Frequency and predictors of dysphagia in patients with recent small subcortical infarcts
Simon Fandler (MD)1, Thomas Gattringer (MD, PhD)1*, Sebastian Eppinger (MD)1, Kathrin Doppelhofer1, Daniela Pinter (PhD)1, Kurt Niederkorn (MD)1, Christian Enzinger (MD)1,2, Joanna Wardlaw (MD)3 and Franz Fazekas (MD)1
1 Department of Neurology, Medical University of Graz (MUG), Austria
2 Division of Neuroradiology, Vascular and Interventional Radiology, Department of Radiology, MUG
3 Brain Research Imaging Centre, The University of Edinburgh, Edinburgh, UK
*Correspondence:Thomas Gattringer, MD, PhD
Department of Neurology, MUG
Auenbruggerplatz 22, A-8036 Graz, Austria
Phone: 0043/316/385-80231
Mail:
Cover title: Dysphagia in subcortical infarcts
Table: 1,figure: 1
Key words:Stroke, Lacunar; Dysphagia; Swallowing; Magnetic Resonance Imaging
Word count:2000
Abstract
Background and Purpose
Detailed data on the occurrence of swallowing dysfunction in patients with recent small subcortical infarcts (RSSI) in the context of cerebral small vessel disease is lacking. This prompted us to assess the frequency of and risk factors for dysphagia in RSSI patients.
Methods
We identified all inpatients with MRI-confirmed RSSI between January, 2008 and February, 2013. Demographic and clinical data were extracted from our stroke database and MRI scans were reviewed for morphologic changes. Dysphagia was determined according to the Gugging Swallowing Screen.
Results
We identified 332 patients with RSSI (mean age: 67.7±11.9 years, 64.5% male). Overall, 83 patients (25%) had dysphagia, whichwas mild in 46 (55.4%), moderate in 26 (31.3%) and severe in 11 patients (13.3%).The rate of dysphagia in patients with supratentorial RSSI was 20%. Multivariate analysis identifieda higher NIHSSscore (p<0.001), pontine infarction (p<0.01) andmore severe white matter hyperintensities(WMH; Fazekasgrades 2 and 3, p=0.03) as risk factors for swallowing dysfunction.
Conclusions
Dysphagia is present in a quarter of patients with RSSI and has to be expected especially in those with higher stroke severity, pontine infarction and severe WMH.
Introduction
Attention to swallowing impairment is important as it may lead to serious complicationsand has been identified as an independent predictor of stroke outcome.1,2
Dysphagia is commonly expected to occur in patients with severestroke and large infarct size.1,3Brainstem infarction represents another risk factor for swallowing dysfunction.4However, to what extent dysphagia occurs in subcortical infarction and especially stroke from presumed cerebral small vessel disease (cSVD) is still largely unknown.
cSVD-related stroke is characterized by recent small subcortical infarcts (RSSI; formerly often termed as “lacunar infarction”).5Many anatomical structures/pathways associated with swallowing functionare located in subcortical regions,6and may not only be disrupted by a RSSI but also by co-existing morphologic damage such as lacunes, white matter hyperintensities (WMH) and microbleeds.
We thereforesought to assess the frequencyand severity of dysphagia in a large group of patients with MRI-confirmed RSSI and to identify clinical and morphological predictors of disturbed swallowing.
Methods
RSSI identification came from a previous neuroimaging study7where we hadsearched the medical documentation system of our primary and tertiary care university hospital for inpatients with the discharge diagnoses ‘cerebral infarction’ from January 1, 2008 to February 5, 2013. Of 4118 identified patients, brain MRI had been performed in 3363 patients. Two experts independently reviewed these MRI examinations for selection criteriabased on the STandards for ReportIng Vascular changes on nEuroimagingconsensus criteria of RSSI.8Patients were excluded if their scans showed multiple acute subcortical infarcts, additional acute infarcts in other locations, or other acute intracranial lesions.
We extracted all information from the medical records including the assessment of swallowing function according to the “Gugging Swallowing Screen” (GUSS).9Severity of dysphagia was graded as absent (20 GUSS points), mild (15-19 points), moderate (10-14 points) and severe (≤9 points).10The median delay from stroke onset to first GUSS was one day (range 0-9). We always used the first documented score. Three patients with preexisting dysphagia were excluded from the analysis. The MRI scans were interpreted for the presence of old lacunar and cortical infarcts, microbleeds and WMH severity11blinded to the clinical data. The Ethics Committee of the Medical University of Graz approved the study.
Besides descriptive statistics, a multivariate binary logistic regression model for the occurrence of dysphagia as the dependent variable was calculated. The model was loaded with all variables demonstrating a significant difference between patients with and without dysphagia in univariate analyses. Further details about methods and statistics are available in the online-only Data Supplement.
Results
We identified 332 patients with MRI-confirmed RSSI. Demographic, clinical and MRI characteristics are shown in table 1.
83 (25.0%) patients had dysphagia. Dysphagia was mild in 46 (55.4%), moderatein26 (31.3%) and severe in 11 (13.3%) patients.
The majority of RSSI were located in thebasal ganglia including the internal capsule(n=108, 32.5%), followed bypons (n=87, 26.2%), thalamus (n=76, 22.9%) and centrum semiovale (n=61, 18.4%). Neuroimaging examples of these pre-specified RSSI locations are given in figure 1.Among the 245 patients withsupratentorial RSSI 49 (20.0%) had dysphagia.
Univariate comparisons between patients with and without dysphagia are given in table 1.Patients with dysphagia were older, had more severe strokes and more often had a pontine infarction.Patients with swallowing dysfunction also had more severe WMH (Fazekasgrades 2 and 3), while other vascular brain changes were not significantly different between the two groups. Thalamic location of the RSSI and hyperlipidemia were less frequent in patients with dysphagia.There were no associations between dysphagia and supratentorial RSSI side(left: n=28/136 versus right: n=21/109; p=0.8)nor pontine RSSI pattern (paramedian: n=19/47 versus lateral lesions: 15/40; p=0.8).
Multivariate analysis (online-only Data Supplement) identified higher NIHSS (p<0.001),pontine RSSI(p<0.01) and more severe WMH (p=0.03) as factors independently associated with dysphagia(GUSS≤19). Higher NIHSS (p=0.001) remained in the model asthe single independent risk factor for dysphagia when restricting the analysis to patients withsupratentorial RSSI.
Discussion
In our study population, a quarter of patients with RSSIoverall and 20 % of those with supratentorial infarcts had dysphagia. These rates indicate the necessity for at least a bedside screening for swallowing dysfunction also in patients with RSSI/lacunar stroke syndromes to avoid potentially severe complications like aspiration and pneumonia.12
Although studies investigating dysphagia specifically in RSSI patients in the context ofcSVDare lacking, our results lie in the range of studies with less stringent infarct definitions.3,13However, different methods used to test for dysphagia, variable infarct definitions and small sample sizes prohibit a more detailed comparison.We also confirm previous findings showing that pontine infarct location and stroke severity are strong predictors for dysphagia.2,4,14
Dysphagia in subcortical stroke may be caused by damage to various structures including the corticonuclear tracts,extrapyramidal pathways, periventricular connections of cortical regionsand others. Widely distributedmorphologic changes fromcSVD(such as lacunes, microbleedsand WMH)may thus have a high chance to become a contributing factor. Our finding that more severe WMH represent an independent predictor of dysphagiain patients with RSSI supports this assumption. However, this association was lost when restricting our analysis to patients with supratentorial stroke. This may indicate that preservedintegrity of supratentorial networks is specificallycritical regarding the preservation of swallowing function in patients with brainstem RSSI. Another explanation might be a lack of statistical power when excluding patients with pontine infarction from the analysis. Statistical power might have also been too low to show an association of dysphagia with other SVD markers despite our overall large patient group.
The retrospective identification of RSSI patients for this study could be viewed as a limitation although the GUSS has been applied in every patient prospectively. Alsoinvestigated patients should be representative of patients with RSSI as our center receives all stroke patients from a defined catchment area and the study period was five years.It has to be conceded, however, thateven though diagnosing dysphagia through clinical testing has been shown to be effective and the GUSS represents a well-validated clinical instrument,9instrumental testing such as fiber-endoscopic evaluation of swallowingmighthave yielded even higher rates of dysphagia.1Also, a more detailed analysis of the impact of lesion topography for supratentorial RSSI on the occurrence of dysphagia appears warranted and is underway.
This work received no funding.
On behalf of all authors, the corresponding author states that there is no conflict of interest.
The authors have nothing to disclose relating to this article.
References
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Table 1:Demographic, clinical and radiological data in dysphagia and non-dysphagia RSSI patients
Variable / Study population / Dysphagia / Nodysphagia / p-value
n=332 / n=83 (25.0%) / n=249 (75.0%)
Demographicandclinicaldata
Meanage(years) / 67.7 (±11.9) / 70.2 (±9.9) / 66.8 (±12.5) / 0.01
Male sex, n, % / 214 (64.5%) / 58 (70.0%) / 156 (62.6%) / 0.23
Median NIHSS / 3 (range 0-13) / 4 (range 0-13) / 2 (range 0-9) / <0.0001
NIHSS 0-4 / 263 (79.2%) / 48 (57.8%) / 215 (86.3%) / <0.0001
NIHSS ≥5 / 69 (20.8%) / 35 (42.2%) / 34 (13.7%) / <0.0001
Vascularriskfactors
Hypertension / 282 (84.9%) / 75 (90.4%) / 207 (83.1%) / 0.10
Hyperlipidemia / 197 (59.3%) / 41 (49.4%) / 156 (62.7%) / 0.03
Smoking / 97 (29.3%) / 20 (24.1%) / 77 (30.9%) / 0.25
Diabetes / 93 (28.0%) / 28 (33.7%) / 65 (26.1%) / 0.19
Previousstroke / 73 (22.0%) / 22 (26.5%) / 51 (20.5%) / 0.25
RSSI location
Basal ganglia / 108 (32.5%) / 28 (33.7%) / 80 (32.1%) / 0.79
Pons / 87 (26.2%) / 34 (41.0%) / 53 (21.3%) / <0.001
Thalamus / 76 (22.9%) / 9 (10.8%) / 67 (26.9%) / <0.01
Centrum semiovale / 61 (18.4%) / 12 (14.5%) / 49 (19.7%) / 0.28
Concomitant MRI findings
Microbleeds / 108 (34.1%) / 32 (40.5%) / 76 (31.9%) / 0.17
WMH Fazekas 0-1 / 144 (43.4%) / 28 (33.7%) / 116 (46.6%) / 0.04
WMH Fazekas 2-3 / 188 (56.6%) / 55 (66.3%) / 133 (53.4%) / 0.04
Lacunes / 141 (42.5%) / 40 (48.2%) / 101 (40.6%) / 0.22
Old corticalinfarcts / 57 (17.2%) / 17 (20.5%) / 40 (16.1%) / 0.36
Abbreviations: RSSI=recent small subcortical infarct, NIHSS=National Institutes of Health Stroke Scale, MRI=magnetic resonance imaging, WMH=white matter hyperintensities
Figure 1:Examples for the four different RSSI locations ondiffusion-weighted MRI: basal ganglia/internal capsule (A), pons (B), thalamus (C) and centrum semiovale (D)
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