EBRSR
[Evidence-Based Review of Stroke Rehabilitation]
16
Nutritional Interventions Following
Stroke
Norine Foley MSc, Robert Teasell MD, Marina Richardson MSc, Sanjit Bhogal MSc, Mark Speechley PhD
(We gratefully acknowledge the contribution of Dr. Hillel Finestone)
Last Updated: August 2013
Abstract
Nutritional status following stroke can have a negative impact on functional recovery and mortality.
Complications associated with malnutrition include a greater incidence of infections and pressure sores,
and longer lengths of hospital stays. Clinical nutritional management requires effective methods of
assessment, an understanding of the underlying causes of nutritional deficiencies, and effective
methods of administering nutrients via feeding techniques and supplementation. In this review, the
incidence of malnutrition post stroke is evaluated and markers used to identify deficiencies are
discussed. A summarization of potential causes of nutritional deficiencies is provided including
hypermetabolism, increased catabolism, and gastrointestinal and food intake issues. Interventions
including enteral feeding and oral supplementation are then discussed as well as treatments for
dysphagia.
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Key Points
Prevalence of Malnutrition

Malnutrition is a relatively common problem post stroke.

Patients consume fewer calories and protein following stroke.

Patients are not hypermetabolic acutely following stroke.
Nutritional Interventions

Intragastric feeding tubes are associated with fewer complications, compared with naso-enteric
tubes, when patients require nutrition support for at least 28 days.

Oral supplementation improves energy and protein intake although it does not improve
functional outcomes.

The one-year survival rate of patients with feeding tubes, discharged to the community varied
widely following stroke.

The use of TPN has not been studied in the stroke population.
Dr. Robert Teasell
801 Commissioners Road East, London, Ontario, Canada, N6C 5J1
Phone: 519.685.4000 ● Web: www.ebrsr.com ● Email: Robert.Teasell@sjhc.london.on.ca
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Table of Contents
Abstract ....................................................................................................................... 1
Key Points .................................................................................................................... 2
Table of Contents ........................................................................................................ 3
16. Nutritional Interventions Following Stroke ............................................................. 4
16.1 Markers Used in the Assessment of Nutritional Status ................................................ 4
16.2 The Prevalence of Malnutrition Post Stroke ................................................................ 5
16.3 Factors Associated With the Development of Malnutrition ....................................... 11
16.3.1 Hypermetabolism Following Stroke ........................................................................... 12
16.3.2 Increased Catabolism Following Stroke ..................................................................... 13
16.3.3 Gastrointestinal Function Following Stroke ............................................................... 14
16.3.4 Nutrient Intake Following Stroke ............................................................................... 15
16.3.5 Stroke-Related Factors ............................................................................................... 15
16.4 Nutritional Interventions Following Stroke ............................................................... 15
16.4.1 Enteral Feeding ........................................................................................................... 16
16.4.2 Oral Supplementation ................................................................................................ 19
16.4.3 Dysphagia Treatment ................................................................................................. 23
16.4.4 Effect of Nutritional Interventions on Changes in Nutritional Parameters ............... 24
16.5 Enteral Feeding in the Community ............................................................................ 25
16.6 Total Parenteral Nutrition (TPN) ............................................................................... 27
16.7 Cochrane Reviews of Nutritional Interventions Following Stroke............................... 27
16.8 Summary .................................................................................................................. 29
References ................................................................................................................. 31
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16. Nutritional Interventions Following Stroke
Declines in nutritional status following stroke are potentially important because of the negative impact
on functional recovery and mortality. Preliminary results from the FOOD trial reported poor nutritional
status was associated with an increase in the odds of death and dependency at six months after
adjusting for a number of confounders (OR 1.82; 95% CI, 1.34 to 2.47) (FOOD Trial Collaboration 2003).
Poor nutrition has been found to predict lower functional status following stroke. In a study focusing on
the functional consequences of malnutrition in stroke rehabilitation, patients’ serum albumin used as an
marker of nutritional status was associated with poorer functional mobility, increased complications,
and lower self-care scores (Aptaker et al. 1994).
Davalos et al. (1996) also reported that malnutrition after the first week of stroke was associated with
an increased risk of poor outcome (death or dependency) at one month, a greater incidence of
infections and pressure sores, and longer lengths of hospital stays, among a group of 104 patients with
acute stroke. Patients, who were considered malnourished had an elevated risk of death or poor
outcome at 30 days follow-up (OR, 3.5; 95% CI, 1.2 to 10.2).
Gariballa et al. (1998a) investigated the associations between a variety of anthropometric and
biochemical parameters assessed on admission to hospital and outcome following stroke, among 201
patients. After adjusting for age, comorbid conditions, sex, medications and stroke severity, serum
albumin was related to an increase in death at three months. Each decline of 1 g/L in serum albumin,
measured on admission, was associated with a 1.13-fold increase in death at follow-up.
16.1 Markers Used in the Assessment of Nutritional Status
Currently, there is no universally accepted gold standard for the assessment of nutritional status. The
identification of malnutrition is typically based on the evaluation of a combination of biochemical and
anthropometric markers and is inferred, based on either a single value or multiple values, falling outside
of specific population reference ranges or below a certain percentile within these ranges. Since the
combination of markers used and the cut-off values are chosen arbitrarily, reports of malnutrition will
vary widely. As a result, the true incidence of malnutrition following stroke is likely unknown. Both
biochemical and anthropometric indicators are used in the evaluation of nutritional assessment Table
16.1 presents some the more commonly used biochemical indicators used as well as their limitations.
Unfortunately, many of these nutrition sensitive markers are affected independently by factors
associated with stroke (or any other acute illness), complicating the process of evaluating the response
to nutritional interventions. Although both albumin and prealbumin are used extensively in nutritional
assessment, the hepatic production of these two proteins is known to be down-regulated during periods
of acute illness, independent of nutritional status (Fleck 1989; Gabay & Kushner 1999). While
hypoalbuminemia has been repeatedly shown to be associated with morbidity and mortality the causal
mechanism is not clear. Akner and Cederholm (2001) did not demonstrate a relationship between
protein and caloric intakes and serum albumin in their institutionalized elderly population. Difficulties
arise due to the fact that biochemical markers of nutrition can change rapidly, whereas a change in
nutritional status is considered more latent and takes longer to manifest. In addition, the presence of
concurrent infection or elevations in temperature can affect serum markers, mimicking signs of
malnutrition.
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Table 16.1 Biochemical Markers of Nutritional Status (Manual of Clinical Dietetics, 2000)
Measure
Serum albumin
Serum transferrin
Thyroxin Binding Prealbumin
Retinol Binding Protein
Total Lymphocyte Count
Limitations
Large body pool
Poor specificity to nutritional changes
Not specific to nutritional status
↓ with acute illness
Not specific to nutritional status
↓ with acute illness
Not specific to nutritional status
↓ with acute illness
Not specific to nutritional status
Poor sensitivity and specificity
Measures of nutrition assessment also include indicators of skeletal muscle mass and subcutaneous fat
stores measures. Examples of these measurements include weight, mid arm muscle circumference and
skinfold thickness. While declines of these indicators may be associated with the development of
malnutrition, factors secondary to stroke may also affect the sensitivity of these measures. Skeletal
muscle losses may occur over prolonged periods of time as a result of atrophy, secondary to immobility
(Deitrick et al. 1948; Schonheyder et al. 1954). It may be difficult to differentiate between these losses
and those that are associated with inadequate food intake, adding to the difficulties of evaluating
nutritional status. Malnutrition is usually considered to be a state that develops over time in response
to inadequate intake, relative to need and results in gradual weight loss with associated losses of lean
body mass (muscle) and subcutaneous fat stores. Since the identification of malnutrition among the
majority of studies was made on the basis of both anthropometric and biochemical markers it is possible
that the higher percentage of patients reported to be malnourished in studies that measured
malnutrition at a later point in the hospitalization period reflected non-nutritional changes in body
composition.
16.2 The Prevalence of Malnutrition Post Stroke
The prevalence of malnutrition following stroke has been reported to be between 6% and 62 % (see
Table 16.2). If the criteria are widened to include the secondary criteria used in two studies, the range of
estimates broadened to 1.3% to 73%. Some of this variability can likely be attributed to differences in
patient characteristics and the timing of assessments among studies. However, a substantial proportion
of the variation in estimates may also be explained by the heterogeneity of nutritional assessment.
Among the 22 trials reviewed below, 18 different assessment methods were used. Only five trials used
previously validated assessment methods; Subjective Global Assessment (SGA), “an informal
assessment”, and Mini Nutritional Assessment (MNA). The nutritional assessment methods used in the
remaining studies used had not been validated previously.
The three valid assessment tools mentioned above were created for differing purposes. The informal
“eyeball” assessment was developed specifically to classify patients into groups based on nutritional
state within the context of the large, multi-centred FOOD trials. Subjective Global Assessment was
designed for use in the prediction of risk for complications following general surgery following general
surgery, based on pre-operative nutritional state, while Mini Nutritional Assessment, the third valid tool,
was developed as a screening and assessment tool to identify geriatric patients at risk for malnutrition.
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Although both SGA and MNA have been validated subsequently for use in other disease or injury states,
validation of these tools for the assessment of individuals with stroke is lacking. In one study, a group of
35 patients with stroke, aged 60 to 89 years were assessed for nutritional status using laboratory
measures and the SGA and MNA. There was strong correlation between SGA and objective measures
when patient nutrition status was classified as normal, mildly malnourished, moderately malnourished
and severely malnourished (r=0. 449), and strong correlation between MNA and objective measures
when patient nutrition status was dichotomized (well-nourished vs. at risk of malnutrition or
malnourished) (r=0.520) (Kim et al. 2013).
Table 16.2 The Prevalence of Malnutrition Following Stroke
Author/Year/Co % of patients identified with malnutrition
untry/Study
and the timing of assessment
Type
Axelsson et al. 16% within 4 days of symptom onset
(1988)
(n=100)
Sweden
Prospective
22% at hospital discharge (n=78)
case series
DePippo et al.
(1994)
USA
5 (RCT)
Unossen et al.
(1994)
Sweden
Prospective
case series
Finestone et
al. (1995)
Canada
Prospective
case series
Davalos et al.
(1996)
Spain
Prospective
case series
Choi-Kwon et
al. (1998)
South Korea
CrossSectional
Aquilani et al.
(1999)
6.1% at any point between
rehabilitation hospital admission
(median of 4.6 weeks post stroke) and
discharge (n=115)
8% within 2 days of symptom onset
(n=50)
Criteria used to detect malnutrition
≥ 2/6 nutrition variables below the reference limit:
serum albumin (<38 g/L male, <37 g/L female),
prealbumin (<.18 g/L), transferrin (<1.7 g/L male, <1.5 g/L
female), body weight (<80% relative body weight), tricep
skinfold thickness (4 levels based on age), arm muscle
circumference (4 levels based on age).
Albumin < 2.5 g/dL or sustained ketonuria without
glycosuria > 2 weeks
≥ 3 nutrition variables below cut-off levels, including 1 of
each of the anthropometric, serum protein and skin test
measurements: weight (< 80% of reference value), tricep
skinfold (<6 mm male, <12 mm female), arm muscle
circumference (4 levels based on age and sex), delayed
hypersensitivity skin testing (< 10 mm induration), serum
albumin (<36 g/L), prealbumin (<.20 g/L male, <.18 g/L
female).
49% on admission to rehabilitation unit ≥ 2/6 nutrition variables below the reference limit:
(mean of 22 days post stroke) (n=49)
serum albumin (<35 g/L) , transferrin (<2.0 g/L), total
34% at 1 month (n=32)
lymphocyte count (<1800n/ mm3)
22% at 2 months (n=9)
body weight (<90% of reference weight, or <95% of usual
19% at follow up (2-4 months) (n=42)
weight, or body mass index < 20), sum of 4 skinfolds (< 5th
percentile of reference population), midarm muscle
circumference (< 5th percentile of reference population).
16.3% within 24 hrs of hospital
Serum albumin < 35 g/L or tricep skinfold or midarm
admission (n=104)
muscle circumference < 10th percentile of reference
population.
26.4% after 1 week (n=91)
35% after 2 weeks (n=43)
25% patients with ischemic stroke
62% patients with hemorrhagic stroke
Assessed in the acute period of stroke
13% control subjects
30% at admission to rehabilitation
(30±10 days post stroke) (n=150)
≥ 1 biochemical marker and ≥ 2 anthropometric markers
below the lower limits of the reference limits. (Lean body
mass, abdominal skinfold thickness, subscapular skinfold,
triceps skinfold, all < 80% of reference values, body mass
index < 20), total lymphocyte count < 1500/ mm3,
hemoglobin < 12 g/dL, serum albumin <3.5 g/dL.
Loss of weight ≥ 10% but with actual weight lower than
reference weight or loss of weight ≥ 5% plus one other
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Italy
Prospective
cohort
abnormal marker: arm muscle area < 5th percentile,
serum albumin < 35 g/L, Total lymphocyte count <1800n/
mm3.
Westergren et 8% within 24 hrs of symptom onset
al. (2001b)
(n=24)
Sweden
Prospective
29% at 1 month (n=24)
case series
33% at 3 months (n=24)
1 abnormal weight measurement and at least 1 other
abnormal marker: Body mass index < 20 or body weight, ≤
80% of reference weight or weight loss > 5% since
admission; Subnormal triceps skinfold or mid-upper arm
muscle circumference or serum albumin < 36 g/L.
Westergren et 32% within 6 days following hospital
al. (2001a)
admission (n=162)
Sweden
Prospective
case series
Author’s modified version of Subjective Global
Assessment:
A= Well nourished
B= Well-nourished but at risk of becoming malnourished
C= Suspected of being malnourished
D= Severely malnourished
SGA classes B or C or D =malnourished
Subjective Global Assessment:
A=Well nourished
B=Moderately (or suspected of being malnourished
C=Severely malnourished
B or C =malnourished
Clinical judgement used to determine if a patient was
undernourished, normal or overweight.
Davis et al.
(2004)
Australia
Prospective
case series
Dennis et al.
(2005a)
UK
7 (RCT)
16% within 24 hrs of symptom onset
(n=185)
Dennis et al.
(2005b)
UK
7 (RCT)
Martineau et
al. (2005)
Australia
Retrospective
audit
8.6% at acute hospital admission
Trial i) (n=859)
Trial ii) (n=321)
Hama et al.
(2005)
Japan
Prospective
cohort
22% within the first day of admission to Either serum albumin < 40 g/L or BMI < 19.
a rehabilitation hospital- an average of
44 days post stroke based on serum
albumin (n=51)
57% based on body mass index (BMI)
Crary et al.
(2006)
USA
Prospective
case series
26.3% at hospital admission(n=76)
Mini Nutritional Assessment score < 23.5.
Brynningsen
35% at one week post stroke(n=100)
≥2 abnormal values: serum albumin <550 mikromol/L,
7.8% within 7 days of symptom onset
(n=4,023)
(A more comprehensive assessment was carried out in
37% of patients)
Same as FOOD 2005 (I).
19.2% within 2 days of symptom onset
(n=73)
Patient Generated Subjective Global Assessment
Scoring identical to SGA.
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et al. (2007)
Denmark
Prospective
cohort
Poels et al.
(2006)
The
Netherlands
Prospective
cohort
33% at 5 weeks
20% at 3 months
22% at 6 months (n=89)
serum transferrin < 49 mikromol/L,
tricep skinfold <10th percentile, arm muscle
circumference < 10th percentile.
Primary criteria: 35% at admission to
rehabilitation (34 days post stroke)
(n=69)
3% at 4 weeks following admission
(n=60)
Primary: Unintentional weight loss of more than 5% in
one month or 10% in 6 months or Body Mass Index < 18
for subjects < 65 years or <22 for subjects ≥65years.
Yoo et al.
(2008)
South Korea
Prospective
cohort
12.2% within 24 hrs of symptom onset
(n=131)
Any single indicator below reference limits: Weight loss of
≥10% for the past 3 months or ≥ 6% during first week of
admission, weight index (actual weight in relation to
reference weight) <80%, serum albumin < 30 g/L, serum
transferrin < 1.5 g/L, serum prealbumin < 0.10 g/L.
Chai et al.
(2008)
USA
Crosssectional
Lim & Choue
(2010)
Korea
Prospective
cohort
8.2% of infirmary residents with a
history of stroke (n=61)
Serum albumin < 35 g/L or BMI < 18.5
19 (26%) well-nourished
36 (49.3%)moderately malnourished
18 (24.7%) severely malnourished
Patient-generated Subjective Global Assessment
Crary et al.
(2013)
USA
Prospective
cohort
Mosselman et
al. (2013)
Netherlands
Prospective
cohort
Secondary: the presence of at least one subnormal
primary or secondary outcome criteria: Serum albumin <
Secondary criteria: 73% at admission to 35 g/L, fat free mass ≤ 16 kg/m2 (men) or 15 kg/m2
rehabilitation
(women), tricep skinfold < 90% of 12.5 mm (men) or 16.5
54% at 4 weeks
mm (women), mid arm muscle circumference < 90% of
25.3 cm (men) or 23.3 cm (women).
19.8% at one week
Timing not stated, but assessments
took place following admission to
hospital an average of 60 days post
stroke.
32% of ischemic stroke patients were
identified as malnourished at
admission, 33% at day 7 following
hospitalization
73 patients assessed at admission to
hospital (between 2 and 5 days):
59 (81%) well nourished
10 (14%) at risk of malnutrition
4 (5%) malnourished
Serum prealbumin level of < 15 mg/dL
Mini Nutritional Assessment score <17 (malnourished),
17-23.5 (at risk of malnutrition), ≥24 (well nourished)
23 patients assessed at 9-12 days after
admission to hospital:
8 (35%) well nourished
9 (39%) at risk of malnutrition
6 (26%) malnourished
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Dysphagia
Eleven studies recruited patients both with and without dysphagia. Greater proportions of patients with
dysphagia were classified as malnourished compared with patients with normal swallowing function in
four trials: (19/59 vs.10/14, p=0.007) (Martineau et al. 2005); (16/24 vs. 15/67, p<0.001) (Davalos et al.
1996); (15/23 vs. 9/26, p=0.032) (Finestone et al. 1995); (4/5 vs. 17/56, p=0.044) (Chai et al. 2008).
Poels et al. (2006) also reported a greater proportion of subjects with dysphagia was malnourished,
although the result was not statistically significant (4/20 vs. 4/40, p= 0.233). Crary et al. (2006) did not
demonstrate a significant association between the dysphagia and malnutrition assessed within several
days of stroke (OR: 1.0; 95% confidence interval 0.4 to 2.8). In a subsequent study, this finding was
repeated. In addition, a relationship between dysphagia and dehydration was reported.
In a systematic review including the results from 8 studies, Foley et al. (2009) reported that the odds of
being malnourished were increased given the presence of dysphagia following stroke. However, they
also suggested that the relationship was not causal. While stroke size and location are the greatest
determinants of swallowing function, it is also true that the presence of dysphagia is itself an indicator
of greater stroke severity.
Stroke Type and Severity
The relationship between stroke severity and malnutrition was examined in three studies (Davis et al.
2004; Dennis et al. 2005a; Yoo et al. 2008). Increasing stroke severity was associated with baseline
malnutrition in one of these trials (Yoo et al. 2008). In all of these studies severity was assessed using the
National Institutes of Health Stroke Scale (NIHSS) and was examined during the first several days
following acute stroke. Only one study examined the relationship between stroke type and malnutrition
(Choi-Kwon et al. 1998). The prevalence of malnutrition reported in this study was much higher among
patients suffering from intracerebral hemorrhagic versus ischemic stroke; however, the authors
suggested that the result was likely attributable to differences in pre-existing malnutrition between
groups.
Variability of Assessment Criteria
With the single exception of the two related FOOD trials, no two studies used the same criteria. Serum
albumin and measures of weight were common to almost all of the studies. However, the cut-off points
used to distinguish well-nourished from malnourished patients were chosen arbitrarily, as were the
choice of reference populations and will potentially affect the degree and proportion of patients who
are considered to be malnourished. For instance, most studies used a cut-off point for serum albumin
level as 35 g/dL, (or using the American system 3.5 g/L) however, Hama et al. used a 40 g/L cut-off point
while DePippo et al. used a much lower point of 2.5 g/L (DePippo et al. 1994; Hama et al. 2005).
Foley et al. (2009b) conducted a systematic review of studies that had reported the prevalence of
malnutrition following stroke. Eighteen studies meeting inclusion criteria were identified. The reported
frequency of malnutrition ranged from 6.1% to 62%. Seventeen different methods of nutritional
assessment were used. Four trials used previously validated assessment methods; Subjective Global
Assessment (SGA), “an informal assessment”, and Mini Nutritional Assessment (MNA). The nutritional
assessment methods used in the remaining studies used had not been validated previously. The authors
suggested that the use of a wide assortment of nutritional assessment tools, most of them, previously
not validated contributed to the wide range of estimates of malnutrition.
The frequency with which both anthropometric and biochemical indicators were used in studies
reporting on malnutrition are presented in Table 16.3.
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Table 16.3. Individual Nutrition Markers Used in the Reviewed Studies
Study
Axelsson 1988
DePippo 1994
Unosson 1994
Finestone 1995
Davaolos 1996
Choi-Kwon 1998
Aquilani 1999
Hama 2005
Poels 2006
Brynningsen 2007
Yoo 2008
Chai et al. 2008
Crary et al. 2012
Study
Axelsson 1988
DePippo 1994
Unosson 1994
Finestone 1995
Davaolos 1996
Choi-Kwon 1998
Aquilani 1999
Hama et al. 2005
Poels 2006
Brynningsen 2007
Yoo 2008
Chai et al. 2008
Albumin
X
X
X
X
X
X
X
X
X
X
X
X
Biochemical Markers
Transferrin
*TLC
X
Prealbumin
X
Ketonuria
X
X
X
X
X
X
X
X
X
X
X
Weight
X
X
X
X
X
X
X
Anthropometric Markers
Fat (TSF, SS)
X
Muscle (AMC, MAMC)
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Composite Clinical Assessments
Westergren et al. 2001a), FOOD I & II (2005), Martineau et al. 2005, Crary et al. 2006, Lim et al. 2010, Mosselman
et al. 2013
* total lymphocyte count
There was variability in the percentiles chosen for anthropometric cut-off points, if they were even
identified. Choi-Kwon et al. (1998) used an undefined reference population, while Unosson et al.
appeared to choose specific, age-dependent cut-off points that were unreferenced and did not appear
to be based on population norms per se (Unosson et al. 1994). Finestone et al., Davalos et al., and
Axelsson et al. all used population-based national survey results as their reference standards (Axelsson
et al. 1988; Davalos et al. 1996; Finestone et al. 1995). However, there was no consistency in choosing
cut-off values; some studies used the 5th percentile (Finestone et al. 1995), while another used the 10th
(Elmstahl et al. 1999). Axelsson et al. and Choi-Kwon et al. (1998) simply made reference to “low
values” when they defined their cut-off threshold (Axelsson et al. 1988). Implicit in the assessment of
malnutrition is that thin people, relative to the rest of the reference population, are malnourished.
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Figure 16.1 Prevalence of Malnutrition Following Stroke
The prevalence of malnutrition post stroke can vary widely depending on the criteria used to define it and
the point at which it is measured. Among the studies represented below, the number of values, which fell
below normal reference ranges, varied from 1 to 3 and the total number of parameters assessed ranged
from 2 to 9. In some cases the reference criterion was grouped according to age or sex, while in other
studies, single cut-off values were used.
50
% Malnutrition
40
30
20
10
20
03
88
D
O
FO
ss
on
19
19
96
A
xe
l
s
D
av
al
o
U
no
ss
on
19
94
19
95
e
Fi
ne
st
on
N
ys
w
on
g
er
1
99
2
0
Timing of Assessment
The timing of the assessment could have also explained the variability of the prevalence rates of
reported malnutrition. Among the 13 studies that assessed nutritional status within one-week of stroke
the frequency of malnutrition was < 20% in 9 of the studies (Axelsson et al. 1988; Davalos et al. 1996;
Davis et al. 2004; Dennis et al. 2006; Dennis et al. 2005a, 2005b; Martineau et al. 2005; Unosson et al.
1994; Westergren et al. 2001b; Yoo et al. 2008). Frequency of malnutrition was 26% at 10 days after
admission to hospital in one study (Mosselman et al. 2013). Among the 7 trials that assessed nutritional
state between 22 and 44 days following stroke, at admission to rehabilitation the frequency of
malnutrition ranged from 30% to 49% in four trials (Aquilani et al. 1999; Finestone et al. 1995; Hama et
al. 2005; Poels et al. 2006).
Conclusions Regarding the Incidence of Malnutrition
The incidence of malnutrition varies from 6% to 62% post stroke, depending on the timing of
assessment and the criteria used to define malnutrition.
There is no “gold standard” for the assessment of nutritional status.
Malnutrition is a relatively common problem post stroke.
16.3 Factors Associated With the Development of Malnutrition
Malnutrition in any disease state develops over a period of time as a result of either increased
metabolism/catabolism or inadequate nutritional intake. There may be occasions when these two
factors are superimposed. The development of malnutrition may also be hastened if the
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gastrointestinal tract is compromised and nutrient absorption is impaired. The evidence with respect to
the potential contributions of these mechanisms is reviewed.
16.3.1 Hypermetabolism Following Stroke
Hypermetabolism has been defined as an increase in metabolic rate above that which is predicted using
equations accounting for age, sex, height and weight (Souba & Wilmore 1999). Elevated metabolic rates
of 140-200% above predicted values have been well described for some disease states including burns,
sepsis (Long 1984) and head injury (Young et al. 1992) and are reflective of increased oxygen
consumption associated with injury severity. It appears that stroke results in similar metabolic
perturbations, although the effect may not be as pronounced. Although 5 studies have examined the
metabolic rate following “stroke”, collectively, the results are difficult to interpret. Patients with severe
stroke (including infarct, SAH and intracerebral hemorrhage) who were mechanically ventilated, some of
whom were sedated, were included in three of the studies. The percentage increase above predicted
levels was reported in only 1 of these studies. Only two studies have been conducted to measure the
resting energy expenditure of non-ventilated patients following uncomplicated stroke. In these studies
metabolic rate was measured at a point beyond 7 days, in a non-ICU setting. Evidence from these 2
studies suggests that stroke patients are mildly hypermetabolic and are not at an increased risk for the
development of malnutrition due to the effects of hypermetabolism (see Table 16.4).
Table 16.4 Studies Examining Resting Energy Expenditure Post Stroke
Author/Year/
Country
Weekes and Elia
(1992)
UK
No Score
Finestone et al. (2003)
Canada
No Score
Methods
Outcome
Resting energy expenditure of 15 patients
was measured 24-72 hrs post stroke.
Measurements were repeated in 11 of the
patients 10-14 days later.
Resting energy expenditure (REE) of 91
stoke patients were measured at admission
to hospital, and on days 7, 11, 14, 21 and
90. Comparisons were made with 10
healthy volunteers of similar ages.
Bardutzky et al. (2004) The metabolic rates of 34 sedated and
Germany
mechanically ventilated patients with
No Score
severe stroke were measured during the
first 5 days of injury. The metabolic rates of
patients with spontaneous ICH (n=13) and
MCA infarction (n=21) were compared.
Esper et al. (2006)
USA
No Score
Frankenfield and
Ashcraft (2012)
USA
No Score
No evidence of hypermetabolism at either of the
study points. Metabolic rate was 107% of
predicted values. No significant differences
between the first or second measurement.
The mean REE of stroke patients ranged from
1521-1663 Kcals/day. This represented 107114% of the predicted expenditure, estimated by
the Harris-Benedict equation. The REE of
controls was similar to that of stroke patients.
Over the study period the metabolic rates of
patients with ICH varied from 1,570- 1,623
kcals/day, compared with 1,560 and 1610
kcals/day for patients with infarction. The
differences were not statistically significant. All
measurements correlated strongly with
estimated REE using the Harris-Benedict
equation.
The resting metabolic rates of 14
No patient was pharmacologically paralyzed.
mechanically ventilated patients with non- Median REE was 1810 (1124-2806) and 2238
traumatic intracerebral (ICH),
(1860-2780) kcal/d for the non-traumatic group
intraventricular (IVH) or subarachnoid
and TBI group, respectively. The increase above
hemorrhage (SAH) were compared with 6
predicted values using the Harris-Benedict
patients with traumatic brain injury (TBI),
equation was 126% (non-traumatic) and 147%
retrospectively. Indirect calorimetry was
(TBI). The differences between groups were not
conducted within 7 days of injury/ ictus.
statistically significantly.
Indirect calorimetry was conducted
Compared with other groups, patients with IS
prospectively in 130 mechanically
had significantly lower metabolic rates: (1,879
ventilated patients within the first 6 days of kcal/d vs. 2,047 (HS) vs. 2,099 (ITBI) vs. 2,127
admission to a critical care unit owing to
(TBI+). Using the Penn State prediction equation,
16. Nutritional Interventions Following Stroke
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ischemic stroke (IS), hemorrhagic stroke
(HS), isolated traumatic brain injury (ITBI),
or traumatic brain injury with collateral
injuries (TBI+).
patients with IS had metabolic rates >15% of
predicted values in 60% of cases, compared with
74% to 86% of the other 3 types of injury.
However, all of the differences in metabolic rates
were eliminated after controlling for maximum
body temperature and minute ventilation.
Conclusion Regarding Hypermetabolism Post Stroke
There is an elevation in metabolic rate following stroke that ranges from 107% above predicted
levels to 126%.
There is conflicting evidence that metabolic rate is elevated more in hemorrhagic stroke compared
with ischemic stroke.
Patients are not hypermetabolic acutely following stroke.
16.3.2 Increased Catabolism Following Stroke
Increases in both metabolic rate and catabolism post-injury have been attributed to the effects of the
acute phase response, mediated largely through the effects of cytokines and counter-regulatory
hormones, following injury or disease (Staal-van den Brekel et al. 1995; Young et al. 1985). Elevations of
peripheral plasma catecholamines, cortisol, glucagons, IL-6, IL-1RA and acute phase proteins have been
well described following stroke (Beamer et al. 1995; Fassbender et al. 1994a; Fassbender et al. 1994b;
Ferrarese et al. 1999; Muir et al. 1999; Murros et al. 1993; Syrjanen et al. 1989) (see Table 16.5).
Prolonged elevations of these compounds may lead to the depletion of lean body mass (muscle) and fat,
which may contribute to the development of malnutrition.
Table 16.5 Studies Reporting Elevations of Acute Phase Reactants Following Stroke
Author/Year
Country
Syrjanen et al. 1989
Finland
“n”
Time Studied Post Stroke
Indicator/Response
50
Within 72 hrs
Murros et al. 1993
Finland
Fassbender et al.
1994 (a)
Germany
Fassbender et al.
1994 (b)
Germany
105 (ischemic stroke)
3 days and 1 week
23 (ischemic stroke)
Up to 7 days
ACTH (-)
Cortisol ( until day 5)
19 (ischemic stroke)
Up to 3 days
Beamer et al. 1995
USA
50
2-6 days
Ferrarese et al. 1999
Italy
40
Days 1-90
IL-1ß ()
IL-6 ()
TNF ()
IL-1RA ()
IL-6 ()
CRP (-)
Fibrinogen ()
IL-6 ( days 1-30)
TNF ( days 1-90)
Muir et al. 1999
228
Within 72 hrs
16. Nutritional Interventions Following Stroke
CRP ()
SAA ()
ACT ()
Cortisol ()
CRP ()
pg. 13 of 37
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Scotland
CRP (C-reactive protein)
SAA (serum amyloid A protein)
ACT ( α-antichymotrypsin)
ACTH (adrenocorticotropic hormone)
TNF (tumor necrosis factor)
IL-1ß (Interleukin-1ß)
IL-6 (Interleukin-6)
IL-1RA (Interleukin-1 receptor antagonist)
(-) indicates no change
Conclusions Regarding an Acute Phase Response Following Stroke
Although there is evidence that an acute phase response accompanies stroke, its contribution to the
development of malnutrition remains unclear.
16.3.3 Gastrointestinal Function Following Stroke
The major effect on the gastrointestinal tract following stroke is impairment of oral, pharyngeal and
esophageal functions, manifested as dysphagia (see Chapter 15. Dysphagia and Aspiration). Dysphagia
may resolve spontaneously in the days following stroke or persist for many months, even years.
For a minority of patients severe dysphagia will preclude safe oral feeding and alternative strategies will
be required. The association between dysphagia and malnutrition was examined in three studies. The
results are presented in Figure 16.2. The odds of developing malnutrition increased significantly
following acute hospital admission at both one week following stroke and upon admission to an
inpatient rehabilitation unit (approximately 3 weeks post stroke). Although the mechanism was not
explored, decreased intake or delayed enteral feeding may have contributed to declines in nutritional
status. At admission to hospital, shortly following stroke onset nutritional status was unrelated to the
presence of dysphagia (Crary et al. 2006; Crary et al. 2013; Davalos et al. 1996). Crary et al. did report a
relationship between the presence of dysphagia and dehydration at both hospital admission and at day
7 following stroke (Crary et al. 2013).
Other significant gastrointestinal impairments have not been reported. Although stroke patients do not
appear to be at increased risk for stress ulcer formation or gastric bleeding (Ullman & Reding 1996),
anticoagulation therapy may increase the risk. Gastric motility could be theoretically altered, since it is
modulated through the central nervous system. However, there is no evidence to suggest that this is
the case. Although constipation is a frequently cited complaint following stroke, this is thought to be
due to a variety of factors, arising secondary to stroke, including reduced mobility, decreased fluid
intake and medication usage. Stroke per se is not known to cause constipation (Johanson et al. 1992;
Sonnenberg et al. 1994). There is no evidence to suggest that nutrient absorption is impaired following
a stroke.
Conclusions Regarding the Alteration of Gastrointestinal Function Following Stroke
There is an absence of literature to confirm or refute whether the significant gastrointestinal
impairments develop following stroke.
Figure 16.2 The Association Between Dysphagia and the Development of Malnutrition
16. Nutritional Interventions Following Stroke
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16.3.4 Nutrient Intake Following Stroke
Stroke patients may be particularly vulnerable to protein-energy malnutrition due to a variety of factors
that affect their willingness or ability to self-feed, such as loss of appetite associated with depression,
cognitive deficits, dysphagia (difficulty swallowing), visual neglect, upper extremity paresis, and apraxia
(an inability to use objects correctly) (Finestone et al. 2003). However, few studies exist that describe
the energy and protein intakes of hospitalized stroke patients. Gariballa et al. reported that the average
two-week energy intake of stroke patients who did not have swallowing difficulty following stroke and
who consumed a regular hospital diet was 1338 kilocalories (Kcals) representing 74 percent of their
predicted requirement (Gariballa 2001). This level of adequacy was not significantly different from 42
age- and sex-matched nonstroke patients who consumed 1317 Kcals, or 73 percent of requirement,
suggesting that the intakes of stroke patients were similar to those of other hospitalized patients. The
only other study which examined protein and energy intakes following stroke reported that, on average,
regardless of diet type (oral or non-oral) and texture (regular diet or texture-modified because of
swallowing impairment), hospitalized patients consumed an average of 85 percent of their energy
requirements, and 86 percent of protein requirements, during the first 21 days following stroke (Foley et
al. 2006).
Conclusions Regarding Nutrient Intake Following Stroke
Stroke patients consume between 74 and 86% of their energy and protein requirements during the
first several weeks following stroke.
Patients consume fewer calories and protein following stroke.
16.3.5 Stroke-Related Factors
A variety of stroke-related deficits may impair the patients’ ability to self-feed. Some of these factors
include upper extremity paresis, apraxia, visual and cognitive, perceptual deficits such as visual neglect.
Voluntary reduced food intake may also result from depression associated with stroke.
16.4 Nutritional Interventions Following Stroke
16. Nutritional Interventions Following Stroke
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Nutrition interventions associated with stroke are usually directed at the improvement of nutrient
intakes through i) oral supplementation, ii) enteral feeding or iii) dysphagia therapy. The goal of all
nutritional interventions is the prevention or correction of “malnutrition”.
16.4.1 Enteral Feeding
Enteral feeding may represent a sole or supplemental source of feeding. Generally, enteral nutrition as
the sole source of nutrient intake is reserved for dysphagic patients for whom oral feeding is considered
unsafe. However, “failure to thrive” non-dysphagic stroke patients may also be candidates for enteral
feeding in the presence of prolonged and inadequate oral intake. The use of feeding tubes in these
stroke patients has been shown to reverse malnutrition (Finestone et al. 1995). Therefore, the use of
feeding tubes can prevent or reverse the effects of malnutrition in patients who are unable to safely eat
and those who may be unwilling to eat. Data from the Post-Stroke Rehabilitation Outcomes Project
(James et al. 2005), which retrospectively studied the outcomes of 919 patients from six inpatient
rehabilitation sites, provides evidence that tube feeding is an effective intervention. Patients with both
moderate and severe stroke who had received tube feeding during hospital stay but who were not
discharged with a feeding tube in place achieved greater increases in total FIM gains and experienced
greater improvement in severity of illness by discharge. Among 143 patients admitted to an inpatient
rehabilitation facility with an enteral feeding tube in place due to dysphagia, 20% were able to have
their tubes removed prior to discharge, having resumed full oral intake (Krieger et al. 2010). Sixty-five
percent were able to return to some type of oral feeding prior to discharge. Patients who were able to
have their FT removed were more likely to be discharged to home. Nakajima et al. reported that of a
cohort of 4,972 consecutively admitted ischemic stroke patients, 723 (14.5%) could not eat orally on day
10 post stroke (Nakajima et al. 2012). Of the 512 dysphagic patients who responded to a questionnaire
at 3 months, 141 (27%) had resumed oral intake. An NIHSS score of ≤17 on day 10 was the strongest
predictor or ability to eat orally at 3 months. NIHSS scores as well as the presence of bihemisperic
lesions were found to be the most predictive factors for PEG placement among a group of 77 stroke
patients following severe stroke (Kumar et al. 2012).
Many feeding tube types and procedures are available. In cases where enteral tube feedings are
indicated, this can be achieved through either a temporary or permanent access. A nasogastric (NG)
feeding tube is often placed in patients who are expected to return to a full oral diet within one month.
There is consensus opinion that permanent feeding access is indicated when a prolonged period of nonoral intake (>1 month) is anticipated (Committee 1995). Examples of available techniques include
percutaneous gastrostomy/jejunostomy (endoscopically or radiologically inserted), percutaneous
gastrojejunostomy (endoscopically or radiologically inserted) and surgically placed gastrostomy/
jejunostomy. In Canada, a greater percentage of feeding tubes are placed by radiologists compared to
gastroenterologists. The differences may be due to issues of financial remuneration, availability of
facilities and technical expertise. Surgically placed feeding tubes are uncommon in the stroke patient
population. Controversy continues as to whether placement of the feeding tube into the small bowel
reduces the risk of aspiration (see Chapter 15. Dysphagia and Aspiration). Therefore, placement of
feeding tubes into the stomach and the small bowel are both commonly employed in dysphagic stroke
patients.
Table 16.6 Efficacy of Enteral Feeding Post Stroke
Author, Year
Country
PEDro Score
Park et al.
(1992)
Methods
Outcomes
40 patients (18 with stroke) with long-standing
dysphagia randomized to receive either a
16. Nutritional Interventions Following Stroke
Treatment failure, including blocked and
dislodged tubes occurred in 18/19 patients in
pg. 16 of 37
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Scotland
6 (RCT)
percutaneous endoscopic gastrojejunostomy (PEG) NG group compared to 0/19 in PEG group.
or a nasogastric tube (NG) for 28 days of enteral
Patients in NG group received significantly
feeding.
less volume of feed compared to PEG group
(55% vs. 93%).
Norton et al.
30 dysphagic patients were randomized to receive At 6 weeks, a significantly greater proportion
(1996)
either a gastrostomy (G) feeding tube or
of patients had died in the NG group
UK
nasogastric (NG) feeding tube for enteral feeding at compared to patients in the G group (2 vs 8).
6 (RCT)
14 days post stroke.
Patients in the G group had better nutritional
indices including weight, serum albumin, midarm circumference. There were no omitted
feeds among patients in the G group
compared to at least one missed feed in 10
patients in the NG group.
Nyswonger and The charts of 52 stroke patients admitted between Patients who had been enterally fed within 72
Helmchen
1988 and 1991 who received enteral nutrition as
hours of admission had significantly shorter
(1992)
inpatients were reviewed. Patients were grouped
hospital length of stay compared to those
USA
according to lag in feeding time from admission to who were fed > 72 hours of admission (20.14
No Score
tube insertion (< or > 72 hours).
± 13 vs. 29.76 ± 20days, p<0.05)
Dennis et al.
(2005a)
UK
8 (RCT)
Dennis et al.
(2005b)
UK
8 (RCT)
Hamidon et al.
(2006)
Malaysia
6 (RCT)
This study was one branch of a RCT evaluating 3
distinct nutritional interventions. 859 acute stroke
patients with dysphagia were randomized to
receive early enteral feeding vs. delayed. The
outcome of death or disability was evaluated at 6
months.
This study was one branch of a RCT evaluating 3
distinct nutritional interventions. 321 acute stroke
patients with dysphagia were randomized to
receive a nasogastric (NG) tube or a percutaneous
endoscopic gastrostomy (PEG) tube for enteral
feeding. The outcome of death or disability was
evaluated at 6 months.
23 consecutive inpatients admitted with acute
ischemic stroke were randomized to receive either
an NG or PEG feeding tube. At baseline and 4
weeks follow-up the following assessments were
conducted: tricep skinfold (TSF), bicep skinfold
(BSF),
mid-arm circumference (MAC), serum albumin,
treatment failure, defined as persistent blocked or
dislodged tubes.
Early tube feeding was associated with an
absolute reduction in risk of death of 5.8%
(95% CI -0.8 to 12.5, p=0.09) and a reduction
in death or poor outcome of 1.2% (-4.2 to 6.6,
p=0.7)
In the PEG versus nasogastric tube trial, 321
patients were enrolled by 47 hospitals in 11
countries. PEG feeding was associated with
an absolute increase in risk of death of 1.0% (10.0 to 11.9, p=0.9) and an increased risk of
death or poor outcome of 7.8% (0.0 to 15.5,
p=0.05).
At the end of four weeks, subjects in the PEG
group had significant increase in the median
serum albumin values compared with
baseline, whereas subjects in the NG group
experienced a decrease (+2.5 vs. -5.0 g/L,
p=0.045). There were more treatment failures
in the NG group (5/10 vs. 0/8, p=0.036).
There were no other significant differences
between groups.
There have been only four RCTs that have addressed the issue of enteral feeding in stroke patients. All
of these trials examined the differences in outcomes of patients with two different types of feeding
tubes-PEG vs. NG tubes. Park et al. randomized a neurologically heterogeneous group of 40 dysphagic
patients (45% with stroke) to receive either a percutaneous endoscopic gastrostomy (PEG) or
nasogastric (NG) tube for 4 weeks of enteral feeding (Park et al. 1992). There was a higher number of
treatment failures associated with the NG tube group while patients in the PEG group received
significantly greater proportion of their prescribed feeds. Hamidon et al. also reported a higher number
of treatment failures in patients fed using NG tubes (Hamidon et al. 2006). The same authors also
reported a significant difference in serum albumin values, favouring the PEG group; however there was
16. Nutritional Interventions Following Stroke
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a difference in the baseline values, suggesting the possibility of a biased treatment effect (PEG group:
37.0 g/l, NG group 37.0 g/l).
A study by Norton et al. randomized 30 stroke patients to receive either a gastrostomy tube or NG tube
for enteral feeding (Norton et al. 1996). A significantly greater number of patients in the NG group had
died at six weeks. The authors concluded that based on the results of this study that PEG tubes were
the preferred method of feeding stroke patients unable to eat orally. However, this finding suggests an
imbalance in the prognostic profiles at entry. Although patients were randomly assigned to the two
treatment groups and had similar Barthel Index score (<3 for both groups), there may have been other
important differences between groups. Several factors suggest that these two groups may had been
clinically quite different: 1) half of the patients who died in the NG group died of complications
attributed to the original stroke suggesting that these patients had more severe strokes, 2) none of the
patients in the NG group recovered their swallowing function by the end of follow-up, whereas all of the
patients in the gastrostomy fed group had their feeding tubes removed and resumed normal oral intake,
3) at six weeks, none of the patients in the NG group had been discharged, compared to all of the
patients in the gastrostomy fed group (who were discharged to nursing homes, 4) there are known floor
and ceiling effects associated with the Barthel Index, which would not be sensitive enough to capture
even clinically significant differences in impairment status and 5) the Barthel Index was used as a proxy
for stroke severity.
More recently Dennis et al. randomized a large number of patients to receive either a NG or PEG type
feeding tube (Dennis et al. 2005a). Large sample sizes, strong methodology, clinically relevant outcomes
and nearly complete follow-up set this inter-related family of trials apart from its predecessors. The
results did not support the purported benefits of PEG tubes reported from previous studies. In fact, a
greater proportion of patients fed with a PEG feeding tube were either dead or dependent at 6 months.
The result approached statistical significance (p=0.05). However, the volume of tube feed formula that
patients received over the study period in the FOOD trial was not reported and, potentially, it may not
have been comparable between the groups. Although the reason for the negative result is unclear, the
authors speculate that differences in nursing interventions may be contributory. Within the same trial,
a delay (>7 days) in initiating enteral feeding was not statistically associated with a worse outcome,
compared to early feeding within 72 hours of admission.
While mortality risk was assessed in four studies, results could be estimated in two (Dennis et al. 2005a;
Norton et al. 1996). The results from the FOOD trial heavily influenced the results of the pooled analysis.
There was no increased risk of either mortality or poor outcome associated with feeding tube type (NG
vs. PEG). Figure 16.3
Conclusions Regarding the Use of Enteric Feeding Tubes
Based on the results of two RCTs of good quality, there is strong (Level 1a) evidence that intragastric
feeding is associated with fewer mechanical complications compared to nasogastric feeding for
stroke patients who require long term (>28 days) non-oral feeding.
Based on the results from a single RCT, in which the results approached statistical significance, there
is moderate (Level 1b) evidence that type of feeding tube (NG vs. PEG) is unrelated to death and
dependency at 6 months.
Intragastric feeding tubes are associated with fewer complications compared with naso-enteric
tubes when patients require nutritional support for at least 28 days.
Figure 16.3 Outcomes Evaluating NG vs. PEG Feeding Routes
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16.4.2 Oral Supplementation
Oral supplementation may be indicated for patients who are safe with oral intake, but who fail to take in
sufficient quantities to meet their nutritional requirements and/or for patients with pre-existing
nutritional deficits. Theoretically, oral supplementation could be effectively used to improve nutritional
intake, which would in turn lead to improvements in nutritional parameters and ultimately functional
outcome. In a review focusing on the treatment of protein-energy malnutrition in chronic nonmalignant disorders, Akner and Cederholm identified three RCTs that included treatment for both
dysphagic and non-dysphagic stroke patients (Akner & Cederholm 2001; DePippo et al. 1994; Gariballa
et al. 1998b; Norton et al. 1996). Four “uncontrolled trials” were also identified (Davalos et al. 1996;
Elmstahl et al. 1999; Nyswonger & Helmchen 1992; Wanklyn et al. 1995). These authors concluded that
the treatment efficacy of protein energy malnutrition treatments could not be measured due to a
“striking lack of published articles”.
Table 16.7 Efficacy of Oral Supplementation Post Stroke
Author, Year
Country
PEDro Score
Gariballa et al.
(1998b)
UK
6 (RCT)
Dennis et al.
(2005b)
UK
8 (RCT)
Aquilani et al.
Methods
Outcomes
42 malnourished stroke patients were randomized
to receive a standard hospital diet or a standard
diet plus an oral supplement supplying an
additional 1200Kcals, 40g protein daily for 4 weeks.
Energy and protein intakes were higher in the
supplemented group (1807 vs. 1084 kcals,
65.1 vs. 44.1 g protein). Patients in the
supplemented group experienced less of a
decline in serum albumin (–1.5 vs. -4.4g/L)
and an improvement in serum iron levels (2.6
vs. –2.7 mol/L) compared to patients in the
unsupplemented group.
8% of patients were judged to be
undernourished at baseline. Supplemented
diet was associated with an absolute
reduction in risk of death of 0.7% (95% CI 1.4 to 2.7) and an increased risk of death or
poor outcome of 0.7% (-2.3 to 3.8). The result
was compatible with a 1% or 2% absolute
benefit or harm from oral supplements.
The mean MMSE scores before and after
This study was one branch of a RCT evaluating 3
distinct nutritional interventions. 4,023 acute
stroke patients without dysphagia were
randomized to receive an oral nutritional
supplement (540 Kcals) in addition to a hospital
diet, provided for the duration of their entire
hospital stay. The outcome of death or disability
was evaluated at 6 months.
48 patients with subacute stroke (14 days or more
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(2008a)a
Italy
6 (RCT)
Aquilani et al.
(2008b)b
Italy
6 (RCT)
Rabadi et al.
(2008)
USA
9 (RCT)
Ha et al.
(2010b)
Norway
5 (RCT)
from onset) admitted for inpatient rehabilitation
were randomized to receive daily supplementation
providing an additional 250 kcal + 20 g protein or to
regular diet alone for 21 days. The primary
outcome measure was the Mini-Mental State
Examination (MMSE) assessed before and after
treatment.
42 patients admitted for inpatient rehabilitation an
average of 16 days following acute stroke were
randomly allocated to receive 21 days of protein
supplementation (n=21) or regular diet (n=21) in
order to investigate the recovery of neurological
changes, measured using the National Institute of
Health Stroke Scale (NIHSS).
102 stroke patients admitted for inpatient
rehabilitation within 4 weeks of onset and who had
lost 2.5% of their pre-stroke weight during the
acute admission period were randomized to
receive a either a regular supplement (381 Kcals,
15 g protein) or intensive supplement (720 Kcals,
33 g protein) daily throughout their hospital stay.
The primary outcome was FIM, assessed before
and after treatment. The secondary outcome
measurements included the FIM motor and
cognitive subscores, length of stay (taken from day
of admission), 2-minute and 6-minute timed walk
tests measured at admission and on discharge, and
discharge disposition (home/not home).
Acute stroke patients (malnourished or at
nutritional risk) were randomized to receive either
individualized, nutritional care to prevent weight
loss (n=58) or routine care (n=66) while in hospital.
Primary outcome measure was the percentage of
patients with weight loss >/=5% at 3 months.
Secondary outcomes measures were quality of life
(QoL), handgrip strength and length of hospital
stay.
Ha et al. (2010a) Additional analyses from 2010a) study assessing
Norway
body composition.
5 (RCT)
treatment for were: experimental group 16.4
to 20.3 and control group 18.4 to 19.2. The
difference between groups was not
significant. The difference between groups
when using the log transformed values of the
MMSE were statistically significant.
At the end of the study period, the mean
NIHSS scores had improved significantly more
for patients in the supplemented group (-4.4
+/- 1.5 score versus -3 +/- 1.4 of control
group; P<0.01).
Patients receiving intensive nutritional
supplementation improved more than those
on standard nutritional supplements on
measures of motor function (total FIM, FIM
motor subscore, 2-minute and 6-minute
timed walk tests, all significant at p < 0.002).
The difference in FIM change scores was 31.5
(intensive group) vs. 22.9 (regular group).
They did not, however, improve on measures
of cognition (FIM cognition score). A higher
proportion of patients who received the
intensive nutritional supplementation went
home compared to those on standard
supplementation (43% vs. 63%, p = 0.05).
During hospitalization, patients in the
intervention group consumed significantly
more energy, but not protein, compared with
patients in the control group. At 3 months,
20.7% of the patients in the intervention
group had lost ≥5% weight compared with
36.4% of patients in the control (p=0.055).
Patients in the intervention group had a
significantly higher QoL scores (P = 0.009) and
greater handgrip strength (P = 0.002). Length
of hospital stays were similar between groups
(median of 12 vs. 13 days).
At 3 months, men and women in both groups
had experienced weight loss. Whereas there
were no differences in any of the body
composition outcomes between the groups in
men (weight, BMI, MAUC, TSF or AMC),
women in the intervention group lost less
weight (P = 0.022) and fat (P = 0.005)
compared with the controls.
Dennis et al. (2005) routinely randomized all non-dysphagic patients, regardless of their nutritional
status to receive a daily oral supplement, which contained 2,257 kJ (or 540 Kcals/day) and 22.5 g protein
until discharge, in addition to a regular diet, or to regular diet alone (Dennis et al. 2005b). There were no
differences in the proportion of patients who were dead or dead/disabled (defined as a Modified Rankin
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Score of 3-5) at six months. The percentage of patients in each group who had experienced death or
poor outcome was identical between groups (59%). The odds of death or poor outcome were reduced
for the 8% of undernourished patients (presumably patients who would benefit the most from
treatment) receiving supplementation, although the results did not reach statistical significance.
Theoretically, oral supplementation should increase the likelihood that patients will consume sufficient
energy and protein to meet their actual requirements. However, both under-feeding and over-feeding
can still result and neither condition would be expected to improve outcome. No indication of actual
nutrient intake or its relationship to estimated nutrient requirement is provided, although the authors
do note this as a limitation of the study.
Gariballa et al. (1998b) selectively randomized only patients considered to be malnourished to receive
an oral supplement in addition to regular diet, or to regular diet alone (Gariballa et al. 1998b). Although
they reported significant changes in two nutritional parameters at follow-up, albumin and iron, there
were no differences between the groups in terms of non-nutrition outcome measures including Barthel
Index scores, infective complications and length of hospital stay and mortality (see Figures 16.4). There
may be several reasons for the null result. The length of the intervention period could have affected the
magnitude of the observed effect sizes. Perhaps a longer period of study is required to fully elucidate
the effects of poor intake on function. Given that malnutrition is a condition that develops over time, it
is unclear how long poor intake needs to continue before declines of nutritional markers will be
manifested as increased morbidity and mortality and declines of functional outcomes. The Barthel Index
may not be a sensitive enough measure to capture clinically significant changes in functional outcome.
Patients in this study were considered to be malnourished if both tricep skinfold measurements (TSF)
and midarm circumference (MAC) were 1 SD of reference norms. While these criteria would definitely
favour the identification of slim individuals as malnourished, it may not necessarily have selected only
those who were truly malnourished. Nutritional supplementation may fail to improve outcome
indicators or markers of nutritional status in well-nourished individuals.
Aquilani et al. (2008a) examined the potential benefit of oral supplementation to enhance cognitive
recovery following stroke (Aquilani et al. 2008a). The authors hypothesized that, among other
mechanisms, the additional supply of amino acids could help to re-activate the synthesis of neural
proteins, thereby increasing neuron energy and neurotransmitter function. Although the authors stated
that the treatment was successful as demonstrated by a significantly greater improvement in MMSE
scores over the study period, it should be noted that the MMSE is a screening tool and was never
intended to be used to assess responsiveness to treatment. Furthermore, there were statistically
significant differences in the baseline MMSE scores between treatment and control groups, which were
not adjusted for in their analysis. In a related study Aquilani et al. demonstrated that 3 weeks of a
protein-supplemented diet resulted in greater neurological recover, measured by the NIHSS scale
(Aquilani et al. 2008b). The authors suggested that increased protein synthesis could “induce axonal
sprouting and formation of new cortical connections” in both perilesionsal and remote areas of the
brain and may also improve training-induced plasticity.
Rabadi et al. (2008) randomized stroke patients who they determined to have experienced significant
weight loss over a 2-week period to receive either routine of intensive oral supplementation for the
duration of their hospital stay (Rabadi et al. 2008). Although the authors reported that there were
significantly greater improvements in FIM scores experienced by the intensive group, the generalizability
of their findings is questionable. Stroke severity was measured using the MMSE, not by a scale designed
to measure severity. Therefore, potential baseline differences between groups remain unknown. Also,
while the volumes, protein, energy content and compliance with supplement use is reported, the
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authors provide no data on actual caloric intake over the study period. There were no significant
changes in nutritional indicators (weight, serum albumin, pre-albumin or transferin) between groups.
Ha et al. (2010a) examined whether an individualized nutritional program including oral sip
supplementation during hospitalization in the acute stage of stroke could prevent or minimize weight
loss at 3 months (Ha et al. 2010a). Although there was no statistically significance difference in the
proportion of patients who lost 5% of more of their weight, the authors thought that the mere
completion of diet records for patients in the control group increased aware of, and attention to,
adequacy of energy intake. In a separate analysis excluding the 38 control group patients for whom
dietary records had been kept, revealed a significantly lower proportion of patients in the intervention
group who had dropped 5% of body weight (20.7% vs. 42.9%, p=0.032). Woman appeared to benefit
preferentially from the treatment and experienced less weight loss and reductions in fat stores
compared with men (Ha et al. 2010b).
The pooled outcomes of mortality and death/poor outcome associated with oral supplementation are
presented in Figure 16.4. There was no protective effect association with supplementation on either
outcome.
Figure 16.4. The Effectiveness of Oral Supplementation
Conclusions Regarding Oral Supplementation
There is conflicting (Level 4) evidence that oral sip supplementation improves functional outcomes in
stroke patients.
Based on the results from a single RCT, there is moderate (Level 1b) evidence that routine oral sip
supplementation does not reduce the incidence of death or dependency following stroke.
There is moderate (Level 1b) evidence that oral supplementation improves the energy and protein
intakes of stroke patients.
There is moderate (Level 1b) evidence that oral supplementation improves the nutritional
parameters of stroke patients.
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Oral supplementation improves energy and protein intake although it may not necessarily improve
functional outcomes.
16.4.3 Dysphagia Treatment
Several studies have examined the use of dysphagia treatment programs to improve the nutritional
status of patients post stroke. The results from these trials can be used to inform treatment decisions.
Table 16.8 Efficacy of Dysphagia Treatment Programs
Author, Year
Country
PEDro Score
DePippo et al.
(1994)
USA
5 (RCT)
Elmstahl et al.
(1999)
Sweden
No Score
(cohort)
Lin et al. (2003)
Taiwan
No Score
Carnaby et al.
(2006)
USA
8 (RCT)
Methods
Outcomes
115 patients randomized to receive either one
formal dysphagia treatment session and choice of
modified-texture diet, one dysphagia session with
prescribed texture-modified diet or daily
intervention by SLP and prescribed diet.
During inpatient rehabilitation stay, there
were no differences in proportions of patients
developing “calorie-nitrogen deficit” between
the 3 groups. 7 patients in total (6%) were
classified as malnourished.
38 dysphagic stroke patients received dysphagia
therapy for approximately 2 months, which
included oral motor exercises, swallowing
techniques, positioning and dietary modifications.
Albumin and total iron-binding capacity (TIBC)
increased significantly following treatment.
The percentage of patients with albumin and
TIBC below normal levels decreased from
72% to 42% and 50% to 19%, respectively.
The results of between group comparisons on
change scores (pre-test, post test) showed
statistically significant improvements
favouring the treatment group for:
swallowing function (incidence of
coughing/choking, volume/second
swallowed, volume per swallow), neurological
examination and nutrition parameters (midarm circumference and weight)
A quasi-experimental parallel, cluster design study
that recruited 61 patients (2:1) from 7 long-term
care facilities to receive either swallowing training
or no therapy (Patients received therapy following
data collection). Swallowing training consisted of
direct therapies (compensatory strategies, diet
modification, environmental arrangement, the
Mendelssohn maneuver, supraglottic swallowing
and effortful swallowing) and indirect therapies
(thermal stimulation, oral motor and lingual
exercises and were provided 30 min/days 6
days/week x 8 weeks.
306 patients with clinical dysphagia admitted to
hospital with acute stroke were randomly assigned
to receive usual care (n=102), standard lowintensity intervention (n=102), or standard highintensity intervention and dietary prescription
(n=102). Treatment continued for up to a month.
The primary outcome measure was survival free of
an abnormal diet at 6 months
Of patients randomly allocated usual care,
56% (57/102) survived at 6 months free of a
modified diet compared with 64% (65/102)
allocated to standard (low-intensity)
swallowing therapy and 70% (71/102)
patients who received high-intensity
swallowing therapy. Compared with usual
care and low-intensity therapy, high-intensity
therapy was associated with an increased
proportion of patients who returned to a
normal diet (p=0.04) and recovered
swallowing (p=0.02) by 6 months.
Three studies have examined the impact of formal dysphagia therapy on nutritional status, although
nutritional indicators were the secondary end points in all of the studies and not the primary focus of
the trial. DePippo et al. (1994) conducted the only RCT of formal dysphagia therapy, which
demonstrated no benefit of treatment (DePippo et al. 1994). There were no differences in the
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percentage of patients classified as suffering from calorie-nitrogen between treatment groups at the
end of the follow-up period (Figure 16.5). To enable pooling of results two groups, which provided
varying levels of involvement with a Speech-Language Pathologist (SLP) were combined and compared
to a group where SLP involvement was minimal and dysphagic patients, were free to choose their diet.
However, the two-week treatment period may have been too short to actually demonstrate a significant
difference. Lin et al. (2003) also reported improvements in various nutrition parameters and choking
frequency among patients who participated in a swallowing training program (Lin et al. 2003). Elmstahl
et al. (1999) reported that 38 patients who received two months of dysphagia therapy experienced
significant increases in two nutrition indicators (Elmstahl et al. 1999).
DePippo et al. (1994) failed to report a difference in the outcome of malnutrition, as defined by nitrogen
deficit when assessing the efficacy of dysphagia therapy across three treatment arms (Figure 16.6)
(DePippo et al. 1994). The negative result may have been the result of a true lack of effect of therapy, or
it could be that the intervention was not provided for a sufficient length of time to reveal an observable
effect.
Carnaby-Mann et al. (2005) found a trend towards statistical significance when examining the impact of
two levels of dysphagia treatment programs (low and high intensity) on decreasing the need for a
modified diet (Carnaby-Mann & Crary 2005). Compared to usual care, patients who received instruction
on compensatory swallowing strategies, swallowing exercises and regular re-evaluation of dietary
modifications were more likely to have returned to an unmodified diet at six months.
Figure 16.5 The Effectiveness of Dysphagia Therapy
Conclusions Regarding the Efficacy of Dysphagia Treatment
Based on the results from a single RCT, there is moderate (Level 1b) evidence that that dysphagia
therapy does not prevent the development of malnutrition.
16.4.4 Effect of Nutritional Interventions on Changes in Nutritional Parameters
The results from trials, which assessed changes in nutritional parameters following any form of
nutritional intervention, were pooled. The results are presented in Figure 16.6.
The following outcomes were assessed:
1. Changes in serum albumin concentration
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2. Changes in weight
3. Changes in mid-arm circumference
4. Changes in triceps skinfold measurement
Sufficient data was presented in the four studies to enable either the generation of an unadjusted odds
ratio or a weighted mean difference for at least one of the outcomes (DePippo et al. 1994; Gariballa et
al. 1996; Norton et al. 1996; Park et al. 1992). (Nasogastric tubes were considered the control condition
in studies assessing feeding tubes).
Figure 16.6 Changes in Nutritional Indices Associated with Nutritional Intervention
All three of the RCTs included in the pooled analysis reported a positive treatment effect associated with
some form of nutritional intervention; all studies reported a significant improvement in serum albumin,
mid-arm circumference and weight among patients in the treatment groups. Overall, there was a
statistically significant improvement in nutrition markers following a period of nutritional intervention
(WMD: 2.44; 95% CI: 0.06-4.83), with significant heterogeneity (2 = 33.2, p< 0.00001, df=6). The
heterogeneity could be explained by the differences in follow-up periods, interventions provided,
sample sizes, (which ranged from 30-208) and the length of time the treatments were provided.
16.5 Enteral Feeding in the Community
There has been an increasing trend to place enteral feeding tubes in stroke patients who required long
term, non-oral feeding. This has raised many ethical and practical issues surrounding feeding. Although
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there have been no RCTs published on the efficacy of long-term enteral feeding following stroke, there
have been many cohort studies (see Table 16.9).
Table 16.9 Summary of Studies Evaluating Percutaneous Endoscopic Gastrostomy Tube Use
Author/Year/
Country
PEDro score
Wanklyn et al.
(1995)
UK
No Score
Methods
Outcome
Retrospective study of 41
stroke patients. (37 records
were reviewed).
Median time to tube insertion was 26 days complications
included 5 chest infections and 1 perforation. 57% of patients
had died during their original hospital admission. 16% of patients
were alive at 1 year. One patient experienced a good functional
recovery.
Median time to tube insertion was 22 days. 41 (33%) patients
recovered their swallowing function. 63 (50%) patients
experienced complications: aspiration pneumonia occurred in 22
(18%) patients. 47% of patients were alive at 1 year.
James et al.
(1998)
UK
No Score
Retrospective study of 126
stroke patients.
Wijdicks and
McMahon (1999)
USA
No Score
Retrospective study of 63
stroke patients.
Callahan et al.
(2000)
USA
No Score
Retrospective study of 150
patients aged 60 years (41%
stroke patients).
Sanders et al.
(2000)
UK
No Score
Elia et al. (2001)
UK
No Score
Subset of 25 stroke patients
from Norton et al. (1996)
followed prospectively.
12,977 patients from 282
centres received a PEG tube
between 1996-1999 (37%
stroke patients).
Median time to tube insertion was 11 days.
21 (33%) patients died. 36 (57%) remained severely disabled
and institutionalized. PEGs were removed 2-36 months after
placement in 18 patients. Aspiration pneumonia was reported in
4 (6%) patients transferred to nursing homes.
72 patients were followed for 1 year (42% strokes). 50% of
patients were alive at 1 year.
15% of patients were treated for pneumonia over the year. Of
those surviving at least 60 days, 70% did not experience
significant improvement in functional, nutritional or health
status.
PEG tubes were placed 14 days following stroke.
64% of patients were alive at 6 months.
16% of patients had returned to oral intake at 20 weeks.
92% were fed by gastrostomy tube. 70% of patients were alive at
1 year. 13% of patients had returned to oral feeding at 1 year. A
complication rate of ~1% was reported.
Table 16.10 Summary of Studies Evaluating Long-term Nasogastric Tube Use
Author/Year/
Country
PEDro score
Shah et al. (2012)
Malaysia
No Score
Methods
Outcome
Prospective study of 140
patients (70 on NG tube
feeding; 70 controls). Cases
were recruited from
residential homes or stroke
daycare centres and were on
NG tube feeding for at least
8 weeks.
64.3% of patients had at least one complication from NG feeding
(tube dislodgment or insertion damage or aspiration). Nutritional
status in this group was poor. Compared to patients with normal
feeding, a greater percentage of patients on NG feeding were
classified as severely malnourished (38.6%) and 71.4% of
patients did not meet daily caloric requirements.
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Conclusions Regarding the Use of Enteral Feeding in the Community
On average, feeding tubes were placed within the first month following stroke.
The one-year survival rate of patients with feeding tubes varied widely from 16% to 70%. Aspiration
pneumonia was reported in 6-18% of patients with feeding tubes.
The one-year survival rate of patients with feeding tubes, discharged to the community varied
widely following stroke.
16.6 Total Parenteral Nutrition (TPN)
TPN is a form of aggressive nutritional intervention usually reserved for patients with a non-functioning
gastrointestinal tract. Unless a stroke patient presented with a pre-existing medical condition that
precluded safe oral or enteral feeding, parenteral feeding would rarely be indicated. Examples of such a
situation may include a dysphagic patient who had refused an enteral feeding device, in whom a central
line had been placed for an unrelated purpose or a patient with inflammatory bowel disease, when
enteral feeding may be contraindicated. As a result of the limited use of this feeding modality, there
have been no studies investigating the efficacy of parenteral feeding post stroke.
Conclusions Regarding the Use of TPN
There have been no studies that have evaluated the efficacy of TPN in the treatment of stroke
patients.
The use of TPN has not been studied in the stroke population.
16.7 Cochrane Reviews of Nutritional Interventions Following Stroke
There is currently one Cochrane Review evaluating nutritional interventions following stroke. Table 6.11
provides a summary of this review.
Table 16.11 Summary of Cochrane Reviews for Nutritional Interventions Following Stroke
Author, Year
Country
Methods
Title
Geeganage et al. 33 RCT’s were included in the review
(2012)
consisting of 6,779 patients.
U.K.
Studies Included: RCT’s assessing
swallowing therapy, route of feeding,
Interventions for timing of feeding, fluid supplementation
dysphagia and
and/or nutritional supplementation.
nutritional
support in acute Patients Included: Acute and subacute,
and subacute
ischemic or hemorrhagic stroke.
stroke
Results
Nutritional Therapies:
PEG vs. NG (n=5 studies; 455 patients):
Primary outcomes: no effect on death or
dependency/disability.
Secondary outcomes: fewer treatment failures (OR
0.09; 95% CI 0.01 to 0.51; P=0.007), higher
concentrations of albumin (MD 4.92; 95% CI 0.19 to
9.65) for PEG vs. NG. No statistically significant
differences between the groups were found for midarm circumference, pressure sores, case fatality,
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Time since stroke: <6 months
Only results from
the Nutritional
Mean age of patients: 71 years
therapies section
are reported
here (Refer to
Chapter 15 for
other results)
institutionalization, length of stay, infection or
pneumonia, dysphagia, or weight.
Timing of feeding: data from only one study.
Fluid supplementation: data from only one study.
Nutritional supplementation (n=8 studies; 4391
patients):
Primary outcomes: no effect on death or
dependency/disability.
Secondary outcomes: fewer pressure sores (OR 0.56;
CI 0.32 to 0.96; P=0.03), greater energy intake (MD
430.18; 95% CI 141.61 to 718.75; P=0.003), and
greater protein intake (MD 17.28; 1.99 to 32.56;
P=0.03). No statistically significant differences were
found between groups for length of hospital stay or
albumin concentrations.
Overall, the Cochrane review found no statistically significant evidence for decreases in death or
dependency using nutritional interventions. However, the use of a PEG tube compared to a NG tube
resulted in fewer treatment failures. Only single studies evaluated the timing of feeding and the effects
of fluid supplementation. Nutritional supplementation resulted in fewer pressure sores and greater
nutritional intake. Another non-stroke specific Cochrane review (Gomes et al. 2012) compared PEG to
NG with respect to the number of intervention failures, patient nutritional status, mortality,
complications, time on the intervention, quality of life, length of stay in hospital and economic
outcomes. This review included several stroke specific studies (Bath et al. 2000; Dennis et al. 2005a;
Hamidon et al. 2006; Norton et al. 1996; Park et al. 1992), similar to those included in the Cochrane by
Geeganage and colleagues, and found similar results. PEG and NG did not differ significantly in terms of
patient outcomes, however, the PEG was found to have fewer treatment failures.
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Summary
1.
The incidence of malnutrition varies from 8 to 49% post stroke, depending on the timing
of the assessment and the criteria used to define malnutrition.
2.
There is no “gold standard” for the assessment of nutritional status.
3.
There is an elevation in metabolic rate following stroke that ranges from 107% above
predicted levels to 126%.
4.
There is conflicting evidence that metabolic rate is elevated more in hemorrhagic stroke
compared with ischemic stroke.
5.
There is evidence that an acute phase response accompanies stroke, although its
contribution to the development of malnutrition is unclear.
6.
Although dysphagia is common, there is an absence of literature to confirm or refute
the development of other significant gastrointestinal impairments following stroke.
7.
Stroke patients consume between 74 and 86% of their energy requirements during the
first 3 weeks post stroke.
8.
There is strong (Level 1a) evidence that intragastric feeding is associated with fewer
mechanical complications compared to nasogastric feeding for stroke patients who
require long term (>28 days) non-oral feeding. Based on the results from a single RCT, in
which the results approached statistical significance, there is moderate (Level 1b)
evidence that type of feeding tube (NG vs. PEG) is unrelated to death and dependency at
6 months.
9.
There is moderate (Level 1b) evidence that oral supplementation improves the energy
and protein intakes of stroke patients. There is conflicting (Level 4) evidence that oral
sip supplementation improves functional outcomes in stroke patients. Based on the
results from a single RCT, there is moderate (Level 1b) evidence that routine oral sip
supplementation does not reduce the incidence of death or dependency following
stroke.
10. There is moderate (Level 1b) evidence that that dysphagia therapy does not prevent the
development of malnutrition.
11. The one-year survival rate of patients with gastrostomy feeding tubes varies widely
from 16% to 70%. On average, feeding tubes are placed within the first month following
stroke. Aspiration pneumonia was reported in 6-18% of patients.
12. There is moderate (Level 1b) evidence that dysphagia therapy does not impact on
nutritional status. However, the one RCT upon which this conclusion was based had
small patient numbers and the treatment period was only two weeks.
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13. There have been no studies that have evaluated the efficacy of total parenteral
nutrition in the treatment of stroke patients.
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