Do bone geometric properties of the proximal femoral diaphysis reflect loading history, muscle properties, or body dimensions?

Abstract

Objectives: The aim of this study was to investigate activity-induced effects from bone geometric properties of the proximal femur in athletic vs nonathletic healthy females by statistically controlling for variation in body size, lower limb isometric, and dynamic muscle strength, and cross-sectional area of Musculus gluteus maximus. Methods: The material consists of hip and proximal thigh magnetic resonance images of Finnish female athletes (N = 91) engaged in either high jump, triple jump, soccer, squash, powerlifting, endurance running or swimming, and a group of physically active nonathletic women (N = 20). Cross-sectional bone geometric properties were calculated for the lesser trochanter, sub-trochanter, and mid-shaft of the femur regions. Bone geometric properties were analyzed using a general linear model that included body size, muscle size, and muscle strength as covariates. Results: Body size and isometric muscle strength were positively associated with bone geometric properties at all three cross-sectional levels of the femur, while muscle size was positively associated with bone properties only at the femur mid-shaft. When athletes were compared to nonathletic females, triple jump, soccer, and squash resulted in greater values in all studied cross-sections; high jump and endurance running resulted in greater values at the femoral mid-shaft cross-section; and swimming resulted in lower values at sub-trochanter and femur mid-shaft cross-sections. Conclusions: Activity effects from ground impact loading were associated with higher bone geometric values, especially at the femur mid-shaft, but also at lesser and sub-trochanter cross-sections. Bone geometric properties along the femur can be used to assess the mechanical stimuli experienced, where ground impact loading seems to be more important than muscle loading.

Muscle force interacts with stature to influence functionally related polar second moments of area in the lower limb among adult women

“…When inferred behavior differs distinctly, for example among foragers relative to farmers or industrialized populations, the former tend to exhibit higher size‐standardized mean midshaft femoral and tibial J, attributed to relatively higher terrestrial mobility (Bridges, Blitz, & Solano, 2000; Ruff et al, 1984). These inferences are supported by consistent and similar differences among living athletes relative to controls, where behavior is known (Macintosh & Stock, 2019; Niinimäki et al, 2019; Shaw & Stock, 2009a; Shaw & Stock, 2009b). However, our ability to infer more nuanced detail about the loading environment that has shaped patterns in limb bone structural variation in the past is limited by an inability to reconstruct more specifically the parameters exerting force on the bones during locomotor behaviors.…”

“…Biological anthropologists often utilize variation in limb bone diaphyseal cross‐sectional geometry (CSG) to infer patterns of loading in the past related to locomotion, mobility, and/or habitual behavior. The polar second moment of area (J) provides a measure of cross‐sectional bending and torsional rigidity and is often used in behavioral interpretations, as it is readily quantifiable from lower limb diaphyses in skeletal remains, can be estimated accurately from much of the periosteal contour alone (Macintosh, Davies, Ryan, Shaw, & Stock, 2013; Stock & Shaw, 2007), and varies substantially in relation to both inferred behavior (Marchi, 2008; Ruff et al, 2015; Ruff, Larsen, & Hayes, 1984; Stock & Pfeiffer, 2001) and known behavior (Macintosh, Pinhasi, & Stock, 2017; Macintosh & Stock, 2019; Niinimäki et al, 2019; Shaw & Stock, 2009a; Shaw & Stock, 2009b). Observed differences in lower limb bone J relative to known and inferred mobility derive from the responsiveness of bone surfaces to prevailing strain conditions (Garn, 1972; Gosman, Stout, & Larsen, 2011).…”

“…These high impacts have been associated with substantial bone functional adaptation in the lower limb, leading to increases of over 20% in midshaft tibial bone strength indices (BSIs) among triple jump athletes relative to controls (Heinonen, Sievänen, Kyröläinen, Perttunen, & Kannus, 2001). In contrast, sport‐specific loading regimes involving lower‐impact activities, for example power‐lifting or rowing, may not necessarily provide sufficient loading stimulus to enhance limb bone CSG properties among athletes relative to controls, despite substantial muscular effort (Macintosh & Stock, 2019; Niinimäki et al, 2017, 2019; Nikander, Sievänen, Uusi‐Rasi, Heinonen, & Kannus, 2006). In some instances, muscle activity explains more variance in bone strength parameters than sport‐related impact loading.…”

“…However, the importance of muscle activity in shaping lower limb bone strength parameters is such that some of the behavioral signature being inferred from skeletal variation, even among otherwise similarly‐sized individuals, may be attributable to variation in body composition , as well as age‐related changes in it. Body size variation is known to impact polar second moments of area through its influence on diaphyseal diameters, the amount of weight borne by the lower limb bones, the extent of mechanical stimulation on them during ground impact, the amount of contractile muscle tissue, and the lever arms about which that muscle tissue exerts bending and joint moments during movement (Niinimäki et al, 2019; Ruff, 2000; Ruff, 2018). As a result, many CSG properties scale with body mass (Parfitt, 1994; Seeman et al, 1996), and polar second moments of area must be standardized to bone length (a proxy for lever arm length) and estimated body mass prior to comparison among individuals and populations (Ruff, 2000; Ruff, 2008; Ruff, 2018).…”

“…Functional adaptation is influenced by a variety of loading‐related parameters such as weight‐bearing, body size and shape, ground reaction forces, muscle contractions, and the magnitude and frequency of loading (Niinimäki et al, 2019; Robling, 2009). Loading also modulates the normal sequence of bone deposition and resorption that is ultimately under biochemical regulation, involving reproductive hormones, growth hormones, and others (Gosman et al, 2011; Libanati, Baylink, Lois‐Wenzel, Srinvasan, & Mohan, 1999; Parfitt, 2002; Tanner, 1989).…”