Clinical applications of spleen ultrasound elastography – a review

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VOLUME 18 , ISSUE 72 (May 2018) > List of articles

Clinical applications of spleen ultrasound elastography – a review

Rafał Mazur / Milena Celmer / Jurand Silicki / Daniel Hołownia / Patryk Pozowski / Krzysztof Międzybrodzki

Keywords : spleen sonoelastography, liver fibrosis, portal hypertension, esophageal varices, myelofibrosis

Citation Information : Journal of Ultrasonography. Volume 18, Issue 72, Pages 37-41, DOI: https://doi.org/10.15557/JoU.2018.0006

License : (OPEN-ACCESS)

Received Date : 25-June-2017 / Accepted: 28-December-2017 / Published Online: 30-March-2018

ARTICLE

ABSTRACT

In the last few years, notable technical progress has taken place in ultrasound elastography. Qualitative methods have been replaced by quantitative ones, such as: transient elastography, acoustic radiation force impulse and shear wave elastography. Owing to the fact that the spleen is superficially located, it is possible to obtain reliable measuring accuracy of its hardness using sonoelastography. Lately, many researchers have been investigating how spleen elasticity changes in patients infected with hepatitis B virus or hepatitis C virus and in patients suffering from liver fibrosis, portal hypertension, esophageal varices or myelofibrosis. In this article, we review the role and current status of accessible qualitative ultrasound elastography methods, including recent advances in the evaluation of spleen stiffness and its clinical utility. As study results demonstrate, spleen stiffness correlates with liver fibrosis and is helpful in determining the level of fibrosis in the METAVIR scoring system. In patients infected with hepatitis B virus or hepatitis C virus, spleen stiffness increases even when liver elasticity remains unaltered. Furthermore, it is useful in diagnosing portal hypertension or predicting existence of esophageal varices. Moreover, in patients suffering from biliary atresia after Kasai portoenterostomy, spleen sonoelastography may be helpful in selecting patients for liver transplantation as well as for choosing the best strategy for portal vein reconstruction before liver transplantation. In myelofibrosis, spleen stiffness correlates with bone marrow fibrosis and may be used to assess the response to treatment. Spleen sonoelastography is also useful in the monitoring of transjugular intrahepatic portosystemic shunt function.

Graphical ABSTRACT

Background

The spleen is the largest lymphatic organ in the human body. The capital functions of the spleen are connected with formation, storage and breakdown of blood cells as well as formation and storage of blood clotting factor VIII. Lymphocytes in splenic lymph follicles take part in antibody biosynthesis. The splenic pulp is responsible for lymphocyte formation, thrombocyte destruction, old red blood cell breakdown as well as keeping and releasing granulocytes(1).

Spleen function abnormalities, splenomegaly and hypersplenism usually result from systemic diseases. Spleen malfunction may be induced by infectious diseases, hemolytic anemia, myeloproliferative disorders, lymphoproliferative diseases, acute leukemia or autoimmune diseases. The splenic vein is directly connected to the portal vein. As a consequence, diseases that affect blood flow in the portal vein may also affect the spleen. Spleen stiffness examinations may therefore be useful in the diagnostic process of liver fibrosis, portal hypertension and esophageal varices.

Elastography is a relatively new non-invasive diagnostic method, which allows the assessment of tissue stiffness(2). It is based on the assumption that pathologically changed tissue is harder than healthy tissue(3). Studies on liver fibrosis, the musculoskeletal system as well as breast, prostate, testicular and thyroid nodules acknowledge this assumption(49). There are two main different types of elastography: ultrasound elastography (EUS) and magnetic resonance elastography. EUS, for the sake of its simplicity, may be divided into qualitative and quantitative. The qualitative method, whereby elasticity values are obtained by exerting rhythmical pressure on the examined tissue, is the least technically advanced. Measurements may be also performed with the probe held motionlessly owing to the internal organs’ physiological movements which generate strain images. Technical progress has resulted in the improvement of this method and led to the formation of quantitative elastography methods such as: transient elastography (FibroScan), acoustic radiation force impulse (ARFI) and shear wave elastography (SWE) (Fig. 1).

Fig. 1

SWE view of the spleen in a healthy patient. ROI put at a site of homogeneous hardness

JoU-2018-0006-g001.jpg

Spleen stiffness evaluation has been of interest to numerous researchers in the last few years. Since it is known that dynamic elastography methods produce reliable outcomes, they have been used to assess how the spleen hardness changes in different diseases. The aim of this review was to systemize the latest discoveries relating to spleen stiffness assessment carried out with quantitative ultrasound elastography techniques.

Spleen elastography in healthy subjects

Spleen examination with sonoelastography requires determination of normal values for healthy individuals. Different studies have been conducted to assess the mean value of spleen stiffness and standards for its examination. The measurements of spleen stiffness are obtained with the patient in the supine position; in most cases, the examination has been conducted with the left arm in maximum abduction and by placing the probe in the left intercostal space(1015). Increased spleen stiffness on deep breaths in adults has been confirmed(12). In order to minimize respiratory motion, it is common to instruct patients to hold their breath(4,14). This enables one to obtain a stable homogeneous elastogram with complete filling, both spatially and temporally. In children, who cannot control breathing, the measurements are performed during free respiration and are not invalidated by breathing or other motions(1011). The measurements can be taken using a linear or convex probe. Research has proven that there is no significant difference in the mean values obtained using the two types of probes, but a higher variability was observed when using a convex transducer(10). Moreover, Mi-Jung Lee et al. have proven that ARFI measurements are feasible for solid abdominal organs in children using high- or low-frequency probes(11).

The spleen is the organ with the highest rigidity as measured by ARFI in the abdominal viscera in adults(10,16). According to Pawluś et al. the mean value of spleen stiffness is 16.6 ± 2.5 kPa: in men (N = 25) it is 17.3 ± 2.7 kPa, and women (N = 34) 16.1 ± 2.2 kPa. Leung et al. obtained similar values at a level of 17.3 ± 2.6 kPa(4,14). The mean ARFI-derived velocity for the spleen in adults equals 2.46 ± 0.35 m/s(12,16). No correlation between gender and elasticity of the spleen has been detected, although there are studies suggesting that gender may influence ARFI SWVs(1011,1314). Authors have also assessed the dependence of the dimensions of the spleen on its stiffness and did not find any interconnections(1314). The data on spleen stiffness dependence on age are divergent in various studies. The results of research in adults are independent of age, while studies in children show age-related correlations(1011,1314). Spleen stiffness in elastography techniques increases after food intake. Patients may be misclassified with higher stages of fibrosis if they are assessed within less than a three-hour fasting period(15).

Spleen stiffness in liver fibrosis

One of the applications of spleen elastography is the assessment of liver fibrosis and determining its METAVIR score. As it is known, the spleen is one of the extrahepatic reservoirs of hepatitis C virus and extrahepatic hepatitis B virus replication sites(1719). Studies have provided evidence that spleen stiffness correlates with the progression of liver fibrosis(4,2025). The more advanced the liver fibrosis, the stiffer the spleen (Tab. 1, Fig. 2)(4,2025). The dependence is stronger in significant liver fibrosis (METAVIR ≥2). Worth mentioning is the fact that spleen hardness increases in patients infected with HBV or HCV, even when liver elasticity remains unaltered(25).

Tab. 1

METAVIR score of liver fibrosis based on spleen elastography

AuthorSpleen stiffness in kPa
F0F1F2F3F4
Leung et al.17.3 ± 2.619.419.820.622
Rewisha et al.19.41 ± 3.6325.56 ± 5.3646.19 ± 16.29
Giunta et al.--36-46
Grgurevic et al.-232435
Fig. 2

SWE view of the spleen in a patient with advanced liver fibrosis. ROI put at a site of increased hardness

JoU-2018-0006-g002.jpg

Correlation between portal hypertension, esophageal varices and spleen stiffness

Cirrhosis is the last stage of liver fibrosis and may be induced by many factors such as: liver viral infections, chronic alcohol abuse, autoimmune hepatitis, congenital and acquired metabolic diseases, chronic biliary tract diseases accompanied by cholestasis and chronic treatment with certain drugs (e.g. methotrexate, amiodarone, isoniazid). Portal hypertension and esophageal varices are the consequences of advanced liver fibrosis. The portal vein is directly connected with the splenic vein, and therefore, disorders in the portal vein blood flow may affect the spleen. The superiority of spleen elastography over liver elastography results from the fact that the spleen is not affected by the disease that is the primary cause of portal hypertension. This suggests that spleen stiffness may be a more accurate parameter for the detection of portal hypertension and esophageal varices than liver stiffness. In cirrhotic patients, screening for esophageal varices is highly recommended and extremely important. As a few studies have proven, spleen stiffness correlates with the presence of portal hypertension(2632), but this dependence is not precise enough to assess its degree. Nevertheless, study results show that spleen elastography could be used to suggest the presence of clinically significant portal hypertension(2632). The values of spleen stiffness obtained in patients with clinically significant portal hypertension were between 35.6–75 kPa(2632).

A meta-analysis conducted by Ma et al. proves that spleen elastography may be applicable in identifying patients with esophageal varices, and there is evidence concerning its superiority over liver elastography in this particular disease(27). However, Park et al. demonstrates that the usefulness of spleen elastography in detecting esophageal varices depends on the cause of cirrhosis. According to this study spleen elastography is not a reliable predictor of esophageal varices induced by alcoholic cirrhosis(33). According to available studies, spleen elastography is not useful in assessing the grade of esophageal varices(27,3335). Single studies show that spleen stiffness correlates with clinical history of variceal bleeding(3637), but its utility in determining the risk of bleeding from esophageal varices requires further investigation.

Other applications

Sonoelastography of the spleen is also used to diagnose and evaluate other medical conditions. Spleen stiffness correlates with the portal vein diameter, portal hypertension and liver dysfunction in patients suffering from biliary atresia after Kasai protoenterostomy(38). According to Uchida et al., spleen elastography in these patients could be used to assess the severity of portal hypertension and liver dysfunction in a non-invasive way, and may be helpful in selecting patients for liver transplantation, as well as for choosing the best strategy for portal vein reconstruction before liver transplantation(38).

Patients suffering from myelofibrosis can be distinguished from healthy individuals by FibroScan and SWE of the spleen. However, these measurements have little ability to distinguish between patients with myelofibrosis and cirrhosis of the liver(39). Other authors suggest that Transient Elastography is a user-friendly approach to the evaluation of spleen stiffness in primary myelofibrosis patients as a marker of the bone marrow fibrosis status and as a means of monitoring their response to innovative myelofibrosis therapies(40). Another example of spleen elastography utilization is monitoring of transjugular intrahepatic portosystemic shunt (TIPS) function; it has been proven that splenic SWV is compatible with splenoportal venous velocity in the quantitative monitoring of the TIPS function and in determining TIPS dysfunction(41).

To conclude, spleen sonoelastography is useful in miscellaneous groups of disorders, inter alia those that cause splenomegaly, including infections, deposition diseases and lymphoproliferative disorders. However, there are few publications available on this subject, which makes it an interesting field for new research.

Conclusion

Even though spleen elastography is not widely applied, it has been proven to be clinically helpful. Firstly, it might be used for non-invasive liver fibrosis assessment. As research reveals, spleen stiffness changes earlier than liver hardness in patients infected with HCV or HBV without significant liver fibrosis. Secondly, it correlates with blood flow changes in the portal vein, which helps detect portal hypertension. Additionally, spleen stiffness is helpful in the prediction of esophageal varices. Several studies have shown the value of spleen elasticity assessment as a supplementary tool in the treatment of biliary atresia and in myelofibrosis (diagnosis, bone marrow fibrosis assessment and evaluation of the treatment response). The practical usefulness of spleen elastography in other hematological diseases remains unclear and requires further investigation.

Conflict of interest

There are no financial or other relations that could lead to a conflict of interest.

References


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  9. Jędrzejwski G,Wieczorek AP,Wieloparametryczna ultrasonografia w diagnostyce worka mosznowego i jąder niezstąpionych u chłopców J Ultrason 2013 13 425 430
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  10. Cañas T,Fontanilla T,Miralles M,Maciá A,Malalana A,Román E,Normal values of spleen stiffness in healthy children assessed by acoustic radiation force impulse imaging (ARFI): Comparison between two ultrasound transducers Pediatr Radiol 2015 45 1316 1322
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  11. Lee MJ,Kim MJ,Han KH,Yoon CS,Age-related changes in liver, kidney, and spleen stiffness in healthy children measured with acoustic radiation force impulse imaging Eur J Radiol 2013 82 e290 e294
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  12. Karlas T,Lindner F,Tröltzsch 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
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  13. Arda K,Ciledag N,Aktas E,Aribas BK,Köse K,Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography AJR Am J Roentgenol 2011 197 532 536
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  14. Pawluś A,Inglot MS,Szymańska K,Kaczorowski K,Markiewicz BD,Kaczorowska A,Shear wave elastography of the spleen: evaluation of spleen stiffness in healthy volunteers Abdom Radiol (NY 2016 41 2169 2174
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  15. Kjaergaard M,Thiele M,Madsen BS,Jansen C,Trebicka J,Krag A,High risk of misclassifying liver stiffness using 2D shear-wave and transient elastography during a moderate or high calorie meal Hepatology 2015 62 594A 595A
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  16. Gallotti A,D’Onofrio M,Pozzi Mucelli R,Acoustic Radiation Force Impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen Radiol Med 2010 115 889 897
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  17. Baré P,Hepatitis C virus and peripheral blood mononuclear cell reservoirs Patricia Baré World J Hepatol 2009 1 67 71
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  18. Laskus T,Radkowski M,Wang LF,Vargas H,Rakela J,Search for hepatitis C virus extrahepatic replication sites in patients with acquired immunodeficiency syndrome: Specific detection of negative-strand viral RNA in various tissues Hepatology 1998 28 1398 1401
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  19. Di Bisceglie AM,Hoofnagle JH,Hepatitis B virus replication within the human spleen J Clin Microbiol 1990 28 2850 2852
  20. Trovato FM,Atzori S,Musumeci G,Tooley V,Marcinkowski H,Crossey MM,Liver and spleen transient elastography and Acoustic Radiation Force Impulse Measurements Performance and comparison of measurements in the same area concurrently assessed for liver fibrosis by biopsy. Adv Med Sci 2015 60 300 306
  21. Rewisha EA,Elsabaawy MM,Alsebaey A,Elmazaly MA,Tharwa ES,Evaluation of the role of liver and splenic transient elastography in chronic hepatitis C related fibrosis J Liver Disease Transplant 2016 5 3.
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  22. Giunta M,Conte D,Fraquelli M,Role of spleen elastography in patients with chronic liver diseases World J Gastroenterol 2016 22 7857 7867
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  23. Grgurevic I,Puljiz Z,Brnic D,Bokun T,Heinzl R,Lukic A,Liver and spleen stiffness and their ratio assessed by real-time two dimensional-shear wave elastography in patients with liver fibrosis and cirrhosis due to chronic viral hepatitis Eur Radiol 2015 25 3214 3221
    [CROSSREF]
  24. Ye XP,Ran HT,Cheng J,Zhu YF,Zhang DZ,Zhang P,Liver and spleen stiffness measured by acoustic radiation force impulse elastography for noninvasive assessment of liver fibrosis and esophageal varices in patients with chronic hepatitis B J Ultrasound Med 2012 31 1245 1253
    [CROSSREF]
  25. Pawluś A,Inglot M,Chabowski M,Szymańska K,Inglot M,Patyk M,Shear wave elastography (SWE) of the spleen in patients with hepatitis B and C but without significant liver fibrosis Br J Radiol 2016 89 20160423.
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  26. Jansen C,Bogs C,Verlinden W,Thiele M,Möller P,Görtzen J,Shear-wave elastography of the liver and spleen identifies clinically significant portal hypertension: A prospective multicentre study Liver Int 2017 37 396 405
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  27. Ma X,Wang L,Wu H,Feng Y,Han X,Bu H,Spleen stiffness is superior to liver stiffness for predicting esophageal varices in chronic liver disease: A meta-analysis PLoS ONE 2016 11 e0165786
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  28. Rosselli M,Roccarina D,Patch D,Sekhar M,Majumdar A,O’Beirne J,Point shear wave elastography (ElastPQ) is a reliable non-invasive tool for the diagnosis and characterisation of portal hypertension J Hepatol 2017 66 S667.
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  38. Uchida H,Sakamoto S,Kobayashi M,Shigeta T,Matsunami M,Sasaki K,The degree of spleen stiffness measured on acoustic radiation force impulse elastography predicts the severity of portal hypertension in patients with biliary atresia after portoenterostomy J Pediatr Surg 2015 50 559 564
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  39. Webb M,Shibolet O,Halpern Z,Nagar M,Amariglio N,Levit S,Assessment of liver and spleen stiffness in patients with myelofibrosis using FibroScan and shear wave elastography Ultrasound Q 2015 31 166 169
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  40. Iurlo A,Cattaneo D,Giunta M,Gianelli U,Consonni D,Fraquelli M,Transient elastography spleen stiffness measurements in primary myelofibrosis patients: A pilot study in a single centre Br J Haematol 2015 170 890 892
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  41. Gao J,Zheng X,Zheng YY,Zuo GQ,Ran HT,Auh YH,Shear wave elastography of the spleen for monitoring transjugular intrahepatic portosystemic shunt function: A pilot study J Ultrasound Med 2016 35 951 958
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FIGURES & TABLES

Fig. 1

SWE view of the spleen in a healthy patient. ROI put at a site of homogeneous hardness

Full Size   |   Slide (.pptx)

Fig. 2

SWE view of the spleen in a patient with advanced liver fibrosis. ROI put at a site of increased hardness

Full Size   |   Slide (.pptx)

REFERENCES

  1. Traczyk W,Fizjologia człowieka w zarysie PZWL, Warszawa journal 1992 231 237
  2. Bamber J,Cosgrove D,Dietrich CF,Fromageau J,Bojunga J,Calliada F,EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography Part 1: Basic principles and technology. Ultraschall Med 2013 34 169 184
  3. Ophir J,Céspedes I,Ponnekanti H,Yazdi Y,Li X,Elastography: A quantitative method for imaging the elasticity of biological tissues Ultrason Imaging 1991 13 111 134
    [CROSSREF]
  4. Leung VY,Shen J,Wong VW,Abrigo J,Wong GL,Chim AM,Quantitative elastography of liver fibrosis and spleen stiffness in chronic hepatitis B carriers: Comparison of shear-wave elastography and transient elastography with liver biopsy correlation Radiology 2013 269 910 918
    [CROSSREF]
  5. Zaleska-Dorobisz U,Pawluś A,Szymańska K,Łasecki M,Ziajkiewicz M,Ultrasound elastography: Review of techniques and its clinical applications in pediatrics Part 2. Adv Clin Exp Med 2015 24 725 730
    [CROSSREF]
  6. Porsch M,Görner C,Wendler JJ,Liehr UB,Lux A,Siedentopf S,Elastografia fali poprzecznej nie pozwala na odróżnienie zmian w sterczu o charakterze złośliwym i łagodnym – analiza porównawcza wyników biopsji, badania histopatologicznego i elastografii J Ultrason 2016 16 348 358
    [CROSSREF]
  7. Dobruch-Sobczak K,Różnicowanie charakteru litych zmian ogniskowych w piersiach w sonoelastografii kompresyjnej Część II: Ocena wartości diagnostycznej klasyfikacji BIRADS-usg, skali Tsukuba oraz wskaźnika FLR. J Ultrason 2012 13 31 49
  8. Paluch Ł,Nawrocka-Laskus E,Wieczorek J,Mruk B,Frel M,Walecki J,Use of ultrasound elastography in the assessment of the musculoskeletal system Pol J Radiol 2016 81 240 246
    [CROSSREF]
  9. Jędrzejwski G,Wieczorek AP,Wieloparametryczna ultrasonografia w diagnostyce worka mosznowego i jąder niezstąpionych u chłopców J Ultrason 2013 13 425 430
    [CROSSREF]
  10. Cañas T,Fontanilla T,Miralles M,Maciá A,Malalana A,Román E,Normal values of spleen stiffness in healthy children assessed by acoustic radiation force impulse imaging (ARFI): Comparison between two ultrasound transducers Pediatr Radiol 2015 45 1316 1322
    [CROSSREF]
  11. Lee MJ,Kim MJ,Han KH,Yoon CS,Age-related changes in liver, kidney, and spleen stiffness in healthy children measured with acoustic radiation force impulse imaging Eur J Radiol 2013 82 e290 e294
    [CROSSREF]
  12. Karlas T,Lindner F,Tröltzsch 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
    [CROSSREF]
  13. Arda K,Ciledag N,Aktas E,Aribas BK,Köse K,Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography AJR Am J Roentgenol 2011 197 532 536
    [CROSSREF]
  14. Pawluś A,Inglot MS,Szymańska K,Kaczorowski K,Markiewicz BD,Kaczorowska A,Shear wave elastography of the spleen: evaluation of spleen stiffness in healthy volunteers Abdom Radiol (NY 2016 41 2169 2174
    [CROSSREF]
  15. Kjaergaard M,Thiele M,Madsen BS,Jansen C,Trebicka J,Krag A,High risk of misclassifying liver stiffness using 2D shear-wave and transient elastography during a moderate or high calorie meal Hepatology 2015 62 594A 595A
    [CROSSREF]
  16. Gallotti A,D’Onofrio M,Pozzi Mucelli R,Acoustic Radiation Force Impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen Radiol Med 2010 115 889 897
    [CROSSREF]
  17. Baré P,Hepatitis C virus and peripheral blood mononuclear cell reservoirs Patricia Baré World J Hepatol 2009 1 67 71
    [CROSSREF]
  18. Laskus T,Radkowski M,Wang LF,Vargas H,Rakela J,Search for hepatitis C virus extrahepatic replication sites in patients with acquired immunodeficiency syndrome: Specific detection of negative-strand viral RNA in various tissues Hepatology 1998 28 1398 1401
    [CROSSREF]
  19. Di Bisceglie AM,Hoofnagle JH,Hepatitis B virus replication within the human spleen J Clin Microbiol 1990 28 2850 2852
  20. Trovato FM,Atzori S,Musumeci G,Tooley V,Marcinkowski H,Crossey MM,Liver and spleen transient elastography and Acoustic Radiation Force Impulse Measurements Performance and comparison of measurements in the same area concurrently assessed for liver fibrosis by biopsy. Adv Med Sci 2015 60 300 306
  21. Rewisha EA,Elsabaawy MM,Alsebaey A,Elmazaly MA,Tharwa ES,Evaluation of the role of liver and splenic transient elastography in chronic hepatitis C related fibrosis J Liver Disease Transplant 2016 5 3.
    [CROSSREF]
  22. Giunta M,Conte D,Fraquelli M,Role of spleen elastography in patients with chronic liver diseases World J Gastroenterol 2016 22 7857 7867
    [CROSSREF]
  23. Grgurevic I,Puljiz Z,Brnic D,Bokun T,Heinzl R,Lukic A,Liver and spleen stiffness and their ratio assessed by real-time two dimensional-shear wave elastography in patients with liver fibrosis and cirrhosis due to chronic viral hepatitis Eur Radiol 2015 25 3214 3221
    [CROSSREF]
  24. Ye XP,Ran HT,Cheng J,Zhu YF,Zhang DZ,Zhang P,Liver and spleen stiffness measured by acoustic radiation force impulse elastography for noninvasive assessment of liver fibrosis and esophageal varices in patients with chronic hepatitis B J Ultrasound Med 2012 31 1245 1253
    [CROSSREF]
  25. Pawluś A,Inglot M,Chabowski M,Szymańska K,Inglot M,Patyk M,Shear wave elastography (SWE) of the spleen in patients with hepatitis B and C but without significant liver fibrosis Br J Radiol 2016 89 20160423.
    [CROSSREF]
  26. Jansen C,Bogs C,Verlinden W,Thiele M,Möller P,Görtzen J,Shear-wave elastography of the liver and spleen identifies clinically significant portal hypertension: A prospective multicentre study Liver Int 2017 37 396 405
    [CROSSREF]
  27. Ma X,Wang L,Wu H,Feng Y,Han X,Bu H,Spleen stiffness is superior to liver stiffness for predicting esophageal varices in chronic liver disease: A meta-analysis PLoS ONE 2016 11 e0165786
    [CROSSREF]
  28. Rosselli M,Roccarina D,Patch D,Sekhar M,Majumdar A,O’Beirne J,Point shear wave elastography (ElastPQ) is a reliable non-invasive tool for the diagnosis and characterisation of portal hypertension J Hepatol 2017 66 S667.
    [CROSSREF]
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