Open access Original research BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Healthcare-­related cost of oropharyngeal dysphagia and its complications pneumonia and malnutrition after stroke: a systematic review Sergio Marin ‍ ‍,1,2 Mateu Serra-­Prat ‍ ‍,3,4 Omar Ortega ‍ ‍,1,4 Pere Clavé ‍ ‍1,4 To cite: Marin S, Serra-­ Abstract Prat M, Ortega O, et al. Strengths and limitations of this study Objectives To assess the healthcare costs associated Healthcare-­related cost of with poststroke oropharyngeal dysphagia (OD) and its oropharyngeal dysphagia and ►► This systematic review was performed using the complications (malnutrition, dehydration, pneumonia and Preferred Reporting Items for Systematic Reviews its complications pneumonia and malnutrition after stroke: a death). and Meta-­Analyses recommendations. systematic review. BMJ Open Design Systematic review following Preferred Reporting ►► The bibliographic research considers MEDLINE, 2020;10:e031629. doi:10.1136/ Items for Systematic Reviews and Meta-­Analyses Embase and the National Health Service Economic bmjopen-2019-031629 recommendations. Evaluation Database databases. Data sources MEDLINE, Embase and the National Health ►► A quality evaluation using an adaptation of the ►► Prepublication history and additional material for this Service Economic Evaluation Database were searched up Drummond’s tool was performed. paper are available online. To to 31 December 2019. ►► Strength of evidence was assessed using the Grading view these files, please visit Participants Patients with poststroke. of Recommendations Assessment, Development Protected by copyright. the journal online (http://​dx.​doi.​ Primary outcome measures The costs associated to and Evaluation methodology. org/​10.​1136/​bmjopen-​2019-​ poststroke OD and its complications. ►► The heterogeneity between the included studies and 031629). Data analysis Data were synthetised narratively, quality the variation on costs depending on the context pre- evaluation was done using an adaptation of Drummond’s cluded a quantitative data synthesis. Received 16 May 2019 Revised 03 March 2020 checklist and Grading of Recommendations Assessment, Accepted 28 May 2020 Development and Evaluation recommendations were used to assess strength of evidence. Results A total of 166 articles were identified, of Introduction which 10 studies were included. The cost of OD during Oropharyngeal dysphagia (OD) is a common the hospitalisation was assessed in four studies. One condition in patients with poststroke, as a prospective study showed an increase of US$6589 for result of the brain injuries suffered.1 Inci- patients requiring tube feeding. Two retrospective studies dence is high (37%–78%) in the acute phase2 found higher costs for those patients who developed OD, and, while improvements can be observed (US$7329 vs US$5939) among patients with haemorrhagic in many patients during the first weeks after stroke transferred to inpatient rehabilitation and an stroke, OD persists as a chronic condition in increase of €3000 (US$3950) and SFr14 000 (US$15 300) nearly 50% and complications arise.3 The in hospitalisation costs. One study did not found OD as latest editions of the International Classifi- a predictor for total medical costs in the multivariate cation of Diseases (ICD) and Related Health analysis. One retrospective study showed an increase of US$4510 during the first year after stroke for those Problems promoted by WHO ICD-9 and patients with OD. For pneumonia, five retrospective studies ICD-10 classifies poststroke OD with specific showed an increase in hospitalisation costs after stroke codes I-69.391.4 of between US$1456 and US$27 633. One prospective OD can have a high impact on the general study showed an increase in hospitalisation costs during health of affected patients and can produce © Author(s) (or their 6 months after stroke in patients at high malnutrition risk. two main types of complications in patients employer(s)) 2020. Re-­use Strength of evidence was considered moderate for OD and with poststroke: (1) those caused by impaired permitted under CC BY-­NC. No commercial re-­use. See rights pneumonia and low for malnutrition. efficacy of swallow, present in 25%–75% of and permissions. Published by Conclusions This systematic review shows moderate patients, which leads to malnutrition and BMJ. evidence towards higher costs for those patients who dehydration5 and (2) impaired safety of For numbered affiliations see developed OD after stroke. The available literature is swallow which leads to tracheobronchial end of article. heterogeneous, and some important aspects have not aspiration that may cause pneumonia in been studied yet. Further studies are needed to define the Correspondence to 50% of cases.6–10 Both OD and aspiration specific cost of poststroke OD. Dr Sergio Marin; are highly prevalent conditions in patients PROSPERO registration number CRD42018099977. ​sergiomarinrubio@​gmail.​com with stroke.2 6 A recent study on patients with Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 1 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. stroke has shown a prevalence of OD of 45.06% on admis- (malnutrition, dehydration, aspiration pneumonia and sion, and that OD after stroke was an independent risk death) in patients with stroke was performed. The main factor for prolonged hospital stay and institutionalisa- outcome of interest was the additional costs attributable tion after discharge. Moreover, this study has shown that to poststroke OD and its complications during the hospi- OD was independently associated with poorer functional talisation and follow-­up after discharge. Task organisa- capacity and increased mortality 3 months after stroke.6 A tion in this systematic review including those processes significant increase in length of stay and a poor prognosis performed by two or more authors (selection of studies, has also been observed by other authors in patients with data extraction, quality assessment) is explained in the poststroke OD.11 The impact of all these complications protocol of this systematic review. on the costs of poststroke OD is still unknown. The state-­of-­ the-­ art of OD management in patients Patient and public involvement statement with poststroke aims for early detection, with swallowing There was no public or patient involvement in the elabo- being assessed in the first hours after stroke diagnosis12 ration of this systematic review. in order to prevent the potential complications of OD. Search strategy Application of specific explorations in the acute setting, We searched Medline, Embase and the National Health therapy development aimed at compensating deficient Service Economic Evaluation Database (NHS EED) up mechanisms related to this pathology and the recovery until 31 December 2019. The references of the studies of swallowing function in these patients in the long term included were further revised to identify possible addi- are key aspects of the management of this condition.13 tional eligible studies. Used search terms are available in Poststroke OD is an underdiagnosed and undertreated the protocol of this systematic review and in the online condition and the most appropriate care is not avail- supplementary appendix.17 18 able for most patients. Significant reductions in rates of pneumonia (9.0% vs 2.8%) and mortality (7.4% vs 4.2%) Eligibility criteria have been demonstrated through screening and basic Studies were included if they were cost studies, studies OD treatment application and is reflected in antibiotic that provide information on costs in adult (>17 years) expenditure with significant savings of around 50%.14 patients with stroke with OD and/or its complications Protected by copyright. The treatment paradigm for poststroke OD is changing or economic evaluation studies in which the cost of the from compensatory strategies, which aim to compensate disease was estimated. Studies were excluded if they deficient mechanisms related to OD by using fluid adap- were not related to OD or if they refer to oesophageal tation and postural changes, to the recovery of swallowing dysphagia or OD caused by causes other than stroke. function with the promotion of brain plasticity with Full-­text assessments were done in order to reject those neurorehabilitation techniques such as transcutaneous or ones not fulfilling all selection criteria. Two independent intrapharyngeal electrical stimulation, repetitive transcra- reviewers participated in this process. In case of disagree- nial magnetic stimulation and transcranial direct current ment over one or more studies, a third reviewer revised stimulation. These neurorehabilitation strategies are still the study and a final consensus was made. A posterior task in the research phase but can already be perceived as an was carried out to identify possible duplicated informa- important progress in poststroke OD management.15 tion between the articles. Costs related to poststroke OD comprise acute in-­hos- Data presentation and summary measures pital and long-­term sanitary costs, direct non-­healthcare Data were reported in its original format using tables costs, indirect costs such as productivity losses and intan- and narrative. A narrative method was used to synthe- gible costs. In the recent years, more data on the cost of sise this evidence. Results are presented according to poststroke OD has become available. However, no system- the following order: (1) costs related to poststroke OD, atic literature review has been conducted as yet on this (2) costs related to OD complications in the following topic. The objective of this systematic review is to assess order: (A) aspiration, (B) pneumonia, (C) malnutrition, and summarise all the evidence on the cost related to OD (D) dehydration and (E) death. A synthesis of studies and its complications (malnutrition, dehydration, aspira- separating acute and long-­ term costs was performed. tion pneumonia and death) in patients with poststroke. Whenever feasible, data on cost adjusted for the stroke This study is a first step towards establishing the cost severity (according to National Institutes of Health Stroke benefits of appropriate management of poststroke OD as (NIHSS) or Canadian scale) or other confounding factors an aspect to be taken into consideration by healthcare were considered. Information was presented following decision-­makers. recommendations of the Centre for Reviews and Dissem- ination.19 Results were also discussed as those assessing cost during the hospitalisation compared with cost after Methods discharge and long-­term follow-­up. This systematic review was carried out using methodology Preferred Reporting Items for Systematic Reviews and Quality evaluation and strength of the evidence Meta-­Analyses.1617 18 In summary, a systematic review of In this study, we used an adaptation of Drummond’s check- studies related to the cost of OD and its complications list in order to assess the risk of bias and the reporting 2 Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Table 1 Main design characteristics Quality assessment* (%) (yes (1)+partly Time horizon and Country, year (0.5)/total Study ID Aim Study population Design perspective and currency applicable)x100 Wojner22 Cost of TF Ischaemic and Prospective Hospitalisation time USA 50 AACN Clin Issues haemorrhagic Hospital 1995–1996 2000 stroke perspective USD (year not ≥18 years available) Katzan27 Cost of Ischaemic and Retrospective Hospitalisation time USA 69 Neurology pneumonia haemorrhagic Hospital 1991–1997 2007 stroke perspective 2000 USD Christensen28 Cost of Ischaemic and Retrospective Hospitalisation time Argentina 75 Acta Neurol Scand 2009 pneumonia haemorrhagic Hospital 2004–2006 stroke perspective 2005 USD ≥21 years Christensen29 Cost of Ischaemic and Retrospective Hospitalisation time Brazil 83 Neuroepidemiology 2009 pneumonia haemorrhagic Hospital 2006–2007 stroke perspective 2005 USD ≥21 years Wilson Cost of Ischaemic and Retrospective Hospitalisation time USA 67 J Stroke Cerebrovasc Dis pneumonia haemorrhagic Hospital 2005–2006 201230 stroke perspective 2009 USD ≥18 years Bonilha23 Cost of OD Ischaemic stroke Retrospective One year USA 80 Dysphagia ≥65 years poststroke 2004 2014 Financer 2014 USD Protected by copyright. perspective Chen24 Cost of OD Ischaemic stroke Retrospective Hospitalisation time Taiwan 67 J Rehabil Med Transferred to Hospital and patient 2002–2012 2015 a rehabilitation perspective 2013 USD ward during hospitalisation Chen25 Cost of OD Haemorrhagic Retrospective Hospitalisation time Taiwan 64 Top Stroke Rehabil 2016 cost of stroke Hospital and patient 2002–2012 pneumonia Transferred to perspective USD (year not a rehabilitation available) ward during hospitalisation Gomes31 Cost of Ischaemic and Prospective 6 months after England 69 J Stroke Cerebrovasc Dis malnutrition haemorrhagic stroke 2011–2012 2016 stroke Hospital GBP (year not ≥18 years perspective available) Muehlemann26 Cost of OD Ischaemic stroke Retrospective Hospitalisation France and 80 PLoS One Hospital Switzerland 2019 perspective 2012 2013 Euros and Swiss Francs *Quality assessment: a higher score indicates a lower risk of bias. OD, oropharyngeal dysphagia; TF, tube feeding. quality for each study only using the points in the checklist studies in this systematic review is presented in table 1 that were applicable to cost studies.20 Each of these points and expanded in the online supplementary appendix. In was rated as: yes, no, partly, not available or not applicable. addition, we rated the quality of evidence across studies as Two independent reviewers participated in this process. high, moderate, low or very low using Grading of Recom- A global score presented as a percentage was calculated mendations Assessment, Development and Evaluation for each study dividing the total number of points rated methodology.21 The hypothesis of this systematic review as ‘yes’ (‘partly’ counted as 0.5) between the total points is that OD and its main complications are related to high applicable for each study. No study was excluded from costs in patients with poststroke. If a study demonstrated this review based on risk of bias results. A higher score significantly higher costs for patients with poststroke who indicates a lower risk of bias. Quality assessment of the developed OD than for those who did not, higher costs Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 3 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. design. Studies’ sample size ranged from 171 to 68 334 participants and the mean age of participants ranged from 61.3 to 78.1 years.22–26 Two studies were performed in the USA,22 23 two were performed in Taiwan,24 25 and one was performed in France and Switzerland.26 The US studies and the study performed in France and Switzer- land were cost analysis studies22 23 26 and the Taiwanese studies were cost prediction studies.24 25 Incidence of OD ranged from 4.2% to 65.9%. Screening for OD on admission was performed only in the study by Wojner and Alexandrov.22 One study analysed hospitalisation costs in patients depending on tube feeding (TF) from a hospital perspective.22 One study analysed hospital care, nursing home, care provider, home health, outpatient and durable medical equipment costs during the first year after ischaemic stroke and from the perspective of Medicare.23 Two studies analysed hospital costs including diagnoses, ward, laboratory, X-­ rays, therapeutic and surgical procedures, blood/plasma, anaesthesia, special materials, TF, rehabilitation, drugs, dispensing and injec- tion services, haemodialysis and psychiatric treatment Figure 1 Selection process flow diagram. NHS EED, for patients transferred to a rehabilitation ward after National Health Service Economic Evaluation Database; OD, ischaemic24 and haemorrhagic25 stroke from the hospital oropharyngeal dysphagia. and patient perspectives. One study analysed the cost of hospital stay from the hospital perspective.26 Wojner and Alexandrov found significantly higher Protected by copyright. for those who develop a complication related to OD or an costs during the hospitalisation for those patients who effect of OD or its complications on total costs of stroke, depended on a TF. Mean hospitalisation costs were the study was qualified as a ‘positive study’. US$12 538±US$6247 for those patients who depended on a TF and US$5949±US$3428 for those who did not Results (p<0.0001), suggesting a non-­ adjusted effect of TF of In the data base search, 121 articles were identified using approximately US$6300. The study also showed that those the search terms (67 through Medline using PubMed, 12 patients depending on a TF were older, with a greater through Embase using Ovid and 42 through NHS EED) neurological impairment and had longer hospital stays. and 45 articles were identified through reference check. NIHSS score was found to be an independent risk factor A total of 166 studies were assessed in the selection phase. for TF dependency.22 Bonilha et al found an increase of After screening both title and abstract of these articles, US$4510 (p<0.0001) on the total medical costs during the 108 articles were excluded because they did not provide first year after stroke for patients with ischaemic stroke information on poststroke OD costs or those of its compli- who developed OD, controlling for age, comorbidities, cations or at least minimal relevant information on this ethnicity and time alive. Nevertheless, stroke severity was aspect. A second evaluation phase was carried out with the not shown as a significant independent predictor for the 58 remaining studies. After this second evaluation phase, cost model.23 Chen et al examined the predictors for total 48 articles were excluded because they did not meet the medical costs in first ischaemic stroke patients transferred criteria for inclusion (4 were duplicated articles, 38 did to a rehabilitation ward in Taiwan. In this study, OD was not provide information on costs and 6 did not refer significantly related with total medical costs during hospi- to OD) and 10 articles were included in this systematic talisation in the univariate analysis but not in the multi- review (figure 1). Included study data and features were variate analysis. Significant predictors for total medical summed up and presented in both a narrative presen- costs after multivariate analysis were: impaired conscious- tation and evidence (tables 1–4). A great heterogeneity ness, hypoalbuminaemia, fever, hypokalaemia and hypo- regarding the economic design among studies was found natraemia. Mean total costs for dysphagia patients during (mainly among study perspective, type of included costs the hospitalisation were 5134.5±3064.6, and total medical and follow-­up time). Results were, therefore, not compa- costs for all patients (including those who already had rable and studies were evaluated separately. dysphagia) were US$4606.8±US$2926.1.24 Following the same methodology and perspectives, Chen et al exam- Costs of OD after stroke ined the predictors for total medical costs in patients Five studies have assessed the cost of OD in patients with with a first haemorrhagic stroke event. This study shows stroke from different perspectives and using different that OD is related to a significant increase in the total methodologies. These five studies had a longitudinal medical costs with a beta coefficient of 1025.8 (95% CI 4 Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Table 2 Specific characteristics of included studies Epidemiological design characteristics: Economic design characteristics: (a) Type of study (a) Analysis perspective Elements of cost considered: (b) Epidemiological approach (b) Use of temporary discount (a) Direct healthcare costs (c) Data gathering rate (b) Direct non- healthcare costs Study ID (d) Time horizon (c) Sensitivity analysis Data source (c) Indirect costs Wojner22 a. Cost analysis. a. Hospital perspective. Data collected from medical a. Yes. Hospitalisation costs. AACN Clin Issues b. Longitudinal. b. Not available. records and the hospital’s cost b. No. 2000 c. Prospective. c. Not available. accounting system. c. No. d. Hospitalisation time. Katzan27 a. Cost analysis. a. Hospital perspective. Data collected from the Cleveland a. Yes. Hospitalisation costs. Neurology b. Longitudinal. b. Not available. Health Quality Choice Programme b. No. 2007 c. Retrospective. c. Not available. from non-­federal hospitals in c. No. d. Hospitalisation time. northeast Ohio. Patient charges were obtained from Medicare files. Christensen28 a. Cost analysis. a. Hospital perspective. Medical records. Costs data were a. Yes. Hospitalisation costs. Acta Neurol Scand 2009 b. Longitudinal. b. Not available. obtained from FLENI database. b. No. c. Retrospective. c. Yes. c. No. d. Hospitalisation time. Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Christensen29 Neuroepidemiology 2009 a. Cost analysis. a. Hospital perspective. Medical records. Costs data were a. Yes. Hospitalisation costs. b. Longitudinal. b. Not available. obtained from Sistema Único de b. No. c. Retrospective. c. Yes. Saúde, 2007 values. c. No. d. Hospitalisation time. Wilson a. Cost analysis. a. Hospital perspective. Data collected from the 2005 a. Yes. Hospitalisation costs. J Stroke Cerebrovasc Dis b. Longitudinal. b. Not available. and 2006 Nationwide Inpatient b. No. 201230 c. Retrospective. c. Not available. Sample from the United States. c. No. d. Hospitalisation time. Bonilha23 a. Cost analysis. a. Financer perspective. Data collected from South a. Yes, hospital care, nursing home, Dysphagia b. Longitudinal. b. Not available. Carolina Medicare database. provider, home health, outpatient 2014 c. Retrospective. c. Not available. and durable medical equipment. d. One year poststroke. b. No. c. No. Chen24 a. Predictors of cost study. a. Hospital and patient Medical records and the hospital’s a. Yes, hospital costs including J Rehabil Med b. Longitudinal. perspective. management information system. diagnoses, ward, laboratory, X-­ 2015 c. Retrospective. b. Not available. rays, therapeutic and surgical d. Hospitalisation time. c. Not available. procedures, blood/plasma, anaesthesia, special materials, tube feeding, rehabilitation, drugs, dispensing and injection services, haemodialysis and psychiatric treatment. b. No. c. No. Continued Open access 5 Protected by copyright. BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. 6 Open access Table 2 Continued Epidemiological design characteristics: Economic design characteristics: (a) Type of study (a) Analysis perspective Elements of cost considered: (b) Epidemiological approach (b) Use of temporary discount (a) Direct healthcare costs (c) Data gathering rate (b) Direct non- healthcare costs Study ID (d) Time horizon (c) Sensitivity analysis Data source (c) Indirect costs Chen25 a. Predictors of cost study. a. Hospital and patient Medical records and the hospital’s a. Yes, hospital costs including Top Stroke Rehabil 2016 b. Longitudinal. perspective. management information system. diagnoses, ward, laboratory, X-­ c. Retrospective. b. Not available. rays, therapeutic and surgical d. Hospitalisation time. c. Not available. procedures, blood/plasma, anaesthesia, special materials, tube feeding, rehabilitation, drugs, dispensing and injection services, haemodialysis and psychiatric treatment. b. No. c. No. Gomes31 a. Cost predictors. a. Hospital perspective. Medical records. Cost data was a. Yes. Hospitalisation costs. J Stroke Cerebrovasc Dis b. Longitudinal. b. Not available. obtained from the Department of b. No. 2016 c. Prospective. c. Yes. Health Payment by Results Tariff c. No. d. 6 months after stroke. Information Spreadsheet. Muehlemann26 a. Cost analysis. a. Hospital perspective. Data collected from the French a. Yes. Hospitalisation costs. PLoS One b. Longitudinal. b. Not available. Medical Information System b. No. 2019 c. Retrospective. c. Not available. Programme and the Swiss OFS c. No. d. Hospitalisation time. Database ‘Office federal de la statistique: Statistique des couts par cas 2012’. Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Protected by copyright. BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Table 3 Specific characteristics of study populations OD and/or complication Previous OD or stroke in Study ID Age and gender Patient inclusion or exclusion criteria Method of OD diagnostic incidence patients Wojner22 Age: Inclusion criteria: Dysphagia screening on TF dependence prevalence during Not available. AACN Clin Issues Overall 67.2 (14.3)* ►► ≥18 years. admission and during hospitalisation: 30 (17.54).† 2000 TF dependency 72.7 (13.9)* ►► Haemorrhagic or ischaemic stroke hospitalisation .The assessment No TF: 64.8 (13.4)* Exclusion criteria: method was not described. Gender (male): ►► Subarachnoid haemorrhage. Overall 80 (46.78%)† ►► Aneurism or intravenous deformation. ►► Craniotomy management. Katzan27 Age: Inclusion criteria: Not available. Dysphagia: Not available. Neurology Total: 76.8 (8.14)* ►► Haemorrhagic or ischaemic stroke Not available. 2007 Pneumonia: 77.6 (8.24)* Exclusion criteria: Pneumonia (%): No pneumonia: 76.7 (8.13)* ►► Patients with a code of ‘occlusion/ Hospitalisation: 5.6 Gender (female): stenosis of precerebral artery’ (ICD- Total: 6.405 (56.7)† 9 433). Pneumonia: 266 (41.9)† ►► Died within 3 days of admission. No pneumonia: 6.139 (57.6)† ►► Those in which medical records of 3 days of admission could not be recovered. Christensen28 Age: Inclusion criteria: Not available. Dysphagia: Only first haemorrhagic or Acta Neurol Scand 2009 Ischaemic stroke: 64.8 (15.5)* ►► ≥21 years. Not available ischaemic stroke patients. Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Haemorrhagic stroke: 61.8 ►► First-­ever ischaemic or Pneumonia : Presence of previous dysphagia (15.5)* haemorrhagic stroke according to Not available was not recorded. Gender (male, %): brain image. Ischaemic stroke: 66.7 Exclusion criteria: Haemorrhagic stroke: 58.6 ►► Previous stroke. Christensen29 Neuroepidemiology 2009 Age: Inclusion criteria: Not available. Dysphagia: Only first haemorrhagic or Ischaemic stroke: 61(14)* ►► ≥21 years. Not available ischaemic stroke patients. Haemorrhagic stroke: 64(13).* ►► First-­ever ischaemic or Pneumonia (%): Presence of previous dysphagia Gender (male): haemorrhagic stroke according to Hospitalisation: 6 was not recorded. Ischaemic stroke: 145(54)† brain image. Haemorrhagic stroke: 26(60).† Exclusion criteria: ►► Previous stroke. Wilson Age (mean): Inclusion criteria: Not available. Dysphagia: Not available. J Stroke Cerebrovasc Dis Pneumonia: 73.3 ►► Stroke Hospitalisation: 201230 No pneumonia: 70.6 Exclusion criteria: Pneumonia: 0.43 Gender (female, %): ►► Died within 3 days of admission. No pneumonia: 0.115 Pneumonia: 49.4 ►► <18 years. Pneumonia (%): No pneumonia: 54.6 ►► Patients who had missing values. Hospitalisation: ►► Hospitalisation in Texas on 2005. 8.1 (95% CI. 7.8 to 8.3) Bonilha23 Age: Inclusion criteria: Not available. Dysphagia: Not available. Dysphagia Overall: 78.1 (6.9)* Primary diagnosis of ischaemic stroke. Hospitalisation: 317 (9.9%) 2014 OD: 79.4 (6.7)* Exclusion criteria: patients.† No OD: 78.0 (6.9).* ►► <65 years. Gender (male): ►► A complication associated to a Overall: 1228 (38.4)† previous stroke. OD: 118 (37,2)† ►► Ethnicity data missed. No OD: 1110 (38.5)† ►► Cost data not available. Continued Open access 7 Protected by copyright. BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. 8 Open access Table 3 Continued OD and/or complication Previous OD or stroke in Study ID Age and gender Patient inclusion or exclusion criteria Method of OD diagnostic incidence patients Chen24 Age: Inclusion criteria: Examination or bedside test Dysphagia: Only first ischaemic stroke J Rehabil Med Overall: 68.9 (12.2)* ►► First-­time ischaemic stroke performed by a physiatrist. Admission: 205 (65.9)† patients. Presence of previous 2015 Gender (male): according to WHO criteria. dysphagia was not recorded. Overall: 137 (44.1)† ►► Transferred to a rehabilitation ward from acute ward during hospitalisation. ►► Discharged from the rehabilitation ward. Chen25 Age: Inclusion criteria: Examination or bedside test Dysphagia: Only first haemorrhagic stroke Top Stroke Rehabil 2016 Overall: 61.3 (13.5)* ►► First-­time haemorrhagic stroke. performed by a clinician. Hospitalisation: 118 (49.8)† patients. Presence of previous Gender (male): ►► Transferred to a rehabilitation ward . dysphagia was not recorded. Overall: 137 (57.8%)† ►► Discharged from the rehabilitation ward. Gomes31 Age (mean): Inclusion criteria: Screening test (not specified) by Dysphagia (%): Presence of previous dysphagia J Stroke Cerebrovasc Dis Overall: 74.5 ►► ≥18 years. nurses on admission. Low RoM: 19 was not recorded. 22% of the 2016 Gender (male, %): ►► Not pregnant. Medium RoM: 26 patients had a previous stroke. Overall: 51 ►► Stroke diagnosis. High RoM: 61 ►► National Health Service No. RoM: 156/537(29)† were at high RoM Muehlemann26 Age (mean): Inclusion criteria: Not available. Dysphagia (%): Not available. PLoS One Not available. -Cerebral infarction or sequelae of Hospitalisation: 4.2 (France), 8.4 2019 Gender (male, %): cerebral infarction. (Switzerland). OD: 47% No OD:52% (France) Exclusion criteria: OD: 51% No OD: 55% ►► Subarachnoid haemorrhage, (Switzerland) intracerebral haemorrhage, non-­traumatic intracerebral haemorrhage, transient ischaemic attack and related symptoms as secondary diagnoses. ►► Head and neck cancer, dementia, Parkinson’s disease, multiple sclerosis or other acute brain injury. *Values are mean (SD). †Values are n (%). ICD, International Classification of Diseases ; OD, oropharyngeal dysphagia; RoM, risk of malnutrition; TF, stands for tube feeding. Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Protected by copyright. BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Table 4 Results of individual studies Adjusted Sample incremental Study ID Aim size Crude incremental costs P value costs P value 22 Wojner Cost of TF 171 Mean cost for TF patients: <0.0001 – – AACN Clin Issues US$12 538±US$6247. 2000 Mean cost for non-­TF patients: US$5949±US$3428=. Katzan27 Cost of 11 286 US$14 901 (95% CI – US$14 836 (95% – Neurology pneumonia US$14 279 to US$15 524) CI US$14 436 to 2007 US$15 236 Christense28 Cost of 167 Ischaemic stroke: =0.003 – – Acta Neurol Scand 2009 pneumonia US$36 149 – Haemorrhagic stroke: =0.003 US$16 893 Christensen29 Cost of 316 Ischaemic stroke: <0.001 US$1456 <0.001 Neuroepidemiology 2009 pneumonia Mean cost for non-­ – pneumonia patients: US$1776. =0.015 Mean cost for patients who developed pneumonia: US$4251. Haemorrhagic stroke: Mean cost for non-­ pneumonia patients: US$3553. Mean cost for patients who Protected by copyright. developed pneumonia: US$8485. Wilson Cost of 183 976 US$23 102 – US$27 633 (95% – J Stroke Cerebrovasc Dis pneumonia CI US$27 078 to 201230 US$27 988) Bonilha23 Cost of OD 3200 Mean total payments for OD <0.0001 Mean adjusted <0.0001 Dysphagia patients: total payments 2014 US$22 379±US$14 250 for OD patients: Mean total payments for US$22 266 (95% non-­OD patients: CI US$20 839 to US$18 560±US$14 429 US$23 787) Crude incremental costs: Mean adjusted US$3819 total payments for non-­OD patients: US$17 756 (95% CI US$17 372 to US$18 150) Adjusted incremental costs: US$4510 Chen24 Cost of OD 311 Mean cost for OD patients: <0.001 – – J Rehabil Med US$5134.5±US$3064.6 2015 Mean patients cost: US$4606.80±US$2926.1. Chen25 Cost of OD 237 Mean cost for OD patients:  <0.001 – – Top Stroke Rehabil 2016 Cost of US$7329.2±US$3977.2.  <0.001 pneumonia Mean cost for patients who developed pneumonia: US$9053.7±US$5142.0. Mean patients cost: US$5939.5±US$3578.5D Continued Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 9 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. Table 4 Continued Adjusted Sample incremental Study ID Aim size Crude incremental costs P value costs P value 31 Gomes Cost of 543 Median costs low-­risk <0.001 – – J Stroke Cerebrovasc Dis malnutrition patients: 4920 (£ 437–£38 2016 200) Median costs medium-­risk patients: 6490 (£1050–£19 600) Median costs high-­risk patients: 8720 (£552–£31 900) Muehlemann26 Cost of OD 62 297 (F) 2926 euros (F) – – – PLoS One 6037 (S) 13 959 Swiss Francs (S) 2019 F, France; OD, oropharyngeal dysphagia; R, range minimum-­maximum; S, Switzerland; TF, tube feeding. 193.9 to 1857.8; p<0.001). Total cost for OD patients was during the hospitalisation of US$14 863 (95% CI 14 436 US$7329.2±US$3977.2 while total medical cost for all to 15 236) adjusting for stroke severity, stroke patients’ patients (including those who already had OD or pneu- propensity for pneumonia and other factors associated monia) was US$5935.5±US$3578.5.25 Muehlemann et with higher hospitalisation costs. Pneumonia was more al found an incremental cost for patients who had OD commonly identified in those patients with a more severe of €3000 (approx. US$4300, 2019 USD) in France and stroke (p<0.001).27 Wilson found an additional adjusted SFr14 000 (approx. US$16 900, 2019 USD) in Switzerland. cost of US$27 633 (95% CI 27 078 to 27 988) for a pneu- Protected by copyright. OD was associated with a significant increase in hospital monia episode during hospitalisation after stroke. Costs costs during admission after adjusting for the presence of were adjusted for age, gender, hospital factors (teaching, motor or/and sensory stroke complications (p<0.0001).26 rural, urban), admission from emergency department, illness severity, propensity for pneumonia and comorbidi- Cost of poststroke safety of swallow complications: ties.30 Christensen et al estimated that patients who devel- pneumonia oped pneumonia incurred significantly higher costs in We found five studies that evaluated the cost of pneu- both ischaemic (US$36 149; p=0.003), and haemorrhagic monia in patients with stroke,25 27–30 one of which has stroke (US$16 893; p=0.003) in Argentina.28 Finally, been previously mentioned for providing information in the Christensen et al study performed in Sao Paulo, on the cost of OD after stroke.25 These five studies had Brazil, an increase in hospitalisation cost for patients who a longitudinal, retrospective cost analysis design with developed pneumonia was observed for haemorrhagic sample sizes between 167 and 183 976 participants with stroke (US$8485 vs US$3553; p=0.015) and for ischaemic a mean age of 61.3–76.8 years.25 27–30 Two studies were stroke (US$4251 vs US$1776; p<0.001). Development of performed in the USA,27 30 one in Taiwan,25 one in Argen- pneumonia during admission was found to be a signifi- tina28 and one in Brazil.29 Presence of OD among anal- cant independent predictor of acute treatment costs in ysed patients was reported in two studies.25 30 Chem et al the multivariate analysis. An adjusted cost of pneumonia found that 49.8% of the assessed patients suffered OD of US$1456 was found when adjusting for all patient and during hospitalisation25 and Wilson et al found that OD treatment characteristics (p<0.001).29 was present in 42.9% of patients who developed pneu- monia and in 11.5% of those who did not (p<0.0001).30 Cost of poststroke efficacy of swallow complications: Pneumonia incidence ranged from 5.6% to 8.1%25 27–30 malnutrition The studies, except for the one performed by Chen and Gomes et al aimed to assess the validity of a nutrition-­ Ke,25 analysed hospitalisation costs after stroke from the screening tool (Malnutrition Universal Screening Tool) hospital perspective.27–30 to predict poor outcomes and hospitalisation costs in Chen and Ke showed that pneumonia was related to a patients after a stroke episode. A total of 543 patients were significant increase in the total medical costs with a beta enrolled in a longitudinal, prospective study. Costs were coefficient of 2330.1 (95% CI 1339.5 to 3320.7; p<0.001). measured during 6 months after stroke from a hospital Total cost for patients who developed pneumonia was perspective. Mean age of participants was 74.5 years. The US$9053.7±US$5142.0 while total medical cost for all study was performed in London in two hyperacute stroke patients (including those who already had pneumonia) units and compared the hospitalisation costs according to was US$5939.5±US$3578.5.25 Katzan et al showed an risk of malnutrition. The study showed that an increase in incremental cost for patients who developed pneumonia malnutrition risk involved an increase in hospitalisation 10 Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. costs, from £4920 sterling (GBP) 2011 (approx. US$8780, underdiagnosed. We suspect that OD and/or pneumonia 2019 USD) in low risk patients to £8720 (approx. US$15 underdiagnosis could occur in some studies due to the 560, 2019 USD) in high-­risk patients (p<0.001). Risk of absence of screenings for OD and low codification of malnutrition was identified as an independent predictor these events in the databases. for hospitalisation costs. Moreover, the study showed an association between high risk of malnutrition and inade- Confidence in cumulative evidence quate swallow on hospital admission.31 In the case of OD, one prospective and four retrospec- tive studies were assessed. The risk of bias ranged from Synthesis of the study’s findings 50 to 80. High consistency with a large and direct effect Short-term cost of OD and its complications during hospital was found among the results of four studies. In the study admission performed by Chen et al, OD was significantly correlated In the case of patients admitted to a rehabilitation ward with the total medical costs in univariate analysis but not due to haemorrhagic stroke, the median cost for those in multivariate analysis so we have not qualified this study who developed OD was US$7329.2 while for the entire as a positive study.24 We consider the level of evidence sample it was US$5939.5.25 In the case of ischaemic stroke regarding higher costs related to poststroke OD to be patients admitted to a rehabilitation ward, OD was not moderate. In the case of pneumonia, we also consider the identified as a predictor for the total medial costs in the level of evidence in favour of higher costs related to this multivariate analysis. An additional cost for those patients complication to be moderate based on the five retrospec- may be US$528 per case.24 For patients who needed TF, tive positive studies. The risk of bias punctuation ranged an approximate increase of US$6300 was observed.22 from 64 to 83. Despite the fact that the longitudinal design For patients hospitalised in France and Switzerland after of the considered studies indicates moderate strength of stroke an increase of €3000 and SFr14 000 was observed.26 scientific evidence, a high consistency with a large and In the five studies reporting data on the cost of pneu- direct effect was found among the results of the different monia after stroke, an adjusted effect of pneumonia on studies. In the case of malnutrition, we only found one costs during hospitalisation after stroke was found to prospective study and the level of evidence was low. be between US$1456 and US$27 633 depending on the Protected by copyright. setting and the design of the study.25–30 Discussion Long-term cost of OD and it’s complications including post hospital This systematic review shows moderate quality evidence discharge costs towards higher costs for those patients who developed We found only two studies assessing cost related to OD OD or pneumonia after stroke. Acute in-­hospital costs or it’s complications beyond the first hospital stay due to related to OD were analysed in five studies. Despite this, acute stroke. The study performed by Bonilha et al found design and results were very different across studies and an increase of US$4510 for those patients who developed it is difficult to show definitive conclusions as a quantita- OD during the first year after acute stroke.23 In malnutri- tive synthesis of the results cannot be made. The results tion, Gomes et al showed an increase in all hospitalisation of these economic studies do not match recent clinical costs during the first 6 months after stroke. These costs studies that clearly show OD after stroke is an indepen- increased from £4920 (approx.US$8780, 2019 USD) in dent risk factor for prolonged hospital stay and institu- low risk of malnutrition patients to £8720 (approx. US$15 tionalisation after discharge; OD has been shown to be 560, 2019 USD) in high-­risk patients.31 an independent risk factor for poorer functional capacity and increased mortality 3 months after stroke.6 A recent Quality assessment study performed in the USA also related OD to longer Risk of bias was assessed for each study. Total scores for length of stay, higher inpatient costs and likelihood of each study are available in table 1 and specific results being transferred to postacute care facility and inpatient for each study are available in the online supplementary mortality during hospitalisation.32 Monetisation of these appendix. Productivity losses secondary to the pathology poor clinical outcomes specifically caused by OD is urgent were not assessed in any of the studies and quantities of and would probably indicate specific incremental costs consumed resources were only reported by Christensen for OD. Regarding the costs of pneumonia, Christensen et al and Muehlemann et al and separately from their et al showed, in Brazil and Argentina, an increase in hospi- unit costs26 28 Methods for the estimation of quantities talisation costs for stroke patients who developed pneu- and units costs were barely described in the studies, the monia of between US$1456 and US$36 149 depending on studies by Katzan et al and Christensen et al were the only the type of the stroke and the country.28 29 These higher ones to completely include them.27–29 A sensitivity analysis health costs more closely approximate what we estimate was only offered in the studies by Christensen et al and could be the increment in costs from OD and pneumonia Gomes et al.28 29 31 The majority of data for these studies from the clinical trials we are performing: US$27 633 to was retrospectively obtained from databases based on US$36 149 seem reasonable and can be translated to a diagnosis codes. This can cause major information loss 2019 USD value of US$32 500 to US$48 000. In the study when calculating a disease cost as some conditions are performed by Gomes et al, an association between OD Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 11 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. and malnutrition is observed on admission. However, this acute hospital setting, social costs and non-­sanitary costs study did not directly assess OD costs or deglutition alter- have been barely studied. This systematic review shows ations and it cannot be directly extrapolated that malnu- the need for future high-­quality studies to quantify the trition costs were a consequence of OD although we can acute and chronic cost of poststroke OD and its specific assume that malnutrition in OD patients can also lead to complications. higher costs31 It should be noted that the cost associated with complications related to OD accounted for a large part of the total costs of hospitalisation in the included Conclusions studies and that it is possible that hospitalisation costs This systematic review only partially fulfils the proposed do not include all the costs attributable to these compli- objectives. The studies found were conducted in cations. Health economic studies on the cost of other very different contexts and following very different complications of stroke are scarce. No article measuring approaches, limiting the analysis to a narrative explana- aspiration, dehydration or mortality costs was found. tion of what has been investigated to date. In addition, We believe that from our data we can estimate the for those studies related to complications associated with cost of OD in the acute phase might be up to €15 000 OD, the relationship between OD and the complication (approx. US$16 900) and the cost of an episode of aspi- was not clearly established. Despite this, this systematic ration pneumonia up to €24 000 (approx. US$27 600). review shows increased economic costs during hospitalisa- Our systematic review differs from a previously published tion and long-­term follow-­up in patients who developed systematic review because it focused on poststroke OD poststroke OD or its complications. Future studies on OD and explored the costs related to OD complications. This after stroke on patients screened and detected early for previous systematic review aimed to assess the influence OD will enable the long-­term costs of OD and the true of OD secondary to all aetiologies on length of stay and cost of its severe complications to be calculated. Taking costs showed an increase of 40.36% in costs of patients into account the chronic nature of this condition, it is with OD. A subgroup evaluation showed a higher and necessary to discover the real health and social costs asso- more variable length of stay of 4.73 days (95% CI 2.7 to ciated with this pathology. In addition, due to the severe 7.2) for patients with stroke.33 complications that patients with poststroke with OD Protected by copyright. Two important aspects in this field must be highlighted. present and their increased associated cost, it would be First, poststroke OD is a condition for which effective interesting to assess the cost-­effectiveness of the current interventions are available that may reduce long-­ term available treatments for these patients. cost and related complications. Costs related to caring for poststroke OD patients have been little reported. Author affiliations 1 Gastrointestinal Physiology Laboratory, Universitat Autònoma de Barcelona, Further research should be done to assess the poststroke Hospital de Mataró, Consorci Sanitari del Maresme, Mataro, Catalunya, Spain OD economic and social burden to better understand 2 Pharmacy Department, Hospital Universitari Germans Trias i Pujol, Badalona, and raise awareness about minimal care for this common Catalunya, Spain and severe complication in patients with poststroke. 3 Research Unit, Hospital de Mataró, Consorci Sanitari del Maresme, Mataro, It is becoming increasingly difficult to ignore the need Catalunya, Spain 4 Centro de Investigación Biomédica en Red de enfermedades hepáticas y digestivas for early screening and basic treatment in poststroke (CIBERehd), Instituto de Salud Carlos III, CIBEREHD, Barcelona, Spain OD patients to reduce their mortality rate and improve their outcomes. Second, in most of the included studies, Acknowledgements The authors thank Agustí Viladot, member of Mataró patients with poststroke were not screened for OD so Hospital Library Service, for his assistance with literature search development only the most severe patients may have been diagnosed and realization, Jane Lewis for reviewing the English and Maurice Driessen for reviewing the final version of this manuscript and advice on healthcare economics. with OD. This fact could affect the prevalence of OD This work has been conducted within the framework of a doctoral thesis in in these studies and the results of this systematic review medicine from the Medicine Department of the Autonomous University of Barcelona. and explain the underdiagnosis of OD in some of these Contributors SM is the guarantor. He drafted the first version of this manuscript. studies compared with the literature.2 Furthermore, the He provided expertise on health economics. He contributed to the realisation of high presence of false negatives could have led to a dilu- the introduction and the conclusions. He reviewed and extracted data of selected tion of the effect. A future prospective study on costs studies and contributed with Drummond’s and GRADE application. He contributed with data synthesis. MS-­P provided expertise on investigation methodology and related to poststroke OD in a sample of patients screened health economics. He collaborated in writing the manuscript. He provided important early for dysphagia could provide more accurate results. references for the development of the methodology of this work. He reviewed and We found only one study providing information on made contributions on the methodology of all the sections of this protocol. He OD cost beyond the first admission due to acute stroke. reviewed the correct use of all the economic terms included in this manuscript. He reviewed and extracted data of selected studies and contributed with Drummond’s However, we could not find any economic evaluation and GRADE application. He contributed with data synthesis. He read and approval regarding other relevant complications of poststroke the final revision of this systematic review. OO provided expertise on poststroke OD such as: (1) the need for institutionalisation after OD treatments and interventions. He collaborated in writing the manuscript. discharge, (2) loss of functional capacity, (3) costs related He contributed on the development of the data collection, quality assessment and data synthesis sections. He provided a critical revision of all the sections of to home care of these patients, (4) and the related short-­ this systematic review. He reviewed and extracted data of selected studies and term and long-­term mortality and impaired quality of contributed with Drummond’s and GRADE application. He contributed with data life.6 Furthermore, costs of patient care outside the synthesis. PC provided expertise on poststroke OD and the design of the study. 12 Marin S, et al. BMJ Open 2020;10:e031629. doi:10.1136/bmjopen-2019-031629 Open access BMJ Open: first published as 10.1136/bmjopen-2019-031629 on 11 August 2020. Downloaded from http://bmjopen.bmj.com/ on September 4, 2023 at Univesity Autonomous of Barcelona. He reviewed the correct use of all the medical terms included in this manuscript. 10 Cook IJ, Kahrilas PJ. AGA technical review on management of He contributed on the study design, and the development and writing of the oropharyngeal dysphagia. Gastroenterology 1999;116:455–78. introduction, the methodology and the conclusions of the manuscript. He provided 11 Altman KW, Yu G-­P, Schaefer SD. Consequence of dysphagia in the a critical revision of all the sections of this protocol. He contributed to the correct hospitalized patient: impact on prognosis and hospital resources. Arch Otolaryngol Head Neck Surg 2010;136:784–9. following of the recommendations proposed by PRISMA. He provided a critical 12 European Society for swallowing disorders (2012) ESSD position revision of all the sections of this systematic review. He reviewed and extracted statements: oropharyngeal dysphagia in adult patients. Available: data of selected studies and contributed with Drummond’s and GRADE application. www.​myessd.​org/​docs/​position_​statements/​ESSD_​Position_​ He contributed with data synthesis. All authors provided a critical revision and read Statements_​on_​OD_​in_​adult_​patients_​for_​web.​pdf [Accessed 10 Feb and approved the final revision of this systematic review. All authors contributed 2019]. with the realisation of the protocol for this systematic review. 13 Cabib C, Ortega O, Kumru H, et al. Neurorehabilitation strategies for poststroke oropharyngeal dysphagia: from compensation Funding This study is funded by an educational grant from Nutricia Advanced to the recovery of swallowing function. Ann N Y Acad Sci Medical Nutrition. This study is supported by Fundació Salut del Consorci Sanitari 2016;1380:121–38. del Maresme, Ciberehd (in turn supported by the Instituto de Salud Carlos III, 14 Ickenstein GW, Riecker A, Höhlig C, et al. Pneumonia and in-­hospital Barcelona, Spain) and Fundació de Recerca en Gastroenterologia (FUREGA). mortality in the context of neurogenic oropharyngeal dysphagia (NOD) in stroke and a new NOD step-­wise concept. J Neurol Competing interests None declared. 2010;257:1492–9. 15 Rofes L, Arreola V, Almirall J, et al. Diagnosis and management Patient consent for publication Not required. of oropharyngeal dysphagia and its nutritional and respiratory Ethics approval This systematic review is the first part of a research project. The complications in the elderly. Gastroenterol Res Pract full extent of this project includes (1) a systematic review on the cost of OD and 2011;2011:1–13. its complications after stroke; (2) a systematic review on economic evaluations 16 Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-­analyses of studies that of interventions related to screening, diagnosis, management and treatment of evaluate health care interventions: explanation and elaboration. BMJ OD after stroke; (3) a cost of illness study with one year follow up in patients with 2009;21:b2700. poststroke to assess the acute and chronic cost of OD and its complications; and 17 Marin S, Serra-­Prat M, Ortega O, et al. Cost of oropharyngeal (4) a cost-­effectiveness study of compensatory versus active interventions aimed at dysphagia after stroke: a systematic review. prospero: International recovering swallowing function in patients with poststroke. prospective register of systematic reviews. 2018. CRD42018099977. Available: https://www.​crd.​york.​ac.​uk/​prospero/​display_​record.​php?​ Provenance and peer review Not commissioned; externally peer reviewed. RecordID=​99977 Data availability statement No additional data is available. 18 Marin S, Serra-­Prat M, Ortega O, et al. Cost of oropharyngeal dysphagia after stroke: protocol for a systematic review. BMJ Open Open access This is an open access article distributed in accordance with the 2018;8:e022775. Creative Commons Attribution Non Commercial (CC BY-­NC 4.0) license, which 19 Centre for Reviews and Dissemination. Systematic Reviews: CRD’s permits others to distribute, remix, adapt, build upon this work non-­commercially, Guidance for Undertaking Reviews in Health Care. York: Centre for Protected by copyright. and license their derivative works on different terms, provided the original work is Reviews and Dissemination, University of York, 2009. properly cited, appropriate credit is given, any changes made indicated, and the use 20 Drummond MF, O'Brien B, Torrance GW, et al. Methods for the is non-­commercial. See: http://​creativecommons.​org/​licenses/​by-​nc/​4.​0/. economic evaluation of healthcare programmes. 2nd ed. Oxford: Oxford University Press, 1997. 21 Guyatt G, Oxman AD, Akl EA, et al. Grade guidelines: 1. Introduction-­ ORCID iDs GRADE evidence profiles and summary of findings tables. J Clin Sergio Marin http://​orcid.​org/​0000-​0001-7​ 709-​6504 Epidemiol 2011;64:383–94. Mateu Serra-P­ rat http://​orcid.​org/​0000-​0002-​6554-​9913 22 Wojner AW, Alexandrov AV. 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