Environmental Intervention as a Therapy for Adverse Programming by Ancestral Stress

McCreary, J. Keiko; Erickson, Zachary T.; Hao, Yongxin; Ilnytskyy, Yaroslav; Kovalchuk, Igor; Metz, Gerlinde A. S.

doi:10.1038/srep37814

Cited by 52 publications

(43 citation statements)

References 87 publications

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“…Our results in mice are partially in agreement with those reported in rats; cessation of prenatal maternal stress in rats does not fully restore timing of delivery (26). This discrepancy could be explained by variations in how different species respond to stress (94,95). Yet, our finding in mice holds tangible and immediate public health relevance given the implication that daughters of stressed mothers may be able to manage the impacts of ancestral stress during their pregnancy.…”

Section: Discussionsupporting

confidence: 85%

Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

et al. 2020

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Maternal stress is a well-established risk factor for preterm birth and has been associated with adverse neonatal outcomes in the first and subsequent generations, including increased susceptibility to disease and lasting immunological changes. However, a causal link between prenatal maternal stress and preterm birth, as well as compromised neonatal immunity, has yet to be established. To fill this gap in knowledge, we used a murine model of prenatal maternal stress across three generations and high-dimensional flow cytometry to evaluate neonatal adaptive immunity. We report that recurrent prenatal maternal stress induced preterm birth in the first and second filial generations and negatively impacted early neonatal growth. Strikingly, prenatal maternal stress induced a systematic reduction in T cells and B cells, the former including regulatory CD4+ T cells as well as IL-4-and IL-17A-producing T cells, in the second generation. Yet, neonatal adaptive immunity gained resilience against prenatal maternal stress by the third generation. We also show that the rate of prenatal maternal stress-induced preterm birth can be reduced upon cessation of stress, though neonatal growth impairments persisted. These findings provide evidence that prenatal maternal stress causes preterm birth and affects neonatal immunity across generations, adverse effects that can be ameliorated upon cessation.

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Section: Discussionsupporting

confidence: 85%

Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

et al. 2020

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“…However, ST-housed zebrafish may feel unprotected and vulnerable in a barren environment, and thus stay alert and respond more intensely to stress. Similarly, a study has recently found that EE during adolescence increased the amount of glucocorticoid receptors in the hippocampus and reduced circulating levels of corticosterone, improving the negative feedback of the neuroendocrine axis in rats from stressed strains (McCreary et al, 2016). At the same time, EE attenuated the increase in corticosterone after alcohol ingestion (Lopez and Laber, 2015) and decreased corticosterone production as measured by fecal corticosterone metabolites in mice (Gurfein et al, 2017).…”

Section: Discussionmentioning

confidence: 88%

Environmental enrichment modulates the response to chronic stress in zebrafish

Marcon

Mocelin

Benvenutti

et al. 2018

Journal of Experimental Biology

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Several studies have shown that manipulations to the housing environment modulate susceptibility to stress in laboratory animals, mainly in rodents. Environmental enrichment (EE) is one such manipulation that promotes neuroprotection and neurogenesis, besides affecting behaviors such as drug self-administration. Zebrafish are a popular and useful animal model for behavioral neuroscience studies; however, studies evaluating the impact of housing conditions in this species are scarce. In this study, we verified the effects of EE on behavioral (novel tank test) and biochemical [cortisol and reactive oxygen species (ROS)] parameters in zebrafish submitted to unpredictable chronic stress (UCS). Consistent with our previous findings, UCS increased anxiety-like behavior, cortisol and ROS levels in zebrafish. EE for 21 or 28 days attenuated the effects induced by UCS on behavior and cortisol, and prevented the effects on ROS levels. Our findings reinforce the idea that EE exerts neuromodulatory effects across species, reducing vulnerability to stress and its biochemical impact. Also, these results indicate that zebrafish is a suitable model animal to study the behavioral effects and neurobiological mechanisms related to EE.

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“…[ 15 , 16 ] However, if the stressed subject is placed into a supportive environment, many of the adverse effects of stress can be reversed, suggesting that stress is a modifiable risk factor. [ 17 , 18 ] In human research, prenatal maternal stressors, such as natural disasters [ 19 ] adverse life events, and daily perceived stress [ 20 ] are associated with adverse pregnancy outcomes. Abuse and in particular, intimate partner violence (IPV), are the widely researched stressors associated with pregnancy outcomes.…”

Section: Introductionmentioning

confidence: 99%

Does a maternal history of abuse before pregnancy affect pregnancy outcomes? A systematic review with meta-analysis

Nesari

Olson

Vandermeer

et al. 2018

BMC Pregnancy Childbirth

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BackgroundEvidence relating maternal history of abuse before pregnancy with pregnancy outcomes is controversial. This study aims to examine the association between maternal histories of abuse before pregnancy and the risk of preterm delivery and low birth weight.MethodsWe searched Subject Headings and keywords for exposure and the outcomes through MEDLINE, EMBASE, Cochrane Database of Systematic Reviews, Cochrane Central Register of Controlled Trials, Psycinfo, CINAHL, Scopus, PILOTS, ProQuest Dissertations & Theses Global and Web of Science Core Collection in April 2017. We selected original studies that reported associations between maternal histories of abuse of any type and either preterm delivery or low birth weight. Studies that included interventions during pregnancy to lower maternal stress but reported no control data were excluded. We utilized the Newcastle-Ottawa Quality Assessment Scales for observational studies to assess the risk of bias in the primary studies. Two independent reviewers performed the selection of pertinent studies, assessment of risk of bias, and data extraction. Unadjusted pooled odds ratios (OR) with 95% Confidence Interval (CI) were calculated for the two outcomes of preterm delivery and low birth weight in 16 included studies.ResultsMaternal history of abuse before pregnancy was significantly associated with preterm delivery (OR 1.28, 95% CI: 1.12–1.47) and low birth weight (OR 1.35, 95% CI: 1.14–1.59). A substantial level of heterogeneity was detected within the two groups of studies reporting preterm birth and low birth weight (I2 = 75% and 69% respectively). Subgroup analysis based on the specific time of abuse before pregnancy indicated that childhood abuse increases the risk of low birth weight by 57% (95% CI: 0.99–2.49). When the included studies were categorized based on study design, cohort studies showed the highest effect estimates on preterm delivery and low birth weight (OR: 1.69, 95%CI: 1.19–2.40, OR: 1.56, 95% CI: 1.06–2.3, respectively).ConclusionsWe recommend that more high quality research studies on this topic are necessary to strengthen the inference. At the practice level, we suggest more attention in detecting maternal history of abuse before pregnancy during antenatal visits and using this information to inform risk assessment for adverse pregnancy outcomes.Trial registrationRegistration number: PROSPERO (CRD42016033231).Electronic supplementary materialThe online version of this article (10.1186/s12884-018-2030-8) contains supplementary material, which is available to authorized users.

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Environmental Intervention as a Therapy for Adverse Programming by Ancestral Stress

Cited by 52 publications

References 87 publications

Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

Environmental enrichment modulates the response to chronic stress in zebrafish

Does a maternal history of abuse before pregnancy affect pregnancy outcomes? A systematic review with meta-analysis

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