What’s new?

C NICE guidance on nutrition support in adults

C Detailed nationwide BAPEN survey assessing nutritional status

of hospital admissions revealed the extent of the problem

C The high estimated financial cost of malnutrition has focused

political attention on addressing the problem of malnutrition

UNDERNUTRITION AND CLINICAL NUTRITION

Malnutrition andundernutritionJohn Saunders

Trevor Smith

Mike Stroud

C Objectives for Nutrition in Undergraduate Medical Training

(ICGN/Academy of Royal Medical Colleges)

Causes of malnutrition and further deterioration innutritional status among hospital in-patients

Medical causes of

inadequate and/or

poor’quality oral intake

C Anorexia of disease

C Nausea and vomiting

C Gastrointestinal dysfunction

C Reduced absorption of macro-

and/or micro-nutrients

C Increased nutrient loses

C ‘Nil by mouth’ for investigation

or medical reasons

C Physical disability and inability

AbstractThe term malnutrition is used to describe a deficiency, excess or imbal-

ance of a wide range of nutrients, resulting in measurable adverse effects

on body composition, function and clinical outcome.1 As such it can refer

to individuals who are either over- or under-nourished although it is

frequently used synonymously with undernutrition, as is the case in

this article. Although it is well known that malnutrition is common

in the developing world, the fact that significant malnourishment occurs

in UK society and health settings is not widely appreciated. Malnutrition

occurs for psychosocial reasons and as a consequence of disease. It has

direct effects on clinical outcomes and is associated with massive health-

care expenditure. Recognition and treatment can have a significant

impact on patient care and can reduce costs. Failure to diagnose and

manage carries medico-legal risks. It is the responsibility of all doctors

to recognize the fundamental importance of proper nutritional care to

good clinical practice.2 The focus of this article is predominantly con-

cerned with malnutrition and its consequences in the UK.

Keywords clinical outcome; health economics; malnutrition; MUST

score; re-feeding syndrome; screening

The term malnutrition is used to describe a deficiency, excess or

imbalance of a wide range of nutrients, resulting in measurable

adverse effects on body composition, function and clinical

outcome.1 It is the responsibility of all doctors to recognize the

importance of proper nutritional care to good clinical practice.2

Worldwide, more than 3.5 million mothers and children under 5

die unnecessarily each year owing to malnutrition,3 and around

178 million children have stunted growth. Micronutrient defi-

ciencies affect huge numbers; iodine deficiency alone is thought

to affect about 2 billion people.

John Saunders MRCP is a Research Fellow in Clinical Nutrition at the

Institute of Human Nutrition and a Specialist Registrar in

Gastroenterology at Southampton University Hospital, Southampton,

UK. Competing interests: none declared.

Trevor Smith MRCP is a Consultant in Clinical Nutrition and Gastroenterology

at the Institute of Human Nutrition and Southampton University Hospital,

Southampton, UK. Competing interests: none declared.

Mike Stroud BSc MD DSci FRCP is a Consultant Gastroenterologist and

Senior Lecturer in Medicine and Nutrition at the Institute of Human

Nutrition and Southampton University Hospital, Southampton, UK.

Competing interests: none declared.

MEDICINE 39:1 45

In the UK, malnutrition remains an under-recognized problem

facing patients, clinicians and the wider society. It is not only very

common in hospital and institutional care settings but iswidespread

in the community. It is both a consequence and a cause of disease.

Approximately 2%of theUKpopulation are underweighte defined

as a body mass index (BMI) below 18.5 kg/m2 e but this is an

underestimate ofmalnutrition, since thosewhounintentionally lose

weight from a position of relative excess may also be at risk what-

ever their BMI. The prevalence of malnutrition in the free-living

elderly or thosewith chronic diseases increases at least two-fold and

individuals in institutional care have a prevalence of malnutrition

between 30 and 42%.4

UKhospitalpatientswithmalnutrition are particularly likely tobe

malnourished for reasons summarized in Table 1. In a large national

survey conducted in 2008, 28%of patients admitted in hospitalwere

at risk as indicated by a high score on the MUST screening tool. The

prevalence was particularly high in specific sub-populations (e.g.

34% of all emergency admissions and 52% of admissions from care

to feed self

Environmental causes of

inadequate and/or poor’

quality oral intake

C Inadequate food quality

C Inadequate food availability

C No protected meal times

C Inadequate training and

knowledge of medical and

nursing staff

Altered requirements C In critical illness there are altered

substrate demands and several

sub-groups of patients have a

increased energy expenditure

(see below)

Table 1

� 2010 Elsevier Ltd. All rights reserved.

UNDERNUTRITION AND CLINICAL NUTRITION

homes).4 Many patients also see a further decline in their nutritional

status during their hospital admission,which can then increase their

risk of complications and length of stay.

Micronutrient deficiencies: in the UK, specific micronutrient defi-

ciencies are also surprisingly common, especially in the elderly.

Folate deficiency has been described in 29% of independent adults

over 65 years old and 35% of those in institutions, while vitamin C

deficiency affects 40% of those in institutional care.5

Causes of malnutrition

Although a proportion of malnutrition in developed countries is

associated with poverty, social isolation and substance misuse,

exacerbating the health inequalities in vulnerable populations,

most adult malnutrition in the UK is associated with disease,

arising from several sources (Figure 1).

Reduced dietary intake is probably the single most important

aetiological factor in disease-related malnutrition. This can be the

result of many psychosocial conditions, importantly including

age, depression, and dementia. During illness there is commonly

reduction in appetite sensation owing to modified secretion of

cytokines, glucocorticoids, peptides, insulin and insulin-like

growth factors.6 In hospital in-patients, these problems may be

compounded by failure to provide regular nutritious meals, to

protect them from routine clinical activities, and to offer help and

support with feeding when required.7 Among patients under-

going abdominal surgical procedures, varying degrees of intes-

tinal failure (whether short-term or more sustained) add further

nutritional risks. While there is usually a rebound of appetite

after recovery, to restore lost weight and functional capacity, this

response is suppressed by continued inflammation, or by the

Causes of malnutrition

Altered nutrient processing• Increased/altered

metabolic demands

• Liver dysfunction

Inadequate intake• Poor diet

• Poor appetite

• Pain/nausea with

food

• Dysphagia

• Depression

• Unconsciousness

Malabsorption• Pathology of stomach,

intestine, pancreas

and liver

Excess losses• Vomiting

• NG tube

drainage

• Diarrhoea

• Surgical

drains

• Fistulae

• Stomas

Figure 1

MEDICINE 39:1 46

early recurrence of the precipitate illness, e.g. in patients with

chronic obstructive pulmonary disease (COPD).

Although for many years it was thought that increased energy

expenditure was predominantly responsible for disease-related

malnutrition, there is now clear evidence that inmany disease states

total energy expenditure is actually less than that measured in

normal health. The basal hypermetabolism of disease is offset by

a reduction in physical activity, with studies in intensive care

patients demonstrating that energy expenditure is usually below

2000 kcal/day.8Weight loss in patientswith persistent inflammation

or neoplasia may be accompanied by altered demands for specific

amino acids in disease states. The body meets these needs by

drawingon its reserves,with excess lean tissuewasting.Thismaybe

evident as cachexia in a thin patient, but loss of lean tissue (sac-

rcopenia) can be more difficult to detect in an overweight patient.

Consequences of malnutrition

Malnutrition affects the function and recovery of every organ

system (see Figure 2).

Muscle andbone:weight loss causedbydepletion of fat andmuscle

mass, including organ mass, is often the most obvious clinical sign

of malnutrition. The visible loss of lean tissue is often described as

cachexia and may be hidden in obese patients. Muscle function

declines before changes in muscle mass occur, suggesting that

altered nutrient intake has an important functional impact inde-

pendent of the effects on muscle mass; similarly, improvements in

muscle functionwith nutrition support occurmore rapidly than can

be accounted for by replacement ofmusclemass alone.9 Bonemass

is lost during weight loss and specifically when intakes of calcium,

Effects of malnutrition

• Ventilation:

loss of muscle

and hypoxic

responses

• Psychology:

depression/

apathy

• Reduced cardiac

output

• Impaired renal

function

• Reduced

strength

• Hypothermia

• Impaired liver

function and fatty

change/necrosis

• Decreased

immunity and

resistance to

infection

• Impaired

wound healing

• Impaired gut

intregrity and

immunity

Figure 2

� 2010 Elsevier Ltd. All rights reserved.

Clinical features of classical re-feeding syndrome

Cardiovascular Cardiac failure

Pulmonary oedema

Dysrhythmias

Peripheral oedema

Electrolyte disturbance Hypophosphataemia

Hypokalaemia

Hypomagnesaemia (rarely hypocalcaemia)

Metabolic Hyperglycaemia

Neurological Wernicke’s encephalopathy

Confusion

Seizures

Hepatological Abnormalities in liver function

Musculoskeletal Rhabdomyolysis

Haematological Bone marrow dysfunction

Table 2

UNDERNUTRITION AND CLINICAL NUTRITION

magnesium and/or vitamin D are insufficient. Bones are slow to re-

form during recovery, and fracture risk is high.

Cardiovascular and respiratory: a reduction in cardiacmusclemass

is recognized in malnourished individuals. The resulting decrease in

cardiac output has a corresponding impact on renal function by

reducing renal perfusionand glomerular filtration rate.Micronutrient

(e.g. thiamine) and electrolyte deficiencies may also affect cardiac

function, particularly during re-feeding. Poor diaphragmatic and

respiratory muscle function reduces cough pressure and expectora-

tion of secretions, delaying recovery from respiratory tract infections.

Gastrointestinal: adequate nutrition is important for preserving

gastrointestinal function; chronicmalnutrition results in changes in

pancreatic exocrine function, intestinal blood flow, villous archi-

tecture and intestinal permeability. Loss of digestive enzymes

occurs early with dietary energy restriction and commonly leads to

secondary lactose intolerance, with diarrhoea. The colon loses its

ability to reabsorb water and electrolytes, and secretion of ions and

fluid occurs in the small and large bowel. This may result in diar-

rhoea, which is associated with a high mortality rate in severely

malnourished patients.

Immunity and tissue repair: immune function is suppressed early

with underfeeding as a result of impaired cell-mediated immunity

and cytokine, complement and phagocyte function, and this

increases the risk of infection. Delayed wound healing is also well

described in malnourished surgical patients.10 Malnourished

patients are at particular risk from respiratory tract infections, and

any bacterial or parasitic infection is liable to progress rapidly.

Fever, and usual markers of acute inflammation (WBC, CRP) may

be suppressed inmalnutrition, so early antibioticsmay be advised.

Endocrine: most endocrine functions are suppressed by malnu-

trition. Specifically, T4 and T3 are reduced, while reverse T3

rises. Thyroid-stimulating hormone is usually normal, unless

iodine status is impaired. Gonadotrophins are suppressed, and

testerone and oestrogen/progesterone all fall. Amenorrhoea is

usual. Insulin secretion is reduced, but insulin sensitivity rises

during undernutrition, so blood glucose remains low-normal.

Hypoglycaemia is a very late pre-terminal development but may

also indicate occult sepsis. During re-feeding, insulin resistance

may result in a form of ‘malnutrition-related diabetes’.

Psychological: in addition to these physical consequences,

malnutrition also results in psychosocial effects, such as apathy,

depression, anxiety and self-neglect.

Reductive adaptation: a down-regulation of energy-dependent

cellular membrane pumping (Na/K-ATPase) and other basic

cellular metabolic functions, is one explanation for the conse-

quences of malnutrition. In complete starvation, the process

begins very early. It is less striking when dietary intake is simply

insufficient tomeet requirements and the body has time to drawon

its functional tissue reserves within muscle, adipose tissue and

bone, although this then leads to detrimental changes in body

composition. Both reductive adaptation and tissue wasting have

direct consequences on tissue function, with loss of functional

capacity and a potentially brittle metabolic state. Rapid decom-

pensation occurs with insults such as infection and trauma.11

MEDICINE 39:1 47

Re-feeding syndrome describes the potentially life-threatening

consequences that can occur as a result of acute micronutrient

deficiencies, fluid and electrolyte imbalance and organ dysfunc-

tion caused by administration of unbalanced or over-rapid

nutritional support in patients at risk (see Table 2). Patients

particularly at risk are those with little or no oral intake for

protracted periods and those who are severely malnourished (see

Table 3). Patients with limited nutritional intake, altered meta-

bolic demands and/or increased losses undergo reductive adap-

tation and, as a result are deficient in vitamins, trace elements

and electrolytes. There is a whole body and intracellular deple-

tion of potassium, magnesium and phosphate, and a consequen-

tial increase in intracellular sodium and water. There is also

a switch away from carbohydrate to lipid metabolism as the

predominant source of energy. The provision of nutrients will

reverse these changes but administration that is either too rapid

or in an unbalanced form can result in dangerous shifts in elec-

trolytes and precipitate deficiencies in micronutrients. Patients

most at risk are those receiving enteral tube feeding or parenteral

nutrition, but care should also be taken with oral nutritional

supplements. The National Institute for Health and Clinical

Excellence (NICE) has specific guidance for managing these

complex patients.12 An intercollegiate working group, MARSI-

PAN (Management of Really Sick Patients with Anorexia Nerv-

osa), has produced guidelines on the medical and psychiatric

management of patients with anorexia nervosa.13

Assessment of nutritional status and diagnosis of malnutrition

Nutritional status is a composite concept, incorporating dietary

intake (what we eat), body composition (what we are) and

functional capacity (what we can do). Information is needed

about all these components.

Screening

Identification of patients at risk of malnutrition at an early stage

of hospital admission, or during attendance at the outpatient

� 2010 Elsevier Ltd. All rights reserved.

Criteria for determining patients at high risk ofdeveloping re-feeding problems12

The patient has one or

more of the following

C BMI less than 16 kg/m2

C Unintentional weight loss of greater

than 15% within the last 3e6 months

C Little/no nutritional intake for more

than 10 days

C Low levels of potassium, phosphate

or magnesium prior to feeding

The patient has two or

more of the following

C BMI <18.5 kg/m2

C Unintentional weight loss of greater

than 10% within the last 3e6 months

C Little/no nutritional intake for more

than 5 days

C History of alcohol abuse or drugs

including insulin, chemotherapy,

antacids or diuretics

Table 3

UNDERNUTRITION AND CLINICAL NUTRITION

clinic, is a screening step to determine which patients need

formal assessment of nutritional status by a qualified trained

person, with a view to early intervention with nutritional

therapy. The Malnutrition Universal Screening Tool (MUST) is

a simple, rapid and easy method to screen patients and has been

shown to be reliable and valid.14 It aims to identify those at risk

by incorporating simple information which is collected routinely

for other reasons:

� current weight and height (BMI)

� history of recent unintentional weight loss

� likelihood of future weight loss.

Figure 3 provides a guide for using MUST e the total score has been

shown to be a better predictor of outcome than scores from the indi-

vidual componentsused in isolation, and identifiesmostpatientswho

have malnutrition.

The screening process identifies patients who require a more

detailed assessment, and formulation of an individualized stepwise

managementplanbyanutritionspecialist.Re-screeningof in-patients

at 7-day intervals throughout a hospital admission alerts clinicians to

those who have lost weight and require greater intervention.

Detailed nutritional assessment

Full nutritional assessment to diagnose malnutrition is based on

mainly history and examination, with rather less emphasis on labo-

ratory investigations than is usual for most diagnostic processes.

Medical history

� Normal and varied recent dietary intake; an overview of daily

food intake, pattern of meals and portion size. Food

intolerance, allergies, religious or other restrictions. Specialist die-

tetic input is appropriate in patients where concern has been raised.

� History of recent intentional or unintentional weight loss.

Weight loss in obesity or in patients with oedema can be more

challenging to assess.

� Is the patient able to eat, swallow, digest and absorb sufficient

amounts of food to meet their requirements?

MEDICINE 39:1

� Are there any physical, medical, psychiatric or treatment

limitations that prevent patients meeting their requirements and

lead to weight loss?

� Does the patient have particularly high requirements for

certain nutrients (e.g. burns patients)?

� Does the patient have excessive nutrient losses, e.g. persistent

diarrhoea or enterocutaneous fistulae? Chronic pancreatitis can

cause malabsorption without steatorrhoea.

� Psychosocial history (e.g. recent social stress, social isolation,

previous eating disorders, alcohol consumption, prescription or

recreational drugs).

48

Examination

A focused examination should include:

� weight and BMI

� muscle wasting (e.g. appearance of temporalis)

� general condition of skin: fragile or dry

� general condition of mouth; presence of angular cheilitis and

mouth ulcers

� hydration status

� assessment of oedema.

Investigations

Most biochemical nutrient measures are acute-phase reactants, so

difficult to interpret. There are no specific laboratory tests to

‘diagnose malnutrition’. Blood tests can diagnose some specific

nutrient deficiencies (e.g. iron, folate, B12), provide supportive

information for monitoring and assessing specific electrolytes e.g.

magnesium. Low serum albumin is still commonly listed as an

indicator of malnutrition. Simple starvation does not suppress

serum albumin, but the presence of infection, or another inflam-

matory process reduces albumin more than in a well-nourished

patient. Low serum albumin thus usually implies reduced

synthetic capacity in the liver, which cannot be corrected by

increased protein or aminoacid supply. Bedside tests (e.g. mid-

arm muscle circumference, hand-grip strength and indirect calo-

rimetry) can be useful aids but are usually reserved for clinical

studies or departments with specialist interests, owing to the costs

of equipment, expertise required and time involved.

The diagnosis of malnutrition is very important. It must be

documented together with a management plan, coded and

included in discharge letters.

Management

All hospitals should have an established multidisciplinary

nutrition support team for managing patients with complex

nutritional problems. Within each organization there should also

be a nutrition steering committee to develop policies for nutri-

tional care, which should be regularly audited as part of clinical

governance frameworks.12

Individual patients’ needs vary enormously, depending on

their circumstances. The aim of nutrition support is to ensure

that total nutrient intake provides enough energy, protein, fluid

and micronutrients to meet the patients’ needs. In practice, the

majority of patients are managed by clinicians, nursing staff,

ward catering staff and dietitians, with more complex patients

having input from nutrition support teams.

In vulnerable patient groups the simple provision of regular

meals or food with better nutritional content may be enough to

� 2010 Elsevier Ltd. All rights reserved.

1995 1997 1999 2001 2003

The Malnutrition Universal Screening Tool (MUST)

STEP 1BMI score

STEP 4Overall risk of malnutrition

STEP 5Management guidelines

0Low risk

Routine clinical care

1Medium risk

Observe

2 or moreHigh risk

Treat*

• Repeat screening:

Hospital, weekly;

Care homes, monthly;

Community, annually

for special e.g. those >75 yrs

All risk categories• Treat underlying condition and provide help and advice on

food choices, eating and drinking when necessary

• Record malnutrition risk category

• Record need for special diets and follow local policy

Obesity• Record presence of obesity. For those with underlying

conditions, these are generally controlled before the

treatment of obesity

• Document dietary intake for 3 days if

subject in hospital or care home

• If improved or adequate intake – little

clinical; if not improvement – clinical

concern – follow local policy

• Repeat screening:

Hospital, monthly;

Care home, at least monthly

Community, at least every 2–3 months

• Refer to dietitian, nutritional

support team or implement local

policy

• Improve and increase overall

nutritional intake

• Monitor and review care plan:

Hospital, weekly;

Care home, monthly;

Community, monthly

STEP 2Weight loss score

Re-assess subjects identified at risk as they move through care settings. A BMI of <20 kg/m2 (i.e. above the WHO BMI <18.5 kg/m2

cut-off for undernutrition) is used in the MUST score when screening patients who are unwell, to capture those whose weight is lowerthan average (BMI 18.5–20) together with other criteria of undernutrition. In this setting it is more important to identify all patientswho are undernourished (high sensitivity) and less important to exclude false-positives from a dietetic assessment.

STEP 3Acute disease effect score

BMI kg/m2 Score>20 (>30 obese) –0

18.5–20 –1

<18.5 –2

Unplanned weight loss in past 3–6 months

>20 (>30 obese) –0

18.5–20 –1

<18.5 –2

If patient is acutely ill and there has

been, or is likely to be, no nutritional

intake for >5 days

Score 2

Add scores together to calculate overall risk of malnutrition

Score 0: Low risk Score 1: Medium risk Score 2 or more: High risk

Figure 3

UNDERNUTRITION AND CLINICAL NUTRITION

address nutritional risk. Additional measures may include broader

menu choices or providing assistance with feeding. Where these

‘social’ interventions are insufficient to ensure that nutritional

requirements are met, patients will need the addition of oral nutri-

tional supplements or enteral tube feeding, under dietetic supervi-

sion. Parenteral nutrition is rarely necessary, except in the context of

an inaccessible or non-functioning gastrointestinal tract.

Management of severe malnutrition includes initial resusci-

tation, to restore hydration, and replace electrolytes. Before

feeding starts, thiamine must be provided, to avoid Wernicke’s

encephalopathy when carbohydrate is consumed or fed (espe-

cially if there is a history of alcohol excess). Severely

MEDICINE 39:1 49

malnourished patients are at risk of re-feeding syndrome, and

death. This risk is reduced if electrolytes are monitored closely,

and extra phosphate, potassium and magnesium are provided.

Nutritional replenishment will be successful in restoring body

composition and functional capacity sustainably, only if the

underlying cause can be removed or controlled. A persisting

inflammatory state (high WBC, CRP, TNF) is a major obstacle to

synthesis and re-growth of lean tissue, so surplus energy is stored

as fat, with little functional gain. Excess energy supply leads

rapidly to ectopic fat deposition especially in the liver, with

potentially fatal results. Attempts to increase appetite pharma-

cologically are seldom effective.

� 2010 Elsevier Ltd. All rights reserved.

Practice points

C Malnutrition is a common, under-recognized and under-treated

condition in hospital patients.

C Disease-related malnutrition arises from reduced dietary

intake, malabsorption, increased nutrient losses or altered

metabolic demands.

C Wide-ranging changes in physiological function occur in

malnourished patients, leading to increased rates of morbidity

and mortality.

C Re-feeding syndrome is a serious and potentially fatal

complication, which is avoidable by careful consideration of

nutritional treatment.

C Routine nutritional screening should be undertaken in all

patients admitted to hospital using a validated tool such as

the Malnutrition Universal Screening Tool (MUST).

C Healthcare costs are significantly increased in malnourished

patients.

C The diagnosis of malnutrition is vital for medical, social and

medico-legal reasons.

UNDERNUTRITION AND CLINICAL NUTRITION

Malnutrition, clinical outcome and the health economics

The consequences of malnutrition for physiological function

have an important impact on clinical outcome. Malnourished

surgical patients have complication and mortality rates three to

four times higher than normally nourished patients, with longer

hospital admissions, and incur up to 50% greater costs. Similar

findings have also been described in medical patients, particu-

larly the elderly.15,16 It is often difficult to separate the delete-

rious effects of malnutrition from the underlying disease process

itself, especially because each can be a cause and consequence of

the other. However, there is clear evidence that nutrition support

significantly improves outcomes in these patients and it is vital

that malnutrition is identified through screening.

Malnutrition is also a major resource issue for public expen-

diture. The British Association of Parenteral and Enteral Nutri-

tion (BAPEN) have recently calculated that the costs associated

with disease-related malnutrition in 2007 in the UK were more

than £13 billion (greater than those associated with obesity). The

potential cost savings associated with the prevention and treat-

ment of malnutrition are considerable e a saving as small as 1%

represents £130 million per year. In specific situations, treating

malnutrition produces cost savings of 10e20% or more.17

Nutritional education

The importance of training medical students and junior doctors in

nutrition has been widely recognized; a report from a working

party of the Royal College of Physicians stated “Every doctor

should recognize that proper nutritional care is fundamental to

good clinical practice”.2 By addressing deficiencies in education of

all healthcare professionals and exerting influence through clinical

leadership there can be genuine improvements in nutritional care.

Learning objectives for Human Nutrition within Medical

Training have been published on-line by the Intercollegiate

Group on Nutrition, through its position within the Academy of

Royal Medical Colleges.18

Conclusions

Malnutrition has wide-ranging effects on physiological function

applicable to all disciplines of medicine, yet is often overlooked

by clinicians. It is associated with increased complications

resulting in increased morbidity and mortality in hospital in-

patients and significantly increased healthcare costs. Identifica-

tion of at-risk patients through better assessment and the use of

screening tools and efficient full assessment to make the diag-

nosis allows appropriate treatment to be instituted, which can

significantly improve clinical outcomes. A

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� 2010 Elsevier Ltd. All rights reserved.