PhD project: Microscopic markers of biorhythms in human juvenile hand tissue
Bodily growth is controlled by biological rhythms, some of which leave permanent markings in the internal structure of teeth. By comparing the age-related changes in bone microstructure to the markings retained in the teeth, information about the biorhythms control over growth can be obtained. In her PhD, Rosie intends to explore the link between biorhythms and the growth of bones and teeth in juveniles, and how an individual's particular biorhythm affects both their enamel development and their bone growth. This will further understanding of modern human growth and its control.
Prior to starting this project, Rosie obtained a BSc in Biological Anthropology and an MSc by Research in Anthropology, both from the University of Kent. Her undergraduate dissertation focused on the sex differences in the distribution of osteoarthritis, and her Master’s research examined the microscopic changes within the humerus during the juvenile growth period.
Dora Harvey Memorial Research Scholarship.
Pitfield, R., Miszkiewicz, J. and Mahoney, P. (2019). Microscopic markers of an infradian biorhythm in human juvenile ribs. Bone [Online] 120:403-410. Available at: https://doi.org/10.1016/j.bone.2018.11.019.Recent studies have indicated that there may be an infradian systemic biorhythm
that coordinates aspects of human hard tissue growth and influences adult body size. Here we
investigate if evidence of this biorhythm retained in human teeth as the periodicity of Retzius
lines (RP) corresponds with the microstructural growth of a non-weight bearing bone, the rib,
in a sample of 50 human juvenile skeletons. Using static histomorphometric methods, the RP
of one permanent tooth from each skeleton was calculated and combined with measures of
bone remodeling in a rib from the same individual. Results provide the first evidence that the
infradian biorhythm is linked to bone remodeling in children. Retzius periodicity was
negatively correlated with relative osteon area (r = -0.563, p = 0.008) and positively related to
Haversian canal area (r = 0.635, p = 0.002) and diameter (r = 0.671, p = 0.001) in children
between the age of 8 to 12 years. There was also a negative correlation between RP and the
relative cortical area of ribs (r = -0.500, p = 0.048). Relationships between bone remodeling
and the biorhythm were much more variable in younger children. Results imply that as the
biorhythm speeds up there is increased bone deposition during remodeling of the rib, leading
to the larger osteonal lamellar bone areas and smaller Haversian canals in children between 8
and 12 years of age. Our results support the idea that there is an infradian biorhythm that
coordinates aspects of human hard tissue growth.
Pitfield, R., Deter, C. and Mahoney, P. (2019). Bone histomorphometric measures of physical activity in children from Medieval England. American Journal of Physical Anthropology [Online]. Available at: http://dx.doi.org/10.1002/ajpa.23853.Objectives: Histomorphometric studies show consistent links between physical activity patterns and the microstructure underlying the size and shape of bone. Here we adopt a combined bone approach to explore variation in microstructure of ribs and humeri related to physical activity and historical records of manual labor in skeletal samples of children (n=175) from medieval England. The humerus reflects greater biomechanically induced microstructural variation than the rib which is used here as a control. Variation in microstructure is sought between regions in England (Canterbury, York, Newcastle), and between high- and low-status children from Canterbury.
Materials and Methods: Thin-sections were prepared from the humerus or rib and features of bone remodeling were recorded using high-resolution microscopy and image analysis software.
Results: The density and size of secondary osteons in the humerus differed significantly in children from Canterbury when compared to those from York and Newcastle. Amongst the older children, secondary osteon circularity and diameter differed significantly between higher and lower status children.
Discussion: By applying bone remodeling principles to the histomorphometric data we infer that medieval children in Canterbury engaged in less physically demanding activities than children from York or Newcastle. Within Canterbury, high-status and low-status children experienced similar biomechanical loading until around seven years of age. After this age low-status children performed activities that resulted in more habitual loading on their arm bones than the high-status children. This inferred change in physical activity is consistent with historical textual evidence that describes children entering the work force at this age.
Fahy, G. et al. (2017). Bone deep: variation in stable isotope ratios and histomorphometric measurements of bone remodelling within adult humans. Journal of Archaeological Science [Online] 87:10-16. Available at: https://doi.org/10.1016/j.jas.2017.09.009.Stable carbon (?13C) and nitrogen (?15N) isotope studies of ancient human diet increasingly sample several skeletal elements within an individual. Such studies draw upon differences in bone turnover rates to reconstruct diet during different periods of time within an individualâs lifetime. Rib and femoral bone, with their respectively fast and slow remodeling rates, are the bones most often sampled to reconstruct shorter and longer term signals of diet prior to death. It is poorly understood if ?13C and ?15N vary between bone types within a single individual, or if this variation corresponds with bone turnover rate (BTR). Here, we determined ?13C and ?15N for ten different bones from ten adult human skeletons (n=5 males; n=5 females). Isotope values were compared to the rate that each bone remodeled, calculated from osteon population (OPD) density. Results reveal that isotope ratios varied within each skeleton (?13C: max= -1.58â°; ?1542 N: max= 3.05â°). Humeri, metacarpals, and ribs had the highest rate of bone remodelling; the occipital bone had the lowest. A regression analyses revealed that higher rates of bone remodeling are significantly and negatively correlated with lower ?15N. Our results suggest that the occipital bone, with its slow rate of bone renewal, may prove useful for isotopic studies that reconstruct diet over longer periods of time within an individualâs lifetime. Isotope studies that compare individual skeletal elements between populations should standardize their methodology to bones with either a slow or fast turnover rate.
Pitfield, R., Miszkiewicz, J. and Mahoney, P. (2017). Cortical histomorphometry of the human humerus during ontogeny. Calcified Tissue International [Online] 101:148-158. Available at: http://dx.doi.org/10.1007/s00223-017-0268-1.Modeling and remodeling are two key determinants of human skeletal growth though little is
known about the histomorphometry of cortical bone during ontogeny. In this study we
examined the density and geometric properties of primary and secondary osteons (osteon area
and diameter, vascular canal area and diameter) in sub-periosteal cortical bone from the human
humerus (n=84) between birth and age 18 years. Sections were removed from the anterior
midshaft aspect of humeri from skeletons. Age-at-death was reconstructed using standard
osteological techniques. Analyses revealed significant correlation between the
histomorphometric variables and age. Higher densities of primary osteons occurred between
infancy and seven years of age but were almost completely replaced by secondary osteons after
14 years of age. The geometry of primary osteons was less clearly related to age. Secondary
osteons were visible after two years of age, and reached their greatest densities in the oldest
individuals. Osteon size was positively but weakly influenced by age. Our data implies that
modeling and remodeling are age dependent processes that vary markedly from birth to
adulthood in the human humerus.
Mahoney, P. et al. (2017). Enamel biorhythms of humans and great apes: the Havers-Halberg Oscillation hypothesis reconsidered. Journal of Anatomy [Online] 230:272-281. Available at: http://dx.doi.org/10.1111/joa.12551.The Havers-Halberg Oscillation (HHO) hypothesis links evidence for the timing of a biorhythm retained in permanent tooth enamel (Retzius periodicity) to adult body mass and life history traits across mammals. Potentially, these links provide a way to access life history of fossil species from teeth. Recently we assessed intra-specific predictions of the HHO on human children. We reported Retzius periodicity (RP) corresponded with enamel thickness, and cusp formation time, when calculated from isolated deciduous teeth. We proposed the biorhythm might not remain constant within an individual. Here, we test our findings. RP is compared between deciduous second and permanent first molars within the maxillae of four human children. Following this, we report the first RPs for deciduous teeth from modern great apes (n = 4), and compare these with new data for permanent teeth (n = 18) from these species, as well as with previously published values. We also explore RP in teeth that retain hypoplastic defects. Results show RP changed within the maxilla of each child, from thinner to thicker enameled molars, and from one side of a hypoplastic defect to the other. When considered alongside correlations between RP and cusp formation time, these observations provide further evidence that RP is associated with enamel growth processes and does not always remain constant within an individual. RP of 5 days for great ape deciduous teeth lay below the lowermost range of those from permanent teeth of modern orangutan and gorilla, and within the lowermost range of RPs from chimpanzee permanent teeth. Our data suggest associations between RP and enamel growth processes of humans might extend to great apes. These findings provide a new framework from which to develop the HHO hypothesis, which can incorporate enamel growth along with other physiological systems. Applications of the HHO to fossil teeth should avoid transferring RP between deciduous and permanent enamel, or including hypoplastic teeth.
Conference or workshop item
Mahoney, P. et al. (2017). Biorhythm tracks enamel thickness in humans and great apes. in: The 86th Annual Meeting of the American Association of Physical Anthropologists. WILEY-LISS, DIV JOHN WILEY & SONS INC. Available at: http://meeting.physanth.org/program/2017/session28/mahoney-2017-biorhythm-tracks-enamel-thickness-in-humans-and-great-apes.html.Although evidence of a biorhythm retained in tooth enamel as Retzius periodicity (RP) was identified in the 19th century its significance for mammalian growth and life history has only recently been discovered. This study builds upon our recent work where we hypothesised the biorhythm may have a role in enamel growth, and that its periodicity may change from deciduous to permanent teeth. Here we test this hypothesis. We compare RP between deciduous second and permanent first molars within the maxillae of four human children. We report the first RPâs for deciduous teeth from modern great apes (n=4), and compare these to new data for permanent teeth (n=18) from these species, as well as to previously published values. Results show RP changed within the maxilla of each child, from thinner to thicker enameled molars. RP of 5 days for great ape deciduous teeth lay below the lowermost range of those from permanent teeth from modern orangutan and gorilla, and within the lowermost range of RPâs from chimpanzee permanent teeth. When considered alongside our earlier reported correlation between RP and formation time, these observations provide further evidence that RP is associated with enamel growth processes in humans, and can change from deciduous to permanent teeth within an individual. Our data suggest these associations might extend to great apes. We conclude that enamel growth should be considered alongside other physiological systems when developing predictions around RP as a measure of an underlying biorhythm.
Mahoney, P. et al. (2016). Biorhythms, deciduous enamel thickness, and primary bone growth in modern human children: a test of the Havers-Halberg Oscillation hypothesis. in: The 85th Annual Meeting of the American Association of Physical Anthropologists (2016). Wiley. Available at: http://meeting.physanth.org/program/2016/session12/mahoney-2016-biorhythms-deciduous-enamel-thickness-and-primary-bone-growth-in-modern-human-children-a-test-of-the-havers-halberg-oscillation-hypothesis.html.Across mammalian species, the periodicity with which enamel layers form (Retzius periodicity) in permanent teeth corresponds with average body mass and the pace of life history. According to the Havers-Halberg Oscillation hypothesis (HHO), Retzius periodicity (RP) is a manifestation of a biorhythm that is also expressed in lamellar bone. Potentially, these links provide a basis for investigating aspects of a speciesâ biology from fossilized teeth. Here, we tested intra-specific predictions of this hypothesis on skeletal samples of modern human juveniles. We measured daily enamel growth increments to calculate RP in deciduous molars (n=25). Correlations were sought between RP, molar average enamel thickness (AET), and the average amount of primary bone growth in humeri from age-matched juveniles.
Results show a previously un-described relationship between RP and enamel thickness. Reduced major axis regression reveals RP is significantly and positively correlated with AET, and scales isometrically. The scaling relationship could not be explained through body mass. Juveniles with higher RPs and thicker enamel had more primary bone formation, which suggests a coordinating biorhythm. However, the direction of the correspondence was opposite to that predicted by the HHO. Next, we compared RP from deciduous molars to new data for permanent molars, and previously published values. The lowermost RP of four and five days in deciduous enamel was less than the lowermost value of six days in permanent enamel. A lowered range of RP values in deciduous enamel indicates that the underlying biorhythm might change with age. Our results develop the HHO.
Pitfield, R. (2015). Ontogenetic perspectives on modern human long bone growth: the humerus.Biological anthropologists routinely infer ancient human behaviour from macroscopic skeletal markers, although the underlying relationship between bone growth and functional adaptation remains complex. To date, few studies have undertaken a microstructural analysis of bone plasticity in relation to ontogeny. The primary aim of this study is to map histological changes within the humerus with age. If the histological changes have a strong correlation with age then it will be possible to produce a regression equation to predict juvenile age-at-death. This is the secondary aim of the study. The final aim is to ascertain how bone robusticity influences bone growth, within age-matched juveniles.
A sample of 83 juvenile skeletons from St. Gregoryâs Priory, Canterbury were aged using standard methods. One 0.5 cm histological section was removed from the anterior humeral midshaft of each skeleton. Histological slides were prepared using standard methods. The density and morphometrics of primary osteons and secondary osteons were recorded using a high resolution microscope.
Results show that primary osteon population density has a strong negative correlation with age (rs = -0.672, N = 83, p < 0.0005). Secondary osteon population density has a strong positive correlation with age (rs = 0.878, N = 83, p < 0.0005). A regression equation to estimate age at death from primary and secondary osteon population density was produced. The equation can be used to estimate juvenile age-at-death, between 0 - 17 years of age, with 86.1% accuracy. In an age matched sub-group robusticity was found to have a negative correlation with secondary osteon population density (rs = -0.642, N = 35, p < 0.001).
Walker, M. et al. (2019). Chapter 3: Ancient human bone microstructure case studies from Medieval England. in: Miszkiewicz, J. J., Brennan-Olsen, S. and Riancho, J. A. eds. Bone Health: A Reflection of the Social Mosaic. Springer. Available at: http://dx.doi.org/10.1007/978-981-13-7256-8.