Relationship of Objectively-Measured Habitual Physical Activity to Chronic Inflammation and Fatigue in Middle-Aged and Older Adults.
Journal: 2017/July - The journals of gerontology. Series A, Biological sciences and medical sciences
ISSN: 1758-535X
Abstract:
Habitual (non-exercise) physical activity (PA) declines with age, and aging-related increases in inflammation and fatigue may be important contributors to variability in PA.
This study examined the association of objectively-measured PA (accelerometry over 7 days) with inflammation (plasma interleukin-6 and C-reactive protein) and with self-reported fatigue (SF-36 Vitality) at baseline and 18 months after a diet-induced weight loss, exercise, or diet-induced weight loss plus exercise intervention in 167 overweight/obese, middle-aged, and older adults.
At baseline, individuals with higher plasma interleukin-6, as well as those who reported feeling less energetic (more fatigued), took less steps per day and had lower PA energy expenditure and minutes of light and moderate-vigorous PA (p < .05 for all). At the 18-month follow-up, inflammation was lower in both weight loss groups, fatigue was reduced in all three groups with larger decreases in the combined group, and mean levels of habitual PA were not changed in any group. In longitudinal analyses with all groups combined, we found that participants reporting larger increases in vitality (eg, declines in fatigue) had greater increases in PA (p < .05 for all). Also, changes in steps/d and physical activity energy expenditure were indirectly associated with changes in interleukin-6 (β [SEM] for steps/d = -565 [253]; β [SEM] for physical activity energy expenditure = -22.4 [10.17]; p < .05).
Levels of habitual PA are lower in middle-aged and older adults with higher levels of chronic inflammation and greater self-reported fatigue. In addition, participants who experienced greater declines in inflammation during the interventions had greater declines in fatigue and larger increases in PA.
Relations:
Content
Citations
(3)
References
(42)
Conditions
(4)
Chemicals
(2)
Organisms
(1)
Processes
(1)
Affiliates
(3)
Similar articles
Articles by the same authors
Discussion board
J Gerontol A Biol Sci Med Sci 71(11): 1437-1443

Relationship of Objectively-Measured Habitual Physical Activity to Chronic Inflammation and Fatigue in Middle-Aged and Older Adults

Background:

Habitual (non-exercise) physical activity (PA) declines with age, and aging-related increases in inflammation and fatigue may be important contributors to variability in PA.

Methods:

This study examined the association of objectively-measured PA (accelerometry over 7 days) with inflammation (plasma interleukin-6 and C-reactive protein) and with self-reported fatigue (SF-36 Vitality) at baseline and 18 months after a diet-induced weight loss, exercise, or diet-induced weight loss plus exercise intervention in 167 overweight/obese, middle-aged, and older adults.

Results:

At baseline, individuals with higher plasma interleukin-6, as well as those who reported feeling less energetic (more fatigued), took less steps per day and had lower PA energy expenditure and minutes of light and moderate–vigorous PA (p < .05 for all). At the 18-month follow-up, inflammation was lower in both weight loss groups, fatigue was reduced in all three groups with larger decreases in the combined group, and mean levels of habitual PA were not changed in any group. In longitudinal analyses with all groups combined, we found that participants reporting larger increases in vitality (eg, declines in fatigue) had greater increases in PA (p < .05 for all). Also, changes in steps/d and physical activity energy expenditure were indirectly associated with changes in interleukin-6 (β [SEM] for steps/d = −565 [253]; β [SEM] for physical activity energy expenditure = −22.4 [10.17]; p < .05).

Conclusions:

Levels of habitual PA are lower in middle-aged and older adults with higher levels of chronic inflammation and greater self-reported fatigue. In addition, participants who experienced greater declines in inflammation during the interventions had greater declines in fatigue and larger increases in PA.

Funding

This work was supported by an independent research grant from the National Institutes of Health (R01 AR052528), as well as the Wake Forest University Claude D. Pepper Center Older Americas Independence Center (P30-AG21332) and Wake Forest University General Clinical Research Center (M01-RR07122); and General Nutrition Centers, Inc.

Conflict of Interest

None to declare.

Section on Gerontology and Geriatric Medicine, J. Paul Sticht Center on Aging, Department of Internal Medicine, and
Department of Biostatistical Sciences, Wake Forest School of Medicine, Winston-Salem, North Carolina.
Department of Health and Exercise Science, Wake Forest University, Winston-Salem, North Carolina.
Thurston Arthritis Research Center and the Division of Rheumatology, Allergy, and Immunology, University of North Carolina, Chapel Hill.
Corresponding author.
Address correspondence to Barbara J. Nicklas, PhD, Section on Gerontology and Geriatric Medicine, Department of Internal Medicine, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157. E-mail: ude.htlaehekaw@salkcinb
Decision Editor: James Goodwin, MD
Received 2016 Mar 24; Accepted 2016 Jun 22.

Abstract

Background:

Habitual (non-exercise) physical activity (PA) declines with age, and aging-related increases in inflammation and fatigue may be important contributors to variability in PA.

Methods:

This study examined the association of objectively-measured PA (accelerometry over 7 days) with inflammation (plasma interleukin-6 and C-reactive protein) and with self-reported fatigue (SF-36 Vitality) at baseline and 18 months after a diet-induced weight loss, exercise, or diet-induced weight loss plus exercise intervention in 167 overweight/obese, middle-aged, and older adults.

Results:

At baseline, individuals with higher plasma interleukin-6, as well as those who reported feeling less energetic (more fatigued), took less steps per day and had lower PA energy expenditure and minutes of light and moderate–vigorous PA (p < .05 for all). At the 18-month follow-up, inflammation was lower in both weight loss groups, fatigue was reduced in all three groups with larger decreases in the combined group, and mean levels of habitual PA were not changed in any group. In longitudinal analyses with all groups combined, we found that participants reporting larger increases in vitality (eg, declines in fatigue) had greater increases in PA (p < .05 for all). Also, changes in steps/d and physical activity energy expenditure were indirectly associated with changes in interleukin-6 (β [SEM] for steps/d = −565 [253]; β [SEM] for physical activity energy expenditure = −22.4 [10.17]; p < .05).

Conclusions:

Levels of habitual PA are lower in middle-aged and older adults with higher levels of chronic inflammation and greater self-reported fatigue. In addition, participants who experienced greater declines in inflammation during the interventions had greater declines in fatigue and larger increases in PA.

Keywords: Accelerometry, C-reactive protein, Interleukin-6, SF-36 Vitality subscale
Abstract

Physical activity (PA) is comprised of both “purposeful” exercise, as well as non-exercise movement comprised primarily of mobility-related activities occurring throughout the day. This habitual (non-exercise) activity declines across the lifespan (1), an observation that is biologically inherent to aging, as it is evident even among highly fit older exercisers (2) and is observed across species (3). Habitual PA is inversely related to sedentary behavior (sitting or lying down), and more sedentary behavior is associated with worse physical function and loss of mobility in older adults, even independent of structured exercise (4–6).

Despite the fundamental ubiquitous nature of reduced habitual PA with age, very little is known regarding the biological, environmental, and/or psychosocial factors that contribute to one’s propensity to move and to inter-individual variation in movement. An important factor underlying less habitual activity may be fatigue, or the subjective lack of physical and/or mental energy (7). Fatigue also increase with age (8,9), and some studies report an association between fatigue and low levels of PA and greater sedentary behavior (10–17). However, the biological link between fatigue and sedentary behavior is not known. Acute inflammation from infection results in fatigue (ie, “sickness behavior”) and chronic inflammation underlies fatigue symptoms common to specific diseases (18–21). Aging is characterized by an increasingly elevated pro-inflammatory state, but one that is far below that observed during acute infections or disease states (22–24). This persistent, low-grade inflammation is likely a contributing factor to loss of muscle function and onset of disability with age (25,26); however, its role in fatigue and reduced PA is less studied (14,15,27,28).

The purpose of this study was to determine the cross-sectional and longitudinal relationships of objectively-measured habitual PA to biomarkers of inflammation and self-reported fatigue in middle-aged and older adults. We examined these relationships using baseline and follow-up data collected from participants before and 18 months after either: diet-induced weight loss alone, exercise alone, or diet-induced weight loss plus exercise. We hypothesized that individuals with higher inflammation would report feeling more fatigued and have lower levels of PA at baseline; and that individual changes in habitual PA over the 18 months of intervention would be associated with individual changes in inflammation and fatigue, independent of treatment arm.

References

  • 1. Westerterp KR. Daily physical activity and ageing. Curr Opin Clin Nutr Metab Care. 2000;3:485–488. [[PubMed]
  • 2. Madden KM, Ashe MC, Chase JM. Activity profile and energy expenditure among active older adults, British Columbia, 2011-2012. Prev Chronic Dis. 2015;12:E112. doi:10.5888/pcd12.150100
  • 3. Ingram DK. Age-related decline in physical activity: generalization to nonhumans. Med Sci Sports Exerc. 2000;32:1623–1629. [[PubMed]
  • 4. Chmelo E, Nicklas B, Davis C, Miller GD, Legault C, Messier S. Physical activity and physical function in older adults with knee osteoarthritis. J Phys Act Health. 2013;10:777–783.
  • 5. Gennuso KP, Gangnon RE, Matthews CE, Thraen-Borowski KM, Colbert LH. Sedentary behavior, physical activity, and markers of health in older adults. Med Sci Sports Exerc. 2013;45:1493–1500. doi:10.1249/MSS.0b013e318288a1e5
  • 6. Santos DA, Silva AM, Baptista F, et al Sedentary behavior and physical activity are independently related to functional fitness in older adults. Exp Gerontol. 2012;47:908–912. doi:10.1016/j.exger.2012.07.011 [[PubMed][Google Scholar]
  • 7. Avlund K. Fatigue in older adults: an early indicator of the aging process?Aging Clin Exp Res. 2010;22:100–115. [[PubMed]
  • 8. Cheng H, Gurland BJ, Maurer MS. Self-reported lack of energy (anergia) among elders in a multiethnic community. J Gerontol A Biol Sci Med Sci. 2008;63:707–714. [[PubMed]
  • 9. Junghaenel DU, Christodoulou C, Lai JS, Stone AA. Demographic correlates of fatigue in the US general population: results from the patient-reported outcomes measurement information system (PROMIS) initiative. J Psychosom Res. 2011;71:117–123. doi:10.1016/j.jpsychores.2011.04.007
  • 10. O’Connor PJ, Puetz TW. Chronic physical activity and feelings of energy and fatigue. Med Sci Sports Exerc. 2005;37:299–305. [[PubMed]
  • 11. Puetz TW. Physical activity and feelings of energy and fatigue: epidemiological evidence. Sports Med. 2006;36:767–780. [[PubMed]
  • 12. Moreh E, Jacobs JM, Stessman J. Fatigue, function, and mortality in older adults. J Gerontol A Biol Sci Med Sci. 2010;65:887–895. doi:10.1093/gerona/glq064 [[PubMed]
  • 13. Resnick HE, Carter EA, Aloia M, Phillips B. Cross-sectional relationship of reported fatigue to obesity, diet, and physical activity: results from the third national health and nutrition examination survey. J Clin Sleep Med. 2006;2:163–169. [[PubMed]
  • 14. Silva JP, Pereira DS, Coelho FM, Lustosa LP, Dias JM, Pereira LS. Clinical, functional and inflammatory factors associated with muscle fatigue and self-perceived fatigue in elderly community-dwelling women. Rev Bras Fisioter. 2011;15:241–248. [[PubMed]
  • 15. Valentine RJ, Woods JA, McAuley E, Dantzer R, Evans EM. The associations of adiposity, physical activity and inflammation with fatigue in older adults. Brain Behav Immun. 2011;25:1482–1490. doi:10.1016/j.bbi.2011.06.002 [[PubMed]
  • 16. Egerton T, Chastin SF, Stensvold D, Helbostad JL. Fatigue may contribute to reduced physical activity among older people: an observational study. J Gerontol A Biol Sci Med Sci. 2016;71:670–676. doi:10.1093/gerona/glv150 [[PubMed]
  • 17. Ward-Ritacco CL, Adrian AL, O’Connor PJ, et al Feelings of energy are associated with physical activity and sleep quality, but not adiposity, in middle-aged postmenopausal women. Menopause. 2015;22:304–311. doi:10.1097/GME.0000000000000315 [[PubMed][Google Scholar]
  • 18. Dantzer R, Heijnen CJ, Kavelaars A, Laye S, Capuron L. The neuroimmune basis of fatigue. Trends Neurosci. 2014;37:39–46. doi:10.1016/j.tins.2013.10.003
  • 19. Bower JE, Lamkin DM. Inflammation and cancer-related fatigue: mechanisms, contributing factors, and treatment implications. Brain Behav Immun. 2013;30(Suppl):S48–S57. doi:10.1016/j.bbi.2012.06.011
  • 20. Johansson P, Riegel B, Svensson E, et al Sickness behavior in community-dwelling elderly: associations with impaired cardiac function and inflammation. Biol Res Nurs. 2014;16:105–113. doi:10.1177/1099800412466170 [[PubMed][Google Scholar]
  • 21. Lasselin J, Layé S, Dexpert S, et al Fatigue symptoms relate to systemic inflammation in patients with type 2 diabetes. Brain Behav Immun. 2012;26:1211–1219. doi:10.1016/j.bbi.2012.03.003 [[PubMed][Google Scholar]
  • 22. Nash SD, Cruickshanks KJ, Klein R, et al Long-term variability of inflammatory markers and associated factors in a population-based cohort. J Am Geriatr Soc. 2013;61:1269–1276. doi:10.1111/jgs.12382 [Google Scholar]
  • 23. Ferrucci L, Corsi A, Lauretani F, et al The origins of age-related proinflammatory state. Blood. 2005;105:2294–2299. [[PubMed][Google Scholar]
  • 24. Franceschi C, Capri M, Monti D, et al Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128:92–105. [[PubMed][Google Scholar]
  • 25. Singh T, Newman AB. Inflammatory markers in population studies of aging. Ageing Res Rev. 2011;10:319–329. doi:10.1016/j.arr.2010.11.002
  • 26. Penninx BW, Kritchevsky SB, Newman AB, et al Inflammatory markers and incident mobility limitation in the elderly. J Am Geriatr Soc. 2004;52:1105–1113. [[PubMed][Google Scholar]
  • 27. Cho HJ, Kivimäki M, Bower JE, Irwin MR. Association of C-reactive protein and interleukin-6 with new-onset fatigue in the Whitehall II prospective cohort study. Psychol Med. 2013;43:1773–1783. doi:10.1017/S0033291712002437
  • 28. Bautmans I, Gorus E, Njemini R, Mets T. Handgrip performance in relation to self-perceived fatigue, physical functioning and circulating IL-6 in elderly persons without inflammation. BMC Geriatr. 2007;7:5.
  • 29. Messier SP, Mihalko SL, Legault C, et al Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. JAMA. 2013;310:1263–1273. doi:10.1001/jama.2013.277669 [Google Scholar]
  • 30. Ware JE, Jr, Sherbourne CD. The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care. 1992;30:473–483. [[PubMed]
  • 31. Van RH, Giavedoni S, Raste Y, et al Validity of activity monitors in health and chronic disease: a systematic review. Int J Behav Nutr Phys Act. 2012;9:84. doi:10.1186/1479-5868-9-84 [Google Scholar]
  • 32. Kumahara H, Schutz Y, Ayabe M, et al The use of uniaxial accelerometry for the assessment of physical-activity-related energy expenditure: a validation study against whole-body indirect calorimetry. Br J Nutr. 2004;91:235–243. [[PubMed][Google Scholar]
  • 33. Woloshin S, Schwartz LM. Distribution of C-reactive protein values in the United States. N Engl J Med. 2005;352:1611–1613. [[PubMed]
  • 34. Abramson JL, Vaccarino V. Relationship between physical activity and inflammation among apparently healthy middle-aged and older US adults. Arch Intern Med. 2002;162:1286–1292. [[PubMed]
  • 35. Nicklas BJ, You T, Pahor M. Behavioural treatments for chronic systemic inflammation: effects of dietary weight loss and exercise training. CMAJ. 2005;172:1199–1209.
  • 36. Adams SA, Wirth MD, Khan S, et al The association of C-reactive protein and physical activity among a church-based population of African Americans. Prev Med. 2015;77:137–140. doi:10.1016/j.ypmed.2015.05.010 [Google Scholar]
  • 37. Plaisance EP, Grandjean PW. Physical activity and high-sensitivity C-reactive protein. Sports Med. 2006;36:443–458. [[PubMed]
  • 38. Hawkins M, Belalcazar LM, Schelbert KB, Richardson C, Ballantyne CM, Kriska A. The effect of various intensities of physical activity and chronic inflammation in men and women by diabetes status in a national sample. Diabetes Res Clin Pract. 2012;97:e6–e8. doi:10.1016/j.diabres.2012.03.019 [[PubMed]
  • 39. Henson J, Yates T, Biddle SJ, et al Associations of objectively measured sedentary behaviour and physical activity with markers of cardiometabolic health. Diabetologia. 2013;56:1012–1020. doi:10.1007/s00125-013-2845-9 [[PubMed][Google Scholar]
  • 40. Gennuso KP, Gangnon RE, Matthews CE, Thraen-Borowski KM, Colbert LH. Sedentary behavior, physical activity, and markers of health in older adults. Med Sci Sports Exerc. 2013;45:1493–1500. doi:10.1249/MSS.0b013e318288a1e5
  • 41. Leon-Latre M, Moreno-Franco B, Andres-Esteban EM, et al Sedentary lifestyle and its relation to cardiovascular risk factors, insulin resistance and inflammatory profile. Rev Esp Cardiol (Engl Ed). 2014;67:449–455. doi:10.1016/j.rec.2013.10.015 [[PubMed][Google Scholar]
  • 42. Beavers KM, Beavers DP, Newman JJ, et al Effects of total and regional fat loss on plasma CRP and IL-6 in overweight and obese, older adults with knee osteoarthritis. Osteoarthritis Cartilage. 2015;23:249–256. doi:10.1016/j.joca.2014.11.005 [Google Scholar]
  • 43. Kroes M, Osei-Assibey G, Baker-Searle R, Huang J. Impact of weight change on quality of life in adults with overweight/obesity in the United States: a systematic review. Curr Med Res Opin. 2016;32:485–508. doi:10.1185/03007995.2015.1128403 [[PubMed]
Collaboration tool especially designed for Life Science professionals.Drag-and-drop any entity to your messages.