Ultraschall Med 2015; 36(06): 603-610
DOI: 10.1055/s-0041-107971
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Evaluation of Liver and Spleen Stiffness with Acoustic Radiation Force Impulse Quantification Elastography for Diagnosing Clinically Significant Portal Hypertension

Evaluation der Leber- und Milzfestigkeit mittels Acoustic Radiation Force Impulse Imaging für die Diagnose einer klinisch-signifikanten portalen Hypertension
D. Attia*
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
3   Departement of Gastroenterology, Hepatology and Endemic Medicine, Faculty of Medicine, Beni Suef University, Beni Suef, Egypt
,
B. Schoenemeier*
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
T. Rodt
2   Hannover Medical School, Diagnostic and Interventional Radiology, Hannover, Germany
,
A. A. Negm
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
H. Lenzen
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
T. O. Lankisch
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
M. Manns
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
M. Gebel
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
,
A. Potthoff
1   Zentrum f. Innere Medizin, Hannover Medical School, Hannover, Germany
› Author Affiliations
Further Information

Publication History

18 January 2015

02 September 2015

Publication Date:
13 November 2015 (online)

Abstract

Purpose: Hepatic vein pressure gradient (HVPG) is the gold standard for diagnosing clinically significant portal hypertension (CSPH). The aim of this study was to investigate—in comparison to HVPG—the ability to diagnose CSPH by liver and spleen stiffness measurements obtained by acoustic radiation force impulse (ARFI) imaging.

Materials and Methods: A total of 78 patients (mean age: 53 ± 13 years, 62 % male) with chronic liver disease were enrolled in this study. Each patient received liver (LSM) and spleen (SSM) stiffness measurements by ARFI, an HVPG measurement and a transjugular liver biopsy on the same day. Patients were classified according to their HVPG into three different groups: HVPG < 10 mmHg, HVPG ≥ 10–< 12 mmHg and HVPG ≥ 12 mmHg.

Results: LSM, SSM were significantly higher in patients with HVPG ≥ 10 – < 12 in comparison to HVPG < 10 mmHg (p < 0.001 and p < 0.001, respectively), and in patients with HVPG ≥ 12 mmHg in comparison to ≥ 10 – < 12 mmHg (p < 0.001 and p < 0.001, respectively). LSM and SSM were able to diagnose HVPG ≥ 10 mmHg and HVPG ≥ 12 mmHg with high diagnostic performance (AUC LSM: 0.93 and 0.87, respectively; AUC SSM: 0.97 and 0.95, respectively). The AUC of SSM in predicting esophageal varices (EVs) plus HVPG ≥ 10 mmHg and EVs plus HVPG ≥ 12 mmHg were higher compared to LSM in both groups of patients (SSM: 0.90 and 0.93 vs. LSM: 0.84 and 0.88, respectively). No significant difference between both AUCs was detected in the different HVPG groups. In the multivariate ­analysis SSM remained a factor predicting HVPG (HVPG > 10 mmHg p = 0.007; HVPG ≥ 12 mmHg p = 0.003).

Conclusion: LSM and SSM by ARFI are noninvasive diagnostic tools that may help in diagnosing CSPH. LSM and SSM could be used as a guiding noninvasive screening tool in patients with esophageal varices requiring endoscopic evaluation.

Zusammenfassung

Hintergrund: Die Lebervenenverschlussdruck-Messung (HVPG) stellt den Goldstandard für die Diagnose einer klinisch-signifikanten portalen Hypertension (CSPH) dar. Das Ziel der Studie lag darin zu evaluieren, inwiefern die Leber (LSM)- und Milz-Elastographie (SSM) mittels Acoustic Radiation Force Impulse Imaging (ARFI) geeignet ist, eine CSPH vorherzusagen.

Material und Methodik: Insgesamt wurden 78 Patienten (Alter: 53 ± 13 Jahre, 62 % männlich) mit einer chronischen Lebererkrankung in die Studie eingeschlossen. Bei allen Patienten wurden am selben Tag eine LSM und SSM mittels ARFI, eine HVPG-Messung und eine transjuguläre Leberbiopsie durchgeführt. In Abhängigkeit zu den HVPG-Ergebnissen wurden die Patienten in drei Gruppen eingeteilt: (1) HVPG < 10 mmHg, (2) HVPG ≥ 10–< 12 mmHg, (3) HVPG ≥ 12 mmHg.

Ergebnisse: Die Leber- und Milzsteife war bei Patienten mit einem HVPG ≥ 10 – < 12 signifikant höher als bei den Patienten mit einem HVPG < 10 mmHg (LSM: p < 0,001 und SSM: p < 0,001). Auch ein HVPG ≥ 12 mmHg ging im Vergleich zu einem HVPG ≥ 10 – < 12 mmHg mit signifikant höheren Werte für die LSM und SSM einher (p < 0,001 und p < 0,001). Ein HVPG ≥ 10 mmHg und ≥ 12 mmHg konnte sowohl durch die LSM, als auch durch die SSM mit einer hohen diagnostischen Genauigkeit vorhergesagt werden (AUC LSM: 0,93 und 0,87; AUC SSM: 0,97 und 0,95). Die AUC-Werte der SSM zur Vorhersage von Ösophagusvarizen + HVPG ≥ 10 mmHg und Ösophagusvarizen + HVPG ≥ 12 mmHg waren höher als die der LSM (SSM: 0,90 und 0,93 vs. LSM: 0,84 and 0,88). Innerhalb der verschiedenen HVPG-Gruppen konnte aber kein signifikanter Unterschied festgestellt werden. In der Multivarianz-Analyse war die SSM ein signifikanter Prädiktor für den HVPG (HVPG > 10mmHg, p = 0,007; HVPG ≥ 12 mmHg p = 0,003).

Schlussfolgerung: Die Leber- und Milzelastographie mittels ARFI sind hilfreiche nicht-invasive Verfahren für die Diagnose einer CSPH. Sie könnten zukünftig als Screening-Verfahren genutzt werden, um Patienten mit Ösophagusvarizen zu identifizieren, die einer endoskopischen Evaluation bedürfen.

* These authors have contributed equally to this work.


 
  • References

  • 1 D'Amico G, Garcia-Pagan JC, Luca A et al. Hepatic vein pressure gradient reduction and prevention of variceal bleeding in cirrhosis: a systematic review. Gastroenterology 2006; 131: 1611-1624
  • 2 Berzigotti A, Seijo S, Arena U et al. Elastography, spleen size, and platelet count identify portal hypertension in patients with compensated cirrhosis. Gastroenterology 2013; 144: 102-111 e1
  • 3 de Franchis R, Baveno VF. Revising consensus in portal hypertension: report of the Baveno V consensus workshop on methodology of diagnosis and therapy in portal hypertension. J Hepatol 2010; 53: 762-768
  • 4 Berzigotti A, Gilabert R, Abraldes JG et al. Noninvasive prediction of clinically significant portal hypertension and esophageal varices in patients with compensated liver cirrhosis. Am J Gastroenterol 2008; 103: 1159-1167
  • 5 Thabut D, Moreau R, Lebrec D. Noninvasive assessment of portal hypertension in patients with cirrhosis. Hepatology 2011; 53: 683-694
  • 6 Pinzani M, Gentilini P. Biology of hepatic stellate cells and their possible relevance in the pathogenesis of portal hypertension in cirrhosis. Semin Liver Dis 1999; 19: 397-410
  • 7 Castera L, Pinzani M, Bosch J. Non invasive evaluation of portal hypertension using transient elastography. J Hepatol 2012; 56: 696-703
  • 8 Bureau C, Metivier S, Peron JM et al. Transient elastography accurately predicts presence of significant portal hypertension in patients with chronic liver disease. Aliment Pharmacol Ther 2008; 27: 1261-1268
  • 9 Rockey DC. Noninvasive assessment of liver fibrosis and portal hypertension with transient elastography. Gastroenterology 2008; 134: 8-14
  • 10 Lemoine M, Katsahian S, Ziol M et al. Liver stiffness measurement as a predictive tool of clinically significant portal hypertension in patients with compensated hepatitis C virus or alcohol-related cirrhosis. Aliment Pharmacol Ther 2008; 28: 1102-1110
  • 11 Robic MA, Procopet B, Metivier S et al. Liver stiffness accurately predicts portal hypertension related complications in patients with chronic liver disease: a prospective study. J Hepatol 2011; 55: 1017-1024
  • 12 Augustin S, Millan L, Gonzalez A et al. Detection of early portal hypertension with routine data and liver stiffness in patients with asymptomatic liver disease: a prospective study. J Hepatol 2014; 60: 561-569
  • 13 Colecchia A, Colli A, Casazza G et al. Spleen stiffness measurement can predict clinical complications in compensated HCV-related cirrhosis: A prospective study. J Hepatol 2014; 60: 1158-1164
  • 14 Kim BK, Han KH, Park JY et al. A liver stiffness measurement-based, noninvasive prediction model for high-risk esophageal varices in B-viral liver cirrhosis. Am J Gastroenterol 2010; 105: 1382-1390
  • 15 Berzigotti A, Bosch J, Boyer TD. Use of noninvasive markers of portal hypertension and timing of screening endoscopy for gastroesophageal varices in patients with chronic liver disease. Hepatology 2014; 59: 729-731
  • 16 Friedrich-Rust M, Nierhoff J, Lupsor M et al. Performance of Acoustic Radiation Force Impulse imaging for the staging of liver fibrosis: a pooled meta-analysis. J Viral Hepat 2012; 19: e212-e219
  • 17 Cosgrove D, Piscaglia F, Bamber J et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall in Med 2013; 34: 238-253
  • 18 Vermehren J, Polta A, Zimmermann O et al. Comparison of acoustic radiation force impulse imaging with transient elastography for the detection of complications in patients with cirrhosis. Liver Int 2012; 32: 852-858
  • 19 Han JY, Cho JH, Kwon HJ et al. Predicting portal hypertension as assessed by acoustic radiation force impulse: correlations with the Doppler ultrasound. Br J Radiol 2012; 85: e404-e409
  • 20 Takuma Y, Nouso K, Morimoto Y et al. Measurement of spleen stiffness by acoustic radiation force impulse imaging identifies cirrhotic patients with esophageal varices. Gastroenterology 2013; 144: 92-101 e2
  • 21 Singh S, Eaton JE, Murad MH et al. Accuracy of Spleen Stiffness Measurement in Detection of Esophageal Varices in Patients With Chronic Liver Disease: Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol 2014; 12: 935-945 e4
  • 22 Chen SH, Li YF, Lai HC et al. Noninvasive assessment of liver fibrosis via spleen stiffness measurement using acoustic radiation force impulse sonoelastography in patients with chronic hepatitis B or C. J Viral Hepat 2012; 19: 654-663
  • 23 Salzl P, Reiberger T, Ferlitsch M et al. Evaluation of Portal Hypertension and Varices by Acoustic Radiation Force Impulse Imaging of the Liver Compared to Transient Elastography and AST to Platelet Ratio Index. Ultraschall in Med 2014; 35: 528-533
  • 24 Berzigotti A, Piscaglia F, Education E et al. Ultrasound in portal hypertension--part 2--and EFSUMB recommendations for the performance and reporting of ultrasound examinations in portal hypertension. Ultraschall in Med 2012; 33: 8-32 ; 30–31
  • 25 Bamber J, Cosgrove D, Dietrich CF et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in Med 2013; 34: 169-184
  • 26 Nightingale K, Soo MS, Nightingale R et al. Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 2002; 28: 227-235
  • 27 Potthoff A, Attia D, Pischke S et al. Influence of different frequencies and insertion depths on the diagnostic accuracy of liver elastography by acoustic radiation force impulse imaging (ARFI). Eur J Radiol 2013; 82: 1207-1212
  • 28 Karlas T, Lindner F, Troltzsch M et al. Assessment of spleen stiffness using acoustic radiation force impulse imaging (ARFI): definition of examination standards and impact of breathing maneuvers. Ultraschall in Med 2014; 35: 38-43
  • 29 Bosch J, Abraldes JG, Berzigotti A et al. The clinical use of HVPG measurements in chronic liver disease. Nat Rev Gastroenterol Hepatol 2009; 6: 573-582
  • 30 Ishak K, Baptista A, Bianchi L et al. Histological grading and staging of chronic hepatitis. J Hepatol 1995; 22: 696-699
  • 31 The French METAVIR Cooperative Study Group. Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. Hepatology 1994; 20: 15-20
  • 32 Glas AS, Lijmer JG, Prins MH et al. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 2003; 56: 1129-1135
  • 33 D'Amico G, Pasta L, Morabito A et al. Competing risks and prognostic stages of cirrhosis: a 25-year inception cohort study of 494 patients. Aliment Pharmacol Ther 2014; 39: 1180-1193
  • 34 Colecchia A, Montrone L, Scaioli E et al. Measurement of spleen stiffness to evaluate portal hypertension and the presence of esophageal varices in patients with HCV-related cirrhosis. Gastroenterology 2012; 143: 646-654
  • 35 Carrion JA, Navasa M, Bosch J et al. Transient elastography for diagnosis of advanced fibrosis and portal hypertension in patients with hepatitis C recurrence after liver transplantation. Liver Transpl 2006; 12: 1791-1798
  • 36 Sanchez-Conde M, Montes-Ramirez ML, Miralles P et al. Comparison of transient elastography and liver biopsy for the assessment of liver fibrosis in HIV/hepatitis C virus-coinfected patients and correlation with noninvasive serum markers. J Viral Hepat 2010; 17: 280-286
  • 37 Morishita N, Hiramatsu N, Oze T et al. Liver stiffness measurement by acoustic radiation force impulse is useful in predicting the presence of esophageal varices or high-risk esophageal varices among patients with HCV-related cirrhosis. J Gastroenterol 2014; 49: 1175-1182
  • 38 Bota S, Sporea I, Sirli R et al. Spleen assessment by Acoustic Radiation Force Impulse Elastography (ARFI) for prediction of liver cirrhosis and portal hypertension. Med Ultrason 2010; 12: 213-217
  • 39 Vizzutti F, Arena U, Romanelli RG et al. Liver stiffness measurement predicts severe portal hypertension in patients with HCV-related cirrhosis. Hepatology 2007; 45: 1290-1297
  • 40 Castera L, Garcia-Tsao G. When the spleen gets tough, the varices get going. Gastroenterology 2013; 144: 19-22
  • 41 Reiberger T, Ferlitsch A, Payer BA et al. Non-selective beta-blockers improve the correlation of liver stiffness and portal pressure in advanced cirrhosis. J Gastroenterol 2012; 47: 561-568