Professional Documents
Culture Documents
DOI 10.1007/s00455-014-9578-x
ORIGINAL ARTICLE
Received: 24 July 2014 / Accepted: 10 September 2014 / Published online: 25 October 2014
The Author(s) 2014. This article is published with open access at Springerlink.com
C. E. A. Barbon
e-mail: carly.barbon@uhn.ca
C. M. Steele
e-mail: Catriona.steele@uhn.ca
J. Chen
e-mail: jschen@zjgsu.edu.cn
J. A. Y. Cichero
e-mail: Julie.cichero@iddsi.org
R. O. Dantas
e-mail: rodantas@fmrp.usp.br
J. Duivestein
e-mail: jduivestein@cw.bc.ca
B. Hanson
e-mail: ben.hanson@ucl.ac.uk
P. Lam
e-mail: peter.lam@iddsi.org
C. Lecko
e-mail: caroline.lecko@nhs.net
C. M. Steele (&) C. E. A. Barbon L. Giosa C. Leigh
A. Nagy A. M. Namasivayam H. Wang
Toronto Rehabilitation Institute University Health Network,
550 University Avenue, #12-101, Toronto, ON M5G 2A2, Canada
123
L. Giosa
e-mail: lidia.giosa@mail.utoronto.ca
C. Leigh
e-mail: leigh.chelsea@gmail.com
A. Nagy
e-mail: ahmed.nagy@uhn.ca
A. M. Namasivayam
e-mail: ashwini.namasivayam@uhn.ca
H. Wang
e-mail: helenyi.wang@gmail.com
C. M. Steele C. E. A. Barbon A. M. Namasivayam
Department of Speech-Language Pathology, University of
Toronto, Toronto, Canada
W. A. Alsanei
School of Food Science and Nutrition, University of Leeds,
Leeds, UK
e-mail: woroooud@hotmail.com
S. Ayanikalath
Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates
e-mail: sonanarayanan4@gmail.com
Introduction
The use of texture-modified foods and thickened liquids
has become a cornerstone of clinical practice to address
dysphagia (swallowing impairment) [1, 2]. The principle
behind this pervasive practice arises from the assumption
that modifying the properties of normal foods and liquids
will make them easier and safer to swallow. In the case of
liquids, it is widely accepted that thin liquids (such as
water) pose safety challenges for people with dysphagia
because they flow quickly [3, 4]. The speed of bolus flow
from the mouth into the pharynx may be sufficiently fast
that it does not provide enough time for the person to
engage airway closure before the bolus arrives at the
entrance to the larynx and airway. Thickened liquids are
frequently recommended with the goal of slowing down
the flow of liquids to allow more time for airway closure
J. Chen
Zhejiang Gongshang University, Hangzhou, China
P. Lam
Peter Lam Consulting, Vancouver, BC, Canada
J. A. Y. Cichero
School of Pharmacy, The University of Queensland, Brisbane,
Australia
P. Lam
Faculty of Land and Food Systems, University of British
Columbia, Vancouver, BC, Canada
K. Coutts
Helen Joseph Hospital, Johannesburg, South Africa
e-mail: kim.coutts@gauteng.gov.za
C. Lecko
National Health Service Commissioning Board Special Health
Authority, London, UK
R. O. Dantas W. V. Nascimento
Medical School of Ribeirao Preto - University of Sao Paulo,
Ribeirao Preto, Brazil
e-mail: fono.weslania@gmail.com
A. Nagy
Fayoum University, Fayoum, Egypt
J. Duivestein
Sunny Hill Health Centre, Vancouver, BC, Canada
B. Hanson
Department of Mechanical Engineering, University College
London, London, UK
I. Odendaal
University of KwaZulu-Natal, Durban, South Africa
e-mail: ingeoden@gmail.com
C. H. Smith
Division of Psychology and Language Sciences, University
College London, London, UK
e-mail: christina.smith@ucl.ac.uk
123
123
2.
3.
4.
Methods
A comprehensive literature search for literature published
between 1985 and January, 2013 was conducted using
multiple search engines, including Ovid MEDLINE(R),
Ovid MEDLINE(R) In-process and other non-indexed
citations, AMED (Allied and Complementary Medicine),
EMBASE, Health and Psychosocial Instruments, and PsycINFO. The search was also conducted in Scopus using the
following subject area limits: medicine, agricultural and
biological sciences, pharmacology etc., chemistry, nursing,
neuroscience, chemical engineering, engineering, health
professions, psychology, materials science, multidisciplinary, dentistry. Search terms were broadly specified with the
goal of finding as much relevant literature as possible, and
included MeSH Headings of Swallowing or Deglutition or Dysphagia. Inclusion of one or more key-word
(Scopus) or text terms (all other search engines) was also
specified with the goal of focusing the results on the topic
of interest. These terms were: Visco*; Bolus;
rheo*; dens*; yield*; fluid*; mechani*;
elastic*; Newton*; carbohydrate; colloid*;
starch; gum; alginate; cohes*; thick*;
Table 1 Questions addressed during the full-text relevancy and quality review
Number
Question
Clarifying instructions
10
11
12
13
14
15
Questions indicating properties that require a Yes response for inclusion in the qualitative synthesis
123
Results
Fig. 1 PRISMA flow diagram of the search process used in this
systematic review
123
Participant Characteristics
Demographic information regarding the participants of the
36 studies selected for qualitative synthesis is shown in
Table 2. Notably, only three of these studies described
swallowing or oral processing in children; one of these was
a study of swallowing in premature infants [17], while a
second [18] explored differences in chewing behaviors in
infants aged 6 months to 2 years of age. The third study
involving children explored oral processing behaviors in
two groups of typically developing girls aged 5 and 8 years
old, as well as a control group of healthy adult women [19].
Of the 29 studies describing swallowing or oral processing
in adults, 27 reported data for healthy adult participants
[1945], with two studies restricting their focus to denture
wearers [46, 47]. A total of 10 studies reported data for
adults with dysphagia [2024, 4852]. Four of these studies
described swallowing in stroke patients in comparison to
healthy controls [2124] and a 5th paper described a group
of patients with dysphagia secondary to Chagas disease,
again with comparison to a group of healthy controls [20].
Two papers reported data for individuals with dysphagia
related to head and neck cancer, in one case following
surgical resection of the soft palate [48] and the second
exploring post-radiation dysphagia in patients treated for
nasopharyngeal carcinoma [49]. The remaining papers
described swallowing in patients with Parkinsons disease
[50], in unspecified neurogenic dysphagia [51], or in
unspecified dysphagia [52]. Sample sizes ranged from 3
[25] to 205 [24] participants.
Table 2 Demographics of the study samples of the 36 articles selected for detailed review
Author
Year
Title
Pediatric
patient
sample?
Adult
patient
sample?
Gisel [18]
1991
2002
30
2012
29
Videofluoroscopic evaluation of
swallowing in Chagas disease
32
2013
23
2011
20
1992
41
Neurogenic
disorders
2008
10
Parkinsons
disease
2005
20
Stroke patients
1994
28
Stroke patients
2011
72
Stroke patients
2010
Stroke patients
Karkazis and
Kossioni [47]
1998
Denture wearers
Karkazis [46]
2002
Edentulous
participants
with
mandibular
overdentures
supported by
implants
10
26
Premature
infants
4
Adults with
dysphagia
(no etiology
specified)
4
Chagas disease
Head and neck
cancer patients
post soft palate
resection and
reconstruction
Nasopharyngeal
carcinoma
patients post
radiation
123
Table 2 continued
Author
Year
Title
12
Karkazis and
Kossioni [41]
1997
22
1998
12
2012
9; 7
2007
18
1989
Reimers-Neils
et al. [26]
1994
2007
15
2004
2005
2010
12
2002
12
2010
17
2004
22
Chi-Fishman and
Sonies [53]
2002
31
96
2008
123
Pediatric
patient
sample?
Adult
patient
sample?
Table 2 continued
Author
Year
Title
Pediatric
patient
sample?
Adult
patient
sample?
The three studies by Inagaki et al. appear to deal with data from a single experiment
Stimulus Characteristics
The various food and liquid stimuli used in the studies
selected for inclusion in the qualitative synthesis are
summarized in Tables 3 (radio-opaque liquid stimuli), 4
(non-opaque liquid stimuli), and 5 (solid stimuli). Of the 36
studies selected for detailed review, seven reported comparative data for swallows of thin liquid (either barium,
water or juice) and an extremely thick liquid (i.e., pureed or
spoon-thick consistency) [19, 26, 33, 35, 48, 51, 53]. A
total of 13 articles described swallowing measures for a
narrower contrast, i.e., thin liquid compared to either a
mildly thick liquid (also known as nectar-thick) [17, 19, 23,
26, 2830, 32, 35, 48, 51, 53] and/or a moderately thick
liquid (also known as honey-thick) [2830, 32, 33, 35, 53],
with six of these articles including both mildly thick and
moderately thick liquids [2830, 32, 35, 53]. In terms of
solid stimuli, which were explored in a total of 18 studies
(Table 5) [18, 19, 21, 24, 27, 31, 3948, 51, 52], there were
effectively no stimuli that were the same in any two or
more studies. Solid foods ranged from items that were
described by authors as being softer (i.e., banana with
barium paste [31]; cooked rice mixed with barium [52];
corned beef [45]; gummy bears [19]; konjac jelly [27], or
gelatin cubes [18]) to items at the harder end of the continuum (e.g., fresh raw carrots [27]; biscuits or cookies [24,
31, 48, 51] or peanuts [31]). The description of certain
items as softer in these studies illustrates the subjectivity
with which texture descriptors may be applied. For
example, crisp, peeled apple were described as being
softer [46] in comparison to raw carrot [46], despite the
fact that a crisp apple would not generally be regarded as a
soft texture. Three studies, all originating from Asia,
explored the combination of solid and liquid consistencies
using either corned beef in a liquid barium [45], a thick rice
gruel (the consistency of which was not further described)
[21] or 12 g of cooked rice added to 100 ml of liquid
barium [52].
Given the available data, it appears reasonable to synthesize observations regarding differences in swallowing
physiology and function across the spectrum of liquid
consistencies, from the thin to the extremely thick end of
the continuum. However, caution is warranted with respect
to delineating quantitative values to capture levels or categories of liquids along this continuum, based on incomplete reporting and the variety of methods and measures
used to characterize liquid flow in the studies reviewed.
This variety challenges the idea that the stimulus labels
used in the literature (e.g., thin, nectar-thick, honey-thick)
map to defined ranges of flow. For example, a wide variety
of different studies reported using thin liquid barium, but
where recipes were reported, these used different concentrations of barium and different dilutions with water or
other thin liquids. Insufficient information was provided in
the majority of these studies to support recipe replication,
or to calculate the weight to volume concentrations of the
resulting barium suspensions. Furthermore, given that
commercial barium preparations frequently involve additional components to reduce foaming or aid suspension,
including gums and starches, viscosity cannot be presumed
without additional information.
Very few studies provided objective measures of stimulus characteristics such as viscosity, yield stress, or density (see Tables 3, 4). In several cases, the authors used
metaphors to describe the apparent viscosities of stimuli,
such as with a viscosity similar to water, but failed to
provide adequate evidence to support these descriptions.
Indeed, several of the metaphors used were scientifically
implausible; for example, 120 % w/v E-Z-HD barium is
described as being similar in viscosity to water in one study
[51], although barium solutions typically have non-Newtonian flow characteristics and viscosities well above those
of water [54, 55]. The fact that both starch- and xanthangum thickeners are acknowledged to produce liquids with
non-Newtonian flow [54, 5662] presents a challenge when
comparing the stimuli used across these studies; the measured value of viscosity (i.e., apparent viscosity) is very
sensitive to the shear rate at which the measurement is
taken. In cases where viscosity measures were reported, the
literature lacked any apparent convention with respect to
reporting values at specific shear rates. From the data
reported, it can be noted that the non-opaque stimuli
labeled as thin had viscosities ranging up to 12 mPa s @
45/s [28], while the radio-opaque thin liquid stimuli
spanned a larger viscosity range, reaching reported values
as high as 351 mPa s at 25/s [29]. Non-opaque liquids
123
10
Table 3 Radio-opaque liquid stimuli used in studies exploring swallowing of different consistencies
Author
Thin (opaque)
Nectar-thick (opaque)
Honey-thick (opaque)
Liquid barium
dos Santos
et al. [20]
Goldfield
et al. [17]
Pudding-thick barium
Polibar (100 % w/v, E-Z-EM)
with a viscosity similar to
that of syrup
8 g of chicken spread
(Underwood Chunky
Chicken) mixed with
a little Esophotrast
barium paste
Commercially pre-thickened
nectar-thick apple juice
(RESOURCE, Novartis
Nutrition)
Paste barium: 15 ml of
the thin barium
preparation plus an
additional 12 ml of
E-Z-HD powder
Esophotrast barium
paste (100 % w/v)
with the consistency
of pudding
30 ml of 100 % liquid
barium sulfate with
3 g of Nutilis
thickener (Nutricia)
Kim and
Han [21]
Pudding-thick/paste/
puree (opaque)
Esophotrast
123
Novartis RESOURCE
Novartis RESOURCE HoneyNectar-thick Apple juice
thick Apple juice mixed four
mixed four parts to one with
parts to one with EZ-HD
EZ-HD 250 % w/v barium
250 % w/v barium sulfate
sulfate powder (E-Z-EM
powder (E-Z-EM Therapex):
Therapex): (density: 1.15 g/
(density: 1.13 g/cc; yield stress:
cc; yield stress: 1.055 Pa;
2.109 Pa; viscosity:
viscosity: 863 mPa s @ 25/s
1541 mPa s @ 25/s
(Varibar Puddingbarium Sulfate
Esophageal Paste,
230 ml 40 % w/v,
30 % w/w (E-Z-EM)
11
123
12
Thin
Nectar-thick
Nectar-thick liquid
Juice
Chi-Fishman and
Sonies [53]
Lemon-flavored water,
7 mPa s
Honey-thick
Puree
Honey-thick thick apple
Applesauce (Lucky Leaf,
juice (Diamond Crystal
Peach Glen, PA)
Medical Food): viscosity of
1,1001,900 mPa s
Lemon-flavored water
Lemon-flavored water
Lemon-flavored water
thickened with corn-starch
thickened with corn-starch
thickened with corn-starch
to 243260 mPa s
to 724759 mPa s
to spoon-thick,
27602819 mPa s
Gisel [18]
Igarashi et al. [30]
Pudding-thick/paste/puree
Unsweetened applesauce
A test food consisting of
A test food consisting of
A test food consisting of
water, 0.15 % citric acid,
water, 0.17 % citric acid,
water, 0.24 % citric acid,
9 % sucrose, 0.04 % flavor 13.5 % sucrose, 0.08 %
15 % sucrose, 0.12 %
flavor and 1.5 % of a
flavor and 3 % of a
thickening agent comprised thickening agent comprised
of guar gum, tara gum,
of guar gum, tara gum,
carrageenan, xanthan gum, carrageenan, xanthan gum,
starch and dextrin
starch and dextrin
2 % concentration of
mousse-up thickening
agent in 100 ml distilled
water
2 % concentration of
mousse-up thickening
agent in 100 ml distilled
water
2 % concentration of
mousse-up thickening
agent in 100 ml distilled
water
Water
Reimers-Neils
et al. [26]
Water
123
Commercially pre-thickened
honey-thick apple juice
(RESOURCE, Novartis
Nutrition)
13
Table 4 continued
Author
Thin
Nectar-thick
Honey-thick
Novartis RESOURCE
Novartis RESOURCE
Nectar-thick Apple juice
Honey-thick Apple juice
(density: 1.067 g/cc; yield
(density: 1.073 g/cc; yield
stress: 0.264 Pa; viscosity:
stress: 1.424 Pa; viscosity:
466 mPa s @ 25/s)
1140 mPa s @ 25/s)
Pudding-thick/paste/puree
123
14
Discussion
Evidence Supporting or Refuting Thickening of Liquids
Collectively, the selected studies clearly show a reduction
in the risk of penetrationaspiration with liquids, as they
progress from the thin to the very thick end of the viscosity
continuum. This finding is limited, by definition, to studies
in which objective measures of penetrationaspiration were
available, which for the purposes of the present review
meant studies involving barium swallowed under videofluoroscopy. Evidence regarding penetrationaspiration
was also limited to studies involving adult participants with
dysphagia.
However, an important cautionary note arises from this
review given the convergence of evidence across several
studies, showing a heightened risk of post-swallow residue
in the pharynx for liquids with higher viscosities. This
123
points to an important clinical challenge in terms of identifying suitable and safe consistencies for patients with
dysphagia; namely, that of identifying liquids that are thick
enough to be swallowed safely (without penetrationaspiration) while avoiding the pitfall of post-swallow residue.
As a post-script on this particular question, an additional
source of data was brought to the attention of the authors
after completion of the qualitative synthesis of the selected
articles. This as-yet unpublished doctoral dissertation [72]
involved rigorous videofluoroscopic exploration of swallowing with thin and nectar-thick VaribarTM barium by
infants aged 3 weeks to 3 months, referred for evaluation
of swallowing secondary to respiratory compromise. This
dissertation is particularly noteworthy given the relative
dearth of information regarding pediatric feeding and
swallowing uncovered in our search process [1719]. The
Gosa study [72] reports several findings that concur with
the observations gleaned from our qualitative synthesis,
including prolongations of oral transit time and a reduction
in penetrationaspiration with the nectar-thick stimulus
compared to the thin liquid barium. Additionally, residue
was reported to be present for 80 % of the nectar-thick
swallows compared to only 44 % of thin liquid swallows.
An additional gap to highlight with respect to the lack of
identified studies in either the healthy or dysphagic infant
population is the challenge of matching assessment stimuli
to the rheological properties of breast milk or infant formula. This is a question of emerging interest in the dysphagia literature [9, 73] and definitely an area where
additional research is needed.
Evidence Regarding the Number and Definitions
of Levels of Liquid Thickening
Although this systematic review finds a convergence of
evidence showing that thicker liquids are less likely to be
aspirated, and more likely to cause post-swallow residue,
the available data are insufficient to suggest particular
viscosity values or other quantitative measures of material
properties along the continuum from thin to extremely
thick liquids that represent boundaries of clinical importance [74]. Historically, clinical guidelines regarding the
use of thickened liquids have proposed quantitative
boundaries that arise either from clinical consensus, or
represent an educated guess. For example, the National
Dysphagia Diet in the United States proposes 4 levels of
liquid viscosity, labeled thin, nectar-thick, honeythick and spoon-thick and corresponding to apparent
viscosity ranges of 150, 51350, 3511,750, and
C1,751 mPa s, measured at a shear rate of 50/s [10]. The
Japanese guideline provides a larger number of categories
with viscosity ranges of 150, 51150, 151300, 301500,
and [500 mPa s, again measured at a shear rate of 50/s
15
Table 5 Solid stimuli (both radio-opaque and non-opaque) used in studies of oral processing and swallowing
Author
Opaque/
non-opaque
Mixed consistency
Soft solids
Hard solids
Soft chewing gum (hardness = 440 g Hard chewing gum (hardness = 670 g
measured on a durometer)
measured on a durometer)
Non-opaque
Non-opaque
Toasted biscuits
Opaque
Opaque
Non-opaque
Gisel [18]
Non-opaque
Non-opaque
Opaque
Karkazis [46]
Non-opaque
Karkazis and
Kossioni [47]
Non-opaque
Karkazis and
Kossioni [41]
Non-opaque
Raw carrots
Non-opaque
Opaque
12 g cooked rice
24 g cooked rice mixed with 5 ml
mixed with 100 ml liquid barium
liquid barium
Cheese
Non-opaque
Opaque
[14, 15]. In the current review, we found no specific evidence to support or refute the specific numeric categorical
viscosity boundaries suggested in these or other guidelines.
123
16
123
17
Table 6 continued
Author
Author
Anderson et al.
[39]
Karkazis and
Kossioni [41]
Karkazis and
Kossioni [47]
Karkazis [46]
Chi-Fishman and
Sonies [53]
Funami et al.
[43]
Nagatomi et al.
[40]
Oommen et al.
[23]
Reimers-Neils
et al. [26]
Gisel [18]
Goldfield et al.
[17]
Hoebler et al.
[42]
Igarashi et al.
[30]
123
18
Table 6 continued
Author
Taniwaki et al.
[27]
Youmans et al.
[35]
123
19
Table 7 Summary of study results, listed by technology, with levels of evidence rated according to the scheme of the National Health and
Medical Research Council of Australia [66]
Author
Technology
Finding
Level of
evidence
17
Accelerometry
IV
Articulography
Greater variation in tongue movement for honeythick items and least for thin items
IV
Articulography
IV
Auscultation/acoustics
IV
26
Camera recordings
of chewing behavior
IV
143
Camera recordings
of chewing behavior
III-2
Gisel [18]
Sample
size
23
Naso-endoscopy
IV
22
sEMG
IV
12
sEMG
IV
sEMG
IV
sEMG
IV
sEMG
IV
Karkazis [46]
sEMG
IV
123
20
Table 7 continued
Author
Sample
size
Technology
Finding
Level of
evidence
22
sEMG
IV
sEMG
IV
sEMG
IV
30
sEMG
III-2
12
IV
12
IV
96
Tongue pressure
measurement
31
Ultrasound
IV
VFSS
III-2
123
205
III-2
21
Table 7 continued
Author
Sample
size
Technology
Finding
Level of
evidence
28
VFSS
III-2
41
VFSS
IV
32
10
VFSS
VFSS
III-2
IV
12
VFSS
IV
29
VFSS
IV
20
VFSS
IV
VFSS
72
VFSS
III-2
15
VFSS
IV
10
VFSS
IV
9; 7
Multiple methods:
mechanical bolus
compression; sensory
profiling;
sEMG; acoustics
IV
IV
123
22
Table 7 continued
Author
Sample
size
Technology
Finding
Level of
evidence
20
Multiple methods:
salivary measures
and viscosity
measures
after oral processing
III-2
18
Multiple methods:
sEMG and texture
profile analysis after
oral processing
IV
Levels of evidence: III-2: evidence from comparative studies with concurrent controls without randomized allocation (cohort studies), case
control studies, or interrupted time-series with a control group; III-3: evidence from comparative studies with historical control, two or more
single-arm studies, or interrupted time-series without a parallel control group; IV: evidence from case series, either post-test or pre-test and posttest, or superseded reference standards; V: expert opinion, physiology, bench research or first principles studies
sEMG surface electromyography, VFSS videofluoroscopic swallowing study
123
23
Conclusions
Fig. 2 a Prevalence of penetrationaspiration by liquid bolus consistency, as reported in a study of stroke patients by Bingjie et al. [24].
Penetrationaspiration scale scores of 1 and 2 are considered normal;
scores of 35 indicate penetration of the laryngeal vestibule, while
scores of 68 indicate aspiration of material below the true vocal
folds. b Differences in the severity of penetrationaspiration as a
function of liquid bolus consistency, as reported in a study of patients
with Parkinsons disease by Troche et al. [50]
123
24
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123
PhD
Catriona M. Steele
PhD Cand
MSc
Sona Ayanikalath
MA
Carly E. A. Barbon
Jianshe Chen PhD
PhD
Julie A. Y. Cichero
Kim Coutts
MA
PhD, MD
Roberto O. Dantas
MRSc, OT/PT
Janice Duivestein
Lidia Giosa
MHSc Cand
Ben Hanson
PhD
Peter Lam
RD, CFE
Caroline Lecko
Chelsea Leigh
RN
BSc
PhD Cand
PhD