DR.

JOÃO PINHO (Orcid ID : 0000-0002-3977-7146)

Article type : Original Article

Accepted Article
Impact of the systematic use of the Gugging Swallowing Screen in

acute ischemic stroke patients

Margarida Lopes, MSc, Neurology Department, Hospital de Braga, Portugal

Eduardo Freitas, MSc, Neurology Department, Unidade Local de Saúdo do Alto Minho,

Portugal

Marta Oliveira, MSc, Physical Medicine anf Rehabilitation Department, Hospital de Braga,

Portugal

Ester Dantas, Lic, Neurocritical Care Unit, Hospital de Braga, Portugal

Nídia Azevedo, Lic, Neurocritical Care Unit, Hospital de Braga, Portugal

Pedro Rodrigues, Lic, Neurocritical Care Unit, Hospital de Braga, Portugal

João Pinho, MD, Neurology Department, Hospital de Braga, Portugal

Carla Ferreira, MD, Neurology Department, Hospital de Braga, Portugal

Corresponding author:

João Pinho

Sete Fontes, São Victor, 4710-243 Braga, Portugal

jdpinho@gmail.com

+351253027000

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1111/ene.13825
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 Running title: GUSS in acute ischemic stroke

Keywords: Dysphagia; screening; ischemic stroke; pneumonia.

Accepted Article
ABSTRACT

Background: Post-stroke dysphagia occurs in up to three fourths of patients and is associated

with a higher risk of respiratory infections and poor outcome. Systematic screening of

dysphagia in the acute stroke unit (ASU) is essential to identify patients at risk of aspiration

and to provide dietary recommendations. Our study aimed to assess the impact of the

systematic application of the Gugging Swallowing Screen (GUSS) in acute ischemic stroke

patients.

Methods: Retrospective study of consecutive acute ischemic stroke patients admitted to an

ASU in two time periods: pre-GUSS, February/2014-July/2015, when the 10mL water

swallowing test was systematically administered; GUSS, August/2015-October/2016, when

the GUSS test was systematically administered. Groups were compared regarding baseline

and stroke characteristics, and the occurrence of stroke-associated pneumonia (SAP), in-

hospital death and 3-month outcome.

Results: 344 patients were included in the study, median age 71 years, 51.7% were male,

median NIHSS 11. 204 patients were included during the pre-GUSS period and 140 during

the GUSS period. Patients in the GUSS period more frequently had diabetes, partial anterior

circulation syndromes and were more frequently treated with thrombectomy. There was no

difference in the occurrence of SAP between the two groups (pre-GUSS=12.5%,

GUSS=15.1%, p=0.490), and no differences were found concerning in-hospital mortality

(p=0.996), 3-month functional independence (p=0.647), or 3-month mortality (p=0.598).

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 Conclusions: The systematic administration of GUSS in a population of acute ischemic stroke

patients did not reduce the occurrence of SAP, mortality, or 3-month functional dependence,
Accepted Article
when compared to the systematic administration of the 10mL water swallowing test.

INTRODUCTION

Pos-stroke dysphagia (PSD) is a frequent complication of acute stroke and may result in

aspiration of food and liquids to the respiratory tract and consequent stroke-associated

pneumonia (SAP). In studies which used a diagnostic clinical or instrumental assessment,

dysphagia was found in up to 78% of acute stroke patients [1,2]. SAP is associated with

increased mortality and poor outcome, occurs in 7-33% of all acute stroke patients, and is

more frequent in patients who have PSD [1,3]. Systematic screening of PSD is a fundamental

part of a multidomain protocol of care in stroke units, which has been demonstrated to be

associated with reduced 90-day mortality and dependency [4]. The goal of PSD screening is

to identify patients with dysphagia and at risk of aspiration during swallowing, using tests

with high sensibility, so that they can be more extensively evaluated using other diagnostic

tools [5]. Several screening tools have been developed for this purpose, each with different

strengths and limitations, and their selection has been recommended to follow local

characteristics of the health resources [6]. The Gugging Swallowing Screen (GUSS) is a

validated bedside dysphagia screen with excellent sensitivity to identify patient with acute

stroke with aspiration risk, consisting of a non-instrumental stepwise assessment of

swallowing and non-swallowing functions, with scores between 20 (minimal risk of

aspiration) and 0 (high risk of aspiration), that provides recommendations concerning diet

and further evaluation [7,8]. Our goal was to assess the clinical impact of a change in the

screening method for dysphagia in acute ischemic stroke patients admitted in an Acute Stroke

Unit (ASU).

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 METHODS

A retrospective observational single-hospital study was conducted to evaluate the occurrence

Accepted Article
of in-hospital SAP and 3-month outcome in consecutive acute ischemic stroke patients

admitted in a 6-bed ASU, during two distinct time periods according the method used for

screening dysphagia. In the first time period (pre-GUSS, February/2014 – July/2015), all

patients were routinely screened for dysphagia using a 10mL water swallowing test [9] which

established the presence or absence of dysphagia, and was being routinely administered in the

ASU since 2007. In the second period (GUSS, August/2015 – October/2016) all patients

were routinely screened for dysphagia using the GUSS test [7], which was performed by all

nurses in the ASU after a period of comprehensive training of 2 weeks by one of the authors

(MO). The dysphagia screening tests were performed in both groups (pre-GUSS and GUSS)

at a median time of 2 days after stroke onset (interquartile range = 1-2), and “nil per os” was

ordered for all patients until then. Further management of dysphagia in the ASU included the

formal assessment by a multidisciplinary team comprising a rehabilitation specialist, speech-

language therapist, rehabilitation nurse, ear-nose-throat specialist and neurologist, which

advised the need for nasogastric tube, dietary recommendations concerning texture and

viscosity, swallowing therapy, and/or additional assessment with videoendoscopic or

videofluoroscopic swallowing studies. Clinical records were reviewed to collect clinical

variables, presence of dysphagia, occurrence of SAP, in-hospital mortality, 3-month

functional independence (assessed using the modified Rankin Scale) and 3-month mortality.

Individual GUSS score sheets were prospectively collected and analyzed. SAP was defined

as the presence of a pulmonary consolidation or infiltration in thoracic imaging and ≥3 of the

following manifestations: fever ≥38ºC, productive cough, abnormal respiratory examination,

arterial hypoxemia, elevation of blood inflammatory markers and microbiological

identification of a relevant pathogen. Five patients were excluded from the analyses related

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 to SAP, because even though they had clinical manifestations of respiratory infection, no

thoracic imaging was performed (among these, 2 had hypoxemia or abnormal respiratory
Accepted Article
examination).

Pre-GUSS and GUSS groups were compared using chi-square and Mann-Whitney U tests as

adequate. Multivariate logistic regression analyses were performed, with occurrence of SAP

as the dependent variable, and other variables of interest, namely the inclusion period,

dysphagia defined by the 10mL water swallowing test or GUSS score as independent

variables. Additional co-variates for adjustment of the odds ratio in the regression models

were selected according to significant imbalances in the distribution between GUSS and pre-

GUSS groups (diabetes, partial anterior circulation infarct syndrome, mechanical

thrombectomy), and variables known to be associated with the occurrence of SAP and

outcome (age, stroke severity, intravenous thrombolysis, cardioembolic etiology). Statistical

analyses were performed using SPSS version 22 and MedCalc version 18.2.1. The study

complies with the Declaration of Helsinki and was conducted in accordance to the local

ethics committee requirements (Comissão de Ética para a Saúde do Hospital de Braga).

RESULTS

During the study period 348 acute ischemic stroke patients were admitted in the ASU, 4 of

which were excluded because no early follow-up data was available. Among the final

population of patients (n=344), 204 were admitted during the pre-GUSS period, and 140

during the GUSS period. Median age was 71 years (interquartile range [IQR] 59-79), 178

were male (51.7%) and median NIHSS was 11 (IQR=6-18). Baseline characteristics of the

study population according to the inclusion period are detailed in Table 1. Patients included

in the GUSS period more frequently had diabetes (p=0.023), more frequently presented

partial anterior circulation syndrome (p=0.030), and more frequently were submitted to

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 mechanical thrombectomy (p<0.001). Insertion of nasogastric tube, and timing of insertion

was similar in both groups (p=0.377 and p=0.918 respectively). SAP occurred in 13.6% of
Accepted Article
patients (95% confidence interval [95%CI] = 8.3 - 18.9%), at a median time of 3 days after

stroke (IQR = 2 - 4), and there was no difference in its occurrence between the pre-GUSS and

GUSS periods (12.5% Vs. 15.1%, p=0.490). The characteristics of patients according to the

occurrence of SAP are described in the Supplementary Table 1. After adjustment for

variables of interest, the inclusion period (pre-GUSS as reference) was not associated with

the occurrence of SAP in the multivariate regression model (odds ratio [OR] = 1.41, 95%CI =

0.67 - 2.99, p=0.367) (Table 2). In the two inclusion periods there were also no differences in

the occurrence of in-hospital death (7.8% Vs. 7.9%, p=0.996), 3-month functional

independence (54.3% Vs. 51.8%, p=0.647), or 3-month mortality (11.8% Vs. 12.9%,

p=0.598).

Dysphagia, as defined by the 10mL water swallowing test, was present in 103/204 patients

(50.5%). The prevalence of risk of aspiration as defined by the GUSS score was 50.0% for

the cut-off of ≤14 (70/140 patients), and 60.0% for the cut-off of ≤19 (84/140 patients).

During the pre-GUSS period, 24/100 (24.0%) patients with dysphagia developed SAP, while

only 1/100 (1.0%) patients without dysphagia developed SAP (p<0.001). During the GUSS

period, 17/69 (24.6%) patients with GUSS score ≤19 developed SAP, and only 4/70 (5.7%)

patients with GUSS score = 20 developed SAP (p=0.002). The occurrence of dysphagia

(during the pre-GUSS period) was associated with more prolonged in-hospital stay (median

20 Vs. 10 days, p<0.001), which also occurred in patients with a GUSS score ≤19 during the

GUSS period (median 19 Vs. 10.5 days, p<0.001). Multivariate logistic regression analysis

for the prediction of SAP in the pre-GUSS period revealed that dysphagia, as defined by the

10mL water test, was independently associated with a significant increase in the risk of in-

hospital SAP (OR = 15.28, 95%CI = 1.78 - 131.46, p=0.013) (Supplementary Table 2).

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 During the GUSS period, each 1-point increment in the GUSS score was independently

associated with a decreased risk of in-hospital SAP (OR = 0.89, 95%CI = 0.82 – 0.98,
Accepted Article
p=0.012) (Supplementary Table 3).

DISCUSSION

Our study failed to demonstrate a difference in the occurrence of in-hospital pneumonia in

patients with acute ischemic stroke admitted in an ASU, after the implementation of a

systematic structured bedside swallowing test (GUSS), when compared to a period when a

simple 10mL water swallowing test was systematically administered. Likewise, no

differences were found regarding in-hospital or 3-month mortality and 3-month functional

independence. Even though early systematic assessment of dysphagia is essential to identify

ischemic stroke patients at risk of developing aspiration and SAP, there are no randomized

controlled trials comparing the benefit of different dysphagia screening tests, or that the

isolated implementation of a specific dysphagia screen has a clear benefit on outcomes such

as pneumonia and mortality [10]. There are, however, several observational studies based in

stroke patients registries that show an association of early (versus late) dysphagia screen with

reduced occurrence of stroke-associated pneumonia [11,12,13]. In a small prospective

register-based study of consecutive acute stroke patients admitted to an intensive care unit,

the systematic administration of a dysphagia screen resulted in a non-significant borderline

reduction of pneumonia and did not change in-hospital mortality when compared to a period

when patients did not receive a dysphagia screen [14]. Another prospective study of acute

stroke patients showed that after incorporation of a dysphagia management protocol which

included the cough reflex test, swallowing trials and instrumental assessment of swallowing

with videofluoroscopy, the frequency of aspiration pneumonia reduced to 10%, compared to

28% in the historical control group of patients whose management was not protocol-based,

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 however these results were not adjusted for stroke severity [15]. It may be difficult to discern

the real clinical impact of the implementation of a dysphagia screening test, specifically in a
Accepted Article
setting where it integrates a complex and multidomain protocol of stroke patient

management, which is already in place in medium and high patient volume ASUs. The

assessment of dysphagia using the apparently simple 10mL water swallowing test, may

provide reliable information if administered by experienced nurses and doctors, who will

inevitably also consider other variables, such as level of vigilance, severity of neurological

deficits and ischemic lesion topography, to assess the risk of aspiration. However, some

observational studies have demonstrated that acute stroke patients who were not screened for

dysphagia have a higher risk of pneumonia [11,16], and suggested that clinical judgement

alone is inadequate for assessing the risk of aspiration and subsequent complications. Even

though the GUSS test may theoretically be associated with a decreased aspiration risk during

its administration, it has the additional advantage of providing categorized dietary

recommendations [7]. Other studies have also demonstrated the utility of the systematic

application of the GUSS test in acute stroke, and found that it could provide prognostic

information, namely concerning the occurrence of pneumonia, discharge destination,

outcome and mortality at 3 months [17], however, this was not the goal of our study.

The prevalence of dysphagia in the pre-GUSS period (50.5%) is in accordance with other

studies in which similar screening test were used [1]. The risk of aspiration assessed by

GUSS in our study (50-60%, according to the definition) is similar to the original study [7]

but also to another independent study which used the GUSS test in an ASU setting [18].

Likewise, the prevalence of SAP was similar to that reported in the literature [1,19] and was

significantly higher in patients with dysphagia or at risk of aspiration, which has also been

previously demonstrated [20]. It is interesting to note that, in our study, the predictive value

of the identification of dysphagia (using the 10mL water swallowing test) and risk of

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 aspiration (using the GUSS test) for the occurrence of SAP, was independent of admission

stroke severity, and further supports the need of a systematic dysphagia screening
Accepted Article
administered by experienced professionals. Prevention of SAP is not solely dependent on the

correct identification of dysphagia, because even with correct dietary recommendations,

transient “nil per os” order or nasogastric tube insertion, pneumonia may still occur. Other

important factors such as head position, mobilization out of bed, circadian regime of

continuous enteric nasogastric tube feeding, experience of health personnel in feeding per

mouth, occurrence of vomiting and gastroesophageal reflux, oral hygiene and stroke-induced

immunosupression, are also involved in the pathogenesis of SAP, and must be taken into

account while designing personalized strategies to prevent respiratory infections in acute

stroke patients [21].

Our study has limitations mainly related to its population size and retrospective nature. Bias

may have been introduced by the imbalance in baseline characteristics of patients however,

missing information was not frequent. Additionally, dysphagia and the risk of aspiration as

defined by both tests were not systematically assessed using instrumental methods such as

videofluoroscopy, and we have no systematic information on which attitudes or treatments

were initiated after detection or on dysphagia follow-up.

In conclusion, the change in the method of screening dysphagia from the 10mL water

swallowing test to the GUSS test did not reduce the occurrence of in-hospital pneumonia, in-

hospital mortality, 3-month functional dependence or 3-month mortality, in ischemic stroke

patients admitted in an acute stroke unit. Despite this, the identification of dysphagia in

screening tests is an independent predictor of pneumonia after ischemic stroke.

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 ACKNOWLEDGMENTS

None
Accepted Article
SOURCES OF FUNDING

None

DISCLOSURES

The authors have no disclosures

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 Table 1. Baseline characteristics of the study population according to the inclusion period
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Pre-GUSS GUSS period p
period (n=140)
(n=204)
Age 71 (58-79) 71 (59-79) 0.754
Male sex 99 (48.5) 79 (56.4) 0.150
Hypertension 145 (42.2) 93 (66.4) 0.359
Diabetes 42 (20.6) 44 (31.4) 0.023
Dyslipidemia 111 (54.4) 67 (47.9) 0.232
Active smoking 28 (13.7) 17 (12.1) 0.669
Coronary heart disease / previous 18 (8.8) 14 (10.0) 0.712
myocardial infarction
Vertebrobasilar artery ischemic 45 (22.1) 24 (17.1) 0.263
stroke
Ischemic stroke in multiple 8 (3.9) 4 (2.9) 0.768
territories
OCSP classification
Total anterior circulation infarct 103 (50.5) 65 (46.4) 0.459
Partial anterior circulation infarct 33 (16.2) 36 (25.7) 0.030
Lacunar infarct 18 (8.8) 16 (11.4) 0.426
Posterior circulation 44 (21.6) 22 (15.7) 0.176
Undetermined 6 (2.9) 1 (0.7) 0.248
Admission NIHSS 12 (6-17) 10.5 (6-18) 0.864
Intravenous thrombolysis 128 (62.7) 101 (72.1) 0.069
Mechanical thrombectomy 13 (6.4) 27 (19.3) <0.001
Stroke etiologya
Cardioembolism 80 (41.2) 61 (45.9) 0.407
Large vessel disease 26 (13.4) 21 (15.8) 0.546
Small vessel disease 5 (2.6) 2 (1.5) 0.705
Arterial dissection 15 (7.7) 5 (3.8) 0.164
Cryptogenic 61 (31.4) 36 (27.1) 0.395
Other causes 7 (3.6) 6 (4.5) 0.776
Nasogastric tube 78 (38.2) 47 (33.6) 0.377

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 Day of nasogastric tube insertion 1 (1-2) 1 (1-2) 0.918
Percutaneous endoscopic 9 (4.4) 3 (2.1%) 0.373
gastrostomy
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Stroke-associated pneumoniab 25 (12.5) 21 (15.1) 0.490
First day of stroke-associated 3 (2-4) 3 (2-5) 0.450
pneumonia manifestations
In-hospital stay (days) 15 (9-28) 16 (10-27) 0.244
In-hospital death 16 (7.8) 11 (7.9) 0.996
Discharge to home 113 (60.4) 90 (70.3) 0.072
c
3-month functional independence 107 (54.3) 71 (51.8) 0.654
Death at 3 months 24 (11.8) 18 (12.9) 0.761

Results are presented as n (%) or median (interquartile range).

OCSP: Oxfordshire Community Stroke Project. NIHSS: National Institutes of Health Stroke
Scale
a
17 patients had incomplete investigation (10 in the pre-GUSS and 7 in the GUSS period)
b
5 patients with respiratory infection excluded from this analysis, because did not perform
thoracic imaging (4 in the pre-GUSS and 1 in the GUSS period)
c
Information missing in 10 patients (7 patients in the pre-GUSS and 3 in the GUSS period)

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 Table 2. Multivariable binomial logistic regression with stroke-associated pneumonia as the

dependent variable
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Odds Ratio (95% confidence p
interval)
Age (per 1-year increment) 1.02 (0.99-1.05) 0.251
Diabetes 0.84 (0.34-2.07) 0.706
Admission NIHSS (per 1-point 1.13 (1.06-1.20) <0.001
increment)
Partial anterior circulation infarct 0.68 (0.21-2.18) 0.514
Intravenous thrombolysis 1.23 (0.44-3.50) 0.692
Mechanical thrombectomy 1.24 (0.44-3.49) 0.687
Cardioembolism 1.22 (0.56-2.68) 0.621
GUSS period (pre-GUSS as reference) 1.40 (0.66-2.97) 0.378

NIHSS: National Institutes of Stroke Stroke Scale. GUSS: Gugging Swallowing Screen

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