Ageism against older adults in the context of the COVID-19 pandemic: an integrative review

ABSTRACT OBJECTIVE To report the main results of studies on prejudice, stereotyping, and age-based discrimination (ageism) in the context of the COVID-19 pandemic. METHODS This is an integrative review of the literature on ageism in the context of the COVID-19 pandemic, conducted between May and June 2020, with data collected from the following databases: Medical Literature Analysis and Retrieval System Online (MEDLINE/PubMed), Web of Science (Thompson Reuters), Scopus (Elsevier Science), Literatura Latino-Americana e do Caribe em Ciências da Saúde (Lilacs) and Scientific Eletronic Library Online (SciELO). RESULTS Twenty-one publications addressing ageism during the pandemics, its origins, consequences, and ethical and political implications were analyzed. All publications were theoretical with a critical/reflexive approach, being 90,5% opinion articles (n = 19) and 9,5% research (n = 2). The main findings indicate criticisms regarding resources allocation and intensive care based exclusively on age. The results also highlight the impacts of social isolation, the use of technologies and social media, and intergenerational relationships within the COVID-19 scenario. CONCLUSION According to most publications, although ageism has always been present, it became more evident during the COVID-19 pandemic as a form of discrimination against older adults. “Ageist” discourses may exert a negative influence in older adults’ lives, causing severe social and psychological impacts.


INTRODUCTION
In December 2019, a severe respiratory disease of unknown etiology was detected in the city of Wuhan, China. Later on, it was identified as an infectious disease caused by the novel coronavirus (Severe Acute Respiratory Syndrome Coronavirus-2 or Sars-Cov-2) and named coronavirus disease 2019 (COVID-19) 1 . Due to the rapid spread of the virus and the growing number of cases worldwide, the World Health Organization (WHO) declared COVID-19 a global pandemic on March 11, 2020 2 .
The novel coronavirus pandemic is one of the biggest public health issues over the last century, posing challenges such as the implementation of measures that ensure social health protection and minimize economic and social damage while respecting human rights 3 . Although everyone is susceptible to the disease, countries with older populations have felt the impacts of the pandemic in a larger scale, especially regarding morbidity and mortality. Studies show that older adults are at higher risk of developing severe forms of COVID-19, possibly leading to death [4][5][6] . Among other factors, this may be explained by immunosenescence -a process characterized by the gradual deterioration of the immune system and the consequent increased susceptibility to infections 6 . Besides age, the high prevalence of multimorbidity, frailty, and inflammatory changes make this age group more vulnerable and may complicate the disease course 7 .
As a measure to contain the pandemic expansion, the WHO suggested all countries to adopt social distancing measures to contain virus spread, prevent health systems collapse, and reduce the number of victims of COVID-19 8 . However, this strategy may generate negative impacts in various segments of society. Bezerra et al. 9 conducted an opinion survey on perceived social isolation during the COVID-19 pandemic in Brazil (n = 16,440) and found social interaction to be the most affected aspect, followed by financial condition.
Global health authorities then began to recommend other strategies to reduce virus transmission, such as prohibiting agglomerations, restricting movement, and limiting contact with special populations (as in long-term institutions, such as prisons). Such measures incur social, economic, and health-related consequences 10 .
Various age groups may be vulnerable to the effects of COVID-19 control and preventive measures, including the social distancing and isolation stemming from them. Nowadays, older adults are increasingly likely to live alone and have fewer opportunities for social interaction 11 , besides going out less often for social, recreational, religious, and utilitarian activities due to mobility difficulties and inadequate environmental conditions. This population also uses less online communication systems to inform themselves, shop, contact other people, and have fun when compared to younger individuals. With that, older adults are particularly exposed to the risks arising from social isolation and loneliness enforced by social distancing measures 12,13 .
Social isolation is the absence of social contact or communication, participation in social activities, or confidants contact, increasing the risk of death by almost one third (OR = 1.29) 14 . Often associated with social isolation 13,15 , emotional loneliness is a personal experience of lack of significant social connections that evokes negative emotions such as disinterest, boredom, fatigue, and apathy, besides potentiating pain, sleep disorders, decreased appetite, and physical inactivity. Together, the consequences of social isolation and emotional loneliness in older adults increase their vulnerability to depression and risk of death 15,16 .
The COVID-19 pandemic and the consequent risk of overloading health systems in some countries and regions sparked discussions on health resources allocation primarily to young and adult patients. This possibility provoked and fueled the controversy surrounding fundamental ethical issues, including the right to life and professional's decision on who lives and who dies 17 . Concurrently, derogatory memes, negative stereotypes, and biased discourses against older adults featured on the Internet, media, and social networks, evincing age-based discrimination in society 18 .
That is, the pandemic brought to light the issue of prejudice toward older populations, which is not recent in history. The term "ageism" was first used in 1969 by the American psychiatrist and gerontologist Robert Butler to designate the prejudice by one age group toward other age groups, or as any form of stereotyping and discriminating people based on their chronological age 19 . Robert Butler also emphasizes ageism essential vocationsbeing oriented toward older adults and including systematic processes of stereotyping and discriminating people due to their age. The author classified ageism as a form of intolerance comparable to sexism and racism. Six years later, he refined the concept by stating that ageism includes biased attitudes toward older people, old age, and the aging process; discriminative social practices against older adults; and institutional practices and policies that perpetuate stereotypes against these age groups 20 .
Ageism may be perpetuated against young people and adults 21,22 , but most theoretical studies and research on the theme focus on older adults. This is particularly true regarding the treatment provided to older populations during the COVID-19 pandemic, considering this group greater biological vulnerability and lower political power when compared to younger groups. The term ageism was translated to Brazilian Portuguese as discriminação por idade, etarismo, or ageismo, and recorded in the list of Descriptors of Health Sciences (DeCS) of the Latin American & Caribbean Health Sciences Literature (Lilacs) and the Virtual Health Library (VHL).
Considering aging as a complex, dynamic, and heterogeneous process, discrimination against older adults and age-based stigmatization have been more evident in view of the COVID-19 pandemic, requiring major ethical and political discussions. This review sought to describe the main results of studies on prejudice, stereotyping, and age-based discrimination (ageism) in the context of the COVID-19 pandemic.

METHODS
The integrative literature review is a methodological approach used to provide knowledge on a given theme in a systematic, orderly, and comprehensive manner. It is organized into six phases: identifying the theme, hypothesis, or research question; identifying in the literature pre-established search criteria; defining information to be extracted from selected studies/categorizing studies; evaluating studies critically; interpreting results; and presenting the review/synthesis of knowledge 23 .
This study conducted a literature search on national and international journals addressing age discrimination (ageism) against older adults in the context of the COVID-19 pandemic. Between May 1 and June 15, 2020, two independent researchers conducted the electronic search in to the following databases: Medical Literature Analysis and Retrieval System Online (MEDLINE/PubMed), Web of Science (Thompson Reuters), Scopus (Elsevier Science), Lilacs, and the Scientific Eletronic Library Online (SciELO). To solve divergences, a third researcher was consulted for an opinion on whether to include or not the selected publications.
Descriptors were used according to the Medical Subject Heading (MeSH) and its Portuguese equivalents, provided by the Descriptors in Health Sciences (DeCS). The search strategy, elaborated for each database, comprised terms combined using the Boolean operators "AND" and "OR." The following terms were used as descriptors for database search: covid- 19  All publications approaching ageism in older adults (people aged ≥ 60 years) and its impacts on the COVID-19 pandemic were eligible for inclusion. We applied no restrictions regarding year, methodological design, or language. Articles discussing ageism in age groups below 60 years or unrelated to the COVID-19 pandemic were excluded. Publications duplicated in different databases were considered only once.

RESULTS
The initial search identified 43 publications based on the title. After title and abstract screening, 21 were excluded for being duplicate or unrelated to the theme of interest. Twenty-two studies were selected for full-text reading, from which one was excluded after consultation by the third researcher for not addressing ageism in the pandemic as main theme. Thus, this integrative review comprised 21 articles. Of these, 18 were identified in the MEDLINE/Pubmed, seven in the Web of Science, four in the VHL/Lilacs, and three in Scopus. Some articles were published in two or more databases. Figure 1 shows the flowchart outlining the process for selecting the publications.
Chart 1 synthesizes the publications contemplated in this review according to database, journal, author(s), publication year, title, type of study, considerations/objectives, and the results of interest. Nineteen articles (90,5%) were published in English, one in Spanish and one Portuguese. All publications were theoretical with a critical/reflexive approach, being 90% opinion articles (n = 19) and 9,5% research (n = 2).
Opinion pieces outlined the importance of researchers to position themselves regarding a global bioethical, cultural, social, and ethical issue. By doing that, the authors take a stand not only as health professionals, but also as human beings before their equals, experiencing an issue that will scar many people's fate. The novel coronavirus bursts a new paradigm for searching for knowledge, common good, and solidarity.  Decisions regarding mechanical ventilation should be made by the health team together with the patient and grounded on aspects other than simply age or disability -as this could be jaundiced.
Recognizing that people should not be arbitrarily discriminated, the authors suggest using "preventive utilitarianism" to ensure equality, so that the largest number of people would benefit from the greatest good in an equal manner. Older adults should be prioritized in preventive measures against coronavirus given they are at higher risk of contamination. Yet, decisions should not be grounded solely on age, but rather consider those more likely to survive. Social isolation incur physical and psychological risks to older adults, not only within their household, but also in hospitals, institutions, and even at wakes.

Journal of Aging & Social Policy
Reynolds, 2020 39 The COVID-19 pandemic exposes limited understanding of ageism b Article It addresses the lack of knowledge on ageism and its impacts on the ageing process.
With the COVID-19, the lack of knowledge regarding ageism was very evident. An important example of ageism dimensions and constructions in the context of COVID-19 was the case of the Lieutenant Governor of Texas, who said he would give up his own life to save his grandchildren's generation. Health professionals and caregivers also state unintentional ageist comments. We must implement this biopsychosocial concept within different spheres.

Continue
Most studies 18,24,[27][28][29]31,33,35,36,38,40 indicate that ageism was more evident during the COVID-19 pandemic, causing several negative impacts for older adults. Brooke e Jackson 18 stress that prolonged isolation may lead to loneliness, decreased mobility, increased frailty, and depression among older persons. Besides that, "ageist" discourses may increase elder abandonment 18 . According to Banerjee 29 , elder neglect, loneliness, depression, anxiety, isolation, and abuse are evils associated with social distancing during the pandemic. Such scenario may be even more problematic among institutionalized adults, when distancing and hygiene measures may be inadequate. Morrow-Howell et al. 27 stress that older persons may have long-term emotional effects due to increased isolation and anxiety.
By analyzing a series of tweets, Jimenez-Sotomayor et al. 25 found 21.1% to contain age-biased comments or underestimate COVID-19 severity for believing it would only affect older groups. Other studies 17,18,28 also verified ageism in social networks by the hashtag #boomerremover, often followed by derogatory images and jokes related to older persons. Some publications 24,33,36,40 . critically addressed resources allocation, intensive care, mechanical ventilation, and/or decision-making based exclusively on the age criterion.
The studies also addressed the issue of ageism and intergenerational relationships 17,32 . "Ageist" discourses were increasingly present in the media during the pandemics, provoking conflicts between people of different generations. Social stratification by age makes it even more difficult for older adults to cope with a devastating natural disaster such as the pandemic 17 . Health professionals likewise reinforced the emphasis on age as a determining factor of COVID-19 severity, highlighting the knowledge gap on ageism by them and the general population. Although rarely intentional, ageism may ensue negative consequences for older persons' lives. Considering that, understanding ageism as a biopsychosocial concept and disseminating its definition through different spaces is crucial 41 . Article It deals with the COVID-19 cumulative incidence, addressing the classification of the group at greater risk, which is not only questionable, but also problematic.
Labeling older adults as a risk group relying entirely on age is a form of ageism that may accelerate social isolation and increase levels of psychosocial pain.
Besides age, social, cultural, and contextual factors must be taken into account for formulating these groups. Social media platforms should be used positively to spread facts and avoid panic. The heterogeneity inherent to the aging process must be recognized, and positive attitudes toward older adults must start within our homes and enter digital media.

Review and comment
It assesses the protective role of feelings considered important for older people in typical and atypical times, such as the COVID-19 pandemic.
The authors present the concept of "mattering" and its particularities in the older population. All people want to feel important and valued, and this fact is even more pronounced among older adults during the pandemic. Many older adults may feel more vulnerable and helpless as a result of government recommendations and the comments made. Social isolation likewise causes further hazards to the health of this population. Considering that, biased comments on aging should be avoided and measures should be developed to preserve the physical and mental health of older people.

DISCUSSION
Our main findings show that ageism has become present in different aspects of the lives of older adults during the COVID-19 pandemic. Although everyone is vulnerable to the novel coronavirus, older adults are at the core of the media and in most discussions about the theme.
A study 42 found that ageism experiences were more common among older and young adults than in middle-aged people. While young adults reported experiencing ageism more often within their workplace, older and middle-aged individuals suffered it when looking for goods and services. For older persons, family members were not the main practitioners of ageism -although comments of this type made by a family member are interpreted as less aggressive. Regarding experiences, young people witnessed lack of respect whereas middle-aged and older adults were victims of assumptions regarding their social and physical capacity 42 .
Ageism may occur at the structural level, whereby social institutions reinforce systemic discrimination against older persons, or at the individual level, whereby individuals have negative opinions regarding ageing. A systematic review with 422 studies (including over 7 million participants) found ageism to lead to poorer health outcomes in older adults in 95.5% of the studies. Moreover, less developed countries presented a higher prevalence of the negative effects of ageism than more developed countries (p = < 0.001), so that it was associated with decreased health in all domains analyzed 43 .
Given that many older adults have to remain within their households, depending on other people's help and service provision to obtain, for example, basic items, ageism may occur more frequently during the pandemic. In that way, studies may misfocus older adults' physical characteristics, categorizing them as a heterogeneous group of frail and dependent people 36 .
A study conducted with older adults from Australia 44 found those presenting with some type of disability to be more likely to report discrimination than those without disability or with chronic diseases. Victims of prejudice reached lower scores of self-efficacy and life satisfaction, evincing the negative effects of discrimination on older adults' lives 44 .
Previtali et al. 37 emphasize that, despite the association between chronic diseases and age, being chronologically older does not presuppose being vulnerable or less valuable or having a precarious health. The notion that chronological age objectively defines groups, neglecting their internal differences, is an ageist assumption that supports age-based prejudices, stereotypes, and discrimination 37 .
Some studies report the presence of ageism in health services during the COVID-19 pandemic based mainly on resources allocation, such as prioritizing the allocation of mechanical ventilators for young people in detriment to older people. Due to the large and growing number of COVID-19 patients in Italy, the country began to implicitly adopt the age criterion for deciding the allocation of scarce resources 24 . According to Ouchida 45 , how health professionals cope with the aging process and the older adult may determine their medical assistance and treatment. Resources allocation based solely on age characterizes ageism, given that other parameters should be considered in critical situations, such as clinical conditions, frailty, functional status, and comorbidities 24 . Everyone has the right to life, and quick decisions should be made by the health team together with the patient and family 33,36 .
Ageism may be either implicit or explicit and might not be recognized as such. As a result of the growth in the world's older population, an adequate communication between health professionals and individuals, a better understanding of aging heterogeneity, and the resignation of age-related stereotypes are increasingly important 46 . For Cesari et al. 24 , physicians familiarized with geriatrics and gerontology principles must help formulating more contemporary recommendations, identifying valid and efficient ways to assess morbidities and functional status in different contexts and specialties.
The publications analyzed indicate that social isolation has a negative impact on older adults' lives. Plagg 47 evaluated the benefits and harms caused by long-term social isolation and found that, despite primarily aiming to avoid or reduce virus spread, this situation increased the risk of neurological and cardiovascular diseases, depression, cognitive decline, and mortality among older adults 45 . Thus, authorities must implement measures to reduce possible harms in the case of long-term social isolation. Distancing does not implicate the termination of social relationships and support networks, and health professionals, family, and society as a whole should work together to nurture the feeling of belonging among older adults.
With physical distancing and home isolation recommendations, social media emerged as the main alternative for individuals to keep some human interaction, even if indirect. Media coverage of the COVID-19 pandemic played a key role in quick disseminating scientific research and information from health authorities. Conversely, fake news, derogatory memes, and offensive opinions spread (such as the hashtag #boomerremover) evinced the ageism prevailing in society, which misconceives coronavirus as a disease "of the old" and potentiates the discriminatory content against older persons 25,27 . Creating reliable, highquality content that confronts ageism is necessary to reduce the harmful effects of negative age-based stereotypes on older adults' health and well-being 25,48 .
Intergenerational tension (the conflict between people of different generations) is manifested on social networks in the form of anger and hatred as a result of some older adults' resistance in wearing masks or adhering to social isolation measures. Such social scenario also coined the notion that older individuals "have already lived their lives" and now it is time for them to resign, ignoring their autonomy and independence, and disregarding their social needs 17 .
By relying solely on age as a risk and lethality marker for COVID-19, these facts reveal the sharp difference and animosity between generations 17 .
Stereotyping older adults as fragile and dependent may incur issues in all generations, as younger ones will internalize and project this image into their own aging process. Besides age, other factors make individuals more vulnerable to COVID-19, such as the presence of chronic diseases and comorbidities 32 . Solidarity between generations is important to maximize support, interaction, and the social support network of older individuals during the pandemic 28 . A systematic review and meta-analysis of 63 studies (6,124 participants) found that interventions focused on education, intergenerational contact, and the combination of education and intergenerational contact were associated with ageism reduction 49 .
Social behavior in old age is yet another aggravating factor, often characterized by reduced social networks and decreased participation in social activities 50 . Likewise, older adults' limited access or capacity to use digital technologies may impede or hinder them from obtaining required goods, services, and social support during the pandemic, thus leaving them more vulnerable to isolation, depression, and loneliness 32 . For Previtali et al. 37 , access to technology and digital literacy were key elements for dealing with the challenges posed by quarantine.
Although protecting older adults from COVID-19 is crucial, respecting and supporting them in this complex situation is also important 26 . Considering the emergence of numerous ageist dilemmas and moral conflicts regarding the value of older people's lives in the midst of the pandemic, Ehni et al. 34 elaborated six aspects to combat ageism in pandemic reactions based on gerontological knowledge and the ethics of aging: 1) older adults are highly heterogeneous -their health and functioning are better than negative stereotypes suggest; 2) age limits for intensive care and other forms of medical care are inappropriate and unethical; 3) the deficient perspective regarding old age is dangerous for older adults and societies in general -intergenerational solidarity must be strengthened; 4) individuals must resist the assumption of a paternalistic attitude towards older groups; 5) the COVID-19 crisis requires older adults to use modern information and communication technologies; 6) for political orientation and for understanding the consequences of the COVID-19 crisis, not only the best of virology is necessary, but also that of gerontology.
Among the limitations of this study, we must consider that ageism in the context of the COVID-19 pandemic is still little discussed, which may explain the reduced number of publications addressing the theme and the higher prevalence of opinion pieces (editorials and comments). However, the critical-reflexive nature sustained by important theoretical assumptions enabled us to analyze several critical sociocultural aspects, comprehensive in public health.
Our results show an overview of the context and phenomenon addressed in the primary studies, bringing to light the issue of ageism, so important but little discussed in regard to the pandemic in Brazil and worldwide.
"Ageist" discourses may have negative social and psychological impacts on older adults' lives, so that authorities should redouble efforts to reduce ageism and the dissemination of information on this harmful practice. Further public policies and scientific studies addressing the theme should be developed to promote a more just and egalitarian society, with intergenerational solidarity and respect for the rights and lives of the older people.