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A shortened Stroop test to identify covert hepatic encephalopathy and predict overt hepatic encephalopathy in patients with cirrhosis

  • Original Article―Liver, Pancreas, and Biliary Tract
  • Published:
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Abstract

Background

Covert hepatic encephalopathy (CHE) adversely affects the clinical outcomes of patients with cirrhosis but remains largely undiagnosed and untreated. Although the Stroop test is a useful method for CHE detection, a faster, simpler, and more accurate test is required to diagnose CHE. This prospective study aimed to develop a new shortened Stroop test that can detect CHE and predict overt hepatic encephalopathy (OHE) in Japanese patients with cirrhosis.

Methods

Patients who underwent neuropsychological tests (NPT) and the Stroop test between November 2018 and December 2021 were enrolled and followed until OHE occurrence or March 2022. The discriminative ability of various run combinations in the off and on states to detect CHE was evaluated using the area under the receiver-operating characteristic curve (AUC) and compared with that of the total Stroop test time.

Results

Among the 227 eligible patients, the On1–2Time cutoff value of 44.4 s had a comparable discriminative ability with the total Stroop test time to detect CHE, with an AUC of 0.791, a sensitivity of 0.827, and a specificity of 0.685. During a median follow-up period of 16 months, 37 patients developed OHE. On1–2Time ≥ 44.4 s (hazard ratio [HR], 3.93; 95% confidence interval [CI] 1.36–11.36) and serum albumin levels (HR, 0.28; 95% CI 0.11–0.67) were independently associated with OHE occurrence.

Conclusions

The shortened Stroop test (On1–2Time) is equivalent to the total Stroop test not only for identifying CHE but also for estimating the risk of progression to OHE.

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References

  1. Vilstrup H, Amodio P, Bajaj J, et al. Hepatic encephalopathy in chronic liver disease: 2014 practice guideline by the American association for the study of liver diseases and the European association for the study of the liver. Hepatology. 2014;60:715–35.

    Article  PubMed  Google Scholar 

  2. Patidar KR, Bajaj JS. Covert and overt hepatic encephalopathy: diagnosis and management. Clin Gastroenterol Hepatol. 2015;13:2048–61.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Rose CF, Amodio P, Bajaj JS, et al. Hepatic encephalopathy: Novel insights into classification, pathophysiology and therapy. J Hepatol. 2020;73:1526–47.

    Article  PubMed  Google Scholar 

  4. Patidar KR, Thacker LR, Wade JB, et al. Covert hepatic encephalopathy is independently associated with poor survival and increased risk of hospitalization. Am J Gastroenterol. 2014;109:1757–63.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Miyaaki H, Hiraoka A, Haraguchi M, et al. Proposal for new sleep disorder criteria in patients with chronic liver disease: Influence of liver-related complications. Hepatol Res. 2022;52:364–70.

    Article  CAS  PubMed  Google Scholar 

  6. Bajaj JS, Lauridsen M, Tapper EB, et al. Important unresolved questions in the management of hepatic encephalopathy: an ISHEN consensus. Am J Gastroenterol. 2020;115:989–1002.

    Article  PubMed  Google Scholar 

  7. Yoshiji H, Nagoshi S, Akahane T, et al. Evidence-based clinical practice guidelines for liver cirrhosis 2020. J Gastroenterol. 2021;56:593–619.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Yoshiji H, Nagoshi S, Akahane T, et al. Evidence-based clinical practice guidelines for liver cirrhosis 2020. Hepatol Res. 2021;51:725–49.

    Article  PubMed  Google Scholar 

  9. Bajaj JS, Etemadian A, Hafeezullah M, et al. Testing for minimal hepatic encephalopathy in the United States: An AASLD survey. Hepatology. 2007;45:833–4.

    Article  PubMed  Google Scholar 

  10. Tapper EB. Predicting overt hepatic encephalopathy for the population with cirrhosis. Hepatology. 2019;70:403–9.

    PubMed  Google Scholar 

  11. Bajaj JS, Thacker LR, Heuman DM, et al. The Stroop smartphone application is a short and valid method to screen for minimal hepatic encephalopathy. Hepatology. 2013;58:1122–32.

    Article  PubMed  Google Scholar 

  12. Bajaj JS, Heuman DM, Sterling RK, et al. Validation of EncephalApp, smartphone-based stroop test, for the diagnosis of covert hepatic encephalopathy. Clin Gastroenterol Hepatol. 2015;13:1828-35.e1.

    Article  PubMed  Google Scholar 

  13. Allampati S, Duarte-Rojo A, Thacker LR, et al. Diagnosis of minimal hepatic encephalopathy using Stroop EncephalApp: a multicenter US-based norm-based study. Am J Gastroenterol. 2016;111:78–86.

    Article  PubMed  Google Scholar 

  14. Hanai T, Shiraki M, Nishimura K, et al. Usefulness of the Stroop test in diagnosing minimal hepatic encephalopathy and predicting overt hepatic encephalopathy. Hepatol Commun. 2021;5:1518–26.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zeng X, Li XX, Shi PM, et al. Utility of the EncephalApp stroop test for covert hepatic encephalopathy screening in Chinese cirrhotic patients. J Gastroenterol Hepatol. 2019;34:1843–50.

    Article  PubMed  Google Scholar 

  16. Acharya C, Shaw J, Duong N, et al. QuickStroop, a shortened version of EncephalApp, detects covert hepatic encephalopathy with similar accuracy within one minute. Clin Gastroenterol Hepatol. 2022;S1542–3565(22):00005–12. https://doi.org/10.1016/j.cgh.2021.12.047.

    Article  Google Scholar 

  17. Kondo Y, Iwasa M, Kawaratani H, et al. Proposal of Stroop test cut-off values as screening for neuropsychological impairments in cirrhosis: a Japanese multicenter study. Hepatol Res. 2021;51:674–81.

    Article  CAS  PubMed  Google Scholar 

  18. United Nations Development Programm: Human Development Reports. http://hdr.undp.org/en/data. Accessed 2 March 2022.

  19. Corrias M, Turco M, Rui MD, et al. Covert hepatic encephalopathy: does the mini-mental state examination help? J Clin Exp Hepatol. 2014;4:89–93.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kawaguchi T, Konishi M, Kato A, et al. Updating the neuropsychological test system in Japan for the elderly and in a modern touch screen tablet society by resetting the cut-off values. Hepatol Res. 2017;47:1335–9.

    Article  PubMed  Google Scholar 

  21. Tapper EB, Parikh ND, Waljee AK, et al. Diagnosis of minimal hepatic encephalopathy: a systematic review of point-of-care diagnostic tests. Am J Gastroenterol. 2018;113:529–38.

    Article  PubMed  Google Scholar 

  22. Ferenci P, Lockwood A, Mullen K, et al. Hepatic encephalopathy–definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology. 2002;35:716–21.

    Article  PubMed  Google Scholar 

  23. Bajaj JS, Cordoba J, Mullen KD, et al. Review article: the design of clinical trials in hepatic encephalopathy–an International Society for Hepatic Encephalopathy and Nitrogen Metabolism (ISHEN) consensus statement. Aliment Pharmacol Ther. 2011;33:739–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Banich MT, Milham MP, Atchley R, et al. fMri studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. J Cogn Neurosci. 2000;12:988–1000.

    Article  CAS  PubMed  Google Scholar 

  25. Gruber SA, Rogowska J, Holcomb P, et al. Stroop performance in normal control subjects: an fMRI study. Neuroimage. 2002;16:349–60.

    Article  PubMed  Google Scholar 

  26. Kaps L, Hildebrand K, Nagel M, et al. Validation of EncephalApp_Stroop as screening tool for the detection of minimal hepatic encephalopathy in German patients with liver cirrhosis. Clin Res Hepatol Gastroenterol. 2022;46: 101873.

    Article  CAS  PubMed  Google Scholar 

  27. Luo M, Yu XB, Hu SJ, et al. EncephalApp Stroop App predicts poor sleep quality in patients with minimal hepatic encephalopathy due to hepatitis B-induced liver cirrhosis. Saudi J Gastroenterol. 2020;26:120–8.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Cunha-Silva M, Neto FLP, de Araújo PS, et al. EncephalApp Stroop test validation for the screening of minimal hepatic encephalopathy in Brazil. Ann Hepatol. 2022;27: 100543.

    Article  PubMed  Google Scholar 

  29. Enomoto H, Ueno Y, Hiasa Y, et al. Transition in the etiology of liver cirrhosis in Japan: a nationwide survey. J Gastroenterol. 2020;55:353–62.

    Article  PubMed  Google Scholar 

  30. Kamimura K, Sakamaki A, Kamimura H, et al. Considerations of elderly factors to manage the complication of liver cirrhosis in elderly patients. World J Gastroenterol. 2019;25:1817–27.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Montagnese S, Pierre-Emmanuel R, Romero-Gómez M, Stolze Larsen F, Shawcross DL, Thabut D, Vilstrup H, Weissenborn K. EASL clinical practice guidelines on the management of hepatic encephalopathy. J Hepatol. 2022. https://doi.org/10.1016/j.jhep.2022.06.001.

    Article  Google Scholar 

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Acknowledgements

This work was supported by a Grant-in-Aid for Research from the Japan Agency for Medical Research and Development (JP22fk0210113).

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All the authors contributed to the conception and design of this study. TH, KN, TM, TM, YN, KI, AS, and KT: collected and analyzed the data. The first draft of the manuscript was written by TH, and all the authors commented on the previous versions of the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Tatsunori Hanai.

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Hanai, T., Nishimura, K., Miwa, T. et al. A shortened Stroop test to identify covert hepatic encephalopathy and predict overt hepatic encephalopathy in patients with cirrhosis. J Gastroenterol 57, 981–989 (2022). https://doi.org/10.1007/s00535-022-01925-0

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  • DOI: https://doi.org/10.1007/s00535-022-01925-0

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