Received: 28 March 2021 | Accepted: 7 June 2021 DOI: 10.1111/ene.14998 ORIGINAL ARTICLE Healthcare costs of post-­stroke oropharyngeal dysphagia and its complications: malnutrition and respiratory infections Sergio Marin1,2,3 | Mateu Serra-­Prat3,4 | Omar Ortega1,3 | 5 6 4 Monica Audouard Fericgla | Jordi Valls | Elisabet Palomera | Ramon Cunillera6 | Ernest Palomeras7 | Josep Maria Ibàñez8 | Pere Clavé1,3 1 Gastrointestinal Physiology Laboratory, Hospital de Mataró, Universitat Autònoma de Barcelona, Mataró, Spain 2 Pharmacy Department, Hospital Universitari Germans Trias i Pujol, Badalona, Spain 3 Centro de Investigación Biomédica en Red de enfermedades hepáticas y digestivas (CIBERehd), Instituto de Salud Carlos III, Barcelona, Spain 4 Research Unit, Hospital de Mataró, Consorci Sanitari del Maresme, Mataró, Spain 5 Pharmacy Department, Hospital Universitari Dexeus, Barcelona, Spain 6 Hospital Management, Hospital de Mataró, Consorci Sanitari del Maresme, Mataró, Spain 7 Department of Neurology, Hospital de Mataró, Consorci Sanitari del Maresme, Mataró, Spain 8 Chief Medical Officer, Hospital de Mataró, Consorci Sanitari del Maresme, Mataró, Spain Correspondence Abstract Sergio Marin, Consorci Sanitari del Maresme, Carretera de Cirera, w/n. Background and purpose: The healthcare economic costs of post-­stroke oropharyngeal Mataró, Barcelona 08304, Spain. dysphagia (OD) are not fully understood. The purpose of this study was to assess the Email: sergiomarinrubio@gmail.com acute, subacute and long-­term costs related to post-­stroke OD and its main complications Funding information (malnutrition and respiratory infections). Financial support received from research grants from Nutricia Danone Methods: A cost of illness study of patients admitted to Mataró Hospital (Catalonia, Spain) Advanced Medical Nutrition (HESDY from May 2010 to September 2014 with a stroke diagnosis was performed. OD, malnu- Grant); Fundació Salut del CSdM, Strategic Action Grant in Oropharyngeal trition and respiratory infections were assessed during hospitalization and follow-­up (3 Dysphagia provided by the Centro de and 12 months). Hospitalization and long-­term costs were measured from hospital and Investigación Biomédica en Red en el Área de Enfermedades Hepáticas y Digestivas healthcare system perspectives. Multivariate linear regression analysis was performed to (CIBERehd), Instituto de Salud Carlos III, assess the independent effect of OD, malnutrition and respiratory infections on health- DJO Global, and la Fundació la Marató de TV3 (11/2310). care costs during hospitalization, and at 3 and 12 months’ follow-­up. Results: In all, 395 patients were included of whom 178 had OD at admission. Patients with OD incurred major total in-­hospital costs (€5357.67 ± €3391.62 vs. €3976.30 ± €1992.58, p < 0.0001), 3-­month costs (€8242.0 ± €5376.0 vs. €5320.0 ± €4053.0, p < 0.0001) and 12-­month costs (€11,617.58 ± €12,033.58 vs. €7242.78 ± €7402.55, p < 0.0001). OD was independently associated with a cost increase of €789.68 (p = 0.011) during hospitalization and of €873.5 (p = 0.084) at 3 months but not at 12 months. However, patients with OD who were at risk of malnutrition or malnourished and suffered res- piratory infections incurred major mean costs compared with those patients without OD (€19,817.58 ± €13,724.83 vs. €7242.8 ± €7402.6, p < 0.0004) at 12 months’ follow-­up. This is an open access article under the terms of the Creat​ive Commo​ns Attri​butio​n-­NonCo​mmerc​ial-­NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-­commercial and no modifications or adaptations are made. © 2021 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology 3670 |  wileyonlinelibrary.com/journal/ene Eur J Neurol. 2021;28:3670–3681. COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS | 3671 Conclusion: Oropharyngeal dysphagia causes significant high economic costs during hos- pitalization that strongly and significantly increase with the development of malnutrition and respiratory infections at long-­term follow-­up. KEYWORDS deglutition disorders, economics, malnutrition, respiratory tract infections, stroke BAC KG RO U N D hospitalization, and at 3 months’ (subacute phase) and 12 months’ follow-­up (chronic phase) from the hospital and the healthcare sys- Oropharyngeal dysphagia (OD) is a common complication after tem perspectives, respectively. It aims to establish the basis for stroke [1]. In the acute stroke phase, the incidence of OD is very cost-­effectiveness of appropriate PS-­OD management to influence high (37%–­78%) [2] but improves after hospital discharge, remaining healthcare policies. as a chronic condition in over 50% of patients [3]. OD impairs the efficacy and the safety of deglutition in acute and long-­term stroke patients [4]. This can lead to dehydration, malnutrition and tracheo- M E TH O D S bronchial aspiration that may cause respiratory infections and pneu- monia with an associated mortality of up to 50% [1, 4–­6]. The main Design and study population causes of mortality for stroke survivors at 1-­year follow-­up are re- spiratory infections and aspiration pneumonia, two well recognized This is an observational, longitudinal, cost-­of-­illness study in two complications of post-­stroke OD (PS-­OD) [7, 8]. phases: (a) an acute phase that includes a cost analysis of OD after Key aspects of PS-­OD management are early evaluation of pa- an acute stroke episode during hospitalization from the hospital per- tient deglutition in the acute phase, compensation of the deficient spective and (b) a subacute and a chronic phase that includes a cost mechanisms related to the efficacy and safety of deglutition and res- analysis of OD, malnutrition and the presence of respiratory infec- toration of the swallowing function [9]. American Heart Association/ tions at 3 months’ and 12 months’ follow-­up from the healthcare American Stroke Association guidelines recommend early screening system perspective. of OD before patients begin eating, drinking or taking oral drugs after The study sample included all patients admitted to the Mataró acute stroke [10]. Moreover, position statements of the European Hospital, Catalonia, Spain, from May 2010 to September 2014 with Society for Swallowing Disorders also recommend screening for OD a confirmed diagnosis of stroke and who gave their written informed with a validated tool in the first hours after acute stroke followed by consent to participate. Patients were excluded if they had a previous expert assessment if required (videofluoroscopy or fibre optic endo- diagnosis of OD, if the final diagnosis on admission was transient scopic evaluation of swallowing) [11, 12]. ischaemic attack or if they were transferred to another hospital be- A 45.06% prevalence of new-­onset dysphagia after stroke was fore admission to Mataró Hospital. Recruited patients were classi- found recently. Moreover, it was found that presenting PS-­OD was fied into two groups according to the presence or absence of OD. associated with high mortality rates during hospital stay and was an The presence of OD was assessed during the first 24–­48 h of ad- independent risk factor for prolonged hospital stay and to be insti- mission by specially trained nursing staff using the volume–­viscosity tutionalized after hospital discharge; OD was also an independent swallow test previously described by our group [17, 18]. risk factor for poorer functional capacity and increased risk of mor- tality 3 months after stroke [13]. OD has also been associated with increased length of stay and mortality during hospitalization, inpa- Cost elements considered (health resource tient costs and probability of transfer to a post-­acute care facility consumption) independent of its aetiology in other studies [14]. Recently, health economic data on the cost of PS-­OD have become available [15]. Phase 1 A recent systematic review by our group estimates up to €15,000 (approximately US$16,900) as the cost of PS-­OD in the acute phase Acute hospitalization costs included (a) fixed costs (stay in neurol- and €24,000 (approximately US$27,600) as the cost of an episode ogy department, stay in intensive care unit and transfers to a tertiary of pneumonia in patients with PS-­OD based on studies performed care centre—­Hospital Universitari Germans Trias i Pujol, Badalona, in France, Switzerland, Argentina, Brazil, Taiwan and the USA. The Barcelona—­for medical attention, revascularization, nursing, imag- review revealed few studies describing health economic and social ing and laboratory tests) and (b) variable costs (medication, enteral costs of PS-­OD after acute hospitalization (subacute and long-­term feeding [EF] and nutritional supplementation [NS]). Medication in- costs) or related to PS-­OD complications [16]. cluded fibrinolysis, anticoagulation, antiplatelet inhibitors, acute in-­ The objective of this study was to assess the costs related to hospital drugs and chronic medication reconciliation during hospital OD, malnutrition and respiratory infections after stroke, during stay. 3672 | MARIN et al. Phase 2 and 12 months’ follow-­up were also collected. Costs for those patients with and without OD who were at risk of or had malnutrition and who Cost in phase 2 comprised subacute (from discharge to 3 months’ developed respiratory infections were also calculated. follow-­up) and chronic (from 3 months’ to 12 months’ follow-­up) costs. Subacute and long-­term costs included visits to the emer- gency department, re-­hospitalization, stays in a socio-­sanitary insti- Statistical analysis tution (Hospital de Sant Jaume, Mataró, Barcelona) or in long-­term rehabilitation/convalescence facilities (Casal de Curació, Vilassar de The main outcome of interest was the independently associated Mar, Barcelona) or in a nursing home, and chronic medication. Costs cost increase for OD, malnutrition and respiratory infections in post-­ related to institutionalization were based on length of stay at each stroke patients. Statistical analysis was performed using GraphPad institution. Costs related to chronic medication were assessed ac- Prism 6.01 (San Diego, CA, USA). Comparisons of qualitative vari- cording to electronic prescriptions of the Catalan Health Service and ables between groups were made using Fisher's exact test or the drug consumption during re-­hospitalization and socio-­sanitary care chi-­squared test. Continuous data were presented as mean ± SD and stay. compared between groups with the non-­parametric Mann–­Whitney U test or the Kruskal–­Wallis test for multiple comparisons (with Dunn's post-­test). To assess normality the D'Agostino and Pearson Translation into monetary units (€) omnibus normality test was used. First, a bivariate analysis of the association of OD, malnutrition The cost of 1 day in the neurology ward or in the intensive care unit and risk of malnutrition and the presence of respiratory infections was estimated from price data on diagnosis related groups (brain is- with acute, subacute and chronic healthcare costs was assessed chaemia and intracerebral haemorrhage) in the hospital discharge re- using a simple linear regression analysis. Secondly, a multivariate cords of the Spanish National Health Services and were considered linear regression analysis was used in three different multivariate as €626.38 and €569.78 (brain ischaemia, 201–­500 and 501–­1000 models to adjust for the effect of OD, malnutrition or respiratory bed tertiary care hospital, respectively) and €681.88 and €591.96 infections on costs by age, comorbidities, baseline functionality and (intracerebral haemorrhage, 201–­500 and 501–­1000 bed tertiary stroke severity. Statistical significance was set at p < 0.05. care hospital), respectively [19]. Costs related to 1 day in medium-­ term socio-­sanitary centres, long-­term rehabilitation/convalescence facilities and nursing homes were estimated from the published Legal and ethical issues public price health agreements of the Catalan Health Service, the Catalan Institute for Social Assistance and Services, the Consorci This research was performed and reported following the recommen- Sanitari del Maresme (CSdM) and the Fundació Casal de la Salut dations stated in the Strengthening the Reporting of Observational and were estimated as €92.91, €91.58 and €62.9 respectively [20]. Studies in Epidemiology (STROBE) statement: guidelines for report- Cost of acute in-­hospital medication, EF and NS for each patient was ing observational studies [23]. obtained from the billing data of the CSdM Pharmacy Department. The protocol of this study was evaluated and approved by Cost attributable to each drug of chronic medication was obtained the Ethical Committee for Clinical Investigation of the Hospital from the published public prices of reference of the Spanish National de Mataró (protocol code 35/14), ‘La Marató’ de TV3 register Health Services and the Ministerio de Sanidad, Servicios Sociales e code 11/2310. All procedures contributing to this investigation Igualdad [21]. All resource use was translated into costs using 2019 were conducted according to the principles stated in the Helsinki unitary values. Cost updates were performed using the correspond- Declaration of 1975 and its subsequent amendments. The General ing annual Consumer Price Index of Spain provided by the Instituto Data Protection Regulation of the European Union 2016/679 was Nacional de Estadística [22]. followed. All patients included in this study or their legal representa- tive signed an informed consent. Other study variables R E S U LT S Age and gender, as well as the Charlson Comorbidity Index and the number of comorbidities, the modified Rankin Scale, the Barthel index Recruitment and main sample characteristics and the Mini Nutritional Assessment Short Form were assessed and recorded on admission. Stroke type (ischaemic or haemorrhagic) and A total of 608 patients were recruited and 395 were included in the neurological status using the National Institutes of Health Stroke Scale study following eligibility criteria, of whom 178 had OD on admis- were assessed. The risk and presence of malnutrition were assessed sion (45.0%). Figure S1 (Appendix S1) shows the number of indi- using the Mini Nutritional Assessment Short Form at 3 months’ follow- viduals at each phase of the study. Descriptive sociodemographic ­up. Respiratory infections and/or pneumonia diagnosis at 3 months’ and clinical characteristics of patients included in this study were COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS | 3673 previously published in a study on the prevalence, risk factors and Costs in the acute phase complications of PS-­OD [13, 24]. Table 1 shows a summary of the main sociodemographic, clinical characteristics and nutritional sta- Mean costs during hospitalization were €4598.79 ± €2799.51 but tus of patients on admission. A total of 21 patients died during hos- patients with OD cost significantly more during hospitalization for pitalization and early follow-­up (5.31% hospital mortality) and 41 both fixed and variable costs: hospital stay, €5265.11 ± €3319.62 during long-­term follow-­up (10.38% mortality at long term). versus €3902.55 ± €1925.78, p < 0.0001; in-­hospital medication, €87.86 ± €264.16 versus €73.57 ± €216.25, p < 0.0001; EF and/or NS, €4.69 ± €23.28 versus €0.18 ± €1.33, p < 0.0001; and total in-­ Health resource consumption in the acute phase hospital costs, €5357.67 ± €3391.62 versus €3976.30 ± €1992.58, p < 0.0001, patients with OD being reported first. Table 2 summa- Mean hospitalization days were 7.16 ± 4.30. Patients with OD rizes these findings. had longer stays (mean stay, OD 8.33 ± 5.21 days vs. non-­O D 6.20 ± 3.05 days; p < 0.0001). Also, more patients with OD used EF and NS (patients treated with EF and/or NS, OD 23 (12.92), Health resource consumption in the subacute and non-­O D 5 (1.26); p < 0.0001). A total of seven patients were re- chronic phases ferred to a tertiary care centre (mean stay, OD 0.08 ± 0.64 days vs. non-­O D 0.07 ± 0.50 days; p < 0.926). Table S1 shows a sum- In the subacute phase, mean patient visits to the emergency de- mary of patient stays and resource consumption including EF and partment were 0.16 ± 0.36, and mean stays in re-­hospitalizations NS. 0.61 ± 2.3; in a socio-­s anitary institution, 6.9 ± 17.5; in a long-­term TA B L E 1 Main sociodemographic and clinical characteristics of the 395 patients included in this study OD using V-­VST All patients (n = 395) OD admission (n = 178) Non-­OD admission (n = 217) p value Sociodemographic data Age, years (mean ± SD) 73.2 ± 13.3 77.9 ± 11.1 69.4 ± 13.7 <0.0001 Male, n (%) 211 (53.42) 85 (47.75) 126 (58.06) 0.043 Patient status on admission Comorbidity, n (%) No comorbidity, 0 35 (8.86) 9 (5.01) 26 (11.98) 0.0008 Moderate comorbidity, 1–­2 172 (43.54) 67 (37.64) 105 (48.39) Severe comorbidity, ≥3 188 (47.59) 102 (57.30) 86 (39.63) CCI, n (%) 0–­1 111 (28.10) 34 (19.10) 77 (35.48) 0.002 2 108 (27.34) 55 (30.89) 53 (24.42) ≥3 176 (44.55) 89 (50.00) 87 (40.09) Barthel index (mean ± SD) 91.00 ± 18.41 85.28 ± 23.59 95.69 ± 10.64 <0.0001 Barthel ≤ 90, n (%) 105 (26.58) 68 (38.2) 37 (17.05) <0.0001 mRS (mean ± SD) 0.78 ± 1.38 1.16 ± 1.57 0.47 ± 1.10 <0.0001 mRS > 1, n (%) 93 (23.54) 62 (34.83) 31 (14.29) <0.0001 NIHSS admission (mean ± SD) 5.06 ± 6.04 8.10 ± 7.60 2.56 ± 2.30 <0.0001 NIHSS admission >6, n (%) 42 (10.63) 27 (15.17) 15 (6.91) 0.009 All patients (n = 266) OD admission (n = 114) Non-­OD admission (n = 152) Nutritional status on admission MNA-­sf (mean ± SD) 12.18 ± 2.04 11.87 ± 1.97 12.41 ± 1.76 0.023 Well-­nourished (12–­14), n (%) 174 (65.41) 68 (59.65) 106 (69.74) 0.190 At risk (8–­11), n (%) 80 (30.08) 39 (34.21) 41 (26.97) Malnourished (0–­7 ), n (%) 12 (4.51) 7 (6.14) 5 (3.29) Bold indicates statistical significance value (p < 0.05). Abbreviations: CCI, Charlson Comorbidity Index; MNA-­sf, Mini Nutritional Assessment Short Form; mRS, modified Rankin Scale; NIHSS, National Institutes of Health Stroke Scale; OD, oropharyngeal dysphagia; V-­VST, volume–­viscosity swallow test. 3674 | MARIN et al. TA B L E 2 Total mean direct healthcare related and non direct healthcare related costs during acute in-­hospital admission, and at 12 months’ follow-­up (euros, 2019) OD using V-­VST All patients (n = 395) OD (n = 178) Non-­OD (n = 217) p value Acute in-­hospital costs Hospitalization (ICU + neurology 4516.57 ± 2731.84 5265.11 ± 3319.62 3902.55 ± 1925.78 <0.0001 ward + tertiary hospital) Medication 80.01 ± 254.57 87.86 ± 264.16 73.57 ± 216.25 <0.0001 Enteral feeding and nutritional 2.21 ± 15.82 4.69 ± 23.28 0.18 ± 1.33 <0.0001 supplementation Total 4598.79 ± 2799.51 5357.67 ± 3391.62 3976.30 ± 1992.58 <0.0001 OD using V-­VST All patients (n = 374) OD (n = 158) Non-­OD (n = 216) Subacute costs (3 months’ follow-­up) Direct healthcare and direct non-­ healthcare costs Chronic medication 232.3 ± 270.3 265.7 ± 296.8 207.9 ± 247.0 0.036 Re-­hospitalization 388.6 ± 2055.4 416.3 ± 1651.0 368.3 ± 2310.0 0.163 In-­hospital medication cost 4.7 ± 50.4 3.8 ± 19.9 5.4 ± 64.1 0.226 In-­hospital enteral feeding and 0.02 ± 0.35 0.04 ± 0.50 0.01 ± 0.2 0.824 nutritional supplementation Emergency department 14.4 ± 33.2 11.0 ± 29.7 16.9 ± 35.4 0.090 Socio-­sanitary care 641.7 ± 1628.6 992.6 ± 1946.0 385.0 ± 1296.0 0.0002 Long-­term rehabilitation facilities 221.1 ± 1270.8 266.0 ± 1401.0 188.2 ± 1169.0 0.582 Nursing home 458.6 ± 1402.9 843.6 ± 1798.0 177.1 ± 930.3 <0.0001 Total 1961.4 ± 3284.5 2799.0 ± 3395.0 1349.0 ± 3067.0 <0.0001 Total (admission + subacute) 6554.3 ± 4870.7 8242.0 ± 5376.0 5320.0 ± 4053.0 <0.0001 Long-­term costs (12 months’ follow-­up) Direct healthcare and direct non-­ healthcare costs Chronic medication 881.75 ± 961.48 936.94 ± 893.07 841.38 ± 1.006.67 0.169 Re-­hospitalization 930.84 ± 4.423.50 1083.76 ± 5.985.29 818.98 ± 2765.23 0.970 In-­hospital medication cost 10.73 ± 84.88 14.98 ± 104.50 7.64 ± 66.98 0.875 In-­hospital enteral feeding and 0.09 ± 1.48 0.21 ± 2.21 0.01 ± 0.18 0.389 nutritional supplementation Emergency department 64.49 ± 120.49 64.52 ± 125.98 64.48 ± 116.30 0.162 Socio-­sanitary care 716.69 ± 2.146.19 1156.67 ± 2.834.90 394.86 ± 1360.72 0.0002 Long-­term rehabilitation facilities 428.76 ± 2.820.82 395.30 ± 2.243.84 453.24 ± 3176.97 0.597 Nursing home 1464.53 ± 5.002.62 2522.37 ± 6392.77 690.73 ± 3467.16 <0.0001 Total 4497.89 ± 8839.78 6174.68 ± 10,957.68 3271.34 ± 6626.48 <0.0001 Acute and long-­term direct healthcare and non-­healthcare costs 1-­year total costs 9090.88 ± 9873.82 11,617.58 ± 12,033.58 7242.78 ± 7402.55 <0.0001 Bold indicates statistical significance value (p < 0.05). Abbreviations: ICU, intensive care unit; OD, oropharyngeal dysphagia; V-­VST, volume–­viscosity swallow test. rehabilitation/convalescence facility, 2.4 ± 13.9; and in nurs- At 12 months’ follow-­up, mean patient visits to the emergency ing homes, 7.3 ± 22.3. Significantly higher patient stays in socio-­ department were 0.71 ± 1.32, and mean stays in re-­hospitalizations sanitary institutions (10.7 ± 20.9 days vs. 4.1 ± 14.00 days, 1.47 ± 7.02; in a socio-­sanitary institution, 7.71 ± 23.09; in a long-­ p = 0.0002) and nursing homes (13.4 ± 28.6 days vs. 2.8 ± 17.8 term rehabilitation/convalescence facility, 4.69 ± 30.84; and in days, p < 0.0001) were observed for patients with OD. nursing homes, 23.28 ± 79.53. Significantly higher patient stays COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS | 3675 in socio-­sanitary institutions (12.45 ± 30.51 days vs. 4.25 ± 14.64 follow-­up, total costs (acute plus long-­term direct healthcare and days, p = 0.0002) and nursing homes (40.10 ± 101.63 days vs. non-­healthcare costs) were higher for those patients with PS-­OD 10.98 ± 55.12 days, p < 0.0001) were observed for patients with (€11,617.58 ± €12,033.58 vs. €7242.78 ± €7402.55, p < 0.0001). PS-­OD. Table S1 summarizes long-­term resource consumption of the Table 2 summarizes these findings. variables measured in this study. Resource consumption and costs associated with Costs in the subacute and chronic phases nutritional risk or malnutrition on admission and at 3 months’ follow-­up At 3 months’ follow-­up, mean costs were €6554.3 ± €4870.7 per patient. The only significant differences found between patients with and with- Patients at risk of malnutrition or malnourished on admission had out PS-­OD were related to socio-­sanitary care (€992.6 ± €1946.0 vs. significantly higher hospital stays (8.4 ± 4.8 days vs. 6.9 ± 4.2 days, €385.0 ± €1296.0, p = 0.0002) and nursing homes (€843.6 ± €1798.0 p = 0.004) and EF and NS consumption (9.8% vs. 2.3%, p = 0.013) and vs. €177.1 ± €930.3, p < 0.0001), higher for patients with PS-­OD. At incurred major costs (€5370.0 ± €3052.0 vs. €4445.0 ± €2759.0, 3 months’ follow-­up, total costs (acute plus subacute direct healthcare p = 0.004) during acute hospitalization and at 3 months’ fol- and non-­healthcare costs) were higher for those patients with PS-­OD low-­up (€8145.0 ± €5868.0 vs. €5830.0 ± €4204.0, p = 0.001). (€8242.0 ± €5376.0 vs. €5320.0 ± €4053.0, p < 0.0001). Table 3 shows a summary of the main sociodemographic and clini- At 12 months’ follow-­up, mean costs were €9090.88 ± €9873.82 cal characteristics and nutritional status of patients on admission. per patient. Although there was a constant trend towards higher At 3 months’ follow-­up, 69 out of 231 patients (29.8%) that could costs related to chronic medication, re-­hospitalizations, in-­ be evaluated were at risk of malnutrition or malnourished, with hospital EF and NS and visits to the emergency department, no more visits to the emergency department (1.0 ± 1.4 vs. 0.67 ± 1.2, significant differences were found between those patients with p = 0.029) and stays in nursing homes (47.1 ± 118.1 days vs. PS-­OD and those without. Costs related to socio-­sanitary care 4.3 ± 38.8 days, p < 0.0001) at 1-­year follow-­up without significant (€1156.67 ± €2834.90 vs. €394.86 ± €1360.72, p = 0.0002) and differences on stays related to re-­hospitalizations, socio-­sanitary in- nursing homes (€2522.37 ± €6392.77 vs. €690.73 ± €3467.16, stitution and long-­term rehabilitation/convalescence facilities. Table p < 0.0001) were higher for patients with PS-­OD. At 12 months of S2 summarizes acute and long-­term resource consumption and its TA B L E 3 Main sociodemographic and clinical characteristics of the patients included in the study with and without malnutrition or risk of malnutrition No risk MN/MN Risk MN/MN using MNA-­sf All patients (n = 395) Risk MN/MN (n = 92) (n = 174) p value Sociodemographic data Age, years (mean ± SD) 73.2 ± 13.3 75.0 ± 12.5 70.9 ± 12.7 0.008 Male, n (%) 211 (53.42) (41) (112) 0.003 Patient status before admission Comorbidity, n (%) No comorbidity, 0 35 (8.86) 12 (13.0) 8 (4.6) 0.037 Moderate comorbidity, 1–­2 172 (43.54) 37 (40.2) 84 (48.3) Severe comorbidity, ≥3 188 (47.59) 43 (46.7) 82 (47.1) CCI, n (%) 0–­1 111 (28.10) 21 (22.8) 54 (31.0) 0.346 2 108 (27.34) 29 (31.5) 46 (26.4) ≥3 176 (44.55) 42 (45.7) 74 (42.5) Barthel index (mean ± SD) 91.00 ± 18.41 86.9 ± 21.6 95.7 ± 10.2 <0.0001 Barthel ≤ 90, n (%) 105 (26.58) 33 (35.9) 29 (16.7) 0.0007 mRS (mean ± SD) 0.78 ± 1.38 0.9 ± 1.5 0.4 ± 1.0 0.002 mRS > 1, n (%) 93 (23.54) 25 (27.2) 24 (13.8) 0.012 NIHSS admission (mean ± SD) 5.06 ± 6.04 5.3 ± 5.6 3.6 ± 3.9 0.012 NIHSS admission >6, n (%) 42 (10.63) 22 (23.9) 25 (14.4) 0.063 Bold indicates statistical significance value (p < 0.05). Abbreviations: CCI, Charlson Comorbidity Index; MN, malnutrition; MNA-­sf, Mini Nutritional Assessment Short Form; mRS, modified Rankin Scale; NIHSS, National Institutes of Health Stroke Scale. 3676 | MARIN et al. relation with nutritional status. Long-­term costs were significantly Costs from the hospital and the healthcare system higher for those patients at risk of malnutrition or malnourished perspectives compared with well-­nourished patients (€10,678.0 ± €10,466.9 vs. €6230 ± €4326.0, p = 0.01). Table 4 summarizes these findings. In the case of patients with PS-­OD, mean hospitalization costs Table 5 summarizes differences in costs between those patients (hospital perspective) were lower than costs outside acute hospi- with and without OD and with and without risk of malnutrition or talization (health care system perspective) (€5357.67 ± €3391.62 malnutrition. vs. €6174.68 ± €10,957.68, respectively), whilst in those patients without OD mean hospitalization costs were higher than subacute and chronic costs (€3976.30 ± €1992.58 vs. €3271.34 ± €6626.48, Respiratory infections at 1-­year follow-­up and their respectively). In the case of patients affected or not by risk of influence on costs malnutrition or malnutrition, chronic costs were higher in both cases compared to hospitalization costs (€2945.00 ± €4593.00 Sixty-­t wo out of 374 patients (16.6%) who underwent the 1-­year vs. €6029.00 ± €9018.00 and €1384.00 ± €2397.00 vs. follow-­up suffered at least one episode of respiratory infection €2120.00 ± €3494.00, respectively). (78 episodes in total, mean 1.26/affected patient) and incurred significantly higher long-­term costs (€13,806.0 ± €11,834.0 vs. €8154.0 ± €9190.0, p < 0.0001). Table 5 summarizes differences in DISCUSSION costs between patients with and without PS-­OD and with or with- out respiratory infections. This study shows a significant and independent increase in health economic costs of €789.68 during hospitalization for patients with PS-­OD, and €873.5 at 3 months’ follow-­up. Patients with poor nu- Total acute and long-­term costs on those patients tritional status at 3 months showed a significant and independent who suffered from OD and its complications cost increase of €2303.38 at 12 months’ follow-­up, and for patients with at least one respiratory infection at 3 and 12 months’ follow-­up Those patients with PS-­OD and at risk of malnutrition or malnour- the costs were increased by €3792.62 and €3034.08, respectively. ished at 3 months’ follow-­up incurred higher costs at 12 months’ This shows an independent increase in costs associated with PS-­OD follow-­up than patients without PS-­OD (€14,295.6 ± €11,334.5 during hospitalization that can increase exponentially with the devel- vs. €7242.8 ± €7402.6, p < 0.001). Patients with PS-­OD and res- opment of its main complications (malnutrition and respiratory infec- piratory infection incurred higher costs than patients without PS-­ tions) during long-­term follow-­up. The 1-­year cost of a patient with OD (€16,487.0 ± €11,603.9 vs. €7242.8 ± €7402.6, p < 0.0001) PS-­OD, malnutrition and at least one episode of respiratory infection at 12 months’ follow-­up. Patients with PS-­OD at risk of or mal- is €19,817.58 ± €13,724.83 versus €7242.8 ± €7402.6 for post-­stroke nourished who had a respiratory infection incurred greater mean patients without OD, a clear indication of the economic burden of costs than patients without PS-­OD (€19,817.58 ± €13,724.83 vs. PS-­OD from both the hospital and the healthcare system perspective. €7242.8 ± €7402.6, p < 0.0004) at 12 months’ follow-­up. Table 6 In this study, about half the costs incurred by our post-­stroke shows a comparison of mean costs between patients with and with- patients were attributed to acute hospitalization. Significant out PS-­OD, risk of or malnutrition, and respiratory infections. mean cost increases were observed for patients with PS-­OD (€5357.67 ± €3391.62 vs. €3976.30 ± €1992.58) and patients at risk of malnutrition or malnourished on stroke admission Multivariate analysis (€5370.0 ± €3052.0 vs. €4445.0 ± €2759.0), mainly due to longer hospital stays (8.33 ± 5.21 vs. 6.20 ± 3.05 days and 8.40 ± 4.80 After adjusting for possible confounding factors, OD was indepen- vs. 6.90 ± 4.20 days respectively). These data coincide with a pre- dently associated with an increased cost of €789.68 (p = 0.011) dur- viously published systematic review that assessed the influence of ing hospitalization in the acute phase and €873.5 (p = 0.084) in the OD secondary to all aetiologies on length of stay and costs find- subacute phase but no significant effect was observed in the chronic ing that PS-­OD patients had a longer and more variable length of phase. For nutritional status, moving from one category (well-­ stay of 4.73 days (95% confidence interval 2.7–­7.2) and an increase nourished, at risk of malnutrition and malnourished) to the next, of 40.36% in costs [25]. Moreover, previous studies showed an worse one, was independently associated with a cost increase of increase of €3000 on hospitalization costs for patients with isch- €1277.39 (p = 0.004) at subacute phase and of €2303.38 (p = 0.001) aemic PS-­OD in France and of 14,000 Swiss Francs in Switzerland at chronic phase. The presence of at least one respiratory infection [26], and an increase of approximately US$6589 on patients need- was independently associated with a cost increase of €3792.62 ing tube feeding after ischaemic or haemorrhagic stroke in the USA (p < 0.001) in the subacute phase and of €3034.08 (p < 0.011) in [27]. In patients transferred to a rehabilitation ward after haemor- the chronic phase. Results of the multivariate analysis are described rhagic stroke, OD has been identified as a significant predictor of in Table S3. the total medical costs using a stepwise multivariate analysis with a COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS | 3677 TA B L E 4 Total mean direct healthcare related and non direct healthcare related costs during acute in-­hospital admission and at 12 months’ follow-­up Risk of MN/MN at admission All patients (n = 395) Risk MN/MN (n = 92) No risk MN/MN (n = 174) p value Acute in-­hospital costs Hospitalization 4516.57 ± 2731.84 5321.0 ± 3038.0 4350.0 ± 2655.0 0.004 (ICU + neurology ward + tertiary hospital) Medication 80.01 ± 254.57 46.6 ± 149.0 93.3 ± 294.8 0.007 Enteral feeding and nutritional 2.21 ± 15.82 3.2 ± 14.3 2.4 ± 21.1 0.013 supplementation Total 4598.79 ± 2799.51 5370.0 ± 3052.0 4445.0 ± 2759.0 0.004 Risk of MN/MN at admission All patients (n = 374) Risk MN/MN (n = 88) No risk MN/MN (n = 174) Subacute costs (3 months’ follow-­up) Direct healthcare and direct non-­healthcare costs Chronic medication 232.3 ± 270.3 260.9 ± 295.6 236.4 ± 275.8 0.344 Re-­hospitalization 388.6 ± 2055.4 797.2 ± 3534.0 237.6 ± 1250.0 0.177 In-­hospital medication cost 4.7 ± 50.4 12.7 ± 100.1 2.1 ± 15.4 0.188 In-­hospital enteral feeding and nutritional 0.02 ± 0.35 0.03 ± 0.3 0.04 ± 0.5 1.000 supplementation Emergency department 14.4 ± 33.2 13.5 ± 32.5 13.6 ± 32.6 1.000 Socio-­sanitary care 641.7 ± 1628.6 821.4 ± 1998.0 575.1 ± 1310.0 0.963 Long-­term rehabilitation facilities 221.1 ± 1270.8 368.4 ± 1596.0 142.1 ± 1076.0 0.123 Nursing home 458.6 ± 1402.9 671.2 ± 1654.0 177.5 ± 932.2 0.0002 Total 1961.4 ± 3284.5 2945.0 ± 4593.0 1384.0 ± 2397.0 0.022 Total (admission + subacute) 6554.3 ± 4870.7 8145.0 ± 5868.0 5830.0 ± 4204.0 0.001 Risk of MN/MN assessed at 3 months’ follow-­up All patients (n = 374) Risk MN/MN (n = 69) No risk MN/MN (n = 162) Long-­term costs (12 months’ follow-­up) Direct healthcare and direct non-­healthcare costs Chronic medication 881.75 ± 961.48 993.4 ± 746.1 884.4 ± 1060.0 0.048 Re-­hospitalization 930.84 ± 4.423.50 930.6 ± 2837.0 478.0 ± 1664.0 0.358 In-­hospital medication cost 10.73 ± 84.88 17.51 ± 113.4 3.2 ± 24.5 0.363 In-­hospital enteral feeding and nutritional 0.09 ± 1.48 0.0 ± 0.0 0.0 ± 0.0 1.000 supplementation Emergency department 64.49 ± 120.49 93.7 ± 126.8 61.3 ± 111.5 0.029 Socio-­sanitary care 716.69 ± 2.146.19 681.3 ± 1719.0 421.0 ± 1357.0 0.068 Long-­term rehabilitation facilities 428.76 ± 2.820.82 526.9 ± 3089.0 0.0 ± 0.0 0.088 Nursing home 1464.53 ± 5002.62 2965.0 ± 7431.0 271.8 ± 2441.0 <0.0001 Total 4497.89 ± 8839.78 6029.0 ± 9018.0 2120.0 ± 3494.0 0.0008 Acute and long-­term direct healthcare and non-­healthcare costs 1-­year total costs according to risk or 9090.88 ± 9873.82 10,678.0 ± 10,446.0 6230.0 ± 4326.0 0.010 malnutrition at 3-­month follow-­up Bold indicates statistical significance value (p < 0.05). Abbreviations: ICU, intensive care unit; MN, malnutrition. beta coefficient of 1025.8 (95% confidence interval 193.9–­1857.8, was performed by Bonilha et al. in the USA. This study reported p < 0.001) in Taiwan [28]. an adjusted incremental cost at 1-­year follow-­up of US$4510 for To our knowledge, the only study that has previously reported Medicare for patients with ischaemic PS-­OD [29]. In the case of data on the long-­term adjusted effect of PS-­OD on sanitary costs respiratory infections, five previous retrospective studies reported 3678 | MARIN et al. TA B L E 5 Chronic, 12 months’ follow-­up mean total cost of patients with PS-­OD, patients at risk of malnutrition/malnutrition at 3 months’ follow-­up and patients with respiratory tract infections Acute and long-­term direct healthcare and non-­healthcare costs Well-­nourished All patients (n = 374) Risk MN/MN (n = 69) (n = 162) Non-­OD (n = 216) OD (n = 158) Comparison between OD and risk of MN/MN 1-­year total 9090.88 ± 9873.82 10,678.0 ± 10,446.0 6230.0 ± 4326.0 7242.8 ± 7402.6 11,617.6 ± 12,033.6 costs p value Risk MN/MN ** * ns Well-­nourished ns **** Non-­OD **** OD All patients (n = 374) RTI (n = 62) Non-­RTI (n = 312) Non-­OD (n = 216) OD (n = 158) Comparison between OD and RTI 1-­year total costs 9090.88 ± 9873.82 13,806.0 ± 11,834.0 8154.0 ± 9190.0 7242.8 ± 7402.6 11,617.6 ± 12,033.6 p value RTI *** **** ns Non-­RTI ns **** Non-­OD **** OD Abbreviations: MN, malnutrition; OD, oropharyngeal dysphagia; RTI, respiratory tract infection. * p < 0.05. ** p < 0.01. *** p < 0.001. **** p < 0.0001. cost increases between US$1456 and US$27,633 during hospitaliza- complications. Considering that OD, malnutrition and respiratory tion after stroke on patients who developed pneumonia, but did not infections are associated with higher costs after stroke, massive study beyond acute hospitalization [28, 30–­33]. Regarding malnu- screening and specialized management of patients with PS-­OD and trition, the prospective study performed by Gomes et al. reported malnutrition could significantly improve patient outcome and cost-­ an increase in costs during hospitalization at 6 months after stroke effectiveness. A recent Cochrane review on the treatment of PS-­OD for patients at high risk of malnutrition in the UK (£8720 vs. £4920, concluded that, whilst new treatment strategies improved swallow- p < 0.001) [34]. ing parameters, they seemed not enough to reduce clinical outcomes In our patients with PS-­OD, total mean hospitalization costs such as mortality or respiratory infections [35]. Early screening after (acute phase) were lower than subacute and long-­term chronic costs admission, accurate clinical and instrumental assessment and appro- (subacute and chronic phases) whilst in patients without PS-­OD priate compensatory and rehabilitation strategies would reduce dys- most costs occurred during hospitalization. The multivariate analysis phagia costs and complications in post-­stroke patients. showed that the long-­term costs of OD could be more related to its Costs of PS-­OD comprise acute in-­hospital and long-­term san- complications (malnutrition and respiratory infections) and the costs itary and social costs related to nutritional and respiratory com- during hospitalization due to its effect on resource consumption. plications, but also direct non-­healthcare costs and indirect costs This would explain why the chronification of OD together with the associated with loss of patient productivity and other unknown appearance of its long-­term complications is the main explanation intangible costs. In addition, the healthcare expenses related to in- for the exponential increase of costs in these patients. strumental diagnosis and treatment of PS-­OD should also be con- The early and appropriate management of PS-­OD patients is es- sidered. In centres with protocols using instrumental explorations sential in the acute phase of hospitalization and the subacute and (videofluoroscopy or fibre optic endoscopic evaluation of swallow- chronic phases of patient rehabilitation. These data agree with a ing), the costs of these explorations during the acute phase must be previously published systematic review on PS-­OD but add insights added. In centres using behavioural intervention provided by speech into the costs of OD beyond acute admission, and the impact of mal- and language therapists or neurorehabilitation strategies (electri- nutrition and respiratory infections, which are direct consequences cal or pharmacological), the cost of these treatments must also be of OD [15, 16]. The data provided in this study could be a first step considered for patients with PS-­OD. Costs related to patient stays to study the cost-­effectiveness of appropriate management of these were estimated from public prices. Costs related to patient mortality TA B L E 6 Mean total cost of PS-­OD including respiratory tract infections and risk of malnutrition/malnutrition (3 months) Non-­ Non-­OD Non-­OD OD+risk non-­risk OD + risk OD + non-­ All patients admission Non-­OD+RTI MN/MN Non-­OD non-­ MN/MN OD + RTI MN/MN 3m OD non-­RTI risk MN/MN OD V-­VST (n = 374) (n = 216) (n = 28) (n = 40) RTI (n = 188) (n = 103) OD (n = 158) (n = 34) (n = 29) (n = 124) (n = 59) Acute and long-­term direct healthcare and non-­healthcare costs 1-­year total COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS 9090.9 ± 7242.8 ± 10,550.0 ± 8055.0 ± 6750.0 ± 5726.0 ± 11,617.6 ± 16,487.0 ± 14,295.6 ± 10,282.0 ± 7111.0 ± costs 9873.8 7402.6 11,260.0 8829.0 6566.0 4070.0 12,033.6 11,603.9 11,334.5 11,851.0 4645.0 p value Non-­OD ns ns ns ns **** **** *** ** ns Non-­OD + RTI ns ns ns ns ns ns ns ns Non-­OD + MN ns ns ns ** * ns ns Non-­OD –­RTI ns **** **** *** *** ns Non-­OD –­MN **** **** *** *** ns OD ns ns ns ns OD + RTI ns ns ** OD + MN ns ns OD –­RTI ns OD –­MN Abbreviations: MN, malnutrition; OD, oropharyngeal dysphagia; PS-­OD, post-­stroke oropharyngeal dysphagia; RTI, respiratory tract infection; V-­VST, volume–­viscosity swallow test. * p < 0.05. ** p < 0.01. *** p < 0.001. **** p < 0.0001. | 3679 3680 | MARIN et al. were not measured which could lead to an artificial reduction of the editing (supporting). Jordi Valls: Conceptualization (supporting); real cost of the dysphagia group, as they had a significantly higher data curation (supporting); formal analysis (supporting); investiga- mortality. This study was performed at Mataró Hospital, a 300-­bed tion (supporting); methodology (lead); resources (supporting); su- community hospital near Barcelona that serves more than 275,000 pervision (supporting); validation (supporting). Elisabet Palomera: inhabitants. Management of all types of strokes is performed at the Conceptualization (supporting); data curation (supporting); for- emergency room and neurology ward by specialized nursing and mal analysis (supporting); investigation (supporting); methodol- medical teams and at the intensive care unit if required. Strokes can ogy (supporting); software (supporting); supervision (supporting); be treated with thrombolysis and transferred to our referral centre if validation (supporting). Ramon Cunillera: Conceptualization (sup- thrombectomy is required. The results of a prospective stroke regis- porting); data curation (supporting); formal analysis (supporting); try of patients admitted to Mataró Hospital during the last 10 years investigation (supporting); methodology (lead); resources (sup- describing the main clinical characteristics and the outcomes of porting); supervision (supporting); validation (supporting). Ernest treatment have been published [36]. Palomeras: Conceptualization (supporting); data curation (support- In summary, this study shows increased costs—­direct and re- ing); formal analysis (supporting); investigation (supporting); meth- source consumption—­during hospitalization and long-­term follow-­up odology (lead); resources (supporting); supervision (supporting); in patients with PS-­OD and/or its main complications, malnutrition validation (supporting). Josep Maria Ibáñez: Conceptualization (sup- and respiratory infections. Future studies are needed to assess cost porting); data curation (supporting); formal analysis (supporting); savings related to the correct management of PS-­OD, malnutrition investigation (supporting); methodology (lead); resources (support- and the risk of aspiration which can cause pneumonia. This increase ing); supervision (supporting); validation (supporting). Pere Clave: in the economic costs of OD is also a reflection of the severe clinical Conceptualization (lead); data curation (lead); formal analysis (lead); consequences for stroke patients with these complications. funding acquisition (lead); investigation (lead); methodology (lead); project administration (lead); resources (lead); software (lead); AC K N OW L E D G E M E N T S supervision (lead); validation (lead); visualization (lead); writing—­ This work has been conducted within the framework of a doctoral original draft (lead); writing—­review and editing (lead). thesis in medicine from the Medicine Department of the Autonomous University of Barcelona. The authors thank Dr Desiree Muriana, MD, DATA AVA I L A B I L I T Y S TAT E M E N T PhD, from the Neurology Department of Mataró Hospital for her Due to the sensitive nature of the data collected for this study, re- assistance with the performance of this study; David López Faixó, quests to access the dataset from qualified researchers trained in BPharm, from the Pharmacy Department of Mataró Hospital for his human subject confidentiality protocols may be sent to CSdM at assistance with the recompilation of in-­hospital and socio-­sanitary Professor Pere Clavé, Director of Research and Innovation. care institution medication and nutrition data; and Laura Chercoles and Jane Lewis for editing the English. ORCID Sergio Marin http://orcid.org/0000-0001-7709-6504 C O N FL I C T O F I N T E R E S T Mateu Serra-­Prat http://orcid.org/0000-0002-6554-9913 The authors affirm that there are no conflicts of interest. The spon- Omar Ortega http://orcid.org/0000-0001-6178-3748 sors had no role in the design or development of this study. Elisabet Palomera http://orcid.org/0000-0002-4384-5746 Ernest Palomeras http://orcid.org/0000-0002-0724-8653 AU T H O R C O N T R I B U T I O N S Josep Maria Ibàñez http://orcid.org/0000-0003-0366-6580 Sergio Marin: Conceptualization (lead); data curation (lead); for- Pere Clavé http://orcid.org/0000-0002-0696-8560 mal analysis (lead); investigation (lead); methodology (lead); soft- ware (lead); supervision (lead); validation (lead); visualization (lead); REFERENCES writing—­original draft (lead); writing—­review and editing (lead). 1. Rofes L, Arreola V, Romea M, et al. Pathophysiology of oropha- Mateu Serra-­Prat: Conceptualization (lead); data curation (lead); ryngeal dysphagia in the frail elderly. Neurogastroenterol Motil. 2010;22(8):851-­858, e230. formal analysis (lead); investigation (lead); methodology (lead); re- 2. Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. sources (supporting); software (supporting); supervision (lead); vali- Dysphagia after stroke: incidence, diagnosis, and pulmonary com- dation (lead); visualization (lead); writing—­original draft (supporting); plications. Stroke. 2005;36:2756-­2763. writing—­review and editing (supporting). Omar Ortega Fernández: 3. Mann G, Hankey GJ, Cameron D. Swallowing function after Conceptualization (lead); data curation (lead); formal analysis (lead); stroke: prognosis and prognostic factors at 6 months. Stroke. 1999;30(4):744-­748. investigation (lead); methodology (lead); software (lead); supervi- 4. Clavé P, De kraa M, Arreola V, Girvent M, Farré R, Palomera E, Serra-­ sion (lead); validation (lead); visualization (lead); writing—­original prat M. The effect of bolus viscosity on swallowing function in neu- draft (supporting); writing—­review and editing (supporting). Monica rogenic dysphagia. Aliment Pharmacol Ther. 2006;24:1385-­1394. Audouard Fericgla: Data curation (supporting); formal analysis (sup- 5. Cabre M, Serra-­Prat M, Palomera E, Almirall J, Pallares R, Clave P. porting); investigation (supporting); methodology (supporting); Prevalence and prognostic implications of dysphagia in elderly pa- tients with pneumonia. Age Ageing. 2010;39(1):39-­45. software (supporting); validation (supporting); writing—­review and COST OF STROKE DYSPHAGIA AND ITS COMPLICATIONS | 3681 6. Ortega O, Martín A, Clavé P. Diagnosis and management of oropha- 23. von Elm E, Altman DG, Egger M, et al. The Strengthening the ryngeal dysphagia among older persons, state of the art. J Am Med Reporting of Observational Studies in Epidemiology (STROBE) Dir Assoc. 2017;18(7):576-­582. statement: guidelines for reporting observational studies. 7. Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW. The effect Epidemiology. 2007;18:800-­8 04. of pneumonia on mortality among patients hospitalized for acute 24. Muriana D, Palomeras E, Clavé P, Álvarez-­Sabín J. Factors de risc stroke. Neurology. 2003;60:620-­625. clínics, fisiopatològics i topogràfics associats a disfàgia orofaríngia 8. Smith CJ, Kishore AK, Vail A, et al. Diagnosis of stroke-­associated en pacients amb ictus. Dipòsit Digital de Documents de la UAB. pneumonia: recommendations from the Pneumonia in Stroke https://ddd.uab.cat/recor​d/168518. Published June 01, 2016. Consensus Group. Stroke. 2015;46:2335-­2340. Accessed December 10, 2020. 9. Cabib C, Ortega O, Kumru H, et al. Neurorehabilitation strat- 25. Attrill S, White S, Murray J, Hammond S, Doeltgen S. Impact of egies for poststroke oropharyngeal dysphagia: from compen- oropharyngeal dysphagia on healthcare cost and length of stay in sation to the recovery of swallowing function. Ann N Y Acad Sci. hospital: a systematic review. BMC Health Serv Res. 2018;18(1):594. 2016;1380(1):121-­138. 26. Muehlemann N, Jouaneton B, de Léotoing L, et al. Hospital 10. Winstein CJ, Stein J, Arena R, et al. Guidelines for adult stroke re- costs impact of post ischemic stroke dysphagia: database anal- habilitation and recovery: a guideline for healthcare professionals yses of hospital discharges in France and Switzerland. PLoS One. from the American Heart Association/American Stroke Association. 2019;14(1):e0210313. Stroke. 2016;47(6):e98-­e169. 27. Wojner AW, Alexandrov AV. Predictors of tube feeding in acute stroke 11. Schepp SK, Tirschwell DL, Miller RM, Longstreth WT Jr. patients with dysphagia. AACN Clin Issues. 2000;11(4):531-­540. Swallowing screens after acute stroke: a systematic review. Stroke. 28. Chen CM, Ke YL. Predictors for total medical costs for acute hem- 2012;43:869-­871. orrhagic stroke patients transferred to the rehabilitation ward at a 12. European Society for Swallowing Disorders (2012) ESSD Position regional hospital in Taiwan. Top Stroke Rehabil. 2016;23(1):59-­66. Statements: Oropharyngeal Dysphagia in Adult Patients. www.my- 29. Bonilha HS, Simpson AN, Ellis C, Mauldin P, Martin-­Harris B, essd.org/docs/posit​ion_state​ments/​ESSD_Posit​ion_State​ments_on_ Simpson K. The one-­year attributable cost of post-­stroke dyspha- OD_in_adult_patie​nts_for_web.pdf. Accessed December 30, 2019. gia. Dysphagia. 2014;29(5):545-­552. 13. Rofes L, Muriana D, Palomeras E, et al. Prevalence, risk factors and 30. Katzan IL, Dawson NV, Thomas CL, Votruba ME, Cebul complications of oropharyngeal dysphagia in stroke patients: a co- RD. The cost of pneumonia after acute stroke. Neurology. hort study. Neurogastroenterol Motil. 2018;23:e13338. 2007;68(22):1938-­1943. 14. Patel DA, Krishnaswami S, Steger E, et al. Economic and survival 31. Christensen MC, Previgliano I, Capparelli FJ, Lerman D, Lee WC, burden of dysphagia among inpatients in the United States. Dis Wainsztein NA. Acute treatment costs of intracerebral hem- Esophagus. 2018;31(1):1-­7. orrhage and ischemic stroke in Argentina. Acta Neurol Scand. 15. Marin S, Serra-­Prat M, Ortega O, Clavé P. Cost of oropharyngeal 2009;119(4):246-­253. dysphagia after stroke: protocol for a systematic review. BMJ Open. 32. Christensen MC, Valiente R, Sampaio Silva G, et al. Acute treatment 2018;8(12):e022775. costs of stroke in Brazil. Neuroepidemiology. 2009;32(2):142-­149. 16. Marin S, Serra-­Prat M, Ortega O, Clavé P. Healthcare related cost 33. Wilson RD. Mortality and cost of pneumonia after stroke for differ- of oropharyngeal dysphagia and its complications after stroke: a ent risk groups. J Stroke Cerebrovasc Dis. 2012;21(1):61-­67. systematic review. BMJ Open. 2020;10(8):e031629. 34. Gomes F, Emery PW, Weekes CE. Risk of malnutrition is an in- 17. Rofes L, Arreola V, Mukherjee R, Clavé P. Sensitivity and spec- dependent predictor of mortality, length of hospital stay, and ificity of the eating assessment tool and the volume–­viscosity hospitalization costs in stroke patients. J Stroke Cerebrovasc Dis. swallow test for clinical evaluation of oropharyngeal dysphagia. 2016;25(4):799-­8 06. Neurogastroenterol Motil. 2014;26:1256-­1265. 35. Bath PM, Lee HS, Everton LF. Swallowing therapy for dyspha- 18. Guillén-­Solà A, Marco E, Martínez-­Orfila J, et al. Usefulness of gia in acute and subacute stroke. Cochrane Database Syst Rev. the volume–­viscosity swallow test for screening dysphagia in sub-­ 2018;10:CD000323. acute stroke patients in rehabilitation income. NeuroRehabilitation. 36. Palomeras Soler E, Fossas Felip P, Casado Ruiz V, Cano Orgaz A, 2013;33:631-­638. https://pubmed.ncbi.nlm.nih.gov/24018​371/ Sanz Cartagena P, Muriana BD. The Mataró Stroke Registry: a 10-­ 19. Registro de Altas de los Hospitales Generales del Sistema Nacional year registry in a community hospital. Neurologia. 2015;30(5):283-­ de Salud. CMBD. Norma Estatal. Ministerio de Sanidad, Consumo y 289. https://pubmed.ncbi.nlm.nih.gov/24953​4 07/ Bienestar Social. Gobierno de España. https://www.mscbs.gob.es/ estad​Estud​ios/estad​istic​as/cmbd.htm. Accessed December 30, 2019. 20. Atenció sociosanitària (convenis i contractes). Servei Català de la S U P P O R T I N G I N FO R M AT I O N Salut (CatSalut). Generalitat de Catalunya. Departament de Salut. Additional supporting information may be found online in the https://catsa​lut.gencat.cat/ca/conei​x-­catsa​lut/conve​nis-­contr​actes/​ Supporting Information section. relac​io/atenc​io-­socio​sanit​aria/. Accessed December 30, 2019. 21. Orden SCB/953/2019, de 13 de septiembre, por el que se procede a la actualización en 2019 del sistema de precios de referencia de me- How to cite this article: Marin S, Serra-­Prat M, Ortega O, et al. dicamentos en el Sistema Nacional de Salud. Agencia Estatal Boletín Oficial del Estado. Ministerio de la Presidencia, Relaciones con las Healthcare costs of post-­stroke oropharyngeal dysphagia and Cortes e Igualdad. Gobierno de España. https://www.boe.es/diario_ its complications: malnutrition and respiratory infections. Eur J boe/txt.php?id=BOE-­A-­2019-­13312. Accessed December 30, 2019. Neurol. 2021;28:3670–­3681. https://doi.org/10.1111/ 22. Actualización de rentas con el IPC general (sistema IPC base 2016) ene.14998 para periodos anuales completos. Instituto Nacional de Estadística. https://www.ine.es/calcu​la/. Accessed December 30, 2019.