Hospital transfer of people with dementia: results of the European RightTimePlaceCare project on their frequency, factors associated and costs

is a critical moment for people with and a major challenge for health care The of this study were 1) to describe the frequency of hospital transfer among people with from eight European countries, 2) to examine the factors associated with hospital and evaluate The present study is a secondary data analysis of the RightTimePlaceCare European project. A cross-sectional survey was carried out with data collected from people with dementia who lived either at home or had been admitted to a nursing home in the last three months, as well as from their caregivers. Data on hospital transfers at three months were gathered with the "The Resource Utilization in Dementia" instrument. Demographic data, functional, cognitive and neuropsychiatric symptoms, comorbidity, polypharmacy, caregiver burden, nutritional status and falls were evaluated with validated tools. Multivariate regression models were used to investigate the factors associated with hospital transfers. Costs were estimated by multiplying quantities of resources used with the unit cost of each resource and inflated to the year 2018. A recently published systematic review on hospitalization rates among PwD people with dementia in the community found hospitalisation rates between 0.37 and 1.26 per person per year in high quality studies (i.e. with low risk of bias), and percentages of hospitalisation between 26% and 65% as reported in four studies with low risk of bias where participants were followed for one year (16). The estimated hospital transfer rate per person with dementia and year observed in our study is therefore within the previously published ranges.

nosocomial infections, pressure ulcers, delirium, functional decline and an elevated risk of mortality (12)(13)(14). The identification of factors associated with hospitalisation may help preventing unnecessary adverse events (15,16). However, only few studies have investigated which factors may be associated with hospital admissions among people with dementia. Higher comorbidity, older age, male sex, previous acute hospitalisation and shorter duration of dementia symptoms have been identified as factors associated with hospitalisation among people with dementia living in the community (6,17).
These factors are less known among older people with dementia who live in nursing homes (16). In addition, there is a lack of studies comparing hospital or ED use of people with dementia living the community with those living in nursing homes (18).
Healthcare costs, including inpatient care, outpatient care and pharmaceutical costs represent a significant burden on the total costs of dementia care. Several reviews of cost-of-illness (COI) studies of dementia have been conducted in previous years (19)(20)(21)(22)(23) highlighting the heterogeneities and important limitations existing because of methodological differences (24). Although there is still no consensus on how to carry out these studies, different aspects such as disease severity, care setting and cost perspective, have been identified as main factors to be considered for future research (21,22,25).
Analysis of the costs associated with the hospital admission of people with dementia living in the community and in NH is a research area of interest, as the optimisation of resources or their refocusing towards targeted interventions in the area of home care or in nursing homes can lead to the prevention of unnecessary and costly events of hospital transfer (26).

Aim
The aims of the present study are: 1) to describe the frequency of hospital transfer (including emergency department and hospital admissions), among people with dementia from eight European countries living in the community or in nursing homes settings; 2) to examine the factors associated with hospital transfer; 3) to evaluate the costs associated with hospital transfer.

Methods Design
This study is a secondary analysis of a large European research project called 'RightTimePlaceCare' (RTPC). The RTPC survey was a longitudinal prospective study, conducted in eight European countries (Estonia, Finland, France, Germany, Netherlands, Spain, Sweden, and the United Kingdom). The project aimed to improve health and social care services for European citizens with dementia and focused on the transition from professional home care towards institutional nursing care. Further details are published elsewhere (27).

Participants
The RTPC survey comprised two groups of participants: 1) People with dementia newly admitted to NH (i.e. within one to three months after admission) and their informal caregivers; 2) People with dementia who received professional home care and were at risk of institutionalization (as judged by a professional responsible for their care) along with their informal caregivers.
Inclusion criteria for people with dementia were if they (1) had a primary diagnosis of dementia as diagnosed by an expert (e.g. physician, psychiatrist, neurologist, geriatrician, or general practitioner, depending on countries' diagnostic procedures); (2) scored 24 points or lower on the Standardized Mini Mental State Examination (S-MMSE) (28); and (3) had an informal caregiver who visited the people with dementia at least twice a month. People with dementia were excluded when they (1) were younger than 65 years; (2) had a primary psychiatric diagnosis or Korsakoff syndrome; and, for the group recently admitted to NH, (3) were only temporarily resident in the NH (e.g. rehabilitation, respite of the informal caregiver) with the intention of moving back home.

Procedures
Each country obtained ethical approval from a country specific legal authority for research on human beings (for example an ethical committee specialized in medical or nursing science) to conduct the study in accordance with their national standards and regulations. Country-specific consent procedures were followed. Data were collected by trained interviewers at baseline between November 2010 and April 2012 and follow-up interviews were conducted after 3 months (27). All interviewers were professionals in health or social care or medical/nursing/social care students with practical experience and at least a Bachelor's degree. The interviews were conducted with informal caregivers as informants (usually spouses/partners or children), formal caregivers and the people with dementia (to assess cognitive impairment).
Furthermore, several quality of care indicators based on recent literature (34) were assessed at baseline: nutritional status (one item question 'did the patient experience a weight loss of 4% or more of his/her weight in the past year?') (35), polypharmacy (≥ 5 drugs) (36) and the occurrence of falls during the preceding three months.

Information on hospital transfer
The Resource Utilization in Dementia (RUD) instrument was used to determine the health care resources used for people with dementia (39). The RUD instrument captures medical care resources use (e.g. medication, inpatient and outpatient care), community care services (e.g. home care, transportation, meals on wheels, day care), special accommodation (e.g. nursing home) and time spent with caring activities by informal caregivers. Information on hospital transfer since the baseline interview was gathered using an adapted version of the RUD instrument in the follow-up assessment that included the two concepts Hospital Admission (HA) and Emergency Department Admissions (EDA). With regard to HA, caregivers were asked: "since the last visit, was the person with dementia admitted to a hospital (for more than 24 hours)?"; "how many times was your relative/the resident hospitalised?"; "for each hospitalisation, please provide the diagnosis or reasons for hospitalisation"; "for each hospitalisation, please specify the total number of nights spent in each type of ward". The following types of ward were asked about: geriatric ward, surgery ward, internal medicine ward, psychiatry ward and other hospital stays. With regard to EDA, caregivers were asked: "Since the last visit, did the person with dementia receive care in an accident and emergency hospital department (for less than 24 hours)?"; and if yes, "how many times"? Participants with at least one episode of HA or EDA were considered to have experienced a hospital transfer.

Estimate of cost for hospital transfer
While the costs of dementia were previously measured from a societal perspective in the RTPC project (40)(41)(42), our study focused on the assessment of direct medical costs generated by EDA and HA and calculated as average costs per capita and year in Euros (€). In the absence of valid and comparable unit costs for all participating countries, a common price vector based mainly on Swedish sources was used for all countries (40,43). For HA, the length of stay in each medical department was taken into account in the measurement. In the case of fees not being available for daily stay in departments other than internal medicine, geriatrics or surgery it was decided to assume a cost per day similar to the daily expense in the department of geriatrics. In addition, we calculated the average costs per capita and year specifically among those people with dementia who had suffered ≥ 1 hospital transfer. All costs were inflated to the year 2018 and currency conversion adjustments based on 2018 exchange rates were made for the non-EURO countries. Cost components, unit costs, the international adjustment schemes and their sources are shown in Table 1 (43,44).

Sample characteristics
The total RTPC sample at baseline comprised 2,014 dyads of people with dementia and their informal caregivers. For the present study, only participants with data available on EDA and HA were included.
Thus, the study sample comprised 1,700 people with dementia and their informal caregivers (n = 1,054 (62%) from the HC setting and 646 (38%) from the NH setting).
The mean age of the study sample was 82.8 years (standard deviation (SD) 6.5), and 68.5% were women. The characteristics of the study participants are summarized in Table 2.  Hospital transfer Two-hundred and eighty-four of the people with dementia (16.7%) experienced at least one EDA (< 24 hours) or HA between the baseline and follow-up assessments. Out of the people with dementia experiencing at least one EDA and HA episode, the frequency of experiencing 2 or more episodes was 27.8% and 19.5%, respectively. We found an estimated HA rate per person with dementia/year of department to which people with dementia were most frequently admitted and for a longer time period. Table 3 describes the frequencies of hospital transfer (EDA and HA) as well as, for HA, the frequencies of admission and the average length of stay in days in the different medical departments evaluated. Factors associated with hospital transfer Table 4 (see Additional file 1: Table 4) contains the univariate analyses comparing the characteristics of people with dementia with and without at least one hospital transfer (HA or EDA). People with dementia with at least one hospital transfer compared to people who did not attend hospital were more frequently men, displayed more severe neuropsychiatric symptoms, presented more often polypharmacy, were more likely to suffer falls and weight loss, and had an informal caregiver who experienced a higher burden of care, especially in people living at home. By country, Germany and France recorded the highest percentage of referrals and Sweden the lowest.
The results of the multivariate logistic regression analysis are displayed in Table 5 Table 7 shows the estimated annual medical cost of each person with dementia referred to the emergency department or hospital, according to the department of admission and country.

Discussion
In this cross-sectional study, 1,700 people with dementia from eight European countries participating in the RTPC study were investigated. Within a time period of three months, 1 out of 6 people living with dementia were transferred to the hospital at least once, with an estimated rate of hospital admission per person with dementia/year of 0.45 and an estimated rate of emergency department admission per person with dementia/year of 0.55. Four factors were identified as being associated with a higher probability of suffering at least one hospital transfer: living at home and receiving HC (versus living in NH), suffering weight loss, accidental falls and presenting polypharmacy.
A recently published systematic review on hospitalization rates among PwD people with dementia in the community found hospitalisation rates between 0.37 and 1.26 per person per year in high quality studies (i.e. with low risk of bias), and percentages of hospitalisation between 26% and 65% as reported in four studies with low risk of bias where participants were followed for one year (16). The estimated hospital transfer rate per person with dementia and year observed in our study is therefore within the previously published ranges.
People with dementia living at their homes had a higher risk of hospital transfer than those in the NH setting in the present study. This result could be explained because the people with dementia included in the HC subsample of the present study had to be identified as being at risk for nursing home admission and, therefore were likely to be a selected sample of persons with complex needs, while the people with dementia included in the NH setting had to be recently admitted to the NH. The caregivers of people with dementia who live at home may have had less support in managing health needs or higher levels of care burden (46), leading to a greater need for emergency service utilization and hospital transfer. Other reasons for lower hospital transfer needs in the nursing home setting compared with home care suggested in the literature are that, even if EDA rates at nursing home are high (13), some of these institutions may be equipped with specific care units for people with advanced dementia (47), have a wider availability to perform post-acute attention (48), receive specialized health support from geriatric (49) or end-of-life care more frequently, and they may have policies to prevent transferring those persons to hospital.

Sleeman et al. also found in a retrospective cohort study of 4,867 people with dementia, in their last
year of life in England, that being in a nursing home was associated with a significantly lower number of ED visits (49). The authors argued that increasing bed capacity in NHs may have explained their results, as it may have played an important role in reducing pressure on emergency hospital care.
Conversely, other studies analyzing the impact of dementia on hospital and ED use among fee-forservice Medicare beneficiaries reported that people with dementia who lived in nursing homes were significantly more likely to visit the emergency department and be hospitalised than those who resided in their own homes (18). However, these studies included the general population of people with dementia living at home and thus their population was not comparable with the participants of the present study.
Our study evaluated geriatric syndromes as markers of vulnerability and complexity in people with dementia. Geriatric syndromes are known to predict an increased likelihood of hospitalization, affect quality of life (50), increase the use and cost of health care, and raise overall mortality among the general elderly population (51). In the present study, the presence of three geriatric syndromes (malnutrition, history of falls or polypharmacy) was associated with a higher risk of hospital transfer.
Unintentional weight loss has been found associated with increased morbidity and mortality among older adults (52), but the relationship between unintentional weight loss in people with dementia and the risk of hospitalization has been underreported. Conversely, falls are of great concern for people with dementia given their potentially higher number of visits to emergency departments and severe consequences, mainly hip fracture (53). Similarly, the concurrent use of multiple medications by an individual, has been found to be associated with several negative health outcomes including hospital admission (54,55).
Currently, evidence for effective interventions to reduce the risk of falls, to reduce polypharmacy and to improve nutrition is limited and requires further development (56)(57)(58)(59)(60). Nevertheless, the results of the present study suggest that the identification and management of these three geriatric syndromes might help preventing hospitalisation events among people with dementia. Furthermore, the promotion of an advanced and individualised care plan among people with dementia showing these geriatric syndromes may be particularly advisable.
In our study, a worse functional status according to the Katz Index was not found to be associated with a higher frequency of hospital transfer. In contrast, previous studies have documented a statistically significant association between an increased dependency on activities of daily living (ADL) and the risk of hospital admission (15,61,62). Furthermore, a lower MMSE and higher NPI scores were not associated with hospital transfer. Conversely, Albert et al. previously reported that advanced dementia was a significant risk factor for hospitalisation in contrast to people with mild or moderate dementia (7). Finally, higher comorbidity was not associated with a higher frequency of hospital transfer, consistent with previous reports (63), but with a different pattern than shown by Sheperd et al. in a recent meta-analysis, where multimorbidities were associated with hospitalisation with moderate confidence (16).
Although the comparison of hospital transfer between countries was not the aim of this study, the results showed some differences, with higher risk of hospital transfer among people with dementia living in United Kingdom, France and Germany. These differences may be explained by the different patterns of organization of health and social care or family support.
In the present study, we found an estimated expenditure per person/year attributable to hospital transfers of 1,944.55 €, with a higher estimated cost for people with dementia included in the HC group (2,535.39 €) compared to the NH group (980.56 €). Other costs related to health and social care (medications, informal and community care) have been evaluated in previous RTPC studies (40)(41)(42), highlighting that in most countries the main cost driver in the HC setting were the costs of informal care, followed by the community and medical care costs. In addition, it was noted that NH expenditure in each country was dominated by indirect (non-medical) costs generated by living in nursing homes (institutional care). Contrary to our expectations and similar to other previous studies (21,64), the argument of rising medical costs resulting from living in NH was not confirmed in the RTPC sample. It was observed that medical costs associated with hospital admission (including EDA) were lower in the NH setting.
Possible reasons for this have been argued before: this could be explained by the special characteristics of the participants in the HC setting of the RTPC study, on one side, but on the other side this could also indicate different diagnostic or therapeutic approaches in the NH group of people.
These results may suggest that living in a nursing home may be more cost effective in terms of hospital transfer for those people with dementia with similar characteristics to the participants of the RTPC study, especially if we consider that the nursing home admission is generally not associated with a deleterious impact on their quality of life (65), health or emotional status (66).
Added to the cost calculation, we calculated the average estimated annual expenditures specifically for the group of people with dementia who suffered EDA and/or HA, which were 270.62 € and 4,103 € per person with dementia/year, respectively. It is important to emphasize that no broader direct costs related to medical care are shown since costs generated by the use of outpatient clinics, medication or rehabilitation were not included in our study. Even so, the medical costs of our study are in accordance with previously published European data (40,67,68). In this way, the estimated cost of hospitalisation of 2,368 € per person with dementia/year identified in our study is close to previous findings.
Our results suggest that the identification of people with dementia who are at particular risk of suffering a hospital transfer may be of special interest, as they are those with higher estimated average annual expenditures related with hospital transfer. The provision of interventions aimed at preventing these events and an adequate care planning may be particularly cost-effective for this group of people with dementia.
The findings of our study should be interpreted considering its limitations. First, the time period investigated for each participant was limited to three months, which may not represent the entire population of people with dementia requiring hospital admission over the one-year period, taking into account seasonal fluctuations; however, the prospective character of the study may have facilitated the acquisition of reliable data. Furthermore, the RTPC country samples may not be representative of the general national population of people with dementia. Next, although we accounted for multiple variables that may affect the need for hospital admission, there may also be additional unmeasured confounding factors that influence the use of hospital care, for example, specific health support at the community or nursing home setting in each country or even at the local level. Finally, several years have passed between data compilation and secondary analysis. However, the amount of published data on this topic is still scarce, and we do not expect that important structural and process changes in the health and social care systems have occurred within this time period.

Conclusions
To the best of our knowledge, this is the first study that evaluates internationally (across Europe) the frequency of hospital transfers among people with dementia living in nursing homes and home care settings, and analyses the associated factors and costs. Within three months, 17% of the people with dementia suffered at least one episode of hospital or emergency department admission. People with dementia living in the community were more often transferred to hospital and health care costs due to hospitalisation were higher, compared with those living in a nursing home. Also, people with dementia with unintentional weight loss, falls and polypharmacy were more frequently transferred to hospital, suggesting a need for supportive interventions that focus on the assessment and management of these geriatric syndromes and that promote individualised care planning for them.
The analysis of the health costs associated with hospitalisation show a remarkable economic burden and supports the need to identify those people with dementia at special risk of hospital transfers. Committee, the United Kingdom (11/NW/0003) (Verbeek et al., 2012). Participants were informed of the study purpose, and they were free to participate or withdraw from the study at any time. They were asked to sign the informed consent form.

Consent for publication
No identifying information on any individual's data is presented in this paper. All participants gave written informed consent.

Availability of data and materials
The datasets analysed during the current study are available from the RightTimePlaceCare (RTPC) consortium on reasonable request.