A MERICAN A SSOCIATION FOR

T HE STUDY OF LIVER D I S E ASES

REVIEW | HEPATOLOGY, VOL. 65, NO. 3, 2017

A Practical Approach to Nutritional

Screening and Assessment in Cirrhosis
Puneeta Tandon,1* Maitreyi Raman,2* Marina Mourtzakis,3** and Manuela Merli4**

Malnutrition is one of the most common complications of cirrhosis, associated with an increased risk of morbidity and
mortality. As a potentially modifiable condition, it is of particular importance to identify malnourished patients so that
nutritional therapy can be instituted. Nutrition screening and assessment are infrequently performed in patients with cir-
rhosis. The reasons for this are multifactorial, including the absence of a validated “rapid” screening tool, multiple defini-
tions of what constitutes malnutrition, and challenges with interpreting body composition and laboratory results in the
setting of volume overload and liver dysfunction. This article summarizes the clinically relevant evidence and presents key
issues, tools, and clinical options that are applicable to patients with cirrhosis. The definition, etiology, and clinically rele-
vant outcomes associated with malnutrition are reviewed. Rapid nutritional screening is differentiated from more detailed
nutritional assessment. Nutritional assessment in special populations, including women and the obese, and the role of
inflammation are discussed. Multicenter studies using a common nutritional screening/assessment strategy are the
next steps to fast-track adoption and implementation of nutrition-related evaluations into routine clinical practice.
(HEPATOLOGY 2017;65:1044-1057).

M
alnutrition is one of the most common to determine if they are at risk of malnutrition. Those
complications associated with cirrhosis and at risk should complete a more detailed nutritional
is diagnosed in anywhere from 5% to 99% assessment to confirm the presence and severity of
of patients depending upon the assessment methods malnutrition.(8) Nutrition screening and assessment
that are used.(1) Malnutrition is associated with are performed infrequently in patients with cirrhosis
increased risk of mortality, higher prevalence of portal due to the absence of a validated “rapid” screening tool,
hypertension–related complications and infections, as multiple definitions of what constitutes malnutrition,
well as longer stays in hospital.(2-4) In mixed popula- and challenges with interpreting body composition and
tions of malnourished patients, the benefits of nutri- laboratory results in the setting of volume overload and
tion therapy are evidenced by reductions in mortality, liver dysfunction.
infections, systemic inflammatory responses, and hos- This article presents key issues, tools, and clinical
pital length of stay.(5,6) Although cirrhosis-specific options to enhance the practice of nutrition screening
studies are limited by cohort size and trial design, and assessment that are applicable to both outpatients
nutrition therapy has also shown benefit.(7) and hospitalized patients with cirrhosis. A PubMed
As a potentially modifiable condition, it is of partic- search using the search terms “malnutrition,”
ular relevance to identify malnourished patients so that “nutritional assessment,” “cirrhosis,” and related terms
nutritional therapy can be instituted. Ideally, all was carried out in April 2016 and supplemented by
patients should first undergo a rapid nutrition screen articles identified from the gray literature and the

Abbreviations: ASPEN, American Society for Parenteral and Enteral Nutrition; BIA, bioelectrical impedance analysis; BMI, body mass index; CT,
computed tomography; ESPEN, European Society for Parenteral and Enteral Nutrition; MRI, magnetic resonance imaging; RFH-NPT, Royal Free
Hospital-Nutritional Prioritizing Tool; SGA, Subjective Global Assessment.
Received August 17, 2016; accepted November 16, 2016.
Additional Supporting Information may be found at onlinelibrary.wiley.com/doi/10.1002/hep.29003/suppinfo.
*These authors contributed equally to this work.
**These authors share senior authorship.
Copyright VC 2016 by the American Association for the Study of Liver Diseases.

View this article online at wileyonlinelibrary.com.

DOI 10.1002/hep.29003
Potential conflict of interest: Nothing to report.

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HEPATOLOGY, Vol. 65, No. 3, 2017 TANDON, RAMAN, ET AL.

authors’ content expertise. Due to the limited evidence index (BMI) of <18.5 kg/m2(10) to define malnutri-
in this area, this article also incorporates the authors’ tion, we propose that Child-Pugh C patients are at
opinions and experience to raise awareness and provide very high risk of malnutrition and do not need to be
a practical approach applicable to the clinical setting. “screened” for malnutrition but instead can proceed
The details of the nutrition prescription, including directly to a nutritional assessment (Fig. 1).
methods of calculation and nutrient distribution, and
the approach to nutritional therapy in patients with
cirrhosis are also important topics but fall beyond the Towards a Practical Approach:
scope of the current review.
 There is a compelling need for consensus
on accurate and readily useable tools to
Defining Malnutrition in diagnose malnutrition in cirrhosis.
 Cirrhosis patients with a BMI <18.5 or
the Setting of Cirrhosis those with Child-Pugh C are at high risk
for malnutrition.
“Malnutrition” can refer to a state of either undernu-
trition or overnutrition. For the purpose of this review,
“malnutrition” will be used synonymously with
“undernutrition.” Malnutrition is diagnosed following Etiology and Mechanisms of
a comprehensive nutritional assessment. Major nutri-
tion and cirrhosis research groups/organizations have Malnutrition in Hepatic
proposed expert consensus-based definitions of malnu-
trition, including the American Society for Parenteral
Cirrhosis
and Enteral Nutrition (ASPEN),(9) the European The etiology of malnutrition in cirrhosis involves
Society for Parenteral and Enteral Nutrition multiple processes resulting from combined disturban-
(ESPEN),(10,11) the International Society for Hepatic ces of oral intake, absorption, and metabolism of
Encephalopathy and Nitrogen Metabolism,(1) and a nutrients.(12) First, impaired dietary intake is a princi-
recent guideline in the American Journal of Gastroenter- pal cause of malnutrition and may arise as a conse-
ology.(6) Some of these guidelines are targeted to a gen- quence of gastrointestinal symptoms, anorexia,
eral cohort of adult patients, and others are specific to dysgeusia, and prescription of unpalatable diets.
cirrhosis. Although there is no unifying tool for the Anorexia may be triggered by an imbalance between
diagnosis of malnutrition, there is significant overlap in orexigenic and anorexigenic hormones and by the
the components used to objectively define malnutri- chronic increase in circulating cytokines. Nausea, vom-
tion, with all societies notably recommending some iting, and early satiety are often related to intra-
form of muscle mass assessment (Table 1). abdominal pressure secondary to ascites. Dysgeusia
It is accepted that malnutrition increases with wors- may result from zinc deficiency, while unpalatability is
ening liver disease severity. To date, however, in the often the result of rigid sodium-restricted diets.
cirrhosis-specific guidelines, liver disease severity has Second, nutrient malabsorption may occur in
not been used to stratify patients for their risk of mal- patients with cirrhosis due to multiple factors, the
nutrition. In addition to the well-accepted body mass mechanisms for which are incompletely understood.(13)

ARTICLE INFORMATION:
From the 1Cirrhosis Care Clinic and CEGIIR, University of Alberta, Edmonton, AB, Canada; 2Division of Gastroenterology, Department
of Medicine, University of Calgary, Calgary, AB, Canada; 3Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada;
4
Gastroenterology, Department of Clinical Medicine, Sapienza University of Rome, Rome, Italy.

ADDRESS CORRESPONDENCE AND REPRINT REQUESTS TO:

Puneeta Tandon, M.D., M.Sc. Edmonton, Alberta, Canada
Division of Gastroenterology, University of Alberta E-mail: [email protected]
130-University Campus Tel: 11-780-4929844

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TANDON, RAMAN, ET AL. HEPATOLOGY, March 2017

TABLE 1. Society Guidelines for Defining Malnutrition—Common Components

Food Weight Muscle Subcutaneous Fluid Functional

intake loss mass loss fat loss accumulation status BMI Inflammation SGA
General ASPEN(1) X X X X X X X
Hospitalized inpatient(2) X X
General ESPEN(3) X X X
Cirrhosis ESPEN(4) X X X X X
Cirrhosis ISHEN(5) X X X X X X

Abbreviation: ISHEN, International Society for Hepatic Encephalopathy and Nitrogen Metabolism.

Fat malabsorption, secondary to decreased production  Malnutrition in cirrhosis is multifactorial.

of bile acids, occurs in cholestatic liver diseases. Intra-  Treating malnutrition requires a compre-
luminal bile acid deficiency, resulting from decreased hensive and multidisciplinary strategy and
bile production and portosystemic shunting, impairs surveillance.
micelle formation and absorption of long chain fatty
acids through lymphatics. Pancreatic insufficiency fre-
quently coexists in patients with alcoholic cirrhosis.
Portal hypertensive gastropathy and enteropathy,
altered intestinal flora, and chronic lactulose use may
Relationship of Malnutrition
also lead to malabsorption. and Clinical Outcomes in
Third, altered macronutrient metabolism is a cor-
nerstone mechanism contributing to malnutrition in Cirrhosis
cirrhosis. Carbohydrate metabolism is abnormal (e.g.,
Historically, malnutrition was believed to influence
peripheral insulin resistance, hyperinsulinemia,
the health outcome of patients with liver cirrhosis. As
impaired hepatic glycogen synthesis) and promotes
such, it was included in the 1964 Child-Turcotte classi-
gluconeogenesis from amino acids, glycerol, pyruvate,
fication for the prognosis of patients with cirrhosis
and lactate. These effects are already evident after a
undergoing surgery. In 1972, the nutritional status
short overnight fast and may resemble the catabolic
parameter was removed. Since then, many studies on
state of healthy subjects undergoing 2-3 days of star-
cirrhosis have associated malnutrition with worse health
vation. Abnormal amino acid metabolism leads to low
plasma levels of methionine and branched chain ami- outcomes and lower survival rates (Fig. 2).(2-4,15,16)
no acids, which associate with muscle atrophy. Pro- Multiple methods have been applied to evaluate
tein catabolism is increased in the postabsorptive malnutrition (e.g., Subjective Global Assessment
state, and protein synthesis that usually occurs in [SGA], anthropometry, nutritional index, dual X-ray
response to a meal is normal or attenuated compared absorptiometry, computed tomography [CT]/magnetic
with matched controls. Hypermetabolism is a rela- resonance imaging [MRI]), which has led to divergent
tively infrequent feature in stable cirrhosis and is not results. The depletion of muscle mass (commonly
associated with sex, etiology, or severity of liver dis- termed “sarcopenia”) has emerged as the “central core”
ease; however, it may result from up-regulation of the of the nutrition assessment in cirrhosis. Muscle tissue
sympathetic nervous system, and hypermetabolism stores a large proportion of amino acids and proteins,
has been reported when energy expenditure is which are mobilized in catabolic conditions. Muscle is
expressed per kilogram of lean body mass. Recent crucial for mobility, metabolic regulation of glucose
research has also increased our knowledge about and lipids, heart and respiratory function, immune
molecular mechanisms contributing to the pathophys- function, and cytokine activity. Muscle wasting, quan-
iology of muscle wasting in patients with cirrhosis, tified either by anthropometry or by imaging techni-
and more information can be derived from a recent ques, is related to a higher rate of mortality in patients
review on this topic.(14) with cirrhosis.(3,4,15,16) The strong interplay between
malnutrition, sarcopenia, and poor prognosis is further
demonstrated by the association of nutritional impair-
Towards a Practical Approach: ment and liver disease–related complications.(17,18)

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mortality as the majority of these are patients with
decompensated cirrhosis and advanced liver insuffi-
ciency.(4) Following transplantation, malnourished
patients commonly present with increased length of
hospitalization, prolonged intensive care unit stay, lon-
ger time of intubation, and higher rate of infections
compared with those who are well nourished.(21)
Although it is generally accepted that malnourished
patients may require greater support in the posttrans-
plantation setting,(22) malnutrition is not currently
considered a contraindication to transplantation.

Towards a Practical Approach:

 Evidence suggests that malnutrition is an
FIG. 1. A proposed algorithm for nutritional screening and independent predictor of poor clinical out-
assessment in patients with cirrhosis. comes and lower survival in cirrhosis.
  Loss of muscle mass loss is objectively
measureable and has been the most com-
In patients with hepatocellular carcinoma, sarcopenia mon nutritional variable associated with
is an independent prognostic factor decreasing surviv- mortality.
al(19) and increasing treatment complications and related
mortality.(20) Sarcopenia plays a negative prognostic role
in candidates for surgical treatment of hepatocellular
carcinoma. Malnutrition is also a well-established risk Nutrition Screening and
factor in patients with cirrhosis undergoing surgery.
In patients awaiting liver transplantation, muscle Nutrition Risk
depletion is predictive of increased waiting list ASPEN defines nutrition screening as a process to

identify individuals who are malnourished or at risk of
malnutrition for referral to a comprehensive nutritional
assessment and intervention if appropriate.(23) ESPEN
states that screening should be a rapid and simple pro-
cess conducted by admitting staff or community health
care teams.(24) An ideal screening tool should be usable
by an untrained health care professional (or even the
patient) and have reasonable sensitivity and specific-
ity.(25) Routine system-wide nutrition screening is not
widely practiced, even though it is recommended for
high-risk patient groups. As such, patients at risk for
malnutrition are often overlooked until they are mal-
nourished and/or have a major health event requiring
intervention. By ignoring preventative strategies, mal-
nutrition increases the economic burden of cirrhosis.(26)
Nutrition risk acknowledges the interplay between
inflammation and malnutrition and is determined by
not only nutritional status but also disease severi-
FIG. 2. Overview of the complex relationship between malnutri-
tion, cirrhosis-related complications, transplantation, and survival. ty.(6,27,28) ESPEN defines nutrition risk as “Chances of
Data about the prognostic value of malnutrition for survival after a better or worse outcome from disease or surgery
liver transplantation are controversial. according to actual or potential nutritional and metabol-
 ic status.”(8) The literature does not provide a

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TANDON, RAMAN, ET AL. HEPATOLOGY, March 2017

TABLE 2. Summary of Nutrition Screening Tools

Screening Tool
 Care Setting Advantages Disadvantages Tool Components
MUST(6) High interrater reliability Weight from fluid collections (ascites, BMI
 Community Content and predictive validity for length peripheral edema) not accounted Unplanned weight loss
of hospital stay and mortality Disease severity not considered in past 3-6 months
Practical Acutely ill and unable to
eat for 5 days
NRS-2002(7) Content and predictive validity Weight from fluid collections (ascites, Weight loss
 Hospital Moderately reliable peripheral edema) not accounted Food intake
Practical BMI
Considers disease severity Disease severity
NUTRIC(2) Externally validated (n 5 >1,000 Interleukin-6 not widely available Age
 Critically ill patients) Requires training APACHE II and SOFA scores
Classic nutrition parameters not Comorbidities
considered Days in hospital pre-ICU
Interleukin-6
MNA(8) Includes physical and mental Content validity not reported GI symptoms
 Elderly (home-care components plus dietary questionnaire Interrater reliability modest Weight loss
programs, nursing Predictive validity for adverse Weight from fluid collections (ascites, Mobility
homes, and hospitals) outcome, social functioning, mortality, peripheral edema) not accounted Psychological stress/acute
and doctor visits Disease severity not considered disease
Practical Neuropsychological problems
BMI
SNAQ(9) Simple/practical Weight from fluid collections (ascites, Unintentional weight loss
 Hospital Facilitates identification and treatment of peripheral edema) not accounted Decreased appetite
malnourished inpatients Disease severity not considered Use of supplements or tube feeding
MST(10) Simple/practical Weight from fluid collections (ascites, Unintentional weight loss
 Hospital Predictive validity for length of stay peripheral edema) not accounted Quantity of weight lost
Excellent reliability Disease severity not considered Decreased appetite
Highly sensitive
RFH-NPT(11) Simple/practicalcirrhosis-specific features Valid in population with cirrhosis only Alcoholic hepatitis or tube feeding
 Ambulatory Excellent intraobserver and interobserver Impact of nutritional therapy based on Considers fluid overload
Hospital reproducibility screening score unknown Dietary intake reduction
Good external validity Weight loss 1 option for assessing
Predictive of clinical deterioration and diuretic use
transplant-free survival
CNST(12) Simple/practical Weight from fluid collections (ascites, Unintentional weight loss
 Hospital Validated against SGA (sensitivity 67%- peripheral edema) not accounted Dietary reduction
73%, specificity 80%-86%) Disease severity not considered
High reliability Symptoms not considered

Abbreviations: APACHE II, Acute Physiology and Chronic Health Evaluation II; CNST, Canadian Nutrition Screening Tool; GI,
gastrointestinal; MNA, Mini Nutritional Assessment; MST, Malnutrition Screening Tool; MUST, Malnutrition Universal Screening
Tool; NRS-2002, Nutritional Risk Screening 2002; NUTRIC, Nutrition Risk in Critically Ill; SNAQ, Short Nutritional Assessment
Questionnaire; SOFA, Sequential Organ Failure Assessment.

unanimous definition for nutrition screening, and there diet technicians, or nurses). Importantly, to date, none of
is no consensus regarding the concept of nutrition the frequently recognized nutrition screening tools
risk.(8) (Table 2) have been validated in the setting of cirrhosis.
Nutritional Risk Screening 2002(28) and the Nutrition
Risk in Critically Ill(27) are examples of two scoring sys-
tems to determine nutrition risk. Other validated nutri- Which Nutrition Screening/
tion screening tools can be used as general screens for
malnutrition (Table 2).(29) Although many tools demon-
Nutrition Risk Tool(s) Can
strate sensitivity and specificity values over 70% (mini- Be Used in Cirrhosis?
mally accepted prerequisite), flaws in the validation
processes have been observed,(25) including the use of Cirrhosis-specific tools have been developed. The
expert trained professionals and lack of validation of tool Royal Free Hospital-Nutritional Prioritizing Tool
administration by nonexperts (e.g., nutrition assistants, (RFH-NPT) was developed by validation against the

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Royal Free Hospital SGA (Supporting Fig. S1).(1) It

takes 3 minutes to complete; discriminates patients
Overview of the
into low, medium, and high-risk categories; and Components of a Detailed
includes the variables of alcoholic hepatitis, fluid over-
load and impact on dietary intake, BMI, unplanned Nutritional Assessment
weight loss, and reduced dietary intake (Supporting
Once patients with cirrhosis have been screened, a
Fig. S2). Importantly, the Malnutrition Universal
detailed nutrition assessment should be performed in
Screening Tool (recommended by ESPEN as the pre-
patients at high nutritional risk to confirm the nutri-
ferred screening tool for outpatients) is incorporated tion risk assessment, characterize nutrition status, and
within the RFH-NPT in patients who do not have flu- identify modifiable variables for nutrition support.
id overload. In a series of 148 patients, the RFH-NPT Repeated assessments can monitor the effects of nutri-
was identified as an independent predictor of clinical tion therapy. As nutritional assessment is more com-
deterioration and transplant-free survival.(30) The con- prehensive, is time-consuming, and requires
tent validity of this tool in a population with cirrhosis interpretation of multiple nutrition indicators, it is
is promising and encompasses features of clinical and preferable but not mandatory to have this performed
metabolic risk, along with classical nutritional variables by a registered dietitian or a dedicated person with spe-
that may influence response to nutrition therapy. cialized knowledge.
Additionally, although it includes BMI as a variable, In patients with cirrhosis whose screen results indi-
this is only considered in the absence of fluid overload. cate a high risk for malnutrition, we suggest that each
A second liver-specific nutrition screening tool is the component be assessed and documented every 1-6
Liver Disease Undernutrition Screening Tool (Support- months in outpatients as well as inpatients at admis-
ing Fig. S3). This tool uses a series of six patient- sion and periodically throughout their hospital stay.
directed questions covering the domains of nutrient Regardless of which tools are used, clinically relevant
intake, weight loss, subcutaneous fat loss, muscle mass information is obtained and awareness of nutrition
loss, fluid accumulation, and decline in functional status risks is raised by repeating the assessments in patients
to determine whether undernutrition is present or with cirrhosis to improve quality of health care.
absent. This tool was based on the Academy of Nutri- Although the assessment provided below focuses on
tion and Dietetics and ASPEN consensus statements macronutrient deficiencies, patients with advanced liv-
for identifying malnutrition(31) and may have limitations er disease are also at risk of micronutrient deficiencies.
as it relies on the patient’s subjective judgment of each Zinc deficiency may be observed as a consequence of
of the measured parameters. Preliminary data compar- diuretic use and restricting animal protein intake.
ing it against a dietitian’s nutrition assessment in a Hypomagnesemia may arise secondary to diuretic use.
setting of cirrhosis (n 5 22) suggest that the Undernu- Frequently, fat-soluble vitamin deficiencies, particular-
trition Screening Tool had a high positive predictive ly of vitamins A and D, are encountered. Considering
value (93%) but a low negative predictive value (37.5%), the high prevalence of micronutrient deficiencies in
leading to the conclusion that a negative screen was this population, it is reasonable to incorporate basic
unable to reliably rule out undernutrition. As with the micronutrient screening into the broader nutrition
RFA-NPT, further validation is needed with compari- assessment. There are few guidelines to reference
son to clinical outcomes in patients with cirrhosis. regarding the frequency of micronutrient screening.
At a minimum, our group would recommend 6-
monthly testing of serum magnesium, serum 25-
Towards a Practical Approach: hydroxyvitamin D3 and vitamin A, and serum zinc
 Screening tools including either weight or levels.
BMI have limited clinical value in cirrhosis
due to known fluctuations in body water. #1 DIETARY ASSESSMENT
 The cirrhosis-specific nutrition risk screen-
ing tool, RFH-NPT, is currently preferred
Dietary Intake
as it considers metabolic and nutritional A detailed assessment of dietary intake (i.e., food,
parameters. fluids, and supplements) may include a 3-day food dia-
ry. Notably, this method is only useful if patients are

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TANDON, RAMAN, ET AL. HEPATOLOGY, March 2017

provided with standardized instructions to understand determinations of lean mass; however, BIA is highly
how to complete the diary properly. Although this for- influenced by fluid shifts, especially edema, and its use
mal assessment may be burdensome for the patient, in longitudinal evaluations in this population have
the diary is preferred over a 24-hour dietary recall, been deferred. Studies have varied in their estimation
which is simple to use but heavily reliant on recall skills of dry weight BMI using either the postparacentesis
and may not accurately represent routine food choices body weight or by subtracting a percentage of weight
and behaviors. based upon severity of ascites (mild, 5%; moderate,
With the exception of dietitians, most health care 10%; severe, 15%), with an additional 5% subtracted if
providers have insufficient “food” knowledge to incor- bilateral pedal edema was present.(4,34,35) More
porate, analyze, and interpret these tools during rou- advanced tools quantify specific body composition
tine clinical practice. At a minimum, patients should compartments (such as adipose tissue depots [e.g., vis-
be asked if their relative food intake has changed and, ceral adiposity] and/or skeletal muscle) with varying
if so, over what duration. Although it requires valida- accuracy and specificity (Table 3). These tools are
tion in cirrhosis, parts of the abridged scored Patient- important in nutrition practices as they relate to poor
Generated SGA, developed and validated in oncologi- metabolic, clinical, and functional outcomes and will
cal patients (Supporting Fig. S4),(32) may be useful to be the focus of this section.(3,4,15,16)
initiate nutritional intake discussions with patients Importantly, in addition to quantifying body com-
who have cirrhosis. Given the detrimental effects of position compartments, CT imaging can be used to
fasting in cirrhosis, additional questions should be evaluate the potential infiltration of fat into muscle by
asked, such as the duration of fasting between meals, examining changes in Hounsfield units, which crudely
snacking routines, and use of nutritional supplements. reflect the density of muscle tissue. Similarly, the use
Inadequate protein intake is linked to sarcopenia and of echogenicity with ultrasonography may provide sim-
has also been independently associated with mortality ilar measures of changes in muscle density, which may
in patients with cirrhosis(33); therefore, inquiry into reflect fatty infiltration or muscle damage. These mea-
adequate protein sources is important. sures may provide additional insight on possible rela-
tionships and mechanisms of poor muscle function
Barriers to Dietary Intake and health(36) but require validation before routine use
in clinical settings.
To effectively address oral intake, it is also essential to
delve into the factors that may compromise intake (e.g., Special Considerations in Body Com-
dysgeusia, taste fatigue, low-sodium diet, early satiety,
position—Identifying Patients With
socioeconomic factors). Tools such as the abridged
scored Patient-Generated SGA(32) can be useful. Valida- Low Muscle Mass
tion of such tools is required in cirrhosis, but engaging Cutoff points for low muscle mass in a cirrhosis
dietetic staff is helpful in assessing this information. population have yet to be clearly defined or validated
using CT, MRI, or ultrasonography. This and stan-
#2 BODY COMPOSITION dardized landmarks are needed to identify patients
ASSESSMENT WITH A FOCUS ON with low muscle mass and compare results from differ-
MUSCLE MASS ent studies (Table 4).

Body composition is an important parameter for Special Considerations in Body

evaluation in nutrition assessment; however, choosing Composition—Understanding Sources
a modality can be challenging, and one needs to con-
sider feasibility, cost, and level of accuracy or precision
of Error
that is required in practice. Body size by weight or Understanding and controlling potential sources of
BMI provides a crude classification of patients in the both modifiable errors (e.g., anatomical landmarking,
underweight, normal weight, overweight, or diverse skill of tester) and nonmodifiable errors (i.e., base
obese categories. There is no well-validated means of assumptions incorporated into calculations) affect the
adjusting BMI for the fluid retention that occurs in interpretation of results (Table 3). These errors are
cirrhosis. Similarly, bioelectrical impedance analysis particularly important in cirrhosis as patients frequently
(BIA) offers the opportunity for quick and easy present with fluid retention or shifts, ascites, or edema,

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TABLE 3. Characteristics of Diverse Body Composition Modalities That Have Been Used in Liver Cirrhosis

Relative Accuracy Level of

Modality Measures and Precision Training Merits and Limitations
Anthropometrics Overall body size: Accuracy: Low Minimal Highly feasible, accessible, and inex-
weight, height for Precision: Low pensive for large patient popula-
BMI; MAC tions and clinics
Predicted Muscle: MAMC Results need to be interpreted cau-
Predicted visceral adi- tiously as these are crude and
posity: WC, W:H, predictive
skinfold
BIA Prediction equations to Accuracy: Moderate Minimal to May present inaccuracies in patients
calculate lean and fat Precision: High moderate with ascites and/or edema
mass Feasible as a bedside tool and rela-
tively inexpensive to moderately
expensive
Proper positioning of inpatients or
patients who have a larger body
size may be challenging
Equations are used to predict whole-
body lean tissue based on same
device and population
Ultrasound Muscle thickness and Accuracy: Moderate Ultrasonographer Moderately feasible and accessible in
imaging CSA to high may be helpful clinics
Subcutaneous adipose Precision: Moderate Prediction equations for whole-body
tissue to high lean or skeletal muscle mass are
Echogenicity for tissue needed
integrity Cutoff points for low muscularity have
not been developed for cirrhosis
CT or MRI CSA and integrity of spe- Accuracy: High Certified medical Can capture specific lean and adi-
cific muscle and adi- Precision: High radiologist pose tissue deposits
pose tissue groups Not performed on all patients
Only capture a single or few slice(s),
and prediction equations are
needed for whole-body lean mass
Specific cutoff points have not been
established in cirrhosis
Dual-energy X-ray Whole-body and regional Accuracy: High Certified medical radiologist Low-dose radiation for prospective
absorptiometry fat, lean, and bone Precision: High studies
mineral content Can perform regional analysis
Bone mineral density May not be available in clinic
Cannot specifically distinguish
between different tissue
compartments

Abbreviations: CSA, cross-sectional area; MAC, mid-arm circumference; MAMC, mid-arm muscle circumference; WC, waist cir-
cumference; W:H, weight to height ratio.

factors that may confound single-point and longitudi- the development of a universal approach as well as vali-
nal assessments. For example, although a patient’s dation in cirrhosis and correlation with clinical
weight may not change over time, muscle and adipose outcomes.(34)
tissue changes (i.e., fat and muscle loss) may be masked
by fluid retention or ascites. Although there are tools #3 FUNCTIONAL ASSESSMENT
(e.g., bioimpedance spectroscopy) to discriminate fluid
shifts from body composition changes, these devices The quality of lean tissue, particularly skeletal muscle,
are not widely available due to cost. Further, repeated is optimally evaluated through functional measures. Sev-
CT or MRI scanning is limited by the expense, avail- eral studies have demonstrated that muscle strength
ability, and, in the case of CT, significant risk of ioniz- deteriorates more quickly than mass, suggesting that it
ing radiation and contrast exposure to the patient.(37) may be a more sensitive measure of “muscle health.”(38-
40)
Preliminary data are available for thigh ultrasound as a Moreover, in patients with cirrhosis, functional mea-
predictor of sarcopenia in cirrhosis, but this requires sures (e.g., handgrip, 6-minute walk, physical frailty,

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TANDON, RAMAN, ET AL. HEPATOLOGY, March 2017

TABLE 4. Methods of Identifying Low Muscularity Using Various Body Composition Modalities and
Low Muscle Strength Using Hand Grip

Population in
Cutoff Point for Low Which Cutoff Point
Modality Calculations Required Muscularity/Strength Was Derived
MAMC(13,14) MAMC (cm) 5 MAC (cm) – Females: <19.2 cm 80 years old
(3.14 3 TSF [cm]) Males: <21.1 cm
BIA Skeletal muscle mass (kg) 5 Females: 5.76-6.75 kg/m2 Multiethnic
[(Ht2 [m2]/R (Ohms) 3 0.401) associated with moderate physical 60 years old(16)
1 (sex [M 5 1, F 5 0] 3 disability
3.825) 1 (age 3 –0.071)] 1 5.75 kg/m2 associated with high
5.102(15) physical disability
Skeletal muscle index (kg/m2) 5 Males:
skeletal muscle mass 8.51-10.75 kg/m2 associated with
(kg)/height2 (m2) moderate physical disability
8.50 kg/m2 associated with high
physical disability
Ultrasound None None for the 4-site protocol Liver cirrhosis and ICU
CT or MRI Muscle index 5cross-sectional Females: <39 cm2/m2 Cancer(17,18)
area at L3 (cm2) / height2 (m2) Males: <54 cm2/m2
Dual-energy X-ray Appendicular lean mass index 5 Females: <5.45 kg/m2 Young and elderly(19)
absorptiometry sum of lean mass in upper and Males: <7.26 kg/m2
lower limbs (kg)/height2 (m2)
Handgrip strength None Males: 65 years of age,
BMI 24: 29 kg community-dwelling
BMI 24.1-28: 30 kg participants in the
BMI >28: 30 kg Cardiovascular
Women: Health Study(20)
BMI 23: 17 kg
BMI 23.1-26: 17.3 kg
BMI 26.1-29: 18 kg
BMI >29: 21 kg

Abbreviations: ICU, intensive care unit; MAC, mid-arm circumference; MAMC, mid-arm muscle circumference; TSF, triceps
skinfold.

and volume of O2 peak tests) have been associated with examination parameters (loss of subcutaneous fat, loss
clinical decompensation.(41-43) These measures are com- of muscle mass, and edema/ascites). The components
plemented with body composition assessments to better are combined to obtain a rating of A, well nourished;
understand the metabolic integrity of the muscle and its B, moderately malnourished; or C, severely malnour-
ability to perform its tasks. ished. The SGA correlates well with adverse postoper-
ative outcomes in patients without cirrhosis(44) but
#4 GLOBAL ASSESSMENT TOOLS underestimates the prevalence of sarcopenia.(34) In a
recent study, of 69 patients identified to have sarcope-
IN CIRRHOSIS
nia by CT or MRI, only 46% were identified by the
As a supplement to the performance of a detailed SGA as being moderately or severely malnourished.
nutritional assessment, we are aware of two global Moreover, in the setting of cirrhosis, unlike more
assessment tools that incorporate some of the above objective measures, the SGA has had a limited capacity
nutritional assessment parameters. to predict clinical outcomes.(34,41)

Subjective Global Assessment Royal Free Hospital SGA

(44)
The SGA (Supporting Fig. S5) divides patients Recognizing the limitations of the traditional SGA
into three categories based on five historical parameters in the setting of cirrhosis, Morgan et al. devised the
(weight change, dietary intake relative to usual, gastro- Royal Free Hospital SGA, a global scheme incorporat-
intestinal symptoms, functional capacity, and metabol- ing both subjective and objective variables.(35) This
ic stress of underlying diagnosis) and three physical algorithm includes BMI (estimated dry body weight),

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mid-arm muscle circumference, and dietary intake TABLE 5. Minimum Components of a Detailed Nutritional
Assessment For Patients With Cirrhosis
(Supporting Fig. S1). Notably, although nutritional
status as diagnosed by the Royal Free Hospital SGA
was significantly associated with a shorter survival in
men, it was not found to be prognostic in women, rais-
ing questions about its generalizability to both sexes.
The subjective interpretation required for scoring two
of the three variables, estimated dry body weight BMI
and dietary intake, may also raise some challenges.
Additional external validation is required before this
tool can be widely accepted.

Toward a Practical
Approach
 In cirrhosis, we suggest a minimum base-
line and longitudinal assessment of a 3-
day food diary, barriers to intake (question
3 of the patient-generated global SGA), INFLAMMATION
estimated dry weight BMI, and mid-arm Recognizing the importance of inflammation in pro-
muscle circumference (Tables 4 and 5). moting catabolism, Jensen and colleagues, as part of the
 Additional muscle health measures can be international clinical nutrition support community,(47)
used based on clinic capacity (budget, proposed an etiology-based diagnosis of adult starvation
training, etc.) and disease-related malnutrition. They incorporated the
 Repetition of the base measures is essential concept of inflammation, as an energy demanding con-
to inform clinical practice. dition, to define three different categories of malnutri-
tion. Across the categories, energy needs progressively
increase and the response to nutritional therapy
decreases: (1) pure chronic starvation without inflam-
Special Considerations mation (e.g., anorexia nervosa), (2) chronic diseases or
conditions that impose sustained inflammation of a
IS THERE A DIFFERENCE IN mild to moderate degree (e.g., organ failure, pancreatic
NUTRITIONAL ASSESSMENT cancer), and (3) acute disease or injury with a marked
BETWEEN THE SEXES? inflammatory response (e.g., major infection, burns). At
present, the evidence suggests that patients with cirrho-
As a major objective component of malnutrition, sis are conservatively designated as having mild to mod-
low muscularity or sarcopenia differs in men and wom- erate inflammation. Hospitalized patients with acute-
en. This may result from the different prevalence of on-chronic liver failure are elevated to category 3.(48)
autoimmune or cholestatic disease in women, but it is The use of specific inflammatory markers (i.e., C-
likely that other factors also play a role. Usually women reactive protein or procalcitonin) to further refine the
have greater fat stores than men, while a progressive categorization and predict the responsiveness to nutri-
depletion in muscle tissue is more evident in men.(45) tional supplementation requires evaluation.
Moreover, the prognostic implications of low muscle
mass and function are less clear in female than in male
OBESITY
patients.(16) It has been suggested that hypogonadism
and testosterone deficiency in men with cirrhosis may The epidemic of obesity and the association between
lead to chronic muscle depletion even before malnutri- nonalcoholic steatohepatitis and cryptogenic cirrhosis
tion is clinically evident.(46) have significantly increased the number of obese and

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TANDON, RAMAN, ET AL. HEPATOLOGY, March 2017



FIG. 3. A case example using the proposed algorithm for nutritional screening and assessment. Abbreviation: INR, international nor-
malized ratio.


morbidly obese patients with cirrhosis. As evidence, masked by adiposity when using BMI and BIA.
nonalcoholic fatty liver disease is becoming a leading In ultrasound, distinguishing between the muscle
indication for liver transplantation. Obese patients typ- and subcutaneous adipose tissue border may also be
ically exhibit low inflammation, muscle and hepatic challenging in obese individuals, decreasing accura-
insulin resistance, dyslipidemia, and/or other comor- cy and reliability of ultrasound. While CT and
bidities. The combination of cirrhosis and obesity MRI may distinguish between muscle and adipose
exacerbates complications that may require specific tissue deposits, many obese individuals may not be
nutrition advice. Skeletal muscle atrophy may be scanned due to the size restrictions of the scanner.

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HEPATOLOGY, Vol. 65, No. 3, 2017 TANDON, RAMAN, ET AL.

Generally, obesity increases the rate of clinical Acknowledgment: The authors acknowledge the assis-
decompensation in patients with cirrhosis,(49) and tance of Tannaz Eslamparast, R.D., and Kathleen
morbid obesity (BMI >35) has been associated Ismond, Ph.D., for their valuable review of the man-
with decreased survival after liver transplanta- uscript content.
tion.(50) Given the limitations of existing bedside
tools in these patients and the practical issues asso-
ciated with repeated CT/MRI-based imaging, fur-
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Supporting Information
2011;54:555-561.
Additional Supporting Information may be found at
onlinelibrary.wiley.com/doi/10.1002/hep.29003/suppinfo.

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