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Role of Spleen Stiffness Measurement by 2D-Shear Wave Elastography in Ruling Out the Presence of High-Risk Varices in Cirrhotic Patients

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Abstract

Background and Aim

To evaluate if spleen stiffness measurement (SSM) can rule out the presence of high-risk varices in patients with cirrhosis, avoiding an upper gastrointestinal endoscopy (UGE).

Methods

We enrolled 71 cirrhotic patients irrespective of liver disease’s etiology. 2D shear wave elastography (SWE) of spleen and UGE was performed. High-risk varices (HRV) were defined as esophageal varices ≥ 5 mm and/or red spots and any gastric varices.

Results

Esophageal varices were documented in 37 (52.1%) and HRV in 25 (35.2%) patients. SSM was not technically feasible in 7/71 patients (9.8%). From the remaining 64 patients, when those with cholestatic liver disease were excluded (n = 17), SSM < 35.8 kPa was found to exclude well the existence of HRV offering an AUROC of 0.854 (p < 0.001), sensitivity 88.9%, negative predictive value (NPV) 91.3%, specificity 72.4%, and positive predictive value (PPV) 66.7%. Only 2/47 patients (4.3%) were misclassified, and 23 (48.9%) could avoid endoscopy. In the total cohort of 64 patients, SSM < 33.7 kPa was found to exclude well the presence of HRV offering AUROC 0.792 (p < 0.001), sensitivity 91.7%, specificity 60%, NPV 92.3%, and PPV 57.9%. The misclassification rate was 3.1% (2/64), while 26/64 (40.6%) could avoid endoscopy.

Conclusions

2D-SWE of spleen is a reliable method for ruling out the presence of HRV in cirrhotic patients. If larger studies confirm our results, a large number of endoscopies could be avoided.

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Abbreviations

HVPG:

Hepatic venous pressure gradient

CSPH:

Clinically significant portal hypertension

GEV:

Gastroesophageal varices

HRV:

High-risk varices

UGE:

Upper gastrointestinal endoscopy

LSM:

Liver stiffness measurements

TE:

Transient elastography

SSM:

Spleen stiffness measurement

SWE:

Shear wave elastography

HCC:

Hepatocellular carcinoma

TIPS:

Transjugular intrahepatic portosystemic shunt

INR:

International normalized ratio

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

MELD:

Model for end stage liver disease

SD:

Standard deviation

AUROC:

Area under receiving operating characteristic

PPV:

Positive predictive value

NPV:

Negative predictive value

ARFI:

Acoustic radiation force impulse imaging

References

  1. De Franchis R. 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.

    Article  PubMed  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. Groszmann RJ, Garcia-Tsao G, Bosch J, et al. Beta-blockers to prevent gastroesophageal varices in patients with cirrhosis. N Engl J Med. 2005;353:2254–2261.

    Article  CAS  PubMed  Google Scholar 

  4. Casado M, Bosch J, Garcia-Pagan JC, et al. Clinical events after transjugular intrahepatic portosystemic shunt: correlation with hemodynamic findings. Gastroenterology. 1998;114:1296–1303.

    Article  CAS  PubMed  Google Scholar 

  5. Garcia-Tsao G, Groszmann RJ, Fisher RL, et al. Portal pressure, presence of gastroesophageal varices and variceal bleeding. Hepatology. 1985;5:419–424.

    Article  CAS  PubMed  Google Scholar 

  6. Ripoll C, Groszmann R, Garcia-Tsao G, et al. Hepatic venous pressure gradient predicts clinical decompensation in patients with compensated cirrhosis. Gastroenterology. 2007;133:481–488.

    Article  CAS  PubMed  Google Scholar 

  7. Garcia-Tsao G, Abraldes JG, Berzigotti A, et al. Portal hypertensive bleeding in cirrhosis: Risk stratification, diagnosis, and management: 2016 practice guidance by the American Association for the study of liver diseases. Hepatology. 2017;65:310–335.

    Article  PubMed  Google Scholar 

  8. Angeli P, Bernardi M, Villanueva C, et al. EASL clinical practice guidelines for the management of patients with decompensated cirrhosis. J Hepatol. 2018;69:406–460.

    Article  Google Scholar 

  9. De Franchis R, Baveno T. Faculty. Expanding consensus in portal hypertension: report of the Baveno VI consensus workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol. 2015;63:743–752.

    Article  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. 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;12:1791–1799.

    Article  PubMed  Google Scholar 

  12. Karagiannakis DS, Voulgaris T, Siakavellas SI, Papatheodoridis GV, Vlachogiannakos J. Evaluation of portal hypertension in the cirrhotic patient: hepatic vein pressure and beyond. Scand J Gastroenterol. 2018;53:1153–1164.

    Article  CAS  PubMed  Google Scholar 

  13. Castera L, Pinzani M, Bosch J. Non invasive evaluation of portal hypertension using transient elastography. J Hepatol. 2012;56:696–703.

    Article  PubMed  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. European Association for Study of Liver; Associacion Latinoamericana para el Estudio del Higado. EASL-ALEH clinical practice guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol. 2015;63:237–264.

  16. 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.

    Article  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. Kumar A, Khan NM, Anikhindi SA, et al. Correlation of transient elastography with hepatic venous pressure gradient in patients with cirrhotic portal hypertension: a study of 326 patients from India. World J Gastroenterol. 2017;23:687–696.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Reiberger T, Ferlitsch A, Payer BA, et al. Noninvasive screening for liver fibrosis and portal hypertension by transient elastography—a large single center experience. Wien Klin Wochenschr. 2012;124:395–402.

    Article  PubMed  Google Scholar 

  20. Pilette C, Oberti F, Aubé C, et al. Non-invasive diagnosis of esophageal varices in chronic liver diseases. J Hepatol. 1999;31:867–873.

    Article  CAS  PubMed  Google Scholar 

  21. Thomopoulos KC, Labropoulou-Karatza C, Mimidis KP, et al. Non-invasive predictors of the presence of large oesophageal varices in patients with cirrhosis. Dig Liver Dis. 2003;35:473–478.

  22. Giannini E, Botta F, Borro P, et al. Platelet count/spleen diameter ratio: proposal and validation of a non-invasive parameter to predict the presence of oesophageal varices in patients with liver cirrhosis. Gut. 2003;52:1200–1205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Berzigotti A, Seijo S, Arena U, et al. Elastography, spleen size, and platelet count identify portal hypertension in patients with compensated cirrosis. Gastroenterology. 2013;144:102–111.

    Article  PubMed  Google Scholar 

  24. Kim BK, Han KH, Park JY, et al. A liver stiffness measurement-based, non invasive prediction model for high-risk esophageal varices in B-viral liver cirrhosis. Am J Gastroenterol. 2010;105:1382–1390.

    Article  PubMed  Google Scholar 

  25. Maurice JB, Brodkin E, Arnold F, et al. Validation of the Baveno VI criteria to identify low risk cirrhotic patients not requiring endoscopic surveillance for varices. J Hepatol. 2016;65:899–905.

    Article  PubMed  Google Scholar 

  26. Jangouk P, Turco L, De Oliveira A, et al. Validating, deconstructing and refining Baveno criteria for ruling out high-risk varices in patients with compensated cirrhosis. Liv Int. 2017;37:1177–1183.

    Article  Google Scholar 

  27. Llop E, Lopez M, de la Revilla J, et al. Validation of noninvasive methods to predict the presence of gastroesophageal varices in a cohort of patients with compensated advanced chronic liver disease. J Gastroenterol Hepatol. 2017;32:1867–1872.

    Article  PubMed  Google Scholar 

  28. Marot A, Trépo E, Doerig C, et al. Liver stiffness and platelet count for identifying patients with compensated liver disease at low risk of variceal bleeding. Liv Int. 2017;37:707–716.

    Article  Google Scholar 

  29. Petta S, Sebastiani G, Bugianesi E, et al. Non-invasive prediction of esophageal varices by stiffness and platelet in nonalcoholic fatty liver disease cirrhosis. J Hepatol. 2018;69:878–885.

    Article  PubMed  Google Scholar 

  30. Colecchia A, Marasco G, Taddia M, et al. Liver and spleen stiffness and other noninvasive methods to assess portal hypertension in cirrhotic patients: a review of the literature. Eur J Gastroenterol Hepatol. 2015;27:992–1001.

    Article  PubMed  Google Scholar 

  31. 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.e4–945.e4.

    Google Scholar 

  32. 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.

    Article  PubMed  Google Scholar 

  33. Procopet B, Berzigotti A, Abraldes JG, et al. Real-time shear-wave elastography: applicability, reliability and accuracy for clinically significant portal hypertension. J Hepatol. 2015;62:1068–1075.

    Article  PubMed  Google Scholar 

  34. Elkrief L, Rautou P-E, Ronot M, et al. Prospective comparison of spleen and liver stiffness by using shear-wave and transient elastography for detection of portal hypertension in cirrhosis. Radiology. 2015;275:589–598.

    Article  PubMed  Google Scholar 

  35. Jansen C, Bogs C, Verlinden W, et al. Shear-wave elastography of the liver and spleen identifies clinically significant portal hypertension: a prospective multicentre study. Liv Int. 2017;37:396–405.

    Article  Google Scholar 

  36. Kim TY, Jeong WK, Sohn JH, et al. Evaluation of portal hypertension by real-time shear wave elastography in cirrhotic patients. Liv Int. 2015;35:2416–2424.

    Article  Google Scholar 

  37. Wiesner RH, McDiarmid SV, Kamath PS, et al. MELD and PELD: application of survival models to liver allocation. Liver Transpl. 2001;7:567–580.

    Article  CAS  PubMed  Google Scholar 

  38. Bavu E, Gennisson J-L, Couade M, et al. Noninvasive in vivo liver fibrosis evaluation using supersonic shear imaging: a clinical study on 113 hepatitis C virus patients. Ultrasound Med Biol. 2011;37:1361–1373.

    Article  PubMed  Google Scholar 

  39. Karlas T, Lindner F, Troltzsch M, Keim V. Assessment of spleen stiffness using acoustic radiation force impulse imaging (ARFI): definition of examination standards and impact of breathing maneuvers. Ultraschall Med. 2014;35:38–43.

    Article  CAS  Google Scholar 

  40. Dietrich CF, Bamber J, Berzigotti A, et al. EFSUMB guidelines and recommendations on the clinical use of liver ultrasound elastography, update 2017 (long version). Ultraschall Med. 2017;38:e16–e47.

    PubMed  Google Scholar 

  41. Thiele M, Madsen BS, Procopet B, et al. Reliability criteria for liver stiffness measurements with real-time 2D shear wave elastography in different clinical scenarios of chronic liver disease. Ultraschall Med. 2017;38:648–654.

    Article  PubMed  Google Scholar 

  42. Cho EJ, Kim MY, Lee JH, et al. Diagnostic and prognostic values of noninvasive predictors of portal hypertension in patients with alcoholic cirrhosis. PLoS ONE. 2015;10:e0133935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tsochatzis EA, Bosch J, Burroughs AK. Liver cirrhosis. Lancet. 2014;383:1749–1761.

    Article  PubMed  Google Scholar 

  44. Sikuler E, Groszmann RJ. Interaction of flow and resistance in maintenance of portal hypertension in a rat model. Am J Physiol. 1986;250:G205–G212.

    CAS  PubMed  Google Scholar 

  45. Bhathal PS, Grossman HJ. Reduction of the increased portal vascular resistance of the isolated perfused cirrhotic rat liver by vasodilators. J Hepatol. 1985;1:325–327.

    Article  CAS  PubMed  Google Scholar 

  46. Bolognesi M, Merkel C, Sacerdoti D, et al. The role of spleen enlargement in cirrhosis with portal hypertension. Dig Liv Dis. 2002;34:144–150.

    Article  CAS  Google Scholar 

  47. Tosetti G, Mura VL, Aghemo A, et al. Screening of oesophagogastric varices in virus-related compensated advanced chronic liver disease: beyond the Baveno VI criteria. Dig Liv Dis. 2017;49:e38.

    Article  Google Scholar 

  48. Abraldes JG, Bureau C, Stefanescu H, et al. Noninvasive tools and risk of clinically significant portal hypertension and varices in compensated cirrhosis: the “Anticipate” study. Hepatology. 2016;64:2173–2184.

    Article  CAS  PubMed  Google Scholar 

  49. Hirooka M, Ochi H, Koizumi Y, et al. Splenic elasticity measured with real-time tissue elastography is a marker of portal hypertension. Radiology. 2011;261:960–968.

    Article  PubMed  Google Scholar 

  50. Song J, Huang J, Huang H, et al. Performance of spleen stiffness measurement in prediction of clinical significant portal hypertension: a meta-analysis. Clin Res Hepatol Gastroenterol. 2018;42:216–226.

    Article  PubMed  Google Scholar 

  51. Fraquelli M, Giunta M, Pozzi R, et al. Feasibility and reproducibility of spleen transient elastography and its role in combination with liver transient elastography for predicting the severity of chronic viral hepatitis. J Viral Hepat. 2014;21:90–98.

    Article  CAS  PubMed  Google Scholar 

  52. Stefanescu H, Grigorescu M, Lupsor M, et al. Spleen stiffness measurement using Fibroscan for the noninvasive assessment of esophageal varices in liver cirrhosis patients. J Gastroenterol Hepatol. 2011;26:164–170.

    Article  PubMed  Google Scholar 

  53. Sharma P, Kirnake V, Tyagi P, et al. Spleen stiffness in patients with cirrhosis in predicting esophageal varices. Am J Gastroenterol. 2013;108:1101–1107.

    Article  PubMed  Google Scholar 

  54. 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.e2–101.e2.

    Google Scholar 

  55. Ma X, Wang L, Wu H, et al. Spleen stiffness is superior to liver stiffness for predicting esophageal varices in chronic liver disease: a meta-analysis. PLoS ONE. 2016;11(11).

  56. Colecchia A, Ravaioli F, Marasco G, et al. A combined model based on spleen stiffness measurement and Baveno VI criteria to rule out high risk varices in advanced chronic liver disease. J Hepatol. 2018;69:308–317.

    Article  PubMed  Google Scholar 

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Correspondence to Dimitrios S. Karagiannakis.

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Karagiannakis, D.S., Voulgaris, T., Koureta, E. et al. Role of Spleen Stiffness Measurement by 2D-Shear Wave Elastography in Ruling Out the Presence of High-Risk Varices in Cirrhotic Patients. Dig Dis Sci 64, 2653–2660 (2019). https://doi.org/10.1007/s10620-019-05616-4

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