Hepatic Artery and Portal Vein Hemodynamics in Nonalcoholic Fatty Liver Disease in Adult Saudi Patients: A Doppler Ultrasound Study

ORIGINAL ARTICLE
Abdullah Sulaiman Alshehri, Moawia Gameraddin, Yousef Saeedullah, Marwan Hamid Alaeinbawi, Bilal Rabah Altamimi, Awadia Gareeballah, Suliman Salih, Moa'ath Abdullah Sindi

 
International Journal of Biomedicine. 2023;13(2):259-264.
DOI: 10.21103/Article13(2)_OA10
Originally published June 5, 2023

Abstract: 

Background: Nonalcoholic fatty liver disease (NAFLD) is a growing public health problem. With the growing severity of NAFLD, there are considerable alterations in the hemodynamics of the hepatic circulation that might affect the prognosis of the condition, according to numerous reports written to assess the vasculature of the liver in patients affected with fatty liver disease. The aim of the study was to examine hemodynamic alterations in the hepatic artery (HA) and portal vein (PV) in NAFLD patients and determine how they relate to the severity of the condition, and to classify patients into various categories of NAFLD and connect the results to liver size and body mass index (BMI).
Methods and Results: One hundred and six diagnosed NAFLD patients who attended the Imaging department at King Fahad Hospital from December 2019 to January 2020 were retrospectively studied. The mean age of the patients was 45.75±15.6 years, with a range of 10-79 years. The patients were examined by a TOSHIBA Xario, SSA-660A ultrasound system utilizing a multifrequency convex transducer (2–5 MHz) for all sonographic exams. B-mode assessed the liver parenchyma, and spectral Doppler estimated the HA and PV. The US appearance of hepatosteatosis, according to the severity of echogenicity, was graded (0-3).
Most participants were asymptomatic (76.4%), and diabetes and diabetes with hypertension were diagnosed in 12.3% and 11.3%, respectively. It was observed that grade 1 hepatosteatosis was more prevalent than the other grades: 54 cases versus 41 cases for grade 2 and 11 cases for grade 3. The mean values of liver size and BMI in grade 3 were higher than in grade 1 (P=0.0033 and P=0.0054, respectively). A Spearman test found that the liver size (R=0.19, P=0.05) and BMI (R=0.26, P=0.01) had weak positive, but statistically significant, correlations with the severity of the hepatosteatosis grade. Doppler indices of the HA and PV in NAFLD patients did not differ significantly in hepatosteatosis grades 1-3. Only the PSV and EDV of the main PV showed a significant decrease in the hepatosteatosis grade 2 compared to grade 1 (P=0.0065 and P=0.0234, respectively). Despite the insignificant differences, the Doppler flow parameters of the HA decreased with the severity of hepatic steatosis; for example, the hepatic artery resistive index (HARI) was 0.77±0.16 in grade 1, 0.72±0.16 in grade 2, and 0.75±0.10 in grade 3, respectively. The hepatic artery pulsatility index (HAPI) was 1.62±49 in grade 1, 1.63±.68 in grade 2, and 1.74±0.77 in grade 3. There was also a trend toward a decrease in PSV and end-diastolic velocity (EDV) of HA with the severity of hepatosteatosis. 
Conclusion: The severity of hepatic steatosis is significantly correlated with liver size and BMI. The blood flow parameters of PV and HA decrease with the severity of hepatic steatosis except for the pulsatility index. 

Keywords: 
NAFLD • body mass index • hepatosteatosis • hepatic circulation
References: 
  1. Pouwels S, Sakran N, Graham Y, Leal A, Pintar T, Yang W, Kassir R, Singhal R, Mahawar K, Ramnarain D. Non-alcoholic fatty liver disease (NAFLD): a review of pathophysiology, clinical management and effects of weight loss. BMC Endocr Disord. 2022 Mar 14;22(1):63. doi: 10.1186/s12902-022-00980-1. 
  2. Ahmed A, Wong RJ, Harrison SA. Nonalcoholic Fatty Liver Disease Review: Diagnosis, Treatment, and Outcomes. Clin Gastroenterol Hepatol. 2015 Nov;13(12):2062-70. doi: 10.1016/j.cgh.2015.07.029.
  3. Machado MV, Diehl AM. Pathogenesis of Nonalcoholic Steatohepatitis. Gastroenterology. 2016 Jun;150(8):1769-77. doi: 10.1053/j.gastro.2016.02.066
  4. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo P. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005 Jul;129(1):113-21. doi: 10.1053/j.gastro.2005.04.014.
  5. Chen SH, He F, Zhou HL, Wu HR, Xia C, Li YM. Relationship between nonalcoholic fatty liver disease and metabolic syndrome. J Dig Dis. 2011 Apr;12(2):125-30. doi: 10.1111/j.1751-2980.2011.00487.x. 
  6. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016 Jul;64(1):73-84. doi: 10.1002/hep.28431.
  7.  Strobel D, Bernatik T, Blank W, Will U, Reichel A, Wüstner M, et al. Incidence of bleeding in 8172 percutaneous ultrasound-guided intraabdominal diagnostic and therapeutic interventions - results of the prospective multicenter DEGUM interventional ultrasound study (PIUS study). Ultraschall Med. 2015 Apr;36(2):122-31. doi: 10.1055/s-0034-1399282. 
  8. Webb M, Yeshua H, Zelber-Sagi S, Santo E, Brazowski E, Halpern Z, Oren R. Diagnostic value of a computerized hepatorenal index for sonographic quantification of liver steatosis. AJR Am J Roentgenol. 2009 Apr;192(4):909-14. doi: 10.2214/AJR.07.4016. 
  9. Borges VF, Diniz AL, Cotrim HP, Rocha HL, Andrade NB. Sonographic hepatorenal ratio: a noninvasive method to diagnose nonalcoholic steatosis. J Clin Ultrasound. 2013 Jan;41(1):18-25. doi: 10.1002/jcu.21994. 
  10. Petzold G, Lasser J, Rühl J, Bremer SCB, Knoop RF, Ellenrieder V, Kunsch S, Neesse A. Diagnostic accuracy of B-Mode ultrasound and Hepatorenal Index for graduation of hepatic steatosis in patients with chronic liver disease. PLoS One. 2020 May 1;15(5):e0231044. doi: 10.1371/journal.pone.0231044. 
  11. Lupsor-Platon M, Serban T, Silion AI, Tirpe GR, Tirpe A, Florea M. Performance of Ultrasound Techniques and the Potential of Artificial Intelligence in the Evaluation of Hepatocellular Carcinoma and Non-Alcoholic Fatty Liver Disease. Cancers (Basel). 2021 Feb 14;13(4):790. doi: 10.3390/cancers13040790.
  12. Baz AAM, Mohamed RM, El-kaffas KH. Doppler ultrasound in liver cirrhosis: correlation of hepatic artery and portal vein measurements with model for end-stage liver disease score in Egypt. Egypt J Radiol Nucl Med. 2020;51, 228. doi: 10.1186/s43055-020-00344-6
  13. Adams LA, Angulo P. Role of liver biopsy and serum markers of liver fibrosis in non-alcoholic fatty liver disease. Clin Liver Dis. 2007 Feb;11(1):25-35, viii. doi: 10.1016/j.cld.2007.02.004. 
  14. Charatcharoenwitthaya P, Lindor KD. Role of radiologic modalities in the management of non-alcoholic steatohepatitis. Clin Liver Dis. 2007 Feb;11(1):37-54, viii. doi: 10.1016/j.cld.2007.02.014.
  15. Mottin CC, Moretto M, Padoin AV, Swarowsky AM, Toneto MG, Glock L, Repetto G. The role of ultrasound in the diagnosis of hepatic steatosis in morbidly obese patients. Obes Surg. 2004 May;14(5):635-7. doi: 10.1381/096089204323093408.
  16. Gallix BP, Taourel P, Dauzat M, Bruel JM, Lafortune M. Flow pulsatility in the portal venous system: a study of Doppler sonography in healthy adults. AJR Am J Roentgenol. 1997 Jul;169(1):141-4. doi: 10.2214/ajr.169.1.9207514.
  17. Abangah G, Yousefi A, Asadollahi R, Veisani Y, Rahimifar P, Alizadeh S. Correlation of Body Mass Index and Serum Parameters With Ultrasonographic Grade of Fatty Change in Non-alcoholic Fatty Liver Disease. Iran Red Crescent Med J. 2014 Jan;16(1):e12669. doi: 10.5812/ircmj.12669.
  18. Mihmanli I, Kantarci F, Yilmaz MH, Gurses B, Selcuk D, Ogut G, Altug A, Uysal O. Effect of diffuse fatty infiltration of the liver on hepatic artery resistance index. J Clin Ultrasound. 2005 Mar-Apr;33(3):95-9. doi: 10.1002/jcu.20095.
  19. Alizadeh A, Mansour-Ghanaei F, Roozdar A, Joukar F, Sepehrimanesh M, Hojati SA, Mansour-Ghanaei A. Laboratory Tests, Liver Vessels Color Doppler Sonography, and FibroScan Findings in Patients with Nonalcoholic Fatty Liver Disease: An Observation Study. J Clin Imaging Sci. 2018 Apr 3;8:12. doi: 10.4103/jcis.JCIS_93_17. 
  20. Balci A, Karazincir S, Sumbas H, Oter Y, Egilmez E, Inandi T. Effects of diffuse fatty infiltration of the liver on portal vein flow hemodynamics. J Clin Ultrasound. 2008 Mar-Apr;36(3):134-40. doi: 10.1002/jcu.20440. 
  21. Soresi M, Giannitrapani L, Noto D, Terranova A, Campagna ME, Cefalù AB, Giammanco A, Montalto G. Effects of steatosis on hepatic hemodynamics in patients with metabolic syndrome. Ultrasound Med Biol. 2015 Jun;41(6):1545-52. doi: 10.1016/j.ultrasmedbio.2015.01.020. 
  22. Ulusan S, Yakar T, Koc Z. Evaluation of portal venous velocity with Doppler ultrasound in patients with nonalcoholic fatty liver disease. Korean J Radiol. 2011 Jul-Aug;12(4):450-5. doi: 10.3348/kjr.2011.12.4.450. 
  23. Mohammadinia AR, Bakhtavar K, Ebrahimi-Daryani N, Habibollahi P, Keramati MR, Fereshtehnejad SM, Abdollahzade S. Correlation of hepatic vein Doppler waveform and hepatic artery resistance index with the severity of nonalcoholic fatty liver disease. J Clin Ultrasound. 2010 Sep;38(7):346-52. doi: 10.1002/jcu.20696. 
  24. Mohammadi A, Ghasemi-rad M, Zahedi H, Toldi G, Alinia T. Effect of severity of steatosis as assessed ultrasonographically on hepatic vascular indices in non-alcoholic fatty liver disease. Med Ultrason. 2011 Sep;13(3):200-6.
  25. Balasubramanian P, Boopathy V, Govindasamy E, Venkatesh BP. Assessment of Portal Venous and Hepatic Artery Haemodynamic Variation in Non-Alcoholic Fatty Liver Disease (NAFLD) Patients. J Clin Diagn Res. 2016 Aug;10(8):TC07-10. doi: 10.7860/JCDR/2016/20697.8267. 
  26. Gaiani S, Avogaro A, Bombonato GC, Bolognesi M, Amor F, Vigili de Kreutzenberg S, Guarneri G, Sacerdoti D. Nonalcoholic fatty liver disease (NAFLD) in nonobese patients with diabetes: Prevalence and relationships with hemodynamic alterations detected with Doppler sonography(). J Ultrasound. 2009 Mar;12(1):1-5. doi: 10.1016/j.jus.2008.12.002.
  27. Solhjoo E, Mansour-Ghanaei F, Moulaei-Langorudi R, Joukar F. Comparison of portal vein doppler indices and hepatic vein doppler waveform in patients with nonalcoholic fatty liver disease with healthy control. Hepat Mon. 2011 Sep;11(9):740-4. doi: 10.5812/kowsar.1735143X.729. 
  28. Sabry M, Youssef T, Shaker M, Salama MM, Assem N, Anwar CA. al. Portal venous and hepatic artery hemodynamic variation in non-alcoholic fatty liver disease. Egypt Liver Journal.2021; 11, 58 doi: 10.1186/s43066-021-00130-7
  29. Tana C, Tana M, Rossi S, Silingardi M, Schiavone C. Hepatic artery resistive index (HARI) and non-alcoholic fatty liver disease (NAFLD) fibrosis score in NAFLD patients: cut-off suggestive of non-alcoholic steatohepatitis (NASH) evolution. J Ultrasound. 2016 Mar 29;19(3):183-9. doi: 10.1007/s40477-016-0203-8. 
  30. Aslan A, Türeli D, Aslan M, Tüney D. Effects of nonalcoholic fatty liver disease on the hepatic vein and artery. Journal of Medical Diagnostic Methods. 2014; 3(2):161. doi: 10.4172/2168-9784.1000161
  31. Khanal UP, Paudel B, Gurung G, Hu YS, Kuo CW. Correlational Study of Nonalcoholic Fatty Liver Disease Diagnosed by Ultrasonography with Lipid Profile and Body Mass Index in Adult Nepalese Population. J Med Ultrasound. 2019 Jan-Mar;27(1):19-25. doi: 10.4103/JMU.JMU_53_18. 

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Received January 28, 2023.
Accepted April 9, 2023.
©2023 International Medical Research and Development Corporation.