Behavioral benefits of maternal swimming are counteracted by neonatal hypoxia-ischemia in the offspring

Marcelino, Thiago Beltram; Rodrigues, Pedro; Klein, Caroline; Santos, Bernardo Gindri dos; Miguel, Patrícia Maidana; Netto, Carlos Alexandre; Pereira, Lenir Orlandi

doi:10.1016/j.bbr.2016.06.009

Cited by 20 publications

(22 citation statements)

References 69 publications

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“…; Marcelino et al . ). Children from mothers who were active during pregnancy scored high levels in the orientation and state regulation subscales of the Brazelton Neonatal Behavioural Assessment Scales (Clapp et al .…”

Section: Introductionmentioning

confidence: 97%

Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats

Fragoso

Lira

Chagas

et al. 2017

Experimental Physiology

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What is the central question of this study? In the present study, a reproducible model of maternal voluntary physical activity was developed to evaluate the adaptive response of physical activity by attenuating the effects of maternal undernutrition on physical features, reflex ontogeny and growth trajectory of offspring during development. What is the main finding and its importance? Maternal physical activity may induce neuronal maturation of sensorimotor connections impacting on the patterns of locomotor activity in malnourished offspring. Thus, physical activity should be considered as a therapeutic means of countering the effects of maternal undernutrition, by providing a useful strategy for enhancing the neuronal activity of children born to mothers who experience a restricted diet during pregnancy. This study evaluated the effects of maternal voluntary physical activity during pregnancy and lactation on somatic growth (SG), reflex ontogeny (RO) and locomotor activity (LA) of rats whose mothers were protein restricted. Virgin female Wistar rats were divided into the following six groups: control, normal protein (C-NP, n = 4); control, low protein (C-LP, n = 4); inactive, normal protein (I-NP, n = 8); inactive, low protein (I-LP, n = 7); very active, normal protein (VA-NP, n = 8); and very active, low protein (VA-LP, n = 6). Voluntary physical activity was recorded daily in dams. The LP groups were fed an 8% casein diet, whereas control groups were fed a 17% casein diet during pregnancy and lactation. Offspring were evaluated in terms of SG (body weight and length, latero-lateral skull axis and anteroposterior head axis) and RO (palmar grasp, righting, free-fall righting, negative geotaxis, cliff avoidance, auditory startle response and vibrissa placing). The LA was evaluated at 23, 45 and 60 days old in the open field. Voluntary physical activity was reduced during pregnancy and lactation independent of the maternal diet. Pups from LP dams showed delayed SG, reflex maturation and patterns of LA when compared with control pups. The C-LP and I-LP pups showed a delayed SG, RO and LA. Pups from VA-LP mothers showed no delay in SG and RO and presented a faster development of patterns of LA. Maternal voluntary physical activity attenuated the effects of LP diet on indicators of neurodevelopment and patterns of LA of offspring.

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Section: Introductionmentioning

confidence: 97%

Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats

Fragoso

Lira

Chagas

et al. 2017

Experimental Physiology

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“…In view of existing data on ontogeny of motor development, these data suggest a slight acceleration of motor development elicited by maternal swimming (Table 2). In a previous study, we have demonstrated that maternal exercised adult (PD60) female and male littermates’ performance in the locomotor and exploratory parameters observed in the open field test did not differ from controls (Marcelino et al, 2016). Moreover, in the same study we have demonstrated that male offspring born to exercised dams displayed an improved recognition memory over male offspring born to sedentary dams, and no difference was observed between female pups (Marcelino et al, 2016).…”

Section: Discussionmentioning

confidence: 87%

“…Despite most studies showing that gestational outcomes did not differ between maternal groups, some differences obtained among studies examining the effect of maternal exercise are thought to be due to different rodent models used (distinct mice and rat strains), exercise modality employed (voluntary or involuntary), timing (before and during pregnancy, only before or only during pregnancy) and duration (days or weeks) (Marcelino et al, 2013; Quiclet et al, 2016; Moser et al, 2017; Akhavan et al, 2008). Low and moderate intensity exercise improves offspring's outcomes, such as improved glucose metabolism (Stanford et al, 2017, 2015) and memory (Marcelino et al, 2016; Akhavan et al, 2008). In contrast, submaximal intensity exercise during pregnancy has been associated with worsened glucose metabolism in adult offspring (Quiclet et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…The effects of maternal exercise to the fetus are highlighted by benefits such as improved glucose metabolism (Wasinski et al, 2015; Stanford et al, 2017; Harris et al, 2018), enhanced insulin sensitivity (Carter et al, 2013; Stanford et al, 2015), enhanced brain antioxidant defenses (Marcelino et al, 2013) and improved memory (Fidalgo et al, 2013; Kim et al, 2007; Robinson and Bucci, 2014), which persist in adulthood. In a previous work we demonstrated that swimming during pregnancy enhances mitochondrial function in the brain of 7‐day‐old pups (Marcelino et al, 2013) and that recognition memory is enhanced in 60‐day‐old male offspring (Marcelino et al, 2016). Lee et al (2006) demonstrated that swimming during pregnancy enhances aversive memory in 28‐day old rats’ offspring by increasing neurogenesis.…”

Section: Introductionmentioning

confidence: 95%

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Swimming exercise before and during pregnancy: Promising preventive approach to impact offspring's health

Klein

Hözer

Couto-Pereira

et al. 2018

Intl J of Devlp Neuroscience

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Several environmental factors affect child development, such as the intrauterine environment during the embryonic and fetal development and early postnatal environment provided by maternal behavior. Although mechanistic effects of maternal exercise on offspring health improvement are not yet completely understood, the number of reports published demonstrating the positive influence of maternal exercise have increase. Herein, we addressed issues related to early postnatal environment provided by maternal behavior and early developmental physical landmarks, sensorimotor reflexes, and motor movements ontogeny. In brief, adult female rats underwent involuntary swimming exercise, in a moderated intensity, one week before mating and throughout pregnancy, 30 min a day, 5 days a week. Maternal exercised dams have unchanged gestational outcomes compared to sedentary dams. We found no differences concerning the frequency of pup-directed behavior displayed by dams. However, sedentary dams displayed a poorer pattern of maternal care quality during dark cycle than exercised dams. Physical landmarks and sensorimotor reflexes development of female and male littermates did not differ between maternal groups. Developmental motor parameters such as immobility, lateral head movements, head elevation, pivoting, rearing with forelimb support and crawling frequencies did not differ between groups. Pups born to exercised dams presented higher frequency of walking and rearing on the hind legs. These data suggest that female and male littermates of exercised group present a high frequency of exploratory behavior over sedentary littermates. Taken together, the present findings reinforce that maternal exercise throughout pregnancy represent a window of opportunity to improve offspring's postnatal health.

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“…Nevertheless, no significant differences were observed in the levels of reactive species and the antioxidant activity in the parietal cortex and the striatum, pointing that some brain areas are more sensitive to HI insult (Marcelino et al, 2015). Maternal exercise also induces early metabolic programming, as well as sex‐specific responses following HI, being the male offspring the most benefited from maternal exercise (Marcelino et al, 2016).…”

Section: Lifestyle Interventions ‐ Physical Exercise and Environmentamentioning

confidence: 99%

Pregnancy as a valuable period for preventing hypoxia‐ischemia brain damage

Netto

Sanches

Odorcyk

et al. 2018

Intl J of Devlp Neuroscience

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Neonatal brain Hypoxia-Ischemia (HI) is one of the major causes of infant mortality and lifelong neurological disabilities. The knowledge about the physiopathological mechanisms involved in HI lesion have increased in recent years, however these findings have not been translated into clinical practice. Current therapeutic approaches remain limited; hypothermia, used only in term or near-term infants, is the golden standard. Epidemiological evidence shows a link between adverse prenatal conditions and increased risk for diseases, health problems, and psychological outcomes later in life, what makes pregnancy a relevant period for preventing future brain injury. Here, we review experimental literature regarding preventive interventions used during pregnancy, i.e., previous to the HI injury, encompassing pharmacological, nutritional and/or behavioral strategies. Literature review used PubMed database. A total of forty one studies reported protective properties of maternal treatments preventing perinatal hypoxia-ischemia injury in rodents. Pharmacological agents and dietary supplementation showed mainly anti-excitotoxicity, anti-oxidant or anti-apoptotic properties. Interestingly, maternal preconditioning, physical exercise and environmental enrichment seem to engage the same referred mechanisms in order to protect neonatal brain against injury. This construct must be challenged by further studies to clearly define the main mechanisms responsible for neuroprotection to be explored in experimental context, as well as to test their potential in clinical settings.

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Behavioral benefits of maternal swimming are counteracted by neonatal hypoxia-ischemia in the offspring

Cited by 20 publications

References 69 publications

Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats

Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats

Swimming exercise before and during pregnancy: Promising preventive approach to impact offspring's health

Pregnancy as a valuable period for preventing hypoxia‐ischemia brain damage

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