Abstract
Herein we considered the role of oxidative stress on deficiencies of functional physical performance that could affect a future pre-frailty condition. Using principal component analyses (PCA), we created new variables to better describe the functionality regarding the physical performance of the upper and lower body limbs. Gait speed and the Short Physical Performance Battery (SPPB) score were classified by PCA to describe functional performance of the lower body limbs. Variables describing the general physical status, including weekly consumption of kilocalories and the musculoskeletal index, were classified together with grip strength of the dominant hand as indicators of functional performance of the upper body limbs. An intimate association between the functional physical performance of the upper body limbs and the total antioxidant capacity was observed in older subjects. Low levels of total antioxidant capacity were found in women 76 years or younger with deficiencies in the physical performance of both upper and lower body limbs. Similarly, we observed a close association between the functional physical performance of the lower body limbs and the levels of hemoglobin. In particular, low levels of hemoglobin were mostly found in men older than 76 years of age, showing impaired functional physical performance. In addition, the physical performance of the lower body limbs was shown to be more important than that of the upper body limbs in the statistical association with pre-frailty in the elderly. Therefore, specific low levels of hemoglobin and deficient oxidative defense in the elderly could significantly affect the functional physical performance and future outcomes of pre-frailty.
Similar content being viewed by others
References
Abizanda P, Navarro JL, Romero L, Leon M, Sanchez-Jurado PM, Dominguez L (2007) Upper extremity function, an independent predictor of adverse events in hospitalized elderly. Gerontology 53(5):267–273
Abizanda P, Lopez-Torres J, Romero L et al (2011a) Fragilidad y dependencia en Albacete (estudio FRADEA): razonamiento, diseno y metodología. Rev Esp Geriatr Gerontol 46:81–88
Abizanda P, Sanchez-Jurado PM, Romero L, Paterna G, Martinez-Sanchez E, Atienzar-Nunez P (2011b) Prevalence of frailty in a Spanish elderly population: the frailty and dependence in Albacete study. J Am Geriatr Soc 59:1356–1359
Abizanda P, Romero L, Sanchez-Jurado PM, Atienzar-Nunez P, Esquinas-Requena JL, Garcia-Noguera I (2012) Association between functional assessment instruments and frailty in older adults: the FRADEA study. J Frailty Aging 1:1–7
Abizanda P, Romero L, Sanchez-Jurado PM, Martinez-Reig M, Gomez-Arnedo L, Alfonso SA (2013) Frailty and mortality, disability and mobility loss in a Spanish cohort of older adults: the FRADEA study. Maturitas 74:54–60
Alcala MV, Puime AO, Santos MT, Barral AG, Montalvo JI, Zunzunegui MV (2010) Prevalence of frailty in an elderly Spanish urban population. Relationship with comorbidity and disability. Aten Primaria 42(10):520–527. doi:10.1016/j.aprim.2009.09.024S0212-6567(09)00632-5
Alosco ML, Brickman AM, Spitznagel MB, Griffith EY, Narkhede A, Raz N, Cohen R, Sweet LH, Colbert LH, Josephson R, Hughes J, Rosneck J, Gunstad J (2013) Poorer physical fitness is associated with reduced structural brain integrity in heart failure. J Neurol Sci 328:51–57
Balducci L (2007) Aging, frailty and chemotherapy. Cancer Control 14:7–12
Bandeen-Roche K, Xue QL, Ferrucci L, Walston J, Guralnik JM, Chaves P, Zeger SL, Fried LP (2006) Phenotype of frailty: characterization in the women's health and aging studies. J Gerontol A Biol Sci Med Sci 61:262–266
Baztán JJ, Pérez del Molino J, Alarcón T, San Cristóbal E, Izquierdo G, Manzarbeitia J (1993) Índice de Barthel: instrumento válido para la valoración funcional de pacientes con enfermedad cerebrovascular. Rev Esp Geriatr Gerontol 28:32–40
Bermejo F, Morales JM, Valerga C, Del Ser T, Artolazábal J, Gabriel R (1999) Comparación entre dos versiones españolas abreviadas de evaluación del estado mental en el diagnóstico de demencia. Datos de un estudio en ancianos residentes en la comunidad. Med Clin (Barc) 112:330–334
Ble A, Cherubini A, Volpato S, Bartali B, Walston JD, Windham BG, Bandinelli S, Lauretani F, Guralnik JM, Ferrucci L (2006) Lower plasma vitamin E levels are associated with the frailty syndrome: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 61:278–283
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Caballero B, Veenman L, Gavish M (2013) Role of mitochondrial translocator protein (18 kDa) on mitochondrial-related cell death processes. Recent Pat Endocr Metab Immune Drug Discov 7:86–101
Cabrero-Garcia J, Munoz-Mendoza CL, Cabanero-Martinez MJ, Gonzalez-Llopis L, Ramos-Pichardo JD, Reig-Ferrer A (2012) Short physical performance battery reference values for patients 70 years-old and over in primary health care. Aten Primaria 44:540–548
Campbell AJ, Buchner DM (1997) Unstable disability and the fluctuations of frailty. Age Ageing 26:315–318
Cesari M, Kritchevsky SB, Nicklas BJ, Penninx BW, Holvoet P, Koh-Banerjee P, Cummings SR, Harris TB, Newman AB, Pahor M (2005) Lipoprotein peroxidation and mobility limitation: results from the Health, Aging, and Body Composition Study. Arch Intern Med 165:2148–2154
Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383
Coto-Montes A, Hardeland R (1999) Antioxidative effects of melatonin in Drosophila melanogaster: antagonization of damage induced by the inhibition of catalase. J Pineal Res 27:154–158
Dayhoff-Brannigan M, Ferrucci L, Sun K, Fried LP, Walston J, Varadhan R, Guralnik JM, Semba RD (2008) Oxidative protein damage is associated with elevated serum interleukin-6 levels among older moderately to severely disabled women living in the community. J Gerontol A Biol Sci Med Sci 63:179–183
de Gonzalo-Calvo D, Neitzert K, Fernandez M, Vega-Naredo I, Caballero B, Garcia-Macia M, Suarez FM, Rodriguez-Colunga MJ, Solano JJ, Coto-Montes A (2010) Differential inflammatory responses in aging and disease: TNF-alpha and IL-6 as possible biomarkers. Free Radic Biol Med 49:733–737
de Gonzalo-Calvo D, Neitzert K, Fernandez M, Vega-Naredo I, Caballero B, Garcia-Macia M, Suarez FM, Rodriguez-Colunga MJ, Solano JJ, Coto-Montes A (2011) Defective adaption of erythrocytes during acute hypoxia injury in an elderly population. J Gerontol A Biol Sci Med Sci 66:376–384
de Gonzalo-Calvo D, de Luxan-Delgado B, Martinez-Camblor P, Rodriguez-Gonzalez S, Garcia-Macia M, Suarez FM, Solano JJ, Rodriguez-Colunga MJ, Coto-Montes A (2012a) Chronic inflammation as predictor of 1-year hospitalization and mortality in elderly population. Eur J Clin Invest 42:1037–1046
de Gonzalo-Calvo D, de Luxan-Delgado B, Rodriguez-Gonzalez S, Garcia-Macia M, Suarez FM, Solano JJ, Rodriguez-Colunga MJ, Coto-Montes A (2012b) Interleukin 6, soluble tumor necrosis factor receptor I and red blood cell distribution width as biological markers of functional dependence in an elderly population: a translational approach. Cytokine 58:193–198
de Gonzalo-Calvo D, de Luxan-Delgado B, Rodriguez-Gonzalez S, Garcia-Macia M, Suarez FM, Solano JJ, Rodriguez-Colunga MJ, Coto-Montes A (2012c) Oxidative protein damage is associated with severe functional dependence among the elderly population: a principal component analysis approach. J Gerontol A Biol Sci Med Sci 67:663–670
Fernandez-Bolanos M, Otero A, Zunzunegui MV, Beland F, Alarcon T, de Hoyos C, Castell MV (2008) Sex differences in the prevalence of frailty in a population aged 75 and older in Spain. J Am Geriatr Soc 56:2370–2371
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198
Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56:M146–M156
Fried LP, Ferrucci L, Darer J, Williamson JD, Anderson G (2004) Untangling the concepts of disability, frailty, and comorbidity: implications for improved targeting and care. J Gerontol A Biol Sci Med Sci 59:255–263
Garcia-Garcia FJ, Gutierrez Avila G, Alfaro-Acha A et al (2011) The prevalence of frailty syndrome in an older population from Spain. The Toledo Study for Healthy Aging. J Nutr Health Aging 15:852–856
Gill TM (2010) Assessment of function and disability in longitudinal studies. J Am Geriatr Soc 58(Suppl 2):S308–S312
Graf C (2008) The Lawton instrumental activities of daily living scale. Am J Nurs 108:52–62
Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, Scherr PA, Wallace RB (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85–M94
Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, Waite LM, Seibel MJ, Sambrook PN (2010) Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc 58:2055–2062
Hardy R, Cooper R, Aihie Sayer A, Ben-Shlomo Y, Cooper C, Deary IJ, Demakakos P, Gallacher J, Martin RM, McNeill G, Starr JM, Steptoe A, Syddall H, Kuh D (2013) Body mass index, muscle strength and physical performance in older adults from eight cohort studies: the HALCyon programme. PLoS One 8:e56483
Howard C, Ferrucci L, Sun K, Fried LP, Walston J, Varadhan R, Guralnik JM, Semba RD (2007) Oxidative protein damage is associated with poor grip strength among older women living in the community. J Appl Physiol 103:17–20
Jurschik Gimenez P, Escobar Bravo MA, Nuin Orrio C, Botigue Satorra T (2011) Frailty criteria in the elderly: a pilot study. Aten Primaria 43:190–196
Kao TW, Chou CH, Wang CC, Chou CC, Hu J, Chen WL (2012) Associations between serum total bilirubin levels and functional dependence in the elderly. Intern Med J 42:1199–1207
Kiesswetter E, Pohlhausen S, Uhlig K, Diekmann R, Lesser S, Heseker H, Stehle P, Sieber CC, Volkert D (2013) Malnutrition is related to functional impairment in older adults receiving home care. J Nutr Health Aging 17:345–350
Koufaki P, Kouidi E (2010) Current best evidence recommendations on measurement and interpretation of physical function in patients with chronic kidney disease. Sports Med 40:1055–1074
Kuo HK, Liao KC, Leveille SG, Bean JF, Yen CJ, Chen JH, Yu YH, Tai TY (2007) Relationship of homocysteine levels to quadriceps strength, gait speed, and late-life disability in older adults. J Gerontol A Biol Sci Med Sci 62:434–439
Kuo HK, Al Snih S, Kuo YF, Raji MA (2012) Chronic inflammation, albuminuria, and functional disability in older adults with cardiovascular disease: the National Health and Nutrition Examination Survey, 1999-2008. Atherosclerosis 222:502–508
Landi F, Russo A, Cesari M, Pahor M, Bernabei R, Onder G (2007a) HDL-cholesterol and physical performance: results from the ageing and longevity study in the sirente geographic area (ilSIRENTE Study). Age Ageing 36:514–520
Landi F, Russo A, Liperoti R, Barillaro C, Danese P, Pahor M, Bernabei R, Onder G (2007b) Impact of inappropriate drug use on physical performance among a frail elderly population living in the community. Eur J Clin Pharmacol 63:791–799
Landi F, Cruz-Jentoft AJ, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G (2013) Sarcopenia and mortality risk in frail older persons aged 80 years and older: results from ilSIRENTE study. Age Ageing 42:203–209
Lawton MP, Brody EM (1969) Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 9:179–186
Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478
Li C, Ford ES, Zhao G, Balluz LS, Giles WH, Liu S (2011) Serum alpha-carotene concentrations and risk of death among US Adults: the Third National Health and Nutrition Examination Survey Follow-up Study. Arch Intern Med 171:507–515
Lundby C, Calbet JA, Robach P (2009) The response of human skeletal muscle tissue to hypoxia. Cell Mol Life Sci 66:3615–3623
Mahoney FI, Barthel DW (1965) Functional evaluation: the Barthel Index. Md State Med J 14:61–65
Marini M, Sarchielli E, Brogi L, Lazzeri R, Salerno R, Sgambati E, Monaci M (2008) Role of adapted physical activity to prevent the adverse effects of the sarcopenia. A pilot study. Ital J Anat Embryol 113:217–225
Martí D, Miralles R, Llorach I, García-Palleiro P, Esperanza A, Guillén J et al (2000) Trastornos depresivos en una unidad de convalecencia: experiencia y validación de una versión española de 15 preguntas de la escala de depresión geriátrica de Yesavage. Rev Esp Geriatr Gerontol 35:7–14
Miralles Basseda R, Esperanza Sanjuán A (2007) Instrumentos y escalas de valoración. In: Sociedad Española de Geriatría y Gerontología (ed) Tratado de Geriatría para Residentes. Madrid, pp 771–89.
Patel KV, Guralnik JM (2009) Prognostic implications of anemia in older adults. Haematologica 94:1–2
Peel NM, Kuys SS, Klein K (2013) Gait speed as a measure in geriatric assessment in clinical settings: a systematic review. J Gerontol A Biol Sci Med Sci 68:39–46
Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111:1805–1812
Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148
Ray AL, Semba RD, Walston J, Ferrucci L, Cappola AR, Ricks MO, Xue QL, Fried LP (2006) Low serum selenium and total carotenoids predict mortality among older women living in the community: the women's health and aging studies. J Nutr 136:172–176
Ridker PM, Hennekens CH, Buring JE, Rifai N (2000) C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 342:836–843
Riva E, Tettamanti M, Mosconi P, Apolone G, Gandini F, Nobili A, Tallone MV, Detoma P, Giacomin A, Clerico M, Tempia P, Guala A, Fasolo G, Lucca U (2009) Association of mild anemia with hospitalization and mortality in the elderly: the health and anemia population-based study. Haematologica 94:22–28
Santos-Eggimann B, Cuenoud P, Spagnoli J, Junod J (2009) Prevalence of frailty in middle-aged and older community-dwelling Europeans living in 10 countries. J Gerontol A Biol Sci Med Sci 64:675–681
Sayers SP, Jette AM, Haley SM, Heeren TC, Guralnik JM, Fielding RA (2004) Validation of the late-life function and disability instrument. J Am Geriatr Soc 52:1554–1559
Semba RD, Ferrucci L, Sun K, Walston J, Varadhan R, Guralnik JM, Fried LP (2007) Oxidative stress and severe walking disability among older women. Am J Med 120:1084–1089
Shardell MD, Alley DE, Hicks GE, El-Kamary SS, Miller RR, Semba RD, Ferrucci L (2011) Low-serum carotenoid concentrations and carotenoid interactions predict mortality in US adults: the Third National Health and Nutrition Examination Survey. Nutr Res 31:178–189
Shin H, Liu PY, Panton LB, Ilich JZ (2013a) Physical performance in relation to body composition and bone mineral density in healthy, overweight, and obese postmenopausal women. J Geriatr Phys Ther. doi:10.1519/JPT.0b013e31828af203
Shin SY, Julian L, Katz P (2013b) The relationship between cognitive function and physical function in rheumatoid arthritis. J Rheumatol 40:236–243
Topinkova E (2008) Aging, disability and frailty. Ann Nutr Metab 52(Suppl 1):6–11
Torres Moreno B, Núñez González E, Pérez Hernández Dde G, Simón Turriate JP, Alastuey Giménez C, Díaz Melián J et al (2009) Barthel and Charlson indexes for the prognosis of mortality and institutionalization in hospitalized geriatric patients. Rev Esp Geriatr Gerontol 44:209–212
Vogiatzis I, Zakynthinos G, Andrianopoulos V (2012) Mechanisms of physical activity limitation in chronic lung diseases. Pulm Med. doi:10.1155/2012/634761
Wells M, Avers D, Brooks G (2012) Resilience, physical performance measures, and self-perceived physical and mental health in older Catholic nuns. J Geriatr Phys Ther 35:126–131
Yesavage JABT, Rose TL, Lum O (1983) Development and validation of a geriatric depression scale: a preliminary report. J Psychiatr Res 17:37–49
Ylitalo KR, Herman WH, Harlow SD (2013) Performance-based physical functioning and peripheral neuropathy in a population-based cohort of women at midlife. Am J Epidemiol 177:810–817
Acknowledgments
The authors thank Dr. Mamen Oliván for her excellent statistical advice. Beatriz Caballero, Ana Coto-Montes, Pedro Abizanda, and Juan José Solano are participants of the National Net RETICEF for Aging studies [Red Temática de Investigación Cooperativa en Envejecimiento y Fragilidad (RETICEF)]. Likewise, Ana Coto is a member of INEUROPA.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Caballero, B., Rubio-González, A., Potes, Y. et al. Associations of the antioxidant capacity and hemoglobin levels with functional physical performance of the upper and lower body limbs. AGE 36, 851–867 (2014). https://doi.org/10.1007/s11357-013-9607-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11357-013-9607-y