Top

Published in:

Open Access 01-12-2018 | Research article

Contrast-enhanced ultrasonography of the pancreas shows impaired perfusion in pancreas insufficient cystic fibrosis patients

Authors: Trond Engjom, Kim Nylund, Friedemann Erchinger, Marcus Stangeland, Birger Norderud Lærum, Martin Mézl, Radovan Jiřík, Odd Helge Gilja, Georg Dimcevski

Published in: BMC Medical Imaging | Issue 1/2018

Abstract

Background

Perfusion assessment of the pancreas is challenging and poorly evaluated. Pancreatic affection is a prevalent feature of cystic fibrosis (CF). Little is known about pancreatic perfusion in CF. We aimed to assess pancreatic perfusion by contrast-enhanced ultrasound (CEUS) analysed in the bolus-and-burst model and software.

Methods

We performed contrast enhanced ultrasound of the pancreas in 25 CF patients and 20 healthy controls. Perfusion data was analysed using a dedicated perfusion model providing the mean capillary transit-time (MTT), blood flow (BF) and blood-volume (BV). CF patients were divided according to exocrine function.

Results

The pancreas insufficient CF patients had longer MTT (p ≤ 0.002), lower BF (p < 0.001) and lower BV (p < 0.05) compared to the healthy controls and sufficient CF patients. Interrater analysis showed substantial agreement for the analysis of mean transit time.

Conclusion

The bolus-and-burst method used on pancreatic CEUS-examinations demonstrates reduced perfusion in CF patients with pancreas affection. The perfusion model and software requires further optimization and standardization to be clinical applicable for the assessment of pancreatic perfusion.

Available only for authorised users

D'Onofrio M, Zamboni G, Faccioli N, Capelli P, Pozzi MR. Ultrasonography of the pancreas. 4. Contrast-enhanced imaging. Abdom Imaging. 2007;32(2):171–81.CrossRefPubMed

Kersting S, Konopke R, Kersting F, Volk A, Distler M, Bergert H, Saeger HD, Grutzmann R, Bunk A. Quantitative perfusion analysis of transabdominal contrast-enhanced ultrasonography of pancreatic masses and carcinomas. Gastroenterology. 2009;137(6):1903–11.CrossRefPubMed

Matsubara H, Itoh A, Kawashima H, Kasugai T, Ohno E, Ishikawa T, Itoh Y, Nakamura Y, Hiramatsu T, Nakamura M, et al. Dynamic quantitative evaluation of contrast-enhanced endoscopic ultrasonography in the diagnosis of pancreatic diseases. Pancreas. 2011;40(7):1073–9.CrossRefPubMed

Piscaglia F, Nolsoe C, Dietrich CF, Cosgrove DO, Gilja OH, Bachmann NM, Albrecht T, Barozzi L, Bertolotto M, Catalano O, et al. The EFSUMB guidelines and recommendations on the clinical practice of contrast enhanced ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med. 2012;33(1):33–59.CrossRefPubMed

Azemoto N, Kumagi T, Yokota T, Hirooka M, Kuroda T, Koizumi M, Ohno Y, Yamanishi H, Abe M, Onji M, et al. Utility of contrast-enhanced transabdominal ultrasonography to diagnose early chronic pancreatitis. Biomed Res Int. 2015;2015:393124.CrossRefPubMedPubMedCentral

Delrue L, Blanckaert P, Mertens D, Van MS, Ceelen W, Duyck P. Tissue perfusion in pathologies of the pancreas: assessment using 128-slice computed tomography. Abdom Imaging. 2012;37(4):595–601.CrossRefPubMed

Tsushima Y, Miyazaki M, Taketomi-Takahashi A, Endo K. Feasibility of measuring human pancreatic perfusion in vivo using imaging techniques. Pancreas. 2011;40(5):747–52.CrossRefPubMed

Bali MA, Metens T, Denolin V, De Maertelaer V, Deviere J, Matos C. Pancreatic perfusion: noninvasive quantitative assessment with dynamic contrast-enhanced MR imaging without and with secretin stimulation in healthy volunteers--initial results. Radiology. 2008;247(1):115–21.CrossRefPubMed

Ishida H, Makino T, Kobayashi M, Tsuneoka K. Laparoscopic measurement of pancreatic blood flow. Endoscopy. 1983;15(3):107–10.CrossRefPubMed

10.

Lewis MP, Lo SK, Reber PU, Patel A, Gloor B, Todd KE, Toyama MT, Sherman S, Ashley SW, Reber HA. Endoscopic measurement of pancreatic tissue perfusion in patients with chronic pancreatitis and control patients. Gastrointest Endosc. 2000;51(2):195–9.CrossRefPubMed

11.

Claudon M, Dietrich CF, Choi BI, Cosgrove DO, Kudo M, Nolsoe CP, Piscaglia F, Wilson SR, Barr RG, Chammas MC, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver--update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultraschall Med. 2013;34(1):11–29.PubMed

12.

Nylund K, Jirik R, Mezl M, Leh S, Hausken T, Pfeffer F, Odegaard S, Taxt T, Gilja OH. Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn's disease. Ultrasound Med Biol. 2013;39(7):1197–206.CrossRefPubMed

13.

Lassau N, Bonastre J, Kind M, Vilgrain V, Lacroix J, Cuinet M, Taieb S, Aziza R, Sarran A, Labbe-Devilliers C, et al. Validation of dynamic contrast-enhanced ultrasound in predicting outcomes of antiangiogenic therapy for solid tumors: the French multicenter support for innovative and expensive techniques study. Invest Radiol. 2014;49(12):794–800.CrossRefPubMedPubMedCentral

14.

Saevik F, Nylund K, Hausken T, Odegaard S, Gilja OH. Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn's disease. Inflamm Bowel Dis. 2014;20(11):2029-37.

15.

D'Onofrio M, Canestrini S, Crosara S, De RR, Pozzi MR. Contrast enhanced ultrasound with quantitative perfusion analysis for objective characterization of pancreatic ductal adenocarcinoma: a feasibility study. World J Radiol. 2014;6(3):31–5.CrossRefPubMedPubMedCentral

16.

Fan Z, Li Y, Yan K, Wu W, Yin S, Yang W, Xing B, Li X, Zhang X. 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.CrossRefPubMed

17.

Tranquart F, Mercier L, Frinking P, Gaud E, Arditi M. Perfusion quantification in contrast-enhanced ultrasound (CEUS)--ready for research projects and routine clinical use. Ultraschall in der Medizin (Stuttgart, Germany : 1980). 2012;33(Suppl 1):S31–8.

18.

Jirik R, Nylund K, Taxt T, Mézl M, Hausken T, Harabi V, Kol R et al: Parametric ultrasound perfusion analysis combining bolus tracking and replenishment. In: 2012 IEEE International Ultrasonics Symposium: 7–10 Oct. 2012 2012; 2012: 1323–1326.

19.

Jirik R, Nylund K, Gilja OH, Mezl M, Harabis V, Kolar R, Standara M, Taxt T. Ultrasound perfusion analysis combining bolus-tracking and burst-replenishment. IEEE Trans Ultrason Ferroelectr Freq Control. 2013;60(2):310–9.CrossRefPubMed

20.

Stangeland M, Engjom T, Mezl M, Jirik R, Gilja OH, Dimcevski G, Nylund K: Interobserver variation of the bolus-and-burst method for pancreatic perfusion with dynamic contrast-enhanced ultrasound. Ultrasound Int Open 2017: 3 (3):E99-E106. doi: https://doi.org/10.1055/s-0043-110475. Epub 2017 Sep 12.

21.

Durie PR, Forstner GG. Pathophysiology of the exocrine pancreas in cystic fibrosis. J R Soc Med. 1989;82(Suppl 16):2–10.PubMedPubMedCentral

22.

Kopelman H, Corey M, Gaskin K, Durie P, Weizman Z, Forstner G. Impaired chloride secretion, as well as bicarbonate secretion, underlies the fluid secretory defect in the cystic fibrosis pancreas. Gastroenterology. 1988;95(2):349–55.CrossRefPubMed

23.

Kopito LE, Shwachman H. The pancreas in cystic fibrosis: chemical composition and comparative morphology. Pediatr Res. 1976;10(8):742–9.PubMed

24.

Pitkaranta P, Kivisaari L, Nordling S, Nuutinen P, Schroder T. Vascular changes of pancreatic ducts and vessels in acute necrotizing, and in chronic pancreatitis in humans. Int J Pancreatol. 1991;8(1):13–22.PubMed

25.

Farrell PM, Rosenstein BJ, White TB, Accurso FJ, Castellani C, Cutting GR, Durie PR, Legrys VA, Massie J, Parad RB, et al. Guidelines for diagnosis of cystic fibrosis in newborns through older adults: Cystic Fibrosis Foundation consensus report. J Pediatr. 2008;153(2):S4–S14.CrossRefPubMedPubMedCentral

26.

Smyth AR, Bell SC, Bojcin S, Bryon M, Duff A, Flume P, Kashirskaya N, Munck A, Ratjen F, Schwarzenberg SJ, et al. European cystic fibrosis society standards of care: best practice guidelines. J Cystic Fibros. 2014;13(Suppl 1):S23–42.CrossRef

27.

Schafer S, Nylund K, Saevik F, Engjom T, Mezl M, Jirik R, Dimcevski G, Gilja OH, Tonnies K. Semi-automatic motion compensation of contrast-enhanced ultrasound images from abdominal organs for perfusion analysis. Comput Biol Med. 2015;63:229–37. https://doi.org/10.1016/j.compbiomed.2014.09.014. Epub 2014 Oct 17CrossRefPubMed

28.

Urbaniak G PS: Research Randomizer (Version 4.0). computer software Available at: https://www.randomizer.org. Accessed 10 May 2018.

29.

Engjom T, Erchinger F, Laerum BN, Tjora E, Aksnes L, Gilja OH, Dimcevski G. Diagnostic accuracy of a short endoscopic secretin test in patients with cystic fibrosis. Pancreas. 2015;44(8):1266–72.CrossRefPubMedPubMedCentral

30.

Erchinger F, Engjom T, Tjora E, Hoem D, Hausken T, Gilja OH, Dimcevski G. Quantification of pancreatic function using a clinically feasible short endoscopic secretin test. Pancreas. 2013;42(7):1101–6.CrossRefPubMed

31.

Landis J, Koch G. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.CrossRefPubMed

32.

Gauthier M, Tabarout F, Leguerney I, Polrot M, Pitre S, Peronneau P, Lassau N. Assessment of quantitative perfusion parameters by dynamic contrast-enhanced sonography using a deconvolution method: an in vitro and in vivo study. J Ultrasound Med. 2012;31(4):595–608.CrossRefPubMed

33.

Engjom T, Erchinger F, Laerum BN, Tjora E, Gilja OH, Dimcevski G. Ultrasound echo-intensity predicts severe pancreatic affection in cystic fibrosis patients. PLoS One. 2015;10(3):e0121121.CrossRefPubMedPubMedCentral

34.

WMA general assembly 2015. World medical association declaration of Helsinki. Ethical Principles for Medical Research Involving Human Subjects. Available at: https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/. Accessed 16 June 2017.

Title: Contrast-enhanced ultrasonography of the pancreas shows impaired perfusion in pancreas insufficient cystic fibrosis patients
Authors: Trond Engjom
Kim Nylund
Friedemann Erchinger
Marcus Stangeland
Birger Norderud Lærum
Martin Mézl
Radovan Jiřík
Odd Helge Gilja
Georg Dimcevski
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: BMC Medical Imaging / Issue 1/2018
Electronic ISSN: 1471-2342
DOI: https://doi.org/10.1186/s12880-018-0259-3

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Contrast-enhanced ultrasonography of the pancreas shows impaired perfusion in pancreas insufficient cystic fibrosis patients

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2018

A consistency evaluation of signal-to-noise ratio in the quality assessment of human brain magnetic resonance images

Gadoxetic acid-enhanced magnetic resonance imaging significantly influences the clinical course in patients with colorectal liver metastases

The segmentation of bones in pelvic CT images based on extraction of key frames

Systemic air embolism after percutaneous computed tomography-guided lung biopsy due to a kink in the coaxial biopsy system: a case report

Accurate hybrid template–based and MR-based attenuation correction using UTE images for simultaneous PET/MR brain imaging applications

Evaluation of the diagnostic performance of the simple method of computed tomography in the assessment of patients with shoulder instability: a prospective cohort study