Incidence and Risk Factors for Dysphagia Following Cerebellar Stroke: A Retrospective Cohort Study

doi:10.21203/rs.3.rs-2478193/v1

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Research Article

Incidence and Risk Factors for Dysphagia Following Cerebellar Stroke: A Retrospective Cohort Study

https://doi.org/10.21203/rs.3.rs-2478193/v1

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published 19 May, 2023

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The cerebellum is known to play a supportive role in swallowing-related functions, however, wide discrepancies about the incidence rate of swallowing disorders following cerebellar strokes exist within the literature. This study aimed to investigate the incidence rate of dysphagia and the factors which may affect the presence of dysphagia and clinical recovery in individuals diagnosed with cerebellar stroke. A retrospective chart audit of 1651 post-stroke patients (1049 males and 602 females) admitted with a cerebellar stroke to a tertiary comprehensive hospital in China was conducted. Data of demographics, medical, along with swallowing function assessment were collected. Differences between dysphagic and non-dysphagic groups were evaluated using t-tests and Pearson’s chi-square test. Univariate logistic regression analysis was performed to establish factors associated with the presence of dysphagia. A total of 11.45% of participants were identified with dysphagia during inpatient admission. Individuals with mixed types of stroke, multiple lesions in the cerebellum, and ages older than 85 years old were more likely to develop dysphagia. Moreover, the prognosis of dysphagia following a cerebellar stroke was associated with lesions in different parts of the cerebellum. The cumulative recovery rate from the best to worse was: the right hemisphere group, the cerebellum vermis or peduncle group, both the hemisphere group and the left hemisphere group respectively.

Dysphagia

Cerebellar Stroke

Incidence Rate

Prognosis

The cerebellum, located in the lower portion of the brain and occupies about one-eighth of the intracranial space, has less than 10% stroke incidence among all strokes[1,2]. Approximately, 2%-3% of all ischemic strokes and 10%-15% of all intracerebral hemorrhages occur in the cerebellum [1,3]. Several studies reported that lesions in the cerebellum did not contribute to the presence of dysphagia[4–8]. However, one cohort study reported that seven of the eleven subjects presenting with a lesion to the cerebellum exhibited aspiration in the swallow evaluation[9]. Previous studies also reported that pathology affecting the cerebellum could impair swallowing physiology both in the oral and pharyngeal phases[10–12]. Meanwhile, findings of the cerebellum in controlling swallowing in studies using brain imaging techniques are also not consistent. Some studies demonstrated that the cerebellum participated in the control of swallowing[13–17], and other studies reported that the cerebellum was not activated during the deglutition process[18,19].

Recent evidence support that the cerebellum acts to modulate the cerebral motor cortical areas and ensure accurate, smooth and coordinated muscular activity [10]. The cerebellum has recently become a focus of interest in treating dysphagia in the field of neuromodulation[20,21]. Evidence suggested that cerebellar repetitive transcranial magnetic stimulation(rTMS) could reverse the suppressed activity in the cortical swallowing system, facilitate corticobulbar pathways to the pharynx and restore swallowing function in healthy adults[22,23]. Moreover, evidence revealed that cerebellar transcranial magnetic stimulation (TMS) could intensify cortical firing for swallowing and evoke motor responses in the pharynx for patients with dysphagia[15,20,22,24]. Swallow function was modulated through rTMS/TMS indicated that the cerebellum has connections with cortical, subcortical, brainstem and peripheral structures, through which the cerebellum may regulate the neuron related to swallowing and organize the coordinated sequence of muscle activity during the swallowing process [10,13,15,16,25]. This evidence supports the theory that the cerebellum may complement cortical and brainstem control for swallowing, intensifying neural responses and coordinating selective attention to aid the execution of generated in the cortex, plays an important role in feed-forward mechanisms, and controlling timing, sequencing, feedback, and internal coordination for sensory input and motor outputs of oral-lingual and pharyngeal musculature during deglutition [10,15,26]. The role of the cerebellum in deglutition has become increasingly evident.

Nevertheless, the data focused on cerebellar lesions is limited, and the exact nature of this role is still under-explored. Lesions in the cerebellum were testified to disrupt the motor modulatory influence on cerebral motor cortical areas and develop swallowing disorders[27,28]. However, the incidence of dysphagia after a cerebellar stroke reported in the previous literature varies greatly from 0–63%. And the risk factors for dysphagia, such as demographic characteristics, lesioned locations, ischemic or hemorrhagic stroke, and the evolution of dysphagia are still not fully understood[5,15,29]. Although studies demonstrated that patients with cerebellar stroke had favorable outcomes, those patients with dysphagia would have less favorable outcomes, increased mortality, and a longer stay in healthcare facilities with higher institutionalization rates at 3 months post stroke[30–32]. During decades of clinical practice and research on people with dysphagia, the authors’ team also found that some cases with pure lesions in the cerebellum could relieve swallowing difficulties while others with pure lesions in the cerebellum had less benefit from the existing intervention for dysphagia and had a poor prognosis(included in this retrospective study), which drew our attention of the potential relationship between the dysphagia and the lesions in the cerebellum (i.e. right/left cerebellum, bilateral cerebellum, vermis, and peduncle).

Therefore, this study aims to investigate the incidence of dysphagia and risk factors potentially influencing the risk of developing dysphagia after a cerebellar stroke from a retrospective cohort. We preliminarily speculated that the cerebellum had a role in the regulation of swallowing function, and there might exist a dominant region of swallowing function in the cerebellum, which once is damaged, dysphagia might be irrecoverable.

Research Design

A retrospective chart review of the medical records of post-stroke patients who were hospitalized in Shanghai Yueyang Hospital of Integrated Traditional Chinese and Western Medicine Affiliated to Shanghai University of Traditional Chinese Medicine (YY Hospital) in China between January 2014 and May 2021 (8-year period) was conducted. Post-stroke patients admitted to YY Hospital involves those who have an acute onset of stroke, look for rehabilitation service, and are readmitted for promoting health with integrated western and traditional Chinese medicine. The study was approved by the medical ethics committee of YY Hospital.

Study Population

The World Health Organization ICD-10 diagnostic code ‘I63.904-cerebellar infarction’ or ‘I61.401-cerebellar hemorrhage’, in addition to CT or MRI reports demonstrating lesions in the cerebellum were used to identify all appropriate cases in the digital medical records system. A total of 2673 cases were identified and were further screened by two researchers. A binary rating of “+/-” was used to identify dysphagia (“+”) or no dysphagia (“-”) resulting from the lesions in the cerebellum.

The inclusion criteria of dysphagia resulting from the lesions in the cerebellum (“+”) were as follows: 1) the first onset of a cerebellar stroke, and dysphagia was reported after assessing with the videofluoroscopic swallowing study (VFSS) and/or the fiberoptic endoscopic evaluation of swallowing (FEES) by a speech-language pathologist (SLP) after admission; 2) the first onset of a cerebellar stroke, with stroke history but without lesions in the cerebellum and without dysphagia records in the medical record (the results of the previous Kubota water swallowing test were grade 1)[33,34], and dysphagia was reported in the acute phase after assessing with VFSS and/or FEES by a SLP after admission; 3) in the subacute or chronic stage of a cerebellar stroke with the first onset, with dysphagia records during the previous hospitalization in other hospitals (the results of the previous Kubota water swallowing test ranged from grade 3 to grade 5, and the patient wore a nasogastric tube on admission), and dysphagia was reported after assessing with VFSS and/or FEES by a SLP after current admission.

The inclusion criteria of no dysphagia resulting from the lesions in the cerebellum (“-”) were as follows: 1) the first onset of a cerebellar stroke and no dysphagia (grade 1) was reported through the Kubota water swallowing test by a physician; 2) the first onset of a cerebellar stroke, with stroke history but without lesions in the cerebellum and without dysphagia records in the medical record (the results of the previous Kubota water swallowing test were grade 1), and no dysphagia was reported through the Kubota water swallowing test by a physician; 3) in the subacute or chronic stage of a cerebellar stroke with the first onset, without dysphagia records during the previous hospitalization in other hospitals (the results of the previous Kubota water swallowing test were grade 1), and no dysphagia was reported through the Kubota water swallowing test by a physician.

The exclusion criteria were as follows: 1) presence of swallowing difficulties before the first onset of cerebellar stroke; 2) the first onset of a cerebellar stroke, but with other lesion sites outside the cerebellum that were involved in the normal swallowing process [6,18]; 3) unable to receive bedside swallowing examination by a SLP due to severe physical and cognitive impairment; 4) repeated admission. A total of 1651 participants were finally eligible for inclusion in the data analysis.

Data Collection

Data abstraction was conducted according to the methodological guidelines to promote the internal validity and reproducibility of the study[35]. Two reviewers reviewed all of the medical charts independently to ensure consistency of data collection and to ensure validity and reliability[36]. Due to the complexity of some data collection and analysis, a discussion team including a physician, a radiologist, and an SLP was formed to make the final decision: patients with dysphagia following a cerebellar stroke combined with other lesions in the brain were excluded from this study, since dysphagia might not be induced by the cerebellar stroke. However, patients who had the first onset of a cerebellar stroke with other lesions in the brain and reported not having dysphagia after water swallowing screening, would be identified as without dysphagia following a cerebellar stroke.

Data obtained in this study included age, gender, type of stroke (i.e. ischemic or hemorrhage), lesion sites in the cerebellum, date of the first onset of a cerebellar stroke and discharge from hospital of that hospitalization, results of swallowing function assessments at the first onset of a cerebellar stroke and discharge from hospital of that hospitalization. In order to learn the prognosis of dysphagia following cerebellar strokes, the research team made a follow-up for all the participants who were recorded with dysphagia following the cerebellar stroke by telephone and inquired about their current swallowing function status in November 2021. Therefore, data were collected at three points: the first onset of cerebellar stroke, discharge from YY hospital, and follow-up by telephone in November 2021.

Data Analysis

All collected data were entered into a Microsoft Excel spreadsheet. Descriptive statistics were used to establish the mean (standard deviation [SD]) for continuous variables with normal distribution or median (interquartile range [IQR]) for those with non-normal distribution. Categorical variables were reported as a frequency (percentage). The two groups (dysphagia at discharge vs. dysphagia at follow-up point) were compared using Pearson’s chi-square test for binary variables. Due to the retrospective nature of this study, data for all variables were not available. When sufficient detail was lacking or data were unreported, a percentage of ‘lost’ was reported. Logistic regression analysis was performed to evaluate predictive risk factors with a positive report of dysphagia as the primary outcome variable. The possible risk factors included age, gender (male/female), type of stroke, and lesion locations in the cerebellum. The results of logistic regression analyses were recorded as odds ratio (OR), 95% confidence interval (CI), and p-value. Cumulative recovery of dysphagia in different risk factors groups from the final follow-up point back to the first onset point was visually depicted by survival curves. We performed all analyses using SPSS software version 25.0, and two-sided statistical significance was defined as p < 0.05.

A total of 1651 post-stroke individuals with lesions in the cerebellum were enrolled in this study, including 1049 male participants and 602 female participants with a mean age of 73.10 (SD = 11.61) years. The majority type of stroke was ischemic stroke (n = 1535, 92.97%). The most to least lesions in the cerebellum were right cerebellum alone (n = 599,36.28%), left cerebellum alone (n = 540, 32.71%), both the right and left cerebellum (n = 382, 23.14%), and cerebellar vermis or peduncle (n = 26, 1.57%). There was a significant difference between the male and female groups based on age (p < 0.05) and none for all other variables. Table 1 summarizes the baseline characteristics of the study population.

Table 1

The demographic feature among patients with stroke in Yueyang Hospital of Shanghai, China
Variables	Total patients (n = 1651)	Male patients (n = 1049)	Female patients (n = 602)
Age (years)*, (mean, SD)	73.10 (11.61)	70.92 (11.48)	76.89 (10.84)
Age (years)*, (median, IQR)	74.00 (65.00, 83.00)	71.00 (63.00, 80.00)	79.00 (70.00, 85.00)
Age groups (years)*, n (%)
Less than 65	401 (24.29)	318 (30.31)	83 (13.79)
65–75	455 (27.56)	313 (29.84)	142 (23.59)
76–85	498 (30.16)	286 (27.26)	212 (35.22)
Over 85	297 (17.99)	132 (12.58)	165 (27.41)
Type of stroke, n (%)
Ischemic stroke	1535 (92.97)	969 (92.37)	566 (94.02)
Hemorrhagic stroke	83 (5.03)	60 (5.72)	23 (3.82)
Mixed stroke	33 (2.00)	20 (1.91)	13 (2.16)
Lesion location of stroke, n (%)
Left cerebellum	540 (32.71)	352 (33.56)	188 (31.23)
Right cerebellum	599 (36.28)	371 (35.37)	228 (37.87)
Left and right cerebellum	382 (23.14)	238 (22.69)	144 (23.92)
Cerebellar vermis and peduncle	26 (1.57)	15 (1.43)	11 (1.83)
Mixed (at least 3 lesion location)	104 (6.30)	73 (6.96)	31 (5.15)
Dysphagia induced by cerebellar injury, n (%)
Yes	189 (11.45)	116 (11.06)	73 (12.13)
No	1462 (88.55)	933 (88.94)	529 (87.87)
Dysphagia at discharge,n(%)
Yes	128 (67.72)	77 (66.38)	51 (69.86)
No	43 (22.75)	27 (23.28)	16 (21.92)
Lost to follow-up	18 (9.52)	12 (10.34)	6 (8.22)
*: the differences between male and female patients on demographic feature was statistically significant (P < 0.05)
SD: standard deviation
IQR: Interquartile Range

Incidence Of Dysphagia Following A Cerebellar Stroke

The overall incidence of dysphagia induced by a cerebellar stroke was 11.45% (n = 189), and the incidence of that in males and females was 11.06% (n = 116) and 12.13% (n = 73) respectively. At the point of discharge from the hospital, 67.72% (n = 128) of overall participants with dysphagia during admission reported remained dysphagia, 22.75% (n = 43) of these patients reported recovery from dysphagia, and 9.52% (n = 18) of these patients’ relevant information of dysphagia could not be found (see Table 1).

Factors Potentially Influencing The Risk Of Developing Dysphagia Following A Cerebellar Stroke

Ischemic and/or hemorrhagic strokes, lesion location in the cerebellum and age were risk factors for dysphagia in the univariate model. Patients with mixed stroke (OR = 3.00, 95% CI: 1.02–8.83) and mixed (at least 3) lesion locations (OR = 2.16, 95% CI: 1.19–3.90) were associated with higher odds ratios of dysphagia. Moreover, patients with ages older than 85 (OR = 2.53, 95% CI: 1.58–4.07) had a significantly higher odds ratio for dysphagia compared to other age groups (Table 2).

Table 2

The dysphagia induced by cerebellar injury among patients with stroke in Yueyang Hospital of Shanghai, China
Variables	Percentage of dysphagia in stroke patients, n (%)	Uni-variate Logistic Regression
Variables	Percentage of dysphagia in stroke patients, n (%)	OR	95% CI
Type of stroke, n (%)
Hemorrhagic stroke	8 (9.64)	1.00	-
Ischemic stroke	173 (11.27)	1.19	0.57–2.51
Mixed stroke*	8 (24.24)	3.00	1.02–8.83
Lesion location of stroke, n (%)
Left and right cerebellum	38 (9.95)	1.00	-
Left cerebellum	64 (11.85)	1.22	0.80–1.86
Right cerebellum	63 (10.52)	1.06	0.69–1.63
Cerebellar vermis and peduncle	4 (15.38)	1.65	0.54–5.03
Mixed (at least 3 lesion location)†	20 (19.23)	2.16	1.19–3.90
Sex, n (%)
Male	116 (11.06)	0.90	0.66–1.23
Female	73 (12.13)	1.00	-
Age groups (years) *, n (%)
Less than 65	31 (7.73)	1.00	-
65–75	52 (11.43)	1.54	0.97–2.46
76–85	54 (10.84)	1.45	0.91–2.31
Over 85	52 (17.51)	2.53	1.58–4.07
* the differences between stroke patients with and without dysphagia was statistically significant (P < 0.05)
OR: Odds Ratio
CI: Confidence Interval

Recovery Of Dysphagia Following Stroke With Lesions In Cerebellum

Table 3 shows the dysphagia condition of participants during admission (n = 189) at the point of hospital discharge and follow-up in September 2021. Dysphagia conditions in different lesions in the cerebellum at the point of hospital discharge were significantly different, and so were the dysphagia conditions at different ages at the point of follow-up in September 2021. Other variables at the two points had no statistical difference (Table 3). Figure 1 demonstrates the case frequency of patients with dysphagia (n = 189) every 10-months follow-up. Looking back from September 2021, the greater number of case frequencies occurred in the closer follow-up time (Mean = 45.31, SD = 37.64), and fewer case frequencies with the increased follow-up time.

Table 3

The dysphagia condition among stroke patients in different follow-up times in Yueyang Hospital of Shanghai, China (n = 189)
Variables	Dysphagia at discharge			Dysphagia at time of follow-up in year of 2021
Variables	Lost	Yes	No	Lost	Yes	No
Sex, n (%)
Male	12 (10.34)	77 (66.38)	27 (23.28)	66 (57.39)	33 (28.70)	16 (13.91)
Female	6 (8.22)	51 (69.86)	16 (21.92)	51 (69.86)	15 (20.55)	7 (9.59)
Age groups (years)*, n (%)
Less than 65	1 (3.23)	20 (64.52)	10 (32.26)	12 (40.00)	11 (36.67)	7 (23.33)
65–75	5 (9.62)	35 (67.31)	12 (23.08)	30 (57.69)	13 (25.00)	9 (17.31)
76–85	8 (14.81)	37 (68.52)	9 (16.67)	32 (59.26)	16 (29.63)	6 (11.11)
Over 85	4 (7.69)	36 (69.23)	12 (23.08)	43 (82.69)	8 (15.38)	1 (1.92)
Type of stroke, n (%)
Ischemic stroke	18 (10.40)	113 (65.32)	42 (24.28)	110 (63.95)	41 (23.84)	21 (12.21)
Hemorrhagic stroke	0 (0.00)	7 (87.50)	1 (12.50)	2 (25.00)	5 (62.50)	1 (12.50)
Mixed stroke	0 (0.00)	8 (100.00)	0 (0.00)	5 (62.50)	2 (25.00)	1 (12.50)
Lesion location of stroke**, n (%)
Left cerebellum	5 (7.81)	45 (70.31)	14 (21.88)	38 (60.32)	19 (30.16)	6 (9.52)
Right cerebellum	3 (4.76)	38 (60.32)	22 (34.92)	41 (65.08)	10 (15.87)	12 (19.05)
Left and right cerebellum	7 (18.42)	26 (68.42)	5 (13.16)	24 (63.16)	11 (28.95)	3 (7.89)
Cerebellar vermis and peduncle	0 (0.00)	3 (75.00)	1 (25.00)	1 (25.00)	2 (50.00)	1 (25.00)
Mixed (at least 3 lesion location)	3 (15.00)	16 (80.00)	1 (5.00)	13 (65.00)	6 (30.00)	1 (5.00)
**: the differences at discharge was statistically significant (P < 0.05)
*: the differences in follow-up in the year of 2021 was statistically significant (P < 0.05)

ROC analysis was completed to evaluate the recovery trend of dysphagia resulting from a cerebellar stroke. Four curves represented the influence of age, gender, ischemic and/or hemorrhagic strokes and lesions in the cerebellum on the recovery of dysphagia. The overall cumulative recovery rate of dysphagia due to a cerebellar stroke in the male group is higher than that in the female group. With the age increased, the cumulative recovery rate became lower. Patients in the hemorrhagic group recovered quicker than those in the ischemic and mixed group, and the number of patients who recovered from dysphagia was greater than that in the ischemic and mixed group. The cumulative recovery rate from the best to worse was: the right hemisphere group, the cerebellum vermis or peduncle group, both the hemisphere group and the left hemisphere group respectively (Fig. 2).

A growing body of literature has investigated the incidence of dysphagia in people with cerebellar strokes, and the role of the cerebellum in swallowing. As previously mentioned, the findings from such studies were inconsistent [6, 8, 11, 12, 37]. The incidence rate of dysphagia identified in this study was 11.45%, which supported the evidence that lesions in the cerebellum could induce dysphagia[11, 12, 37]. The discrepancy in the incidence rate of dysphagia secondary to cerebellar strokes may be because the cerebellum is not a part of the primary motor swallowing pathway, but an adjunctive force to enhance oropharyngeal muscle[27]. The representations of swallowing musculature occur in multiple locations over the cerebellum, isolated damage to the cerebellum may cause an element of incoordination of swallowing muscular activity[27]. The cerebellum can influence other swallowing circuits, not just the fine-tuning of distantly initiated motor activity, but also the generation of a hypothetical internal model of motor activity immediately prior to movements being initiated to allow movements to be compared and adjusted against this internal ideal[26,27,38]. The incidence rate identified in the current study still supports the need for timely referral for swallowing assessment by SLPs for individuals admitted with cerebellar stroke.

Multiple lesions in the cerebellum were related to an increased risk of dysphagia in this study (Table 2), which corroborated with the finding that cumulative damage to the brain (either from the current or a previous lesion) was more likely to cause dysphagia and would limit the functional reserve and possibility of recruitment of compensatory neural networks [39–42]. However, lesions in the bi-hemisphere, left hemisphere, right hemisphere, vermis and peduncle did not show any statistical difference in developing swallowing disorder. Previous studies reported that TMS stimulation at each cerebellar hemisphere could increase pharyngeal motor activities, but bi-hemispheric cerebellar stimulation was more effective than unilateral cerebellar stimulation[23]. This observation might due to the fact that both cerebellar hemispheres could send impulses to contralateral cortical motor areas via dentate nuclei whose axons exit the cerebellum through the superior cerebellar peduncle[27, 28, 43, 44]. Meanwhile, fastigial nuclei in each cerebellar hemisphere could send projections to the central pattern generator, and then connect to the higher swallowing centers in the cortex[25, 27, 45]. Besides, there is evidence suggesting that TMS stimulation at the midline vermis could facilitate the pharyngeal motor responses[13, 22, 24, 43]. In addition, the evidence demonstrated that three peduncles, attaching the cerebellum to the brainstem, could influence the activity in the brainstem and the motor cortices [44]. Therefore, our result might imply that both hemispheres of the cerebellum, the vermis and peduncles were involved in the swallowing process, which was in line with the above evidence.

A mixed type of cerebellar stroke was shown to be independently associated with an increased risk of dysphagia in the current study, which was consistent with the report that recurrent stroke was a predictive factor for worsened conditions in post-stroke patients [46,47]. There was no statistical difference between ischemic type and hemorrhagic type, but the incidence rate of ischemic type was higher than hemorrhagic type, which was in line with the finding that varying degrees of swallowing impairment were prevalent in ischemic type[1,48]. The difference in age between patients with and without dysphagia had statistical significance and ages older than 85 years old were an independent factor for a higher possibility of dysphagia in the logistic regression model. This result was similar to the evidence that older age is one of the potential risk factors for swallowing disorders after strokes [49, 50]. Therefore, special attention is needed when assessing swallowing problems in patients of older age and with mixed types of cerebellar stroke[7].

The rate of presence of dysphagia on discharge from the hospital was 67.72% in this study, which was similar to a previous finding that 66.29% of patients with dysphagia on admission would discharge with dysphagia[42]. Moreover, our results indicated that lesions in the cerebellum and the age of the patient were correlated with the presence or absence of dysphagia on discharge and in November 2021 respectively, which were consistent with the suggestion that lesioned locations had a relevant effect on swallowing dysfunction[13, 51]. Moreover, the dysfunction courses for patients with dysphagia (n = 189), tracing back from November 2021 to the first month of dysphagia onset, showed that the mean course of dysphagia was about 3.8 years, the longest course was 20.8 years, and the course of most recruited patients in this study was less than the mean course. To our knowledge, a large number of patients lost in this study was due to different causes of death after stroke, which was similar to the report that dysphagia had a large impact on survival and clinical recovery after strokes, and the mortality for post-stroke dysphagia ranged from 20–37%[30,42.52-54]. However, one study demonstrated that death attributed to stroke-associated dysphagia mostly occurs during the hospital stay and the first 90 days after a stroke episode[42], which was not consistent with our result that more patients lost in the follow-up point of November 2021(n = 117) than on discharge(n = 18).

Several potential factors may influence the clinical recovery from dysphagia. As for gender, more male participants were recruited in this study than female, which corroborated with the report that the prevalence rate of stroke was higher among men than women in the Chinese population[54]. Male patients were found to have a better recovery than female patients, which was consistent with the finding that female was associated with prolonged dysphagia and increased death[30, 50, 55]. Besides, increased age was shown to have poorer recovery from dysphagia, which was consistent with the advocate that the elder had reduced cognitive function and decreased ability to compensate for changes in skeletal muscle strength, and these factors could affect the outcome of post-stroke swallowing impairment[29,48,49,55–58]. However, the above findings were not consistent with the result from one previous study that age and sex were not significant predictors of persistent dysphagia[59].In addition, patients with ischemic strokes were reported to have poorer recovery than those with hemorrhagic strokes since patients with ischemic strokes were more likely to have a relatively poor overall condition[60].However, our result demonstrated that the cumulative recovery of the ischemic type was better than that of the hemorrhagic and mixed type, which was not consistent with the previous studies[60].

The recovery rate of the lesions in the cerebellum from best to worst was right cerebellum, vermis or peduncle, bilateral cerebellar hemisphere, and left cerebellum in this study. Several studies revealed that the left hemisphere, bilateral superior and posterior portions of the cerebellum was correlated with swallowing function[14, 16, 61, 62]. Damage to the left cerebellum and deep cerebellar nuclei was reported to be more likely to affect the severity of dysphagia in patients with the isolated cerebellar lesion, though the association between lesioned locations and dysphagia was not statistically significant [10]. A PET study involving eight healthy participants showed that the cerebellar hemispheres and the cerebellar vermis were activated during swallowing, with noticeably strong activation in the left cerebellar hemisphere[62]. One case study reported that delayed swallow initiation, impaired laryngeal closure, oral and hypopharyngeal residue and aspiration had been observed in a patient with a left cerebellar lesion[63]. Reduced clinical symptoms of swallowing disorders were observed collaborating with increased connectivity and the number of fibers in the left cerebellar peduncle after transcranial direct current stimulation in one patient with post-stroke dysphagia [64]. Besides, fMRI cerebellar mapping studies showed that the lips and tongue involved in swallowing were represented over the cerebellar hemispheres and vermis[65]. Cerebellar vermis rTMS was demonstrated to have a suppressive effect on pharyngeal motor cortical activity and swallowing behavior[23]. The results in the current study were in line with previous studies. Therefore, it supports the assumption that the cerebellum has a multi-limbed motor homunculus, with its surface corresponding to different body areas, however, the same muscle groups are represented multiple times in different locations over the cerebellum[23,27,65,66]; and it also supports the opinion that there may exist functional lateralization for swallowing in the cerebellum[10, 27].

Limits And Outlook

Despite this study providing promising insights into dysphagia incidence and potential risk factors following the cerebellum, there are some limitations in this study related to its retrospective design. First, among the subjects with dysphagia resulting from cerebellar stroke included in this study between 2014 and 2021, some of them participated in national research on swallowing-related topics, their swallowing function assessment (including swallowing bedside examination, VFSS and FEES, etc.) before and after treatment during hospitalization were recorded; However, the patients with routine in-patient healthcare for dysphagia mostly receive swallowing function assessment at admission, and these patients after discharge generally seldom participate in swallowing instrumenting examinations voluntarily. The SLP's bedside examination and the results of the Kubota water test were the only assessment data that existed. At the same time, the main complaints of the patient or his family are used as the basis for judging the treatment effect after discharge and follow-up time; These may affect the accuracy of the judgment on the recovery of dysphagia after cerebellar stroke. The presence of swallowing difficulties after discharge is mostly reported by the patients themselves and their family members, which may influence the accuracy of the prognosis of dysphagia following a cerebellar stroke. Second, patients who had acute medical care for the first onset of a cerebellar stroke in other hospitals, with records of dysphagia or intervention for dysphagia, or wore a nasogastric tube on admission to this hospital were also included in this study. For this population, we could only judge the presence of dysphagia before admission by reviewing medical records, and inquiring about the patient and their family member, which might lead to judgment bias without the results of VFSS/FEES. Moreover, patients who did not cough during the Kubota water swallowing test would not be referred to a SLP for VFSS/FESS, but they might have a possibility of silent aspiration. Therefore, dysphagia following a cerebellar stroke might be underdiagnosed. Third, cases with the cognitive disorder were not included in the current study so the possible impact of cognitive function on swallowing function cannot be identified. Evidence advocated that the cerebellum is involved in motor, cognition and mood, and impaired motor, cognitive and mood function resulting from injuries to the cerebellum could all affect the voluntary process of swallowing[7,10]. Thus, further studies with a prospective design supplementing the volume of lesion, the cognition are needed to allow the analysis of critical predictive factors of dysphagia in the isolated cerebellar lesion.

This study provides preliminary information regarding dysphagia incidence following cerebellar stroke, and factors that may induce swallowing difficulty and influence clinical recovery. Dysphagia can affect a substantial portion of patients in this population, and associate with patients who have both ischemic and hemorrhagic strokes, multiple lesions in the cerebellum, and increasing age. The recovery rate of the lesions in the cerebellum from best to worst was the right cerebellum, vermis or peduncle, bilateral cerebellar hemisphere, and left cerebellum. This information provides insight into the role of the cerebellum in the process of deglutition and enhances awareness of those individuals most at risk of dysphagia and poor clinical outcome.

Funding and Competing interests

This study was supported by a key program of the China National Natural Science Foundation (Grant no. 81772442), and a youth program of the Shanghai Municipal Health Bureau (Grant no. 20214Y0174).

All authors declare they have no financial interests.

The authors have no competing interests to declare that are relevant to the content of this article.

Ethics approval

Ethical approval was waived by the local Ethics Committee of Shanghai Yueyang Hospital of Integrated Traditional Chinese and Western Medicine in view of the retrospective nature of the study and all the procedures being performed were part of the routine care.

Consent to participate and Consent to publish

Informed consent was obtained from all individual participants or legal guardians included in this study.

The participants consented to the submission of their data to the journal.

Author contributions

All authors contributed to the study conception and design. The study was designed by Ping Wan, and supervised by Shan Chunlei, Juntao Yan and Ping Wan. The draft of the manuscript was written by Li Huang and Yunlu Wang. Material preparation was performed by Lequn Zhu. Data collection was performed by Li Huang, Yunlu Wang and Yuwei Wu. Data analysis was performed by Jikang Sun and Jimin Liu. All authors commented on previous versions of the manuscript, and approved the final manuscript.

Acknowledgements

The authors would like to thank all the staff who provided support for this study in Shanghai Yueyang Hospital of Integrated Traditional Chinese and Western Medicine affiliated to Shanghai University of Traditional Chinese Medicine, Professor Ruiying Ding at University of Elmhurst in the US who provided guidance for this manuscript and Dr. Ruiping Wang in Shanghai Skin Disease Hospital affiliated to Tongji University who provided advice regarding statistical analysis.

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No competing interests reported.

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Incidence and Risk Factors for Dysphagia Following Cerebellar Stroke: A Retrospective Cohort Study

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Abstract

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Introduction

Patients And Methods

Research Design

Study Population

Data Collection

Data Analysis

Results

Incidence Of Dysphagia Following A Cerebellar Stroke

Factors Potentially Influencing The Risk Of Developing Dysphagia Following A Cerebellar Stroke

Recovery Of Dysphagia Following Stroke With Lesions In Cerebellum

Discussion

Limits And Outlook

Conclusion

Declarations

References

Additional Declarations

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Journal Publication

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