Pre-frailty, frailty and associated factors in older caregivers of older adults

Roberta de Oliveira Máximo Ingrid Cristina Lopes Allan Gustavo Brigola Bruna Moretti Luchesi Aline Cristina Martins Gratão Keika Inouye Sofia Cristina Iost Pavarini Tiago da Silva Alexandre About the authors

ABSTRACT

INTRODUCTION

Providing care to an older adult is an activity that requires considerable physical effort and can cause stress and psychological strain, which accentuate factors that trigger the cycle of frailty, especially when the caregiver is also an older adult. However, few studies have analyzed the frailty process in older caregivers.

OBJECTIVES

To investigate the prevalence of pre-frailty, frailty and associated factors in older caregivers of older adults.

METHODS

A cross-sectional study was conducted including 328 community-dwelling older caregivers. Frailty was identified using frailty phenotype. Socio-demographic, behavioral and clinical aspects, characteristics related to care and functioning were covariables in the multinomial logistic regression.

RESULTS

The prevalence of pre-frailty and frailty were 58.8% and 21.1%, respectively. An increased age, female sex, not having a conjugal life, depressive symptoms and pain were commonly associated with pre-frailty and frailty. Sedentary lifestyle was exclusively associated with pre-frailty, whereas living in an urban area, low income and the cognitive decline were associated with frailty. A better performance on instrumental activities of daily living reduced the chance of frailty.

CONCLUSION

Many factors associated with the frailty syndrome may be related to the act of providing care, which emphasizes the importance of the development of coping strategies for this population.

Caregivers; Adult; Frail Elderly; Frailty; Epidemiology; Risk Factors; Socioeconomic Factors; Cross-Sectional Studies

INTRODUCTION

Providing care for a dependent person is a complex task that requires substantial effort and is often only one of the many obligations of family members or informal caregivers11. Cassie KM, Sanders S. Familial caregivers of older adults. J Gerontol Soc Work. 2008;50 Suppl 1:293-320. https://doi.org/10.1080/01634370802137975
https://doi.org/10.1080/0163437080213797...
. Moreover, these individuals tend to have little technical knowledge and limited training to perform this task22. Chiao CY, Wu HS, Hsiao CY. Caregiver burden for informal caregivers of patients with dementia: a systematic review. Int Nurs Rev. 2015;62(3):340-50. https://doi.org/10.1111/inr.12194
https://doi.org/10.1111/inr.12194...
.

Informal care is usually provided by a family member in the same age group as the care recipient (generally a wife or daughter)33. Hartmann ML, Mello JA, Anthierens S, DeclercqA, Van Durme T, Cès S, et al. Caring for a frail older person : the association between informal caregiver burden and being unsatisfied with support from family and friends. Age Ageing. 2019;1-7. https://doi.org/10.1093/ageing/afz054
https://doi.org/10.1093/ageing/afz054...
. Besides facing their own aging process and health problems44. Johnson RW, Wiener JM. A profile of frail older Americans and their caregivers. Washington, DC: The Urban Institute; 2006 [cited 23 Nov 2018]. p.5-78. Available from: https://www.urban.org/sites/default/files/publication/42946/311284-A-Profile-of-Frail-Older-Americans-and-Their-Caregivers.PDF
https://www.urban.org/sites/default/file...
, these individuals must deal with a variable and increasing load of tasks throughout the care process55. Sautter JM, Tulsky JA, Johnson KS, Olsen MK, Burton-Chase AM, Lindquist JH, et al. Caregiver experience during patients’ advanced chronic illness and last year of life. J Am Geriatr Soc. 2014;62(6):1082-90. https//doi.org/10.1111/jgs.12841
https//doi.org/10.1111/jgs.12841...
. These tasks generally involve changes in routine, burden, stress, social isolation and the considerable expenditure of economic resources – which have physical and psychological repercussions for the caregiver66. Brinda EM, Rajkumar AP, Enemark U, Attermann J, Jacob KS. Cost and burden of informal caregiving of dependent older people in a rural Indian community. BMC Health Serv Res. 2014;14:207. https://doi.org/10.1186/1472-6963-14-207
https://doi.org/10.1186/1472-6963-14-207...
, making such individuals more vulnerable to diseases88. Berglund E, Lytsy P, Westerling R. Health and wellbeing in informal caregivers and non-caregivers: a comparative cross-sectional study of the Swedish general population. Health Qual Life Outcomes. 2015;13:109. https://doi.org/10.1186/s12955-015-0309-2
https://doi.org/10.1186/s12955-015-0309-...
,99. Ferreira CG Alexandre TS, Lemos ND. [Factors associated with the quality of life of caregivers of elderly individuals in home care]. Saude Soc. 2011;20(2):398-409. Portuguese. https://doi.org/10.1590/S0104-12902011000200012
https://doi.org/10.1590/S0104-1290201100...
. It is therefore plausible to suspect that the task of providing care for a dependent older adult, especially when the caregiver is also an older adult, can further increase the chance of these individuals entering the cycle of frailty.

Frailty is defined as a clinical state in which there is an increased physical and/or psychological vulnerability to the development of dependence and/or even mortality when someone is exposed to stressors1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
,1111. Morley JE, Vellas B, Kan GA, Anker SD, Bauer JM, Bernabei R, et al. Frailty consensus: a call to action. J Am Med Dir Assoc. 2013;14(6):392-7. https://doi.org/10.1016/j.jamda.2013.03.022
https://doi.org/10.1016/j.jamda.2013.03....
. The relationship between providing care and developing frailty in older caregivers of older adults has been explored in the literature. However, the association between frailty and the number of years and hours per day dedicated to providing care, financial and social support offered to the caregiver, and the burden that these individuals experience have not yet been fully clarified.

A case-control study conducted in Belgium with 79 caregivers of spouses and 79 controls found that the older caregivers had a greater chance of being frail, a greater use of antidepressants, shorter nights of sleep and greater difficulty in maintaining social contacts compared with those who were not caregivers. However, neither caregiver burden nor the time dedicated to providing care increased the chance of frailty in this group1212. Potier F, Degryse JM, Aubouy G, Henrard S, Bihin B, Debacq-Chainiaux F, et al. Spousal caregiving is associated with an increased risk of frailty: a case-control study. J Frailty Aging. 2018;7(3):170-5. https://doi.org/10.14283/jfa.2018.11
https://doi.org/10.14283/jfa.2018.11...
.

A cross-sectional study conducted in Brazil with 148 older caregivers of older adults recruited from healthcare services investigated the occurrence of frailty in four groups based on the presence/absence of multimorbidity and high or low care-related burden. The prevalence of pre-frailty and frailty was 46% and 35.1%, respectively, and the authors found a greater chance of frailty only in the group of caregivers with multimorbidity, regardless of care-related burden1313. Alves EVC, Flesch LD, Cachioni M, Neri AL, Batistoni SST. The double vulnerability of elderly caregivers: multimorbidity and perceived burden and their associations with frailty. Rev Bras Geriatr Gerontol. 2018;21(3):301-11. https://doi.org/10.1590/1981-22562018021.180050
https://doi.org/10.1590/1981-22562018021...
.

A cohort study conducted in Belgium followed up 78 caregivers of community-dwelling spouses with cognitive or functional impairment for 16 months. The authors found that most caregivers were pre-frail at baseline and so remained throughout the study, whereas one-third became frail. Moreover, the care-related burden remained stable throughout the follow-up period, but the use of medications and anxiolytics increased1414. Potier F, Degryse JM, Bihin B, Debacq-Chainiaux F, Charlet-Renard C, Martens H, et al. Health and frailty among older spousal caregivers: an observational cohort study in Belgium. BMC Geriatr. 2018;18:291. https://doi.org/10.1186/s12877-018-0980-3
https://doi.org/10.1186/s12877-018-0980-...
.

Therefore, our study aims to determine the prevalence of pre-frailty and frailty in older adults who provide care for other older adults and investigate associations with socio-demographic factors, behavioral characteristics, health status, functioning and characteristics of the care process.

METHODS

A cross-sectional study was conducted with data from community-dwelling older caregivers (age ≥ 60 years) recruited from urban and rural areas of coverage of the 18 Family Health Units (FHU) in the city of São Carlos, southeastern region of the state of São Paulo, Brazil.

The sample was selected based on a list of the total number of households within the catchment area of these 18 centers provided by employees of the primary care units, and which had at least two older people living together. Each caregiver met the following inclusion criteria: 1) aged 60 years or older, 2) registered with and residing in the area of coverage of one of the primary healthcare centers in the city and 3) providing care to a dependent older adult living in the same household. The care recipient had to be dependent on at least one basic activity of daily living (BADL) or instrumental activity of daily living (IADL)1515. Luchesi BM, Souza EN, Gratão ACM, Gomes GA, Inouye K, Alexandre TS, et al. The evaluation of perceived stress and associated factors in elderly caregivers. Arch Gerontol Geriatr. 2016;67:7-13. https://doi.org/10.1016/j.archger.2016.06.017
https://doi.org/10.1016/j.archger.2016.0...
, assessed using the Katz Index1616. Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The Index of ADL: a standardized measure of biological and psychosocial function. JAMA. 1963;185(12):914-9. https://doi.org/10.1001/jama.1963.03060120024016
https://doi.org/10.1001/jama.1963.030601...
and Lawton and Brody Scale1717. Lawton MP. The functional assessment of elderly people. J Am Geriatr Soc. 1971;19(6):465-81. https://doi.org/10.1111/j.1532-5415.1971.tb01206.x
https://doi.org/10.1111/j.1532-5415.1971...
, respectively.

The initial number of households was 594. Of this total, 26 were excluded due to the death of one of the older adults, 28 were excluded because the residents had moved to a different address and 69 were excluded due to a lack of contact (no one at home at three attempts to visit). The remaining 471 families were visited, of which 84 were excluded because the older adults declined to participate in the study. All older adults that resided in a total of 387 households (response rate: 82.2%) were evaluated regarding functioning, and 36 families were excluded because both older adults were classified as independent considering basic and instrumental activities of daily living. Thus, older caregivers were identified and interviewed in 351 households1818. Luchesi BM, Alexandre TS, Oliveira NA, Brigola AG, Kusumota L, Pavarini SCI, et al. Factors associated with attitudes toward the elderly in a sample of elderly caregivers. Int Psychogeriatr. 2016;28(12):2079-89. https://doi.org/10.1017/S1041610216001538
https://doi.org/10.1017/S104161021600153...
. In our study, among the 351 caregivers interviewed, 23 were excluded due to a lack of information on the variables of the frailty phenotype or the independent variables, resulting in a final sample of 328 caregivers. Figure 1 shows the flowchart of sample selection.

Figure 1
Flowchart of sample selection.

This project was approved by the local institutional review board (certificate number: 416.467/2013) and all participants signed an informed consent form.

Frailty

The components of the frailty phenotype were identified using the modified version of the operational model proposed by Fried et al.1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
.

Unintentional weight loss was considered the loss of 4.5 kilograms or 5% of one’s body weight in the previous 12 months1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
.

Fatigue was analyzed using two questions based on the Center for Epidemiologic Studies Depression Scale (CES-D): a) How often have you felt that everything required considerable effort in the last week? b) How often in the past week have you felt that it is was difficult to “get going”? Fatigue was considered for older adults who reported having at least one of these feelings more than three days in the prior week1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
.

Grip strength (in kg) was measured using a dynamometer (Jamar, model SH5001), of which the highest value out of three trials was considered for the analysis. Weakness was considered for the 20% weakest individuals in each quartile of the body mass index (BMI) stratified by sex and using the cutoff points for the Brazilian population1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
. Walking speed was determined by the fastest performance out of three consecutive trials, in which every individual should walk 4.6 meters on a flat surface. Slowness was considered for the 20% slowest individuals based on mean height and stratified by sex1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
.

Physical activity level was evaluated using the Brazilian version of the International Physical Activity Questionnaire (IPAQ) and the estimate of metabolic equivalents (MET – min/week)2020. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al. International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381-95. https://doi.org/10.1249/01.MSS.0000078924.61453.FB
https://doi.org/10.1249/01.MSS.000007892...
. Caloric expenditure lower than 478.15 kcal in women and 390.5 kcal in men (lowest quintile) was considered as an indicative of a low level of physical activity1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
.

Individuals with none of these components were classified as non-frail, those with one or two components as pre-frail and those with three or more components as frail1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
.

Covariables

The variables associated with pre-frailty and frailty, previously tested in a hierarchical model1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
were included in our study along with characteristics related to providing care grouped into the following five hierarchical blocks, as shown in Figure 2:

Socio-demographic aspects: age and sex (caregiver and care recipient), marital status (with/without a conjugal life), private health insurance (yes/no), household income (categorized based on the Brazilian monthly minimum wage in 2014 [R$ 724.00 = US$ 222.80]), schooling level (in years) and place of residence (urban/rural);

Behavioral aspects: based on the results of the IPAQ, caregivers who performed less than 150 minutes of moderate or 75 minutes of vigorous physical activity per week were considered sedentary2020. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al. International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381-95. https://doi.org/10.1249/01.MSS.0000078924.61453.FB
https://doi.org/10.1249/01.MSS.000007892...
,2121. World Health Organization. Global recommendations on physical activity for health. Geneva: WHO; 2010 [cited 2018 Nov 23]. Available from: https://apps.who.int/iris/bitstream/handle/10665/44399/9789241599979_eng.pdf;jsessionid=9FC5BFCDF2F94EC29EE5D6ED7F3D8E56?sequence=1
https://apps.who.int/iris/bitstream/hand...
;

Health status: self-reported arterial hypertension, diabetes, cancer, lung disease, heart disease, stroke, joint disease, anemia, pain and number of medications in use. BMI was classified according to the Pan American Health Organization recommendation2222. Organización Panamericana de la Salud. Guía clínica para atención primaria a las personas adultas mayores. Washington, DC: OPS; 2003.. The screening for cognitive decline of the caregiver and care recipient was evaluated using the Mini Mental State Examination (MMSE) with the cutoff points ≤ 19 for illiterate individuals and ≤ 23 points for those with some level of schooling2323. Almeida OP. [Mini-mental state examination and the diagnosis of dementia in Brazil]. Arq Neuropsiquiatr. 1998;56(3B):605-12. Portuguese. https://doi.org/10.1590/S0004-282X1998000400014
https://doi.org/10.1590/S0004-282X199800...
. Depression was analyzed using the Geriatric Depression Scale (GDS), in which a score > 5 points is considered indicative of depressive symptoms2424. Almeida OP, Almeida SA. Short versions of the Geriatric Depression Scale: a study of their validity for the diagnosis of a major depressive episode according to ICD-10 and DSM-IV. Int J Geriatr Psychiatry. 1999;14(10):858-65. https://doi.org/10.1002/(SICI)1099-1166(199910)14:10<858::AID-GPS35>3.0.CO;2-8
https://doi.org/10.1002/(SICI)1099-1166(...
;

Care characteristics: care recipient’s relationship to caregiver (spouse, parent, mother/father-in-law, sibling), duration of care (in years), number of hours per day dedicated to providing care, whether the caregiver receives material, financial or emotional support with regards to providing care. Caregiver burden was evaluated using the Zarit Caregiver Burden Scale. The caregivers were classified as having a low burden (0-20 points), moderate burden (21-40); moderate to severe burden (41-60) or severe burden (61-88)2525. Schreiner AS, Morimoto T, Arai Y, Zarit S. Assessing family caregiver’s mental health using a statistically derived cut-off score for the Zarit Burden Interview. Aging Ment Health. 2006;10(2):107-11. https://doi.org/10.1080/13607860500312142
https://doi.org/10.1080/1360786050031214...
;

Functionality: BADL were evaluated using the Katz Index (transferring, feeding, continence, toileting, bathing and dressing)1616. Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The Index of ADL: a standardized measure of biological and psychosocial function. JAMA. 1963;185(12):914-9. https://doi.org/10.1001/jama.1963.03060120024016
https://doi.org/10.1001/jama.1963.030601...
, with a score ranging between 0 and 6 points. IADL were evaluated using the Lawton and Brody Scale (using the telephone, using transportation, shopping, preparing meals, housekeeping, managing medications and managing finances)1717. Lawton MP. The functional assessment of elderly people. J Am Geriatr Soc. 1971;19(6):465-81. https://doi.org/10.1111/j.1532-5415.1971.tb01206.x
https://doi.org/10.1111/j.1532-5415.1971...
, with a score ranging between 0 and 21 points. The scores of BADL and IADL were analyzed as continuous variables, with higher score indicating greater recipient’s independence.

Statistical analysis

Simple descriptive analyses were performed to define the characteristics of the sample. The prevalence of frailty was estimated using a 95% confidence interval (CI). Factors associated with pre-frailty and frailty were analyzed using multinomial logistic regression, considering non-frail older caregivers as the reference. Associations with a p-value ≤ 0.20 in the univariate analyses were selected for the hierarchical modeling, which is used in epidemiological studies due to the large number of factors involved in the genesis of diseases or syndromes (making it a good method for studying frailty) and because this type of approach enables the analysis of associations on different levels. The choice of variables should be based on a theoretical model that can explain the probable pathways involved in the development of a disease2626. Witte JS, Greenland S, Haile RW, Bird CL. Hierarchical regression analysis applied to a study of multiple dietary exposures and breast cancer. Epidemiology. 1994 [cited 23 Jul 2019];5(6):612-21. Available from: http://www.jstor.org/stable/3702298
http://www.jstor.org/stable/3702298...
.

The factors analyzed were grouped into blocks and arranged according to the proximity to their influence on frailty (Figure 2). The highest level included socio-demographic variables as distal factors; intermediate level included behavioral variables, and the lowest level included variables that represent health status, the characteristics of providing care and functionality. The first model was used to analyze the relationship between the frailty components and distal factors. The same strategy was adopted for the incorporation of intermediate and proximal factors in the model1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
. The identification of a statistically significant association (p < 0.05) between a particular factor and frailty showed an independent effect on the factor in question on a specific level1919. Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
https://doi.org/10.1177/0898264313519818...
.

Figure 2
Theoretical model for investigation of factors associated with pre-frailty and frailty among older caregivers of older adults structured in hierarchical blocks.

The Stata 14® program (Stata Corp., College Station, TX) was used for all analyses.

RESULTS

The mean age of the care recipients was 73 years. Most recipients were men (70.7%), more than half exhibited cognitive impairment (52.8%) and the mean performance on the Katz Index was 5.1 ± 1.8 and the Lawton Scale was 13.6 ± 4.0. Among the caregivers, mean age was 69 years, 77.4% were women and the most prevalent clinical condition was systemic arterial hypertension, followed by pain, joint disease and diabetes. Regarding functionality, the caregivers showed good performance in both the Katz Index and the Lawton Scale, with averages of 5.8 ± 0.4 points e 19.2 ± 2.3 points, respectively. Regarding frailty, 58.8% (95%CI: 53.3-64.2%) of the caregivers were considered pre-frail and 21.1% (95%CI: 16.8-25.9%) were considered frail. Details of the sample characteristics are shown in Tables 1 and 2.

Table 1
Descriptive socio-demographic, behavioral and health characteristics of older caregivers in São Carlos, Brazil, 2014 – 2015 (n = 328)
Table 2
Descriptive care, functionality and frailty characteristics of older caregivers in São Carlos, Brazil, 2014 – 2015 (n = 328)

The participants excluded were men and had a lower mean level of schooling, worse performance on the activities evaluated using the Katz Index, a greater prevalence of stroke and received less material and financial assistance when compared with the individuals included in the study (p < 0.05, data not shown).

Table 3 displays the final multinomial logistic regression model for factors associated with pre-frailty and frailty among the older caregivers of older adults. The odds ratio (OR) of the final model for factors associated with pre-frailty were 1.10 for each year of increase in age, 12.03 for caregivers without a conjugal life, 4.76 for women, 9.64 for sedentary individuals, 4.61 for those with GDS > 5 points and 2.11 for those who felt pain. The OR of the final model for factors associated with frailty were 1.17 for each year of increase in age, 15.39 for caregivers without a conjugal life, 3.59 for women, 3.85 for those residing in urban areas, 3.86 for those with income between two and five times the Brazilian monthly minimum wage, 10.21 for those with GDS > 5 points, 2.74 for those who felt pain, 2.54 for those with a MMSE score below the cutoff point adjusted for schooling and 0.70 for each unit increase on the Lawton and Brody Scale.

Table 3
Final multinomial logistic regression model for factors associated with pre-frailty and frailty in older caregivers of older adults in São Carlos, Brazil, 2014 – 2015

DISCUSSION

Our main results showed that the prevalence of pre-frailty and frailty was high among older caregivers. Increased age, being woman, not having a conjugal life, depressive symptoms and pain were factors associated with both pre-frailty and frailty. A sedentary lifestyle was exclusively associated with pre-frailty, whereas living in an urban area, low income and cognitive decline were exclusively associated with frailty. Moreover, a better performance on IADL reduced the chance of frailty.

The prevalence of pre-frailty and frailty was high among the older caregivers in our study and differ from those reported in the literature. For example, in Mexican Americans, the prevalence of pre-frailty and frailty were 45.7% and 4.3%, respectively2727. Al Snih S, Graham JE, Ray LA, Samper-Ternent R, Markides KS, Ottenbacher KJ. Frailty and incidence of activities of daily living disability among older Mexican Americans. J Rehabil Med. 2009;41(11):892-7. https://doi.org/10.2340/16501977-0424
https://doi.org/10.2340/16501977-0424...
. In Taiwanese individuals, Chang et al.2828. Chang SF, Yang RS, Nieh HM, Wen GM. Prevalence and risk factors of frailty phenotype among vulnerable solitary elderly individuals. Int J Nurs Pract. 2015;21(3):321-7. https://doi.org/10.1111/ijn.12280
https://doi.org/10.1111/ijn.12280...
found a 19.8% prevalence of pre-frailty and a 35% prevalence of frailty. Runzer-Colmenares et al.2929. Runzer-Colmenares FM, Samper-Ternent R, Al Snih S, Ottenbacher KJ, Parodi JF, Wong R. Prevalence and factors associated with frailty among Peruvian older adults. Arch Gerontol Geriatr. 2014;58(1):69-73. https://doi.org/10.1016/j.archger.2013.07.005
https://doi.org/10.1016/j.archger.2013.0...
found a 47.3% prevalence of pre-frailty and a 27.8% prevalence of frailty in a study involving Peruvians older adults, while Moreira & Lourenço3030. Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
https://doi.org/10.6061/clinics/2013(07)...
found a prevalence of 47.3% and 9.1% for pre-frailty and frailty, respectively, in the Brazilian population.

The difference in prevalence between our investigation and previous studies was expected, since our sample was composed exclusively of caregivers. This suggests that the prevalence of pre-frailty and frailty is higher among caregivers, possibly because the provision of care can easily lead to the entry into the cycle of frailty when performed by another older person, who are already more vulnerable due to their age and morbidities3131. Tomomitsu MRSV, Lemos ND, Perracini MR. Prevalência e fatores associados à fragilidade em cuidadores idosos Geriatr Gerontol. 2010 [cited 23 Jul 2019];4(1):3-12. Available from: https://s3-sa-east-1.amazonaws.com/publisher.gn1.com.br/ggaging.com/pdf/v4n1a02.pdf
https://s3-sa-east-1.amazonaws.com/publi...
. This hypothesis is reinforced by the findings of a study3131. Tomomitsu MRSV, Lemos ND, Perracini MR. Prevalência e fatores associados à fragilidade em cuidadores idosos Geriatr Gerontol. 2010 [cited 23 Jul 2019];4(1):3-12. Available from: https://s3-sa-east-1.amazonaws.com/publisher.gn1.com.br/ggaging.com/pdf/v4n1a02.pdf
https://s3-sa-east-1.amazonaws.com/publi...
involving older Brazilian caregivers of older adults, in which the prevalence of pre-frailty (54%) and frailty (18%) are very similar to that found in our investigation.

The results of our study are consistent with earlier findings of factors associated with pre-frailty and frailty such as the increase in the prevalence of frailty with the increase in age1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
,2727. Al Snih S, Graham JE, Ray LA, Samper-Ternent R, Markides KS, Ottenbacher KJ. Frailty and incidence of activities of daily living disability among older Mexican Americans. J Rehabil Med. 2009;41(11):892-7. https://doi.org/10.2340/16501977-0424
https://doi.org/10.2340/16501977-0424...
,3030. Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
https://doi.org/10.6061/clinics/2013(07)...
,3232. Vieira RA, Guerra RO, Giacomin KC, Vasconcelos KSS, Andrade ACS, Pereira LSM, et al. Prevalência de fragilidade e fatores associados em idosos comunitários de Belo Horizonte, Minas Gerais, Brasil: dados do estudo FIBRA. Cad Saude Publica. 2013;29(8):1631-43. https://doi.org/10.1590/0102-311X00126312
https://doi.org/10.1590/0102-311X0012631...
,3333. Eyigor S, Kutsal YG, Duran E, Huner B, Paker N, Durmus B, et al. Frailty prevalence and related factors in the older adult - FrailTURK Project. 2015;37(3):9791. https://doi.org/10.1007/s11357-015-9791-z
https://doi.org/10.1007/s11357-015-9791-...
and the greater odds of women being pre-frail or frail1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
,3232. Vieira RA, Guerra RO, Giacomin KC, Vasconcelos KSS, Andrade ACS, Pereira LSM, et al. Prevalência de fragilidade e fatores associados em idosos comunitários de Belo Horizonte, Minas Gerais, Brasil: dados do estudo FIBRA. Cad Saude Publica. 2013;29(8):1631-43. https://doi.org/10.1590/0102-311X00126312
https://doi.org/10.1590/0102-311X0012631...
,3333. Eyigor S, Kutsal YG, Duran E, Huner B, Paker N, Durmus B, et al. Frailty prevalence and related factors in the older adult - FrailTURK Project. 2015;37(3):9791. https://doi.org/10.1007/s11357-015-9791-z
https://doi.org/10.1007/s11357-015-9791-...
. Women have less muscle mass and strength than men and undergo a more rapid decline in muscle strength during menopause3434. Duarte YAO, Lebrão ML. Fragilidade e envelhecimento In: Freitas EV, Py L, Cançado FAX, Editores. Tratado de geriatria e gerontologia. 3. ed. Rio de Janeiro: Guabanara Koogan; 2011. p. 1802-19.. Women also have a greater life expectancy and greater frequency of disabling chronic diseases than men3535. Hubbard RE. Sex differences in frailty. Interdiscip Top Gerontol Geriatr. 2015;41:41-53. https://doi.org/10.1159/000381161
https://doi.org/10.1159/000381161...
,3636. Alexandre TS, Corona LP, Brito TRP, Santos JLF, Duarte YAO, Lebrão ML. Gender differences in the incidence and determinants of components of the frailty phenotype among older adults: findings from the SABE Study. J Aging Health. 2018;30(2):190-212. https://doi.org/10.1177/0898264316671228
https://doi.org/10.1177/0898264316671228...
. Thus, women, who are generally responsible for the care provided to a spouse, mother or father, are at a biological disadvantage regarding the intrinsic physical load of providing care and have a greater chance of presenting pre-frailty and frailty when compared with men.

In the sample of our study, caregivers without a conjugal life were usually the care recipient’s son, daughter, brother or sister. Previous studies have shown that these caregivers have a worse perception regarding the reduction in or complete abandonment of professional, social and leisure activities3030. Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
https://doi.org/10.6061/clinics/2013(07)...
. This may imply an increase in the prevalence of depressive symptoms and exhaustion as well as a reduction in physical activity, which may explain the greater chance of pre-frailty and frailty in this group.

The occurrence of depressive symptoms was associated with both pre-frailty and frailty, which agrees with data described by Vieira et al.3232. Vieira RA, Guerra RO, Giacomin KC, Vasconcelos KSS, Andrade ACS, Pereira LSM, et al. Prevalência de fragilidade e fatores associados em idosos comunitários de Belo Horizonte, Minas Gerais, Brasil: dados do estudo FIBRA. Cad Saude Publica. 2013;29(8):1631-43. https://doi.org/10.1590/0102-311X00126312
https://doi.org/10.1590/0102-311X0012631...
and Curcio et al.3737. Curcio CL, Henao GM, Gomez F. Frailty among rural elderly adults. BMC Geriatr. 2014;14:2. https://doi.org/10.1186/1471-2318-14-2
https://doi.org/10.1186/1471-2318-14-2...
, who found that older adults with depressive symptoms had a 160% greater chance of being frail. Depressive symptoms have been evidenced to negatively impact the homeostatic balance of the immune system3838. Kiecolt-Glaser JK, Glaser R. Depression and immune function: central pathways to morbidity and mortality. J Psychosom Res. 2002;53(4):873-6. https://doi.org/10.1016/S0022-3999(02)00309-4
https://doi.org/10.1016/S0022-3999(02)00...
,3939. Reiche EMV, Nunes SOV, Morimoto HK. Stress, depression, the immune system, and cancer. Lancet Oncol. 2004;5(10):617-25. https://doi.org/10.1016/S1470-2045(04)01597-9
https://doi.org/10.1016/S1470-2045(04)01...
, increasing their chance of becoming frail. In a meta-analysis, Segerstrom and Miller4040. Segerstrom SC, Miller GE. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull. 2004;130(4):601-30. https://doi.org/10.1037/0033-2909.130.4.601
https://doi.org/10.1037/0033-2909.130.4....
found that stressful events such as providing care can cause psychosocial and physiological changes. Thus, depressive symptoms may increase the chance of older adults presenting unintentional weight loss, exhaustion and low levels of physical activity1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
,3838. Kiecolt-Glaser JK, Glaser R. Depression and immune function: central pathways to morbidity and mortality. J Psychosom Res. 2002;53(4):873-6. https://doi.org/10.1016/S0022-3999(02)00309-4
https://doi.org/10.1016/S0022-3999(02)00...
, which are important components of frailty. However, we point out that the GDS and the CES-D, which are assessment tools that address exhaustion in the model proposed by Fried et al.1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
, were originally designed to measure the same phenomenon (depression) and that there could be some degree of collinearity in these associations.

Pain was associated with both frailty and pre-frailty. Persistent pain in older adults has been suggested to contribute to the frailty process through mechanisms such as reduced mobility, depression, decreased nutritional intake and the burden of comorbidities4141. Brown L, Young J, Clegg A, Heaven A. Pain in older people with frailty. Rev Clin Gerontol. 2015;25(3):159-71. https://doi.org/10.1017/S0959259815000143
https://doi.org/10.1017/S095925981500014...
. The literature shows that the physical burden of providing care may be one of the causal mechanisms of pain in older caregivers4242. Darragh AR, Sommerich CM, Lavender SA, Tanner KJ, Vogel K, Campo M. Musculoskeletal discomfort, physical demand and caregiving activities in informal caregivers. J Appl Gerontol. 2015;34(6):734-60. https://doi.org/10.1177/0733464813496464
https://doi.org/10.1177/0733464813496464...
.

Sedentarism was exclusively associated with pre-frailty. A sedentary lifestyle contributes to a reduction in muscle mass and strength and tolerance to exercise with ageing1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
. Moreover, taking on the burden of providing care for a family member along with heavy responsibilities other than caregiving, fatigue, anxiety and depressive symptoms may hinder the practice of physical activity4343. Farran CJ, Staffileno BA, Gilley DW, McCann JJ, Li Y, Castro CM, et al. A lifestyle physical activity intervention for caregivers of persons with Alzheimer’s disease. Am J Alzheimers Dis Other Demen. 2008;23(2):132-42. https://doi.org/10.1177/1533317507312556
https://doi.org/10.1177/1533317507312556...
. Thus, the disengagement in physical activity, especially among older women with functional limitations, and the reduction in outdoor activities may explain the association between a sedentary lifestyle and pre-frailty. Such aspects have also been shown in previous studies involving older caregivers of older adults1414. Potier F, Degryse JM, Bihin B, Debacq-Chainiaux F, Charlet-Renard C, Martens H, et al. Health and frailty among older spousal caregivers: an observational cohort study in Belgium. BMC Geriatr. 2018;18:291. https://doi.org/10.1186/s12877-018-0980-3
https://doi.org/10.1186/s12877-018-0980-...
,4444. Gomes GAO, Luchesi BM, Gratão ACM, Orlandi FS, Say KG, Inouye K, et al. Prevalence of physical inactivity and associated factors among older caregivers of older adults. J Aging Health. 2019;31(5):793-813. https://doi.org/10.1177/0898264318756422
https://doi.org/10.1177/0898264318756422...
.

Having a lower income and residing in an urban area were exclusively associated with frailty. Insufficient income, poverty and socio-demographic inequality can result in social and health disadvantages and cause more periods of chronic stress during the course of one’s life, affecting physical and cognitive development, especially among older caregivers1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
,3030. Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
https://doi.org/10.6061/clinics/2013(07)...
,4545. Woo J, Goggins W, Sham A, Ho SC. Social determinants of frailty. Gerontology. 2005;51(6):402-8. https://doi.org/10.1159/000088705
https://doi.org/10.1159/000088705...
. Residing in an urban area agrees with data that state that must be due to the selection of mortality as well as negative impact exert by differences in lifestyle, support networks and other environmental factors. Moreover, studies have suggested that residents of rural areas are more engaged in activities, which could positively effect quality of life, thus reducing the chance of developing frailty4646. Gu D, Dupre ME, Sautter J, Zhu H, Liu Y, Yi Z. Frailty and mortality among chinese at advanced ages. J Gerontol B Psychol Sci Soc Sci. 2009;64(2):279-89. https://doi.org/10.1093/geronb/gbn009
https://doi.org/10.1093/geronb/gbn009...
.

Cognitive impairment was associated with frailty, which agrees with findings described by Moreira & Lourenço3030. Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
https://doi.org/10.6061/clinics/2013(07)...
and Curcio et al.3737. Curcio CL, Henao GM, Gomez F. Frailty among rural elderly adults. BMC Geriatr. 2014;14:2. https://doi.org/10.1186/1471-2318-14-2
https://doi.org/10.1186/1471-2318-14-2...
. We emphasized that Fried et al.1010. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
https://doi.org/10.1093/gerona/56.3.M146...
excluded older adults with cognitive decline during the validation of the frailty phenotype, since these individuals are likely to become frail. Samper-Ternent et al.4747. Samper-Ternent R, Al Snih S, Raji MA, Markides KS, Ottenbacher KJ. Relationship between frailty and cognitive decline in older Mexican Americans. J Am Geriatr Soc. 2008;56(10):1845-52. Available from: https://doi.org/10.1111/j.1532-5415.2008.01947.x
https://doi.org/10.1111/j.1532-5415.2008...
and Buchmann et al.4848. Buchman AS, Boyle PA, Wilson RS, Tang Y, Bennett DA. Frailty is associated with incident Alzheimer’s disease and cognitive decline in the elderly. 2007;69(5):483-9. https://doi.org/10.1097/psy.0b013e318068de1d
https://doi.org/10.1097/psy.0b013e318068...
suggest that cognitive decline and frailty syndrome may have common etiological pathways, resulting in slowness, unintentional weight loss and muscle weakness. However, further studies are needed to establish this relationship and explain the biological and psychological processes by which frailty and cognitive decline are related.

A better performance on IADL reduced the odds of being frail, which may be supported by the fact that better performance in IADL means greater participation in activities away from home, and possibly a better physical status that prevent from frailty.

Despite having analyzed factors associated with pre-frailty and frailty in older caregivers, variables related to providing care did not remain in the final model. A possible explanation may reside in the fact that the associations between frailty and an advanced age, not having a conjugal life, being a woman, having a low income, exhibiting depressive symptoms and experiencing pain per se have been strong characteristics associated with providing care in previous studies. This may have impeded associations with variables that are more directly related to the act of providing care in the present study.

Our study has some strong points. We can cite the involvement of a large sample of older caregivers of other older adults registered in primary healthcare centers. Moreover, it analyzed a broad range of variables capable of increasing the odds of frailty in older caregivers. The main limitation is the fact that a cross-sectional design does not enable the establishment of relationships of causality between the variables studied and the frailty syndrome. Also, individuals excluded due to the lack of information were less schooled, more dependent, had a higher prevalence of stroke and were predominantly men, which may have somehow prevented associations between frailty and these variables.

CONCLUSION

The prevalence of pre-frailty and frailty was high among the older caregivers in our study. Many factors associated with the frailty syndrome may be related to the act of providing care, which emphasizes the importance of a close examination of the need for caregiver support and the development of coping strategies for this population.

REFERENCES

  • 1
    Cassie KM, Sanders S. Familial caregivers of older adults. J Gerontol Soc Work. 2008;50 Suppl 1:293-320. https://doi.org/10.1080/01634370802137975
    » https://doi.org/10.1080/01634370802137975
  • 2
    Chiao CY, Wu HS, Hsiao CY. Caregiver burden for informal caregivers of patients with dementia: a systematic review. Int Nurs Rev. 2015;62(3):340-50. https://doi.org/10.1111/inr.12194
    » https://doi.org/10.1111/inr.12194
  • 3
    Hartmann ML, Mello JA, Anthierens S, DeclercqA, Van Durme T, Cès S, et al. Caring for a frail older person : the association between informal caregiver burden and being unsatisfied with support from family and friends. Age Ageing. 2019;1-7. https://doi.org/10.1093/ageing/afz054
    » https://doi.org/10.1093/ageing/afz054
  • 4
    Johnson RW, Wiener JM. A profile of frail older Americans and their caregivers. Washington, DC: The Urban Institute; 2006 [cited 23 Nov 2018]. p.5-78. Available from: https://www.urban.org/sites/default/files/publication/42946/311284-A-Profile-of-Frail-Older-Americans-and-Their-Caregivers.PDF
    » https://www.urban.org/sites/default/files/publication/42946/311284-A-Profile-of-Frail-Older-Americans-and-Their-Caregivers.PDF
  • 5
    Sautter JM, Tulsky JA, Johnson KS, Olsen MK, Burton-Chase AM, Lindquist JH, et al. Caregiver experience during patients’ advanced chronic illness and last year of life. J Am Geriatr Soc. 2014;62(6):1082-90. https//doi.org/10.1111/jgs.12841
    » https//doi.org/10.1111/jgs.12841
  • 6
    Brinda EM, Rajkumar AP, Enemark U, Attermann J, Jacob KS. Cost and burden of informal caregiving of dependent older people in a rural Indian community. BMC Health Serv Res. 2014;14:207. https://doi.org/10.1186/1472-6963-14-207
    » https://doi.org/10.1186/1472-6963-14-207
  • 7
    Adelman RD, Tmanova LL, Delgado D, Dion S, Lachs MS. Caregiver burden. JAMA. 2014;311(10):1052-60. https://doi.org/10.1001/jama.2014.304
    » https://doi.org/10.1001/jama.2014.304
  • 8
    Berglund E, Lytsy P, Westerling R. Health and wellbeing in informal caregivers and non-caregivers: a comparative cross-sectional study of the Swedish general population. Health Qual Life Outcomes. 2015;13:109. https://doi.org/10.1186/s12955-015-0309-2
    » https://doi.org/10.1186/s12955-015-0309-2
  • 9
    Ferreira CG Alexandre TS, Lemos ND. [Factors associated with the quality of life of caregivers of elderly individuals in home care]. Saude Soc. 2011;20(2):398-409. Portuguese. https://doi.org/10.1590/S0104-12902011000200012
    » https://doi.org/10.1590/S0104-12902011000200012
  • 10
    Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-57. https://doi.org/10.1093/gerona/56.3.M146
    » https://doi.org/10.1093/gerona/56.3.M146
  • 11
    Morley JE, Vellas B, Kan GA, Anker SD, Bauer JM, Bernabei R, et al. Frailty consensus: a call to action. J Am Med Dir Assoc. 2013;14(6):392-7. https://doi.org/10.1016/j.jamda.2013.03.022
    » https://doi.org/10.1016/j.jamda.2013.03.022
  • 12
    Potier F, Degryse JM, Aubouy G, Henrard S, Bihin B, Debacq-Chainiaux F, et al. Spousal caregiving is associated with an increased risk of frailty: a case-control study. J Frailty Aging. 2018;7(3):170-5. https://doi.org/10.14283/jfa.2018.11
    » https://doi.org/10.14283/jfa.2018.11
  • 13
    Alves EVC, Flesch LD, Cachioni M, Neri AL, Batistoni SST. The double vulnerability of elderly caregivers: multimorbidity and perceived burden and their associations with frailty. Rev Bras Geriatr Gerontol. 2018;21(3):301-11. https://doi.org/10.1590/1981-22562018021.180050
    » https://doi.org/10.1590/1981-22562018021.180050
  • 14
    Potier F, Degryse JM, Bihin B, Debacq-Chainiaux F, Charlet-Renard C, Martens H, et al. Health and frailty among older spousal caregivers: an observational cohort study in Belgium. BMC Geriatr. 2018;18:291. https://doi.org/10.1186/s12877-018-0980-3
    » https://doi.org/10.1186/s12877-018-0980-3
  • 15
    Luchesi BM, Souza EN, Gratão ACM, Gomes GA, Inouye K, Alexandre TS, et al. The evaluation of perceived stress and associated factors in elderly caregivers. Arch Gerontol Geriatr. 2016;67:7-13. https://doi.org/10.1016/j.archger.2016.06.017
    » https://doi.org/10.1016/j.archger.2016.06.017
  • 16
    Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The Index of ADL: a standardized measure of biological and psychosocial function. JAMA. 1963;185(12):914-9. https://doi.org/10.1001/jama.1963.03060120024016
    » https://doi.org/10.1001/jama.1963.03060120024016
  • 17
    Lawton MP. The functional assessment of elderly people. J Am Geriatr Soc. 1971;19(6):465-81. https://doi.org/10.1111/j.1532-5415.1971.tb01206.x
    » https://doi.org/10.1111/j.1532-5415.1971.tb01206.x
  • 18
    Luchesi BM, Alexandre TS, Oliveira NA, Brigola AG, Kusumota L, Pavarini SCI, et al. Factors associated with attitudes toward the elderly in a sample of elderly caregivers. Int Psychogeriatr. 2016;28(12):2079-89. https://doi.org/10.1017/S1041610216001538
    » https://doi.org/10.1017/S1041610216001538
  • 19
    Alexandre TS, Corona LP, Nunes DP, Santos JLF, Duarte YAO, Lebrão ML. Similarities among factors associated with components of frailty in elderly. J Aging Health. 2014;26(3):441-57. https://doi.org/10.1177/0898264313519818
    » https://doi.org/10.1177/0898264313519818
  • 20
    Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al. International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381-95. https://doi.org/10.1249/01.MSS.0000078924.61453.FB
    » https://doi.org/10.1249/01.MSS.0000078924.61453.FB
  • 21
    World Health Organization. Global recommendations on physical activity for health. Geneva: WHO; 2010 [cited 2018 Nov 23]. Available from: https://apps.who.int/iris/bitstream/handle/10665/44399/9789241599979_eng.pdf;jsessionid=9FC5BFCDF2F94EC29EE5D6ED7F3D8E56?sequence=1
    » https://apps.who.int/iris/bitstream/handle/10665/44399/9789241599979_eng.pdf;jsessionid=9FC5BFCDF2F94EC29EE5D6ED7F3D8E56?sequence=1
  • 22
    Organización Panamericana de la Salud. Guía clínica para atención primaria a las personas adultas mayores. Washington, DC: OPS; 2003.
  • 23
    Almeida OP. [Mini-mental state examination and the diagnosis of dementia in Brazil]. Arq Neuropsiquiatr. 1998;56(3B):605-12. Portuguese. https://doi.org/10.1590/S0004-282X1998000400014
    » https://doi.org/10.1590/S0004-282X1998000400014
  • 24
    Almeida OP, Almeida SA. Short versions of the Geriatric Depression Scale: a study of their validity for the diagnosis of a major depressive episode according to ICD-10 and DSM-IV. Int J Geriatr Psychiatry. 1999;14(10):858-65. https://doi.org/10.1002/(SICI)1099-1166(199910)14:10<858::AID-GPS35>3.0.CO;2-8
    » https://doi.org/10.1002/(SICI)1099-1166(199910)14:10<858::AID-GPS35>3.0.CO;2-8
  • 25
    Schreiner AS, Morimoto T, Arai Y, Zarit S. Assessing family caregiver’s mental health using a statistically derived cut-off score for the Zarit Burden Interview. Aging Ment Health. 2006;10(2):107-11. https://doi.org/10.1080/13607860500312142
    » https://doi.org/10.1080/13607860500312142
  • 26
    Witte JS, Greenland S, Haile RW, Bird CL. Hierarchical regression analysis applied to a study of multiple dietary exposures and breast cancer. Epidemiology. 1994 [cited 23 Jul 2019];5(6):612-21. Available from: http://www.jstor.org/stable/3702298
    » http://www.jstor.org/stable/3702298
  • 27
    Al Snih S, Graham JE, Ray LA, Samper-Ternent R, Markides KS, Ottenbacher KJ. Frailty and incidence of activities of daily living disability among older Mexican Americans. J Rehabil Med. 2009;41(11):892-7. https://doi.org/10.2340/16501977-0424
    » https://doi.org/10.2340/16501977-0424
  • 28
    Chang SF, Yang RS, Nieh HM, Wen GM. Prevalence and risk factors of frailty phenotype among vulnerable solitary elderly individuals. Int J Nurs Pract. 2015;21(3):321-7. https://doi.org/10.1111/ijn.12280
    » https://doi.org/10.1111/ijn.12280
  • 29
    Runzer-Colmenares FM, Samper-Ternent R, Al Snih S, Ottenbacher KJ, Parodi JF, Wong R. Prevalence and factors associated with frailty among Peruvian older adults. Arch Gerontol Geriatr. 2014;58(1):69-73. https://doi.org/10.1016/j.archger.2013.07.005
    » https://doi.org/10.1016/j.archger.2013.07.005
  • 30
    Moreira VG, Lourenço RA. Prevalence and factors associated with frailty in an older population from the city of Rio de Janeiro, Brazil: the FIBRA-RJ Study. Clinics (São Paulo)]. 2013;68(7):979-85. https://doi.org/10.6061/clinics/2013(07)15
    » https://doi.org/10.6061/clinics/2013(07)15
  • 31
    Tomomitsu MRSV, Lemos ND, Perracini MR. Prevalência e fatores associados à fragilidade em cuidadores idosos Geriatr Gerontol. 2010 [cited 23 Jul 2019];4(1):3-12. Available from: https://s3-sa-east-1.amazonaws.com/publisher.gn1.com.br/ggaging.com/pdf/v4n1a02.pdf
    » https://s3-sa-east-1.amazonaws.com/publisher.gn1.com.br/ggaging.com/pdf/v4n1a02.pdf
  • 32
    Vieira RA, Guerra RO, Giacomin KC, Vasconcelos KSS, Andrade ACS, Pereira LSM, et al. Prevalência de fragilidade e fatores associados em idosos comunitários de Belo Horizonte, Minas Gerais, Brasil: dados do estudo FIBRA. Cad Saude Publica. 2013;29(8):1631-43. https://doi.org/10.1590/0102-311X00126312
    » https://doi.org/10.1590/0102-311X00126312
  • 33
    Eyigor S, Kutsal YG, Duran E, Huner B, Paker N, Durmus B, et al. Frailty prevalence and related factors in the older adult - FrailTURK Project. 2015;37(3):9791. https://doi.org/10.1007/s11357-015-9791-z
    » https://doi.org/10.1007/s11357-015-9791-z
  • 34
    Duarte YAO, Lebrão ML. Fragilidade e envelhecimento In: Freitas EV, Py L, Cançado FAX, Editores. Tratado de geriatria e gerontologia. 3. ed. Rio de Janeiro: Guabanara Koogan; 2011. p. 1802-19.
  • 35
    Hubbard RE. Sex differences in frailty. Interdiscip Top Gerontol Geriatr. 2015;41:41-53. https://doi.org/10.1159/000381161
    » https://doi.org/10.1159/000381161
  • 36
    Alexandre TS, Corona LP, Brito TRP, Santos JLF, Duarte YAO, Lebrão ML. Gender differences in the incidence and determinants of components of the frailty phenotype among older adults: findings from the SABE Study. J Aging Health. 2018;30(2):190-212. https://doi.org/10.1177/0898264316671228
    » https://doi.org/10.1177/0898264316671228
  • 37
    Curcio CL, Henao GM, Gomez F. Frailty among rural elderly adults. BMC Geriatr. 2014;14:2. https://doi.org/10.1186/1471-2318-14-2
    » https://doi.org/10.1186/1471-2318-14-2
  • 38
    Kiecolt-Glaser JK, Glaser R. Depression and immune function: central pathways to morbidity and mortality. J Psychosom Res. 2002;53(4):873-6. https://doi.org/10.1016/S0022-3999(02)00309-4
    » https://doi.org/10.1016/S0022-3999(02)00309-4
  • 39
    Reiche EMV, Nunes SOV, Morimoto HK. Stress, depression, the immune system, and cancer. Lancet Oncol. 2004;5(10):617-25. https://doi.org/10.1016/S1470-2045(04)01597-9
    » https://doi.org/10.1016/S1470-2045(04)01597-9
  • 40
    Segerstrom SC, Miller GE. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull. 2004;130(4):601-30. https://doi.org/10.1037/0033-2909.130.4.601
    » https://doi.org/10.1037/0033-2909.130.4.601
  • 41
    Brown L, Young J, Clegg A, Heaven A. Pain in older people with frailty. Rev Clin Gerontol. 2015;25(3):159-71. https://doi.org/10.1017/S0959259815000143
    » https://doi.org/10.1017/S0959259815000143
  • 42
    Darragh AR, Sommerich CM, Lavender SA, Tanner KJ, Vogel K, Campo M. Musculoskeletal discomfort, physical demand and caregiving activities in informal caregivers. J Appl Gerontol. 2015;34(6):734-60. https://doi.org/10.1177/0733464813496464
    » https://doi.org/10.1177/0733464813496464
  • 43
    Farran CJ, Staffileno BA, Gilley DW, McCann JJ, Li Y, Castro CM, et al. A lifestyle physical activity intervention for caregivers of persons with Alzheimer’s disease. Am J Alzheimers Dis Other Demen. 2008;23(2):132-42. https://doi.org/10.1177/1533317507312556
    » https://doi.org/10.1177/1533317507312556
  • 44
    Gomes GAO, Luchesi BM, Gratão ACM, Orlandi FS, Say KG, Inouye K, et al. Prevalence of physical inactivity and associated factors among older caregivers of older adults. J Aging Health. 2019;31(5):793-813. https://doi.org/10.1177/0898264318756422
    » https://doi.org/10.1177/0898264318756422
  • 45
    Woo J, Goggins W, Sham A, Ho SC. Social determinants of frailty. Gerontology. 2005;51(6):402-8. https://doi.org/10.1159/000088705
    » https://doi.org/10.1159/000088705
  • 46
    Gu D, Dupre ME, Sautter J, Zhu H, Liu Y, Yi Z. Frailty and mortality among chinese at advanced ages. J Gerontol B Psychol Sci Soc Sci. 2009;64(2):279-89. https://doi.org/10.1093/geronb/gbn009
    » https://doi.org/10.1093/geronb/gbn009
  • 47
    Samper-Ternent R, Al Snih S, Raji MA, Markides KS, Ottenbacher KJ. Relationship between frailty and cognitive decline in older Mexican Americans. J Am Geriatr Soc. 2008;56(10):1845-52. Available from: https://doi.org/10.1111/j.1532-5415.2008.01947.x
    » https://doi.org/10.1111/j.1532-5415.2008.01947.x
  • 48
    Buchman AS, Boyle PA, Wilson RS, Tang Y, Bennett DA. Frailty is associated with incident Alzheimer’s disease and cognitive decline in the elderly. 2007;69(5):483-9. https://doi.org/10.1097/psy.0b013e318068de1d
    » https://doi.org/10.1097/psy.0b013e318068de1d

  • Funding: This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPQ (Project 160550/2013-0). PADRD/CNPQ/UFSCar financially supported Ingrid Cristina Lopes. The Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (Project 17/26377-4) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Financial Code 001 financially supported Roberta de Oliveira Máximo. The Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (Project 303981/2017-2) and the Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (Project 18/13917-3) financially supported Tiago da Silva Alexandre.

Publication Dates

  • Publication in this collection
    31 Jan 2020
  • Date of issue
    2020

History

  • Received
    08 Apr 2019
  • Accepted
    09 Aug 2019
Faculdade de Saúde Pública da Universidade de São Paulo São Paulo - SP - Brazil
E-mail: revsp@org.usp.br