Calcaneal Quantitative Ultrasound Indicates Reduced Bone Status Among Physically Active Adult Forager-Horticulturalists

Abstract

Sedentary lifestyle contributes to osteoporosis and fragility fracture risks among modern humans, but whether such risks are prevalent in physically active pre-industrial societies with lower life expectancies is unclear. Osteoporosis should be readily observable in pre-industrial societies if it was regularly experienced over human history. In this study of 142 older adult Tsimane forager-horticulturalists (mean age±SD=62.1±8.6, range=50-85, 51% female) we use calcaneal quantitative ultrasonography (qUS) to assess bone status, document prevalence of adults with reduced bone status, and identify factors (demographic, anthropometric, immunological, kinesthetic) associated with reduced bone status. Men (23%) are as likely as women (25%) to have reduced bone status, although age-related decline in qUS parameters is attenuated for men. Adiposity and fat-free mass positively co-vary with qUS parameters for women but not men. Leukocyte count is inversely associated with qUS parameters controlling for potential confounders; leukocyte count is positively correlated within adults over time, and adults with persistently low counts have higher adjusted qUS parameters (6-8%) than adults with a high count. Reduced bone status characteristic of osteoporosis is common among active Tsimane with minimal exposure to osteoporosis risk factors found in industrialized societies, but with energetic constraints and high pathogen burden.

Growth references for Tsimane forager‐horticulturalists of the Bolivian Amazon

“…On the one hand, a clinical model might argue that any growth deficit relative to standards is evidence of suffering, and a failure of a child to “adapt” to disease. On the other, an adaptationist perspective might suggest that small stature can be adaptive due to reduced energy demands, improved thermoregulation, or faster maturation (Stinson, 1990; Walker et al, 2006; Migliano et al, 2007), or that overall smaller stature in Amazonians may represent an adaptation to high pathogen load, and the need to prioritize energy for immune defenses (Blackwell et al, 2016; Gurven et al, 2016b; Stieglitz et al, 2016; Urlacher et al, 2016a)…”

“…In general Tsimane children are short and lean, but have low rates of wasting and arm muscularity similar to US children, suggesting adequate protein (Foster et al, 2005). However, stunting is prevalent (Gurven, 2012), and low bone mineral density suggests the possibility of micronutrient deficiencies (Stieglitz, Beheim, Trumble, Madimenos, Kaplan, & Gurven, 2015;Stieglitz, Madimenos, Kaplan, & Gurven, 2016). Tsimane are a natural fertility population, with a total fertility rate of 9.1 births per woman (Blackwell, Tamayo, Beheim, Trumble, Stieglitz et al, 2015;Gurven, Kaplan, & Supa, 2007; McAllister, ; women breastfeed their infants on-demand, weaning at 19 months on average (Veile et al, 2014).…”

Horticultural activity predicts later localized limb status in a contemporary pre‐industrial population

“…Whether low bone mass is prevalent in physically active pre‐industrial populations with lower life expectancies and greater nutritional stress, pathogen burden and fertility is an open question. Several recent studies of Tsimane forager‐horticulturalists of lowland Bolivia, the population studied here, found reduced indices of calcaneal stiffness among Tsimane compared with more sedentary American matched controls, and more rapid age‐related stiffness decline among older adult Tsimane compared with Americans, Chinese, Dutch, and Germans (Stieglitz, Beheim, Trumble, Madimenos, Kaplan, & Gurven, ; Stieglitz, Madimenos, Kaplan, & Gurven, ). Relatedly, analysis of skeletal remains reveals that Australian hunter‐gatherers exhibit reduced limb cortical area compared with more sedentary populations (i.e., Khoi‐San, Zulu, African American; Carlson, Grine, & Pearson, ), indicating that increased postcranial thickness is not a hallmark of hunter‐gatherers.…”

“…Women's SOS undergoes accelerated declines around the age at menopause, presumably due to associated changes in mineral regulating hormones (e.g., estrogen, progesterone). Steeper age‐related declines in women's bone strength appears to be a species‐typical pattern (Khosla, ; Stieglitz et al, ), although whether women in contemporary pre‐industrial populations present different cross‐sectional bone geometric properties and increased fragility fracture risk remains unexplored. Consistent with P1 we found that women's radial SOS declines by 0.56 SDs/decade (2.5%), which is greater than their tibial SOS decline of 0.25 SDs/decade (0.9%).…”

“…Third, bio‐archaeological studies often rely on imprecise age estimates, and, fourth, lack direct measures of physical activity and anthropometric status. Fat mass, for example, can affect bone structure independently of loading patterns (e.g., via aromatization of androgens to estrogen) (Ho‐Pham, Nguyen, & Nguyen, ) and may be more strongly associated with bone structure for women than men (Stieglitz et al, ). Fifth, multiple skeletal sites are rarely measured for the same individual, and thus individuals cannot act as their own controls, increasing the likelihood that factors other than activity patterns influence bone structure.…”