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Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling.

ABSTRACT: Early-life adversity is associated with accelerated cellular ageing during development and increased inflammation during adulthood. However, human studies can only establish correlation, not causation, and existing experimental animal approaches alter multiple components of early-life adversity simultaneously. We developed a novel hand-rearing paradigm in European starling nestlings (Sturnus vulgaris), in which we separately manipulated nutritional shortfall and begging effort for a period of 10 days. The experimental treatments accelerated erythrocyte telomere attrition and increased DNA damage measured in the juvenile period. For telomere attrition, amount of food and begging effort exerted additive effects. Only the combination of low food amount and high begging effort increased DNA damage. We then measured two markers of inflammation, high-sensitivity C-reactive protein and interleukin-6, when the birds were adults. The experimental treatments affected both inflammatory markers, though the patterns were complex and different for each marker. The effect of the experimental treatments on adult interleukin-6 was partially mediated by increased juvenile DNA damage. Our results show that both nutritional input and begging effort in the nestling period affect cellular ageing and adult inflammation in the starling. However, the pattern of effects is different for different biomarkers measured at different time points.

SUBMITTER: Nettle D

PROVIDER: S-EPMC5240102 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling.

Nettle Daniel D Andrews Clare C Reichert Sophie S Bedford Tom T Kolenda Claire C Parker Craig C Martin-Ruiz Carmen C Monaghan Pat P Bateson Melissa M

Scientific reports 20170117

Early-life adversity is associated with accelerated cellular ageing during development and increased inflammation during adulthood. However, human studies can only establish correlation, not causation, and existing experimental animal approaches alter multiple components of early-life adversity simultaneously. We developed a novel hand-rearing paradigm in European starling nestlings (Sturnus vulgaris), in which we separately manipulated nutritional shortfall and begging effort for a period of 10 ...[more]

PMID: 28094324

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Project description:BackgroundAdverse childhood experiences (ACEs) have long been known to be related to poorer health across the life course. Previous studies typically relied on cumulative risk scores or individual adversities measured through retrospective self-reports. However, these approaches have important limitations. Cumulative risk scores assume equal weighting of adversities and the single adversity approach ignores the high probability that adversities co-occur. In contrast, latent class analysis (LCA) offers an alternative approach to operationalise ACEs that respects the clustering of adversities and may identify specific patterns of ACEs important for health outcomes. Furthermore, prospective and retrospective reports of ACEs show poor agreement. Therefore, it is important to compare findings based on prospective and retrospective measures in the same individuals. Despite an increasing number of studies applying LCA to ACEs data, no studies have yet simultaneously investigated LCA to cumulative risk and single adversity approaches in their relationships with adult inflammation. Identifying the specific ACEs or combinations of ACEs which are strongly related to inflammation is important for investigating the mechanisms involved and the planning of effective interventions.MethodsUsing data on 8810 members of the 1958 British birth cohort we investigated 12 ACEs - physical, psychological and sexual abuse, physical and emotional neglect, parental mental health problems, witnessing abuse, parental conflict, parental divorce, parental offending, parental substance misuse and parental death. LCA was applied to explore the clustering of prospectively and retrospectively reported ACEs separately. Associations between latent classes, cumulative risk scores and individual adversities with three inflammatory markers (C-Reactive Protein, fibrinogen and von Willebrand Factor) were tested using linear regression.ResultsThere was co-occurrence between adversities, and particularly for retrospectively reported adversities. Three latent classes were identified in the prospective data - 'Low ACEs' (95.7%), 'Household dysfunction' (2.8%) and 'Parental loss' (1.5%) which were related to increased inflammation in mid-life, as were high ACE scores and individual measures of offending, death, divorce, physical neglect and family conflict. Four latent classes were identified in the retrospective data - 'Low ACEs', 'Parental mental health and substance misuse', 'Maltreatment and conflict' and 'Polyadversity.' The latter two (5.2%) were related to raised inflammation in mid-life, as was a retrospective ACE score of 4+ (8.3%) and individual measures of family conflict, psychological and physical abuse, emotional neglect and witnessing abuse.ConclusionsSpecific ACEs or ACE combinations might be important for chronic inflammation. LCA is an alternative approach to operationalising ACEs data but further research is needed.

Project description:Background:It is widely assumed that variation in fitness components has a physiological basis that might underlie selection on trade-offs, but the mechanisms driving decreased survival and future fecundity remain elusive. Here, we assessed whether physiological variables are related to workload ability or immediate fitness consequences and if they mediate future survival or reproductive success. We used data on 13 physiological variables measured in 93 female European starlings (Sturnus vulgaris) at two breeding stages (incubation, chick-rearing), for first-and second-broods over two years (152 observations). Results:There was little co-variation among the physiological variables, either in incubating or chick-rearing birds, but some systematic physiological differences between the two stages. Chick-rearing birds had lower hematocrit and plasma creatine kinase but higher hemoglobin, triglyceride and uric acid levels. Only plasma corticosterone was repeatable between incubation and chick-rearing. We assessed relationships between incubation or chick-rearing physiology and measures of workload, current productivity, future fecundity or survival in a univariate manner, and found very few significant relationships. Thus, we next explored the utility of multivariate analysis (principal components analysis, Mahalanobis distance) to account for potentially complex physiological integration, but still found no clear associations. Conclusions:This implies either that a) birds maintained physiological variables within a homeostatic range that did not affect their performance, b) there are relatively few links between physiology and performance, or, more likely, c) that the complexity of these relationships exceeds our ability to measure it. Variability in ecological context may complicate the relationship between physiology and behavior. We thus urge caution regarding the over-interpretation of isolated significant findings, based on single traits in single years, in the literature.

Dataset Information

Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling.

Publications

Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling.

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