What’s in an Age? [Guest post from Dr. Alice Gooding, Kennesaw State University]

We are happy to present a guest post from Dr. Alice Gooding, Assistant Professor of Anthropology at Kennesaw State University, and recent graduate of The University of Tennessee Anthropology doctoral program.

“Age is just a number. It's totally irrelevant unless, of course, you happen to be a bottle of wine.” 

-Dame Joan Collins

 Even wine bottles succumb to the effects of gravity, loading, and failure. Picture reproduced from https://hiveminer.com/Tags/bottle%2Cshatter.

Even wine bottles succumb to the effects of gravity, loading, and failure. Picture reproduced from https://hiveminer.com/Tags/bottle%2Cshatter.

Nothing is perhaps more universal than the dread that approaches with any birthday after the age of, say, 21. After all, we love to celebrate those adult milestones with black balloons, a tombstone cake, and a cheerful birthday card that exclaims, “It’s all downhill from here!” While I may be a few years shy of an over the hill-themed birthday party*, I have recently been investigating this supposed, yet inevitable, downward spiral. Are we really doomed to mechanical and material breakdowns in our skeletons shortly after we reach adulthood?

On the first day of osteology class (when I was a young, spry graduate student), the professor summarized the lifespan of the skeleton as such:

“The human skeleton grows and develops until fusion commences in the mid-20s. From there, the bones begin to deteriorate. There is no middle age for the skeleton.”

This summary, while not entirely untrue, typifies our cultural perspective regarding skeletal aging. In fact, I would argue that this notion has saturated our understanding of skeletal health to the point of hopelessness. Clinically, bone quality (i.e. deterioration) is most commonly assessed by two measures of bone mass, bone mineral density (BMD) and bone mineral content (BMC). Measured with a dual-energy absorptiometry (DEXA) scanner, BMC is the sum of density across the skeleton, while BMD is the amount of mineral content in a location of interest. Exercise and dietary interventions may slow the loss of bone, but in the end, biology will win. For females in particular, the message seems clear: osteopenia, and its more advanced form, osteoporosis, are waiting for you as the years go on.

It is true that bone loss with age in humans is nearly universal. It has been documented worldwide in both living and past populations, as well as non-human primates. And though bone loss may begin after bones fuse, it accelerates during mid-life (after age 40) and continues after mid-life in humans. Increased bone loss is concurrent with an increased risk of fracture, decreased mobility, and even in industrialized societies, increased mortality. It is prudent, then, to question why humans live long past the years when bone loss begins.

A Matter of Mismatches and Trade-offs

Our species appears to have reached an evolutionary mismatch, in which osteoporosis has become the most common systemic skeletal condition associated with increasing age (Imel et al. 2004). Two related factors likely contribute to the problem: longevity and inactivity. First, with modern advances in healthcare, humans are expressing trade-offs previously less frequently encountered simply as a result of average increased lifespans. Because significant bone loss with age has been documented in non-human primates (Burr 1980), it’s possible that bone loss may have affected early humans if they had lived longer lives. However, in early hominin species, including archaic Homo sapiens, activity levels were much higher during adolescence and early adulthood than those encountered in post-industrial groups. Theoretically, this would have established a greater reservoir of bone tissue for later in life (Lieberman 2013). An increasingly sedentary lifestyle only makes worse the issue of a potential mismatch between skeletal health and longevity.

Past populations of anatomically modern humans generally do not demonstrate the same degree of bone loss, and those that do still appear to have had higher bone quality and lower fracture incidences than their age-matched industrialized counterparts (see Agarwal and Stout’s 2003 tome). Whether this is the result of differences in longevity, subsistence patterns, other environmental factors, or a combination of all of these is still unclear. Further, the morbidity and mortality associated with advanced bone loss and its co-morbidities seem maladaptive. While a longer life may be an adaptation to other biocultural needs, the increased frequency of osteoporosis and related bone diseases cannot be explained through conventional evolutionary models. For myself, this mismatch and seemingly inevitable deterioration of the skeleton raises a few questions. What exactly is deteriorating? Does bone mass capture skeletal senescence in a meaningful way? Is it possible that we’re not all falling apart?

Measuring a Different Kind of Strength

The definition of “bone strength” has not been consistent, as it has been used across clinical and anthropological literature to denote amount of bone mass, mineral density of the skeleton, and bone health (or risk of fracture). Mineral density can be a problematic indicator of risk, as values of density or mass are affected by the amount of adipose tissue over the site of collection, and reference samples are not available for all populations. Bone density differs between ancestral groups, which is understood to be a major determinant of peak bone mass.  As some anatomical regions experience fracture more commonly from a single overload (e.g., wrist), while others from many cycles of small loads (e.g., hip), measurements of density may not be the best predictors of failure.

   
  
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    Generalized stress-strain curve for cortical bone. Under loading, bone is able to resist deformation until it reaches a yield point, or the end of the material’s ability to return to its original shape (elastic deformation). Deformation past this point is considered to be plastic, or unable to return to its original form. When maximum strain and stress levels are reached, the material will fail. Young’s modulus (E) is the slope of the curve. It represents the bone’s ability to resist stress before strain results in failure. Figure adapted from Martin et al. (2015)

Generalized stress-strain curve for cortical bone. Under loading, bone is able to resist deformation until it reaches a yield point, or the end of the material’s ability to return to its original shape (elastic deformation). Deformation past this point is considered to be plastic, or unable to return to its original form. When maximum strain and stress levels are reached, the material will fail. Young’s modulus (E) is the slope of the curve. It represents the bone’s ability to resist stress before strain results in failure. Figure adapted from Martin et al. (2015)

Experimentally, bone strength has also been tested using basic properties of geometry and material properties. Mechanical strength and stiffness of cortical bone decline after 35 years and continue to reduce thereafter by two to five percent per decade. Bone mineralization increases with age, causing older bone to be weaker. This fact, along with increased porosity and slower bone turnover, contribute to a decrease in work to fracture, or a decrease in tensile plastic deformation (Burr and Turner 1999). There is a dramatic decrease in tissue integrity in the older adult years. Even slight loss in density is correlated with a larger decrease in strength. That is, over the span of a few adult years, bone mass may stay relatively the same but fracture risk increases exponentially due to decreasing density. This fact further evidences the incongruent relationship between BMD and bone strength.

Without the use of technology designed for living bodies, assessment of bone health in past populations necessitates a different set of parameters. Here, the utility of BMD is reduced, and instead, measures of mineralization, microarchitecture, and mechanical properties are used to evaluate bone quality (Grynpas 2003). Histological analyses demonstrate the number of remodeled osteons, which increase with age, as well as intra-osteonal modeling (; Peck and Stout 2007). Intra-osteonal modeling results in double osteons, which increase with age, while single osteons decrease after the third decade of life by 2.5% per decade. A decrease in muscle mass in both sexes starting in the third and fourth decades is likely correlated with this remodeling pattern in older adults.

Clearly BMD and BMC are not providing the whole picture, especially outside of the doctor’s office. If we relied on bone mass alone, I might be celebrating my next birthday with black balloons. As a primary descriptor of skeletal health in both past and modern populations, I think a more robust use of the “bone strength” should include all measureable factors that help resist bone failure. Although the definition of bone quality is not necessary universal, a more comprehensive evaluation of bone rigidity and resilience should include diachronic changes, targeted resorption and deposition, and geometric distribution of bone.

Shape Up or Get Out

Let’s propose a supplemental strategy for assessing bone health with age, one that might in fact show that while we may be losing mass, we may not be falling apart. Intrigued? Spoiler alert: we’re talking about bone shape.

Bone shape, as measured by diaphyseal cross-sectional geometry, seems to adapt a particularly interesting age-related pattern. In both adult males and females, long bone diaphyses demonstrate a pattern of subperiosteal apposition and endosteal resorption as age increases (Biver et al. 2016; Mays 2001; Ruff and Hayes 1982). The figure below shows an idealized model of a human long bone cross-section across the lifespan.  Medullary area and subperiosteal area both increase with age along the diaphyses of the, femur and, and the humerus and radius. Across studies, females consistently show greater rates of endosteal resorption, particularly after menopause. In both sexes, this relationship between age and resorption is linear and results in a decrease in cortical bone (but not necessarily bone bending rigidity).

   
  
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    This depicts periosteal expansion with age using an idealized model of a human long bone cross-section across the lifespan. Plus marks (+) indicate patterns of periosteal modeling, which increases with age and results in a net increase in total cross-sectional area. Dashes (-) indicate endosteal and intracortical resorption, causing expansion of the medullary cavity throughout life and a decrease in total cortical area in adulthood. This figure is adapted from Riggs et al. (2004), and van der Meulen and Carter (1999).

This depicts periosteal expansion with age using an idealized model of a human long bone cross-section across the lifespan. Plus marks (+) indicate patterns of periosteal modeling, which increases with age and results in a net increase in total cross-sectional area. Dashes (-) indicate endosteal and intracortical resorption, causing expansion of the medullary cavity throughout life and a decrease in total cortical area in adulthood. This figure is adapted from Riggs et al. (2004), and van der Meulen and Carter (1999).

Ruff and Hayes (1982) examined eleven locations across the diaphyses of the femur and tibia to find that maximum, minimum, and polar SMAs increased with age in the Pecos Pueblo archaeological collection. Although the individuals from Pecos Pueblo displayed the pattern of net bone loss as expected, an increase in SMAs meant that more bone was located farther from the centroid of the cross-section, increasing its rigidity. These results were sex and location-specific within each bone, likely as a result of differential loading conditions from sex-specific work roles within the culture. Martin and Atkinson (1977) found similar results in a modern autopsy collection, but only in males, possibly reflecting a difference in activity patterns between Pecos Pueblo and modern individuals.

So, what’s going on here? Ruff and Hayes suggested that this shape pattern is actually a structural compensation for loss in mass with age. That is, as the bone loses material, it shifts remaining tissue around to maintain the strongest possible structure. This is somatic adaptation at its finest. While your modern lifestyle is weakening your bones and lengthening your lifespan, your skeleton may be picking up the slack. Or, at least trying its best. 

All is Not Lost

While I won’t recommend that you stop eating your calcium chews or reaching for those 10,000 steps, I believe the take-home message is less bleak than we imagine. Examining bone shape and strength provide us with a more nuanced view of how our bone organ system is coping with the years. Structural compensation with age is certainly an interesting phenomenon, and one that I explore further in my recently completed dissertation. I won’t get into the results here, but I invite you to hear about the highlights at the upcoming meeting of the American Association of Physical Anthropologists. I’m betting Austin has an excellent selection of aged wines.

*As a measure of authorial transparency, I am 31. I will point out that the year of my birth, 1986, was a fantastic one for Bordeauxs. However, many winos recommend that the 1986s need another 10-15 years to reach their peak. I say, raise your glasses to aging!

References

Biver E, Perreard Lopreno G, Hars M, van Rietbergen B, Vallee JP, Ferrari S, Besse M, and Rizzoli R. 2016. Occupation-dependent loading increases bone strength in men. Osteoporosis International 27:1169-1179.

Burr D. 1980. The relationships among physical, geometrical and mechanical properties of bone, with a note on the properties of nonhuman primate bone. Yearbook of Physical Anthopology 1980(23):109.

Burr DB, and Turner CH. 1999. Biomechanical measurements in age-related bone loss. In: Rosen CJ, Glowacki J, and Bilezikian JP, editors. The Aging Skeleton. San Diego: Academic Press. p 301-314.

Grynpas M. 2003. The role of bone quality on bone loss and fragility. In: Agarwal S, and Stout S, editors. Bone Loss and Osteoporosis: An Anthropological Perspective. New York: Kluwer Academic/Plenum Publishers. p 33-46.

Imel E, Dimeglio L, and Burr D. 2014. Skeletal Disease and Treatment. In: Burr D, and Allen M, editors. Basic and Applied Bone Biology. Amsertdam: Academic Press. p 317-344.

Lieberman D. 2013. The Story of the Human Body: Evolution, Health, and Disease. New York: Patheon Books.

Martin RB, and Atkinson PJ. 1977. Age and sex-related changes in the structure and strength of the human femoral shaft. Journal of Biomechanics 10:223-231.

Martin R, Burr D, Sharkey N, and Fyhrie D. 2015. Skeletal tissue mechanics. New York: Springer.

Mays S. 2001. Effects of age and occupation on cortical bone in a group of 18th-19th century British men. American Journal of Physical Anthropology 116:34-44.

Peck JJ, and Stout SD. 2007. Intraskeletal variability in bone mass. American Journal of Physical Anthropology 132(1):89-97.

Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, and Khosla S. 2004. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. Journal of Bone and Mineral Research 19(12):1945-1954

Ruff CB, and Hayes WB. 1982. Subperiostealexpansion and cortical remodeling of the human femur and tibia with aging. Science 217(4563):945-948.

van der Meulen MCH, and Carter DR. 1999. Mechanical determinants of peak bone mass In: Rosen CJ, Glowacki J, and Bilezikian JP, editors. The Aging Skeleton. San Diego: Academic Press. p 105-114.