Immune Phenotype and Postoperative Complications After Elective Surgery.
Journal
Annals of surgery
ISSN: 1528-1140
Titre abrégé: Ann Surg
Pays: United States
ID NLM: 0372354
Informations de publication
Date de publication:
01 12 2023
01 12 2023
Historique:
medline:
9
11
2023
pubmed:
14
4
2023
entrez:
13
4
2023
Statut:
ppublish
Résumé
To characterize and quantify accumulating immunologic alterations, pre and postoperatively in patients undergoing elective surgical procedures. Elective surgery is an anticipatable, controlled human injury. Although the human response to injury is generally stereotyped, individual variability exists. This makes surgical outcomes less predictable, even after standardized procedures, and may provoke complications in patients unable to compensate for their injury. One potential source of variation is found in immune cell maturation, with phenotypic changes dependent on an individual's unique, lifelong response to environmental antigens. We enrolled 248 patients in a prospective trial facilitating comprehensive biospecimen and clinical data collection in patients scheduled to undergo elective surgery. Peripheral blood was collected preoperatively, and immediately on return to the postanesthesia care unit. Postoperative complications that occurred within 30 days after surgery were captured. As this was an elective surgical cohort, outcomes were generally favorable. With a median follow-up of 6 months, the overall survival at 30 days was 100%. However, 20.5% of the cohort experienced a postoperative complication (infection, readmission, or system dysfunction). We identified substantial heterogeneity of immune senescence and terminal differentiation phenotypes in surgical patients. More importantly, phenotypes indicating increased T-cell maturation and senescence were associated with postoperative complications and were evident preoperatively. The baseline immune repertoire may define an immune signature of resilience to surgical injury and help predict risk for surgical complications.
Sections du résumé
OBJECTIVES
To characterize and quantify accumulating immunologic alterations, pre and postoperatively in patients undergoing elective surgical procedures.
BACKGROUND
Elective surgery is an anticipatable, controlled human injury. Although the human response to injury is generally stereotyped, individual variability exists. This makes surgical outcomes less predictable, even after standardized procedures, and may provoke complications in patients unable to compensate for their injury. One potential source of variation is found in immune cell maturation, with phenotypic changes dependent on an individual's unique, lifelong response to environmental antigens.
METHODS
We enrolled 248 patients in a prospective trial facilitating comprehensive biospecimen and clinical data collection in patients scheduled to undergo elective surgery. Peripheral blood was collected preoperatively, and immediately on return to the postanesthesia care unit. Postoperative complications that occurred within 30 days after surgery were captured.
RESULTS
As this was an elective surgical cohort, outcomes were generally favorable. With a median follow-up of 6 months, the overall survival at 30 days was 100%. However, 20.5% of the cohort experienced a postoperative complication (infection, readmission, or system dysfunction). We identified substantial heterogeneity of immune senescence and terminal differentiation phenotypes in surgical patients. More importantly, phenotypes indicating increased T-cell maturation and senescence were associated with postoperative complications and were evident preoperatively.
CONCLUSIONS
The baseline immune repertoire may define an immune signature of resilience to surgical injury and help predict risk for surgical complications.
Identifiants
pubmed: 37051915
doi: 10.1097/SLA.0000000000005864
pii: 00000658-202312000-00007
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
873-882Informations de copyright
Copyright © 2023 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors report no conflicts of interest.
Références
Udelsman R, Ramp J, Gallucci WT, et al. Adaptation during surgical stress. A reevaluation of the role of glucocorticoids. J Clin Invest. 1986;77:1377–1381.
Skelton JK, Purcell R. Preclinical models for studying immune responses to traumatic injury. Immunology. 2021;162:377–388.
Tsirogianni AK, Moutsopoulos NM, Moutsopoulos HM. Wound healing: immunological aspects. Injury. 2006;37(suppl 1):S5–S12.
Hazeldine J, Hampson P, Lord JM. The diagnostic and prognostic value of systems biology research in major traumatic and thermal injury: a review. Burns Trauma. 2016;4:33.
Hazeldine J, Naumann DN, Toman E, et al. Prehospital immune responses and development of multiple organ dysfunction syndrome following traumatic injury: a prospective cohort study. PLoS Med. 2017;14:e1002338.
Cabrera CP, Manson J, Shepherd JM, et al. Signatures of inflammation and impending multiple organ dysfunction in the hyperacute phase of trauma: a prospective cohort study. PLoS Med. 2017;14:e1002352.
Sallusto F, Lenig D, Forster R, et al. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401:708–712.
Larbi A, Fulop T. From “truly naive” to “exhausted senescent” T cells: when markers predict functionality. Cytometry A. 2014;85:25–35.
Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015;15:486–499.
Tedeschi V, Paldino G, Kunkl M, et al. CD8(+) T cell senescence: lights and shadows in viral infections, autoimmune disorders and cancer. Int J Mol Sci. 2022;23:3374.
Fribourg M, Anderson L, Fischman C, et al. T-cell exhaustion correlates with improved outcomes in kidney transplant recipients. Kidney Int. 2019;96:436–449.
Moris D, Henao R, Hensman H, et al. Multidimensional machine learning models predicting outcomes after trauma. Surgery. 2022;172:1851–1859.
Espinosa JR, Samy KP, Kirk AD. Memory T cells in organ transplantation: progress and challenges. Nat Rev Nephrol. 2016;12:339–347.
George RP, Mehta AK, Perez SD, et al. Premature T cell senescence in pediatric CKD. J Am Soc Nephrol. 2017;28:359–367.
Chen J, Li J, Lim FC, et al. Maintenance of naive CD8 T cells in nonagenarians by leptin, IGFBP3 and T3. Mech Ageing Dev. 2010;131:29–37.
Benichou G, Kim J. Editorial: allorecognition by leukocytes of the adaptive immune system. Front Immunol. 2017;8:1555.
Eckhoff AM, Connor AA, Thacker JKM, et al. A multidimensional bioinformatic platform for the study of human response to surgery. Ann Surg. 2022;275:1094–1102.
Weir CB, Jan A. BMI Classification Percentile And Cut Off Points, In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022.
National Nosocomial Infections Surveillance S. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control. 2004;32:470–485.
Sun L, Gang X, Li Z, et al. Advances in understanding the roles of CD244 (SLAMF4) in immune regulation and associated diseases. Front Immunol. 2021;12:648182.
Glickman ME, Rao SR, Schultz MR. False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. J Clin Epidemiol. 2014;67:850–857.
Wu Z, Zheng Y, Sheng J, et al. CD3(+)CD4(-)CD8(-) (Double-Negative) T cells in inflammation, immune disorders and cancer. Front Immunol. 2022;13:816005.
Franceschi C, Bonafe M, Valensin S, et al. Inflamm-aging. an evolutionary perspective on immunosenescence. Ann N Y Acad Sci. 2000;908:244–254.
Del Giudice G, Goronzy JJ, Grubeck-Loebenstein B, et al. Fighting against a protean enemy: immunosenescence, vaccines, and healthy aging. NPJ Aging Mech Dis. 2018;4:1.
Koch S, Larbi A, Derhovanessian E, et al. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing. 2008;5:6.
Di Mitri D, Azevedo RI, Henson SM, et al. Reversible senescence in human CD4+CD45RA+CD27- memory T cells. J Immunol. 2011;187:2093–2100.
Franceschi C, Bonafe M, Valensin S. Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine. 2000;18:1717–1720.
Larbi A, Franceschi C, Mazzatti D, et al. Aging of the immune system as a prognostic factor for human longevity. Physiology (Bethesda). 2008;23:64–74.
Appay V, Fastenackels S, Katlama C, et al. Old age and anti-cytomegalovirus immunity are associated with altered T-cell reconstitution in HIV-1-infected patients. AIDS. 2011;25:1813–1822.
Papagno L, Spina CA, Marchant A, et al. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol. 2004;2:E20.
Simanek AM, Dowd JB, Pawelec G, et al. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One. 2011;6:e16103.
Vicente D, Schobel SA, Anfossi S, et al. Viral micro-RNAs are detected in the early systemic response to injury and are associated with outcomes in polytrauma patients. Crit Care Med. 2022;50:296–306.