carcinoma by in vivo proton MR spectroscopy at 3T: initial results. Radiol Med. 2012;117:780–8.

    Article  CAS  PubMed  Google Scholar 

  42. Ahn SJ, Park MS, Lee JD, Kang WJ. Correlation between 18F-fluorodeoxyglucose positron emission tomography and pathologic differentiation in pancreatic cancer. Ann Nucl Med. 2014;28:430–5.

    Article  PubMed  Google Scholar 

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Correspondence to Tiffany Ting-Fang Shih.

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Funding

The study was funded by National Taiwan University Hospital, Taipei, Taiwan; Contract grant number: A1 project no. NTUH103-A124.

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None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Institutional Research Committee and with the principles of the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

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

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Chen, BB., Tien, YW., Chang, MC. et al.  PET/MRI in pancreatic and periampullary cancer: correlating diffusion-weighted imaging, MR spectroscopy and glucose metabolic activity with clinical stage and prognosis. Eur J Nucl Med Mol Imaging 43, 1753–1764 (2016). https://doi.org/10.1007/s00259-016-3356-y

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  • DOI: https://doi.org/10.1007/s00259-016-3356-y

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