Bedside ultrasound in the diagnosis of nonalcoholic fatty liver disease

Abstract

Non-alcoholic fatty liver disease (NAFLD) is the most common liver disease in the United States. While the American Association for the Study of Liver Diseases guidelines define NAFLD as hepatic steatosis detected either on histology or imaging without a secondary cause of abnormal hepatic fat accumulation, no imaging modality is recommended as standard of care for screening or diagnosis. Bedside ultrasound has been evaluated as a non-invasive method of diagnosing NAFLD with the presence of characteristic sonographic findings. Prior studies suggest characteristic sonographic findings for NAFLD include bright hepatic echoes, increased hepatorenal echogenicity, vascular blurring of portal or hepatic vein and subcutaneous tissue thickness. These sonographic characteristics have not been shown to aid bedside clinicians easily identify potential cases of NAFLD. While sonographic findings such as attenuation of image, diffuse echogenicity, uniform heterogeneous liver, thick subcutaneous depth, and enlarged liver filling of the entire field could be identified by clinicians from bedside ultrasound. The accessibility, ease of use, and low-side effect profile of ultrasound make bedside ultrasound an appealing imaging modality in the detection of hepatic steatosis. When used with appropriate clinical risk factors and steatosis involves greater than 33% of the liver, ultrasound can reliably diagnose NAFLD. Despite the ability of ultrasound in detecting moderate hepatic steatosis, it cannot replace liver biopsy in staging the degree of fibrosis. The purpose of this review is to examine the diagnostic accuracy, utility, and limitations of ultrasound in the diagnosis of NAFLD and its potential use by clinicians in routine practices.

Full text

Bedside ultrasound in the diagnosis of nonalcoholic fatty
liver disease
Nancy Khov, Amol Sharma, Thomas R Riley
Nancy Khov, Department of Internal Medicine, Pennsylvania
State Milton S. Hershey Medical Center and School of Medicine,
Hershey, PA 17033, United States
Amol Sharma, Thomas R Riley, Division of Gastroenterology
and Hepatology, Department of Internal Medicine, Pennsylvania
State Milton S. Hershey Medical Center and School of Medicine,
Hershey, PA 17033, United States
Author contributions: Khov N and Sharma A performed the
literature search and wrote the paper; Riley TR participated in
drafting the outline and revised the paper.
Correspondence to: Nancy Khov, MD, Department of Internal
Medicine, Pennsylvania State Milton S. Hershey Medical Cen-
ter and School of Medicine, 500 University Drive, Hershey, PA
17033, United States. nkhov@hmc.psu.edu
Telephone: +1-717-5315160 Fax: +1-717-5312034
Received: November 18, 2013 Revised: January 25, 2014
Accepted: March 19, 2014
Published online: June 14, 2014
Abstract
Non-alcoholic fatty liver disease (NAFLD) is the most
common liver disease in the United States. While the
American Association for the Study of Liver Diseases
guidelines dene NAFLD as hepatic steatosis detected
either on histology or imaging without a secondary
cause of abnormal hepatic fat accumulation, no imag-
ing modality is recommended as standard of care for
screening or diagnosis. Bedside ultrasound has been
evaluated as a non-invasive method of diagnosing
NAFLD with the presence of characteristic sonographic
ndings. Prior studies suggest characteristic sonograph-
ic findings for NAFLD include bright hepatic echoes,
increased hepatorenal echogenicity, vascular blurring
of portal or hepatic vein and subcutaneous tissue thick-
ness. These sonographic characteristics have not been
shown to aid bedside clinicians easily identify potential
cases of NAFLD. While sonographic findings such as
attenuation of image, diffuse echogenicity, uniform
heterogeneous liver, thick subcutaneous depth, and en-
larged liver lling of the entire eld could be identied
REVIEW
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DOI:10.3748/wjg.v20.i22.6821
World J Gastroenterol 2014 June 14; 20(22): 6821-6825
ISSN 1007-9327 (print) ISSN 2219-2840 (online)
© 2014 Baishideng Publishing Group Inc. All rights reserved.
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by clinicians from bedside ultrasound. The accessibility,
ease of use, and low-side effect profile of ultrasound
make bedside ultrasound an appealing imaging modali-
ty in the detection of hepatic steatosis. When used with
appropriate clinical risk factors and steatosis involves
greater than 33% of the liver, ultrasound can reliably
diagnose NAFLD. Despite the ability of ultrasound in
detecting moderate hepatic steatosis, it cannot replace
liver biopsy in staging the degree of brosis. The pur-
pose of this review is to examine the diagnostic accura-
cy, utility, and limitations of ultrasound in the diagnosis
of NAFLD and its potential use by clinicians in routine
practices.
© 2014 Baishideng Publishing Group Inc. All rights reserved.
Key words: Non-alcoholic fatty liver disease; Non-alco-
holic steatohepatitis; Liver brosis; Liver biopsy; Liver
disease; Liver cirrhosis; Steatosis; Bedside ultrasound
Core tip: Ultrasound is a non-invasive, widely available,
and accurate tool in the detection of Non-alcoholic fatty
liver disease (NAFLD). Ultrasound should be used as
the rst-line diagnostic test in patients with abnormal
liver enzymes when other causes are excluded. Clinical
risk factors, when used with ultrasound ndings, have
high accuracy in identifying NAFLD patients. We pres-
ent an algorithm for chronic abnormal liver enzymes
that illustrates the use of ultrasound in reducing the
need for liver biopsy in the diagnosis of NAFLD. Clini-
cians should be aware of the known limitations of ultra-
sound, including the inability to grade or stage brosis
in NAFLD patients.
Khov N, Sharma A, Riley TR. Bedside ultrasound in the diag-
nosis of nonalcoholic fatty liver disease. World J Gastroenterol
2014; 20(22): 6821-6825 Available from: URL: http://www.wjg-
net.com/1007-9327/full/v20/i22/6821.htm DOI: http://dx.doi.
org/10.3748/wjg.v20.i22.6821

INTRODUCTION
The potential role of ultrasound by the clinician is in-
creasing. The estimated prevalence of non-alcoholic fatty
liver disease (NAFLD) is approximately 34%. Strongly
associated with metabolic syndrome, the incidence of
NAFLD will continue to rise with the projected progres-
sion of the obesity epidemic[1,2]. NAFLD includes a wide
spectrum of disease activity, from simple steatosis to
non-alcoholic steatohepatitis (NASH)[3,4]. Simple steatosis
has a benign and potentially reversible course, however,
NASH can progress to advanced brosis, cirrhosis, and
hepatocellular carcinoma[3,4]. The diagnosis of NAFLD
remains under recognized as most patients are asymp-
tomatic until late stages of disease[5]. Liver biopsy is the
gold standard in diagnosing NAFLD and the most accu-
rate tool for grading brosis, however is invasive and car-
ries the risk of complications[2,3]. Bedside ultrasound, as a
non-invasive and readily available tool, has an important
role in diagnosing NAFLD. In this paper we present a
review of current knowledge and literature on the utility
of beside ultrasound in the diagnosis of NAFLD by the
clinician.
CHARACTERISTIC SONOGRAPHIC
FEATURES OF NAFLD
High diagnostic accuracy can be achieved by the ultra-
sound when sonographic features unique to NAFLD are
standardized and used to aid in diagnosis. Bright hepatic
echoes, increased hepatorenal echogenicity and vascular
blurring of portal or hepatic vein have been classied as
unique sonographic features of NAFLD. In a prospec-
tive study by Dasarathy et al[6], real time ultrasound was
performed followed by a liver biopsy to evaluate the ac-
curacy of ultrasound in hepatic steatosis. When steatosis
was greater than 20% on biopsy, these sonographic fea-
tures were able to predict the presence of NAFLD with
greater than 90% sensitivity. Lower levels of fat content
resulted in reduction of sensitivity[6]. A sonographic
scoring system used by Hamaguchi et al[7] was developed
based on similar pre-determined imaging findings. By
using hepatorenal echo contrast, liver brightness, deep
attenuation and vascular blurring, they were able to re-
port similar sensitivities in detecting histologically proven
NAFLD[7].
Subcutaneous tissue thickness, measured as the dis-
tance between the skin surface and the liver surface, has
been shown to be another characteristic sonographic
nding. When compared to other non-NAFLD liver dis-
eases, NAFLD patients had thicker subcutaneous tissue,
with a mean measurement of 25.6 ± 5.6 mm. In com-
parison, the non-NAFLD patients had a mean subcuta-
neous tissue thickness of 19.5 ± 5.2 mm. NAFLD was
unlikely when the subcutaneous tissue thickness was less
than 20 mm[8]. Along with subcutaneous tissue thickness,
Riley et al[9] dened ve characteristic sonographic nd-
ings for NAFLD that can be identied by the clinician:
(1) attenuation of image quickly within 4-5 cm of depth,
making deeper structures difcult to decipher; (2) echo-
genic diffusely but particularly important to note bright-
ness within the rst 2-3 cm of depth; (3) liver uniformly
heterogeneous; (4) thick subcutaneous depth (> 2 cm);
and (5) liver lls entire eld with no edges visible (viewed
as helpful but not necessary for diagnosis), as shown in
a prototypical bedside ultrasound image in Figure 1. Us-
ing these characteristic sonographic findings, bedside
ultrasound yielded a sensitivity of 80% and specicity of
99%.
EASE OF CLINICAL USE AND
INTERPRETATION
These typical sonographic features can be identified by
the clinician with the use of bedside ultrasound. Ultra-
sound can result in an immediate diagnosis and devel-
opment of a plan of care at the initial visit. Riley et al[9]
demonstrated that clinical providers could be trained to
identify ultrasound images consistent with NAFLD after
a brief 20-min session. Healthcare providers were subse-
quently able to reliably identify NAFLD using the proto-
type image with substantial inter-observer agreement, κ
= 0.76[9].
ULTRASOUND AS A DIAGNOSTIC TOOL
In patients with chronic hepatitis, an algorithm weighing
the relative importance between characteristic ultrasound
findings and clinical risk factors has been proposed for
the diagnosis of NALFD, as shown in Figure 2. To use
the algorithm, viral hepatitis, autoimmune liver disease,
alcoholic liver diseases, and genetic diseases must first
be excluded. Clinical risks include any of the follow-
ing: diabetes, body mass index (BMI) greater than 30,
hepatomegaly, and hyperlipidemia[10]. Ultrasound features
include any 4 of the following 5 sonographic features:
(1) attenuation of image quickly within 4-5 cm of depth;
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et al
. Bedside ultrasound in the diagnosis of NAFLD
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Figure 1 Bedside ultrasound image displaying sonographic characteris-
tics on non-alcoholic fatty liver disease. Attenuation of image (green arrow),
diffuse echogenicity, uniform heterogeneous liver, thick subcutaneous depth
(yellow arrow), and enlarged liver lling of the entire eld as described by Riley
et al[9].

(2) echogenic diffusely but particularly important to note
brightness within the rst 2-3 cm of depth; (3) liver uni-
formly heterogeneous; (4) thick subcutaneous depth (> 2
cm); and (5) liver lls entire eld with no visible edges[9].
Characteristic features for NAFLD on ultrasound were
found to be the strongest independent predictor on
multivariable analysis. Other clinical risk factors with sig-
nicant correlation with the biopsy-proven diagnosis of
NAFLD on multivariate analysis include the presence of
diabetes, BMI > 30, hepatomegaly, female gender, age >
55, and triglyceride greater than 250[10]. The severity of
hepatic steatosis on ultrasound in the presence of meta-
bolic syndrome is a better non-invasive tool for monitor-
ing liver disease than liver enzymes[11]. Normal alanine
aminotransferase (ALT) level alone was not sufcient for
exclusions of significant hepatic steatosis[12]. Aspartate
aminotransferase (AST)/ALT ratio greater than 1, how-
ever, has been associated to ndings of advanced brosis
on liver biopsy[13]. The recognition of appropriate clinical
factors in conjunction with characteristic ultrasound nd-
ings can lead to an accurate diagnosis of NAFLD with-
out the use of invasive testing, and also identify those
individuals that should go onto have a liver biopsy.
ULTRASOUND AS A SCREENING TOOL
The prevalence of NAFLD and NASH may be higher
than previously predicted creating the need for an ac-
curate, non-invasive, and easily available modality for the
diagnosis of NAFLD in the asymptomatic patient[12,14].
When Williams et al[14] used ultrasound to screen asymp-
tomatic individuals in the general population without
known liver disease or signicant alcohol use, they found
non-alcoholic fatty liver disease to be more prevalent
than previously reported. All individuals who had ultra-
sound ndings suggestive of fatty liver had a liver biopsy
to conrm their diagnosis. Using ultrasound as a screen-
ing tool, they found NASH and NAFLD to be present at
12.2% and 46% of the population, respectively.
Detection of NAFLD in potential living donor liver
transplantation is an important part of the routine pre-
transplant work-up[12]. During the evaluation of living
donors, invasive procedures for healthy donors should be
minimized. It is well-recognized that the diagnostic accu-
racy of ultrasound diminishes with less than 20% hepatic
steatosis. Identification of living donor candidates with
a higher degree of hepatic steatosis by ultrasound may
allow them to forgo unnecessary liver biopsy needed for
such assessment[15]. A study by Lee et al[12] evaluated 589
living donor candidates with ultrasound, CT scan, and liv-
er biopsy. They found a higher incidence than previously
reported. In their study, 51.4% living donor candidates
has greater than 5% steatosis and 10.4% had greater than
30% steatosis. Ultrasound had a sensitivity of 92.3%
when steatosis was greater than 30% when screening this
population for a pre-transplant work-up.
In comparison to other non-invasive imaging tech-
niques, ultrasound has comparable sensitivities, greater
ease of use, availability, and lower cost in screening for
moderate to severe degrees of NAFLD. Although other
modalities such as dual-gradient echo magnetic resonance
imaging (DGE-MRI) is more accurate with sensitivity and
specificity greater than 90% when hepatic steatosis was
greater than 5%, the difference between DGE-MRI’s sen-
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Presence of chronically
abnormal liver enzymes
Are clinical risks
present?
Are ultrasound features
present?
Proceed to liver
biopsy
Is the AST/ALT > 1 or
has the BMI > 30 for
more than 15 yr?
Proceed to liver
biopsy
Proceed to liver biopsy Initiate lifestyle changes
Yes No
Yes No
Yes No
Figure 2 Diagnostic algorithm for suspected non-alcoholic fatty liver disease. The algorithm illustrates the use of ultrasound in reducing the need for liver biopsy
in the diagnosis of non-alcoholic fatty liver disease. BMI: Body mass index; AST/ALT: Aspartate aminotransferase/alanine aminotransferase.
Khov N
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. Bedside ultrasound in the diagnosis of NAFLD

ultrasound findings that could predict the presence of
steatosis. Although this score showed significant cor-
relation with metabolic derangements, the US-FLI had
poor performance in predicting the presence of NASH.
Similarly, when Charatcharoenwitthaya and Lindor[23]
evaluated various radiologic modalities in NASH, they
found that neither ultrasound, CT scan, nor MRI were
able to distinguish between NASH and other degrees of
NAFLD. Other studies have also shown that ultrasound
cannot be used to grade degrees of brosis and cannot
replace needle biopsy in distinguishing simple steatosis
from steatohepatitis[24,25].
DISCUSSION
Ultrasound represents a non-invasive, widely available,
and accurate tool in the detection of NAFLD. Although
there is limited data available to support the use of ultra-
sound as a screening tool, ultrasound can be a powerful
tool in the setting of known liver abnormality. Ultrasound
should be used as the rst-line diagnostic test in patients
with abnormal liver enzymes. Standardized, characteristic
sonographic ndings are able to reliably identify patients
with NAFLD. Clinical risk factors, when used with ultra-
sound findings, have high utility in identifying NAFLD
patients and initiating an early plan of care. In a study by
Riley et al[26], the risk of advanced brosis was increased
in patients with a BMI greater than 30 for over 15 years.
In this clinical setting, with abnormal liver enzymes and
ultrasound ndings suggestive of NAFLD, these patients
would benet from a liver biopsy to identify the degree
of brosis.
Bedside ultrasound can be incorporated into the
training of clinicians and used in hepatology practices at
outpatient visits. There is also potential use of ultrasound
when screening liver donor candidates. Ultrasound can
be used to exclude candidates with existing hepatic ste-
atosis without putting them through liver biopsy. An early
ultrasound and diagnosis will allow a potential liver donor
candidate with hepatic steatosis to initiate early interven-
tion and re-evaluation at a later date.
In conclusion, the bedside ultrasound is a powerful
and useful diagnostic tool in the detection of NAFLD.
It is an accurate and reliable method that can reduce the
need for liver biopsy in the appropriate clinical setting.
Clinicians should be aware of the known limitations
when interpreting ultrasound, most importantly the in-
ability to grade or stage degree of fibrosis in NAFLD
patients. While bedside ultrasound cannot replace liver
biopsy in monitoring the progression from simple steato-
sis to NASH, its accessibility, ease of use, and low-side
effect prole make it an appealing diagnostic tool when
used in the appropriate clinical setting. As the incidence
of NAFLD continues to rise, we expect an increase in
the use of bedside ultrasound by clinicians as it becomes
integrated into the routine practices of gastroenterolo-
gists and hepatologists.
sitivity and ultrasound were statistically insignicant when
steatosis was greater than 30%[1].
LIMITATIONS OF ULTRASOUND
Ultrasound is limited in its utility in several settings, as
shown in Table 1. As previously mentioned, multiple
studies have shown that ultrasound underestimates the
prevalence of hepatic steatosis when less than 20% of
steatosis is present. The sensitivity for detecting mild de-
grees of steatosis is low, ranging from 55%-90%[1,3,6,13,16,17].
Guajardo-Salinas et al[18] reported a low sensitivity in de-
tecting all degrees of NASH in obese individuals (mean
BMI 46-49) by ultrasound. In his retrospective chart
review of ultrasound reports, the right upper quadrant
ultrasound was an unreliable tool for screening fatty liver,
with a sensitivity of 40%. In another study evaluating the
diagnosis of NAFLD by ultrasound in obese patients un-
dergoing bariatric surgery, de Moura Almeida et al[19] also
found a low sensitivity of 64.9%. In this study, patients
had an average BMI of 43.8. Low sensitivities in both
these studies may be a result of the lack of clearly de-
ned characteristic sonographic ndings for the diagnosis
of NAFLD. Nonetheless, severe obesity may also limit
the ability to reliably detect liver echogenicity due to thick
layers of subcutaneous fat[19,20].
When used in the setting of other chronic liver dis-
eases, such as chronic hepatitis C, ultrasound had unac-
ceptably low sensitivity and specificity in identifying
hepatic steatosis[2,21]. Perez et al[21] revealed in their chronic
hepatitis C patients that ultrasound had only a sensitiv-
ity of 32% for detecting fat on biopsy in these patients.
These low sensitivities suggest that ultrasound should
not be the only modality used in detecting co-existing
NAFLD in patients with chronic hepatitis C.
Perhaps the most important limitation of using ul-
trasound alone is its inability to correlate with the degree
of fibrosis[20]. Ultrasound scoring systems fall short of
distinguishing between progressive NASH and benign
steatosis. Studies have shown poor correlation between
sonographic ndings and the histological stage of brosis
on biopsy[2,20]. Ballestri et al[22] developed the ultrasound
fatty liver indicator (US-FLI), a scoring system based on
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Table 1 Strength and weakness of ultrasound to diagnosis
non-alcoholic fatty liver disease
Utility of ultrasound
Non-invasive
Ease of clinician use
Ease of clinician interpretation
Widely available
Low cost
Allows quick diagnosis
Limitations of ultrasound
Cannot grade degree of brosis
Limited use in pre-existing chronic liver disease
Limited use in obese patients
Low sensitivity when steatosis is less than 20%-30%
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. Bedside ultrasound in the diagnosis of NAFLD

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