Reducing ageism combining ageing education with clinical practice: A prospective cohort study in health sciences students

Abstract Aim To analyse the impact of an intervention combining ageing education with clinical practice in nursing homes on a nursing cohort's negative stereotypes and prejudices towards ageing. Design A prospective cohort study was conducted in September 2019–October 2020 in a population of health sciences students (n = 222). Methods Questionnaire of Negative Stereotypes towards Aging (CENVE) and Aging Semantic Differential (DSE) were used to examine negative stereotypes and prejudices towards ageing in the nursing cohort exposed to the ageing education and practice intervention compared to a medical cohort that received no intervention. Group‐by‐time interaction, controlled by sex and age, for the effect of the intervention on CENVE and DSE scores was determined by mixed‐design ANOVA. Results The nursing cohort significantly reduced negative stereotypes and prejudices towards ageing when compared to the medical cohort in total (F = 26.926; p < 0.001), health factor (F = 16.812; p < 0.001), motivational and social factor (F = 11.266; p = 0.001), and character and personality factor (F = 19.202; p < 0.001) scores of CENVE scale and in DSE (F = 7.826; p = 0.006).

as contempt, dislike and indifference and can place ageing adults in vulnerable situations (Butler, 1969).
The coronavirus disease 2019  pandemic has highlighted ageism in society (Bravo-Segal & Villar, 2020). Although COVID-19 affects all age groups, most deaths occur in older populations and in those with previous health conditions or frailty (Grasselli et al., 2020;Hewitt et al., 2020;Richardson et al., 2020).
Thus, older people are at the forefront as a risk group and a vulnerable population, influencing how they are viewed. In this context, many studies have warned of the potential for increased ageism and discrimination against older people during the COVID-19 pandemic (Ehni & Wahl, 2020;Fraser et al., 2020;García-Soler et al., 2020).
The World Health Organization's recent Global Report on Ageism (World Health Organization, 2021) states that combating ageism is one of the four action areas of the Decade of Healthy Ageing (2021-2030) (Dixon, 2021).
Of note, studies examining these stereotypes were cross-sectional and only revealed the relationship between different variables at a particular time, making it difficult to perform more in-depth analyses. Further, validated questionnaires were not always used, and different components of ageism were not consistently explored.
When ageist attitudes appear in health professionals, they negatively affect the health of older people because such attitudes lead to discriminatory behaviours, including inadequate health communication with the patient and family, underdiagnosis, lack of treatment, exclusion from research and denial of access to health services and treatment (Chang et al., 2020;Franco et al., 2010;Kagan & Melendez-Torres, 2015;Makris et al., 2015). It is therefore important to implement actions to reduce these negative stereotypes and prejudices in health science trainees.
Several studies have observed that education about ageing may be effective in changing attitudes towards ageing in health sciences students (Basran et al., 2012;Rodgers & Gilmour, 2011;Sarabia-Cobo & Castanedo-Pfeiffer, 2015;Wurtele & Maruyama, 2013), yet few studies have used control groups to assess the effects of such educational interventions (Leung et al., 2012;Lucchetti et al., 2017).
Contact with older people is recommended to decrease negative attitudes towards ageing (Burnes et al., 2019;Sum et al., 2016).
However, for health science students, contact with older people often occurs during clinical practice, and exposure is usually with frail older adults, which may increase the risk of developing ageist attitudes (Giles et al., 2002). Therefore, our goal was to analyse the impact of combining ageing education with clinical practice in nursing homes on a nursing cohort's negative stereotypes and prejudices towards ageing and compare outcomes with a medical cohort that did not receive the educational intervention. We hypothesized that this strategy would reduce negative stereotypes and prejudices towards ageing.

| Research question
Could an educational intervention involving ageing education and clinical practice in nursing homes influence on a nursing cohort's negative stereotypes and prejudices towards ageing?

| Design
A prospective cohort study was used for this study.

| Participants
The study was conducted in September 2019-October 2020 at

| Procedure
The nursing cohort was exposed to an educational intervention Nursing and medical students were invited to several information sessions, which introduced the objective of the project, resolved doubts and requested their collaboration. All students interested in participating voluntarily signed informed consent forms and completed the questionnaires.

| Materials
We used an ad hoc self-administered questionnaire and collected sociodemographic information, including age, sex, marital status, number of family members and parents' education level. The Questionnaire of Negative Stereotypes towards Aging (CENVE) was used to examine the cognitive dimension of ageism (how we think) (Blanca et al., 2005). This questionnaire consists of 15 statements regarding the characteristics of older persons, with responses ranging from 1 (strongly disagree) to 4 (strongly agree); therefore, possible scores range 15-60, with higher scores indicating higher negative stereotypes. This questionnaire explores three factors: health factor, motivational and social factor, and character and personality factor. CENVE shows good psychometric properties with a Cronbach's alpha of 0.89 and is the most widely used instrument in The Aging Semantic Differential (DSE) was used to examine prejudices towards ageing [i.e., affective dimension of ageism (how we feel)] and has an optimal level of reliability and high item correlation with a Cronbach's alpha of 0.91 (Villar Posada, 1997). This questionnaire includes 18 pairs of opposing adjectives that can be used to describe the ageing process. Each word pair is rated on a 7-point scale, possible scores range 18-126 and lower scores reflect more negative prejudices.

| Analysis
Statistical analysis was performed using the IBM SPSS Statistics v.26 statistical software package (SPSS Inc., Chicago, IL). Quantitative data were expressed as means (M) with standard deviations (SD) and categorical data as frequency counts (n) and percentages (%).
Quantitative variables were checked for normality of distribution using the Kormogorov-Smirnov test. Differences of baseline characteristics between nursing and medical cohorts were compared by the independent student t-test for quantitative variables and with the chi-squared test for categorical variables. Effect sizes for those tests were calculated by Cohen's d and Cramer's V respectively.
Differences in the evolution of CENVE and DSE scores between both groups were determined by mixed-design ANOVA. Group-bytime effect controlled by sex and age was calculated. Effect size was determined by partial eta-squared. p-value <0.05 was considered statistically significant.
When analysing the effect of the intervention on negative stereotypes and prejudices towards ageing (Table 2) Regarding covariates, there was no significant age-by-time interaction. However, sex-by-time interaction was significant for CENVE health factor (F = 4.901, p = 0.028), motivational and social factor (F = 4.344, p = 0.038) and total score (F = 7.035, p = 0.009) as women showed a greater improvement than men did.

| DISCUSS ION
We aimed to determine the impact of combining ageing education with clinical practice in nursing homes on a nursing cohort's negative stereotypes and prejudices towards ageing and compared outcomes with a medical cohort. Our results support the hypothesis that com- have the potential to improve student skills, knowledge and attitudes in geriatric medicine (Tullo et al., 2010). Further, pedagogical interventions designed to increase knowledge of ageing also can improve attitudes towards older adults (Chonody, 2015). However, previous studies examining how such interventions impact negative stereotypes towards older individuals vary considerably in both the methodology and the questionnaires used. In addition, these studies had limitations, validated questionnaires were not always used, the obtained results were not always significant, and many studies lacked a control group.
Control groups have been used in few studies assessing the effects of educational interventions on changing attitudes towards ageing in health sciences students. In medical trainees, in comparison to a control group receiving no intervention, implementation of two educational strategies has shown different outcomes in terms of attitudes, empathy and knowledge that depend on the strategy used (Lucchetti et al., 2017). However, that study did not focus on negative stereotypes and prejudices towards ageing and only conducted an educational intervention.
In addition, exploration of the long-term effect of a 10-week service-learning project, where one older adult and one student met for 1-2 h per week, on medical and nursing students' knowledge of ageing and attitudes towards older adults demonstrated increased knowledge and reduced negative attitudes immediately after intervention (Leung et al., 2012). However, 1 month after the TA B L E 1 Baseline characteristics of the study population by group. intervention, all groups showed a decrease in positive attitudes towards older adults. Curiously, the nursing student intervention group showed a greater decrease than the nursing student control group with no intervention, suggesting that the knowledge and attitude gains are limited (Leung et al., 2012). In the current study, the intervention was conducted during September 2019-May 2020, and the second data collection took place 4-5 months after intervention, in September-October 2020. Therefore, combining ageing education with clinical practice in nursing homes may be a viable strategy to maintain improvements in attitudes over time.
Recent studies built on the Positive Education about Aging and Contact Experiences (PEACE) model (Levy, 2016) have found improvements in attitudes towards ageing in undergraduates through positive intergenerational contact (Lytle et al., 2021;Lytle & Levy, 2019), an approach that has been supported by other studies (Burnes et al., 2019;Sum et al., 2016), but these studies were not carried out in nursing students. Positive intergenerational contact may be an effective strategy because exposure to only sick and frail older adults may place health professionals at greater risk of developing age-discriminatory attitudes (Giles et al., 2002). In addition, conducting clinical practices in different facilities has various effects on students' attitudes and behaviours towards older people (Hwang et al., 2013). In the current study, there was contact between students and older people through a four-week clinical practice in nursing homes, but the clinical practice was complemented with a course on gerontology and educational content pertinent to the care of older people. Previous studies have concluded that ageing education is important (Willetts et al., 2017) and highlighted that curricula need to be carefully planned to break down negative perceptions (Dahlke et al., 2020;Leung et al., 2012), and perhaps "be delivered by expert gerontological nurses to inspire undergraduate nursing students to care for older adults" (Neville et al., 2013). A literature review concluded that "relevant preparation and support allows students to engage in enriched learning experiences, deliver quality care, and develop positive attitudes in caring for older people in their professional practice" (Koh, 2012). Education on ageing is important, but curricula must ensure that such education is effective in reducing ageism. Considering the lack of interventions that apply the methodology proposed in the current study, linking clinical practice with education about ageing may be key to decreasing both negative stereotypes and prejudices in health sciences students.

| Limitations
One of the limitations of this study is that the COVID-19 pandemic occurred during our study, in the 2019-2020 academic year. It is possible that the pandemic influenced negative stereotypes and prejudices of health sciences students at the University of the Basque Country. Several studies indicate that ageism has increased (Ehni & Wahl, 2020;Fraser et al., 2020), but others show that the pandemic has promoted intergenerational solidarity (Previtali et al., 2020;Vervaecke & Meisner, 2020). Thus, the improvement in our nursing cohort could be due to the pandemic; however, the medical cohort did not show any changes in attitudes towards ageing, indicating that the observed positive changes were associated with the intervention and not the pandemic. Another limitation was that the two groups had different sociodemographic characteristics. Therefore, the results were not entirely free of bias. However, the baseline levels of stereotypes and prejudices about ageing were similar in both groups.
This study has important strengths. To the best of our knowledge, this study is the first to analyse both negative stereotypes and prejudice towards ageing in health sciences students; that is, our study explores ageism from its cognitive and affective components using validated questionnaires. Our study has an innovative, longitu-

| Implications for nursing education
Considering that combating ageism is one of the four action areas of the Decade of Healthy Ageing (2021-2030), educators have the responsibility to implement and analyse specific actions to reduce ageism among nursing students to ensure high quality of care provided to the ageing. These students will be dedicated to care in their future professional lives, and to a great extent, this care will be directed towards older people. It is essential to implement actions to reduce ageism among nursing and health science students, because without intervention there is no improvement, and discriminatory behaviours towards older people may be maintained.

| CON CLUS ION
Analysing possible discrimination against older people and identifying effective interventions are of vital importance, especially in professions that work directly with ageing populations, such as health professionals. Our results suggest that an intervention combining ageing education with clinical practice in nursing homes can significantly reduce negative stereotypes and prejudices about ageing in nursing students. These observed cognitive and affective changes could lead to behavioural changes, which could improve the quality of care provided to older people. These results will benefit nursing students, future health professionals, older people and society and serve as a foundation for further research aimed at developing more inclusive interventions and education for both nursing and health sciences studies.

AUTH O R CO NTR I B UTI O N S
Batirtze San-Martín-Gamboa: Conceptualization, Investigation,

ACK N O WLE D G E M ENTS
Open Access funding provided by University of the Basque Country.
The authors sincerely thank the volunteers for participating in this study.

FU N D I N G I N FO R M ATI O N
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

CO N FLI C T O F I NTE R E S T S TATE M E NT
The authors report no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data available on request due to privacy/ethical restrictions

R E S E A RCH E TH I C S CO M M IT TE E A PPROVA L
The study was conducted in accordance with the Declaration of