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Falls and their association with physical tests, functional capacity, clinical and demographic factors in patients with rheumatoid arthritis

ABSTRACT

Objective:

To evaluate the occurrence of falls reported by rheumatoid arthritis patients and its relation to disease activity, functional capacity and physical fitness.

Materials and methods:

A cross-sectional study constituted by a sample of 97 rheumatoid arthritis patients from the city of Marília (SP) from 2012 to 2013, were assessed for disease activity. Instruments validated for Brazilian population in order to evaluate physical and functional capacity were used. Data analysis was carried out with descriptive statistics, Spearman correlation and Chi-squared test, considering p < 0.05.

Results:

88.7% were female subjects with a mean age of 56 (±11.7) years. The median duration of rheumatoid arthritis was 10 years (P25 = 6 and P75 = 17) and the mean of disease activity was 3.6 (±1.3), what was considered a moderate activity. In the last 12 months 37.1% of patients experienced at least one fall, with a total of 52 episodes, and fear of falling was reported by 74.2% of them, but this was not associated to the occurrence of a fall (χ 2 = 1.19, p = 0.27). Gender, number of medications, age, disease activity, duration of rheumatoid arthritis, functional capacity, and physical tests showed no associations with history of falls in the past year.

Conclusion:

It was observed that the occurrence of falls and the fear of falling are quite common in this population. The occurrence of falls in this sample of rheumatoid arthritis patients bears no relation to disease activity, functional capacity, or physical fitness tests.

Keywords:
Rheumatoid arthritis; Accidental falls; Postural balance; Aptitude tests

RESUMO

Objetivo:

Avaliar a ocorrência de quedas reportadas por pacientes com artrite reumatoide (AR) e sua associação com a atividade da doença, capacidade funcional e aptidão física.

Material e métodos:

Estudo transversal com uma amostra de 97 pacientes com AR em Marília (SP), entre 2012 e 2013. Foram usados instrumentos validados na população brasileira para avaliar capacidade física e funcional. Análise dos dados com estatística descritiva, correlações de Spearman e qui-quadrado, considerado p < 0,05.

Resultados:

Dos pacientes, 88% eram mulheres, média de 56, anos (± 11,7), duração mediana da AR de 10 anos (P25 = 6 e P75 = 17) e média da atividade da doença 3,6 (± 1,3). Nos últimos 12 meses, 37,1% tiveram pelo menos uma queda (total 52 episódios), 74,2% relataram medo de cair, porém sem associação com a ocorrência de quedas (χ2 = 1,19, p = 0,27). Sexo, quantidade de medicamentos, idade, atividade da doença, duração da AR, capacidade funcional e testes físicos não estão associados com história de queda no último ano.

Conclusões:

Observou-se que a ocorrência de quedas e o medo de cair é frequente nessa população. A ocorrência de quedas nessa amostra de pacientes com AR não está relacionada à atividade da doença, à capacidade funcional e a testes de aptidão física.

Palavras-chave:
Artrite reumatoide; Acidentes por quedas; Equilíbrio postural; Testes de aptidão

Introduction

Rheumatoid arthritis (RA) is a systemic inflammatory, autoimmune, chronic, progressive disease of unknown etiology, which can lead to bone destruction and to deformity.11 Mota LMH, Cruz BA, Brenol CV, Pereira IA, Fronza LSR, Bertolo MB, et al. Consenso da Sociedade Brasileira de Reumatologia 2011 para o diagnóstico e avaliação inicial da artrite reumatoide. Rev Bras Reumatol. 2011;51:207-19.

2 Mota LMH, Cruz BA, Brenol CV, Pereira IA, Rezende-Fronza LS, Bertolo MB, et al. Consenso 2012 da Sociedade Brasileira de Reumatologia para o tratamento da artrite reumatoide. Rev Bras Reumatol. 2012;52:152-74.
-33 Wasserman AM. Diagnosis and management of rheumatoid arthritis. Am Fam Physician. 2011;84:1245-52. Patients suffering from RA may have muscle weakness, reduced mobility, postural instability, proprioceptive, postural balance, and gait changes, which are known risk factors for falls.44 Furuya T, Yamagiwa K, Ikai T, Inoue E, Taniguchi A, Momohara S, et al. Associated factors for falls and fear of falling in Japanese patients with rheumatoid arthritis. Clin Rheumatol. 2009;28:1325-30.

5 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.

6 Häkkinen A, Kautiainen H, Hannonen P, Ylinen J, Mäkinen H, Sokka T. Muscle strength, pain, and disease activity explain individual subdimensions of the Health Assessment Questionnaire disability index, especially in women with rheumatoid arthritis. Ann Rheum Dis. 2006;65:30-4.

7 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.

8 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80.

9 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.

10 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.

11 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.

12 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.

13 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.
-1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.

The occurrence of falls has been reported as something between 14.3%77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25. and 54%55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71. in patients with RA. This great range can be explained by the lack of criteria and of standards in the studies, in addition to a few studies involving falls and RA. Some studies in patients with RA have shown an association of falls with higher disease activity, reduced functional capacity, and with physical fitness and balance tests.44 Furuya T, Yamagiwa K, Ikai T, Inoue E, Taniguchi A, Momohara S, et al. Associated factors for falls and fear of falling in Japanese patients with rheumatoid arthritis. Clin Rheumatol. 2009;28:1325-30.,55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.

8 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80.
-99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.,1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.

15 Yamagiwa K, Iijima S, Furuya T, Ikai T, Inoue E, Taniguchi A, et al. Incidence of falls and fear of falling in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2011;21:51-6.

16 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7.
-1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7.

The impact of the falls reaches physical, psychosocial, economic and family aspects. The lesions range from small abrasions to fractures, particularly in osteoporotic bone (a common comorbidity in patients with RA).55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.,99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.,1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1515 Yamagiwa K, Iijima S, Furuya T, Ikai T, Inoue E, Taniguchi A, et al. Incidence of falls and fear of falling in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2011;21:51-6.

16 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7.
-1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. By being a frequent event, the characterization and identification of patients are fundamental, in order to establish specific programs and interventions for its prevention in this population.

In the Brazilian population, we found only one study of Marques et al.1818 Marques WV, Cruz VA, Rego J, Silva NA. Influência da capacidade funcional no risco de quedas em adultos com artrite reumatoide. Rev Bras Reumatol. 2014;54:404-8. on falls in patients with RA, which shows the lack of national studies in order to characterize these patients. In view of this, the aim of this study was to evaluate the occurrence of falls in patients with RA and their relationship to age, disease duration and activity, physical assessment tests, and functional capacity.

Materials and methods

The study was approved by the Human Research Ethics Committee of the Faculdade de Medicina de Marília (FAMEMA) under the Protocol 672/12. All subjects received oral and written explanations and participated in the study after signing the Informed Consent Form.

A cross-section study was performed, with our convenience sample comprising 97 patients of both genders diagnosed with RA, followed in FAMEMA Rheumatology Outpatient Clinic. To calculate the sample size, the following formula1919 Charan J, Biswas T. How to calculate sample size for different study designs in medical research. Indian J Psychol Med. 2013;35:121-6. was used:

Z 1 α / 2 2 P 1 P d 2 , where

  • - Z1−α/2=1.96, for α = 0.05 (type I error);

  • - P = the expected proportion of falls in the RA population, considering 35% (an intermediate value between the extremes of 15% and 55% found in the literature);

  • - d = a precision of 10%.

The sample size obtained by this formula would be 87 patients; we added 10% to compensate for losses and refusals, totaling 96 patients, but there were no refusals as to the participation in this study.

The inclusion criteria were: (a) a diagnosis of RA according to the American College of Rheumatology (ACR) classification criteria of 1987 or to the classification criteria for RA of 2010 from ACR/EULAR (European League Against Rheumatism)11 Mota LMH, Cruz BA, Brenol CV, Pereira IA, Fronza LSR, Bertolo MB, et al. Consenso da Sociedade Brasileira de Reumatologia 2011 para o diagnóstico e avaliação inicial da artrite reumatoide. Rev Bras Reumatol. 2011;51:207-19.,2020 Fuller R. Critério de classificação da artrite reumatoide ACR-Eular 2010 [Editorial]. Rev Bras Reumatol. 2010;50:481-6.,2121 Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62:2569-81.; (b) age over 18; (c) physical ability to perform the tests. The exclusion criteria were: (a) a deficit of comprehension limiting the interview; (b) severe visual or hearing impairment.

Patients were evaluated by a rheumatologist (M.R.A.) to confirm the diagnosis of RA, and at that time measurements of disease activity were carried out. Patients underwent blood sampling performed by a nurse (I.R.), and then were referred to take medical history and a specific interview about falls, as well as to the application of physical tests by a physiotherapist (M.A.L.).

For identification of the falls in the last 12 months, a questionnaire prepared by the researchers was used. The definition adopted for a fall was “an unintentional displacement of the body to a level below the starting position, with the inability of correction in a timely manner, determined by multifactorial circumstances and affecting stability”.2222 Sociedade Brasileira de Geriatria e Gerontologia. Quedas em idosos: prevenção. In: Associação Médica Brasileira, Conselho Federal de Medicina. Projeto Diretrizes; 2008. p. 1–15. The questions concerned the occurrence and description of the falls, being considered the last 12 months (quantity, location, reason, the time of occurrence, the activity involved, consequences, and the presence of fear of falling).

To assess disease activity, the Disease Activity Score (DAS-28), which counts joints with pain and swelling in 28 joints, the overall self-assessment of health obtained with the use of a visual analog scale (VAS) from 0 to 100, and the erythrocyte sedimentation rate, given in millimeters per hour (mm/h) through a hemosedimentation technique performed at the Blood Center of FAMEMA.2323 Pinheiro G. Instrumentos de medida da atividade da artrite reumatoide: por que e como empregá-los. Rev Bras Reumatol. 2007;47:362-5.

24 Mello FM. Análise da correlação dos escores de atividade de doença na artrite reumatóide. [dissertation] Florianópolis, SC: Universidade Federal de Santa Catarina; 2008, 66 pp.

25 Prevoo MLL, Van’t Hof MA, Kuper HH, Van Leeuwen MA, Van de Putte LBA, Van Riel PLCM. Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum. 1995;38:44-8.
-2626 Aletaha D, Smolen J. The Simplified Disease Activity Index (SDAI) and the Clinical Disease Activity Index (CDAI): a review of their usefulness and validity in rheumatoid arthritis. Clin Exp Rheumatol. 2005;23(Suppl. 39):S100-8.

The Health Assessment Questionnaire (HAQ),2727 Corbacho MI, Dapueto JJ. Avaliação da capacidade funcional e da qualidade de vida de pacientes com artrite reumatoide. Rev Bras Reumatol. 2010;50:31-43.,2828 Bruce B, Fries JF. The Health Assessment Questionnaire (HAQ). Clin Exp Rheumatol. 2005;23(Suppl. 39):S14-8. validated in Brazil by Ferraz et al.,2929 Ferraz MB, Oliveira LM, Araujo PM, Atra E, Tugwell P. Crosscultural reliability of the physical ability dimension of the health assessment questionnaire. J Rheumatol. 1990;17:813-7. was used to evaluate the functional capacity and the following tests to measure physical capacity: (a) Berg Balance Scale (Berg), proposed by Berg et al. in 1989 and validated in Brazil by Miyamoto,3030 Miyamoto ST, Lombardi Junior I, Berg KO, Ramos LR, Natour J. Brazilian version of the Berg balance scale. Braz J Med Biol Res. 2004;37:1411-21. which evaluates the balance of the patient in 14 representative situations of his/her daily routine;3030 Miyamoto ST, Lombardi Junior I, Berg KO, Ramos LR, Natour J. Brazilian version of the Berg balance scale. Braz J Med Biol Res. 2004;37:1411-21.

31 Figueiredo KMOB, Lima KC, Guerra RO. Instrumentos de avaliação do equilíbrio corporal em idosos. Rev Bras Cineantropom Desempenho Humano. 2007;9:408-13.
-3232 Resende S, Rassi C, Viana F. Efeitos da hidroterapia na recuperação do equilíbrio e prevenção de quedas em idosas. Rev Bras Fisioter. 2008;12:57-63. (b) the “Timed Up and Go” (TUG) test, proposed by Podsiadlo and Richardson in 1991 to evaluate balance in the sitting position, the transfer from a sitting position to a standing position, stability in ambulation, and changes in the gait course without the use of compensatory strategies;3131 Figueiredo KMOB, Lima KC, Guerra RO. Instrumentos de avaliação do equilíbrio corporal em idosos. Rev Bras Cineantropom Desempenho Humano. 2007;9:408-13.,3333 Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther. 2000;80:896-903.,3434 Guimarães LHCT, Galdino DCA, Martins FLM, Vitorino DFM, Pereira KL, Carvalho EM. Comparação da propensão de quedas entre idosos que praticam atividade física e idosos sedentários. Neurociências. 2004;12:68-72. (c) 6-min Walk Test (6MWT) developed by Balke in 1963 and currently used to evaluate the functional capacity and exercise tolerance;3535 American Thoracic Society. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166:111-7.

36 American College of Rheumatology. Six minute walk test (6MWT); 2011. Available in: http://ww2.rheumatology.org/practice/clinical/clinicianresearchers/outcomes-instrumentation/6MWT.asp [accessed 02.05.14].
http://ww2.rheumatology.org/practice/cli...
-3737 Rondelli RR, Oliveira AN, Dal Corso S, Malaguti C. Uma atualização e proposta de padronização do teste de caminhada de seis minutos. Fisioter Mov. 2009;22:249-59. (d) the Guralnik Test Battery or Short Physical Performance Battery (SPPB) developed by Jack M. Guralnik and validated in Brazil by Nakano,3838 Nakano MM. Versão brasileira da Short Physical Performance Battery (SPPB): adaptação cultural e estudo da confiabilidade. [dissertation] Campinas, SP: Universidade Estadual de Campinas; 2007, 163 pp. used to evaluate static balance, walking ability, and the ability to get up from a chair.3939 Alfieri FM, Riberto M, Gatz LS, Ribeiro CPC, Battistella LR. Uso de testes clínicos para verificação do controle postural em idosos saudáveis submetidos a programas de exercícios físicos. Acta Fisiatr. 2010;17:153-8.,4040 Uhler CR. Análise do controle postural de idosos jovens e idosos muito idosos com história de quedas. [dissertation] São Paulo: Universidade Cidade de São Paulo; 2008, 86 pp.

Descriptive statistics were performed, with the presentation of central tendency and dispersion measures, according to the nature of the distribution of variables (mean, median, standard deviation, and percentiles) for the characteristics of the sample, description of the falls, and test score values. To check the normality of the data, the Kolmogorov-Smirnov test was applied. As the data were nonparametric, a correlation with the Spearman test for the number of falls and physical, functional and disease activity was carried out. The following values were adopted to interpret the strength of correlations: 0.0-0.3 insignificant; 0.3-0.5 low; 0.5-0.7 moderate; 0.7-0.9 high, and 0.9-1.0 very high.4141 Mukaka MM. Statistics Corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 2012;24:69-71. As to the association between groups (fallers and non-fallers) and the variables pharmacologic agents, fear of falling, and gender, the Chi-squared test was used. A significance level of p < 0.05 was adopted and all analyses were performed using the SPSS v. 21 program.

Results

Ninety-seven patients participated in this study; they were mostly women, married, Caucasian subjects showing overweight, according to body mass index (BMI) (Table 1). All patients are in use of at least one pharmacological agent for RA, and 27 (27.8%) are using a disease-modifying drug.

Table 1
Sample characteristics.

Disease duration ranged from 2 to 40 years with a median of 10 years (P25 = 6 and P75 = 17), characterizing an established disease in the sample studied. The mean for DAS28 was 3.6 (±1.3), a value related to a disease in moderate activity (>3.2 and ≤5.1).2626 Aletaha D, Smolen J. The Simplified Disease Activity Index (SDAI) and the Clinical Disease Activity Index (CDAI): a review of their usefulness and validity in rheumatoid arthritis. Clin Exp Rheumatol. 2005;23(Suppl. 39):S100-8. The median of HAQ was 0.6 (1st and 3rd quartiles, 0.1-1.5), which indicates a mild to moderate disability.2828 Bruce B, Fries JF. The Health Assessment Questionnaire (HAQ). Clin Exp Rheumatol. 2005;23(Suppl. 39):S14-8.

In the 12 months preceding the interview, about a third of patients experienced one or more falls, totaling 52 episodes. No patient had 4 or more falls in the past year, and the occurrence of only one episode was the most frequent value during this period. Falls occurred more frequently during the day, at home, as the subject was walking, by stumbling or slipping. In most episodes, the patient did not visit the doctor or the emergency room but suffered some kind of injury/abrasion, or severe pain (Table 2).

Table 2
Characterization of the reported falls in the last 12 months.

Fear of falling was reported by 74.2% of patients, both among those who suffered falling episodes in the previous year and those who did not suffer any fall, but with no significant association (p = 0.274) with the falls reported in the last 12 months (Table 3). Also, there was no significant association between fear of falling and age (p = 0.289), disease duration (p = 0.071) and disease activity (p = 0.082). Patients with a fear of falling had greater functional impairment measured by the HAQ (p = 0.004) and a poorer performance on 6MWT (p = 0.002), TUG (p = 0.007) and SPPB (p = 0.020) tests when compared to those who stated that were not afraid of falling.

Table 3
Results of physical tests TUG, Berg, 6MWT and SPPB.

No significant association was found between the occurrence of falls in the last 12 months and age (ρ = 0.070, p = 0.498), disease activity (ρ = 0.050, p = 0629), duration of RA (ρ = −0015, p = 0.888) and functional capacity (ρ = 0.167, p = 0.102). Also, the amount of drugs taken daily and patient gender had no association with the presence of falls in the last year (Table 4).

Table 4
Associations of reported falls with the number of medications, the presence of fear of falling, and gender.

The worst performance in physical tests was associated with older age, longer disease duration, and increased disease activity. Functional capacity was shown to be moderately associated with performance in all physical tests, indicating that the limitation of functional activities reflects a poorer performance on these tests. There was no association between the numbers of falls with any of the physical performance tests (Table 5).

Table 5
Associations between age, duration of RA, DAS28, HAQ and number of falls versus physical performance tests.

Discussion

The percentage of people who have suffered falls in a period of 12 months ranged from 14.3%77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25. to 54%55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71. (18.8%,1616 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7. 26.9%,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. 30.2%,1818 Marques WV, Cruz VA, Rego J, Silva NA. Influência da capacidade funcional no risco de quedas em adultos com artrite reumatoide. Rev Bras Reumatol. 2014;54:404-8. 30.9%,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8. 33%,1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4. 35.2%,88 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80. 36.4%,1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.,1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8. 37.1%,4242 Schober HC, Maass K, Maass C, Reisinger EC, Schröder G, Kneitz C. Value of fall-risk tests for patients with rheumatoid arthritis. J Rheumatol. 2011;70:609-14. 42%,1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6. and 50%99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.). In this study, about 37% of the participants experienced at least one fall in the last 12 months, similar to the 30.2% found in another study on a Brazilian population.1818 Marques WV, Cruz VA, Rego J, Silva NA. Influência da capacidade funcional no risco de quedas em adultos com artrite reumatoide. Rev Bras Reumatol. 2014;54:404-8. This annual incidence is considered high when compared to the estimated incidence for elders over 65 (28-35%), and over 75 (32-42%) years.2222 Sociedade Brasileira de Geriatria e Gerontologia. Quedas em idosos: prevenção. In: Associação Médica Brasileira, Conselho Federal de Medicina. Projeto Diretrizes; 2008. p. 1–15.

As was reported by Stanmore et al.,1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44. there was a predominance of falls at home, probably because these subjects spend most of their time indoors, due to a more limited lifestyle, where the set of physical limitations, functional dependence, and fear force the patient to refrain from work activities, leisure, and social participation. Another explanation is their great familiarity with the home environment, where those existing extrinsic risk factors for the occurrence of falls are underestimated.

In this study, a minority (32.7%) sought some kind of specialized care after the fall; this finding is similar to that observed in the studies by Fessel and Nevitt1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8. (31%) and Stanmore et al.1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44. (26%). This is perhaps explained by the low severity of these injuries, that indeed were minor lesions, abrasions, and pain, as occurred in the reviewed studies.88 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80.,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.,1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.

RA patients are at increased risk of osteoporotic fracture, which results from the interaction between an increased bone fragility (low bone density) and trauma, and the fall is an important causative factor in adults of all ages with RA. We observed a higher incidence (9.6%) of fractures from falls in our patients, when compared to other studies that range from 1.1% to 5%, as well as in the elderly, whose fractures occur in about 5% of falls.99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.,1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1616 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7.,2222 Sociedade Brasileira de Geriatria e Gerontologia. Quedas em idosos: prevenção. In: Associação Médica Brasileira, Conselho Federal de Medicina. Projeto Diretrizes; 2008. p. 1–15.

The fear of falling causes patients to change their behavior, including a decrease in recreational activities.88 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80.,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8. This fear can lead to a cycle in which the patient physically committed by RA goes on to avoid risky situations and becomes less active, which worsens his/her physical capacity and increases the chances of a future fall. No national data was found to quantify the fear of falling among a population with RA; however, we consider the percentage found in our study as being high (74.2%), when compared with the percentage of other countries (20.6%,44 Furuya T, Yamagiwa K, Ikai T, Inoue E, Taniguchi A, Momohara S, et al. Associated factors for falls and fear of falling in Japanese patients with rheumatoid arthritis. Clin Rheumatol. 2009;28:1325-30. 46.2%,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. 50.5%,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8. 59.8%,88 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80. and 66.7%77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.).

According to Duyur Çakat et al.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25. patients with fear of falling suffer from the disease for longer periods of time and produce worse scores on the Beck Depression Scale, besides a poorer physical performance. It was found that patients with fear of falling showed worse physical/functional capacity, perhaps because these subjects did not perform the tests at their maximum capacity, which hampers to some extent the results of physical tests.

Regarding the use of pharmacological drugs, no significant difference between the groups of fallers and non-fallers was found, as in the study of Smulders et al.1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6. In the literature reviewed, it was observed that a greater risk of falling is related to the greater amount of medication that the patient takes (OR = 1.442828 Bruce B, Fries JF. The Health Assessment Questionnaire (HAQ). Clin Exp Rheumatol. 2005;23(Suppl. 39):S14-8.), and to the use of antidepressants (OR = 2.092828 Bruce B, Fries JF. The Health Assessment Questionnaire (HAQ). Clin Exp Rheumatol. 2005;23(Suppl. 39):S14-8.) and steroids.1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.

As in the literature on this subject, although age is a major risk factor, being commonly associated with the presence of falls, this factor is not associated with the occurrence of falls in patients with RA.44 Furuya T, Yamagiwa K, Ikai T, Inoue E, Taniguchi A, Momohara S, et al. Associated factors for falls and fear of falling in Japanese patients with rheumatoid arthritis. Clin Rheumatol. 2009;28:1325-30.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.,99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.

10 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.

11 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.

12 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.

13 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.

14 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.
-1515 Yamagiwa K, Iijima S, Furuya T, Ikai T, Inoue E, Taniguchi A, et al. Incidence of falls and fear of falling in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2011;21:51-6.,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. A possible explanation for this finding is that people with RA (not controlled, or already with their sequels) have risk factors similar to the physiological characteristics of aging, that predispose these subjects to the falls. Thus, these patients show a premature aging, at least from the standpoint of their locomotor system. Among all studies, only that of Bugdayci et al.1616 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7. found an association between age and the occurrence of falls; on the other hand, Schober et al.4242 Schober HC, Maass K, Maass C, Reisinger EC, Schröder G, Kneitz C. Value of fall-risk tests for patients with rheumatoid arthritis. J Rheumatol. 2011;70:609-14. found that older age was associated with an increased risk of falls in patients with RA, and some studies point to the need to further investigate the relationship between age and the occurrence of falls in this population.1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7.

Regarding the disease duration, the mean of the examined studies was 11-17 years,55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.

8 Jamison M, Neuberger GB, Miller PA. Correlates of falls and fear of falling among adults with rheumatoid arthritis. Arthritis Rheum. 2003;49:673-80.

9 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.

10 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.
-1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.,1515 Yamagiwa K, Iijima S, Furuya T, Ikai T, Inoue E, Taniguchi A, et al. Incidence of falls and fear of falling in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2011;21:51-6.,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. and our median was 10 years. No association was found between disease duration and occurrence of falls in this study (ρ = −0015, p = 0.888) as well as in several other studies.55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.,99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.,1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7.

The mean score of disease activity (assessed by DAS28) found in our study, 3.6 (±1.3), shows a moderate activity, but no association with the occurrence of falls (ρ = 0.050, p = 0629). As in Stanmore et al.1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.,1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8. and in Duyur Çakat et al.77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25. studies, in the group of fallers the score of disease activity is higher versus non-fallers (3.7 and 3.5, respectively). On the other hand, Hayashibara et al.99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33. found no difference in DAS28 between fallers and non-fallers.

As Böhler et al.1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. found, we observed an association between disease activity and performance in physical tests, indicating that patients with higher disease activity may have more difficulty in performing physical tests, thus getting worse results.

In its vast majority, the studied sample shows a mild-to-moderate impairment by HAQ, and there is a moderate association between poor functional score and worst performance in physical tests; but an association with the occurrence of falls could not be demonstrated. According to Marques et al.,1818 Marques WV, Cruz VA, Rego J, Silva NA. Influência da capacidade funcional no risco de quedas em adultos com artrite reumatoide. Rev Bras Reumatol. 2014;54:404-8. functional disability, measured by HAQ, is the main risk factor for falls in Brazilian patients with RA. The literature shows that those patients with higher HAQ scores are at greater risk of falling, suffered a greater number of falls in the last year, have more fear of falling (as was found in our sample), and had a poorer performance on physical tests.44 Furuya T, Yamagiwa K, Ikai T, Inoue E, Taniguchi A, Momohara S, et al. Associated factors for falls and fear of falling in Japanese patients with rheumatoid arthritis. Clin Rheumatol. 2009;28:1325-30.,55 Kaz Kaz H, Johnson D, Kerry S, Chinappen U, Tweed K, Patel S. Fall-related risk factors and osteoporosis in women with rheumatoid arthritis. Rheumatology (Oxford). 2004;43:1267-71.,77 Duyur Çakat B, Nacir B, Erdem HR, Karagoz A, Saraçoglu M. Fear of falling, fall risk, and disability in patients with rheumatoid arthritis. Turk J Rheumatol. 2011;26:217-25.,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.,1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.,1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8.,1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7.

It was observed in the literature a lack of standardization in the choice of physical tests to evaluate the risk of falls. In this study, validated instruments widely used in Brazil were chosen. There was no association between a previous occurrence of falls and the performance on tests applied to our sample of patients with RA. It can be difficult to identify an association between falls and worse performance in tests of balance and physical performance, because the same factors that lead to functional impairment, which is a potential predisponent to the occurrence of falls, also limit the patient's activities and can reduce his/her exposure to risk situations.

This study has some limitations. Information on the occurrence of falls obtained by self-report tend to be underestimated (recall bias) and many studies suggest that prospective studies are carried out, where the falls are controlled by a calendar of falls and/or by phone calls, and over a longer period of time than one year, as this period may not be sufficient to distinguish between fallers versus non-fallers.99 Hayashibara M, Hagino H, Katagiri H, Okano T, Okada J, Teshima R. Incidence and risk factors of falling in ambulatory patients with rheumatoid arthritis: a prospective 1-year study. Osteoporos Int. 2010;21:1825-33.,1010 Fessel KD, Nevitt MC. Correlates of fear of falling and activity limitation among persons with rheumatoid arthritis. Arthritis Care Res. 1997;10:222-8.,1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.,1313 Smulders E, Schreven C, Weerdesteyn V, Van den Hoogen FH, Laan R, Van Lankveld W. Fall incidence and fall risk factors in people with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1795-6.,1515 Yamagiwa K, Iijima S, Furuya T, Ikai T, Inoue E, Taniguchi A, et al. Incidence of falls and fear of falling in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2011;21:51-6.

16 Bugdayci D, Paker N, Rezvani A, Kesiktas N, Yilmaz O, Sahin M, et al. Frequency and predictors for falls in the ambulatory patients with rheumatoid arthritis: a longitudinal prospective study. Rheumatol Int. 2013;33:2523-7.
-1717 Böhler C, Radner H, Ernst M, Binder A, Stamm T, Aletaha D, et al. Rheumatoid arthritis and falls: the influence of disease activity. Rheumatology (Oxford). 2012;51:2051-7. Some studies1111 Armstrong C, Swarbrick CM, Pye SR, O’Neill TW. Occurrence and risk factors for falls in rheumatoid arthritis. Ann Rheum Dis. 2005;64:1602-4.,1212 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Fall incidence and outcomes of falls in a prospective study of adults with rheumatoid arthritis. Arthritis Care Res. 2013;65:737-44.,1414 Stanmore EK, Oldham J, Skelton DA, O’Neill T, Pilling M, Campbell AJ, et al. Risk factors for falls in adults with rheumatoid arthritis: a prospective study. Arthritis Care Res. 2013;65:1251-8. show that samples from a reference outpatient clinic may not adequately represent the population with RA in general: it is expected that these samples present a greater number of severe cases of RA; but even the most severe cases can be in a good condition, thanks to their access to a good treatment. The fact that we did not consider the level of physical activity of our patients, and the wide age range of the sample, are also limitations to this study.

The occurrence of falls is a complex multifactorial event whose prediction can be difficult, even with the combined use of measures of activity of the disease, functionality, and physical tests. Physical tests were not associated with the occurrence of previous falls, and this suggests that prospective studies are needed in order to assess the ability of these and other instruments as predictive of the occurrence of falls in people with RA.

Conclusions

Our results confirm an increased prevalence of falls in patients with RA; but with no association with age, gender, disease duration and activity, functional capacity, the number of drugs used, and physical fitness tests. Physical tests have shown an association with age, disease duration and activity, and, especially, functional capacity.

  • Funding
    A Master's degree fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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Publication Dates

  • Publication in this collection
    May-Jun 2017

History

  • Received
    25 Aug 2015
  • Accepted
    3 Aug 2016
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