Figures
Abstract
Background
Dysphagia is a common yet serious complication in stroke patients. We aimed to conduct a meta-analysis and systematic review to evaluate the risk factors of dysphagia in patients with ischemic stroke, to provide insights to the clinical treatment and nursing care of dysphagia.
Methods
We searched PubMed, Embase, Cochrane Library, Web of Science, China National Knowledge Infrastructure (CNKI) and Wanfang Database, China Biomedical Literature Database (CBM) for studies on dysphagia in patients with ischemic stroke up to January 31, 2022. The quality of the literature was evaluated using the Newcastle-Ottawa scale. Meta-analysis was performed using RevMan 5.3 software.
Results
A total of 10 studies involving 4637 ischemic stroke patients were included, 1183(25.51%) patients had dysphagia after stroke. The synthesized outcomes showed that elder age (SMD = 0.42, 95%CI:0.34–0.50), hypertension (OR = 1.96, 95%CI:1.48–2.61), diabetes (OR = 1.83, 95%CI:1.47–2.28), brainstem stroke (OR = 2.12, 95%CI:1.45–3.09) were associated with dysphagia in patients with ischemic stroke (all P<0.05). There was no significant difference in the gender between dysphagia and no dysphagia patients (OR = 1.07, 95%CI:0.91–1.27, P = 0.40). Egger regression tests indicated there were no significant publication biases in the synthesized outcomes (all P>0.05).
Citation: Yang C, Pan Y (2022) Risk factors of dysphagia in patients with ischemic stroke: A meta-analysis and systematic review. PLoS ONE 17(6): e0270096. https://doi.org/10.1371/journal.pone.0270096
Editor: Massimiliano Toscano, Universita degli Studi di Roma La Sapienza, ITALY
Received: February 24, 2022; Accepted: June 4, 2022; Published: June 16, 2022
Copyright: © 2022 Yang, Pan. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: BDST, Burke Dysphagia Screening Test; BSE, bedside assessment evaluation; CI, confidence intervals; CNKI, China National Knowledge Infrastructure; FEES, fiberoptic endoscopic evaluation of swallowing; NOS, Newcastle-Ottawa scale; OR, odds ratios; PRISMA, preferred reporting items for systematic reviews and meta-analyses; SMD, standardized mean differences; SSA, standardized swallowing assessment; VFSS, video fluoroscopy swallowing study; WST, water swallowing test
Background
Stroke has become the leading cause of death in the world, of which ischemic stroke is the most common type of stroke, accounting for about 80% stroke [1, 2]. Dysphagia is one of the common complications after stroke, the incidence of dysphagia in acute stroke patients is 34.11%-80.05% [3, 4]. Dysphagia can significantly increase the risk of aspiration, pneumonia, and prolong hospital stay in stroke patients [5, 6]. Additionally, dysphagia is an independent risk factor for malnutrition, poor functional recovery, and post-stroke depression [7]. Therefore, the prevention and treatment of dysphagia after stroke is of great significance to the quality of life and prognosis of stroke patients.
Identifying risk factors for dysphagia is critical for the prevention and treatment of dysphagia after stroke. Previous studies [8, 9] have pointed out that the occurrence of dysphagia in stroke patients is affected by many factors. Among them, age, history of cerebrovascular disease, infarction site and other important factors that may affect the occurrence of dysphagia. Besides, the patient gender and muscle strength, etc. may also affect the occurrence of dysphagia, but research results are inconsistent. At present, for the investigations and researches on dysphagia in patients with ischemic stroke, due to the differences in study population, the screening and diagnosis methods of dysphagia, the sample size and other factors, the results are also quite different. Therefore, this meta-analysis aimed to conduct a data synthesis analysis and systematic review of the current risk factors for dysphagia in ischemic stroke patients, to evaluate the risk factors for dysphagia in ischemic stroke patients, to provide evidence support for the clinical prevention, treatment and nursing care of dysphagia.
Methods
Ethical approval was not necessary since our study was a meta-analysis and systematic review. This meta-analysis was conducted and reported according to the guidelines for preferred reporting items for systematic reviews and meta-analyses (PRISMA statement) [10]. In this study, all methods were performed in accordance with the relevant guidelines and regulations.
Inclusion and exclusion criteria
The inclusion criteria for this meta-analysis were as follows: (1) The study population were patients with ischemic stroke diagnosed by head CT or MRI, and the patients were aged ≥18 years; (2) The swallowing function assessment tool was used to determine whether the patients had dysphagia. (3) cohort study or case-control study design. (4) The publication language of the article was limited to Chinese and English. The literature exclusion criteria for this meta-analysis were as follows: (1) patients with non-ischemic stroke; (2) duplicate publications; (3) studies with incomplete information or data for extraction; (4) literature with low quality.
Literature search
The two authors searched PubMed, Embase, Cochrane Library, Web of Science, China National Knowledge Infrastructure (CNKI) and Wanfang Database, China Biomedical Literature Database (CBM) for studies on dysphagia in patients with ischemic stroke. The search time limit of each database was from the establishment of the database to January 31, 2022. We combined subject terms and free terms to conduct the literature search. The search terms used in this meta-analysis were (“stroke” OR “ischemic stroke” OR “brain ischemia” OR “cerebral infarction” OR “intracranial embolism” OR “cerebral embolism”) AND (“’swallowing disorder” OR “swallowing dysfunction” OR "dysphagia").
Literature screening and data extraction
Two authors independently searched the literature according to the retrieval strategy. We initially screened the literature according to the title and abstract, and then we read the full text for re-screening and cross-checking. If there was any disagreement, it would be resolved through negotiation. The contents of the literature data extracted in this meta-analysis included the first author, study site, sample size, number of cases of dysphagia, details of dysphagia assessment methods (tools, evaluators, assessment timepoint), related risk factors for dysphagia, and research conclusions.
Methodological quality assessment
Two authors independently used the Newcastle-Ottawa scale (NOS) [11] to evaluate the quality of included studies. If any disagreements occurred during the evaluation process, they were resolved through discussion. The NOS scale evaluated the quality of the literature in three aspects: patient selection (4 items, 4 points), comparability (1 item, 2 points), and exposure assessment (3 items, 3 points). The total NOS score is 9 points, and literatures with NOS ≥ 7 points are generally considered as high-quality.
Data analysis
RevMan 5.3 software was used for statistical analyses in this meta-analysis. Binary outcomes were presented as Mantel–Haenszel-style odds ratios (OR) with 95% confidence intervals (CI). Continuous outcomes were presented as standardized mean differences (SMD). Fixed-effect model was selected in cases of homogeneity (P value of χ2 test >0.10 and I2 < 50%), and random-effect model was used in cases of obvious heterogeneity (P value of χ2 test >0.10 and I2≥50%). Publication bias were evaluated by using funnel plots, and asymmetry was assessed with Egger regression test. In this meta-analysis, P<0.05 was considered that the difference was statistically significant between groups.
Results
Study inclusion
The process of selecting studies is presented in Fig 1. The first search identified 213 potentially relevant reports. Of those identified articles, 9 reports were excluded as duplicates. After viewing the titles and abstracts of the 204 remaining reports, the full texts of 41 reports were retrieved. Among them, 31 studies were excluded with failure to meet criteria. Finally, 10 studies [12–21] were included in this present meta-analysis.
The characteristics of included studies
Of the 10 included studies [12–21], a total of 4637 ischemic stroke patients were involved, and 1183(25.51%) patients had dysphagia after stroke. As presented in Table 1, Of the 10 included studies [12–21], 4 studies were assessed for dysphagia within 24 hours of admission. The dysphagia assessment tools used in the studies mainly included standardized swallowing assessment (SSA), water swallowing test(WST), Burke Dysphagia Screening Test(BDST), video fluoroscopy swallowing study (VFSS), fiberoptic endoscopic evaluation of swallowing(FEES). The influencing factors analyzed in the 10 reports [12–21] mainly included the general demographic data, underlying diseases, disease severity, and stroke site of patients.
The quality of included studies
As indicated in Table 2, the NOS score of 3 papers was rated as 8 points, and 7 papers were rated as 7 points, the quality of the 10 included articles was generally high.
Meta-analysis
Age and dysphagia after stroke 6 studies [12, 15, 16, 18–20] evaluated the relationship between age and dysphagia, and there was no statistical heterogeneity among the studies (I2 = 0, P = 0.44). The fixed effect model was used for statistical analysis. The results showed that the risk of dysphagia was higher in stroke patients with elder age (SMD = 0.42, 95%CI:0.34–0.50, P<0.001, Fig 2).
Gender and dysphagia after stroke 5 studies [14, 16–19] evaluated the relationship between gender and dysphagia, and there was no statistical heterogeneity among the studies (I2 = 20, P = 0.28). The fixed effect model was used for statistical analysis. The results showed that the there was no significant difference in the gender between dysphagia and no dysphagia patients(OR = 1.07, 95%CI:0.91–1.27, P = 0.40, Fig 3).
Hypertension and dysphagia after stroke 3 studies [12, 14, 19] evaluated the relationship between hypertension and dysphagia, and there was no statistical heterogeneity among the studies (I2 = 0, P = 0.75). The fixed effect model was used for statistical analysis. The results showed that the risk of dysphagia was higher in stroke patients with hypertension (OR = 1.96, 95%CI:1.48–2.61, P<0.001, Fig 4).
Diabetes and dysphagia after stroke 4 studies [12, 14, 19, 20] evaluated the relationship between diabetes and dysphagia, and there was no statistical heterogeneity among the studies (I2 = 0, P = 0.99). The fixed effect model was used for statistical analysis. The results showed that the risk of dysphagia was higher in stroke patients with diabetes (OR = 1.83, 95%CI:1.47–2.28, P<0.001, Fig 5).
Brainstem stroke and dysphagia after stroke 6 studies [13–15, 19–21] evaluated the relationship between stroke site and dysphagia, and there was no statistical heterogeneity among the studies (I2 = 0, P = 0.76). The fixed effect model was used for statistical analysis. The results showed that the risk of dysphagia was higher in patients with brainstem stroke (OR = 2.12, 95%CI:1.45–3.09, P<0.001, Fig 6).
Publication of bias and sensitivity analyses
The publication of bias was evaluated with funnel plot and Egger regression test. As indicated in Fig 7, the dots in the funnel plot of synthesized outcomes were evenly distributed, and results of Egger regression test indicated there were no significant publication biases in the synthesized outcomes (all P>0.05).
Sensitivity analyses, which evaluated the impact of one single study on the overall risk estimated by removing one study in each turn, suggested that the overall risk estimates were not substantially changed by any one study.
Discussions
Stroke is a common and frequently-occurring disease of the nervous system, and it is an important cause of death or disability of residents worldwide, and the recurrence rate is high [22, 23]. According to statistics [24, 25], there are about 2 million new stroke patients in China every year, of which 22%-65% of stroke patients are accompanied by dysphagia, the incidence of dysphagia within 3 days of stroke patients is 12%-67%. Aspiration occurs in 10% of patients with dysphagia, and 33% of patients with dysphagia can develop pneumonia, which significantly increased the risk of death [26]. However, many screenings especially bedside assessment evaluation (BSE) are focused on dysphagia without considering aspiration and vice-versa. It’s been reported that dysphagia may occur without aspiration [27]. Conversely, high sensitive BSEs designed to detect also aspiration and tested against the FEES [28–30] are more likely to depict the real situation, thus being more useful to design studies on post-stroke aspiration prevention. Therefore, in clinical work, it is important to identify the risk factors for dysphagia to prevent and treat dysphagia after stroke. The results of this meta-analysis suggest that age, hypertension, diabetes, and brainstem stroke are independent risk factors for dysphagia in patients with ischemic stroke, early targeted prevention and nursing care are needed for those patients in clinical settings.
Previous studies [31–33] have pointed out that dysphagia after stroke is mainly caused by damage to the swallowing cortex center, cortical descending fibers, medulla oblongata swallowing center and extrapyramidal system. The physiological process of dysphagia includes cognitive and psychological disorders, organic lesions and functional abnormalities. The primary lesions of dysphagia after stroke are located in both cerebral cortex or brainstem tracts [34]. Swallowing disorders can occur in all stages from the cognitive stage to the esophageal stage [35]. Patients will experience prolonged oral passage time and pharyngeal swallowing delay, and they are prone to aspiration before and during swallowing [36]. Treatment and nursing care of patients with dysphagia after stroke is a holistic process from swallowing assessment to rehabilitation, emphasizing multidisciplinary participation and comprehensive training [37–39]. The assessment of dysphagia after stroke should be based on the clinical manifestations of patients, and fully consider the advantages of assessment methods, so as to improve the accuracy and effectiveness of dysphagia screening and treatment [40–42].
Age is an important factor affecting patients with dysphagia after stroke. Previous studies [43, 44] have shown that age is a risk factor for dysphagia, and with age increases, the risk of dysphagia in stroke patients also increases, which is consistent with our findings. The possible reasons may be related to the gradual weakening of various body functions as the patient aging, and the weakening of the body function can further lead to the dysfunction of the patient’s oral and maxillomandibular system (chewing, swallowing, breathing, and vocalization), thereby causing dysphagia [45, 46]. In addition, older patients have a higher probability of degeneration of advanced cranial nerve function and abnormal swallowing reflex function, which further increases the susceptibility of swallowing dysfunction [27, 47–49]. Due to the weakening of the transport capacity of the tongue muscle and the collapse of the tongue muscle in elderly patients, the food bolus will leak in advance and later, and the oral transport time will be prolonged during the feeding process [50, 51]. Clinical medical workers should fully evaluate the swallowing function of elderly stroke patients with dysphagia, and carry out targeted rehabilitation training to prevent the occurrence of aspiration.
Hypertension and diabetes are not only the risk factors for stroke, but also the risk factors for dysphagia in stroke patients [52, 53]. The results of this study have showed that the incidence of dysphagia in ischemic stroke patients with hypertension and diabetes is significantly higher than that of patients without hypertension and diabetes, which may have a joint effect with chronic diseases affecting the overall function of patients, thereby increasing the risk of dysphagia. Brainstem lesions can affect the sensitivity of the tongue and cheeks, and it may cause swallowing and laryngeal muscle dysfunction, which are the independent risk factors for swallowing dysfunction. It’s been reported that patients with brainstem lesions are often accompanied by covert aspiration, leading to aspiration pneumonia [54–56]. The results of this meta-analysis have showed that brainstem infarction is a risk factor for dysphagia in patients with ischemic stroke, which may be related to the existence of cranial nerve nuclei in the medulla oblongata that control and regulate the swallowing reflex [57]. We have not found the gender differences in the occurrence of dysphagia after stroke. However, previous studies [58, 59] have reported that men are at greater risk of dysphagia and pneumonia after stroke than women. Therefore, the gender difference in the occurrence of dysphagia after stroke remains to be further studied in the future.
It must be noted that for silent aspiration, whose detection is usually failed from most BSEs, and that could be of particular relevance for pneumonia after stroke. In fact, by focusing on the overt sign of aspiration to diagnose post-stroke dysphagia, such as cough or voice change, the silent aspiration can be undiagnosed, with a relevant increase in relative risk of pneumonia and poorer stroke clinical outcome. It’s been reported that although advances have been made in dysphagia care, prevalent screening and treatment practices remain insufficient to reduce pneumonia and decrease case fatality in dysphagic stroke patients [50]. Besides, in stroke patients who passed low-sensitive screening for dysphagia compared to those who passed high-sensitive ones who can detect also silent aspiration [60]. The stroke severity, as assessed with the NIHSS, dramatically affects the incidence and severity of post-stroke dysphagia. NIHSS is an independent risk factor for swallowing impairment after stroke. Moreover, it is very relevant that an NIHSS ≥ 12 has been suggested as the cut-off value to predict, upon admission, those stroke patients who will probably remain dysphagic after 14 days follow-up [16, 28]. Thus, identifying dysphagic patients through a highly accurate screening tool might be crucial in reducing the complications after stroke.
There are certain limitations of this meta-analysis worth considering. First, the studies included in the meta-analysis were all derived from published literature, and gray literature was not included, which may have potential publication bias. Second, there are certain differences in swallowing function assessment time, swallowing function assessment screening tools and risk measurement, etc., which may affect the study results even though we did not find the heterogeneity amongst the synthesized outcomes. Third, we only focused on the population with ischemic stroke, the choice to exclude other types of stroke could be reasonable for increasing the certitude of the results but has also the weakness of limiting the generalizability of results. Finally, the data reported for some other potentially influencing factors in the included studies are very limited. Due to the inconsistent data types of NIHSS scores in the literature included in this meta-analysis, some studies were continuous variables, some studies were categorical variables, and the classification thresholds of NIHSS scores were different, so this study could not analyze the effect of NIHSS scores on dysphagia in stroke patients. Some studies have shown that NIHSS score and muscle strength are independent predictors of dysphagia in patients with acute stroke. The association of these factors with dysphagia after stroke requires further analysis and investigation in the future.
Conclusions
In conclusion, this meta-analysis has found that age, hypertension, diabetes, and brainstem stroke are the independent risk factors for dysphagia in patients with ischemic stroke. In clinical work, high-risk patients for dysphagia in patients with ischemic stroke should be vigilant, comprehensive and systematic evaluation should be carried out as soon as possible, and early intervention and early nursing care should be taken for patients with changes in swallowing function, so as to improve the quality of life of patients.
References
- 1. Feske SK: Ischemic Stroke. Am J Med 2021, 134(12):1457–1464. pmid:34454905
- 2. Syahrul S, Maliga HA, Ilmawan M, Fahriani M, Mamada SS, Fajar JK, et al: Hemorrhagic and ischemic stroke in patients with coronavirus disease 2019: incidence, risk factors, and pathogenesis—a systematic review and meta-analysis. F1000Res 2021, 10:34. pmid:33708378
- 3. Li N, Yanjie L, Hewei Q: Research progress in rehabilitation assessment and treatment of dysphagia after strok. China Medical Herald 2020, 17(28):5–6.
- 4. Haixia Q, Lingling Z, Qin Q: Continuous nursing in stroke patients with dysphagia. Chinese Journal of Advanced Nursing 2021, 36(24):6–9.
- 5. Ko N, Lee HH, Sohn MK, Kim DY, Shin YI, Oh GJ, et al: Status Of Dysphagia After Ischemic Stroke: A Korean Nationwide Study. Arch Phys Med Rehabil 2021, 102(12):2343–2352 e2343. pmid:34348122
- 6. Smith EE, Kent DM, Bulsara KR, Leung LY, Lichtman JH, Reeves MJ, et al: Effect of Dysphagia Screening Strategies on Clinical Outcomes After Stroke: A Systematic Review for the 2018 Guidelines for the Early Management of Patients With Acute Ischemic Stroke. Stroke 2018, 49(3):e123–e128. pmid:29367332
- 7. Arnold M, Liesirova K, Broeg-Morvay A, Meisterernst J, Schlager M, Mono ML, et al: Dysphagia in Acute Stroke: Incidence, Burden and Impact on Clinical Outcome. PLoS One 2016, 11(2):e0148424. pmid:26863627
- 8. Zhang L, Tang X, Wang C, Ding D, Zhu J, Zhou Y, et al: Predictive Model of Dysphagia and Brain Lesion-Symptom Mapping in Acute Ischemic Stroke. Front Aging Neurosci 2021, 13:753364. pmid:34744695
- 9. Shenoy AM, McCune M, AbdelRazek MA: A Multifaceted Approach to Improving Postischemic Stroke Dysphagia Screening at a Community Hospital. Neurologist 2021, 26(5):167–169. pmid:34491931
- 10. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009, 6(7):e1000097. pmid:19621072
- 11. Lo CK, Mertz D, Loeb M: Newcastle-Ottawa Scale: comparing reviewers’ to authors’ assessments. BMC Med Res Methodol 2014, 14:45. pmid:24690082
- 12. Hao W, Feng X, Wu X: Analysis of risk factors for dysphagia after ischemic stroke. Medical Review 2018, 24(22):4551–4554.
- 13. Beharry A, Michel P, Faouzi M, Kuntzer T, Schweizer V, Diserens K: Predictive Factors of Swallowing Disorders and Bronchopneumonia in Acute Ischemic Stroke. J Stroke Cerebrovasc Dis 2019, 28(8):2148–2154. pmid:31129105
- 14. Cong L, Jiang H: Analysis of risk factors related to swallowing dysfunction after ischemic stroke. Chinese Journal of Cerebrovascular Diseases 2012, 9(8):408–411.
- 15. Flowers HL, AlHarbi MA, Mikulis D, Silver FL, Rochon E, Streiner D, et al: MRI-Based Neuroanatomical Predictors of Dysphagia, Dysarthria, and Aphasia in Patients with First Acute Ischemic Stroke. Cerebrovasc Dis Extra 2017, 7(1):21–34. pmid:28208139
- 16. Henke C, Foerch C, Lapa S: Early Screening Parameters for Dysphagia in Acute Ischemic Stroke. Cerebrovasc Dis 2017, 44(5–6):285–290. pmid:28903096
- 17. Huang Y, Liang F, Liao H: Analysis of related risk factors for dysphagia after ischemic stroke in 563 cases Chinese Journal of Epidemiology 2007, 28(6):601–604.
- 18. Lapa S, Luger S, Pfeilschifter W, Henke C, Wagner M, Foerch C: Predictors of Dysphagia in Acute Pontine Infarction. Stroke 2017, 48(5):1397–1399. pmid:28400488
- 19. Meng C, Xuemei S, Li L: Analysis of the incidence and influencing factors of dysphagia after acute ischemic stroke Chinese Journal of Nursing 2021, 36(2):4–7.
- 20. Remesso GC, Fukujima MM, Chiappetta AL, Oda AL, Aguiar AS, Oliveira Ade S, et al: Swallowing disorders after ischemic stroke. Arq Neuropsiquiatr 2011, 69(5):785–789. pmid:22042182
- 21. Yang H, Yi Y, Han Y, Kim HJ: Characteristics of Cricopharyngeal Dysphagia After Ischemic Stroke. Ann Rehabil Med 2018, 42(2):204–212. pmid:29765873
- 22. Lapa S, Foerch C, Singer OC, Hattingen E, Luger S: Ischemic Lesion Location Based on the ASPECT Score for Risk Assessment of Neurogenic Dysphagia. Dysphagia 2021, 36(5):882–890. pmid:33159258
- 23. Gu HQ, Yang X, Wang CJ, Zhao XQ, Wang YL, Liu LP, et al: Clinical Characteristics, Management, and In-Hospital Outcomes in Patients With Stroke or Transient Ischemic Attack in China. JAMA Netw Open 2021, 4(8):e2120745. pmid:34387677
- 24. Yongjun W, Zixiao L, Hongqiu G: China Stroke Report 2019 Chinese Journal of Stroke 2020, 9(10):1037–1043.
- 25. Yuan S, Lihua W: Epidemiology and risk factors of stroke in young adults. Journal of Cardiovascular Rehabilitation Medicine 2020, 29(4):4–9.
- 26. Nan T: Field investigation on the current status of rehabilitation intervention for dysphagia after stroke. Chhinese Journal of Nursing 2021, 36(20):4–8.
- 27. Daniels SK, Anderson JA, Willson PC: Valid items for screening dysphagia risk in patients with stroke: a systematic review. Stroke 2012, 43(3):892–897. pmid:22308250
- 28. Toscano M, Vigano A, Rea A, Verzina A, Sasso D’Elia T, Puledda F, et al: Sapienza Global Bedside Evaluation of Swallowing after Stroke: the GLOBE-3S study. Eur J Neurol 2019, 26(4):596–602. pmid:30414300
- 29. Martino R, Silver F, Teasell R, Bayley M, Nicholson G, Streiner DL, et al: The Toronto Bedside Swallowing Screening Test (TOR-BSST): development and validation of a dysphagia screening tool for patients with stroke. Stroke 2009, 40(2):555–561. pmid:19074483
- 30. Boaden E, Burnell J, Hives L, Dey P, Clegg A, Lyons MW, et al: Screening for aspiration risk associated with dysphagia in acute stroke. Cochrane Database Syst Rev 2021, 10:CD012679. pmid:34661279
- 31. Lee WH, Lim MH, Seo HG, Oh BM, Kim S: Hyoid kinematic features for poor swallowing prognosis in patients with post-stroke dysphagia. Sci Rep 2021, 11(1):1471. pmid:33446787
- 32. Kumar S, Doughty C, Doros G, Selim M, Lahoti S, Gokhale S, et al: Recovery of swallowing after dysphagic stroke: an analysis of prognostic factors. J Stroke Cerebrovasc Dis 2014, 23(1):56–62. pmid:23102742
- 33. Barritt AW, Smithard DG: Role of cerebral cortex plasticity in the recovery of swallowing function following dysphagic stroke. Dysphagia 2009, 24(1):83–90. pmid:18716838
- 34. Li S, Luo C, Yu B, Yan B, Gong Q, He C, et al: Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study. J Neurol Neurosurg Psychiatry 2009, 80(12):1320–1329. pmid:19515639
- 35. Ickenstein GW, Hohlig C, Prosiegel M, Koch H, Dziewas R, Bodechtel U, et al: Prediction of outcome in neurogenic oropharyngeal dysphagia within 72 hours of acute stroke. J Stroke Cerebrovasc Dis 2012, 21(7):569–576. pmid:21683618
- 36. Zhang D, Li Y, Li H, Fu W, Zeng J, Zeng X: Analysis of Factors That Influence the Prognosis of Swallowing Function Rehabilitation Therapy in Patients with Dysphagia After Medullary Infarction. Neuropsychiatr Dis Treat 2022, 18:97–107. pmid:35079218
- 37. Morrison RA, Hays SA, Kilgard MP: Vagus Nerve Stimulation as a Potential Adjuvant to Rehabilitation for Post-stroke Motor Speech Disorders. Front Neurosci 2021, 15:715928. pmid:34489632
- 38. Hui C, Yan Z, Chunhua W: Meta-analysis of risk factors for early neurological deterioration in patients with ischemic stroke Journal of Chengde Medical College 2019, 36(5):7–11.
- 39. Matsuo T, Matsuyama M: Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One 2021, 16(3):e0248770. pmid:33730038
- 40. Jones CA, Colletti CM, Ding MC: Post-stroke Dysphagia: Recent Insights and Unanswered Questions. Curr Neurol Neurosci Rep 2020, 20(12):61. pmid:33136216
- 41. Choi JS, Bang H, Lee GJ, Seo HG, Oh BM, Han TR: Epiglottic Retroflexion is a Key Indicator of Functional Recovery of Post-stroke Dysphagia. Ann Rehabil Med 2020, 44(1):1–10. pmid:32130834
- 42. Qiu X, Yao XJ, Han SN, Wu YY, Ou ZJ, Li TS, et al: Acupuncture Reduces the Risk of Dysphagia in Stroke Patients: A Propensity Score-Matched Cohort Study. Front Neurosci 2021, 15:791964. pmid:35069105
- 43. Ran Z, Weixin C, Lili D: Meta-analysis of risk factors for dysphagia in patients with ischemic stroke. Chinese Journal of Stroke 2022, 16(12):7–9.
- 44. Huixian F: Analysis of the influencing factors of neurogenic dysphagia after stroke. China Journal of Practical Neurological Diseases 2013, 16(21):3–5.
- 45. Al-Khaled M, Matthis C, Binder A, Mudter J, Schattschneider J, Pulkowski U, et al: Dysphagia in Patients with Acute Ischemic Stroke: Early Dysphagia Screening May Reduce Stroke-Related Pneumonia and Improve Stroke Outcomes. Cerebrovasc Dis 2016, 42(1–2):81–89. pmid:27074007
- 46. Won SY, Krieger S, Dubinski D, Gessler F, Behmanesh B, Freiman TM, et al: Neurogenic Dysphagia in Subdural Hematoma. Front Neurol 2021, 12:701378. pmid:35153966
- 47. Dziewas R, Michou E, Trapl-Grundschober M, Lal A, Arsava EM, Bath PM, et al: European Stroke Organisation and European Society for Swallowing Disorders guideline for the diagnosis and treatment of post-stroke dysphagia. Eur Stroke J 2021, 6(3):LXXXIX–CXV. pmid:34746431
- 48. Sherman V, Greco E, Martino R: The Benefit of Dysphagia Screening in Adult Patients With Stroke: A Meta-Analysis. J Am Heart Assoc 2021, 10(12):e018753. pmid:34096328
- 49. Dziewas R, Allescher HD, Aroyo I, Bartolome G, Beilenhoff U, Bohlender J, et al: Diagnosis and treatment of neurogenic dysphagia—S1 guideline of the German Society of Neurology. Neurol Res Pract 2021, 3(1):23. pmid:33941289
- 50. Suntrup-Krueger S, Minnerup J, Muhle P, Claus I, Schroder JB, Marian T, et al: The Effect of Improved Dysphagia Care on Outcome in Patients with Acute Stroke: Trends from 8-Year Data of a Large Stroke Register. Cerebrovasc Dis 2018, 45(3–4):101–108. pmid:29533960
- 51. Dallal York J, Leonard K, Anderson A, DiBiase L, Jeng EI, Plowman EK: Discriminant Ability of the 3-Ounce Water Swallow Test to Detect Aspiration in Acute Postoperative Cardiac Surgical Patients. Dysphagia 2021. pmid:34268585
- 52. Umay E, Eyigor S, Ertekin C, Unlu Z, Selcuk B, Bahat G, et al: Best Practice Recommendations for Stroke Patients with Dysphagia: A Delphi-Based Consensus Study of Experts in Turkey-Part I: Management, Diagnosis, and Follow-up. Dysphagia 2021.
- 53. Eltringham SA, Smith CJ, Pownall S, Sage K, Bray B: Variation in Dysphagia Assessment and Management in Acute Stroke: An Interview Study. Geriatrics (Basel) 2019, 4(4).
- 54. Pacheco-Castilho AC, Vanin GM, Dantas RO, Pontes-Neto OM, Martino R: Dysphagia and Associated Pneumonia in Stroke Patients from Brazil: A Systematic Review. Dysphagia 2019, 34(4):499–520. pmid:31111249
- 55. Teuschl Y, Trapl M, Ratajczak P, Matz K, Dachenhausen A, Brainin M: Systematic dysphagia screening and dietary modifications to reduce stroke-associated pneumonia rates in a stroke-unit. PLoS One 2018, 13(2):e0192142. pmid:29389984
- 56. Krishnamurthy R, Balasubramanium RK, Premkumar PK: Systematic Review and Meta-Analysis of Dysphagia and Associated Pneumonia in Patients With Stroke From India: A Call to Arms. Am J Speech Lang Pathol 2022, 31(1):502–514. pmid:34982940
- 57. Liu CH, Huo M, Qin HH, Zhao BL: Critical prognostic factors for poststroke dysphagia: a meta-analysis. Eur Rev Med Pharmacol Sci 2022, 26(2):610–622. pmid:35113437
- 58. Ning S: The application value of water drinking test in patients with dysphagia after acute stroke Chinese Medicine Guide 2020, 12(3):11–14.
- 59. Yang H, Zhiyu G, Xuguang G: Analysis of influencing factors on prognosis of patients with acute cerebral stroke. Chinese Journal of Cardiovascular and Cerebrovascular Diseases in the Aged 2014, 16(3):240–242.
- 60. Jannini TB, Ruggiero M, Vigano A, Comanducci A, Maestrini I, Giuliani G, et al: The role of the Sapienza GLObal Bedside Evaluation of Swallowing after Stroke (GLOBE-3S) in the prevention of stroke-associated pneumonia (SAP). Neurol Sci 2022, 43(2):1167–1176. pmid:34269936