Circum-menarcheal bone acquisition is stress-driven: A longitudinal study in adolescent female gymnasts and non-gymnasts Karen L. Troy a,⇑ , Tamara A. Scerpella b , Jodi N. Dowthwaite c,d a Department of Biomedical Engineering, Worcester Polytechnic Institute, Worcester, MA, United States b Department of Orthopedics & Rehabilitation, University of Wisconsin – Madison, Madison, WI, United States c Department of Orthopedic Surgery, SUNY Upstate Medical University, Syracuse, NY, United States d Department of Anthropology, Binghamton University, Binghamton, NY, United States article info Article history: Accepted 9 July 2018 Available online xxxx Keywords: Pediatric Bone accrual Exercise loading Quantitative computed tomography FEA abstract Mechanical loading through youth exercise is highly modifiable and represents a strategy to maximize peak adult bone mass, with the potential for broad implementation across the population to lower frac- ture risk. For girls, circum-menarcheal growth is critical, with around 50% of adult bone acquired over a 4-year period. Here, we prospectively followed 10 gymnasts and 12 age-matched non-gymnasts across approximately 4 years circum-menarche. A combination of pQCT and subject-specific finite element models were used to measure differences in bone acquisition and structure between the groups, and to determine the degree to which specific mechanical factors predict change in bone structure. At base- line, gymnasts had stronger bone, including 26% higher BMC, 51% greater compressive strength, and 21% higher trabecular density. Over the study period, both groups more than doubled their bone strength. Pre-menarcheal principal stresses predicted change in pQCT variables for non-gymnasts, but not gymnasts. The bone of non-gymnasts became more asymmetrical than the bone of gymnasts. Our results suggest that exposure to the diverse, intense mechanical signals of gymnastic loading during adolescence imparts substantial benefits to bone geometry and mechanical function. Specifically, the bone of gym- nasts is better able to resist loading from multiple directions, and operates with a higher factor of safety compared to non-gymnasts. Ó 2018 Elsevier Ltd. All rights reserved. 1. Introduction In women, 80–90% of peak adult bone mass is accrued by age 16 (Henry et al., 2004), with approximately 40% of mass acquired dur- ing four circum-menarcheal years (McKay et al., 1998). High peak bone mass early in adulthood is associated with a life-long reduc- tion in fragility fracture risk (Hernandez et al., 2003). Thus, the circum-menarcheal years (2 years pre-menarche to 2 years post- menarche) provide a critical window for maximizing bone mass and strength. Bone strength arises from a complex combination of factors including bone mass, macro- and micro-structure, mineralization, and fracture toughness (Fonseca et al., 2014). Each of these factors changes rapidly during growth and adolescence. Mechanical load- ing through youth exercise is highly modifiable and represents a strategy to maximize adult bone strength, with the potential to be implemented broadly across the population to lower fracture risk. Loading induces deformation within the skeleton, initiating a cascade of biochemical signals that result in bone adaptation (Chen et al., 2010). In healthy individuals, this includes modest increases to bone mass and structure, resulting in substantial increases to strength (Vainionpaa et al., 2007). These structural adaptations strengthen bone efficiently to resist the specific mechanical environment to which it is habitually exposed. While it is well-established that mechanical loading elicits ben- eficial adaptations in bone structure (Meakin et al., 2014), it is not well understood how structural changes during adolescence are influenced by mechanical loading. Exposure to physical activities with high and impact loads during growth is associated with both general and site-specific adult advantages in the lower extremity (Dolan et al., 2006; Weeks and Beck, 2008), upper extremity (Kontulainen et al., 2003), and lumbar spine bone mass (Dowthwaite et al., 2011a, 2011b). Gymnastics participation is associated with greater bone strength metrics across a variety of populations (Burt et al., 2013a, 2013b; Krahenbuhl et al., 2018). Recreational gymnasts, https://doi.org/10.1016/j.jbiomech.2018.07.017 0021-9290/Ó 2018 Elsevier Ltd. All rights reserved. ⇑ Corresponding author. Department of Biomedical Engineering, 100 Institute Road, Worcester, MA 01609, United States. E-mail address: ktroy@wpi.edu (K.L. Troy). Journal of Biomechanics xxx (2018) xxx–xxx Contents lists available at ScienceDirect Journal of Biomechanics journal homepage: www.elsevier.com/locate/jbiomech www.JBiomech.com Please cite this article in press as: Troy, K.L., et al. Circum-menarcheal bone acquisition is stress-driven: A longitudinal study in adolescent female gym- nasts and non-gymnasts. J. Biomech. (2018), https://doi.org/10.1016/j.jbiomech.2018.07.017