Stature and frailty during the Black Death: the effect of stature on risks of epidemic mortality in London, A.D. 1348–1350

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Abstract

Recent research has shown that preexisting health condition affected an individual's risk of dying during the 14th-century Black Death. However, a previous study of the effect of adult stature on risk of mortality during the epidemic failed to find a relationship between the two; this result is perhaps surprising given the well-documented inverse association between stature and mortality in human populations. We suggest that the previous study used an analytical approach that was more complex than was necessary for an assessment of the effect of adult stature on risk of mortality. This study presents a reanalysis of data on adult stature and age-at-death during the Black Death in London, 1348–1350 AD. The results indicate that short stature increased risks of mortality during the medieval epidemic, consistent with previous work that revealed a negative effect of poor health on risk of mortality during the Black Death. However, the results from a normal, non-epidemic mortality comparison sample do not show an association between stature and risks of mortality among adults under conditions of normal mortality. Fisher's exact tests, used to determine whether individuals who were growing during the Great Famine of 1315–1322 were more likely to be of short stature than those who did not endure the famine, revealed no differences between the two groups, suggesting that the famine was not a source of variation in stature among those who died during the Black Death.

Highlights

► We examine the relationship between stature and mortality during the Black Death. ► Stature was modeled as a covariate affecting the Gompertz model of adult mortality. ► Results suggest short stature was associated with elevated risks of dying during the Black Death. ► This provides further evidence that mortality during the Black Death was selective.

Introduction

Adult stature reflects, among other things, exposure to chronic stress during development (Haviland, 1967; Powell, 1988; Roberts and Manchester, 2005). According to Steckel (Steckel, 1995: 1903) stature is “a net measure that captures not only the supply of inputs to health but demands on those inputs.” Children who are malnourished or fighting infection and disease must expend precious energy resources in basic tissue maintenance and the immune response, diverting energy from growth and development to these most essential metabolic functions. Therefore short adult stature, relative to other individuals within the population, likely indicates poor health and poor nutrition during the developmental years, at least if everyone's genetic composition with respect to stature is similar.

In general, stature is positively correlated with health condition throughout an individual's life (Komlos and Baur, 2003), and inversely associated with risk of mortality (Gage and Zansky, 1995). In contemporary populations, tall people have greater reproductive success (Pawlowski et al., 2000) and survive longer than their short peers (Steckel, 1995; Gage and Zansky, 1995; Waaler, 1984), while short people are more likely to develop chronic diseases later in life, suffer from cardiovascular issues, and die young relative to tall peers (Deaton, 2007; Paajanen et al., 2010).

Bioarchaeological evidence tends to support the assertion that there is an inverse association between stature and mortality (Gunnell et al., 2001; Kemkes-Grottenthaler, 2005; Steckel, 2005; Watts, 2010), though not without exception (Usher, 2000; DeWitte and Wood, 2008). Gunnell et al. (2001) examined the association between stature and mortality in a skeletal sample from northeast England, dating from the 9th through the 19th centuries and found, for both males and females and for all long bones, the odds ratio of death before 30 years of age decreased as long bone length (a proxy for stature) increased. A one standard deviation increase in bone length was associated with a 10–20% decline in the risk of death before age 35, though the pattern was only statistically significant for overall bone length index (the mean of the z-scores for all long bones) and humeral length. Likewise, Kemkes-Grottenthaler (2005) found the odds of survival beyond age forty, for both males and females, increased by as much as 15% for each one standard deviation increase in bone length, for all long bones except the radius, in a European skeletal sample dating between 500 and 1900 A.D. Steckel (2005) explored the relationship between stature and mortality in an aggregate sample of skeletal remains from the Western hemisphere, dating between 4500 B.C. and the early 20th century and found that among 15–30 years olds, a five centimeter decrease in femur length was associated with a 4.6 percent decrease in the probability of survival. Recently, in a sample from northern England dating between the 10th and 15th centuries, Watts (2010) found that females who failed to survive beyond 25 years of age were significantly shorter than those who did, though there were no statistically significant results for males. On the other hand, Usher (2000) examined osteological material from a 12th century Danish cemetery from the village of Tirup using a multi-state model of health and mortality, and did not find an effect of femur length on risk of mortality.

One of the authors (SND) of this paper assessed the relationship between stature and risk of mortality in a previous study of the mortality patterns of the 14th-century Black Death (DeWitte and Wood, 2008). In that previous study, a variety of skeletal stress markers were examined to determine whether the Black Death was selective with respect to frailty or if preexisting health condition had no discernable effect on risk of death during the epidemic. The results indicated that people with cribra orbitalia, porotic hyperostosis, tibial periostitis, and enamel hypoplasia were more likely to die during the Black Death than their peers without these skeletal pathologies. Thus, it appears that in general, people in poor health before the epidemic were more likely than their healthier peers to die during the Black Death. However, the previous study failed to find an effect of adult femur length (which was used as a proxy for stature) on risk of death during the Black Death.

The previous study used a multi-state hazards model of morbidity and mortality (Usher, 2000) to evaluate the relationship between skeletal pathology and risk of mortality. This model has two living states, and the third state is death, to which everyone eventually transitions. The first living state, State 1, includes people without visible skeletal stress markers, and the other living state, State 2, includes people with stress markers. The transitions between each of the living states and death are determined by age-specific hazard rates. The model allows for the estimation of the differential risk of death associated with having skeletal stress markers, so it is possible to determine for a particular population whether people with stress markers were at higher or lower risks of mortality than their peers without stress markers. The model also includes a transition from State 1 to State 2. This transition, from a condition of not having a particular stress marker to developing the stress marker in response to physiological stress, is appropriate for stress markers such as enamel hypoplasia, porotic hyperostosis, cribra orbitalia, and periostitis, for which the transition from State 1 to State 2 can occur at various childhood or adult ages. However, femur length was assessed only for adults in the previous study – i.e., the analysis of the relationship between stature and mortality was restricted to people who had completed their growth. Because of this, it might not be necessary to include the transition from State 1 (in this case, average or above-average femur length) to State 2 (i.e., short femur) in order to understand how stature might have affected risks of mortality during the Black Death. Though there is certainly variation in achieved adult stature, for individuals who survive to adulthood, there is thereafter no risk (and thus no variation in the risk) of making the transition from State 1 to State 2 (i.e. from average or tall stature to short stature). It is possible that the previous study failed to find a relationship between stature and risk of mortality because it used an analytical approach that was unnecessarily complex for this particular stress marker.

The study presented here is a reanalysis of data on adult long bone length and age-at-death, using a simpler, and thus more appropriate analytical approach than that used in the previous study of the effect of stature on Black Death mortality. The approach used here has the benefit of requiring the estimation of fewer parameters; such a consideration is often important in paleoepidemiology given the relatively small sample sizes typical of bioarchaeological assemblages. The simpler model does suit the goals of this study, so we are therefore not sacrificing insight in favor of simplicity.

To further our understanding of the factors contributing to variation in adult stature and mortality risk within this population, we also examine variation in long bone length within East Smithfield with respect to year of birth to determine whether individuals who were growing (and thus highly vulnerable to malnutrition) during the Great Famine, 1315–1322, were discernibly shorter than others in the sample.

Section snippets

East Smithfield Black Death cemetery

The medieval Black Death skeletal material for this study comes from the East Smithfield cemetery in northeast London, near the Tower of London. The East Smithfield cemetery is one of only a few excavated cemeteries with both documentary and archaeological evidence clearly linking it to the 14th-century Black Death (Grainger et al., 2008).

The Black Death, which arrived in London through the port of Melcombe-Regis, Dorset, in the fall of 1348 (Gottfried, 1983; Horrox, 1994), ravaged the

Results

Table 1 shows the means and standard deviations for femur + tibia measurement, by sex, within the East Smithfield and Danish samples. Table 2 shows the estimated value of the parameter representing the effect of the stature covariate on the adult risk of mortality and the associated likelihood ratio tests. The positive value of the parameter for the East Smithfield sample indicates that during the Black Death, people who were relatively short were more likely than their taller peers to die

Discussion

The results of this study suggest that adult stature had an effect on an individual's risk of mortality during the Black Death such that shorter-than-average individuals were at an elevated risk of dying during the epidemic compared to people of average or above-average height. These results are consistent with those from a previous study that showed that various other skeletal indicators of physiological stress were associated with elevated risks of mortality during the epidemic (DeWitte and

Conclusion

The results of this study provide further evidence of a relationship between stature and risks of mortality, and specifically that short stature was associated with increased risks of mortality during the Black Death. This is consistent with previous research that has found short stature to be associated with increased risks of mortality in both living and past populations (e.g. Steckel, 1995; Gage and Zansky, 1995; Paajanen et al., 2010; Kemkes-Grottenthaler, 2005), and adds to existing

Acknowledgments

We thank Bill White (deceased), Jelena Bekvalac, and Rebecca Redfern at the Museum of London Centre for Human Bioarchaeology and Jesper Boldsen at the University of Southern Denmark for providing access to the East Smithfield and Danish skeletons and for generously providing the physical facilities for this work. Grant Sponsors: National Science Foundation (grant number BCS-0406252), The Wenner-Gren Foundation for Anthropological Research (grant number 7142), University at Albany Center for

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