Teeth getting worse due to lower level of vitamin D during the past 5,000 years

Many items including same author: Megan Brickley

Teeth, and vitamin D, getting worse since ancient times - June 2017

Ancient Vitamin D Deficiency – Long-Term Trends
Current Anthropology Volume 58, Number 3, June 2017
Megan B. Brickley, Lori D’Ortenzio, Bonnie Kahlon, Annabelle Schattmann, Isabelle Ribot, Emeline Raguin, and Benoit Bertrand
Department of Anthropology, McMaster University, Chester New Hall, Room 518, 1280 Main Street West, Hamilton, Ontario L8S 4L9, Canada (Brickley, D’Ortenzio, Kahlon, and Schattmann; brickley at mcmaster.ca)/Facultes des arts et des sciences, Departement d’Anthropologie, Succursale Centre- Ville, BP 6128, Montreal, Quebec H3C 3J7, Canada (Ribot and Raguin)/Unite de Taphonomie Medico-Legale, Universite de Lille 2 Droit et Sante, rue Andre Verhaeghe, 59000 Lille, France (Bertrand). This paper was submitted 8 VIII 16, accepted 23 I 17 and electronically published 18 V 17.
 Download the PDF from VitaminDWiki

Study was reviewed on the web

• Dentistry Today
• RR Magazine

Vitamin D deficiency is now widely recognized as one of the most common health conditions in the world, with important consequences for overall health. Levels of deficiency appear to be rising, but the extent to which past humans were affected by vitamin D deficiency and the roles of this hormone in past human health are currently unknown. The discovery that mineralization defects in tooth dentin reflect periods of deficiency and are preserved in our earliest ancestors offers a unique opportunity to provide information on past social and cultural organization and, with further work, to contribute to ongoing debates on change in skin pigmentation. Here we show that humans from some of the earliest Middle Eastern and European communities were affected by deficiency, but levels and severity appear to have increased notably through time. On a simple comparative scale, severity of deficiency was four times as high in Greek communities in 1948 CE as in early farming communities from ca. 3000 BCE; some individuals in the later periods would have had rickets. Research using interglobular dentin in humans and nonhuman primates has the potential to fill in many important gaps in understanding past and present aspects of vitamin D deficiency.

Vitamin D deficiency is now widely recognized as one of the most common health conditions in contemporary society, with over a billion individuals estimated to be affected worldwide (Robinowitz 2009). The prevalence of this deficiency is thought to be increasing in many regions (Robinson et al. 2006; Wharton and Bishop 2003), prompting considerable concerns about health consequences. There have been many claims regarding the health consequences of vitamin D deficiency (Peterlik xxx, and it is now clear that maintenance of adequate levels of vitamin D has an important effect on immune function (Wei and Christakos 2015) and development of some, but not all, neoplastic diseases (Jacobs et al. 2016). Vitamin D is synthesized in the skin that is exposed to natural light (ultraviolet B [UVB] radiation). A range of factors, including season and latitude, affect individual vitamin D levels (Brickley, Moffat, and Watamaniuk 2014; Robinowitz 2009). Vitamin D can be obtained from dietary sources, but few foods naturally contain the nutrient. Phytates, found in unprocessed nuts and grains, make calcium less biologically available and can be a vitamin D inhibitor (Chaplin and Jablonski 2009). Severe vitamin D deficiency results in skeletal deformity. Defects of growth plates of bones are termed “rickets,” and the term “osteomalacia” is often applied to defects in remodeled bone (Brickley, Moffat, and Watamaniuk 2014). The role of vitamin D in building and maintaining healthy bone is now established (Peterlik 2012; Robinowitz 2009).

Appreciation of the negative health consequences of vitamin D deficiency facing contemporary society has prompted consideration of both evolutionary (Holick 2003) and historical (Holick 2006) perspectives. In particular, the contribution that vitamin D synthesis has made to skin pigmentation has been much debated, with discussions surrounding the adaptive significance of skin pigmentation and protection from UV radiation damage (Jablonski 2012; Jablonski and Chaplin 2013; Robins 2009; Rossberg et al. 2016). Until recently it was widely thought that vitamin D deficiency and cases of rickets were not present before the Industrial Revolution (Holick 2003), but advances in the use of historical texts and skeletal paleopathology have shown these assumptions to be incorrect (Giuffra et al. 2015; Ortner and Mays 1998; Steinbock 1993). Among anthropologists it is widely assumed that vitamin D deficiency occurred only once humans left Africa (Jablonski and Chaplin XXX

. There are, however, still significant questions regarding the paleoepidemiology of vitamin D deficiency, and work on vitamin D metabolism in nonhuman primates (Ziegler et al. 2015) could assist in understanding the development of vitamin D metabolism in humans.
Further progress has been made with the publication of a paper by D’Ortenzio and colleagues (2016) that demonstrated that mineralization defects in dentin (interglobular dentin), found in both modern and archaeological teeth, are due to a disruption in the pathway or homeostasis of vitamin D, phosphate, or calcium. Quite a number of conditions can cause such disruptions, but most are rare, with many being incompatible with life without access to developed healthcare systems. By far the most common cause of mineralization defects in bones and teeth is vitamin D deficiency caused by inadequate UVB radiation (nutritional rickets; D’Ortenzio et al. 2016). Clearer information on the past occurrence of vitamin D deficiency provided by interglobular dentin would contribute to debates on varied skin pigmentation, migration and immigration, and long-term consequences of intrauterine and early infant health.

Evidence for Vitamin D Deficiency in the Past: Texts and Skeletal Paleopathology
Some skeletal changes will be visible in those living with severe rickets. Pathological changes that are attributable to rickets have been recognized in a number of early texts from around the world (Hess 1930). Strong indicators of vitamin D deficiency in children, such as leg deformities, have been identified in the writings of Soranus of Ephesus and Galen (both second century CE). Hess (1930:24) provides the following excerpt from a translation of Soranus’s work on gynecology and pediatrics: “If it stands or walks too early, the legs (especially the thighs) will become crooked.” The first clinical description was made by Whistler (1645), rapidly followed by Glisson’s (1650) classic description of what he believed to be a new disease, De Rachitide. In the nineteenth century, with the increasing urbanization associated with the Industrial Revolution, reports of rickets were widespread (Palm 1890). Cases continued to be reported in large cities of northern Europe and North America in the early twentieth century (Hess and Unger 1922). Texts offer a useful source of information on rickets in the past, but there are challenges in attempting retrospective diagnoses (Mitchell 2011). The key problem in investigating evolutionary aspects of vitamin D deficiency is that for much of human evolution there are no written sources available.
Skeletal paleopathology provides a more direct source of evidence on rickets (fig. 1). With the publication of clear diagnostic criteria (Mays, Brickley, and Ives 2006; Ortner and Mays 1998), cases of rickets have begun to be identified in past communities far beyond the geographic and temporal boundary of northern European cities during the Industrial Revolution (Brickley, Moffat, and Watamaniuk 2014). For example, rickets has now been identified in children from the high-status Medici court in sixteenth- and seventeenth-century Italy (Giuffra et al. 2015) and a seventeenth-to-nineteenth-century farming community from the Netherlands (Veselka, Hoogland, and Waters-Rist 2015). Recent research demonstrates that the occurrence of rickets is linked to a range of social and cultural variables and that there is considerable intracommunity variation (Brickley, Moffat, and Watamaniuk 2014). Care is therefore required in making interpretations when sample size is small. Cases of rickets provide a useful indication of levels of vitamin D deficiency within past communities, although skeletal paleopathology is not without its limitations, as discussed below (Brickley, Mays, and Ives 2010; Brickley, Moffat, and Watamaniuk 2014).

Skeletal paleopathology is unlikely to identify all individuals diagnosed as having vitamin D deficiency by using clinical serum 25(OH)D (25-hydroxyvitamin D) levels, limiting suggestions regarding relative levels of deficiency in past and present communities. Some of the limitations of serum 25(OH)D measurement and reporting are discussed by Ziegler and coworkers (2015). Another problem is that many individuals who survive periods of childhood deficiency may not be identified by skeletal paleopathology. Hess (1930) estimated that in cases of rickets with visible leg deformity, only 10%-25% of individuals retained these changes into adulthood. In paleopathology, where bone can be examined directly, bone deformity would probably be visible in more cases. The 25% retaining deformity into adulthood suggested by Hess can safely be taken as a minimum, but there is a strong possibility that growth, remodeling, and individual variation will preclude identification ofless severe cases. Where cases are identified, the number of episodes of vitamin D deficiency that occurred throughout the individual’s lifetime cannot be determined. It is clear that many cases, and details of cases observed, will be missed.
Evidence for Vitamin D Deficiency: Interglobular Dentin
Dentin defects found in teeth, interglobular dentin, will provide new means of investigating past episodes of vitamin D deficiency. Interglobular dentin is a sign of mineralization defects produced when calcospherites (tiny spherical deposits of calcium salts) do not grow sufficiently and fail to fuse, leaving poorly mineralized patches of dentin (Hillson 1996). It has recently been demonstrated that interglobular dentin is well preserved in archaeological teeth (fig. 2), and analysis of evidence for systemic mineralization defects that follow lines of incremental growth (Hillson 1996:190) can be used to determine the number and severity of periods of deficiency (D’Ortenzio et al. 2016). To date most work on microstruc- tural aspects of teeth has utilized histology: teeth have been embedded in resin and thin sections made. With polarized- light microscopy interglobular dentin can be observed in such sections (Hillson 1996; D’Ortenzio et al. 2016). The discovery of interglobular dentin, first described by Czermak (1850), marks the start of what could be the answer to unraveling evolutionary aspects of vitamin D deficiency. Mellanby (1929) demonstrated that interglobular dentin formed in the teeth of dogs with experimentally produced rickets, but vitamin D was poorly understood at this time (Steinbock 1993).
Although interglobular dentin has been identified in cases of rickets with a genetic cause (Seow, Romaniuk, and Sclavos 1989), the link between vitamin D deficiency and these defects was not fully appreciated. Dental anthropologists and those working in dental histology have long known that inter- globular dentin is not an uncommon finding in both archaeological and recent teeth (Hillson 1996).
Writing in 1956, Sognnaes (1956) noted the experimental work undertaken on dogs by Mellanby (1929) but attributed interglobular dentin to more general metabolic and nutritional stress. Working on nonhuman primates, Molnar and Ward (1975) regarded interglobular dentin as an important indicator of environmental stress, noting the importance of calcium and its balance with phosphorous. Ivanhoe (1982) was far less cautious, directly linking interglobular dentin to rickets. Ivan- hoe (1982) took the position that nutritional rickets was the cause of interglobular dentin, rather than reviewing all potential causes to demonstrate a link between vitamin D deficiency and interglobular dentin. Ivanhoe’s work came before the recent rise in interest in vitamin D deficiency that allowed the link between nutritional rickets and interglobular dentin to be established (D’Ortenzio et al. 2016). Unlike bone, dentin is not remodeled, meaning that interglobular dentin provides the perfect medium with which to explore evolutionary aspects of vitamin D deficiency. The value of interglobular dentin is now clear; it is a precise tool with which to evaluate vitamin D deficiency (D’Ortenzio et al. 2016).
With this new information, the importance of previously published research on interglobular dentin can now be reanalyzed. A search was undertaken for articles reporting data on interglobular dentin, using PubMed and relevant references from articles. Taken together with the current understanding of vitamin D deficiency, these data provide evidence of the date and extent of the occurrence of vitamin D deficiency in past societies and provide a clear foundation for future research.
Results and Discussion
Four reports on interglobular dentin in humans were identified; Sognnaes’s (1956) article on the histological structure of 233 teeth from 12 archaeological and modern collections covering a wide time depth is of particular importance. We took these data and added supporting information from Ivanhoe (1982), Molnar and Ward (1975), and our research (D’Ortenzio et al. 2016) to investigate the first reported appearance of these defects and temporal changes from the late Pleistocene to the twentieth century. Information provided in the papers considered are summarized in table 1. Direct comparisons are possible for the 110 teeth from Greece, dating from 3000 BCE to CE 1948, analyzed by Sognnaes (1956) with a semiquantitative scoring system, and these are shown in table 2.
Factors such as ozone concentration, earth-sun distance, and the obliquity of the earth’s axis have varied through time, affecting the amount of UV radiation reaching the earth’s surface (Chaplin and Jablonski 2009; Relethford 1997). There would have been slight changes in seasonal intensity of UVB radiation over the time periods represented by individuals considered in this paper. Type of clothing is another important determinant of the amount of UVB radiation that will reach the skin (Brickley, Moffat, and Watamaniuk 2014). The wide time depth and geographical distribution of sites in table 1 mean that there was considerable variation in clothing worn due to climatic conditions, technologies and materials available, and cultural preferences. There are many unknowns regarding material used in the study by Sognnaes (1956), and precise reconstruction of past UVB radiation levels, climatic conditions, and clothing types is not possible, but these variables should be kept in mind.
Reported Interglobular Dentin: The Late Pleistocene
The earliest evidence of vitamin D deficiency comes from Tabun and Skhul, late Pleistocene sites from Mount Carmel, Israel (table 1). This finding provides evidence that vitamin D deficiency has been present since very early time periods and is not just an issue faced by current communities. The total number of individuals from these early sites is, however, very small (n = 7). Four out of five disarticulated teeth analyzed from Tabun show some level of interglobular dentin. Two of these teeth, a first permanent mandibular molar and a first permanent maxillary incisor, were suggested to be Neanderthal (Sognnaes 1956). Records relating to the teeth are not sufficiently clear to establish whether they would be considered Neanderthal if subjected to current methods of analysis. Small interglobular spaces were reported in the molar but not in the incisor. Reported differences in age at death of the two individuals represented by these teeth indicate that they may have come from different individuals.
Table 1. Reported cases of interglobular dentin (IGD) in archaeological and modern teeth

The first permanent maxillary incisor and first mandibular molar have considerable overlap in development; in modern humans these teeth start developing approximately 3 months after birth and in utero, respectively (Gustafson and Koch 1974). Notes on the location of interglobular dentin in the molar (Sognnaes 1956) indicate that it may have formed before the age at which dentin starts forming in the incisor. However, there has been discussion of dental development in Homo species, especially the question of whether Neanderthal tooth growth was faster than that of modern humans (Dean, Stringer, and Bromage 1986; Ramirez Rozzi and Bermudez de Castro 2004) or similar (Dean et al. 2001; Macchiarelli et al. 2006) and the issue of whether postcanine and anterior teeth differ (Smith et al. 2010). In light of this, the statement made by Ivanhoe (1970:578) that Sogn- naes had produced “unequivocal evidence of serious vitamin D deficiency in Neandertal man” cannot be accepted. To determine whether interglobular dentin representing systemic mineralization defects was present in Neanderthals, analysis would have to be undertaken on teeth that had been clearly determined to be Neanderthal.
The question of whether Neanderthals experienced vitamin D deficiency is important because genetic information on possible skin pigmentation in the species (Lalueza-Fox et al. 2007) has been used to support suggestions on the speed of such changes in humans with the move from Africa (Holick 2011). Synthesis of vitamin D is widely accepted to be the most significant factor in the development of different levels of skin pigmentation in humans (Holick and Chen 2008; Jab- lonski 2012), although there is still some debate (Robins 2009). Melanin pigmentation plays a significant role in the rate at which synthesis of vitamin D occurs (Holick and Chen 2008), and natural selection has been suggested to influence the development of lighter skin pigmentation (Chaplin and Jablonski 2013). In the future, interglobular dentin should be considered in light of the chronology of dental growth in fossil hominins. Recording episodes of interglobular dentin across the dentition of individuals will provide a valuable tool for future dental development chronology studies. Interglobular dentin yields life-history benchmarks, since timing of the formation of teeth can be considered in light of the manifestation of stress episodes across the dentin (Smith et al. 2007).
Serum 25(OH)D levels have been shown to be high for modern individuals living traditional lifestyles close to the equator in Africa (Luxwolda et al. 2012), and it has been proposed that levels of vitamin D deficiency might have been high for humans leaving Africa (Chaplin and Jablonski 2009).
Table 2. Directly comparable data from Greek teeth

Vitamin D deficiency, revealed through interglobular-dentin data, offers an opportunity to investigate the speed and extent to which vitamin D deficiency played a role in changes in human skin pigmentation. Work on the vitamin D status of nonhuman primates could play a big role in evaluating changes in vitamin D status relative to sun exposure, but consideration will have to be given to recent work that shows differences in vitamin D metabolism between humans and various nonhuman primate species (Ziegler et al. 2015). Other factors that will have to be considered in relation to hominins are developments of clothing, housing/shelter types, and lifeways that may affect the amount of skin exposure and dietary components such as phytates, which can prevent calcium absorption (Brickley, Moffat, and Watamaniuk 2014). Further work using securely dated dental samples is required, but this approach offers a clear opportunity to answer questions relating to skin pigmentation in hominin species.
Reported Interglobular Dentin: 5500 BCE to the Late Twentieth Century
The small numbers of teeth analyzed from early sites, coupled with limited amounts of contextual information, make it difficult to fully evaluate exact changes in prevalence of vitamin D deficiency. The two data sets that can be directly compared (Sognnaes 1956 for Greek data and Ivanhoe 1982 for British data) indicate an increase of vitamin D deficiency through time, particularly with a move to urban living. Direct comparisons of averaged data for each time period are possible for the teeth from Greece dating from 3000 BCE to 1948 CE analyzed by Sognnaes (1956; table 2). Various researchers have used systems to quantify interglobular dentin, with the most recent being that by D’Ortenzio et al. (2016). It is now known that interglobular dentin is linked to severity of disruption in mineralization. Sognnaes developed a semiquantitative scoring system to evaluate the level of defects found in dentin by counting the average number of interglobular spaces per square millimeter and measuring the size of developmental defects (on a scale of + to + + +).
Sognnaes’s paper (1956) indicates that no defects were found in the small sample of teeth from the very earliest time periods but that moderate dentin defects were present in over 80% of individuals from 2000 BCE onward. Teeth from recent and contemporary Greece revealed not only that more people had interglobular dentin but also that the severity of defects had increased. On a simple comparative scale, severity of deficiency was four times as high in Greek communities in 1948 CE as in early farming communities from ca. 2000 BCE. The increase is particularly marked in recent history, after 1800 CE (Sognnaes 1956). The thin sections made by Sognnaes were not available for reanalysis, but from the description of scoring we estimate that Sognnaes’ scores 10-13 approximate D’Ortenzio et al.’s (2016) grade 2 and his scores 14-20 grade 3. All individuals with interglobular dentin scored as grade 2 or 3 in the investigation by D’Ortenzio and coworkers (2016) had severe rickets. For individuals analyzed from Greece, rickets could well have been present from 750 CE, with cases certainly present from 1800 CE onward. Although it has not received widespread attention, rickets was shown to be common in and around Athens in recent history. Lapatsanis and colleagues (1968) found rickets in 23% of those not receiving supplements. Mol- nar and Ward (1975) also found that the teeth with the highest proportion of interglobular dentin came from modern individuals (dating to 1975 CE).
The two groups from the United Kingdom investigated by Ivanhoe (1982) showed marked differences in interglobular dentin, with individuals living in the Industrial Revolution in London (1781-1825 CE) showing higher levels than those from the Anglo-Saxon (425-625 CE) community (see table 1). Ivanhoe estimated that 60% of those from London may have had rickets during infancy, compared to 40% from the earlier group. Using interglobular dentin, the severity of defects was scored, and the scores were also higher in individuals from London. Although Ivanhoe cautioned that the method used should be considered semiquantitative, it appears fairly conclusive that, as expected, levels of vitamin D deficiency were much higher in the group from a large industrial city. Holick (2003) suggests that during the Industrial Revolution levels of vitamin D deficiency would have been epidemic in cities. The two UK groups investigated by Ivanhoe were located at approximately the same latitude and within a 2,000-year time frame. The important differences would have been levels oftechnological development and associated social practices, represented by factors such as the built environment, industrial activity, and atmospheric pollution, along with clothing and sunlight exposure. Ivanhoe (1982) focused on hours of sunlight available due to latitude, but recent research on vitamin D deficiency demonstrates that although latitude and sunlight are important factors, some of the highest levels of vitamin D deficiency come from very low latitudes (Mithal et al. 2009). Social and cultural factors are key variables in the development of vitamin D deficiency. Diet, which Ivanhoe (1982) did consider, is also important. Fish consumption has been shown to be responsible for high vitamin D levels in countries located at high latitudes, such as Finland (Lamberg-Allardt et al. 2013), and phytates, which are a vitamin D inhibitor, have been considered in relation to diets of early humans (Chaplin and Jablonski 2009).

The numbers of individuals investigated by D’Ortenzio et al. (2016) are small, but detailed information on vitamin D deficiency represented by interglobular dentin is provided. Individuals from both sites showed evidence for multiple episodes of deficiency, with a young man from Quebec City showing four episodes (two of the individuals from France showed two episodes). These individuals, from sites dating from the thirteenth to nineteenth centuries, were selected for analysis because of the presence of skeletal indicators of severe childhood rickets (D’Ortenzio et al. 2016) and so are probably not representative of the whole community. Future work on both communities is planned. Investigations on individuals from Quebec City will incorporate isotopic analysis to provide information on diet and immigration status. Work on the collections from St. Jacques in northern France will include examination of the archival material relating to Douai, the location of the cemetery. The archives available are among the richest in France and will provide information on diet and cultural practices.

Lifestyle and evolutionary aspects of vitamin D in human societies have been considered by Chaplin and Jablonski (2009), but until now such investigations have relied on using current data to construct theoretical models of past patterns of deficiency. In a study of Scotland (Chaplin and Jablonski 2013), evidence from environmental archaeology for utilization of marine resources and cow’s blood (relatively high in D3) for making black pudding by past communities is considered. The highland potato famine of the 1840s is suggested to be a decisive moment in time for communities living in Scotland (Chaplin and Jablonski 2013). A significant change in lifestyle occurred for many individuals, as they were forced from the land and moved to urban environments. Diet and time spent outdoors would have changed significantly for many people. Until now it has been difficult to estimate the vitamin D status of past groups (Chaplin and Jablonski 2013). Integration of data on inter- globular dentin would provide clear information on changes in cultural and dietary practice to be determined for past groups and allow more to be learned concerning vitamin D metabolism, including the effect of intrauterine vitamin D deficiency on future health (D’Ortenzio et al. 2016; Ziegler et al. 2015).

Conclusions
Vitamin D deficiency is one of the most significant health problems facing the world’s population today, and it tends to be thought of as a modern health problem. Data reviewed here provide clear evidence that vitamin D deficiency has been present in human communities from the earliest time periods. Understanding past patterns of vitamin D deficiency through interglobular dentin has significant potential to provide information on the importance of intrauterine and early infant vitamin D deficiency for long-term health, variation in skin pigmentation, immigration, and social and cultural factors operating in past communities. Data currently available indicate that the move from simple farming to complex urban communities had a significant impact on levels of vitamin D deficiency. The approaches presented will enable future studies to fully investigate such changes. Application of information on interglobular dentin revealed by the various branches of anthropology will elucidate issues concerning contemporary health problems associated with the deficiency.
Acknowledgments
This work was supported in part by funds made available through the Canada Research Chair program and a McMaster University and Social Sciences and Humanities Research Council Insight Grant, file no. 435-2013-1006 (ID no. 169793). We also thank the following persons for allowing us access to the Quebecois skeletal remains from St. Matthew shown in figure 2: Marie-Sol Gaudreau (Anglican Diocese of Quebec), William Moss (Archaeologist, Quebec City), and Reginald Auger (Uni- versite Laval, Quebec City); and we thank the Museo Nazionale Preistorico Etnoggraphico “L.Pigorini” for access to skeletal material shown in figure 1. Thanks are due to the Communaute d’Agglomeration du Douaisis, for providing the opportunity to examine the St. Jacques osteoarchaeological material, and to the reviewers, who provided valuable feedback on the paper.
References Cited

• Brickley, Megan, Simon Mays, and Rachel Ives. 2010. Evaluation and interpretation of residual rickets deformities in adults. International Journal of Osteoarchaelogy 20(1):54-66.
• Brickley, Megan, Tina Moffat, and Lelia Watamaniuk. 2014. Biocultural perspectives of vitamin D deficiency in the past. Journal of Anthropological Archaeology 36:48-59.
• Chaplin, George, and Nina Jablonski. 2009. Vitamin D and the evolution of human depigmentation. American Journal ofPhysical Anthropology 139(4): 451-461.
  . 2013. The human environment and the vitamin D compromise: Scotland as a case study in human biocultural adaptation and disease susceptibility. Human Biology 85(4):529-552.
• Czermak, Johann. 1850. Beitrage zur mikroskopischen Anatomie der mensch- lichen Zahne. Zeitschriftfur wissenschaftliche Zoologie 2:295-322.
• Dean, Christopher, Maeve G. Leakey, Donald Reid, Friedemann Schrenk, Gary T. Schwartz, Christopher Stringer, and Alan Walker. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.
• Dean, Christopher, Christopher B. Stringer, and Timothy Bromage. 1986. Age at death of the Neanderthal child from Devil’s Tower, Gibraltar and the implications for studies of general growth and development in Neanderthals. American Journal of Physical Anthropology 70(3):301-309.
• D’Ortenzio, Lori, Isabelle Ribot, Emeline Raguin, Annabelle Schattmann, Benoit Bertrand, Bonnie Kahlon, and Megan Brickley. 2016. The rachitic tooth: a histological examination. Journal of Archaeological Science 74:152-163.
• Giuffra, Valentina, Angelica Vitiello, Davide Caramella, Antonio Fornaciari, Davide Giustini, and Gino Fornaciari. 2015. Rickets in a high social class of Renaissance Italy: the Medici children. International Journal ofOsteoarchae- ology 25(5):608-624.
• Glisson, Francis. 1650. De rachitide. London: Sadler & Beaumont.
• Gustafson, Gosta, and Goran Koch. 1974. Age estimation up to 16 years of age based on dental development. Odontologisk Revy 25(3):297-306.
• Hess, Alfred F. 1930. Rickets. Includingosteomalacia and tetany. London: Kimpton.
• Hess, Alfred F., and Lester J. Unger. 1922. Infantile rickets: the significance of clinical, radiographic and chemical examinations in its diagnosis and influence. American Journal of Diseases of Children 24:327-338.
• Hillson, Simon. 1996. Dental anthropology. Cambridge: Cambridge University Press.
• Holick, Michael F. 2003. Vitamin D: a millennium perspective. Journal of Cellular Biochemistry 88(2):296-307.
  2006. Resurrection of vitamin D deficiency and rickets. Journal of Clinical Investigation 116(8):2062-2072.
  2011. Vitamin D: a d-lightful solution for health. Journal of Investigative Medicine 59(6):872-880.
• Holick, Michael F., and Tai C. Chen. 2008. Vitamin D deficiency: a worldwide problem with health consequences. American Journal of Clinical Nutrition 87(suppl):1080S-1086S.
• Ivanhoe, Francis. 1970. Was Virchowright about Neandertal? Nature 227: 577579.
  1982. Interglobular dentine in first and third molars: relation to hours of sunshine during growth in two archeological populations from England. Calcified Tissue International 34(1):136-144.
• Jablonski, Nina. 2012. The evolution of human skin colouration and its relevance to health in the modern world. Journal of the Royal College of Surgeons of Edinburgh 42(1):58-63.
• Jablonski, Nina, and George Chaplin. 2013. Epidermal pigmentation in the human lineage is an adaptation to ultraviolet radiation. Journal of Human Evolution 65(5):671-675.
• Jacobs, Elizabeth T., Lindsay N. Kohler, Andrew G. Kunihiro, and Peter W. Jurutka. 2016. Vitamin D and colorectal, breast, and prostate cancers: a review of the epidemiological evidence. Journal of Cancer 7(3):232-240.
• Lalueza-Fox, Carles, Holger Rompler, David Caramelli, Claudia Staubert, Giulio Catalano, David Hughes, Nadin Rohland, et al. 2007. A melanocor- tin 1 receptor allele suggests varying pigmentation among Neanderthals. Science 318(5855):1453-1455.
• Lamberg-Allardt, Christel, Magritt Brustad, Haakon E. Meyer, and Laufey Steingrimsdottir. 2013. Vitamin D—a systematic literature review for the 5th edition of the Nordic Nutrition Recommendations. Food and Nutrition Research 57:22671. doi:10.3402/fnr.v57i0.22671.
• Lapatsanis, Peter, Vasso Deliyanni, and Spyros Doxiadis. 1968. Vitamin D deficiency rickets in Greece. Journal of Pediatrics 73(2):195-202.
• Leeds, Edward Thurlow, and Donald Benjamin Harden. 1936. The Anglo- Saxon cemetery at Abingdon, Berkshire. Oxford: University of Oxford Press.
• Levine, Frances, and Anna LaBauve. 1997. Examining the complexity of historic population decline: a case study of Pecos Pueblo, New Mexico. Eth- nohistory 44(1):75-112.
• Luxwolda, Martine F., Remko S. Kuipers, Ido P. Kema, D. A. Janneke Dijck- Brouwer, and Frits A. J. Muskiet. 2012. Traditionally living populations in East Africa have a mean serum 25-hydroxyvitamin D concentration of 115 nmol/l. British Journal of Nutrition 108(9):1557-1561.
• Macchiarelli, Roberto, Luca Bondioli, Andre Debenath, Arnaud Mazurier, Jean-Fran^ois Tournepiche, Wendy Birch, and M. Christopher Dean. 2006. How Neanderthal molar teeth grew. Nature 444:748-751.
• Mays, Simon, Megan Brickley, and Rachel Ives. 2006. Skeletal manifestations of rickets in infants and young children in a historic population from England. American Journal ofPhysical Anthropology 129(3):362-374.
• Mellanby, M. 1929. Diet and the teeth: an experimental study. Part I, Dental structure in dogs. Medical Research Council, Special Report Series, no. I40. London: His Majesty’s Stationery Office.
• Mitchell, Piers. 2011. Retrospective diagnosis and the use ofhistorical texts for investigating disease in the past. International Journal ofPalaeopathology 1(2): 81-88.
• Mithal, Ambrish, Danys A. Wahl, Jean-Philippe Bonjour, Peter Burckhardt, Bess Dawson-Hughes, John A. Eisman, Ghada El-Hajj Fuleihan, Robert G. Josse, Paul Lips, and Jorge Morales-Torres. 2009. Global vitamin D status and determinants of hypovitaminosis D. Osteoporosis International 20(11): 1807-1820.
• Molnar, Stephen, and Steven C. Ward. 1975. Mineral metabolism and micro- structural defects in primate teeth. American Journal ofPhysical Anthropology 43(1):3-17.
• Mounier, Aurelien, and Marta Mirazon Lahr. 2016. Virtual ancestor reconstruction: revealing the ancestor of modern humans and Neandertals. Journal ofHuman Evolution 91:57-72.
• Ortner, Donald, and Simon Mays. 1998. Dry-bone manifestations of rickets in infancy and early childhood. International Journal ofOsteoarchaeology 8(1): 45-55.
• Palm, Theobald A. 1890. The geographical distribution and etiology of rickets. Practitioner 45:270-279.
• Peterlik, Meinrad. 2012. Vitamin D insufficiency and chronic diseases: hype and reality. Food and Function 3(8):784-794.
• Ramirez Rozzi, Fernando V., and Jose Maria Bermudez de Castro. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939.
• Relethford, John H. 1997. Hemispheric differences in human skin color. American Journal ofHuman Evolution 104(4):449-457.
• Robinowitz, Carolyn. 2009. Appropriate supplementation of vitamin D: report of the Council on Science and Public Health. CSAPH Report 4-A-09. https:// www.ama-assn.org/sites/default/files/media-browser/public/about-ama/councils /Council%20Reports/council-on-science-public-health/a09-csaph-vitamin-d -supplementation.pdf.
• Robins, Ashley H. 2009. The evolution of light skin color: role of vitamin D disputed. American Journal of Physical Anthropology 139(4):447-450.
• Robinson, Paul, Wolfgang Hogler, Maria Craig, Charles Verge, Jan Walker, Anne Piper, Helen Woodhead, Christopher Cowell, and GeoffAmbler. 2006. The re-emerging burden of rickets: a decade of experience from Sydney. Archives ofDisease in Childhood 91:564-568.
• Rossberg, Willi, Roman Saternus, Stefan Wagenpfeil, Marcus Kleber, Winfried Marz, Sandra Reichrath, Thomas Vogt, and Jorg Reichrath. 2016. Human pigmentation, cutaneous vitamin D synthesis and evolution: variants of genes (SNPs) involved in skin pigmentation are associated with 25(OH)D serum concentration. Anticancer Research 36(3):1429-1437.
• Seow, W. Kim, K. Romaniuk, and Spiros S. Sclavos. 1989. Micromorphologic features of dentin in vitamin D-resistant rickets: correlation with clinical grading of severity. Pediatric Dentistry 11(3):203-208.
• Smith, Tanya M., Paul Tafforeau, Donald J. Reid, Joane Pouech, Vincent Lazzari, John P. Zermeno, Debbie Guatelli-Steinberg, et al. 2010. Dental evidence for ontogenetic differences between modern humans and Neanderthals. Proceedings of the National Academy of Sciences of the USA 107 (49):20923-20928.
• Smith, Tanya M., Michel Toussaint, Donald J. Reid, Anthony J. Olejniczak, and Jean-Jacques Hublin. 2007. Rapid dental development in a Middle Paleolithic Belgian Neanderthal. Proceedings of the National Academy of Sciences ofthe USA 104(51):20220-20225.
• Sognnaes, Reidar Fauske. 1956. Histologic evidence of developmental lesions in teeth originating from Paleolithic, prehistoric, and ancient man. American Journal of Pathology 32(3):547-577.
• Steinbock, R. Ted. 1993. Rickets and osteomalacia. In The Cambridge world history ofdisease. Kenneth F. Kiple, ed. Pp. 978-980. Cambridge: Cambridge University Press.
• Veselka, Barbara, Menno L. P. Hoogland, and Andrea L. Waters-Rist. 2015. Rural rickets: vitamin D deficiency in a post-medieval farming community from the Netherlands. International Journal ofOsteoarchaeology 25(5):665-675.
• Wei, Ran, and Sylvia Christakos. 2015. Mechanisms underlying the regulation of innate and adaptive immunity by vitamin D. Nutrients 7(10):8251- 8260.
• Wharton, Brian, and Nick Bishop. 2003. Rickets. Lancet 362(9393):1389-1400.
• Whistler, Daniel. 1645. Disputatio medica inauguralis, de morbo puerili An- glorum, quem patrio idiomate indigenae vocant the Rickets. London.
• Wright, Lori E., and Henry P. Schwarcz. 1998. Stable carbon and oxygen isotopes in human tooth enamel: identifying breastfeeding and weaning in prehistory. American Journal ofPhysical Anthropology 106(1):1-18.
• Ziegler, Toni E., Amita Kapoor, Curtis J. Hedman, Neil Binkley, and Joseph W. Kemnitz. 2015. Measurement of 25-hydroxyvitamin D2&3 and 1,25- dihydroxyvitamin D2&3 by tandem mass spectrometry: a primate multispecies comparison. American Journal of Primatology 77(7):801-810.

Low vitamin D in N. Europe during 19th and 5th centuries (teeth) – April 2017

New Perspectives on Past Vitamin D Deficiency
Society for American Archaeology 82nd Annual Meeting, Vancouver, BC (2017) • Foundations for Innovation: The Legacies and Influences of Archaeological Science at McMaster
Megan Brickley Year: 2017

Less than half of the current world population is estimated to have adequate vitamin D status and potential consequences are much debated. For those engaged in addressing the challenges that vitamin D deficiency poses, information on past deficiency provides an important time dimension to current debates. Over the last 15 years I have undertaken extensive collaborative work on past deficiency. Investigations at St. Martin’s, a 19th-century UK site, established diagnostic criteria and revealed the socio-cultural complexity of deficiency. Work undertaken at McMaster has demonstrated that contrary to popular belief the condition is not just associated with Northern European cities in the Industrial Revolution.
In the largest scale project undertaken to date (3426 individuals) vitamin D deficiency has been shown to be widespread across the Roman Empire (3rd-6thc.CE). Although latitude plays a role, level of urbanisation and social complexity are clearly also factors.
New work on defects in dentine linked to vitamin D deficiency offers the opportunity to determine the number and severity of episodes of deficiency.
Dentine defects are preserved indefinitely and in combination with skeletal features can illuminate the individual experience of deficiency in the past and contribute to current debates on health.

The rachitic tooth: A histological examination - 2016

Lori D’Ortenzio a, *, Isabelle Ribot b, Emeline Raguin b, Annabelle Schattmann a,
Benoit Bertrand c, d, Bonnie Kahlon a, Megan Brickley
 Download the PDF from VitaminDWiki