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The role of female reproductive history in determining variation in cortical bone remodeling and trabecular architecture in a nonhuman animal model (Papio hamadryas)

  • Author(s): Lipps, Ashley Nicole
  • Advisor(s): Agarwal, Sabrina C
  • et al.
Abstract

This study investigates variance in bone quality and quantity with respect to site, sex, and female reproductive history in a model species, baboons. Three sites are examined: 1) the midshaft humerus, 2) the midshaft femur, and 3) the L1 vertebra. A total of 109 individuals are included in the humerus analyses, 76 in the femur analyses, and 24 in the lumbar analyses. Intracortical remodeling at the midshaft humerus and femur is assessed through static histomorphometry and trabecular architecture of the lumbar vertebra is assessed through micro-CT. Analyses of bone micro and macrostructural variance reveal significant trends.

Site-specific patterns are observed between the humerus and femur in baboons. Most notably: high porosity, percent osteonal bone, and low adjusted cortical area characterize the midshaft humerus as significantly more remodeled and porous than the midshaft femur. Significant sex differences are also observed. At the midshaft humerus, males grow larger osteons and Haversian canals but have lower overall activation of remodeling whereas females have increased secondary osteon activity (e.g. higher osteon population density, and percent osteonal bone) but exhibit smaller osteons and Haversian areas.

Some of the variance observed in females is related to reproductive history. At both the midshaft humerus and femur, osteon sizes are increased in high parity females, and this may be related the cumulative exposure to elevated estrogen levels during multiple pregnancies, as estrogen has been observed experimentally to increase osteoblast activity and decrease osteoclast functioning. Percent porosity at the midshaft humerus is also observed to be significantly higher in females with high lactation histories. Short-term cortical porosity during lactation has been observed in several animal model species (e.g. rat, dog), typically with only partial recovery. Here, the high porosity in females with high lactation histories suggests that full recovery from short-term lactation-related resorption is incomplete, resulting in increased porosity in the long-term. However, despite the increased intracortical porosity in high-lactation females, significant increases in total and cortical cross-sectional areas are seen at the humerus and femur. Increased periosteal apposition during pregnancy (or retrospectively with parity) at appendicular sites has also been observed in macaques, rats, and humans and here, the behavioral aspects of infant-rearing associated with long periods of juvenile care and nursing also appear to increase the outer cortex (periosteum) of the humerus and femur. The inverse reproductive-specific relationship of periosteal deposition with increased endosteal resorption may have an adaptive mechanical significance. Endocortical resorption results in a decrease in mechanical strength of cortical bone and the increases in periosteal apposition and overall cross-sectional area may help protect the maternal skeleton from fracture during this catabolic period. As long as periosteal apposition continues, the effects of increased intracortical porosity should not have detrimental effects on overall cortical bone health and fracture. Therefore, the overall effects of high parity and lactation on appendicular cortical bone health seen here in the humerus and femur are theoretically neutral.

Analyses here also revealed a potentially interesting relationship between lactational history and lumbar trabecular architecture. The female with the highest lactation history (34% of her life was spent nursing) exhibits abnormally high trabecular spacing, and abnormally low trabecular number and connectivity. Although short-term pregnancy-related changes observed here as well as in rats and humans show increased trabecular number and connectivity, the large resorption of cancellous bone that occurs during multiple cycles of long lactation appear to deteriorate these "new" struts, leaving behind large spaces, a reduced number of trabeculae, and overall decreased connectivity. Although this particular female's trabecular spacing is high, and her connectivity is low, she exhibits a bone volume measurement in the normal range. Because bone volume has the most significant effects on bone strength and stiffness it is unclear if this outlier female's abnormal trabecular architecture puts her at a mechanical disadvantage. Therefore, the long-term effects of reproductive differences at the lumbar site studied here also appear to be neutral. However, both the short and long-term alterations observed in this study are based on a small number (n=3) of outliers and need to be more rigorously tested in a larger sample group.

According to evolutionary theory, females in an iteroparous species that produce multiple offspring over time (e.g. monkeys and humans) would have selectively evolved mechanisms to maintain the skeleton over an entire lifetime of reproduction to increase reproductive success and optimal offspring survival. If evolution favored mechanisms that conserve and repair skeletal tissues during these reproductive periods, there should be no or little detrimental effect to the skeleton in the long term. In this study, even though aspects of bone quality and quantity did show variance with respect to reproductive history, these changes likely do not have strong effects on bone fragility and fracture risk. Therefore, the overall effects of high parity and lactation on appendicular cortical bone health and trabecular quality and quantity seen here are theoretically neutral. However, mechanical testing was not directly carried out in this study. Future work investigating both cortical and trabecular micro-architectural changes with reproductive history should include mechanical testing of specimens to clarify how these specific combinations of microstructural and macrostructural alterations affect bone fragility and fracture risk.

The approaches used in this dissertation advance biological anthropology and bone science by implementing thorough examinations of age, sex, and female reproductive history with respect to micro and macrostructural difference in cortical and trabecular bone. This study also contributes methodologically by demonstrating the importance of using multiple lines of evidence when exploring variance in bone quality and quantity.

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