On the origins of sex-based differences in respiratory disorders: Lessons and hypotheses from stress neuroendocrinology in developing rats

Rousseau, Jean‐Philippe; Tenorio‐Lopes, Luana; Baldy, Cécile; Janes, Tara A.; Fournier, Stéphanie; Kinkead, Richard

doi:10.1016/j.resp.2017.03.013

Cited by 19 publications

(19 citation statements)

References 170 publications

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“…This is in line with previous human and animal studies demonstrating that adverse early life experiences such as being exposed as a fetus to maternal stress, is related to the development of health and behavioural problems later in life [4][5][6][7][8][9]. However, the specific underlying mechanism for the association between prenatal stress exposure and dyspnoea perception in adulthood observed in the present study remains unclear.…”

supporting

confidence: 90%

“…Moreover, adverse, separation-related experiences in childhood were linked to the subsequent development of increased anxiety and dyspnoea [3]. However, the effects of adverse experiences in early, prenatal life on dyspnoea perception remain widely unknown, although prenatal exposure to maternal stress and anxiety has convincingly been related to the development of other health and behavioural problems later in life, including impairments of the respiratory control system and high anxiety levels [4][5][6][7][8][9]. Therefore, this study investigated the relationship between prenatal exposure to maternal stress and the perception of dyspnoea in adulthood 28 years later.…”

mentioning

confidence: 99%

“…Therefore, future studies are required to test further potential mechanisms that might underlie the observed association between early life adversity and perception of dyspnoea later in life. These studies might include measures of the autonomic nervous system, the hypothalamic-pituitary-adrenal axis, the endogenous opioidergic and chemosensitive systems as well as functional and structural measures of the brain, which have not only been suggested to be impacted by prenatal stress exposure [5][6][7][8], but are also involved in the processing of dyspnoea [2,3,9].…”

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confidence: 99%

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Prenatal stress exposure is associated with increased dyspnoea perception in adulthood

et al. 2017

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Dyspnoea is the aversive cardinal symptom in various prevalent conditions such as respiratory, cardiovascular and neuromuscular diseases and is associated with great individual and socioeconomic burden [1]. Over the past years, several physiological and also psychological factors have been demonstrated to affect the perception of dyspnoea [1,2]. For example, high levels of anxiety in adulthood were associated with increased dyspnoea perception in patients with asthma or chronic obstructive pulmonary disease (COPD), but also in healthy controls [2]. Moreover, adverse, separation-related experiences in childhood were linked to the subsequent development of increased anxiety and dyspnoea [3]. However, the effects of adverse experiences in early, prenatal life on dyspnoea perception remain widely unknown, although prenatal exposure to maternal stress and anxiety has convincingly been related to the development of other health and behavioural problems later in life, including impairments of the respiratory control system and high anxiety levels [4][5][6][7][8][9]. Therefore, this study investigated the relationship between prenatal exposure to maternal stress and the perception of dyspnoea in adulthood 28 years later.

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confidence: 90%

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confidence: 99%

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confidence: 99%

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Prenatal stress exposure is associated with increased dyspnoea perception in adulthood

et al. 2017

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“…P value for the interaction term between sex and GA category: P = 0.04. The inset histograms show the percentage of males and females with discontinued caffeine treatment in the total study population secretion, which compromises development of the male respiratory network such that male pups are predisposed to prolonged and more severe apnoeas (Baldy, Chamberland, Fournier, & Kinkead, 2018;Fournier et al, 2013;Rousseau et al, 2017). acknowledging the importance of sex as a factor in the prevalence of several respiratory disorders.…”

Section: Discussionmentioning

confidence: 99%

Sex‐based differences in apnoea of prematurity: A retrospective cohort study

Bairam

Laflamme

Drolet

et al. 2018

Experimental Physiology

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This retrospective cohort study assessed whether sex influences the occurrence of apnoea of prematurity (AOP) in preterm infants. The analysis included a cohort of 24,387 preterm infants born between the gestational ages (GA) of 24 and 33 weeks that were admitted to tertiary neonatal care units participating in the Canadian Neonatal Network from January 2011 to December 2015. Of those, 13,983 (57%) were diagnosed with AOP. More females were diagnosed with AOP than males, but the difference in the male/female ratio was marginal (P = 0.058). The majority (89%) of infants diagnosed with AOP received caffeine (89% of males; 89% of females). By using the discontinuation of caffeine therapy as a proxy for the resolution of significant AOP, data analysis showed that females born before 33 weeks of GA stopped caffeine treatment earlier than males whether the caffeine was discontinued before 34 or 37 weeks of GA. Consequently, females had fewer days of caffeine therapy than males, especially infants born between 26 and 27 weeks (P < 0.004), 28 and 29 weeks (P < 0.03), and 32 and 33 weeks of GA (P < 0.04). Similar trends were observed when the corrected GA at discontinuation of caffeine was used. Given that AOP is indicative of an immature respiratory system, our data suggest that the maturation of the respiratory system might occur more rapidly in females than males. We conclude that sex needs to be considered in future studies on AOP.

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“…Although the neural networks that generate and regulate breathing are very robust, there is no evidence indicating that they are exempt from this basic biological principle. Results from clinical and basic research studies have shown how perinatal exposure to stressors such as nicotine, hypoxia, low socioeconomic status or maternal separation compromise the development and function of the respiratory control system at various life stages (Kinney & Thach, ; Rousseau et al., ; Spatola et al., ).…”

Section: Introductionmentioning

confidence: 99%

The influence of sex and neonatal stress on medullary microglia in rat pups

Baldy

Fournier

Boisjoly-Villeneuve

et al. 2018

Experimental Physiology

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Neonatal stress has wide-ranging consequences for the developing brain, including the medullary cardiorespiratory network. In rat pups, the reflexive cardiorespiratory inhibition triggered by the presence of liquids near the larynx is augmented by neonatal maternal separation (NMS), especially in males. Sex-specific enhancement of synaptic connectivity by NMS might explain this cardiorespiratory dysfunction. Microglia influence the formation, maturation, activity and elimination of developing synapses, but their role in the wiring of medullary networks is unknown. Owing to their sensitivity to sex hormones and stress hormones, microglial dysfunction could contribute to the abnormal cardiorespiratory phenotype observed in NMS pups. Here, we first used ionized calcium-binding adapter molecule-1 (Iba-1) immunolabelling to compare the density and morphology of microglia in the medulla of male versus female rat pups (14-15 days old) that were either undisturbed or subjected to NMS (3 h day ; postnatal days 3-12). Neonatal maternal separation augmented the density of Iba-1 cells (caudal region of the NTS), increased the size of the soma and reduced the arborization area (especially in the dorsal motor nucleus of the vagus). Sex-based differences were not observed. Given that the actions of microglia are regulated by neuronal fractalkine (CX CL ), we then used western blot analysis to compare the expression of CX CL and its microglial receptor (CX CR ) in medullary homogenates from control and NMS pups. Although CX CR expression was 59% greater in males versus females, NMS had no effect on CX CL /CX CR signalling. Given that an amoeboid morphology reflects an immature phenotype in developing microglia, NMS could interfere with synaptic pruning via a different mechanism.

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On the origins of sex-based differences in respiratory disorders: Lessons and hypotheses from stress neuroendocrinology in developing rats

Cited by 19 publications

References 170 publications

Prenatal stress exposure is associated with increased dyspnoea perception in adulthood

Prenatal stress exposure is associated with increased dyspnoea perception in adulthood

Sex‐based differences in apnoea of prematurity: A retrospective cohort study

The influence of sex and neonatal stress on medullary microglia in rat pups

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