To observe and assess the diagnostic value of contrast-enhanced ultrasound (CEUS) in patients with iso-/hypervascular solid pancreatic lesions.
METHODS:
70 pancreatic lesions (all confirmed by surgery or biopsy pathology) that manifested iso-/hyperenhancement on CEUS were retrospectively studied from January 2018 to January 2022, including 24 pancreatic ductal adenocarcinomas (PDAC), 15 mass-forming pancreatitis (MFP), 24 pancreatic neuroendocrine tumors (PNET) (14 hyper-PNETs, 10 iso-PNETs), and 7 solid pseudopapillary tumors of pancreas (SPTP). 65 pancreatic ductal adenocarcinomas (PDAC) that manifested hypoenhancement on CEUS were retrospectively studied from January 2020 to January 2022. CEUS patterns and the clinical and pathologic features were analyzed, and the diagnostic ability of CEUS for iso/hyperenhanced solid pancreatic lesions was assessed.
RESULTS:
Centripetal enhancement, heterogeneous enhancement, early washout, and hypoenhancement in the late phase mostly appeared in iso-/hyper-PDACs (p < 0.05). Heterogeneous enhancement in small lesions (< 3 cm) as the diagnostic criterion for iso-/hyper-PDACs had an accuracy of 74.3% and a specificity of 91.3%. Iso-PNETs more commonly had larger tumor sizes and more often showed heterogeneous enhancement than hyper-PNETs (p = 0.007, p = 0.035, respectively). The characteristics of the combination of isoenhancement, homogeneous enhancement, and synchronous wash-in/out for MFP had a high accuracy of 90%. Capsular enhancement with heterogeneous enhancement inside for SPTP had an accuracy of 97.1%.
CONCLUSION:
CEUS enhancement patterns have potentially great value in the differentiation of iso-/hyperenhanced pancreatic lesions.
SiegelRL, MillerKD, JemalA. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.
2.
SidhuPS, CantisaniV, DietrichCF, GiljaOH, SaftoiuA, BartelsE, et al. The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Long Version). Ultraschall Med. 2018;39(2):e2–e44.
3.
WernerJM, ZidekM, KammererS, da SilvaNPB, JungF, SchlittHJ, et al. Intraoperative contrast-enhanced ultrasound can have a crucial role in surgical decision-making during hepato-pancreatico-biliary surgery - Analysis of impact and input. Clin Hemorheol Microcirc. 2021;78(1):103–16.
4.
ZuoD, FengY, ZhangQ, QiuYJ, TianXF, ShiSN, et al. The value of dynamic contrast enhanced ultrasound (DCE-US) in monitoring treatment effect of high-intensity focused ultrasound (HIFU) in locally advanced pancreatic cancer (LAPC). Clin Hemorheol Microcirc. 2021;77(3):323–33.
5.
WiesingerI, JungF, JungEM. Contrast-enhanced ultrasound (CEUS) and perfusion imaging using VueBox®. Clin Hemorheol Microcirc. 2021;78(1):29–40.
6.
WiesingerI, KroissE, ZausigN, HornungM, ZemanF, StroszczynskiC, et al. Analysis of arterial dynamic micro-vascularization with contrast-enhanced ultrasound (CEUS) in thyroid lesions using external perfusion software: First results. Clin Hemorheol Microcirc. 2016;64(4):747–55.
7.
DongY, KochJBH, LöweAL, ChristenM, WangWP, JungEM, et al. VueBox® for quantitative analysis of contrast-enhanced ultrasound in liver tumors. Clin Hemorheol Microcirc. 2021.
8.
YangD, WangD, QiuY, TianX, ZuoD, DongY, et al. Incidental nonfunctioning pancreatic neuroendocrine tumors: Contrast enhanced ultrasound features in diagnosis. Clin Hemorheol Microcirc. 2021.
9.
ClaudonM, CosgroveD, AlbrechtT, BolondiL, BosioM, CalliadaF, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) - update 2008. Ultraschall Med. 2008;29(1):28–44.
10.
WangY, LiG, YanK, FanZ, LongR, ShanJ, et al. Clinical value of contrast-enhanced ultrasound enhancement patterns for differentiating solid pancreatic lesions. Eur Radiol. 2021.
11.
WangY, YanK, FanZ, DingK, YinS, DaiY, et al. Clinical Value of Contrast-Enhanced Ultrasound Enhancement Patterns for Differentiating Focal Pancreatitis From Pancreatic Carcinoma: A Comparison Study With Conventional Ultrasound. J Ultrasound Med. 2018;37(3):551–9.
12.
AdsayNV, BasturkO, BonnettM, KilincN, AndeaAA, FengJ, et al. A proposal for a new and more practical grading scheme for pancreatic ductal adenocarcinoma. Am J Surg Pathol. 2005;29(6):724–33.
13.
NagtegaalID, OdzeRD, KlimstraD, ParadisV, RuggeM, SchirmacherP, et al. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182–8.
14.
WangY, WangY, FanZ, ShanJ, YanK. The Value of Contrast-Enhanced Ultrasound Classification in Diagnosis of Pancreatic Cystic Lesions. Biomed Res Int. 2019;2019:5698140.
15.
NumataK, OzawaY, KobayashiN, KubotaT, AkinoriN, NakataniY, et al. Contrast-enhanced sonography of autoimmune pancreatitis: comparison with pathologic findings. J Ultrasound Med. 2004;23(2):199–206.
16.
Platz Batista da SilvaN, EngeßerM, HacklC, BrunnerS, HornungM, SchlittHJ, et al. Intraoperative Characterization of Pancreatic Tumors Using Contrast-Enhanced Ultrasound and Shear Wave Elastography for Optimization of Surgical Strategies. J Ultrasound Med. 2021;40(8):1613–25.
17.
ChenFM, NiJM, ZhangZY, ZhangL, LiB, JiangCJ. Presurgical Evaluation of Pancreatic Cancer: A Comprehensive Imaging Comparison of CT Versus MRI. AJR Am J Roentgenol. 2016;206(3):526–35.
18.
ParkHS, LeeJM, ChoiHK, HongSH, HanJK, ChoiBI. Preoperative evaluation of pancreatic cancer: comparison of gadolinium-enhanced dynamic MRI with MR cholangiopancreatography versus MDCT. J Magn Reson Imaging. 2009;30(3):586–95.
19.
SemelkaRC, AscherSM. MR imaging of the pancreas. Radiology. 1993;188(3):593–602.
20.
LeeS, KimSH, ParkHK, JangKT, HwangJA, KimS. Pancreatic Ductal Adenocarcinoma: Rim Enhancement at MR Imaging Predicts Prognosis after Curative Resection. Radiology. 2018;288(2):456–66.
21.
KartalisN, LindholmTL, AspelinP, PermertJ, AlbiinN. Diffusion-weighted magnetic resonance imaging of pancreas tumours. Eur Radiol. 2009;19(8):1981–90.
22.
IchikawaT, ErturkSM, MotosugiU, SouH, IinoH, ArakiT, et al. High-b value diffusion-weighted MRI for detecting pancreatic adenocarcinoma: preliminary results. AJR Am J Roentgenol. 2007;188(2):409–14.
23.
NiekelMC, BipatS, StokerJ. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology. 2010;257(3):674–84.
24.
LiXZ, SongJ, SunZX, YangYY, WangH. Diagnostic performance of contrast-enhanced ultrasound for pancreatic neoplasms: A systematic review and meta-analysis. Dig Liver Dis. 2018;50(2):132–8.
25.
D’OnofrioM, BarbiE, DietrichCF, KitanoM, NumataK, SofuniA, et al. Pancreatic multicenter ultrasound study (PAMUS). Eur J Radiol. 2012;81(4):630–8.
26.
D’OnofrioM, ZamboniGA, MalagòR, MantovaniW, PrincipeF, GallottiA, et al. Resectable pancreatic adenocarcinoma: is the enhancement pattern at contrast-enhanced ultrasonography a pre-operative prognostic factor?Ultrasound Med Biol. 2009;35(12):1929–37.
27.
FaccioliN, CrippaS, BassiC, D’OnofrioM. Contrast-enhanced ultrasonography of the pancreas. Pancreatology. 2009;9(5):560–6.
28.
WangZQ, LiJS, LuGM, ZhangXH, ChenZQ, MengK. Correlation of CT enhancement, tumor angiogenesis and pathologic grading of pancreatic carcinoma. World J Gastroenterol. 2003;9(9):2100–4.
29.
WangSH, SunYF, LiuY, ZhouY, LiuY. CT contrast enhancement correlates with pathological grade and microvessel density of pancreatic cancer tissues. Int J Clin Exp Pathol. 2015;8(5):5443–9.
30.
HyodoR, SuzukiK, OgawaH, KomadaT, NaganawaS. Pancreatic neuroendocrine tumors containing areas of iso- or hypoattenuation in dynamic contrast-enhanced computed tomography: Spectrum of imaging findings and pathological grading. Eur J Radiol. 2015;84(11):2103–9.
31.
RodallecM, VilgrainV, CouvelardA, RufatP, O’TooleD, BarrauV, et al. Endocrine pancreatic tumours and helical CT: contrast enhancement is correlated with microvascular density, histoprognostic factors and survival. Pancreatology. 2006;6(1-2):77–85.
32.
KarmazanovskyG, BelousovaE, SchimaW, GlotovA, KalininD, KrigerA. Nonhypervascular pancreatic neuroendocrine tumors: Spectrum of MDCT imaging findings and differentiation from pancreatic ductal adenocarcinoma. Eur J Radiol. 2019;110:66–73.
33.
d’AssigniesG, CouvelardA, BahramiS, VulliermeMP, HammelP, HenticO, et al. Pancreatic endocrine tumors: tumor blood flow assessed with perfusion CT reflects angiogenesis and correlates with prognostic factors. Radiology. 2009;250(2):407–16.
34.
TakumiK, FukukuraY, HigashiM, IdeueJ, UmanodanT, HakamadaH, et al. Pancreatic neuroendocrine tumors: Correlation between the contrast-enhanced computed tomography features and the pathological tumor grade. Eur J Radiol. 2015;84(8):1436–43.
35.
CanzonieriV, BerrettaM, BuonadonnaA, LibraM, VasquezE, BarbagalloE, et al. Solid pseudopapillary tumour of the pancreas. Lancet Oncol. 2003;4(4):255–6.
36.
JiaH, LiJ, HuangW, LinG. Multimodel magnetic resonance imaging of mass-forming autoimmune pancreatitis: differential diagnosis with pancreatic ductal adenocarcinoma. BMC Med Imaging. 2021;21(1):149.
37.
WangY, ChenX, WangJ, CuiW, WangC, ChenX, et al. Differentiation between non-hypervascular pancreatic neuroendocrine tumors and mass-forming pancreatitis using contrast-enhanced computed tomography. Acta Radiol. 2021;62(2):190–7.
38.
RenS, ChenX, WangZ, ZhaoR, WangJ, CuiW, et al. Differentiation of hypovascular pancreatic neuroendocrine tumors from pancreatic ductal adenocarcinoma using contrast-enhanced computed tomography. PLoS One. 2019;14(2):e0211566.
39.
D’OnofrioM, GallottiA, PrincipeF, MucelliRP. Contrast-enhanced ultrasound of the pancreas. World J Radiol. 2010;2(3):97–102.
40.
WangY, YanK, FanZ, SunL, WuW, YangW. Contrast-Enhanced Ultrasonography of Pancreatic Carcinoma: Correlation with Pathologic Findings. Ultrasound Med Biol. 2016;42(4):891–8.
41.
ChenX, HaoF, GuiY, ZhangJ, TanL, XiaoM, et al. Enhancement patterns in the venous phase of contrast-enhanced ultrasounds: diagnostic value for patients with solid pancreatic lesions. Quant Imaging Med Surg. 2021;11(10):4321–33.
42.
FanZ, LiY, YanK, WuW, YinS, YangW, et al. Application of contrast-enhanced ultrasound in the diagnosis of solid pancreatic lesions–a comparison of conventional ultrasound and contrast-enhanced CT. Eur J Radiol. 2013;82(9):1385–90.
43.
ScialpiM, ReginelliA, D’AndreaA, GravanteS, FalconeG, BaccariP, et al. Pancreatic tumors imaging: An update. Int J Surg. 2016;28 Suppl 1:S142–55.
44.
XuM, XieXY, LiuGJ, XuHX, XuZF, HuangGL, et al. The application value of contrast-enhanced ultrasound in the differential diagnosis of pancreatic solid-cystic lesions. Eur J Radiol. 2012;81(7):1432–7.
45.
KuriharaN, KawamotoH, KobayashiY, OkamotoY, YamamotoN, TsutsumiK, et al. Vascular patterns in nodules of intraductal papillary mucinous neoplasms depicted under contrast-enhanced ultrasonography are helpful for evaluating malignant potential. Eur J Radiol. 2012;81(1):66–70.
46.
YamashitaY, UedaK, ItonagaM, YoshidaT, MaedaH, MaekitaT, et al. Usefulness of contrast-enhanced endoscopic sonography for discriminating mural nodules from mucous clots in intraductal papillary mucinous neoplasms: a single-center prospective study. J Ultrasound Med. 2013;32(1):61–8.
47.
KitanoM, KamataK, ImaiH, MiyataT, YasukawaS, YanagisawaA, et al. Contrast-enhanced harmonic endoscopic ultrasonography for pancreatobiliary diseases. Dig Endosc. 2015;27 Suppl 1:60–7.
48.
SugimotoM, TakagiT, HikichiT, SuzukiR, WatanabeK, NakamuraJ, et al. Conventional versus contrast-enhanced harmonic endoscopic ultrasonography-guided fine-needle aspiration for diagnosis of solid pancreatic lesions: A prospective randomized trial. Pancreatology. 2015;15(5):538–41.
