Quantitative perfusion imaging of neoplastic liver lesions: A multi-institution study

Shivani Pahwa, Hao Liu, Yong Chen, Sara Dastmalchian, Gregory O'Connor, Ziang Lu, Chaitra Badve, Alice Yu, Katherine Wright, Hamid Chalian, Shengxiang Rao, Caixia Fu, Ignacio Vallines, Mark Griswold, Nicole Seiberlich, Mengsu Zeng, Vikas Gulani, Shivani Pahwa, Hao Liu, Yong Chen, Sara Dastmalchian, Gregory O'Connor, Ziang Lu, Chaitra Badve, Alice Yu, Katherine Wright, Hamid Chalian, Shengxiang Rao, Caixia Fu, Ignacio Vallines, Mark Griswold, Nicole Seiberlich, Mengsu Zeng, Vikas Gulani

Abstract

We describe multi-institutional experience using free-breathing, 3D Spiral GRAPPA-based quantitative perfusion MRI in characterizing neoplastic liver masses. 45 patients (age: 48-72 years) were prospectively recruited at University Hospitals, Cleveland, USA on a 3 Tesla (T) MRI, and at Zhongshan Hospital, Shanghai, China on a 1.5 T MRI. Contrast-enhanced volumetric T1-weighted images were acquired and a dual-input single-compartment model used to derive arterial fraction (AF), distribution volume (DV) and mean transit time (MTT) for the lesions and normal parenchyma. The measurements were compared using two-tailed Student's t-test, with Bonferroni correction applied for multiple-comparison testing. 28 hepatocellular carcinoma (HCC) and 17 metastatic lesions were evaluated. No significant difference was noted in perfusion parameters of normal liver parenchyma and neoplastic masses at two centers (p = 0.62 for AF, 0.015 for DV, 0.42 for MTT for HCC, p = 0.13 for AF, 0.97 for DV, 0.78 for MTT for metastases). There was statistically significant difference in AF, DV, and MTT of metastases and AF and DV of HCC compared to normal liver parenchyma (p < 0.5/9 = 0.0055). A statistically significant difference was noted in the MTT of metastases compared to hepatocellular carcinoma (p < 0.001*10-5). In conclusion, 3D Spiral-GRAPPA enabled quantitative free-breathing perfusion MRI exam provides robust perfusion parameters.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Perfusion modeling in a patient with metastatic breast cancer. Arterial and portal input function (a), concentration-time curve of the lesion and surrounding tissue (b) for the lesion depicted in T1-weighted image (c). Perfusion modeling revealed the lesion to have an arterial fraction of 95.3%, distribution volume of 48.0% and mean transit time of 96.6 seconds. The corresponding values for the liver parenchyma were arterial fraction of 16.9%, distribution volume of 30.8% and mean transit time of 5.2 seconds.
Figure 2
Figure 2
(a) Standard arterial phase VIBE image depicts an irregular liver contour in a patient with cirrhosis on surveillance for hepatocellular carcinoma- no focal lesion is seen. (b) Spiral DCE acquisition performed 12 days after the clinical study depicts three arterially enhancing lesions. These lesions were detected in the follow up clinical exam performed 3 months after the first exam (c).
Figure 3
Figure 3
Liver perfusion maps for a patient with hepatocellular carcinoma. Free breathing spiral DCE images averaged over 9 frames show the lesion in arterial (a), venous (b) and delayed phases (c). Corresponding liver perfusion maps depict arterial fraction of 77% (d), distribution volume of 45% (e) and mean transit time of 12 seconds (f).
Figure 4
Figure 4
Liver perfusion maps for a patient with metastatic carcinoma lung. Axial CT image shows three hypodense lesions (a). Corresponding liver perfusion maps depict arterial fraction (b), distribution volume (c) and mean transit time (d).

References

    1. Elsayes KM, et al. Focal hepatic lesions: diagnostic value of enhancement pattern approach with contrast-enhanced 3D gradient-echo MR imaging. Radiographics. 2005;25:1299–1320. doi: 10.1148/rg.255045180.
    1. Ichikawa T, et al. Detection and characterization of focal liver lesions: a Japanese phase III, multicenter comparison between gadoxetic acid disodium-enhanced magnetic resonance imaging and contrast-enhanced computed tomography predominantly in patients with hepatocellular carcinoma and chronic liver disease. Investigative radiology. 2010;45:133–141. doi: 10.1097/RLI.0b013e3181caea5b.
    1. Semelka RC, Martin DR, Balci C, Lance T. Focal liver lesions: comparison of dual-phase CT and multisequence multiplanar MR imaging including dynamic gadolinium enhancement. Journal of magnetic resonance imaging: JMRI. 2001;13:397–401. doi: 10.1002/jmri.1057.
    1. O’Connor JP, Jackson A, Parker GJ, Jayson GC. DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. British journal of cancer. 2007;96:189–195. doi: 10.1038/sj.bjc.6603515.
    1. O’Connor JP, Jackson A, Parker GJ, Roberts C, Jayson GC. Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies. Nature reviews. Clinical oncology. 2012;9:167–177. doi: 10.1038/nrclinonc.2012.2.
    1. O’Connor JP, et al. Imaging biomarker roadmap for cancer studies. Nature reviews. Clinical oncology. 2017;14:169–186. doi: 10.1038/nrclinonc.2016.162.
    1. Chandarana H, et al. Estimating liver perfusion from free-breathing continuously acquired dynamic gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced acquisition with compressed sensing reconstruction. Investigative radiology. 2015;50:88–94. doi: 10.1097/RLI.0000000000000105.
    1. Chandarana H, et al. Free-breathing radial 3D fat-suppressed T1-weighted gradient echo sequence: a viable alternative for contrast-enhanced liver imaging in patients unable to suspend respiration. Investigative radiology. 2011;46:648–653. doi: 10.1097/RLI.0b013e31821eea45.
    1. Chen Y, et al. Free-breathing liver perfusion imaging using 3-dimensional through-time spiral generalized autocalibrating partially parallel acquisition acceleration. Investigative radiology. 2015;50:367–375. doi: 10.1097/RLI.0000000000000135.
    1. Feng L, et al. XD-GRASP: Golden-angle radial MRI with reconstruction of extra motion-state dimensions using compressed sensing. Magn Reson Med. 2016;75:775–788. doi: 10.1002/mrm.25665.
    1. Feng L, et al. Golden-angle radial sparse parallel MRI: combination of compressed sensing, parallel imaging, and golden-angle radial sampling for fast and flexible dynamic volumetric MRI. Magn Reson Med. 2014;72:707–717. doi: 10.1002/mrm.24980.
    1. Materne R, et al. Assessment of hepatic perfusion parameters with dynamic MRI. Magn Reson Med. 2002;47:135–142. doi: 10.1002/mrm.10045.
    1. Jones RA, Haraldseth O, Muller TB, Rinck PA, Oksendal AN. K-space substitution: a novel dynamic imaging technique. Magn Reson Med. 1993;29:830–834. doi: 10.1002/mrm.1910290618.
    1. Song T, et al. Optimal k-space sampling for dynamic contrast-enhanced MRI with an application to MR renography. Magn Reson Med. 2009;61:1242–1248. doi: 10.1002/mrm.21901.
    1. Bultman EM, et al. Quantitative hepatic perfusion modeling using DCE-MRI with sequential breathholds. Journal of magnetic resonance imaging: JMRI. 2014;39:853–865. doi: 10.1002/jmri.24238.
    1. Rao SX, Chen CZ, Liu H, Zeng MS, Qu XD. Three-dimensional whole-liver perfusion magnetic resonance imaging in patients with hepatocellular carcinomas and colorectal hepatic metastases. BMC gastroenterology. 2013;13:53. doi: 10.1186/1471-230X-13-53.
    1. Thng CH, Koh TS, Collins DJ, Koh DM. Perfusion magnetic resonance imaging of the liver. World journal of gastroenterology. 2010;16:1598–1609. doi: 10.3748/wjg.v16.i13.1598.
    1. Wang J, Chen LT, Tsang YM, Liu TW, Shih TT. Dynamic contrast-enhanced MRI analysis of perfusion changes in advanced hepatocellular carcinoma treated with an antiangiogenic agent: a preliminary study. AJR. American journal of roentgenology. 2004;183:713–719. doi: 10.2214/ajr.183.3.1830713.
    1. Morgan B, et al. Dynamic contrast-enhanced magnetic resonance imaging as a biomarker for the pharmacological response of PTK787/ZK 222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases, in patients with advanced colorectal cancer and liver metastases: results from two phase I studies. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2003;21:3955–3964. doi: 10.1200/JCO.2003.08.092.
    1. Mross K, et al. Phase I clinical and pharmacokinetic study of PTK/ZK, a multiple VEGF receptor inhibitor, in patients with liver metastases from solid tumours. European journal of cancer (Oxford, England: 1990) 2005;41:1291–1299. doi: 10.1016/j.ejca.2005.03.005.
    1. Posey JA, et al. A phase I study of anti-kinase insert domain-containing receptor antibody, IMC-1C11, in patients with liver metastases from colorectal carcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research. 2003;9:1323–1332.
    1. Reardon DA, et al. Phase I study of AEE788, a novel multitarget inhibitor of ErbB- and VEGF-receptor-family tyrosine kinases, in recurrent glioblastoma patients. Cancer chemotherapy and pharmacology. 2012;69:1507–1518. doi: 10.1007/s00280-012-1854-6.
    1. Vriens D, et al. Chemotherapy response monitoring of colorectal liver metastases by dynamic Gd-DTPA-enhanced MRI perfusion parameters and 18F-FDG PET metabolic rate. Journal of nuclear medicine: official publication, Society of Nuclear Medicine. 2009;50:1777–1784. doi: 10.2967/jnumed.109.064790.
    1. Smith SM, et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23(Suppl 1):S208–219. doi: 10.1016/j.neuroimage.2004.07.051.
    1. Abdullah SS, et al. Characterization of hepatocellular carcinoma and colorectal liver metastasis by means of perfusion MRI. Journal of magnetic resonance imaging: JMRI. 2008;28:390–395. doi: 10.1002/jmri.21429.
    1. Breedis C, Young G. The blood supply of neoplasms in the liver. The American journal of pathology. 1954;30:969–977.
    1. Chen BB, Shih TT. DCE-MRI in hepatocellular carcinoma-clinical and therapeutic image biomarker. World journal of gastroenterology. 2014;20:3125–3134. doi: 10.3748/wjg.v20.i12.3125.
    1. Miyazaki K, et al. Neuroendocrine tumor liver metastases: use of dynamic contrast-enhanced MR imaging to monitor and predict radiolabeled octreotide therapy response. Radiology. 2012;263:139–148. doi: 10.1148/radiol.12110770.
    1. Chen BB, et al. Dynamic Contrast-enhanced MR Imaging of Advanced Hepatocellular Carcinoma: Comparison with the Liver Parenchyma and Correlation with the Survival of Patients Receiving Systemic Therapy. Radiology. 2016;281:983. doi: 10.1148/radiol.2016164030.
    1. Lin G, Lunderquist A, Hagerstrand I, Boijsen E. Postmortem examination of the blood supply and vascular pattern of small liver metastases in man. Surgery. 1984;96:517–526.
    1. Koh TS, et al. Hepatic metastases: in vivo assessment of perfusion parameters at dynamic contrast-enhanced MR imaging with dual-input two-compartment tracer kinetics model. Radiology. 2008;249:307–320. doi: 10.1148/radiol.2483071958.
    1. Taouli B, et al. Hepatocellular carcinoma: perfusion quantification with dynamic contrast-enhanced MRI. AJR. American journal of roentgenology. 2013;201:795–800. doi: 10.2214/AJR.12.9798.
    1. Cuenod C, et al. Early changes in liver perfusion caused by occult metastases in rats: detection with quantitative CT. Radiology. 2001;218:556–561. doi: 10.1148/radiology.218.2.r01fe10556.
    1. Krinsky GA, et al. Transplantation for hepatocellular carcinoma and cirrhosis: sensitivity of magnetic resonance imaging. Liver transplantation: official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society. 2002;8:1156–1164. doi: 10.1053/jlts.2002.35670.
    1. Pandharipande PV, Krinsky GA, Rusinek H, Lee VS. Perfusion imaging of the liver: current challenges and future goals. Radiology. 2005;234:661–673. doi: 10.1148/radiol.2343031362.
    1. Yokoyama N, et al. Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: preliminary results of a prospective study. Cancer. 2012;118:2813–2819. doi: 10.1002/cncr.26594.
    1. Yokoyama N, et al. Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer. 2002;94:1642–1647. doi: 10.1002/cncr.10422.
    1. Van Beers BE, et al. Hepatic perfusion parameters in chronic liver disease: dynamic CT measurements correlated with disease severity. AJR. American journal of roentgenology. 2001;176:667–673. doi: 10.2214/ajr.176.3.1760667.

Source: PubMed

3
Abonnieren