Best Practice & Research Clinical Gastroenterology

Vol. 20, No. 3, pp. 419–439, 2006

doi:10.1016/j.bpg.2006.01.006
available online at http://www.sciencedirect.com

Malnutrition: Etiology, consequences,

and assessment of a patient at risk

1
Cathy Alberda MSc RD
Critical Care Dietitian
Royal Alexandra Hospital, Capital Health Region, 670-1 CSC, 10240 Kingsway Ave,
Edmonton, Alta., Canada T5H 3V9

2
Andrea Graf BSc RD
Clinical Dietitian
Alberta Hospital Edmonton, 17480 Fort Rd Box 307, Edmonton, Alta., Canada T5J 2J7

Linda McCargar* PhD RD

Professor, Human Nutrition
Department of Agricultural, Food and Nutritional Science, 4-10 Agriculture Forestry Centre,
University of Alberta, Edmonton, Alta., Canada T6G 2P5

Malnutrition results from the imbalance of nutrients and energy provided to the body (too low),
relative to its needs (too high). These needs increase dramatically with illness. This is certainly
the case for patients with gastrointestinal diseases. Sub-optimal dietary intake, metabolic
stress, malabsorption and increased nutrient demands, put a patient with gastrointestinal
disease, at high-risk for malnutrition. The causes, consequences and assessment and monitoring
indicators of malnutrition are reviewed herein.

Key words: nutrition; malnutrition; nutrient requirements; nutritional assessment; nutrition

support; gastrointestinal disease.

* Corresponding author. Tel.: C1 780 492 9287; fax: C1 780 492 4265.
E-mail addresses: calberda@cha.ab.ca (C. Alberda), andreagraf@cha.ab.ca (A. Graf), linda.mccargar@
ualberta.ca (L. McCargar).
1
Tel.: C1 780 735 4439; fax: C1 780 735 5105.
2
Tel.: C1 780 472 5604.
1521-6918/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved.
420 C. Alberda et Etiology and Consequences of malnutrition
al 420
DEFINING MALNUTRITION

Definitions and prevalence in hospitals

There is no universally accepted definition of malnutrition, however, the World

Health Organization states that malnutrition is the cellular imbalance between
supply of nutrients and energy, and the body’s demand for them to ensure growth,
1
maintenance, and specific functions. When malnutrition or risk of malnutrition is
being established, it is necessary to specify both the type of nutrient or nutrients
under consideration and the cut-off values that will be used to distinguish between
2
normal and abnormal ranges, or between low and high risk of malnutrition.
Nutrients can be divided into micronutrients (vitamins, minerals, trace
elements) and macronutrients (carbo- hydrates, proteins, fats). Marasmus and
kwashiorkor represent the two major classifications of macronutrient
malnutrition. Marasmus is the type of malnutrition seen in patients with prolonged
starvation. It is easily recognized by a wasted, cachectic appearance. Although the diet
3
may contain an acceptable protein to energy ratio, total dietary intake is inadequate.
This results in utilization of endogenous fat and muscle tissue reserves for energy.
In contrast, kwashiorkor results from a deficit of protein despite a relative adequacy
of energy, and as such, may develop over a shorter period of time. The most common
physical effects of kwashiorkor are depigmentation of both hair and skin, and
3
edema. As a result, these patients may maintain relatively normal weight and
anthropometric measurements. Without careful physical examination and review of
biochemical data to reveal the large serum albumin loss, this form of
3
malnutrition may be overlooked. Protein energy malnutrition (PEM) is used in more
recent literature to describe any individuals with protein or energy malnutrition.
Malnutrition due to vitamin, mineral and trace element deficiencies may also occur in
conjunction with PEM. Isolated vitamin or mineral deficiencies can also be detected in
otherwise well-nourished patients.
First described in the 1920s, PEM was seen in developing, third world countries.
Research and nutritional screening through a variety of nutrition risk classification
systems has shown an increasingly high number of hospitalised patients in developed
1
nations are malnourished. A British study showed that 40% of hospitalised patients
are undernourished at admission and 78% of those suffered further deterioration in
4
their nutritional status during hospitalisation. Despite overwhelming evidence of
the existence of malnutrition in western world hospitals, a widely accepted
screening system to detect malnutrition is a limiting factor to improving the
nutritional status of hospitalised patients. Subjective global assessment (SGA) and the
European model of nutrition risk screening (NRS-2002) will be discussed later in the
chapter.

ETIOLOGY OF MALNUTRITION

Starvation

During short or extended periods of inadequate caloric intake, the human body is
capable of utilizing its own body tissue for fuel. Much of what we know today with
regards to starvation is due to the classic study done by Ancel Keys in the 1950s at
the University of Minnesota. The purpose of this study was to gain insight into the
physical and psychological effects of semi-starvation and the problems of refeeding
civilians who
had been starved during the war. During the experiment, the participants experienced
semi-starvation conditions. Most of them lost O25% of their weight and experienced
anemia, fatigue, apathy, extreme weakness, irritability, neurological deficits, and
5,6
lower extremity edema. As his and other studies show, readily available
carbohydrate stores are the first choice for energy utilization by the body, but no
7
large depot of carbohydrate exists outside of the liver. Fat and protein are the next
option, but the body must preserve its protein stores, as body protein is ‘functional’.
Every gram of catabolised protein represents an incremental decrease in the body’s
7
overall functional capacity. Fat is, therefore, the obvious choice for fuel with the
greatest energy density, large available depots, and the ability to have its metabolites
(glycerol) converted to glucose by the liver. But this is not permanent, as the
human body will undergo numerous metabolic changes during starvation, from the
initial 24–48 hours to adapted starvation, developing weeks after the initial fasting
7–9
state.
The liver and pancreas are the first organs affected by starvation. After a meal,
absorbed carbohydrate enters the portal circulation and the liver. In the liver,
monosaccharides are converted to glucose, glycogen is synthesized and stored, and the
remaining glucose is released into circulation where insulin facilitates uptake by
the tissues. Approximately 2 hours after a meal, blood glucose levels fall, and signal
5,6,10,11
the pancreas to decrease its release of insulin. At the same time, glucagon
release from the pancreas increases, triggering the liver to breakdown its glycogen
stores and to release glucose into the bloodstream (glycogenolysis). However,
glycogen stores are limited and after approximately 4–6 hours they will be
depleted, leaving gluconeogenesis as the only source of glucose production for the
body. For gluconeogenesis, the liver can rely on metabolites from muscle tissue
breakdown
such as lactate and amino acids. Muscle tissue protein can provide a significant amount
of energy during the transition between the fed state and starvation, but never enough
10
to sustain long-term starvation needs. Also, the added nitrogen released from amino
acid substrates produces urea, which in large quantities places an added strain on the
liver and kidneys. As a result, the body switches to utilization of its fat stores for
5,6,10,11
fuel.
From the large adipose stores in the body, fatty acids are mobilized by
circulating glucagon. The liver can readily use glycerol, but the glycerol stores are small
compared to the need for glucose during starvation. Fatty acids are also used during
7,8
this time, being completely oxidized by kidney and muscle tissues. Fatty acids
absorbed into the liver, however, are not oxidized, they are converted into ketone
bodies, a water-soluble form of fat that spares the utilization of glucose by the body. As
for site-specific needs, muscle tissue continues to use fatty acids for energy instead of
ketone bodies as these are primarily used by the central nervous system. The increase
in ketone use by nervous tissue in turn reduces the need for gluconeogenesis in the
liver and this in turn reduces protein breakdown in muscle tissue. As such, the
respiratory quotient (RQ) of a starved patient would be 0.6–0.7 (CO2/O2) to represent
fat oxidation. Full adaptation to starvation with minimization of
protein oxidation can take about 2 weeks. On average, adipose stores can provide up to
2 months supply of calories for basal energy requirements during a period of
5–11
starvation.

Stress

Stress may be initiated from a multitude of stimuli such as a motor vehicle accident,
extensive burns, a head injury, or post-operative sepsis. The metabolic response
associated with a critical illness is often referred to as ‘hypermetabolic’ or
 Table 1. Comparison of starvation and stress hypermetabolism.

Starvation Stress
REE Decreased Increased
RQ 0.6–0.7 0.8–0.9
Mediator activity – CCC
Primary fuels Fat Mixed
Proteolysis CC CCCC
Branch chain oxidation C CCC
Hepatic protein synthesis C CCC
Ureagenesis C CCC
Urinary nitrogen loss C CCC
Gluconeogenesis C CCC
Ketone body production CCC C
5
Adapted from: Barton RG. Nutrition support in critical illness. Nutr Clin Pract 1994 Aug; 9:127–139.

‘hypercatabolic’ stress. Metabolism and substrate utilization in the initial stages of

hypermetabolic stress is heavily influenced by hormones and inflammatory mediators
7,12
linked with a critical illness. Specifically, substrate utilization can be managed
through the balance of insulin, the major storage or anabolic hormone, and the
insulin counterregulatory hormones: glucagon, cortisol, and catecholamines. In
contrast to starvation, stress hypermetabolism is associated with the wasting of lean
body mass and is normally characterized by an RQ of 0.8–0.9 to represent a mixed
7
fuel source. As with starvation, carbohydrate oxidation and glucose production by
glycerol and amino acids via gluconeogenesis does occur, only at an accelerated
rate. As a result, hyperglycemia occurs, not because of insulin resistance, but
13
because the oxidation and production exceeds that of insulin release. The insulin that
is released, does retain its ability to suppress lipolysis and protein breakdown.
However, the insulin counter- regulatory hormones oppose these effects, serving to
14
increase protein catabolism.
Protein synthesis is also increased, but overall, production is significantly less than that
of protein catabolism, producing a marked increase in ureagenesis, mostly due to
increased glucagon and cortisol secretion. The large amount of protein breakdown for
gluconeogenesis by the liver acts as the main contributor to hyperglycemia. The
catecholamines also stimulate gluconeogenesis and glycolysis. The resulting rapid
decrease in lean body mass will produce an increase in urea production and urinary
7
nitrogen losses. During this time, the liver also uses amino acids, primarily the
branched chain amino acids, along with fatty acids and glycerol. The hormonal milieu
is not the sole influence on alterations in substrate metabolism during stress. Research
to date has found at least 200 other distinct chemical entities, or
‘inflammatory mediators’, also associated with hypermetabolic stress and resulting
tissue loss. Of these, tumour necrosis factor (TNF) and interleukin-1 (IL-1) stimulate
proteolysis, both
directly and through their role in increasing stress hormone release. In addition, they
7
inhibit lipoprotein lipase activity, causing impaired lipid uptake. See Table 1 for a
comparison of starvation and stress induced malnutrition.

High-risk gastrointestinal (GI) disease entities

A healthy diet and normally functioning GI tract are critical for the: delivery of
nutrients, prevention of nutrient deficiencies and malnutrition, repair of damaged
 Table 2. Micronutrients and their role in wound

healing. Micronutrient Role in wound healing

Vitamin A Stimulant for the onset of wound healing, stimulates epithelialization and
fibroblast deposition of collagen
Vitamin C Necessary for collagen synthesis
Zinc Cofactor for collagen and other wound protein synthesis
Copper Cofactor for connective tissue production and collagen cross-linking
Manganese Collagen and ground substance synthesis

Adapted from: Protein–Energy Malnutrition, and the Nonhealing Cutaneous Wound available at http://
20
www.medscape.com/viewprogram/714_pnt.

intestinal epithelium, maintenance of normal luminal bacterial populations, promotion

15
of normal GI motility, and maintenance of normal immune function. However, there
are a multitude of single and combination high-risk disease entities that put the GI tract
in jeopardy thereby increasing the chance for malnutrition in an individual.
Malnutrition is prevalent in patients with inflammatory bowel disease (IBD), liver
disease and pancreatitis. These disease entities will be discussed in detail further in
the chapter.

CONSEQUENCES OF MALNUTRITION

Wound healing and skin integrity

Wound healing is a tissue response, which involves increased cellular activity,

synthesis of new proteins and increased tissue energy consumption. There is a direct
correlation between impaired and non-healing wounds and the incidence of PEM.
All aspects of wound healing depend on the prevention and/or reversal of PEM,
optimum nutrition, increased anabolic activity with increased energy and protein,
along with effective local wound care. The wound consumes large quantities of energy
during the healing process both by the population of inflammatory cells and by the
16
fibroblasts’ production of collagen and its matrix. Of major concern is the adaptive
response to preserve lean body mass (LBM). Studies show that malnutrition and
weight loss play a critical role not only in wound healing and anastomoses, but also the
development of decubitus ulcers. Since patients with PEM commonly have edema
(kwashiorkor), the skin can become stretched very thin, making it more susceptible
16,17
to breakdown. Research has shown that up to a 10% loss of LBM, the wound
3
takes priority for protein substrates. At greater than 10% loss, the restoration of
LBM increasingly competes with available protein substrates to restore itself, the
18,19
overall goal being to prevent further LBM loss and morbidity. As the skin protein
decreases throughout the body, new wounds will develop and old wounds will
reopen.
The role of vitamins, minerals and trace elements in wound and skin healing is as
important as that of the macronutrients and any losses due to increased metabolic
consumption, stress or inadequate replacement should be rectified. See Table 2 for a
20
list of micronutrients required for wound healing and synthesis.

3
LBM varies greatly between individuals. It could represent a range from w55 to 85% of body weight. Thus
a general estimate would suggest that the wound takes priority up to a 15% body weight loss.
Ventilated days and length of stay

The diaphragm is the principal muscle responsible for proper respiration. Since it is a
relatively large muscle, a substantial amount of protein can be lost from the
diaphragm during stress and/or starvation induced malnutrition. Recent studies have
shown that with loss of diaphragm contractility and inspiratory muscle strength,
altered breathing patterns along with altered responses to hypoxia will result.
Malnourished patients may require aggressive ventilation support and possibly
long-term home oxygenation therapy.21,22 The added time spent on mechanical
ventilation increases the overall length of hospital stay for the patient. Extra time
spent in hospital increases the risk for developing further infections and delayed
wound healing. Thus, there is a need for initial nutrition assessments and assistance
for the patient in achieving maximal nutrition intake (enterally or parenterally) to
prevent further loss of nutrition status, and to reduce the need for mechanical
23,24
ventilation.

Surgical complications

Malnutrition is associated with an increase in susceptibility, and a decrease in

ability to respond, to post-operative complications such as infection. Studies
evaluating intra-abdominal surgeries have found that malnutrition was a strong
25,26
predictor of post-operative complications. The decision to feed pre-
operatively remains a subjective one, although research supports the benefits that
27–29
pre-operative nutrition confers on the seriously depleted patient. It should
not be the intention to restore lost tissue, but simply to correct fluid and
electrolyte deficits, replenish glycogen stores and allow sufficient time to promote
and maintain protein synthesis as near normal as possible in preparation for the
increased demands on protein and energy metabolism in the post-operative
27–29
period. The next decision is whether enteral or parenteral nutrition is
more beneficial. When not contra- indicated, enteral nutrition remains as the
gold standard for both pre-and post- operative nutrition support: it is more
physiological, contains a more balanced composition of nutrients, and helps
30–32
maintain the function and integrity of the GI tract. However, when
symptoms such as large fistulas, intractable nausea and severe diarrhoea occur
despite altering rate, mode or type of enteral formula, the benefits of parenteral
30–32
nutrition outweigh the risks.

Infections and immune system

Malnutrition contributes to a cascade of adverse metabolic events that compromise

33,34
the immune system and impair the body’s ability to adapt, recover and survive.
The interdependency between the disciplines of nutrition and immunology was
formally recognized in the 1970s when immunological measures were
35
introduced as a component of assessing nutritional status. Several studies have
been published to show the exact effect PEM has on cellular immunity. The first
mechanism is the lack of essential nutrients for the cells of the immune system to
carry out their functions; the second is a more indirect mechanism. As the body
adapts to nutrient deprivation, its metabolism qualitatively changes. This altered
metabolism could be directed toward preserving some bodily functions at the
36–38
expense of others. See the following summary, created from a variety of texts
and studies for a list of specific and non- specific effects PEM has on the immune
system.
 Effects of PEM on the specific immune system

† low percentage of rosette-forming cells, an indicator of the number of

T-lymphocytes
† increased percentage of null cells, an indicator of impaired production of thymic
hormones
† fewer T-cells and a decreased helper-suppressor cell ratio
(T4/T8)
† decreased lymphokine and monokine production (TNF, prostaglandin E2 [PGE2], IL-
1, and fibronectin).

Effects of PEM on non-specific defence mechanisms

† decreased complement C3 and total hemolytic activity

† decreased opsonic function of plasma (i.e. decreased ability for bacteria to be
consumed during phagocytosis) and decreased intracellular killing capacity of
polymorphonuclear leukocytes
† decreased serum toxemic factor (generalized response to infection)
† impaired production of gamma interferon and IL-1 and IL-
2
† phagocyte dysfunction
† decreased antibody affinity
† impaired secretory IgA antibody response
† decreased response of acute-phase reactants to infectious challenge (adapted from
[33–44]).

In addition to the improvements in glycogen and protein stores that nutrition

support provides, the efficacy of new immune-enhancing enteral and parenteral
solutions is being studied. Products enhanced with omega-3 fatty acids, arginine,
glutamine, prebiotics and probiotics, have been demonstrated to reduce infectious
complications, and improve the function of the immune system without impacting
35,39–41
hepatic and renal function or protein synthesis. Pre-operative oral immune-
enhancing nutritional supplements have been shown to confer positive effects on post-
45
operative infections in patients undergoing cardiac surgery. A recent review of
immunonutrition confirmed the benefits of pre-operative administration of immune-
enhancing diets but also demonstrated that post-operative administration offered no
43
advantages. The controversy of immunonutrition for surgical and critically ill patients
remains a topic of debate, as other researchers have found no difference in infection
rate, mortality or length of hospital stay in patients supplied with these highly
42–44
specialized formulas compared to those in control groups. Immunonutrition
remains an area of active clinical research.

Physical strength, rehabilitation and quality of life

Poor nutritional status is also linked with a number of long-term complications after
discharge from hospital. Many studies have found malnourished patients have
increased rehabilitation needs. Once home, these patients may require further
follow-up with respect to homecare nursing visits. Other studies have found that
malnourished patients have shorter survival time following discharge and/or a higher
46
chance of re- admission to hospital within a year. Taking all of these issues into
consideration, it is apparent that quality of life for these patients may be
significantly decreased. Many hospitals, however, are establishing a process to help
determine the best course of
action for discharge. Appointments and discharge planning meetings with physical and
occupational therapists as well as social workers and dietitians are helping to ensure a
positive transition home for more high-risk patients. Such a multidisciplinary approach
is desirable and beneficial. In addition, there are home nutrition support programs,
providing patients with enteral and parenteral feedings at home, so patients can
maintain their family life and work responsibilities. This also helps to maintain
nutritional status and in turn decrease the chance of re-admission and early
47
mortality.

NUTRITIONAL ASSESSMENT: IDENTIFYING THE PATIENT

AT NUTRITION RISK

Malnutrition in hospitalised patients was initially described by Bistrian and Blackburn in

48,49
the 1970s. Since that time, detailed nutritional assessments of hospitalised patients
50
reveal that over half of patients suffer from some degree of malnutrition. Estimates
for the geriatric hospitalised patient and institutionalised patients show an even greater
51
incidence of malnutrition. Gastroenterology patients are particularly at high-risk of
52
developing malnutrition. Since, malnutrition is associated with increased morbidity
and mortality, prevention or correction of nutrient depletion has the potential to
53
minimize malnutrition-related complications. The goals of nutritional assessment are
to identify patients who have, or are at risk of developing protein energy malnutrition,
and to treat them and then monitor the adequacy of nutrition therapy. A conceptual
framework (Figure 1) for the identification of malnutrition in hospitalised patients
54
follows.

Diet history

The diet history can provide valuable information about usual eating habits, potential
nutrition deficiencies, and reasons for sub-optimal intake. From the diet history,
average macronutrient and micronutrient intakes, diet variety, and food resources
can be determined. Other factors to consider that may influence the client’s dietary
intake include: (1) appetite and taste changes, (2) gastrointestinal symptoms, (3)
chewing and swallowing ability, (4) requirements for assistance with feeding and/or
cooking, (5) eating patterns, (6) food intolerances and allergies, and (7) dietary
55
restrictions including ethnic and religious influences. Underreporting or
overreporting of foods in diet histories is common. Underreporting energy intake
56
has been shown to be more common in women and overweight clients.
Experienced dietitians can assist in obtaining accurate dietary information.

Medical history

Nutritional assessment can be incorporated into the patient’s medical history. The
medical history should focus on changes in diet and body weight, psychosocial and
socio-economic conditions, and symptoms unique to each clinical setting (see Table
3). A highly variable factor that should be considered is a patient’s medication profile
and possible drug–nutrient interactions. The malnourished patient with digestive
disease etiology may complain of dysphagia, nausea and vomiting, chronic
54
diarrhoea, or recurrent abdominal pain that is exacerbated by eating. Patients at
high nutritional
 Evaluation of Malnutrition

Etiologies Histroy Physlcal laboratory Procedures

findings
Starvation Unintentional weight Weight <90% Serum albumin, Bioelectric
(hypometabolism) loss > 10% body wt ideal other visceral impedance
Decreased diet intake Decreased diet analysis
assimilation Decreased food Anthropometry proteins
intake Vitamins A, E, Indirect
Stress (hypermetabolism) Critical acute Socioeconomic Muscle wasting calorimetry
illness 25(OH)D,
Anorexia Loss of B12, folic acid
Chronic Creatinie-height
Self-restricted subcutaneous
inflammation Minerals: Zn, Mg, index
diets, e.g., fat
Mixed metabolic alcoholism Phos Nitrogen balance
abnormality Skin rashes
Lymphocyte
AIDS Critical illness Ocular changes Count, skin-test
Cancer Gastrointestinal Mucus Reactivity
Chronic liver symptoms membranes
disease Dysphagia
Nausea/vomiting Neurologic
Chronic diarrhea changes Eti
Abdominal pain olo
Other medical gy
illnesses an
AIDS d
Disseminated Co
Cancer
Chronic liver ns
disease eq
COPD ue
Chronic infection nc
es
of
Figure 1. From Harrison’s Principles of Internal Medicine 16th Ed. (2005); q 2005 by the McGraw-Hill Companies, Inc.54 ma
ln
utr
iti
on
42
7
428 C. Alberda et Etiology and Consequences of malnutrition 429
al

Table 3. The patient history of weight loss and malnutrition.

Finding Example/interpretation
General factors
Involuntary diet restriction Poverty due to inadequate income
Anorexia Anorexia nervosa, severe depression, dementia, AIDS, cancer, chronic
renal disease
Inadequate diet selection Chronic alcoholism, fad diets, strict vegetarianism
Critical illness Untreated stress response to trauma, burn, major surgery, sepsis
Gastrointestinal symptoms
Dysphagia Esophageal obstruction impairs diet transit
Nausea, vomiting Gastric or intestinal obstruction impairs diet transit
Chronic diarrhoea Pancreatic, biliary, or intestinal mucosal disease impairs digestion and
absorption
Protein-losing enteropathy in inflammatory bowel disease
Chronic abdominal pain Self-limited food intake reduces pain: e.g. pancreatitis, intestinal
ischemia, inflammatory bowel disease
Other chronic medical Combinations of anorexia, increased energy demands, and abnormal
diseases nutrient metabolism: e.g. recurrent pancreatitis, AIDS, disseminated
cancer, chronic liver disease, chronic obstructive pulmonary disease,
chronic infectious illness

From Harrison’s Priniciples of Internal Medicine 16th Ed. (2005); q 2005 by The McGraw-Hill
54
Companies, Inc.

risk include those with chronic pancreatitis, liver disease, renal failure, Crohn’s
disease and ulcerative colitis, or chronic infections such as AIDS or tuberculosis.

Weight history

Body weight and recent weight loss are simple measures of total body
53
composition.
Weight can be compared with an ideal body weight, or changes from the patient’s
usual body weight. Weight loss in the previous 6 months can be expressed as a
percentage loss from previous weight. Weight loss of !5% over 6 months is
considered insignificant,
weight loss between 5 and 10% of usual body weight is considered potentially
significant, and weight loss O10% over 6 months is definitely considered significant
57
and worthy of investigation and treatment. In addition to the amount of weight
loss, the pattern of weight loss is also considered to be important. A recent
stabilization or increase in weight can reverse the risk of developing nutritional
complications.
Body mass index (BMI) is a method of evaluating body weight that is becoming
commonplace in clinical practice. The calculation for BMI is as follows: BMIZweight
2 58
(kg)/height (m ). A BMI calculated to be less than 18.5 is considered underweight,
with increased risk of health problems. BMI’s between 18.5 and 24.9 are considered to
be normal, healthy weights, and at lowest disease risk. BMI’s greater than 24.9 are
58
considered overweight or obese (O30). Gender and body type influence BMI results.
In addition, BMI does not take into account ethnic and age variations. For example,
due to differences in body types of Asians and Inuit people, use of BMI cut-off points
are not appropriate for comparison of obesity prevalence and disease risk with these
59,60
ethnic groups. As well, BMI tends to overestimate body fat for muscular
61
athletes, and underestimate fat stores in the elderly.
Body composition measurements

Bioelectrical impedance analysis (BIA) is another simple method of estimating body

composition. It measures total body water, fat-free mass, fat mass, and body cell mass
through the impedance of an electrical current that passes through the body.
BIA has been validated in healthy adults and in some clinical populations
62,63
including Crohn’s disease, HIV and renal disease. DEXA (dual energy X-ray
absorptiometry) measurements have been found to provide an accurate assessment
of body composition however, DEXA analyses are not widely available in
clinical practice.
Skinfold measurements are an indirect method used to determine body
composition. Triceps skinfold is used as a measure of subcutaneous fat. Mid-arm
circumference (MAC) and mid-arm muscle circumference (MAMC) are used to
measure skeletal mass. Since standards were developed for healthy, ambulatory
populations, these anthropometric measures have limited usefulness in the clinical
setting. They do have some validity in evaluating long-term trends in large
64
populations. There are a number of additional techniques available for measurement
of body fat and protein mass, including whole body density by underwater weighing,
isotope dilution techniques used to measure body fluid volumes, neutron activation,
64
and infrared interactance. All of these methods are used primarily for research
purposes, and are not practical clinical tools.

Biochemical assessment

The laboratory measurements most widely used to assess the clinical status of the
patient and degree of malnutrition are measurements of serum protein
55
concentrations, including albumin, transferrin and prealbumin. These proteins are
referred to as visceral proteins. The liver manufactures these proteins; therefore,
hepatic insufficiency may decrease their production. Albumin has been studied the
most extensively. Although albumin levels are a good prognostic index for increased
mortality and risk of complications, it is a relatively poor indicator of early protein
malnutrition due to its long half-life (20 days); and the impact of non-nutritional
factors including renal disease, hepatic disease, hydration status and gastrointestinal
losses on its serum levels. Transferrin has a shorter half-life (8–10 days), however,
it is also impacted by hydration status and iron status. Prealbumin (or transthyretin)
is a carrier protein for retinol binding protein and a transport protein for
thyroid hormones. Prealbumin has a half-life of 2–3 days, potentially increasing its
usefulness as an indicator of visceral protein status, especially in acute stages of
protein–energy
malnutrition. This marker is also impacted by renal disease (falsely elevated) and liver
disease (falsely depressed). Retinol-binding protein has a half-life of 12 hours,
however, it is acutely sensitive to non-nutritional variables, and therefore, not used
in clinical settings. All of the surrogate markers of visceral protein status have been
questioned for their reliability, and no single measurement should be used
65
independently as a marker of nutritional adequacy. Serum levels of visceral
proteins fall in response to an inflammatory process regardless of nutritional
61
status. During inflammation, the liver produces acute-phase proteins, such as
C-reactive protein (CRP). C-reactive protein appears in the serum within
24–48 hours of the onset of inflammation. Obtaining serial CRP levels may be
helpful in interpreting prealbumin levels that remain low, even when there is
provision of adequate nutrition. As the inflammatory process resolves, CRP levels
begin to decrease, and prealbumin levels should rise as long as nutritional intake
remains adequate. If prealbumin is not increasing, and CRP is decreasing, low
66
prealbumin is likely due to poor nutrition vs a stress response, signifying the need
to increase energy and protein intake. Conversely, declining levels of CRP and
increasing levels of prealbumin are suggestive of transitioning to an anabolic phase.
Markers of immune function such as delayed hypersensitivity skin testing and total
lymphocyte counts have limited use in a nutritional assessment due to their poor
sensitivity; as a result of influences of non-nutritional factors.
Nitrogen balance is easily calculated when a 24-hour urine collection is completed
with measurement of urinary urea nitrogen (UUN) excretion. Nitrogen balance is a
calculation of nitrogen intake minus nitrogen losses.
Nitrogen intakeZprotein intake/6.25
Nitrogen lossesZUUN excretionC4 g (commonly used factor to estimate
insensible nitrogen losses)
The goal of nitrogen balance in the hospitalised patient is a positive nitrogen
balance of 2–4 g/24 hours. In an acute catabolic state, a positive nitrogen balance
may not be
possible, and the goal is, therefore, to minimize a negative
balance.
Although nutritional assessment does not routinely warrant the measurement of
nutrient levels, provision of long-term nutrition support or concern of
individual
nutrients based on the clinical condition of the patient may prompt the clinician to
order nutrient levels. Nutrient levels, which can be measured with some validity,
include serum zinc, selenium, copper, retinol, vitamins C, D and E. As with
visceral
protein status, caution should be used in interpretation of nutrient levels due to the
impact of non-nutritional factors.
Creatinine-height index (CHI) is also dependent upon an accurate 24-hour urine
collection. Creatinine is the metabolic end product of creatine metabolism in the
muscle and is released at a constant rate. Twenty-four hour urinary creatinine
excretion is measured and compared with an expected value for a person of the
4
same height and sex. A comparison between actual and expected creatinine
excretion determines the degree of protein depletion. Limitations to the validity of
CHI include advancing age of the patient, malnutrition due to a reduction in muscle
mass, renal insufficiency, rhabdomyolysis, bedrest, catabolic states and high animal
4
protein diets.

Physical assessment

Findings of malnutrition include loss of subcutaneous fat, signs of muscle wasting and
the presence of edema and ascites. The best areas to assess for loss of fat are the
triceps regions of the arms, as well as the appearance of loose skinfolds on the
57
abdomen. Signs of muscle wasting can be visualized through loss of bulk and tone of
muscle groups. Concave appearance of the temporal region of the face provides
evidence of marked muscle wasting, even in the presence of edema. Shifting of fluid
from the intravascular to extravascular space is also a marker of malnutrition. Edema
is best assessed at the ankle or pre-sacral area. Physical manifestations of
nutrient deficiencies are usually a sign of advanced malnutrition. In general, muscle
wasting, poor skin integrity, and loss of subcutaneous tissue are typical findings
associated with
longstanding energy and protein deficits.
 431 C. Alberda et Etiology and Consequences of malnutrition
al 431
Subjective global assessment

Due to the limitations with objective means of assessing nutritional status, the
subjective global assessment (SGA) was developed as a method of assessing
nutritional status. Based on the client’s medical, weight and diet history and a
physical examination, the patient is categorized as (a) well-nourished, (b) suspected
or moderately malnourished or (c) severely malnourished with physical signs of
malnutrition evident. There is no numerical weighting scheme for combining the
history and physical examination into an SGA; instead a subjective assessment of
nutritional status is made. SGA ratings have been shown to be highly reproducible
57
when performed by trained healthcare professionals. However, handgrip strength
of malnourished liver patients, assessed by physicians and physical therapists, was
67
more accurate than SGA in predicting incidence of major complications The
American Society for Parenteral and Enteral Nutrition (ASPEN) board of directors
have suggested routine use of SGA to detect the prevalence of malnutrition in
hospitalised patients.

Nutrition risk screening (NRS)-2002

The purpose of the NRS-2002 system is to detect the presence of undernutrition

68
and the risk of developing undernutrition in the hospital setting. The initial
screening tool consists of four questions; if one of the responses is positive to one
of the four questions, a second, more detailed screening tool is implemented. The
second screen encompasses severity of disease, and has been validated by inter-
observer variation between nurses, dietitians and physicians. ESPEN also
recommends a screening tool for use in the community and another for elderly
patients (MNA) for use in nursing homes, homecare and hospitals.

SGA vs NRS-2002

Although there is no ‘gold standard’ for identification of malnutrition, the

ASPEN board of directors suggest SGA and ESPEN recommend the nutritional
risk screening-2002 (NRS-2002) to detect the prevalence of malnutrition. A
Spanish study was completed in 2005 to assess the prevalence of malnutrition
on admission to hospital, and to compare the two tools used to evaluate
69
nutritional risk. The prevalence of malnutrition was 40.7 and 45.1%, if SGA or
NRS-2002 were used, respectively. Due to the high prevalence of hospital
malnutrition, and the increasing number of cases being brought to the courts
for nutritional neglect, it is of importance that hospitals and healthcare
68
organizations adopt a minimum set of standards in this area. The strong
agreement between SGA and NRS-2002 suggest that either method could be
69
used to identify patients at nutritional risk.

HIGH-RISK DISEASE ENTITIES

Researchers using subjective global assessment (SGA) and other nutrition risk factor
indices, are showing that increasingly more chronically ill hospitalised patients in
 1
the Western World are malnourished. The percentage of GI patients being admitted
with malnutrition is among the highest of any disease or age category. Several studies
have reported that between 24 and 62% of admitted GI patients are malnourished,
52,70–72
depending on the nutritional diagnostic measures used. Specifically, some
researchers found the highest prevalence of malnourished GI patients (O30%) to be
those with inflammatory bowel diseases (Crohn’s disease, ulcerative colitis) while
other studies found patients with some form of liver disease to be the most
70
malnourished (O50%). Despite such high percentages, many studies have found that
malnourished GI patients were not regularly identified and treated, yet the severity of
malnutrition in these patients predicted the occurrence of complications during their
71
hospital stay.
As a result of this research, many practitioners are now encouraging the use of
anthropometric testing and diet related patient questioning in conjunction with
71
admission interviews.

Inflammatory bowel disease

Ulcerative colitis (UC) and Crohn’s disease (CD) are chronic inflammatory diseases
of the GI tract; ulcerative colitis is a process that is limited to the mucosa of the
colon and rectum, whereas the inflammation of Crohn’s disease may involve any
73
portion of the GI tract from the mouth to the anus. Malnutrition is especially
prevalent in patients with Crohn’s disease, and has been reported as high as 75% in
74
hospitalised patients. The mechanisms contributing to chronic malnutrition in
patients with inflammatory bowel disease are multi-factorial and include depressed
oral intake, increased GI losses, malabsorption, increased nutritional requirements,
73
and drug–nutrient interactions. Studies have shown that energy expenditure does
75
not increase significantly in active Crohn’s disease. Although energy expenditures
may not differ, BMI and lean body mass tend to be significantly lower in patients
75
with CD compared to healthy individuals. Malabsorption causes vitamin and
mineral alterations in addition to weight loss and hypoalbuminemia. Anemia
secondary to iron, folate or B12 deficiency is common in patients with
76
inflammatory bowel disease. Zinc deficiency has been reported in approximately
40% of patients with Crohn’s disease especially in patients with severe diarrhoea or
73
enteric fistulas. In recent years, attention has turned to the high incidence of
metabolic bone disease in patients with inflammatory bowel disease. A study by
Abitol et al revealed that of 84 patients with inflammatory bowel disease, 43% had
77
osteopenia of the lumbar spine. Patients receiving corticosteroids were at greater
risk, and patients with Crohn’s disease had a higher incidence of metabolic bone
disease than patients with ulcerative colitis. In general, patients with inflammatory
bowel disease who require nutrition support should initially be considered for
enteral nutrition. There are cases, however, where enteral nutrition is not
feasible, and TPN should be initiated. In cases where EN is not tolerated, or
fistulas become high output, parenteral nutrition with bowel rest is preferred.
In cases of malabsorption resulting from extensive small intestinal resection,
absorptive capacity of all nutrients as well as fluid and electrolytes is reduced.
Resections of the distal ileum may affect absorption of B12 and bile acids. In these
cases, fat restriction should be considered to lessen diarrhoea and steatorrhea. The
presence of the colon following small bowel resection is important from a nutritional
standpoint, as the colon absorbs short chain fatty acids which accelerate water
and sodium
 78
absorption. The length of time since intestinal resection is also an important factor
in determining how well a patient will manage an oral or enteral diet. Intestinal
adaptation occurs over time, improving absorptive capacity. A supply of enteral
nutrients is required to encourage intestinal adaptation. Various hormones such as
IGF-1, cholecystokinin and interleukin-1 are being studied in regards to their
73
role in encouraging intestinal adaptation in inflammatory bowel disease. Research
is also actively being carried out in the usage of fish oil supplementation, rich in n-3
fatty acids, as an anti-inflammatory agent of benefit to prevent and treat
79,80
inflammatory bowel disease. Probiotics are being actively studied for their role in
inflammatory bowel disease. To date, evidence exists to support the use of the
81
probiotic, VSL#3 for prevention of pouchitis in the post-operative course.

Liver disease

The presence of malnutrition compromises the clinical outcome of patients with end-
stage liver disease. As the disease progresses, the effects worsen. The prevalence of
malnutrition in end stage liver disease is fairly similar in both alcoholic (34–62%) and
82,83
non- alcoholic patients (27–67%) with chronic liver disease. In patients
awaiting transplant, the consensus is that malnutrition is ubiquitous, with figures
ranging from
83,84
18 to 65%. The main reason that malnutrition is so widespread is poor dietary
intake. Patients complain of diminished interest in food, altered taste acuity, and early
satiety, especially when ascites is present. Intestinal malabsorption is often present
in those
patients with cholestatic liver diseases including cholangitis and biliary cirrhosis.85 Fat
malabsorption often manifests in deficiencies of the fat-soluble vitamins, vitamin A, D, E
and K. Patients with alcoholic cirrhosis may also have some degree of pancreatic
insufficiency, further compromising fat digestion. Thus, all patients with end stage
liver disease should be supplemented with fat-soluble vitamins. Water-soluble
vitamin malabsorption, in particular, thiamine, pyridoxine and folate, is prevalent in
those patients
who abuse alcohol, and should also be supplemented. Sodium restriction is necessary
with advanced liver disease if ascites or edema are present. Fluid restrictions may need
85,86
to be imposed if patients are hyponatremic. There is a higher incidence of
osteopenia and osteoporosis in patients with end stage liver disease; calcium and
vitamin D supplementation may also be required. Zinc supplementation has also been
investigated as a method of improving encephalopathy,87 however, results have been
inconclusive. Zinc deficiency is common in cirrhotic patients due to a decrease in
hepatic storage capacity. Strong emphasis should be placed on starting nutrition
therapy early in patients with liver failure, as protein energy malnutrition is reversible. If
adequate oral intake is not feasible, early nutrition support via enteral nutrition or TPN
82
has been shown to reduce morbidity and mortality.

Pancreatitis

Acute pancreatitis is an intense inflammatory process of the pancreas. Severe acute

88
pancreatitis may lead to multi-organ failure. Chronic alcohol intake and ductal
89
obstruction due to gallstones account for nearly 3/4 of all cases of acute pancreatitis.
Malnutrition is common in patients with pancreatitis, but reports of prevalence rates
are highly variable. Many patients with severe acute pancreatitis require nutritional
90
support because they are unable to maintain their nutritional status orally. One of
the theories of acute pancreatitis suggests that auto-digestion of the pancreas and
pancreatitic tissues occurs as a result of disruption of the function of the pancreatic
enzymes that occurs during pancreatitis. The conventional treatment of acute
pancreatitis includes avoiding oral intake as a means of reducing pancreatic activity
and enzyme release. Patients with mild or moderate pancreatitis can usually be
89
advanced to an oral diet within seven days of exacerbation. Conversely, patients
with severe disease or those who present with pre-existing signs of malnutrition
should be considered for nutrition support. Parenteral nutrition is often selected
over enteral nutrition in severe pancreatitis in order to provide nutrient requirements
89
and maintain bowel rest with minimal pancreatic stimulation. Recent studies
have shown that enteral nutrition is safe and effective for the patient with acute
pancreatitis.
Chronic pancreatitis is an inflammatory disorder that results in permanent
91
impairment of the glandular anatomy of the pancreas. Chronic pancreatitis differs
from acute pancreatitis in that fibrosis and loss of exocrine tissue are present before
89
and after an acute exacerbation. Malabsorption results from the lack of pancreatic
92
enzymes and may cause malnutrition in these patients. When stool output contains
more than 10 g of fat/day, pancreatic enzyme replacement therapy should be used to
89
combat maldigestion and malabsorption. If steatorrhea cannot be controlled with
enzyme replacements, fat intake should be restricted to less than 30% of total energy
intake. When malabsorption is suspected, supplementation with fat-soluble vitamins
and divalent cations should be replaced as clinically indicated. The availability of
micronutrients such as vitamins, minerals and trace elements is decreased with
malabsorption; and the association of chronic pancreatitis with alcohol abuse
compounds the patient’s risk for micronutrient deficiencies.

CONCLUSIONS

Gastroenterology patients are at increased risk of developing malnutrition.

Malnourished patients have a higher mortality rate, along with more frequent
hospital admissions than their well-nourished counterparts. The objective methods of
assessing nutritional status have their limitations, thus leading to the development of
subjective global assessment or nutrition risk screening. Once recognized, early
nutrition intervention is critical. In this high-risk population, inadequacy of oral intake
should lead the clinician to consider enteral nutrition. Total parenteral nutrition
should be utilized only in those patients who cannot tolerate enteral nutrition
therapy, or in whom enteral nutrition is contraindicated.

Practice points

† malnutrition is common in patients with GI disease histories. Patients are at

risk for malnutrition if (a) they have experienced unintentional weight loss of
w10% of usual body weight over the preceding 3 months or (b) BMI!18.5
† the strong agreement between SGA and NRS-2002 suggest 69
that either method
could be used to identify patients at nutritional risk
 † nutrition support should be implemented early in the disease course when
risk of malnutrition is established
† DEXA, BIA, CRP in combination with prealbumin levels may be useful tools in
GI populations, however, they should be used as part of a comprehensive
nutritional assessment
† IBD patients will have a number of micro and macronutrient deficiencies
depending on intake, severity of diarrhoea and site/length of resection
† enteral or parenteral nutrition may be necessary with small bowel
resections—dependent on the area removed. With early enteral support,
bowel adaptation can occur within 3 weeks
† in severe pancreatitis, feeding enterally (past the ligament of Treitz) should be
attempted before starting parenteral nutrition

Research agenda

† development of more accurate methods of nutritional assessment that would

identify high-risk patients earlier
† development of a key biochemical nutrition marker to identify malnourished
patients
† incorporate and evaluate NRS-2000 or SGA as a standard method of
assessing nutritional status in hospitalised patients; also include as part of
physician and dietitian training programs and evaluate impact
† determine strategies to enhance discharge planning and long-term nutrition
monitoring in high-risk patients

REFERENCES

1. World Health Organization. Malnutrition—The Global Picture, 2000; Available at: http://www.who.int/
home-page/ [Full Text].
2. Stratton RJ, Green CJ & Elia M. Scientific criteria for defining malnutrition. In Disease-related Malnutrition:
An Evidence-based Approach to Treatment. 1st edn. Cambridge: CAB International, 2003, pp. 1–34.
3. Grisby D. Malnutrition. Available at: http://www.emedicine.com/ped/topic1360.htm/ [Full Text].
4. McWhirter JP & Pennington CR. Incidence and recognition of malnutrition in hospital. BMJ 1994;
308(6934): 945–948.
5. Barton RG. Nutrition support in critical illness. Nutr Clin Pract 1994; 9: 127–139.
* 6. Saltzman E, Mogensen KM & Hassoun P M. Malnutrition in the intensive care unit. In Shikora
SA, Matindale RG & Schwaitzberg SD (eds.) Nutritional Considerations in the Intensive Care Unit, 1st
edn. Dubuque: Kendall/Hunt Publishing, 2002, pp. 1–10.
7. Owen OE, Smalley KJ, D’Alessio DA et al. Protein, fat, and carbohydrate requirements during starvation;
anaplerosis and cataplerosis. Am J Clin Nutr 1998; 68: 12–34.
8. Keys A, Brozek J, Henshel A et al. The Biology of Human Starvation. Minneapolis: University of Montana
Press; 1950.
* 9. Kalm LM & Semba RD. They starved so that others be better fed: remembering Ancel Keys and the
Minnesota experiment. J Nutr 2005; 135(6): 1347–1352.
10. Champe PC & Harvey RA. Metabolic effects of insulin and glucagon. In Lippincott’s Illustrated Reviews:
Biochemistry. 2nd edn. Baltimore, MA: Lippincott, 1994, pp. 647–655.
 11. Champe PC & Harvey RA. Metabolism in starvation, diabetes mellitus, and injury. In Lippincott’s Illustrated
Reviews: Biochemistry. 2nd edn. Philadelphia, PA: Lippincott, 1994, pp. 291–302.
12. Campbell IT . Limitations of nutrients intake. The effect of stressors: trauma, sepsis and multiple organ
failure. Eur J Clin Nutr 1999; 53(supplement): S143–S147.
13. Chiolero R, Revelly J & Tappy L. Energy metabolism in sepsis and injury. Nutrition 1997; 13(supplement):
S45–S51.
14. Cerra F . Metabolic and nutritional support. In Feliciano D, Moore E & Mattox K (eds.) Trauma, 3rd edn.
Stamford: Appleton & Lange, 1996.
15. Zoran D. Nutritional management of gastrointestinal disease. Clin Tech Small Anim Pract 2003; 18(4): 211–
217.
16. Kramer J & Kearney M. Patient wound and treatment characteristics associated with healing in pressure
ulcers. Adv Skin Wound Care 2000; 113: 17–24.
17. Breslow R, Halfrish J & Goldberg A. Malnutrition in tubefed nursing home patients with pressure sores.
JPEN 1991; 15(5): 663–667.
18. Breslow R, Hallfrisch J, Guy D et al. The importance of dietary protein in healing pressure ulcers. J Am
Geriatr Soc 1993; 41: 357–362.
19. Wolfe R. An integrated analysis of glucose, fat, and protein metabolism in severely traumatized patients.
Ann Surg 1996; 64: 800–808.
20. Demling R & DeSanti L. Protein-Energy Malnutrition and the Nonhealing Cutaneous Wound, 2003. Available at:
http://www.medscape.com/viewprogram/714_pnt.
21. Can J, Roth H, Court-Ortune I et al. Nutritional depletion I patients on long-term oxygen therapy and/or
home mechanical ventilation. Eur Respir J 2002; 20(10): 30–37.
22. McMahon M, Benotti P & Bistrian B. A clinical application of exercise physiology and nutritional support
for the mechanically ventilated patient. JPEN 1990; 14(5): 538–542.
* 23. Pichard C, Kyle U, Morabia A et al. Nutritional assessment: lean body mass depletion at hospital
admission is associated with an increased length of stay. Am J Clin Nutr 2004; 79(4): 613–618.
24. Ambrosino N & Clini E. Long-term mechanical ventilation and nutrition. Respir Med 2004; 98(5): 413–
420.
* 25. Sungurtekin H, Sungurtekin U, Balci C et al. The influence of nutritional status on complications
after major intrabdominal surgery. J Am Coll Nutr 2004; 23(3): 227–232.
26. Schnelldorfer T & Adams DB. The effect of malnutrition on morbidity after surgery for chronic
pancreatitis. Am Surg 2005; 71(6): 466–473.
* 27. Winsdor A, Braga M, Martindale R et al. Fit for surgery: an expert panel review on optimizing patients
prior to surgery, with a particular focus on nutrition. Surgeon 2004; 2(6): 315–319 [Review].
28. Fearon KC & Luff R. The nutritional management of surgical patients: enhanced recovery after surgery.
Proc Nutr Soc 2003; 62(4): 807–811 [Review].
29. Kudsk KA, Tolley EA, DeWitt RC et al. Pre-operative albumin and surgical site identify surgical risk
for major post-operative complications. JPEN 2003; 27(1): 1–9.
30. Jeejeebhoy KN. Enteral feeding. Curr Opin Gastroenterol 2005; 21(2): 187–191 [Review].
31. Gramlich L, Kichian K, Pinilla J et al. Does enteral nutrition compared to parenteral nutrition result in
better outcomes in critically ill adult patients? A systemic review of the literature. Nutrition 2004;
20(10):
843–848 [Review].
32. Marik PE & Zalonga GP. Meta-analysis of parenteral nutrition versus enteral nutrition in patients with
acute pancreatitis. BMJ 2004; 328(7453): 1407 [Review].
33. Felblinger DM. Malnutrition, infection and sepsis in acute and chronic illness. Crit Care Nurs North Am 2003;
15(1): 71–78.
34. Lesourd B. Nutrition: a major factor influencing immunity in the elderly. J Nutr Health Aging 2004; 8(1):
28–37.
35. Field CJ, Johnson IR & Schley PD. Nutrients and their role in host resistance to infection. J Leukoc Biol
2002; 71(1): 16–32.
36. Amati L, Cirimele D, Pugliese V et al. Nutrition and immunity: laboratory and clinical aspects. Curr Pharm
Des 2003; 9(24): 1924–1931.
37. Cunningham-Rundles S, McNeeliey DF & Moon A. Mechanisms of nutrient modulation of the immune
response. J Allergy Clin Immunol 2005; 115(6): 1119–1128.
 38. Keusch GT. The history of nutrition: malnutrition, infection and immunity. From the Symposium:
Nutrition and Infection, Prologue and Progress Since, 1968. Available at:
http://www.nutrition.org/cgi/content/full/133/
1/336S.
39. Klek S, Kulig J, Szczepanik AM et al. The clinical value of parenteral immunonutrition in surgical patients.
Acta Chir Belg 2005; 105(2): 175–179.
40. Plank LD, McCall JL, Gane EJ et al. Pre-and post-operative immunonutrition in patients undergoing liver
transplantation: a pilot study of safety and efficacy. Clin Nutr 2005; 24(2): 288–296.
41. Farreras N, Artigas V, Cardona D et al. Effect of early post-operative enteral immunonutrition on
wound healing in patients undergoing surgery for gastric cancer. Clin Nutr 2005; 24(1): 55–65.
42. Stechmiller JK, Childress B & Porter T . Arginine immunonutrition in critically ill patients: a
clinical dilemma. Am J Crit Care 2004; 13(1): 17–23 [Review].
43. Sacks GS, Genton L & Kudsk KA. Controversy of immunonutrition for surgical critical-illness patients.
Curr Opin Crit Care 2003; 9(4): 300–305 [Review].
44. Heyland DK & Novak F . Immunonutrition in the critically ill patient: more harm that good? JPEN 2001;
25(2 supplement): S51–S56.
45. Tepaske R, Velthuis H, Oudemans-van Straaten HM et al. Effect of preoperative oral immune-
enhancing nutritional supplement on patients at high risk of infection after cardiac surgery: a
randomised placebo- controlled trial. Lancet 2001; 58(9283): 696–701.
46. Isenring EA, Capra S & Bauer JD. Nutrition intervention is beneficial in oncology outpatients
receiving radiotherapy to the gastrointestinal or head and neck area. Br J Cancer 2004; 91(3): 447–452.
47. Davidson W, Ash S, Capra S et al. Weight stabilization is associated with improved survival duration
and quality of life in unresectable pancreatic cancer. Clin Nutr 2004; 23(2): 239–247.
48. Bistrian BR, Blackburn GL, Hallowell E et al. Protein status of general surgical patients. JAMA 1974; 230:
858–860.
49. Bistrian BR, Blackburn GL, Vitale J et al. Prevalence of malnutrition in general medical patients. JAMA 1976;
235: 1567–1570.
50. Azad N, Murphy J, Amos SS et al. Nutrition survey in an elderly population following admission to a
tertiary care hospital. CMAJ 1999; 161(5): 511–515.
51. Vellas B, Lauque S, Andrieu S et al. Nutrition assessment in the elderly. Curr Opin Clin Nutr Metab Care
2001; 4(1): 5–8.
52. Papini-Berto SJ, Dichi JB, Dichi I et al. Protein-energy malnutrition as a consequence of the
hospitalization of gastroenterologic patients. Arq Gastroenterol 1997; 34(1): 13–21.
53. Gramlich LM. Identifying nutritional risk: nutritional assessment. Gastroenterol Rounds 2000; 4(3).
* 54. Halsted CH. Malnutrition and nutritional assessment. In: Harrison’s Principles of Internal Medicine. 16th edn.
McGraw-Hill, 2005, pp. 411–414.
55. American Dietetics Association. Nutrition assessment of adults. In Manual of Clinical Dietetics. 6th edn.
Chicago, IL: American Dietetic Association, 2000, pp. 3–38.
56. Briefel RR, Sempos CT , McDowell MA et al. Dietary methods research in the third national health
and nutrition examination survey: underreporting of energy intake. Am J Clin Nutr 1997; 65(4
supplement):
1203S–1209S.
57. Detsky AS, Smalley P S & Chang J. Is this patient malnourished? JAMA 1994; 271: 54–58.
58. Obesity Education Initiative Task Force. Clinical Guidelines on the Identification, Evaluation, and Treatment
of Overweight and Obesity in Adults. Bethesda, MD: National Institutes of Health, National Heart, Lung,
and Blood Institute; 1998.
59. Rush E, Plank L, Chandu V et al. Body size, body composition, and fat distribution: a comparison of
young New Zealand men of European, Pacific Island, and Asian Indian ethnicities. N Z Med J 2004;
117(1207): U1203.
60. Charbonneau-Roberts G, Saudny-Unterberger H, Kuhnlein HV et al. Body mass index may
overestimate the prevalence of overweight and obesity among the Inuit. Int J Circumpolar Health 2005;
64(2): 107–109.
* 61. Worthington P. Nutritional assessment and planning in clinical care. In Worthington P (ed.)
Practical Aspects of Nutritional Support: An Advanced Practice Guide. Philadelphia, PA: Saunders, 2004, pp.
159–180.
62. Kyle UG, Bosaeus I, De Lorenzo AD et al. Bioelectrical impedance analysis-part I: review of principles
and methods. Clin Nutr 2004; 23(5): 1226–1243.
 63. Chertow GM, Loazarus JM, Lew NL et al. Bioimpedance norms for the hemodialysis population. Kidney Int
1997; 52(6): 1617–1621.
64. Shopbell JM, Hopkins B & Politzer Shronts E. Nutrition screening and assessment. In Gottschlich M et
al (ed.) The Science and Practice of Nutrition Support: A Case-based Core Curriculum. American Society
for Parenteral and Enteral Nutrition, 2001, pp. 107–140.
* 65. Seres DS. Surrogate nutrition markers, malnutrition, and adequacy of nutrition support. NCP 2005; 20(3):
308–313.
66. Ferard G, Gaudias J, Bourguignat A & Ingenbleek Y. C-reactive protein to transthyretin ratio for the
early diagnosis and follow-up of postoperative infection. Clin Chem Lab Med 2002; 40(12): 1334–1338.
67. Alvares-da-Silva MR & Reverbel da Silveira T . Comparison between handgrip strength, subjective
global assessment, and prognostic nutritional index in assessing malnutrition and predicting clinical
outcome in cirrhotic outpatients. Nutrition 2005; 21(2): 113–117.
68. Kondrup J, Allison SP , Elia M et al. ESPEN guidelines for nutrition screening 2002. Clin Nutr 2003; 22(4):
415–421.
* 69. Valero MA, Diez L, El Kadaoui N et al. Are the tools recommended by ASPEN and ESPEN comparable
for assessing the nutritional status? Nutr Hosp 2005; 20(4): 259–267.
* 70. Pirlich M, Schutz T , Kemps M et al. Prevalence of malnutrition in hospitalized medical patients: impact
of underlying disease. Dig Dis 2003; 21(3): 245–251.
71. Middleton MH, Nazarenko G, Nivison-Smith I et al. Prevalence of malnutrition and 12-month incidence
of mortality in two Sydney teaching hospitals. Intern Med J 2001; 31(8): 455–461.
72. Naber T H, Schermer T , de Bree A et al. Prevalence of malnutrition in nonsurgical hospitalized
patients and its association with disease complications. Am J Clin Nutr 1997; 66(5): 1232–1239.
73. Kelly DG & Nehra V. Gastrointestinal disease. In Gottschlich M et al (ed.) The Science and Practice of
Nutrition Support: A Case-Based Core Curriculum. American Society for Parenteral and Enteral Nutrition,
2001, pp. 517–536.
74. Seidman EG. Nutritional management of inflammatory bowel disease. Gastroenterol Clin North Am 1989;
18: 129–155.
75. Stokes MA & Hill GL. Total energy expenditure in patients with crohn’s disease: measurement by
the combined body scan technique. JPEN 1993; 17(1): 3–7.
76. Fleming CR. Enteral and parenteral nutrition. In Peppercorn MA (ed.) Therapy of Inflammatory Bowel
Disease: New Medical and Surgical Approaches. New York: Marcel Dekker, 1990, pp. 145–157.
77. Abitol V, Roux C, Chaussade S et al. Metabolic bone assessment in patients with inflammatory bowel
disease. Gastroenterology 1995; 108: 417–422.
78. Cummings JA. Short chain fatty acids in the human colon. Gut 1981; 22: 763–779.
79. Dichi I, Frenhane P, Dichi JB et al. Comparison of u-3 fatty acids and sulfasalazine in ulcerative colitis.
Nutrition 2000; 16: 87–90.
80. Tsujikawa T , Satoh J, Uda K et al. Clinical importance of n-3 fatty acid-rich diet and nutritional
education for the maintenance of remission in Crohn’s disease. J Gastroenterol 2000; 35: 99–104.
81. Penner RM & Fedorak RN. Probiotics in the management of inflammatory bowel disease. Med Gen Med
2005; 7(3).
82. Matos C, Porayko K, Francisco-Ziller N & DiCecco S. Nutrition and chronic liver disease. J Clin
Gastroenterol 2002; 35(5): 391–397.
83. McCullough AJ. Malnutrition in liver disease. Liver Transpl 2000; 6(4 supplement): S85–S96.
84. Figueiredo F A, Dickson ER, Pasha T M et al. Utility of standard nutritional parameters in detecting
body cell mass depletion in patients with end-stage liver disease. Liver Transpl 2000; 65: 575–581.
85. Patton KM & Aranda-Michel J. Nutritional aspects in liver disease and liver transplantation. NCP 2002; 17:
332–340.
86. Teran JC & McCullough AJ. Nutrition in liver diseases. In Gottschlich M et al (ed.) The Science and
Practice of Nutrition Support: A Case-Based Core Curriculum. American Society for Parenteral and Enteral
Nutrition,
2001, pp. 537–552.
87. Marchesini G, Fabbri A, Bianchi GP et al. Zinc supplementation and amino acid nitrogen metabolism
in patients with advanced cirrhosis. Hepatology 1996; 23: 1084–1092.
88. Russell MK. Acute pancreatitis: a review of pathophysiology and nutrition management. NCP 2004; 19:
16–24.
89. Seidner DL & Fuhrman MP. Nutrition support in pancreatitis. In Gottschlich M et al (ed.) The Science
and Practice of Nutrition Support: A Case-Based Core Curriculum. American Society for Parenteral and
Enteral Nutrition, 2001, pp. 553–573.
90. Duerksen DR & Siemens JL. Nutritional support in acute pancreatitis. Clin Nutr Rounds 2001; 1(3).
91. Giger U, Stanga Z & DeLegge MK. Management of chronic pancreatitis. NCP 2004; 19: 37–49.
92. Vaona B, Armellini F , Bovo P et al. Food intake with chronic pancreatitis after onset of the disease. Am
J Clin Nutr 1997; 65: 851–854.