medigraphic.com
Órgano Oficial de la Asociación Mexicana de Hepatología

2008, Number 3

<< Back Next >>

Ann Hepatol 2008; 7 (3)

Imaging techniques for assessing hepatic fat content in nonalcoholic fatty liver disease

Roldan-Valadez E, Favila R, Martínez-López M, Uribe M, Méndez-Sánchez N

Language: Spanish
References: 89
Page: 212-220
PDF size: 245.91 Kb.


Text Extraction

Nonalcoholic fatty liver disease (NAFLD), an emerging clinical entity with worldwide recognition, is today the most common cause of abnormal liver function tests among adults in the United States. In Mexico City, its prevalence has been reported by our group to be around 14%, but its incidence is higher in the hispanic population in the United States (hispanic population 45%, white population 33%, black population 24%). The main issues in the diagnosis, follow-up, and management of NAFLD are our limited understanding of its pathophysiology and the difficulties involved in developing a noninvasive diagnostic method. Several imaging techniques can detect fatty infiltration of the liver, each with its own advantages and disadvantages. Ultrasound is still in the first option for diagnosis, but its accuracy depends on the operator and the patient’s features. Computed tomography can detect hepatic fat content, but only at a threshold of 30%, and it involves ionizing radiation. Magnetic resonance (MR) spectroscopy is probably the most accurate and fastest method of detecting fat, but it is expensive and the necessary software is still not easily available in most MRI units. MR elastography, a new technique to detect liver stiffness, has not been demonstrated to detect NAFLD, and is still undergoing research in patients with hepatitis and cirrhosis. In conclusion, all these imaging tools are limited in their ability to detect coexisting inflammation and fibrosis. In this review, we discuss the radiological techniques currently used to detect hepatic fat content.


REFERENCES

  1. Lupsor M, Badea R. Imaging diagnosis and quantification of hepatic steatosis: is it an accepted alternative to needle biopsy? Rom J Gastroenterol 2005; 14: 419-425.

  2. Victor RG, Haley RW, Willett DL, Peshock RM, Vaeth PC, Leonard D, Basit M, et al. The Dallas Heart Study: a population-based probability sample for the multidisciplinary study of ethnic differences in cardiovascular health. Am J Cardiol 2004; 93: 1473-1480.

  3. Lizardi-Cervera J, Laparra DI, Chavez-Tapia NC, Ostos ME, Esquivel MU. Prevalence of NAFLD and metabolic syndrome in asymtomatics subjects. Rev Gastroenterol Mex 2006; 71: 453-459.

  4. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40: 1387-1395.

  5. Mendez-Sanchez N, Chavez-Tapia NC, Uribe M. An update on non-alcoholic fatty liver disease. Rev Invest Clin 2004; 56: 72-82.

  6. Clark JM, Brancati FL, Diehl AM. The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroenterol 2003; 98: 960-967.

  7. Mendez-Sanchez N, Arrese M, Zamora-Valdes D, Uribe M. Current concepts in the pathogenesis of nonalcoholic fatty liver disease. Liver Int 2007; 27: 423-433.

  8. Clark JM. The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol 2006;40 Suppl 1: S5-10.

  9. Mendez-Sanchez N, Villa AR, Chavez-Tapia NC, Ponciano-Rodriguez G, Almeda-Valdes P, Gonzalez D, Uribe M. Trends in liver disease prevalence in Mexico from 2005 to 2050 through mortality data. Ann Hepatol 2005; 4: 52-55.

  10. Saadeh S, Younossi ZM, Remer EM, Gramlich T, Ong JP, Hurley M, Mullen KD, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 2002; 123: 745-750.

  11. Mendez-Sanchez N, Motola-Kuba D, Bahena-Aponte J, Chavez-Tapia N, Pichardo-Bahena R, Uribe M. Hypertransaminasemia and severe hepatic steatosis without inflammation. A case report. Ann Hepatol 2003; 2: 183-185.

  12. Mendez-Sanchez N, Chavez-Tapia NC, Villa AR, Sanchez-Lara K, Zamora-Valdes D, Ramos MH, Uribe M. Adiponectin as a protective factor in hepatic steatosis. World J Gastroenterol 2005; 11: 1737-1741.

  13. Mendez-Sanchez N, Chavez-Tapia NC, Zamora-Valdes D, Medina-Santillan R, Uribe M. Hepatobiliary diseases and insulin resistance. Curr Med Chem 2007; 14: 1988-1999.

  14. Mendez-Sanchez N, Chavez-Tapia NC, Zamora-Valdes D, Uribe M. Adiponectin, structure, function and pathophysiological implications in non-alcoholic fatty liver disease. Mini Rev Med Chem 2006; 6: 651-656.

  15. Mendez-Sanchez N, Chavez-Tapia NC, Medina-Santillan R, Villa AR, Sanchez-Lara K, Ponciano-Rodriguez G, Ramos MH, et al. The efficacy of adipokines and indices of metabolic syndrome as predictors of severe obesity-related hepatic steatosis. Dig Dis Sci 2006; 51: 1716-1722.

  16. Marchesini G, Brizi M, Morselli-Labate AM, Bianchi G, Bugianesi E, McCullough AJ, Forlani G, et al. Association of nonalcoholic fatty liver disease with insulin resistance. Am J Med 1999; 107: 450-455.

  17. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Bugianesi E, Lenzi M, McCullough AJ, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes 2001; 50: 1844-1850.

  18. Seidell JC. Obesity, insulin resistance and diabetes—a worldwide epidemic. Br J Nutr 2000; 83 Suppl 1: S5-8.

  19. Rojas R, Palma O, I. Q: Salud Adultos. In: Olaiz G, Rivera J, Shamah T, Rojas R, Villalpando S, Hernández M, J. S, eds. Encuesta Nacional de Salud y Nutrición 2006. Segunda, octubre de 2006 ed. Cuernavaca, Morelos, México: Instituto Nacional de Salud Pública, 2006: 75-82.

  20. Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA 2004; 291: 2847-2850.

  21. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 2002; 287: 356-359.

  22. Tolman KG, Fonseca V, Tan MH, Dalpiaz A. Narrative review: hepatobiliary disease in type 2 diabetes mellitus. Ann Intern Med 2004; 141: 946-956.

  23. Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, Musso A, et al. Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 2002; 123: 134-140.

  24. Marcos A, Fisher RA, Ham JM, Olzinski AT, Shiffman ML, Sanyal AJ, Luketic VA, et al. Selection and outcome of living donors for adult to adult right lobe transplantation. Transplantation 2000; 69: 2410-2415.

  25. Castera L, Negre I, Samii K, Buffet C. Pain experienced during percutaneous liver biopsy. Hepatology 1999; 30: 1529-1530.

  26. Grant A, Neuberger J. Guidelines on the use of liver biopsy in clinical practice. British Society of Gastroenterology. Gut 1999; 45 Suppl 4: IV1-IV11.

  27. Ryan CK, Johnson LA, Germin BI, Marcos A. One hundred consecutive hepatic biopsies in the workup of living donors for right lobe liver transplantation. Liver Transpl 2002; 8: 1114-1122.

  28. Mehta SR, Thomas EL, Bell JD, Johnston DG, Taylor-Robinson SD. Non-invasive means of measuring hepatic fat content. World J Gastroenterol 2008; 14: 3476-3483.

  29. Rinella ME, McCarthy R, Thakrar K, Finn JP, Rao SM, Koffron AJ, Abecassis M, et al. Dual-echo, chemical shift gradient-echo magnetic resonance imaging to quantify hepatic steatosis: Implications for living liver donation. Liver Transpl 2003; 9: 851-856.

  30. Wenker JC, Baker MK, Ellis JH, Glant MD. Focal fatty infiltration of the liver: demonstration by magnetic resonance imaging. AJR Am J Roentgenol 1984; 143: 573-574.

  31. Valls C, Iannacconne R, Alba E, Murakami T, Hori M, Passariello R, Vilgrain V. Fat in the liver: diagnosis and characterization. Eur Radiol 2006; 16: 2292-2308.

  32. 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; 14: 635-637.

  33. Joy D, Thava VR, Scott BB. Diagnosis of fatty liver disease: is biopsy necessary? Eur J Gastroenterol Hepatol 2003; 15: 539-543.

  34. Palmentieri B, de Sio I, La Mura V, Masarone M, Vecchione R, Bruno S, Torella R, et al. The role of bright liver echo pattern on ultrasound B-mode examination in the diagnosis of liver steatosis. Dig Liver Dis 2006; 38: 485-489.

  35. Hepburn MJ, Vos JA, Fillman EP, Lawitz EJ. The accuracy of the report of hepatic steatosis on ultrasonography in patients infected with hepatitis C in a clinical setting: a retrospective observational study. BMC Gastroenterol 2005; 5: 14.

  36. Mathiesen UL, Franzen LE, Aselius H, Resjo M, Jacobsson L, Foberg U, Fryden A, et al. Increased liver echogenicity at ultrasound examination reflects degree of steatosis but not of fibrosis in asymptomatic patients with mild/moderate abnormalities of liver transaminases. Dig Liver Dis 2002; 34: 516-522.

  37. Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD. Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol 1991; 43: 26-31.

  38. Debongnie JC, Pauls C, Fievez M, Wibin E. Prospective evaluation of the diagnostic accuracy of liver ultrasonography. Gut 1981; 22: 130-135.

  39. Saverymuttu SH, Joseph AE, Maxwell JD. Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J (Clin Res Ed) 1986; 292: 13-15.

  40. Iwasaki M, Takada Y, Hayashi M, Minamiguchi S, Haga H, Maetani Y, Fujii K, et al. Noninvasive evaluation of graft steatosis in living donor liver transplantation. Transplantation 2004; 78: 1501-1505.

  41. Ricci C, Longo R, Gioulis E, Bosco M, Pollesello P, Masutti F, Croce LS, et al. Noninvasive in vivo quantitative assessment of fat content in human liver. J Hepatol 1997; 27: 108-113.

  42. Nishino M, Hayakawa K, Nakamura Y, Morimoto T, Mukaihara S. Effects of tamoxifen on hepatic fat content and the development of hepatic steatosis in patients with breast cancer: high frequency of involvement and rapid reversal after completion of tamoxifen therapy. AJR Am J Roentgenol 2003; 180: 129-134.

  43. Bydder GM, Chapman RW, Harry D, Bassan L, Sherlock S, Kreel L. Computed tomography attenuation values in fatty liver. J Comput Tomogr 1981; 5: 33-35.

  44. Kodama Y, Ng CS, Wu TT, Ayers GD, Curley SA, Abdalla EK, Vauthey JN, et al. Comparison of CT methods for determining the fat content of the liver. AJR Am J Roentgenol 2007; 188: 1307-1312.

  45. Ducommun JC, Goldberg HI, Korobkin M, Moss AA, Kressel HY. The relation of liver fat to computed tomography numbers: a preliminary experimental study in rabbits. Radiology 1979; 130: 511-513.

  46. Piekarski J, Goldberg HI, Royal SA, Axel L, Moss AA. Difference between liver and spleen CT numbers in the normal adult: its usefulness in predicting the presence of diffuse liver disease. Radiology 1980; 137: 727-729.

  47. Johnston RJ, Stamm ER, Lewin JM, Hendrick RE, Archer PG. Diagnosis of fatty infiltration of the liver on contrast enhanced CT: limitations of liver-minus-spleen attenuation difference measurements. Abdom Imaging 1998; 23: 409-415.

  48. Jacobs JE, Birnbaum BA, Shapiro MA, Langlotz CP, Slosman F, Rubesin SE, Horii SC. Diagnostic criteria for fatty infiltration of the liver on contrast-enhanced helical CT. AJR Am J Roentgenol 1998; 171: 659-664.

  49. Panicek DM, Giess CS, Schwartz LH. Qualitative assessment of liver for fatty infiltration on contrast-enhanced CT: is muscle a better standard of reference than spleen? J Comput Assist Tomogr 1997; 21: 699-705.

  50. Park SH, Kim PN, Kim KW, Lee SW, Yoon SE, Park SW, Ha HK, et al. Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology 2006; 239: 105-112.

  51. Brancatelli G. Science to practice: Should biopsy be performed in potential liver donors when unenhanced CT shows an unacceptable degree of steatosis for transplantation? Radiology 2006; 239: 1-2.

  52. Reeder SB, Ranallo F, Taylor AJ. CT and MRI for determining hepatic fat content. AJR Am J Roentgenol 2008; 190: W167; author reply W168.

  53. Birnbaum BA, Hindman N, Lee J, Babb JS. Multi-detector row CT attenuation measurements: assessment of intra- and interscanner variability with an anthropomorphic body CT phantom. Radiology 2007; 242: 109-119.

  54. George DK, Goldwurm S, MacDonald GA, Cowley LL, Walker NI, Ward PJ, Jazwinska EC, et al. Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosis. Gastroenterology 1998; 114: 311-318.

  55. Taylor-Robinson SD. Applications of magnetic resonance spectroscopy to chronic liver disease. Clin Med 2001; 1: 54-60.

  56. Cox IJ. Development and applications of in vivo clinical magnetic resonance spectroscopy. Prog Biophys Mol Biol 1996; 65: 45-81.

  57. Danet IM, Semelka RC, Braga L. MR imaging of diffuse liver disease. Radiol Clin North Am 2003; 41: 67-87.

  58. Levenson H, Greensite F, Hoefs J, Friloux L, Applegate G, Silva E, Kanel G, et al. Fatty infiltration of the liver: quantification with phase-contrast MR imaging at 1.5 T vs biopsy. AJR Am J Roentgenol 1991; 156: 307-312.

  59. Pilleul F, Chave G, Dumortier J, Scoazec JY, Valette PJ. Fatty infiltration of the liver. Detection and grading using dual T1 gradient echo sequences on clinical MR system. Gastroenterol Clin Biol 2005; 29: 1143-1147.

  60. Kim SH, Lee JM, Han JK, Lee JY, Lee KH, Han CJ, Jo JY, et al. Hepatic macrosteatosis: predicting appropriateness of liver donation by using MR imaging—correlation with histopathologic findings. Radiology 2006; 240: 116-129.

  61. Hussain HK, Chenevert TL, Londy FJ, Gulani V, Swanson SD, McKenna BJ, Appelman HD, et al. Hepatic fat fraction: MR imaging for quantitative measurement and display—early experience. Radiology 2005; 237: 1048-1055.

  62. Siegelman ES, Rosen MA. Imaging of hepatic steatosis. Semin Liver Dis 2001; 21: 71-80.

  63. Thomas EL, Hamilton G, Patel N, O’Dwyer R, Dore CJ, Goldin RD, Bell JD, et al. Hepatic triglyceride content and its relation to body adiposity: a magnetic resonance imaging and proton magnetic resonance spectroscopy study. Gut 2005; 54: 122-127.

  64. Kotronen A, Westerbacka J, Bergholm R, Pietilainen KH, Yki-Jarvinen H. Liver fat in the metabolic syndrome. J Clin Endocrinol Metab 2007; 92: 3490-3497.

  65. Seppala-Lindroos A, Vehkavaara S, Hakkinen AM, Goto T, Westerbacka J, Sovijarvi A, Halavaara J, et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 2002; 87: 3023-3028.

  66. Kim H, Taksali SE, Dufour S, Befroy D, Goodman TR, Petersen KF, Shulman GI, et al. Comparative MR study of hepatic fat quantification using single-voxel proton spectroscopy, two-point dixon and three-point IDEAL. Magn Reson Med 2008; 59: 521-527.

  67. Gulizia R, Ferraioli G, Filice C. Open questions in the assessment of liver fibrosis using real-time elastography. AJR Am J Roentgenol 2008; 190: W370-371; author reply W372-373.

  68. Yamanaka N, Okamoto E, Toyosaka A, Ohashi S, Tanaka N. Consistency of human liver. J Surg Res 1985; 39: 192-198.

  69. Nishizaki T, Matsumata T, Kamakura T, Adachi E, Sugimachi K. Significance of intraoperative measurement of liver consistency prior to hepatic resection. Hepatogastroenterology 1995; 42: 5-8.

  70. Kusaka K, Harihara Y, Torzilli G, Kubota K, Takayama T, Makuuchi M, Mori M, et al. Objective evaluation of liver consistency to estimate hepatic fibrosis and functional reserve for hepatectomy. J Am Coll Surg 2000; 191: 47-53.

  71. Carter FJ, Frank TG, Davies PJ, McLean D, Cuschieri A. Measurements and modelling of the compliance of human and porcine organs. Med Image Anal 2001; 5: 231-236.

  72. Yeh WC, Li PC, Jeng YM, Hsu HC, Kuo PL, Li ML, Yang PM, et al. Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med Biol 2002; 28: 467-474.

  73. Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991; 13: 111-134.

  74. Sanada M, Ebara M, Fukuda H, Yoshikawa M, Sugiura N, Saisho H, Yamakoshi Y, et al. Clinical evaluation of sonoelasticity measurement in liver using ultrasonic imaging of internal forced low-frequency vibration. Ultrasound Med Biol 2000; 26: 1455-1460.

  75. Sandrin L, Tanter M, Catheline S, Fink M. Shear modulus imaging with 2-D transient elastography. IEEE Trans Ultrason Ferroelectr Freq Control 2002; 49: 426-435.

  76. Sandrin L, Tanter M, Gennisson JL, Catheline S, Fink M. Shear elasticity probe for soft tissues with 1-D transient elastography. IEEE Trans Ultrason Ferroelectr Freq Control 2002; 49: 436-446.

  77. Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, Christidis C, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol 2003; 29: 1705-1713.

  78. Saito H, Tada S, Nakamoto N, Kitamura K, Horikawa H, Kurita S, Saito Y, et al. Efficacy of non-invasive elastometry on staging of hepatic fibrosis. Hepatol Res 2004; 29: 97-103.

  79. Friedrich-Rust M, Ong MF, Herrmann E, Dries V, Samaras P, Zeuzem S, Sarrazin C. Real-time elastography for noninvasive assessment of liver fibrosis in chronic viral hepatitis. AJR Am J Roentgenol 2007; 188: 758-764.

  80. Ziol M, Handra-Luca A, Kettaneh A, Christidis C, Mal F, Kazemi F, de Ledinghen V, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology 2005; 41: 48-54.

  81. Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, Darriet M, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005; 128: 343-350.

  82. Saftoiu A, Gheonea DI, Ciurea T. Hue histogram analysis of real-time elastography images for noninvasive assessment of liver fibrosis. AJR Am J Roentgenol 2007; 189: W232-233.

  83. Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, Ehman RL. Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 1995; 269: 1854-1857.

  84. Muthupillai R, Rossman PJ, Lomas DJ, Greenleaf JF, Riederer SJ, Ehman RL. Magnetic resonance imaging of transverse acoustic strain waves. Magn Reson Med 1996; 36: 266-274.

  85. Rouviere O, Yin M, Dresner MA, Rossman PJ, Burgart LJ, Fidler JL, Ehman RL. MR elastography of the liver: preliminary results. Radiology 2006; 240: 440-448.

  86. Kruse SA, Smith JA, Lawrence AJ, Dresner MA, Manduca A, Greenleaf JF, Ehman RL. Tissue characterization using magnetic resonance elastography: preliminary results. Phys Med Biol 2000; 45: 1579-1590.

  87. Dresner MA, Rose GH, Rossman PJ, Muthupillai R, Manduca A, Ehman RL. Magnetic resonance elastography of skeletal muscle. J Magn Reson Imaging 2001; 13: 269-276.

  88. Fishbein MH, Gardner KG, Potter CJ, Schmalbrock P, Smith MA. Introduction of fast MR imaging in the assessment of hepatic steatosis. Magn Reson Imaging 1997; 15: 287-293.

  89. Dixon JB, Bhathal PS, O’Brien PE. Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology 2001; 121: 91-100.




2020     |     www.medigraphic.com