Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries

Edward P. Snelling, Roger S. Seymour, Dino A. Giussani, Andrea Fuller, Shane K. Maloney, Anthony P. Farrell, Duncan Mitchell, Keith P. George, Edward M. Dzialowski, Sonnet Jonker, Tilaye Wube

    Research output: Contribution to journalArticle

    Abstract

    Scaling of the heart across development can reveal the degree to which variation in cardiac morphology depends on body mass. In this study, we assessed the scaling of heart mass, left and right ventricular masses, and ventricular mass ratio, as a function of eviscerated body mass across fetal and postnatal development in Horro sheep Ovis aries (~50-fold body mass range; N = 21). Whole hearts were extracted from carcasses, cleaned, dissected into chambers and weighed. We found a biphasic relationship when heart mass was scaled against body mass, with a conspicuous ‘breakpoint’ around the time of birth, manifest not by a change in the scaling exponent (slope), but rather a jump in the elevation. Fetal heart mass (g) increased with eviscerated body mass (M b , kg) according to the power equation 4.90 M b 0.88 ± 0.26 (± 95% CI ) , whereas postnatal heart mass increased according to 10.0 M b 0.88 ± 0.10 . While the fetal and postnatal scaling exponents are identical (0.88) and reveal a clear dependence of heart mass on body mass, only the postnatal exponent is significantly less than 1.0, indicating the postnatal heart becomes a smaller component of body mass as the body grows, which is a pattern found frequently with postnatal cardiac development among mammals. The rapid doubling in heart mass around the time of birth is independent of any increase in body mass and is consistent with the normalization of wall stress in response to abrupt changes in volume loading and pressure loading at parturition. We discuss variation in scaling patterns of heart mass across development among mammals, and suggest that the variation results from a complex interplay between hard-wired genetics and epigenetic influences.

    Original languageEnglish (US)
    JournalJournal of Anatomy
    DOIs
    StatePublished - Jan 1 2019

    Fingerprint

    Domestic Sheep
    sheep
    Sheep
    body mass
    Parturition
    heart
    Mammals
    mammal
    Fetal Heart
    parturition
    Fetal Development
    Epigenomics
    mammals
    fold
    Pressure

    Keywords

    • allometry
    • biphasic
    • cardiac
    • fetal
    • morphogenesis
    • ontogeny

    ASJC Scopus subject areas

    • Anatomy
    • Histology
    • Ecology, Evolution, Behavior and Systematics
    • Molecular Biology
    • Developmental Biology
    • Cell Biology

    Cite this

    Snelling, E. P., Seymour, R. S., Giussani, D. A., Fuller, A., Maloney, S. K., Farrell, A. P., ... Wube, T. (2019). Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries. Journal of Anatomy. https://doi.org/10.1111/joa.12990

    Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries. / Snelling, Edward P.; Seymour, Roger S.; Giussani, Dino A.; Fuller, Andrea; Maloney, Shane K.; Farrell, Anthony P.; Mitchell, Duncan; George, Keith P.; Dzialowski, Edward M.; Jonker, Sonnet; Wube, Tilaye.

    In: Journal of Anatomy, 01.01.2019.

    Research output: Contribution to journalArticle

    Snelling, EP, Seymour, RS, Giussani, DA, Fuller, A, Maloney, SK, Farrell, AP, Mitchell, D, George, KP, Dzialowski, EM, Jonker, S & Wube, T 2019, 'Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries', Journal of Anatomy. https://doi.org/10.1111/joa.12990
    Snelling EP, Seymour RS, Giussani DA, Fuller A, Maloney SK, Farrell AP et al. Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries. Journal of Anatomy. 2019 Jan 1. https://doi.org/10.1111/joa.12990
    Snelling, Edward P. ; Seymour, Roger S. ; Giussani, Dino A. ; Fuller, Andrea ; Maloney, Shane K. ; Farrell, Anthony P. ; Mitchell, Duncan ; George, Keith P. ; Dzialowski, Edward M. ; Jonker, Sonnet ; Wube, Tilaye. / Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries. In: Journal of Anatomy. 2019.
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    abstract = "Scaling of the heart across development can reveal the degree to which variation in cardiac morphology depends on body mass. In this study, we assessed the scaling of heart mass, left and right ventricular masses, and ventricular mass ratio, as a function of eviscerated body mass across fetal and postnatal development in Horro sheep Ovis aries (~50-fold body mass range; N = 21). Whole hearts were extracted from carcasses, cleaned, dissected into chambers and weighed. We found a biphasic relationship when heart mass was scaled against body mass, with a conspicuous ‘breakpoint’ around the time of birth, manifest not by a change in the scaling exponent (slope), but rather a jump in the elevation. Fetal heart mass (g) increased with eviscerated body mass (M b , kg) according to the power equation 4.90 M b 0.88 ± 0.26 (± 95{\%} CI ) , whereas postnatal heart mass increased according to 10.0 M b 0.88 ± 0.10 . While the fetal and postnatal scaling exponents are identical (0.88) and reveal a clear dependence of heart mass on body mass, only the postnatal exponent is significantly less than 1.0, indicating the postnatal heart becomes a smaller component of body mass as the body grows, which is a pattern found frequently with postnatal cardiac development among mammals. The rapid doubling in heart mass around the time of birth is independent of any increase in body mass and is consistent with the normalization of wall stress in response to abrupt changes in volume loading and pressure loading at parturition. We discuss variation in scaling patterns of heart mass across development among mammals, and suggest that the variation results from a complex interplay between hard-wired genetics and epigenetic influences.",
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