Skip to main content
Top
Published in: BMC Anesthesiology 1/2020

Open Access 01-12-2020 | Research article

Preoperative sedentary behavior is neither a risk factor for perioperative neurocognitive disorders nor associated with an increase in peripheral inflammation, a prospective observational cohort study

Authors: Sarah Saxena, Christopher Rodts, Vincent Nuyens, Juliette Lazaron, Victoria Sosnowski, Franck Verdonk, Laurence Seidel, Adelin Albert, Jean Boogaerts, Veronique Kruys, Mervyn Maze, Joseph Vamecq

Published in: BMC Anesthesiology | Issue 1/2020

Login to get access

Abstract

Background

Surgical interventions result in a postoperative rise in circulating inflammatory cytokines and high molecular group box protein 1 (HMGB1). Herein, the impact of a sedentary lifestyle and other age-related factors on the development of perioperative neurocognitive disorders (PND) following non-cardiac surgical procedures was assessed in an older (55–75 years-old) surgical population.

Methods

Prior to surgery, patients were asked questions regarding their sedentary behavior and daily habits. They also passed the Mini Mental State Examination (MMSE) and their blood circulating interleukin 6 (IL-6) and HMGB1 levels were assayed by ELISA. IL-6 and HMGB1 measurements were repeated respectively 6 and 24 h after surgery. MMSE was re-evaluated 6 weeks and whenever possible 3 months after surgery.

Results

Thirty-eight patients were enrolled in the study from January until July 2019. The study identified self-sufficiency, multilinguism, and overall health score on the geriatric depression scale, as protectors against PND. No other demographic (age, sex), environmental (solitary/non-solitary housing, professional and physical activities, smoking, alcohol drinking), comorbidity (antipsychotic drug uptake, diabetic state) and type of surgery (orthopedic, general, genitourinary) influenced the development of PND. Although some factors (surgery type and age) influenced the surgery-induced rise in the circulating IL-6 levels, they did not impact HMGB1.

Conclusion

Inflammaging, reflected by the greater increment of surgery-induced IL-6 in patients with advanced age, was present. As trauma-induced release of HMGB1 was not similarly affected by age, we surmise that HMGB1, rather than circulating cytokines, is the key driver of the trauma-induced inflammatory cascade leading to PND.

Trial registration

Clinicaltrials.gov identifier: NCT03805685.
Literature
1.
go back to reference Savage GH. Insanity following the use of anaesthetics in operations. BMJ. 1887;3:1199–200.CrossRef Savage GH. Insanity following the use of anaesthetics in operations. BMJ. 1887;3:1199–200.CrossRef
2.
go back to reference Evered L, Silbert B, Knopman DS, Scott DA, DeKosky ST, Rasmussen LS, et al. Recommendations for the nomenclature of cognitive change associated with Anaesthesia and Surgery-2018. Anesthesiology. 2018;129:872–9.CrossRef Evered L, Silbert B, Knopman DS, Scott DA, DeKosky ST, Rasmussen LS, et al. Recommendations for the nomenclature of cognitive change associated with Anaesthesia and Surgery-2018. Anesthesiology. 2018;129:872–9.CrossRef
3.
go back to reference Steinmetz J, Christensen KB, Lund T, Lohse N, Rasmussen LS, ISPOCS group. Long-term consequences of postoperative cognitive dysfunction. Anesthesiology. 2009;110:548–55.CrossRef Steinmetz J, Christensen KB, Lund T, Lohse N, Rasmussen LS, ISPOCS group. Long-term consequences of postoperative cognitive dysfunction. Anesthesiology. 2009;110:548–55.CrossRef
4.
go back to reference Patel V, Champaneria R, Dretzke J, Yeung J. Effect of regional versus general anaesthesia on postoperative delirium in elderly patients undergoing surgery for hip fracture: a systematic review. BMJ Open. 2018;8:e020757.CrossRef Patel V, Champaneria R, Dretzke J, Yeung J. Effect of regional versus general anaesthesia on postoperative delirium in elderly patients undergoing surgery for hip fracture: a systematic review. BMJ Open. 2018;8:e020757.CrossRef
5.
go back to reference Moller JT, Cluitmans P, Rasmussen LS, Houx P, Rasmussen H, Rabbitt P, et al. Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet. 1998;351:857–61.CrossRef Moller JT, Cluitmans P, Rasmussen LS, Houx P, Rasmussen H, Rabbitt P, et al. Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet. 1998;351:857–61.CrossRef
6.
go back to reference Sieber FE, Neufeld KJ, Gottscalk A, Bigelow GE, Oh ES, Rosenberg PB, et al. Effect of depth of sedation in older patients undergoing hip fracture repair on postoperative delirium: the STRIDE randomized clinical trial. JAMA Surg. 2018;153:987–95.CrossRef Sieber FE, Neufeld KJ, Gottscalk A, Bigelow GE, Oh ES, Rosenberg PB, et al. Effect of depth of sedation in older patients undergoing hip fracture repair on postoperative delirium: the STRIDE randomized clinical trial. JAMA Surg. 2018;153:987–95.CrossRef
7.
go back to reference Vacas S, Degos V, Tracey KJ, Maze M. High-mobility group box 1 protein initiates postoperative cognitive decline by engaging bone marrow-derived macrophages. Anesthesiology. 2014;120:1160–7.CrossRef Vacas S, Degos V, Tracey KJ, Maze M. High-mobility group box 1 protein initiates postoperative cognitive decline by engaging bone marrow-derived macrophages. Anesthesiology. 2014;120:1160–7.CrossRef
8.
go back to reference Terrando N, Eriksson LI, Ryu JK, Yang T, Monaco C, Feldmann M, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol. 2011;70:986–95.CrossRef Terrando N, Eriksson LI, Ryu JK, Yang T, Monaco C, Feldmann M, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol. 2011;70:986–95.CrossRef
9.
go back to reference Feng X, Valdearcos M, Uchida Y, Lutrin D, Maze M, Koliwad SK. Microglia mediate postoperative hippocampal inflammation and cognitive decline in mice. JCI Insight. 2017;2:e91229.CrossRef Feng X, Valdearcos M, Uchida Y, Lutrin D, Maze M, Koliwad SK. Microglia mediate postoperative hippocampal inflammation and cognitive decline in mice. JCI Insight. 2017;2:e91229.CrossRef
10.
go back to reference Cibelli M, Fidalgo AR, Terrando N, Monaco C, Feldmann M, Takata M, et al. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann Neur. 2010;68:360–8.CrossRef Cibelli M, Fidalgo AR, Terrando N, Monaco C, Feldmann M, Takata M, et al. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann Neur. 2010;68:360–8.CrossRef
11.
go back to reference Hu J, Feng X, Valdearcos M, Lutrin D, Uchida Y, Koliwad SK, et al. Interleukin-6 is both necessary and sufficient to produce perioperative neurocognitive disorder in mice. Br J Anaesth. 2018;120:537–45.CrossRef Hu J, Feng X, Valdearcos M, Lutrin D, Uchida Y, Koliwad SK, et al. Interleukin-6 is both necessary and sufficient to produce perioperative neurocognitive disorder in mice. Br J Anaesth. 2018;120:537–45.CrossRef
12.
go back to reference Feng X, Degos V, Koch LG, Britton SL, Zhu Y, Vacas S, et al. Surgery results in exaggerated and persistent cognitive decline in a rat model of the metabolic syndrome. Anesthesiology. 2013;118:1098–105.CrossRef Feng X, Degos V, Koch LG, Britton SL, Zhu Y, Vacas S, et al. Surgery results in exaggerated and persistent cognitive decline in a rat model of the metabolic syndrome. Anesthesiology. 2013;118:1098–105.CrossRef
13.
go back to reference Terrando N, Gomez-Galan M, Yang T, Carlstrom M, Gustavsson D, Harding RE, et al. Aspirin-triggered Resolvin D1 prevents surgery-induced cognitive decline. FASEBJ. 2013;27:3564–71.CrossRef Terrando N, Gomez-Galan M, Yang T, Carlstrom M, Gustavsson D, Harding RE, et al. Aspirin-triggered Resolvin D1 prevents surgery-induced cognitive decline. FASEBJ. 2013;27:3564–71.CrossRef
14.
go back to reference Yang T, Xu G, Newton PT, Chagin AS, Mkrtchian S, Carlstrom M, et al. Maresin 1 attenuates Neuroinflammation in a mouse model of perioperative neurocognitive disorders. BJA. 2019;122:350–60.CrossRef Yang T, Xu G, Newton PT, Chagin AS, Mkrtchian S, Carlstrom M, et al. Maresin 1 attenuates Neuroinflammation in a mouse model of perioperative neurocognitive disorders. BJA. 2019;122:350–60.CrossRef
15.
go back to reference Saxena S, Lai IK, Li R, Maze M. Neuroinflammation is a putative target for the prevention and treatment of perioperative neurocognitive disorders. Br Med Bull. 2019;130:125–35.CrossRef Saxena S, Lai IK, Li R, Maze M. Neuroinflammation is a putative target for the prevention and treatment of perioperative neurocognitive disorders. Br Med Bull. 2019;130:125–35.CrossRef
16.
go back to reference Monk TG, Weldon BC, Garvan CW, Dede DE, Van der Aa MT, Heilman KM, et al. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108:18–30.CrossRef Monk TG, Weldon BC, Garvan CW, Dede DE, Van der Aa MT, Heilman KM, et al. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108:18–30.CrossRef
17.
go back to reference Hudetz JA, Patterson KM, Amole O, Riley AV, Pagel PS. Postoperative cognitive dysfunction after noncardiac surgery: effects of metabolic syndrome. J Anesth. 2011;25:337–44.CrossRef Hudetz JA, Patterson KM, Amole O, Riley AV, Pagel PS. Postoperative cognitive dysfunction after noncardiac surgery: effects of metabolic syndrome. J Anesth. 2011;25:337–44.CrossRef
18.
go back to reference Jones RN, Fong TG, Metzger E, Tulebaev S, Yang FM, Alsop DC, et al. Aging, brain disease and reserve: implications for delirium. Am J Geriatr Psychiatry. 2010;18:117–27.CrossRef Jones RN, Fong TG, Metzger E, Tulebaev S, Yang FM, Alsop DC, et al. Aging, brain disease and reserve: implications for delirium. Am J Geriatr Psychiatry. 2010;18:117–27.CrossRef
19.
go back to reference Yates T, Khunti K, Wilmot EG, Brady E, Webb D, Srinivasan B, et al. Self-reported sitting time and markers of inflammation, insulin resistance, and adiposity. Am J Prev Med. 2012;42:1–7.CrossRef Yates T, Khunti K, Wilmot EG, Brady E, Webb D, Srinivasan B, et al. Self-reported sitting time and markers of inflammation, insulin resistance, and adiposity. Am J Prev Med. 2012;42:1–7.CrossRef
20.
go back to reference Alves BC, Silva TR, Spritzer PM. Sedentary lifestyle and high-carbohydrate intake are associated with low-grade chronic inflammation in post-menopause: a cross-sectional study. Rev Bras Ginecol Obstet. 2016;38:317–24.CrossRef Alves BC, Silva TR, Spritzer PM. Sedentary lifestyle and high-carbohydrate intake are associated with low-grade chronic inflammation in post-menopause: a cross-sectional study. Rev Bras Ginecol Obstet. 2016;38:317–24.CrossRef
21.
go back to reference Ferrucci L, Semba RD, Guralnik JM, Ershler WB, Bandinelli S, Patel KV, et al. Proinflammatory state, hepcidin, and anemia in older persons. Blood. 2010;115:3810–6.CrossRef Ferrucci L, Semba RD, Guralnik JM, Ershler WB, Bandinelli S, Patel KV, et al. Proinflammatory state, hepcidin, and anemia in older persons. Blood. 2010;115:3810–6.CrossRef
22.
go back to reference Fulop T, Larbi A, Dupuis G, Le Page A, Frost EH, Cohen AA, et al. Immunosenescence and Inflamm-aging as two sides of the same coin: friends or foes? Front Immunol. 2018;8:1960.CrossRef Fulop T, Larbi A, Dupuis G, Le Page A, Frost EH, Cohen AA, et al. Immunosenescence and Inflamm-aging as two sides of the same coin: friends or foes? Front Immunol. 2018;8:1960.CrossRef
23.
go back to reference Cohen HJ, Pieper CF, Harris T, Rao KM, Currie MS. The association of plasma IL-6 levels with functional disability in community-dwelling elderly. J Gerontol A Biol Sci Med Sci. 1997;52:M201–8.CrossRef Cohen HJ, Pieper CF, Harris T, Rao KM, Currie MS. The association of plasma IL-6 levels with functional disability in community-dwelling elderly. J Gerontol A Biol Sci Med Sci. 1997;52:M201–8.CrossRef
24.
go back to reference Luo A, Yan J, Tang X, Zhao Y, Zhou B, Li S. Postoperative cognitive dysfunction in the aged: the collision of neuroinflammaging with perioperative neuroinflammation. Inflammopharmacology. 2019;27:27–37.CrossRef Luo A, Yan J, Tang X, Zhao Y, Zhou B, Li S. Postoperative cognitive dysfunction in the aged: the collision of neuroinflammaging with perioperative neuroinflammation. Inflammopharmacology. 2019;27:27–37.CrossRef
25.
go back to reference Lin X, Chen Y, Zhang P, Chen G, Zhou Y, Yu X. The potential mechanism of postoperative cognitive dysfunction in older people. Exp Gerontol. 2020;130:110791.CrossRef Lin X, Chen Y, Zhang P, Chen G, Zhou Y, Yu X. The potential mechanism of postoperative cognitive dysfunction in older people. Exp Gerontol. 2020;130:110791.CrossRef
26.
go back to reference Degos V, Maze M, Vacas S, Hirsch J, Guo Y, Shen F, et al. Bone fracture exacerbates murine ischemic cerebral injury. Anesthesiology. 2013;118:1362–72.CrossRef Degos V, Maze M, Vacas S, Hirsch J, Guo Y, Shen F, et al. Bone fracture exacerbates murine ischemic cerebral injury. Anesthesiology. 2013;118:1362–72.CrossRef
27.
go back to reference Satoh M, Kotani K, Yamada S, Koinuma K, Horie H, Takeuchi M. Postoperative changes in high mobility group box 1 levels after colorectal cancer surgery. J Int Med Res. 2017;45:1651–7.CrossRef Satoh M, Kotani K, Yamada S, Koinuma K, Horie H, Takeuchi M. Postoperative changes in high mobility group box 1 levels after colorectal cancer surgery. J Int Med Res. 2017;45:1651–7.CrossRef
28.
go back to reference Lin GX, Wang T, Chen MH, Hu ZH, Ouyang W. Serum high-mobility group box 1 protein correlates with cognitive decline after gastrointestinal surgery. Acta Anaesthesiol Scand. 2014;58:668–74.CrossRef Lin GX, Wang T, Chen MH, Hu ZH, Ouyang W. Serum high-mobility group box 1 protein correlates with cognitive decline after gastrointestinal surgery. Acta Anaesthesiol Scand. 2014;58:668–74.CrossRef
29.
go back to reference Terrando N, Yang T, Wang X, Fang J, Cao M, Andersson U, et al. Systemic HMGB1 neutralization prevents postoperative neurocognitive dysfunction in aged rats. Front Immunol. 2016;7:441.CrossRef Terrando N, Yang T, Wang X, Fang J, Cao M, Andersson U, et al. Systemic HMGB1 neutralization prevents postoperative neurocognitive dysfunction in aged rats. Front Immunol. 2016;7:441.CrossRef
30.
go back to reference Lonie JA, Tierney KM, Ebmeier KP. Screening for mild cognitive impairment: a systematic review. Int J Geriatr Psychiatry. 2009;24:902–15.CrossRef Lonie JA, Tierney KM, Ebmeier KP. Screening for mild cognitive impairment: a systematic review. Int J Geriatr Psychiatry. 2009;24:902–15.CrossRef
31.
go back to reference Mitchell A, Larner AJ. The mini-mental state examination (MMSE): update on its diagnostic accuracy and clinical utility for cognitive disorders. In: cognitive screening instruments. Cham: Springer International Publishing; 2017. Mitchell A, Larner AJ. The mini-mental state examination (MMSE): update on its diagnostic accuracy and clinical utility for cognitive disorders. In: cognitive screening instruments. Cham: Springer International Publishing; 2017.
32.
go back to reference Feng X, Uchida Y, Koch L, Britton S, Hu J, Lutrin D, Maze M. Exercise prevents enhanced postoperative Neuroinflammation and cognitive decline and rectifies the gut microbiome in a rat model of metabolic syndrome. Front Immunol. 2017;8:1768.CrossRef Feng X, Uchida Y, Koch L, Britton S, Hu J, Lutrin D, Maze M. Exercise prevents enhanced postoperative Neuroinflammation and cognitive decline and rectifies the gut microbiome in a rat model of metabolic syndrome. Front Immunol. 2017;8:1768.CrossRef
Metadata
Title
Preoperative sedentary behavior is neither a risk factor for perioperative neurocognitive disorders nor associated with an increase in peripheral inflammation, a prospective observational cohort study
Authors
Sarah Saxena
Christopher Rodts
Vincent Nuyens
Juliette Lazaron
Victoria Sosnowski
Franck Verdonk
Laurence Seidel
Adelin Albert
Jean Boogaerts
Veronique Kruys
Mervyn Maze
Joseph Vamecq
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Anesthesiology / Issue 1/2020
Electronic ISSN: 1471-2253
DOI
https://doi.org/10.1186/s12871-020-01200-w

Other articles of this Issue 1/2020

BMC Anesthesiology 1/2020 Go to the issue