Skip to main content

Advertisement

SpringerLink
Log in

Presence of age-associated low-grade inflammation does not worsen the body response to bacterial infection in old male rats

  • Research Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

In the field of frailty, there is an underlying hypothesis that chronic low-grade inflammation contributes to bad outcomes in response to a stressor. The host response to an Escherichia coli infection was assessed in 24 month old male rats exhibiting a chronic low-grade inflammation and in non-inflamed control rats. Mortality, weight loss and sarcopenia were the main outcomes measured. The presence of chronic low-grade inflammation did not affect post-infection mortality, body weight loss and tissue mass decreases. Infection-induced modifications of plasma acute phase proteins concentrations were not higher in low-grade inflamed than non-inflamed rats. Absolute synthesis rates of tissue proteins were independent of the initial inflammatory status, except for liver 10 days after infection. Altogether, age-associated chronic low-grade inflammation in male rats did not worsen the body response to bacterial infection. These results suggest that chronic low-grade inflammation is not an aggravating factor of the spiraling process leading to frailty.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aderka D (1996) The potential biological and clinical significance of the soluble tumor necrosis factor receptors. Cytokine Growth Factor Rev 7:231–240

    Article  PubMed  CAS  Google Scholar 

  • Barbieri M, Ferrucci L, Ragno E, Corsi A, Bandinelli S, Bonafé M et al (2003) Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am J Physiol Endocrinol Metab 284:E481–E487

    PubMed  CAS  Google Scholar 

  • Breuillé D, Arnal M, Rambourdin F, Bayle G, Levieux D, Obled C (1998) Sustained modifications of protein metabolism in various tissues in a rat model of long- lasting sepsis. Clin Sci 94:413–423

    PubMed  Google Scholar 

  • Breuillé D, Voisin L, Contrepois M, Arnal M, Obled C (1999) A sustained rat model for studying long-lasting catabolic state of sepsis. Infect Immun 67:1079–1085

    PubMed  Google Scholar 

  • Bruunsgaard H, Pedersen M, Pedersen BK (2001) Aging and proinflammatory cytokines. Curr Opin Hematol 8:131–136

    Article  PubMed  CAS  Google Scholar 

  • Caso G, Mileva I, Kelly P, Ahn H, Gelato MC, McNurlan MA (2009) Feeding acutely stimulates fibrinogen synthesis in healthy young and elderly adults. J Nutr 139:2032–2036

    Article  PubMed  CAS  Google Scholar 

  • Cesari M, Penninx BWJH, Pahor M, Lauretani F, Corsi AM, Williams GR et al (2004) Inflammatory markers and physical performance in older persons: the inchianti study. J Gerontol A Biol Sci Med Sci 59:242–248

    PubMed  Google Scholar 

  • Cesari M, Kritchevsky SB, Baumgartner RN, Atkinson HH, Penninx BW, Lenchik L et al (2005) Sarcopenia, obesity, and inflammation—results from the trial of angiotensin converting enzyme inhibition and novel cardiovascular risk factors study. Am J Clin Nutr 82:428–434

    PubMed  CAS  Google Scholar 

  • Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F et al (2010) Sarcopenia: european consensus on definition and diagnosis. Age Ageing 39:412–423

    Article  PubMed  Google Scholar 

  • De Martinis M, Franceschi C, Monti D, Ginaldi L (2006) Inflammation markers predicting frailty and mortality in the elderly. Exp Mol Pathol 80:219–227

    Article  PubMed  Google Scholar 

  • El Yousfi M, Breuillé D, Papet I, Blum S, Andre M, Mosoni L et al (2003) Increased tissue protein synthesis during spontaneous inflammatory bowel disease in HLA-B27 rats. Clin Sci 105:437–446

    Article  PubMed  CAS  Google Scholar 

  • Fenton MJ, Golenbock DT (1998) LPS-binding proteins and receptors. J Leukoc Biol 64:25–32

    PubMed  CAS  Google Scholar 

  • Ferrucci L, Harris TB, Guralnik JM, Tracy RP, Corti MC, Cohen HJ et al (1999) Serum IL-6 level and the development of disability in older persons. J Am Geriatr Soc 47:639–646

    PubMed  CAS  Google Scholar 

  • Ferrucci L, Penninx BW, Volpato S, Harris TB, Bandeen-Roche K, Balfour J et al (2002) Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc 50:1947–1954

    Article  PubMed  Google Scholar 

  • Figaro MK, Kritchevsky SB, Resnick HE, Shorr RI, Butler J, Shintani A et al (2006) Diabetes, inflammation, and functional decline in older adults: findings from the Health, aging and body composition (ABC) study. Diabetes Care 29:2039–2045

    Article  PubMed  CAS  Google Scholar 

  • Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E et al (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908:244–254

    Article  PubMed  CAS  Google Scholar 

  • Fried LP, Walston J (2003) Frailty and failure to thrive. In: Hazzard W, Blass JP, Halter JB, Ouslander J, Tinetti M (eds) Principles of geriatric medicine and gerontology. McGraw-Hill, New York, pp 1487–1502

    Google Scholar 

  • Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J et al (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56:M146–M156

    PubMed  CAS  Google Scholar 

  • Fulop T, Pawelec G, Castle S, Loeb M (2009) Immunosenescence and vaccination in nursing home residents. Clin Infect Dis 48:443–448

    Article  PubMed  Google Scholar 

  • Greiwe JS, Cheng B, Rubin DC, Yarasheski KE, Semenkovich CF (2001) Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15:475–482

    Article  PubMed  CAS  Google Scholar 

  • High KP (2004) Infection as a cause of age-related morbidity and mortality. Ageing Res Rev 3:1–14

    Article  PubMed  Google Scholar 

  • Hubbard RE, Woodhouse KW (2010) Frailty, inflammation and the elderly. Biogerontology 11:635–641

    Article  PubMed  Google Scholar 

  • Kritchevsky SB, Cesari M, Pahor M (2005) Inflammatory markers and cardiovascular health in older adults. Cardiovasc Res 66:265–275

    Article  PubMed  CAS  Google Scholar 

  • Larbi A, Franceschi C, Mazzatti D, Solana R, Wikby A, Pawelec G (2008) Aging of the immune system as a prognostic factor for human longevity. Physiology 23:64–74

    Article  PubMed  CAS  Google Scholar 

  • Maeda H, Gleiser CA, Masoro EJ, Murata I, McMahan CA, Yu BP (1985) Nutritional influences on aging of fisher 344 rats: II. Pathology. J Gerontol 40:671–688

    PubMed  CAS  Google Scholar 

  • Markle-Reid M, Browne G (2003) Conceptualizations of frailty in relation to older adults. J Adv Nurs 44:58–68

    Article  PubMed  Google Scholar 

  • Mayot G, Vidal K, Martin J-F, Breuillé D, Blum S, Obled C et al (2007a) Prognostic values of [alpha]2-macroglobulin, fibrinogen and albumin in regards to mortality and frailty in old rats. Exp Gerontol 42:498–505

    Article  PubMed  CAS  Google Scholar 

  • Mayot G, Vidal K, Combaret L, Breuillé D, Blum S, Obled C et al (2007b) Presence of low-grade inflammation in old rats does not worsen skeletal muscle loss under an endotoxemic and dietary stress. Exp Gerontol 42:1167–1175

    Article  PubMed  CAS  Google Scholar 

  • Mayot G, Breuillé D, Jarret AR, Obled C, Papet I (2008) Systemic low-grade inflammation does not decrease skeletal muscle mass and protein synthesis in old rats. J Musculoskelet Neuronal Interact 8:410–417

    PubMed  CAS  Google Scholar 

  • Mercier S, Breuillé D, Mosoni L, Obled C, Patureau Mirand P (2002) Chronic inflammation alters protein metabolism in several organs of adult rats. J Nutr 132:1921–1928

    PubMed  CAS  Google Scholar 

  • Morley JE, Haren MT, Rolland Y, Kim MJ (2006) Frailty. Med Clin North Am 90:837–847

    Article  PubMed  Google Scholar 

  • Obled C, Papet I, Breuillé D (2002) Metabolic bases of amino acid requirements in acute diseases. Curr Opin Clin Nutr Metab Care 5:189–197

    Article  PubMed  CAS  Google Scholar 

  • Papet I, Ruot B, Breuillé D, Walrand S, Farges MC, Vasson MP et al (2002) Bacterial infection affects protein synthesis in primary lymphoid tissues and circulating lymphocytes of rats. J Nutr 132:2028–2032

    PubMed  CAS  Google Scholar 

  • Pawelec G, Derhovanessian E, Larbi A, Strindhall J, Wikby A (2009) Cytomegalovirus and human immunosenescence. Rev Med Virol 19:47–56

    Article  PubMed  CAS  Google Scholar 

  • Pedersen M, Bruunsgaard H, Weis N, Hendel HW, Andreassen BU, Eldrup E et al (2003) Circulating levels of TNF-alpha and IL-6-relation to truncal fat mass and muscle mass in healthy elderly individuals and in patients with type-2 diabetes. Mech Ageing Dev 124:495–502

    Article  PubMed  CAS  Google Scholar 

  • Pinel C, Coxam V, Mignon M, Taillandier D, Cubizolles C, Lebecque P et al (2006) Alterations in glutamine synthetase activity in rat skeletal muscle are associated with advanced age. Nutrition 22:778–785

    Article  PubMed  CAS  Google Scholar 

  • Reuben DB, Cheh AI, Harris TB, Ferrucci L, Rowe JW, Tracy RP et al (2002) Peripheral blood markers of inflammation predict mortality and functional decline in high-functioning community-dwelling older persons. J Am Geriatr Soc 50:638–644

    Article  PubMed  Google Scholar 

  • Ruot B, Béchereau-Rambourdin F, Bayle G, Breuillé D, Obled C (2002) The response of liver albumin synthesis to infection in rats varies with the phase of the inflammatory process. Clin Sci 102:107–114

    Article  PubMed  CAS  Google Scholar 

  • Ruot B, Papet I, Béchereau F, Denis P, Buffičre C, Gimonet J et al (2003) Increased albumin plasma efflux contributes to hypoalbuminemia only during early phase of sepsis in rats. Am J Physiol Regul Integr Comp Physiol 284:R707–R713

    PubMed  CAS  Google Scholar 

  • Schaap LA, Pluijm SMF, Deeg DJH, Visser M (2006) Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 119:U82–U90

    Article  Google Scholar 

  • Schalk BWM, Deeg DJH, Penninx BW, Bouter LM, Visser M (2005) Serum albumin and muscle strength: a longitudinal study in older men and women. J Am Geriatr Soc 53:1331–1338

    Article  PubMed  Google Scholar 

  • Theou O, Jones GR, Overend TJ, Kloseck M, Vandervoort AA (2008) An exploration of the association between frailty and muscle fatigue. Appl Physiol Nutr Metab 33:651–665

    Article  PubMed  Google Scholar 

  • Toth MJ, Matthews DE, Tracy RP, Previs MJ (2005) Age-related differences in skeletal muscle protein synthesis: relation to markers of immune activation. Am J Physiol Endocrinol Metab 288:E883–E891

    Article  PubMed  CAS  Google Scholar 

  • Vellas BJ, Albarede JL, Garry PJ (1992) Diseases and aging: patterns of morbidity with age; relationship between aging and age-associated diseases. Am J Clin Nutr 55:1225S–1230S

    PubMed  CAS  Google Scholar 

  • Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB et al (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: The health ABC study. J Gerontol A Biol Sci Med Sci 57:M326–M332

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Fabienne Béchereau, Philippe Denis, Johan Gimonet, Françoise Glomot and Patrick Serrant for their technical participation, the Staff of the Unité Expérimentale de Nutrition Comparée and Hélène Lafarge for literature acquisition. The research was supported by a PhD studentship and Grants from Institut National de la Recherche Agronomique (INRA), France and Nestlé, Switzerland.

Author information

Authors and Affiliations

  1. Unité de Nutrition Humaine, INRA, Centre Clermont-Ferrand-Theix, UMR 1019 Nutrition Humaine, 63122, Saint-Genès-Champanelle, France

    Gilles Mayot, Christiane Obled & Isabelle Papet

  2. UFR Médecine, UMR 1019 Nutrition Humaine, Clermont Université, 63000, Clermont-Ferrand, France

    Gilles Mayot, Christiane Obled & Isabelle Papet

  3. CRNH Auvergne, 63000, Clermont-Ferrand, France

    Gilles Mayot, Christiane Obled & Isabelle Papet

  4. Nutrition and Health Department, Nestlé Research Center, 1000, Lausanne 26, Switzerland

    Karine Vidal, Denis Breuillé & Stephanie Blum

  5. Plateforme d’Exploration du Métabolisme, INRA, Centre Clermont-Ferrand Theix, UMR 1019 Nutrition Humaine, 63122, Saint-Genès-Champanelle, France

    Carole Migné

Authors
  1. Gilles Mayot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karine Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carole Migné
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denis Breuillé
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephanie Blum
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christiane Obled
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isabelle Papet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Papet.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 86 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mayot, G., Vidal, K., Migné, C. et al. Presence of age-associated low-grade inflammation does not worsen the body response to bacterial infection in old male rats. Biogerontology 12, 133–145 (2011). https://doi.org/10.1007/s10522-010-9302-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-010-9302-7

Keywords

Search

Navigation